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1
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Razmadze D, Salomies L, Di-Poï N. Squamates as a model to understand key dental features of vertebrates. Dev Biol 2024; 516:1-19. [PMID: 39069116 DOI: 10.1016/j.ydbio.2024.07.011] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/01/2023] [Revised: 06/11/2024] [Accepted: 07/23/2024] [Indexed: 07/30/2024]
Abstract
Thanks to their exceptional diversity, teeth are among the most distinctive features of vertebrates. Parameters such as tooth size, shape, number, identity, and implantation can have substantial implications for the ecology and certain social behaviors of toothed species. Despite decades of research primarily focused on mammalian dentition, particularly using the laboratory mouse model, squamate reptiles ("lizards" and snakes) offer a wide array of tooth types and dentition variations. This diversity, which includes differences in size, shape, function, and replacement capacity, provides invaluable opportunities for investigating these fundamental properties. The central bearded dragon (Pogona vitticeps), a popular pet species with well-established husbandry practices, is of particular interest. It features a broad spectrum of morphs and spontaneous mutants and exhibits a wide range of heterodont phenotypes, including variation in the size, shape, number, implantation, and renewal of teeth at both posterior and anterior positions. These characteristics position the species as a crucial model organism for developmental studies in tooth research and for gaining deeper insights into evolutionary patterns of vertebrate dentitions. In this article, we provide an overview of the current understanding of squamate dentition, its diversity, development, and replacement. Furthermore, we discuss the significant advantages offered by squamate species as model organisms for investigating the evolutionary and developmental aspects of vertebrate dentition.
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Affiliation(s)
- Daria Razmadze
- Institute of Biotechnology, Helsinki Institute of Life Science, University of Helsinki, 00014, Helsinki, Finland
| | - Lotta Salomies
- Institute of Biotechnology, Helsinki Institute of Life Science, University of Helsinki, 00014, Helsinki, Finland
| | - Nicolas Di-Poï
- Institute of Biotechnology, Helsinki Institute of Life Science, University of Helsinki, 00014, Helsinki, Finland.
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2
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Calamari ZT, Flynn JJ. Gene expression supports a single origin of horns and antlers in hoofed mammals. Commun Biol 2024; 7:509. [PMID: 38769090 PMCID: PMC11106249 DOI: 10.1038/s42003-024-06134-4] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/27/2020] [Accepted: 04/02/2024] [Indexed: 05/22/2024] Open
Abstract
Horns, antlers, and other bony cranial appendages of even-toed hoofed mammals (ruminant artiodactyls) challenge traditional morphological homology assessments. Cranial appendages all share a permanent bone portion with family-specific integument coverings, but homology determination depends on whether the integument covering is an essential component or a secondary elaboration of each structure. To enhance morphological homology assessments, we tested whether juvenile cattle horn bud transcriptomes share homologous gene expression patterns with deer antlers relative to pig outgroup tissues, treating the integument covering as a secondary elaboration. We uncovered differentially expressed genes that support horn and antler homology, potentially distinguish them from non-cranial-appendage bone and other tissues, and highlight the importance of phylogenetic outgroups in homology assessments. Furthermore, we found differentially expressed genes that could support a shared cranial neural crest origin for horns and antlers and expression patterns that refine our understanding of the timing of horn and antler differentiation.
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Affiliation(s)
- Zachary T Calamari
- Division of Paleontology, American Museum of Natural History, Central Park West at 79th Street, New York, NY, 10024, USA.
- Richard Gilder Graduate School, American Museum of Natural History, Central Park West at 79th Street, New York, NY, 10024, USA.
- Department of Natural Sciences, Baruch College, City University of New York, 17 Lexington Avenue, Box A-920, New York, NY, 10010, USA.
| | - John J Flynn
- Division of Paleontology, American Museum of Natural History, Central Park West at 79th Street, New York, NY, 10024, USA
- Richard Gilder Graduate School, American Museum of Natural History, Central Park West at 79th Street, New York, NY, 10024, USA
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3
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Shao F, Van Otterloo E, Cao H. Computational identification of key transcription factors for embryonic and postnatal Sox2+ dental epithelial stem cell. BIORXIV : THE PREPRINT SERVER FOR BIOLOGY 2023:2023.12.22.573158. [PMID: 38187542 PMCID: PMC10769342 DOI: 10.1101/2023.12.22.573158] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 01/09/2024]
Abstract
While many reptiles can replace their tooth throughout life, human loss the tooth replacement capability after formation of the permanent teeth. It was thought that the difference in tooth regeneration capability depends on the persistence of a specialized dental epithelial structure, the dental lamina that contains dental epithelial stem cells (DESC). Currently, we know very little about DESC such as what genes are expressed or its chromatin accessibility profile. Multiple markers of DESC have been proposed such as Sox2 and Lgr5 . Few single cell RNA-seq experiments have been performed previously, but no obvious DESC cluster was identified in these scRNA-seq datasets, possible due to that the expression level of DESC markers such as Sox2 and Lgr5 is too low or the percentage of DESC is too low in whole tooth. We utilize a mouse line Sox2-GFP to enrich Sox2+ DESC and use Smart-Seq2 protocol and ATAC-seq protocol to generate transcriptome profile and chromatin accessibility profile of P2 Sox2+ DESC. Additionally, we generate transcriptome profile and chromatin accessibility profile of E11.5 Sox2+ dental lamina cells. With transcriptome profile and chromatin accessibility profile, we systematically identify potential key transcription factors for E11.5 Sox2+ cells and P2 Sox2+ cells. We identified transcription factors including Pitx2, Id3, Pitx1, Tbx1, Trp63, Nkx2-3, Grhl3, Dlx2, Runx1, Nfix, Zfp536 , etc potentially formed the core transcriptional regulatory networks of Sox2+ DESC in both embryonic and postnatal stages.
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4
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Green DR, Winkler DE, Leichliter JN, Harms GS, Hatt JM, Clauss M, Tütken T. Formation and Replacement of Bone and Tooth Mineralized Tissues in Green Iguanas (Iguana iguana) Revealed by In-Vivo Fluorescence Marking. Integr Comp Biol 2023; 63:515-529. [PMID: 37475667 DOI: 10.1093/icb/icad089] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/21/2023] [Revised: 06/15/2023] [Accepted: 06/20/2023] [Indexed: 07/22/2023] Open
Abstract
Hard tissue formation patterns and rates reveal details of animal physiology, life history, and environment, but are understudied in reptiles. Here, we use fluorescence labels delivered in vivo and laser confocal scanning microscopy to study tooth and bone formation in a managed group of green iguanas (Iguana iguana, Linné 1758) kept for 1.5 years under experimentally controlled conditions and undergoing several dietary switches. We constrain rates of tooth elongation, which we observe to be slow when enamel is initially deposited (c. 9 µm/day), but then increases exponentially in the dentin root, reaching c. 55 µm/day or more after crown completion. We further constrain the total timing of tooth formation to ∼40-60 days, and observe highly variable timings of tooth resorption onset and replacement. Fluorescent labels clearly indicate cohorts of teeth recruited within Zahnreihen replacement waves, with faster sequential tooth recruitment and greater wave sizes posteriorly, where each wave initiates. Fluorescence further reveals enamel maturation after initial deposition. Rates of hard tissue formation in long bones range from 0.4 to 3.4 µm/day, correlating with animal weight gain and cortical bone recording the entire history of the experiment. We suggest additional labeling experiments to study hard tissue formation patterns in other reptiles, and propose strategies for chemical analyses of hard tissues in order to extract temporal information about past environments, behaviors, and diets from reptilian fossils throughout the Phanerozoic.
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Affiliation(s)
- Daniel R Green
- Lamont-Doherty Earth Observatory, Climate School, Columbia University, 2910 Broadway Level A, New York, NY 10025, USA
| | - Daniela E Winkler
- Applied and Analytical Palaeontology, Institute of Geosciences, Johannes Gutenberg University, J.-J.-Becher-Weg 21, 55128 Mainz, Germany
- Zoological Institute, Christian-Albrechts-Universität zu Kiel, Am Botanischen Garten 1-9, 24118 Kiel, Germany
| | - Jennifer N Leichliter
- Applied and Analytical Palaeontology, Institute of Geosciences, Johannes Gutenberg University, J.-J.-Becher-Weg 21, 55128 Mainz, Germany
- Emmy Noether Group for Hominin Meat Consumption, Max Planck Institute for Chemistry, 55128 Mainz, Germany
| | - Gregory S Harms
- Imaging Core Facility, University Medical Center Mainz, Langenbeckstraße 1, 55131 Mainz, Germany
- Departments of Biology and Earth Systems Science and Mathematics, Physics and Computer Science, WIlkes University, Wilkes-Barre, PA 18766, USA
| | - Jean-Michel Hatt
- Clinic for Zoo Animals, Exotic Pets and Wildlife, Vetsuisse Faculty, University of Zürich, Winterthurerstrasse 260, 8057 Zurich, Switzerland
| | - Marcus Clauss
- Clinic for Zoo Animals, Exotic Pets and Wildlife, Vetsuisse Faculty, University of Zürich, Winterthurerstrasse 260, 8057 Zurich, Switzerland
| | - Thomas Tütken
- Applied and Analytical Palaeontology, Institute of Geosciences, Johannes Gutenberg University, J.-J.-Becher-Weg 21, 55128 Mainz, Germany
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5
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Mitsiadis TA, Pagella P, Capellini TD, Smith MM. The Notch-mediated circuitry in the evolution and generation of new cell lineages: the tooth model. Cell Mol Life Sci 2023; 80:182. [PMID: 37330998 DOI: 10.1007/s00018-023-04831-7] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/14/2023] [Revised: 05/19/2023] [Accepted: 06/09/2023] [Indexed: 06/20/2023]
Abstract
The Notch pathway is an ancient, evolutionary conserved intercellular signaling mechanism that is involved in cell fate specification and proper embryonic development. The Jagged2 gene, which encodes a ligand for the Notch family of receptors, is expressed from the earliest stages of odontogenesis in epithelial cells that will later generate the enamel-producing ameloblasts. Homozygous Jagged2 mutant mice exhibit abnormal tooth morphology and impaired enamel deposition. Enamel composition and structure in mammals are tightly linked to the enamel organ that represents an evolutionary unit formed by distinct dental epithelial cell types. The physical cooperativity between Notch ligands and receptors suggests that Jagged2 deletion could alter the expression profile of Notch receptors, thus modifying the whole Notch signaling cascade in cells within the enamel organ. Indeed, both Notch1 and Notch2 expression are severely disturbed in the enamel organ of Jagged2 mutant teeth. It appears that the deregulation of the Notch signaling cascade reverts the evolutionary path generating dental structures more reminiscent of the enameloid of fishes rather than of mammalian enamel. Loss of interactions between Notch and Jagged proteins may initiate the suppression of complementary dental epithelial cell fates acquired during evolution. We propose that the increased number of Notch homologues in metazoa enabled incipient sister cell types to form and maintain distinctive cell fates within organs and tissues along evolution.
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Affiliation(s)
- Thimios A Mitsiadis
- Institute of Oral Biology, Centre for Dental Medicine, University of Zurich, Plattenstrasse 11, 8032, Zurich, Switzerland.
| | - Pierfrancesco Pagella
- Institute of Oral Biology, Centre for Dental Medicine, University of Zurich, Plattenstrasse 11, 8032, Zurich, Switzerland
- Wallenberg Center for Molecular Medicine (WCMM) and Department of Biomedical and Clinical Sciences, Linköpings Universitet, 581 85, Linköping, Sweden
| | - Terence D Capellini
- Department of Human Evolutionary Biology, Harvard University, Cambridge, MA, 02138, USA
| | - Moya Meredith Smith
- Centre for Craniofacial and Regenerative Biology, Faculty of Dentistry, King's College London, London, UK
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6
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Gruenhagen GW, Mubeen T, Patil C, Stockert J, Streelman JT. Single Cell RNA Sequencing Reveals Deep Homology of Dental Cell Types Across Vertebrates. FRONTIERS IN DENTAL MEDICINE 2022; 3. [DOI: 10.3389/fdmed.2022.845449] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 09/01/2023] Open
Abstract
Like most mammals, humans replace their teeth once throughout their lives and have limited regenerative capabilities. In contrast, mice continually renew tissues lost due to gnawing through a well characterized population of stem cells on the labial surface of the incisor. Most non-mammalian vertebrates replace teeth throughout life; the cellular and molecular mechanisms of successional tooth replacement are largely unknown. Here we use single nuclei RNA sequencing (snRNA-seq) of replacement teeth and adjacent oral lamina in Lake Malawi cichlids, species with lifelong whole–tooth replacement, to make two main discoveries. First, despite hundreds of millions of years of evolution, we demonstrate conservation of cell type gene expression across vertebrate teeth (fish, mouse, human). Second, we used an approach that combines marker gene expression and developmental potential of dental cells to uncover the transcriptional signature of stem-like cells in regenerating teeth. Our work underscores the importance of a comparative framework in the study of vertebrate oral and regenerative biology.
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7
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Salomies L, Eymann J, Ollonen J, Khan I, Di-Poï N. The developmental origins of heterodonty and acrodonty as revealed by reptile dentitions. SCIENCE ADVANCES 2021; 7:eabj7912. [PMID: 34919438 PMCID: PMC8682985 DOI: 10.1126/sciadv.abj7912] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [Grants] [Track Full Text] [Figures] [Subscribe] [Scholar Register] [Received: 06/02/2021] [Accepted: 11/01/2021] [Indexed: 06/14/2023]
Abstract
Despite the exceptional diversity and central role of dentitions in vertebrate evolution, many aspects of tooth characters remain unknown. Here, we exploit the large array of dental phenotypes in acrodontan lizards, including EDA mutants showing the first vertebrate example of positional transformation in tooth identity, to assess the developmental origins and evolutionary patterning of tooth types and heterodonty. We reveal that pleurodont versus acrodont dentition can be determined by a simple mechanism, where modulation of tooth size through EDA signaling has major consequences on dental formula, thereby providing a new flexible tooth patterning model. Furthermore, such implication of morphoregulation in tooth evolution allows predicting the dental patterns characterizing extant and fossil lepidosaurian taxa at large scale. Together, the origins and diversification of tooth types, long a focus of multiple research fields, can now be approached through evo-devo approaches, highlighting the importance of underexplored dental features for illuminating major evolutionary patterns.
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8
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Pospisilova A, Stundl J, Brejcha J, Metscher BD, Psenicka M, Cerny R, Soukup V. The remarkable dynamics in the establishment, rearrangement, and loss of dentition during the ontogeny of the sterlet sturgeon. Dev Dyn 2021; 251:826-845. [PMID: 34846759 DOI: 10.1002/dvdy.444] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/23/2021] [Revised: 11/15/2021] [Accepted: 11/22/2021] [Indexed: 11/07/2022] Open
Abstract
BACKGROUND Sturgeons belong to an early-branching lineage often used as a proxy of ancestor-like traits of ray-finned fishes. However, many features of this lineage, such as the transitory presence and the eventual loss of dentition, exemplify specializations that, in fact, provide important information on lineage-specific evolutionary dynamics. RESULTS Here, we introduce a detailed overview of the dentition during the development of the sterlet sturgeon. The dentition is composed of tooth fields at oral, palatal, and anterior pharyngeal regions. Oral fields are single-rowed, non-renewed and are shed early. Palatal and pharyngeal fields are multi-rowed and renewed from the adjacent superficial epithelium without the presence of the successional dental lamina. The early loss of oral fields and subsequent establishment of palatal and pharyngeal fields leads to a translocation of the functional dentition from the front to the rear of the oropharyngeal cavity until the eventual loss of all teeth. CONCLUSIONS Our survey shows the sterlet dentition as a dynamic organ system displaying differential composition at different time points in the lifetime of this fish. These dynamics represent a conspicuous feature of sturgeons, unparalleled among extant vertebrates, and appropriate to scrutinize developmental and evolutionary underpinnings of vertebrate odontogenesis.
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Affiliation(s)
- Anna Pospisilova
- Department of Zoology, Faculty of Science, Charles University, Prague, Czech Republic
| | - Jan Stundl
- Department of Zoology, Faculty of Science, Charles University, Prague, Czech Republic.,Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, California, USA.,Faculty of Fisheries and Protection of Waters, South Bohemian Research Center of Aquaculture and Biodiversity of Hydrocenoses, Research Institute of Fish Culture and Hydrobiology, University of South Bohemia in České Budějovice, Vodňany, Czech Republic
| | - Jindrich Brejcha
- Department of Philosophy and History of Science, Faculty of Science, Charles University, Prague, Czech Republic
| | - Brian D Metscher
- Department of Evolutionary Biology, University of Vienna, Vienna, Austria
| | - Martin Psenicka
- Faculty of Fisheries and Protection of Waters, South Bohemian Research Center of Aquaculture and Biodiversity of Hydrocenoses, Research Institute of Fish Culture and Hydrobiology, University of South Bohemia in České Budějovice, Vodňany, Czech Republic
| | - Robert Cerny
- Department of Zoology, Faculty of Science, Charles University, Prague, Czech Republic
| | - Vladimír Soukup
- Department of Zoology, Faculty of Science, Charles University, Prague, Czech Republic
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9
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Mao C, Lai Y, Liao C, Chen J, Hong Y, Ren C, Wang C, Lu M, Chen W. Revitalizing mouse diphyodontic dentition formation by inhibiting the sonic hedgehog signaling pathway. Dev Dyn 2021; 251:759-776. [PMID: 34719835 DOI: 10.1002/dvdy.436] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/31/2021] [Revised: 09/24/2021] [Accepted: 10/27/2021] [Indexed: 12/15/2022] Open
Abstract
BACKGROUND Tooth regeneration depends on the longevity of the dental epithelial lamina. However, the exact mechanism of dental lamina regression has not yet been clarified. To explore the role of the Sonic hedgehog (Shh) signaling pathway in regression process of the rudimentary successional dental lamina (RSDL) in mice, we orally administered a single dose of a Shh signaling pathway inhibitor to pregnant mice between embryonic day 13.0 (E13.0) and E17.0. RESULTS We observed that the Shh signaling pathway inhibitor effectively inhibited the expression of Shh signaling pathway components and revitalized RSDL during E15.0-E17.0 by promoting cell proliferation. In addition, mRNA-seq, reverse transcription plus polymerase chain reaction (RT-qPCR), and immunohistochemical analyses indicated that diphyodontic dentition formation might be related to FGF signal up-regulation and the Sostdc1-Wnt negative feedback loop. CONCLUSIONS Overall, our results indicated that the Shh signaling pathway may play an initial role in preventing further development of mouse RSDL in a time-dependent manner.
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Affiliation(s)
- Chuanqing Mao
- Department of Oral and Maxillofacial Surgery, Fujian Medical University Union Hospital, Fuzhou, China.,Fujian Key Laboratory of Oral Diseases & Stomatological Key Lab of Fujian College and University, School and Hospital of Stomatology, Fujian Medical University, Fuzhou, China.,Institute of Stomatology, Fujian Medical University, Fuzhou, China
| | - Yongzhen Lai
- Department of Oral and Maxillofacial Surgery, Fujian Medical University Union Hospital, Fuzhou, China
| | - Caiyu Liao
- Department of Oral and Maxillofacial Surgery, Fujian Medical University Union Hospital, Fuzhou, China.,Fujian Key Laboratory of Oral Diseases & Stomatological Key Lab of Fujian College and University, School and Hospital of Stomatology, Fujian Medical University, Fuzhou, China.,Institute of Stomatology, Fujian Medical University, Fuzhou, China
| | - Jiangping Chen
- Department of Oral and Maxillofacial Surgery, Fujian Medical University Union Hospital, Fuzhou, China.,Institute of Stomatology, Fujian Medical University, Fuzhou, China
| | - Yuhang Hong
- Department of Oral and Maxillofacial Surgery, Fujian Medical University Union Hospital, Fuzhou, China.,Institute of Stomatology, Fujian Medical University, Fuzhou, China
| | - Chengyan Ren
- Department of Oral and Maxillofacial Surgery, Fujian Medical University Union Hospital, Fuzhou, China.,Fujian Key Laboratory of Oral Diseases & Stomatological Key Lab of Fujian College and University, School and Hospital of Stomatology, Fujian Medical University, Fuzhou, China.,Institute of Stomatology, Fujian Medical University, Fuzhou, China
| | - Chengyong Wang
- Department of Oral and Maxillofacial Surgery, Fujian Medical University Union Hospital, Fuzhou, China
| | - Meng Lu
- Department of Oral and Maxillofacial Surgery, Fujian Medical University Union Hospital, Fuzhou, China
| | - Weihui Chen
- Department of Oral and Maxillofacial Surgery, Fujian Medical University Union Hospital, Fuzhou, China.,Fujian Key Laboratory of Oral Diseases & Stomatological Key Lab of Fujian College and University, School and Hospital of Stomatology, Fujian Medical University, Fuzhou, China.,Fujian Biological Materials Engineering and Technology Center of Stomatology, Fuzhou, China
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10
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Rücklin M, King B, Cunningham JA, Johanson Z, Marone F, Donoghue PCJ. Acanthodian dental development and the origin of gnathostome dentitions. Nat Ecol Evol 2021; 5:919-926. [PMID: 33958756 DOI: 10.1038/s41559-021-01458-4] [Citation(s) in RCA: 7] [Impact Index Per Article: 1.8] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/29/2020] [Accepted: 03/30/2021] [Indexed: 11/09/2022]
Abstract
Chondrichthyan dentitions are conventionally interpreted to reflect the ancestral gnathostome condition but interpretations of osteichthyan dental evolution in this light have proved unsuccessful, perhaps because chondrichthyan dentitions are equally specialized, or else evolved independently. Ischnacanthid acanthodians are stem-Chondrichthyes; as phylogenetic intermediates of osteichthyans and crown-chondrichthyans, the nature of their enigmatic dentition may inform homology and the ancestral gnathostome condition. Here we show that ischnacanthid marginal dentitions were statodont, composed of multicuspidate teeth added in distally diverging rows and through proximal superpositional replacement, while their symphyseal tooth whorls are comparable to chondrichthyan and osteichthyan counterparts. Ancestral state estimation indicates the presence of oral tubercles on the jaws of the gnathostome crown-ancestor; tooth whorls or tooth rows evolved independently in placoderms, osteichthyans, ischnacanthids, other acanthodians and crown-chondrichthyans. Crown-chondrichthyan dentitions are derived relative to the gnathostome crown-ancestor, which possessed a simple dentition and lacked a permanent dental lamina, which evolved independently in Chondrichthyes and Osteichthyes.
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Affiliation(s)
- Martin Rücklin
- Naturalis Biodiversity Center, Leiden, The Netherlands.
- School of Earth Sciences, University of Bristol, Life Sciences Building, Bristol, UK.
| | - Benedict King
- Naturalis Biodiversity Center, Leiden, The Netherlands
- Department of Linguistic and Cultural Evolution, Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany
| | - John A Cunningham
- School of Earth Sciences, University of Bristol, Life Sciences Building, Bristol, UK
| | - Zerina Johanson
- Department of Earth Sciences, Natural History Museum, London, UK
| | - Federica Marone
- Swiss Light Source, Paul Scherrer Institut, Villigen, Switzerland
| | - Philip C J Donoghue
- School of Earth Sciences, University of Bristol, Life Sciences Building, Bristol, UK.
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11
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Hulsey CD, Meyer A, Streelman JT. Convergent Evolution of Cichlid Fish Pharyngeal Jaw Dentitions in Mollusk-Crushing Predators: Comparative X-Ray Computed Tomography of Tooth Sizes, Numbers, and Replacement. Integr Comp Biol 2021; 60:656-664. [PMID: 32584994 DOI: 10.1093/icb/icaa089] [Citation(s) in RCA: 6] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/12/2022] Open
Abstract
Dental convergence is a hallmark of cichlid fish adaptive radiations. This type of repeated evolution characterizes both the oral jaws of these fishes as well as their pharyngeal jaws that are modified gill arches used to functionally process prey like hard-shelled mollusks. To test several hypotheses regarding the evolution of cichlid crushing pharyngeal dentitions, we used X-ray computed tomography scans to comparatively examine dental evolution in the pharyngeal jaw of a diversity of New World Heroine cichlid lineages. The substantial variation in erupted tooth sizes and numbers as well as replacement teeth found in these fishes showed several general patterns. Larger toothed species tended to have fewer teeth suggesting a potential role of spatial constraints in cichlid dental divergence. Species with larger numbers of erupted pharyngeal teeth also had larger numbers of replacement teeth. Replacement tooth size is almost exactly predicted (r = 0.99) from the size of erupted teeth across all of the species. Mollusk crushing was, therefore, highly associated with not only larger pharyngeal teeth, but also larger replacement teeth. Whether dental divergence arises as a result of environmental induced plasticity or originates via trophic polymorphism as found in the species Herichthys minckleyi, there appear to be general rules that structure interspecific divergence in cichlid pharyngeal erupted and replacement dentitions.
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Affiliation(s)
- C Darrin Hulsey
- Department of Biology, University of Konstanz, Konstanz, Germany
| | - Axel Meyer
- Department of Biology, University of Konstanz, Konstanz, Germany
| | - J Todd Streelman
- School of Biological Sciences, Institute of Technology, Atlanta, GA 30332, USA
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12
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Jobbins M, Rücklin M, Argyriou T, Klug C. A large Middle Devonian eubrachythoracid 'placoderm' (Arthrodira) jaw from northern Gondwana. SWISS JOURNAL OF PALAEONTOLOGY 2021; 140:2. [PMID: 33488510 PMCID: PMC7809001 DOI: 10.1186/s13358-020-00212-w] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Figures] [Subscribe] [Scholar Register] [Received: 09/23/2020] [Accepted: 11/18/2020] [Indexed: 06/12/2023]
Abstract
For the understanding of the evolution of jawed vertebrates and jaws and teeth, 'placoderms' are crucial as they exhibit an impressive morphological disparity associated with the early stages of this process. The Devonian of Morocco is famous for its rich occurrences of arthrodire 'placoderms'. While Late Devonian strata are rich in arthrodire remains, they are less common in older strata. Here, we describe a large tooth-bearing jaw element of Leptodontichthys ziregensis gen. et sp. nov., an eubrachythoracid arthrodire from the Middle Devonian of Morocco. This species is based on a large posterior superognathal with a strong dentition. The jawbone displays features considered synapomorphies of Late Devonian eubrachythoracid arthrodires, with one posterior and one lateral row of conical teeth oriented postero-lingually. μCT-images reveal internal structures including pulp cavities and dentinous tissues. The posterior orientation of the teeth and the traces of a putative occlusal contact on the lingual side of the bone imply that these teeth were hardly used for feeding. Similar to Compagopiscis and Plourdosteus, functional teeth were possibly present during an earlier developmental stage and have been worn entirely. The morphological features of the jaw element suggest a close relationship with plourdosteids. Its size implies that the animal was rather large.
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Affiliation(s)
- Melina Jobbins
- Paläontologisches Institut und Museum, Universität Zürich, Karl-Schmid-Strasse 4, 8006 Zurich, Switzerland
| | | | - Thodoris Argyriou
- UMR 7207 (MNHN – Sorbonne Université – CNRS) Centre de Recherche en Paléontologie, Muséum National D’Histoire Naturelle, 57 rue Cuvier, 75231 Paris cedex 05, France
| | - Christian Klug
- Paläontologisches Institut und Museum, Universität Zürich, Karl-Schmid-Strasse 4, 8006 Zurich, Switzerland
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13
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Jose M, Rajagopal V, Thankam FG. Oral tissue regeneration: Current status and future perspectives. REGENERATED ORGANS 2021:169-187. [DOI: 10.1016/b978-0-12-821085-7.00009-9] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 01/04/2025]
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14
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Hosmani J, Assiri K, Almubarak HM, Mannakandath ML, Al-Hakami A, Patil S, Babji D, Sarode S, Devaraj A, Chandramoorthy HC. Proteomic profiling of various human dental stem cells - a systematic review. World J Stem Cells 2020; 12:1214-1236. [PMID: 33178402 PMCID: PMC7596439 DOI: 10.4252/wjsc.v12.i10.1214] [Citation(s) in RCA: 8] [Impact Index Per Article: 1.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 03/18/2020] [Revised: 08/06/2020] [Accepted: 09/01/2020] [Indexed: 02/06/2023] Open
Abstract
BACKGROUND The proteomic signature or profile best describes the functional component of a cell during its routine metabolic and survival activities. Additional complexity in differentiation and maturation is observed in stem/progenitor cells. The role of functional proteins at the cellular level has long been attributed to anatomical niches, and stem cells do not deflect from this attribution. Human dental stem cells (hDSCs), on the whole, are a combination of mesenchymal and epithelial coordinates observed throughout craniofacial bones to pulp.
AIM To specify the proteomic profile and compare each type of hDSC with other mesenchymal stem cells (MSCs) of various niches. Furthermore, we analyzed the characteristics of the microenvironment and preconditioning changes associated with the proteomic profile of hDSCs and their influence on committed lineage differentiation.
METHODS Literature searches were performed in PubMed, EMBASE, Scopus, and Web of Science databases, from January 1990 to December 2018. An extra inquiry of the grey literature was completed on Google Scholar, ProQuest, and OpenGrey. Relevant MeSH terms (PubMed) and keywords related to dental stem cells were used independently and in combination.
RESULTS The initial search resulted in 134 articles. Of the 134 full-texts assessed, 96 articles were excluded and 38 articles that met the eligibility criteria were reviewed. The overall assessment of hDSCs and other MSCs suggests that differences in the proteomic profile can be due to stem cellular complexity acquired from varied tissue sources during embryonic development. However, our comparison of the proteomic profile suffered inconsistencies due to the heterogeneity of various hDSCs. We believe that the existence of a heterogeneous population of stem cells at a given niche determines the modalities of regeneration or tissue repair. Added prominences to the differences present between various hDSCs have been reasoned out.
CONCLUSION Systematic review on proteomic studies of various hDSCs are promising as an eye-opener for revisiting the proteomic profile and in-depth analysis to elucidate more refined mechanisms of hDSC functionalities.
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Affiliation(s)
- Jagadish Hosmani
- Diagnostic Dental Sciences, College of Dentistry, King Khalid University, Abha 61471, Asir, Saudi Arabia
| | - Khalil Assiri
- Diagnostic Dental Sciences, King Khalid University, Abha 61471, Asir, Saudi Arabia
| | | | | | - Ahmed Al-Hakami
- Center for Stem Cell Research and Department of Microbiology and Clinical Parasitology, King Khalid University, Abha 61421, Asir, Saudi Arabia
| | - Shankargouda Patil
- Maxillofacial Surgery and Diagnostic Sciences, Division of oral Pathology, Jazan 45142, Jazan, Saudi Arabia
| | - Deepa Babji
- Department of Oral Pathology and Microbiology, Maratha Mandal's NG Halgekar Institute of Dental Sciences and Research Centre, Belgaun 590 010, Karnataka, India
| | - Sachin Sarode
- Department of Oral Pathology, Y Patil Dental College and Hospital, Pune 411018, Maharashtra, India
| | - Anantharam Devaraj
- Center for Stem Cell Research and Department of Microbiology and Clinical Parasitology, King Khalid University, Abha 61421, Asir, Saudi Arabia
| | - Harish C Chandramoorthy
- Center for Stem Cell Research and Department of Microbiology and Clinical Parasitology, King Khalid University, Abha 61421, Asir, Saudi Arabia
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15
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Sánchez N, González-Ramírez MC, Contreras EG, Ubilla A, Li J, Valencia A, Wilson A, Green JBA, Tucker AS, Gaete M. Balance Between Tooth Size and Tooth Number Is Controlled by Hyaluronan. Front Physiol 2020; 11:996. [PMID: 32982773 PMCID: PMC7476214 DOI: 10.3389/fphys.2020.00996] [Citation(s) in RCA: 8] [Impact Index Per Article: 1.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/27/2020] [Accepted: 07/22/2020] [Indexed: 12/20/2022] Open
Abstract
While the function of proteins and genes has been widely studied during vertebrate development, relatively little work has addressed the role of carbohydrates. Hyaluronan (HA), also known as hyaluronic acid, is an abundant carbohydrate in embryonic tissues and is the main structural component of the extracellular matrix of epithelial and mesenchymal cells. HA is able to absorb large quantities of water and can signal by binding to cell-surface receptors. During organ development and regeneration, HA has been shown to regulate cell proliferation, cell shape, and migration. Here, we have investigated the function of HA during molar tooth development in mice, in which, similar to humans, new molars sequentially bud off from a pre-existing molar. Using an ex vivo approach, we found that inhibiting HA synthesis in culture leads to a significant increase in proliferation and subsequent size of the developing molar, while the formation of sequential molars was inhibited. By cell shape analysis, we observed that inhibition of HA synthesis caused an elongation and reorientation of the major cell axes, indicating that disruption to cellular orientation and shape may underlie the observed phenotype. Lineage tracing demonstrated the retention of cells in the developing first molar (M1) at the expense of the generation of a second molar (M2). Our results highlight a novel role for HA in controlling proliferation, cell orientation, and migration in the developing tooth, impacting cellular decisions regarding tooth size and number.
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Affiliation(s)
- Natalia Sánchez
- Department of Anatomy, Faculty of Medicine, Pontificia Universidad Católica de Chile, Santiago, Chile
| | | | | | - Angélica Ubilla
- Department of Anatomy, Faculty of Medicine, Pontificia Universidad Católica de Chile, Santiago, Chile
| | - Jingjing Li
- Centre for Craniofacial and Regenerative Biology, King's College London, London, United Kingdom
| | - Anyeli Valencia
- Department of Anatomy, Faculty of Medicine, Pontificia Universidad Católica de Chile, Santiago, Chile
| | - Andrés Wilson
- Department of Anatomy, Faculty of Medicine, Pontificia Universidad Católica de Chile, Santiago, Chile
| | - Jeremy B A Green
- Centre for Craniofacial and Regenerative Biology, King's College London, London, United Kingdom
| | - Abigail S Tucker
- Centre for Craniofacial and Regenerative Biology, King's College London, London, United Kingdom
| | - Marcia Gaete
- Department of Anatomy, Faculty of Medicine, Pontificia Universidad Católica de Chile, Santiago, Chile
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16
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Hulsey CD, Cohen KE, Johanson Z, Karagic N, Meyer A, Miller CT, Sadier A, Summers AP, Fraser GJ. Grand Challenges in Comparative Tooth Biology. Integr Comp Biol 2020; 60:563-580. [PMID: 32533826 PMCID: PMC7821850 DOI: 10.1093/icb/icaa038] [Citation(s) in RCA: 10] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/12/2022] Open
Abstract
Teeth are a model system for integrating developmental genomics, functional morphology, and evolution. We are at the cusp of being able to address many open issues in comparative tooth biology and we outline several of these newly tractable and exciting research directions. Like never before, technological advances and methodological approaches are allowing us to investigate the developmental machinery of vertebrates and discover both conserved and excitingly novel mechanisms of diversification. Additionally, studies of the great diversity of soft tissues, replacement teeth, and non-trophic functions of teeth are providing new insights into dental diversity. Finally, we highlight several emerging model groups of organisms that are at the forefront of increasing our appreciation of the mechanisms underlying tooth diversification.
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Affiliation(s)
- C Darrin Hulsey
- Department of Biology, University of Konstanz, Konstanz, 78464, Germany
| | - Karly E Cohen
- Friday Harbor Laboratories, School of Aquatic and Fishery Sciences, Department of Biology, University of Washington, WA 98195, USA
| | - Zerina Johanson
- Department of Earth Sciences, Natural History Museum, London SW7 5HD, UK
| | - Nidal Karagic
- Department of Biology, University of Konstanz, Konstanz, 78464, Germany
| | - Axel Meyer
- Department of Biology, University of Konstanz, Konstanz, 78464, Germany
| | - Craig T Miller
- Department of Molecular and Cell Biology, University of California Berkeley, Berkeley, CA 94720, USA
| | - Alexa Sadier
- Department of Ecology and Evolution, University of California Los Angeles, Los Angeles, CA 90032, USA
| | - Adam P Summers
- Friday Harbor Laboratories, School of Aquatic and Fishery Sciences, Department of Biology, University of Washington, WA 98195, USA
| | - Gareth J Fraser
- Department of Biology, University of Florida, Gainesville, FL 32611, USA
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17
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Brink KS, Wu P, Chuong CM, Richman JM. The Effects of Premature Tooth Extraction and Damage on Replacement Timing in the Green Iguana. Integr Comp Biol 2020; 60:581-593. [PMID: 32974642 PMCID: PMC7546963 DOI: 10.1093/icb/icaa099] [Citation(s) in RCA: 6] [Impact Index Per Article: 1.2] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/03/2023] Open
Abstract
Reptiles with continuous tooth replacement, or polyphyodonty, replace their teeth in predictable, well-timed waves in alternating tooth positions around the mouth. This process is thought to occur irrespective of tooth wear or breakage. In this study, we aimed to determine if damage to teeth and premature tooth extraction affects tooth replacement timing long-term in juvenile green iguanas (Iguana iguana). First, we examined normal tooth development histologically using a BrdU pulse-chase analysis to detect label-retaining cells in replacement teeth and dental tissues. Next, we performed tooth extraction experiments for characterization of dental tissues after functional tooth (FT) extraction, including proliferation and β-Catenin expression, for up to 12 weeks. We then compared these results to a newly analyzed historical dataset of X-rays collected up to 7 months after FT damage and extraction in the green iguana. Results show that proliferation in the dental and successional lamina (SL) does not change after extraction of the FT, and proliferation occurs in the SL only when a tooth differentiates. Damage to an FT crown does not affect the timing of the tooth replacement cycle, however, complete extraction shifts the replacement cycle ahead by 4 weeks by removing the need for resorption of the FT. These results suggest that traumatic FT loss affects the timing of the replacement cycle at that one position, which may have implications for tooth replacement patterning around the entire mouth.
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Affiliation(s)
- Kirstin S Brink
- Department of Oral Health Sciences, University of British Columbia, Vancouver, BC V6T 1Z4, Canada
- Department of Geological Sciences, University of Manitoba, 125 Dysart Road, Winnipeg, MB R3T 2N2, Canada
| | - Ping Wu
- Keck School of Medicine, University of Southern California, 2011 Zonal Ave, Los Angeles, CA HMR313, USA
| | - Cheng-Ming Chuong
- Keck School of Medicine, University of Southern California, 2011 Zonal Ave, Los Angeles, CA HMR313, USA
| | - Joy M Richman
- Department of Oral Health Sciences, University of British Columbia, Vancouver, BC V6T 1Z4, Canada
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18
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Abuarqoub D, Aslam N, Almajali B, Shajrawi L, Jafar H, Awidi A. Neuro-regenerative potential of dental stem cells: a concise review. Cell Tissue Res 2020; 382:267-279. [PMID: 32725424 DOI: 10.1007/s00441-020-03255-0] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/06/2020] [Accepted: 07/06/2020] [Indexed: 10/23/2022]
Abstract
This review will summarize the research information regarding the regenerative potential of dental stem cells for the treatment of neurodegenerative disorders. As compared to existing treatment modalities, the stem cell therapy seems promising, and accumulating evidences about the differentiation of stem cells into various lineages are proving it. The incidence of neurodegenerative diseases such as Alzheimer's, Parkinson's, stroke, and peripheral neuropathy is increasing due to the rise in life expectancies of people which have put a huge burden on economies. Finding a promising treatment could benefit not only the patients but also the communities. Dental stem cells hold a great potential to differentiate into neuronal cells. Many studies have reported the differentiation potential of the dental stem cells with the presence of neuronal lineage markers. In this review, we conferred how the use of dental stem cells can benefit the above-mentioned bedridden diseases.
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Affiliation(s)
- Duaa Abuarqoub
- Department of Pharmacology and Biomedical Sciences, Faculty of Pharmacy and Medical Sciences, University of Petra, Amman, Jordan. .,Cell Therapy Center, The University of Jordan, Amman, Jordan.
| | - Nazneen Aslam
- Cell Therapy Center, The University of Jordan, Amman, Jordan
| | - Bayan Almajali
- School of Medicine, The University of Jordan, Amman, Jordan
| | - Leen Shajrawi
- School of Medicine, The University of Jordan, Amman, Jordan
| | - Hanan Jafar
- Cell Therapy Center, The University of Jordan, Amman, Jordan.,School of Medicine, The University of Jordan, Amman, Jordan
| | - Abdalla Awidi
- Cell Therapy Center, The University of Jordan, Amman, Jordan. .,School of Medicine, The University of Jordan, Amman, Jordan.
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19
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Wu J, Tian Y, Han L, Liu C, Sun T, Li L, Yu Y, Lamichhane B, D'Souza RN, Millar SE, Krumlauf R, Ornitz DM, Feng JQ, Klein O, Zhao H, Zhang F, Linhardt RJ, Wang X. FAM20B-catalyzed glycosaminoglycans control murine tooth number by restricting FGFR2b signaling. BMC Biol 2020; 18:87. [PMID: 32664967 PMCID: PMC7359594 DOI: 10.1186/s12915-020-00813-4] [Citation(s) in RCA: 15] [Impact Index Per Article: 3.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/05/2019] [Accepted: 06/17/2020] [Indexed: 02/05/2023] Open
Abstract
BACKGROUND The formation of supernumerary teeth is an excellent model for studying the molecular mechanisms that control stem/progenitor cell homeostasis needed to generate a renewable source of replacement cells and tissues. Although multiple growth factors and transcriptional factors have been associated with supernumerary tooth formation, the regulatory inputs of extracellular matrix in this regenerative process remains poorly understood. RESULTS In this study, we present evidence that disrupting glycosaminoglycans (GAGs) in the dental epithelium of mice by inactivating FAM20B, a xylose kinase essential for GAG assembly, leads to supernumerary tooth formation in a pattern reminiscent of replacement teeth. The dental epithelial GAGs confine murine tooth number by restricting the homeostasis of Sox2(+) dental epithelial stem/progenitor cells in a non-autonomous manner. FAM20B-catalyzed GAGs regulate the cell fate of dental lamina by restricting FGFR2b signaling at the initial stage of tooth development to maintain a subtle balance between the renewal and differentiation of Sox2(+) cells. At the later cap stage, WNT signaling functions as a relay cue to facilitate the supernumerary tooth formation. CONCLUSIONS The novel mechanism we have characterized through which GAGs control the tooth number in mice may also be more broadly relevant for potentiating signaling interactions in other tissues during development and tissue homeostasis.
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Affiliation(s)
- Jingyi Wu
- Southern Medical University Hospital of Stomatology, Guangzhou, 510280, Guangdong, China.,Department of Biomedical Sciences, Texas A&M University College of Dentistry, 3302 Gaston Ave, Dallas, TX, 75246, USA
| | - Ye Tian
- Department of Biomedical Sciences, Texas A&M University College of Dentistry, 3302 Gaston Ave, Dallas, TX, 75246, USA.,West China Hospital of Stomatology, Sichuan University, Chengdu, 610000, Sichuan, China
| | - Lu Han
- Department of Biomedical Sciences, Texas A&M University College of Dentistry, 3302 Gaston Ave, Dallas, TX, 75246, USA.,West China Hospital of Stomatology, Sichuan University, Chengdu, 610000, Sichuan, China
| | - Chao Liu
- Department of Biomedical Sciences, Texas A&M University College of Dentistry, 3302 Gaston Ave, Dallas, TX, 75246, USA.,Department of Oral Pathology, College of Stomatology, Dalian Medical University, Dalian, 116044, Liaoning, China
| | - Tianyu Sun
- Southern Medical University Hospital of Stomatology, Guangzhou, 510280, Guangdong, China.,Department of Biomedical Sciences, Texas A&M University College of Dentistry, 3302 Gaston Ave, Dallas, TX, 75246, USA
| | - Ling Li
- Department of Developmental Biology, Washington University School of Medicine, St. Louis, MO, 63110, USA
| | - Yanlei Yu
- Department of Chemistry and Chemical Biology, Rensselaer Polytechnic Institute, Troy, NY, 12180, USA
| | - Bikash Lamichhane
- Department of Biomedical Sciences, Texas A&M University College of Dentistry, 3302 Gaston Ave, Dallas, TX, 75246, USA
| | - Rena N D'Souza
- School of Dentistry, University of Utah, Salt Lake City, UT, 84108, USA
| | - Sarah E Millar
- Department of Dermatology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, 19104, USA
| | - Robb Krumlauf
- Stowers Institute for Medical Research, Kansas City, MO, 64110, USA.,Department of Anatomy and Cell Biology, Kansas University Medical Center, Kansas City, KS, 66160, USA
| | - David M Ornitz
- Department of Developmental Biology, Washington University School of Medicine, St. Louis, MO, 63110, USA
| | - Jian Q Feng
- Department of Biomedical Sciences, Texas A&M University College of Dentistry, 3302 Gaston Ave, Dallas, TX, 75246, USA
| | - Ophir Klein
- Department of Orofacial Sciences and Program in Craniofacial Biology, University of California, San Francisco, San Francisco, CA, 94143, USA.,Institute for Human Genetics, University of California, San Francisco, San Francisco, CA, 94143, USA
| | - Hu Zhao
- Department of Biomedical Sciences, Texas A&M University College of Dentistry, 3302 Gaston Ave, Dallas, TX, 75246, USA
| | - Fuming Zhang
- Department of Chemistry and Chemical Biology, Rensselaer Polytechnic Institute, Troy, NY, 12180, USA
| | - Robert J Linhardt
- Department of Chemistry and Chemical Biology, Rensselaer Polytechnic Institute, Troy, NY, 12180, USA
| | - Xiaofang Wang
- Department of Biomedical Sciences, Texas A&M University College of Dentistry, 3302 Gaston Ave, Dallas, TX, 75246, USA.
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20
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Kim E, Jung S, Wu Z, Zhang S, Jung H. Sox2 maintains epithelial cell proliferation in the successional dental lamina. Cell Prolif 2020; 53:e12729. [PMID: 31746095 PMCID: PMC6985665 DOI: 10.1111/cpr.12729] [Citation(s) in RCA: 7] [Impact Index Per Article: 1.4] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/26/2019] [Revised: 10/10/2019] [Accepted: 10/31/2019] [Indexed: 02/06/2023] Open
Abstract
OBJECTIVES The successional dental lamina is the distinctive structure on the lingual side of the vertebrate tooth germ. The aim of this study was to investigate the relationship among Sox2, Claudin10 and laminin5 and the role of Sox2 in successional dental lamina proliferation during vertebrate tooth development. MATERIALS AND METHODS To understand the successional dental lamina, two types of successional tooth formation, that in geckos (with multiple rounds of tooth generation) and that in mice (with only one round of tooth generation), were analysed. RESULTS Unique coexpression patterns of Sox2 and Claudin10 expression were compared in the successional dental lamina from the cap stage to the late bell stage in the mouse tooth germ and in juvenile gecko teeth to support continuous tooth replacement. Furthermore, Laminin5 expression was shown in the cap stage and decreased after the bell stage. Upon comparing the epithelial cell cycles and cell proliferation in successional dental lamina regions between mouse and gecko molars using BrdU and IdU staining and pulse-chase methods, distinctive patterns of continuous expression were revealed. Moreover, Sox2 overexpression with a lentiviral system resulted in hyperplastic dental epithelium in mouse molars. CONCLUSIONS Our findings indicate that the regulation of Sox2 in dental lamina proliferation is fundamental to the successional dental lamina in both species.
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Affiliation(s)
- Eun‐Jung Kim
- Division in Anatomy and Developmental BiologyDepartment of Oral BiologyResearch Center for Orofacial Hard Tissue RegenerationBrain Korea 21 PLUS ProjectOral Science Research CenterCollege of DentistryYonsei UniversitySeoulKorea
| | - Seo‐Yoon Jung
- Division in Anatomy and Developmental BiologyDepartment of Oral BiologyResearch Center for Orofacial Hard Tissue RegenerationBrain Korea 21 PLUS ProjectOral Science Research CenterCollege of DentistryYonsei UniversitySeoulKorea
| | - Zhaoming Wu
- Division in Anatomy and Developmental BiologyDepartment of Oral BiologyResearch Center for Orofacial Hard Tissue RegenerationBrain Korea 21 PLUS ProjectOral Science Research CenterCollege of DentistryYonsei UniversitySeoulKorea
| | - Sushan Zhang
- Division in Anatomy and Developmental BiologyDepartment of Oral BiologyResearch Center for Orofacial Hard Tissue RegenerationBrain Korea 21 PLUS ProjectOral Science Research CenterCollege of DentistryYonsei UniversitySeoulKorea
| | - Han‐Sung Jung
- Division in Anatomy and Developmental BiologyDepartment of Oral BiologyResearch Center for Orofacial Hard Tissue RegenerationBrain Korea 21 PLUS ProjectOral Science Research CenterCollege of DentistryYonsei UniversitySeoulKorea
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21
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Fraser GJ, Hamed SS, Martin KJ, Hunter KD. Shark tooth regeneration reveals common stem cell characters in both human rested lamina and ameloblastoma. Sci Rep 2019; 9:15956. [PMID: 31685919 PMCID: PMC6828755 DOI: 10.1038/s41598-019-52406-z] [Citation(s) in RCA: 16] [Impact Index Per Article: 2.7] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/10/2019] [Accepted: 10/17/2019] [Indexed: 11/26/2022] Open
Abstract
The human dentition is a typical diphyodont mammalian system with tooth replacement of most positions. However, after dental replacement and sequential molar development, the dental lamina undergoes apoptosis and fragments, leaving scattered epithelial units (dental lamina rests; DLRs). DLRs in adult humans are considered inactive epithelia, thought to possess limited capacity for further regeneration. However, we show that these tissues contain a small proportion of proliferating cells (assessed by both Ki67 and PCNA) but also express a number of common dental stem cell markers (Sox2, Bmi1, β-catenin and PH3) similar to that observed in many vertebrates that actively, and continuously regenerate their dentition. We compared these human tissues with the dental lamina of sharks that regenerate their dentition throughout life, providing evidence that human tissues have the capacity for further and undocumented regeneration. We also assessed cases of human ameloblastoma to characterise further the proliferative signature of dental lamina rests. Ameloblastomas are assumed to derive from aberrant lamina rests that undergo changes, which are not well understood, to form a benign tumour. We suggest that dental lamina rests can offer a potential source of important dental stem cells for future dental regenerative therapy. The combined developmental genetic data from the shark dental lamina and ameloblastoma may lead to the development of novel methods to utilise these rested populations of adult lamina stem cells for controlled tooth replacement in humans.
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Affiliation(s)
- Gareth J Fraser
- Department of Animal and Plant Sciences, University of Sheffield, Sheffield, UK. .,Department of Biology, University of Florida, Gainesville, FL, USA.
| | - Samar S Hamed
- Integrated Biosciences, School of Clinical Dentistry, University of Sheffield, Sheffield, UK
| | - Kyle J Martin
- Department of Animal and Plant Sciences, University of Sheffield, Sheffield, UK
| | - Keith D Hunter
- Integrated Biosciences, School of Clinical Dentistry, University of Sheffield, Sheffield, UK. .,Oral Biology and Pathology, University of Pretoria, Pretoria, South Africa.
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22
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Haridy Y, Gee BM, Witzmann F, Bevitt JJ, Reisz RR. Retention of fish-like odontode overgrowth in Permian tetrapod dentition supports outside-in theory of tooth origins. Biol Lett 2019; 15:20190514. [PMID: 31506034 DOI: 10.1098/rsbl.2019.0514] [Citation(s) in RCA: 4] [Impact Index Per Article: 0.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/12/2022] Open
Abstract
Teeth are often thought of as structures that line the margins of the mouth; however, tooth-like structures called odontodes are commonly found on the dermal bones of many Palaeozoic vertebrates including early jawless fishes. 'Odontode' is a generalized term for all tooth-like dentine structures that have homologous tissues and development. This definition includes true teeth and the odontodes of early 'fishes', which have been recently examined to gain new insights into the still unresolved origin of teeth. Two leading hypotheses are frequently referenced in this debate: the 'outside-in' hypothesis, which posits that dermal odontodes evolutionarily migrate into the oral cavity, and the 'inside-out' hypothesis, which posits that teeth originated in the oropharyngeal cavity and then moved outwards into the oral cavity. Here, we show that, unlike the well-known one-to-one replacement patterns of marginal dentition, the palatal dentition of the early Permian tetrapods, including the dissorophoid amphibian Cacops and the early reptile Captorhinus, is overgrown by a new layer of bone to which the newest teeth are then attached. This same overgrowth pattern has been well documented in dermal and oral odontodes (i.e. teeth) of early fishes. We propose that this pattern represents the primitive condition for vertebrates and may even predate the origin of jaws. Therefore, this pattern crosses the fish-tetrapod transition, and the retention of this ancestral pattern in the palatal dentition of early terrestrial tetrapods provides strong support for the 'outside-in' hypothesis of tooth origins.
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Affiliation(s)
- Yara Haridy
- Department of Biology, University of Toronto Mississauga, Ontario, Canada.,Museum für Naturkunde, Leibniz-Institut für Evolutions- und Biodiversitätsforschung, Berlin, Germany
| | - Bryan M Gee
- Department of Biology, University of Toronto Mississauga, Ontario, Canada
| | - Florian Witzmann
- Museum für Naturkunde, Leibniz-Institut für Evolutions- und Biodiversitätsforschung, Berlin, Germany
| | - Joseph J Bevitt
- Australian Centre for Neutron Scattering, Australian Nuclear Science and Technology Organisation, New South Wales, Australia
| | - Robert R Reisz
- International Center of Future Science, Dinosaur Evolution Research Centre, Jilin University, Changchun, People's Republic of China
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23
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Salomies L, Eymann J, Khan I, Di-Poï N. The alternative regenerative strategy of bearded dragon unveils the key processes underlying vertebrate tooth renewal. eLife 2019; 8:47702. [PMID: 31418691 PMCID: PMC6744223 DOI: 10.7554/elife.47702] [Citation(s) in RCA: 21] [Impact Index Per Article: 3.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/15/2019] [Accepted: 08/16/2019] [Indexed: 12/24/2022] Open
Abstract
Deep understanding of tooth regeneration is hampered by the lack of lifelong replacing oral dentition in most conventional models. Here, we show that the bearded dragon, one of the rare vertebrate species with both polyphyodont and monophyodont teeth, constitutes a key model for filling this gap, allowing direct comparison of extreme dentition types. Our developmental and high-throughput transcriptomic data of microdissected dental cells unveils the critical importance of successional dental lamina patterning, in addition to maintenance, for vertebrate tooth renewal. This patterning process happens at various levels, including directional growth but also gene expression levels, dynamics, and regionalization, and involves a large number of yet uncharacterized dental genes. Furthermore, the alternative renewal mechanism of bearded dragon dentition, with dual location of slow-cycling cells, demonstrates the importance of cell migration and functional specialization of putative epithelial stem/progenitor niches in tissue regeneration, while expanding the diversity of dental replacement strategies in vertebrates. All multicellular organisms, from lizards to humans, must be able to repair and regrow damaged tissue. This includes not only healing after an injury, but also replacing parts of the body that suffer wear and tear. For example, many animals shed and replace worn out teeth throughout their life, but the number of times this occurs varies greatly between species. Much of the understanding about how teeth grow and develop has come from researching mice. However, mice only develop one set of teeth, making them a poor ‘model’ for studying how species such as fish and reptiles can re-grow and replace their teeth. Recent studies of these species has shown that regenerating teeth relies on a specialised structure known as the dental lamina. In mice, the dental lamina forms but then quickly disappears, preventing new sets of teeth from developing. In most animals that regrow their teeth, however, the dental lamina keeps growing beyond the most recently produced tooth to create an area where its replacement will emerge. Now, Salomies et al. have identified other strategies involved in tooth replacement from studying the bearded dragon lizard, a rare example of an animal that continuously regenerates some, but not all, of its teeth. Analysing the cells in different parts of the re-growing teeth from bearded dragon lizards revealed new features of the dental lamina. Specifically, Salomies et al. found that a previously uncharacterized set of genes within the dental lamina could determine whether or not a tooth will be replaced. Further experiments using microscope imaging revealed that bearded dragon lizards use two distinct groups of stem cells – specialised cells that have the potential to develop into various cell types in the body – to re-grow their teeth. These experiments demonstrate how the bearded dragon lizard uses a previously unknown mechanism to regenerate its teeth, combining elements used by gecko lizards and sharks. These findings are an important step towards understanding the different strategies animals can use to maintain and regenerate their teeth. The knowledge gained could one day help design better therapies for patients suffering from inherited dental disorders or tooth loss.
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Affiliation(s)
- Lotta Salomies
- Program in Developmental Biology, Institute of Biotechnology, University of Helsinki, Helsinki, Finland
| | - Julia Eymann
- Program in Developmental Biology, Institute of Biotechnology, University of Helsinki, Helsinki, Finland
| | - Imran Khan
- Program in Developmental Biology, Institute of Biotechnology, University of Helsinki, Helsinki, Finland
| | - Nicolas Di-Poï
- Program in Developmental Biology, Institute of Biotechnology, University of Helsinki, Helsinki, Finland
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Meredith Smith M, Underwood C, Goral T, Healy C, Johanson Z. Growth and mineralogy in dental plates of the holocephalan Harriotta raleighana (Chondrichthyes): novel dentine and conserved patterning combine to create a unique chondrichthyan dentition. ZOOLOGICAL LETTERS 2019; 5:11. [PMID: 30923631 PMCID: PMC6419362 DOI: 10.1186/s40851-019-0125-3] [Citation(s) in RCA: 11] [Impact Index Per Article: 1.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Subscribe] [Scholar Register] [Received: 10/19/2018] [Accepted: 02/25/2019] [Indexed: 06/09/2023]
Abstract
ABSTRACT The dentition in extant holocephalans (Chondrichthyes) comprises three pairs of continuously growing dental plates, rather than the separate teeth characterizing elasmobranchs. We investigated how different types of dentine in these plates, including hypermineralized dentine, are arranged, and how this is renewed aborally, in adult and juvenile dentitions of Harriotta raleighana (Rhinochimeridae). Individual plates were analysed using x-ray computed tomography (μCT), scanning electron microscopy (SEM) in back scattered mode with energy dispersive X-ray (EDX) analysis, and optical microscopy on hard tissue sections. RESULTS Harriotta dental plates are made entirely of dentine tissue, mostly as trabecular dentine, bone itself being absent. Hypermineralized dentine forms in restricted ovoid and tritor spaces within trabecular dentine, inside a shell of outer and inner dentine layers. Trabecular dentine is ubiquitous but changes to sclerotic osteodentine near the oral surface by increasing density, remaining less mineralized than the hypermineralized dentine. All structures are renewed aborally, within a vascular dental pulp, a tissue suggested to be a source of stem cells for tissue renewal. Ca density profiles and concentrations of Mg, P, and Ca ions reveal extreme differences in the level and type of mineralization. Early mineralization in ovoids and tritors has very high levels of Mg, then a sudden increase in mineralization to a high total mineral content, whereas there is gradual change in trabecular dentine, remaining at a low level.Hypermineralized dentine fills the prepatterned ovoid, rod and tritor spaces, early at the aboral surface within the trabecular dentine. Deposition of the hypermineralized dentine (HD, proposed as new specific name, whitlockin replacing pleromin) is from surfaces that are lined with large specialized odontoblasts, (whitloblasts, instead of pleromoblasts) within cell body spaces connecting with extensive, ramifying tubules. Early mineralization occurs amongst this maze of tubules that penetrate far into the dentine, expanding into a mass of saccules and membranous bodies, dominating in the absence of other organic matrix. This early stage has hydroxyapatite, also significantly rich in Mg, initiated as a poorly crystalline phase. In the hypermineralized dentine, formation occurs as clusters of variably shaped crystals, arising from a sudden phase transition. CONCLUSIONS In the hypermineralized dentine, high MgO + CaO + P2O5 suggests that almost pure Mg containing tricalciumphosphate (MgTCP: (ß-Ca3(PO4)2) (whitlockite) is present, with little or no hydroxyapatite. Serial replacement of tritors and ovoids is suggested to occur within the dental plate, probably representing a relic of patterning, as classically found in elasmobranch dentitions.
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Affiliation(s)
- Moya Meredith Smith
- Centre for Craniofacial and Regenerative Biology, Faculty of Dentistry, Oral and Craniofacial Sciences, King’s College London, London, SE1 9RT, UK
- Department of Earth Sciences, Natural History Museum London, London, SW7 5BD, UK
| | - Charlie Underwood
- Department of Earth and Planetary Sciences, Birkbeck, University of London, London, UK
| | - Tomasz Goral
- Department of Earth Sciences, Natural History Museum London, London, SW7 5BD, UK
- Current address: Center of New Technologies, University of Warsaw, Warsaw, Poland
| | - Christopher Healy
- Centre for Craniofacial and Regenerative Biology, Faculty of Dentistry, Oral and Craniofacial Sciences, King’s College London, London, SE1 9RT, UK
| | - Zerina Johanson
- Department of Earth Sciences, Natural History Museum London, London, SW7 5BD, UK
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Calamari ZT, Kuang-Hsien Hu J, Klein OD. Tissue Mechanical Forces and Evolutionary Developmental Changes Act Through Space and Time to Shape Tooth Morphology and Function. Bioessays 2018; 40:e1800140. [PMID: 30387177 PMCID: PMC6516060 DOI: 10.1002/bies.201800140] [Citation(s) in RCA: 16] [Impact Index Per Article: 2.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/08/2018] [Revised: 10/06/2018] [Indexed: 12/24/2022]
Abstract
Efforts from diverse disciplines, including evolutionary studies and biomechanical experiments, have yielded new insights into the genetic, signaling, and mechanical control of tooth formation and functions. Evidence from fossils and non-model organisms has revealed that a common set of genes underlie tooth-forming potential of epithelia, and changes in signaling environments subsequently result in specialized dentitions, maintenance of dental stem cells, and other phenotypic adaptations. In addition to chemical signaling, tissue forces generated through epithelial contraction, differential growth, and skeletal constraints act in parallel to shape the tooth throughout development. Here recent advances in understanding dental development from these studies are reviewed and important gaps that can be filled through continued application of evolutionary and biomechanical approaches are discussed.
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Affiliation(s)
- Zachary T. Calamari
- Department of Natural Sciences, Baruch College, City University of New York, New York City, New York, 10010, USA
- Department of Orofacial Sciences and Program in Craniofacial Biology, University of California, San Francisco, San Francisco, California, 94143, USA
| | - Jimmy Kuang-Hsien Hu
- Department of Orofacial Sciences and Program in Craniofacial Biology, University of California, San Francisco, San Francisco, California, 94143, USA
| | - Ophir D. Klein
- Department of Orofacial Sciences and Program in Craniofacial Biology, University of California, San Francisco, San Francisco, California, 94143, USA
- Department of Pediatrics and Institute for Human Genetics, University of California, San Francisco, San Francisco, California, 94143, USA
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26
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Balic A. Concise Review: Cellular and Molecular Mechanisms Regulation of Tooth Initiation. Stem Cells 2018; 37:26-32. [DOI: 10.1002/stem.2917] [Citation(s) in RCA: 27] [Impact Index Per Article: 3.9] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/14/2018] [Revised: 08/23/2018] [Accepted: 08/28/2018] [Indexed: 01/06/2023]
Affiliation(s)
- Anamaria Balic
- Research Program in Developmental Biology; Institute of Biotechnology, University of Helsinki; Helsinki Finland
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27
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Meredith Smith M, Underwood C, Clark B, Kriwet J, Johanson Z. Development and evolution of tooth renewal in neoselachian sharks as a model for transformation in chondrichthyan dentitions. J Anat 2018; 232:891-907. [PMID: 29504120 DOI: 10.1111/joa.12796] [Citation(s) in RCA: 10] [Impact Index Per Article: 1.4] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Accepted: 01/25/2018] [Indexed: 12/01/2022] Open
Abstract
A defining feature of dentitions in modern sharks and rays is the regulated pattern order that generates multiple replacement teeth. These are arranged in labio-lingual files of replacement teeth that form in sequential time order both along the jaw and within successively initiated teeth in a deep dental lamina. Two distinct adult dentitions have been described: alternate, in which timing of new teeth alternates between two adjacent files, each erupting separately, and the other arranged as single files, where teeth of each file are timed to erupt together, in some taxa facilitating similarly timed teeth to join to form a cutting blade. Both are dependent on spatiotemporally regulated formation of new teeth. The adult Angel shark Squatina (Squalomorphii) exemplifies a single file dentition, but we obtained new data on the developmental order of teeth in the files of Squatina embryos, showing alternate timing of tooth initiation. This was based on micro-CT scans revealing that the earliest mineralised teeth at the jaw margin and their replacements in file pairs (odd and even jaw positions) alternate in their initiation timing. Along with Squatina, new observations from other squalomorphs such as Hexanchus and Chlamydoselachus, together with representatives of the sister group Galeomorphii, have established that the alternate tooth pattern (initiation time and replacement order) characterises the embryonic dentition of extant sharks; however, this can change in adults. These character states were plotted onto a recent phylogeny, demonstrating that the Squalomorphii show considerable plasticity of dental development. We propose a developmental-evolutionary model to allow change from the alternate to a single file alignment of replacement teeth. This establishes new dental morphologies in adult sharks from inherited alternate order.
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Affiliation(s)
- Moya Meredith Smith
- Tissue Engineering and Biophotonics, Dental Institute, King's College, London, UK.,Department of Earth Sciences, Natural History Museum, London, UK
| | - Charlie Underwood
- Department of Earth Sciences, Natural History Museum, London, UK.,Department of Earth and Planetary Sciences, Birkbeck, University of London, London, UK
| | - Brett Clark
- Department of Earth Sciences, Natural History Museum, London, UK
| | - Jürgen Kriwet
- Department of Palaeontology, University of Vienna, Vienna, Austria
| | - Zerina Johanson
- Department of Earth Sciences, Natural History Museum, London, UK
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28
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Lamoureux DO, LeBlanc ARH, Caldwell MW. Tooth germ initiation patterns in a developing dentition: An in vivo study of Xenopus laevis tadpoles. J Morphol 2018; 279:616-625. [PMID: 29399866 DOI: 10.1002/jmor.20797] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.1] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/30/2017] [Revised: 01/08/2018] [Accepted: 01/18/2018] [Indexed: 11/07/2022]
Abstract
The transparency of soft tissue in Xenopus laevis tadpoles and the anterior-posterior orientation of their developing tooth germs in the upper jaw offer a unique opportunity for the in vivo charting of the first 15-20 days of the developing dentition. Twenty-two X. laevis tadpoles were anesthetized daily and their mouths opened to record the first appearance, position, and development of tooth germs in the upper jaw. The initiation patterns revealed considerable variability between animals, and even between the jaw quadrants in the same animal. This variability appears within a structural boundary and the results are consistent with the presence of an odontogenic band. The final length of dental rows far exceeded the jaw growth for each quadrant during the recording period. This in vivo investigation underlines the limits of cross-sectional studies, and in particular the assumption that tooth germs initiate at the same position in the dental row. The tooth germ initiation patterns in this study did not align with the predictions of standard models for the development of the dentition-Zahnreihen, Clone, and New Progress Zone theories.
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Affiliation(s)
- Denis O Lamoureux
- Department of Biological Sciences, University of Alberta, Edmonton, Alberta, Canada, T6G 2E9
| | - Aaron R H LeBlanc
- Department of Biological Sciences, University of Alberta, Edmonton, Alberta, Canada, T6G 2E9
| | - Michael W Caldwell
- Department of Biological Sciences, University of Alberta, Edmonton, Alberta, Canada, T6G 2E9
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29
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Haridy Y, LeBlanc ARH, Reisz RR. The Permian reptile Opisthodontosaurus carrolli: a model for acrodont tooth replacement and dental ontogeny. J Anat 2017; 232:371-382. [PMID: 29210080 DOI: 10.1111/joa.12754] [Citation(s) in RCA: 17] [Impact Index Per Article: 2.1] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Accepted: 10/30/2017] [Indexed: 11/27/2022] Open
Abstract
Continuous tooth replacement is common for tetrapods, but some groups of acrodont lepidosaurs have lost the ability to replace their dentition (monophyodonty). Acrodonty, where the tooth attaches to the apex of the jawbone, is an unusual form of tooth attachment that has been associated with the highly autapomorphic condition of monophyodonty. Beyond Lepidosauria, very little is known about the relationship between acrodonty and monophyodonty in other amniotes. We test for this association with a detailed study of the dentition of Opisthodontosaurus, an unusual Early Permian captorhinid eureptile with acrodont dentition. We provide clear evidence, both histological and morphological, that there were regular tooth replacement events in the lower jaw of Opisthodontosaurus, similar to its captorhinid relatives. Thus, our study of the oldest known amniote with an acrodont dentition shows that acrodonty does not inhibit tooth replacement, and that many of the characteristics assigned to lepidosaurian acrodonty are actually highly derived features of lepidosaurs that have resulted secondarily from a lack of tooth replacement. In the context of reptilian dental evolution, we propose the retention of the simple definition of acrodonty, which only pertains to the relative position of the tooth at the apex of the jaw, where the jaw possesses equal lingual and labial walls. This definition of implantation therefore focuses solely on the spatial relationship between the tooth and the jawbone, and separates this relationship from tooth development and replacement.
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Affiliation(s)
- Yara Haridy
- Department of Biology, University of Toronto Mississauga, Mississauga, ON, Canada
| | - Aaron R H LeBlanc
- Department of Biology, University of Toronto Mississauga, Mississauga, ON, Canada.,Department of Biological Sciences, University of Alberta, Edmonton, AB, Canada
| | - Robert R Reisz
- Department of Biology, University of Toronto Mississauga, Mississauga, ON, Canada.,Department of Optics and Photonics, National Central University, Jhongli, Taoyuan, Taiwan
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30
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Spatially restricted dental regeneration drives pufferfish beak development. Proc Natl Acad Sci U S A 2017; 114:E4425-E4434. [PMID: 28507130 DOI: 10.1073/pnas.1702909114] [Citation(s) in RCA: 19] [Impact Index Per Article: 2.4] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/28/2022] Open
Abstract
Vertebrate dentitions are extraordinarily diverse in both morphology and regenerative capacity. The teleost order Tetraodontiformes exhibits an exceptional array of novel dental morphologies, epitomized by constrained beak-like dentitions in several families, i.e., porcupinefishes, three-toothed pufferfishes, ocean sunfishes, and pufferfishes. Modification of tooth replacement within these groups leads to the progressive accumulation of tooth generations, underlying the structure of their beaks. We focus on the dentition of the pufferfish (Tetraodontidae) because of its distinct dental morphology. This complex dentition develops as a result of (i) a reduction in the number of tooth positions from seven to one per quadrant during the transition from first to second tooth generations and (ii) a dramatic shift in tooth morphogenesis following the development of the first-generation teeth, leading to the elongation of dental units along the jaw. Gene expression and 1,1'-Dioctadecyl-3,3,3',3'-tetramethylindocarbocyanine perchlorate (DiI) lineage tracing reveal a putative dental epithelial progenitor niche, suggesting a highly conserved mechanism for tooth regeneration despite the development of a unique dentition. MicroCT analysis reveals restricted labial openings in the beak, through which the dental epithelium (lamina) invades the cavity of the highly mineralized beak. Reduction in the number of replacement tooth positions coincides with the development of only four labial openings in the pufferfish beak, restricting connection of the oral epithelium to the dental cavity. Our data suggest the spatial restriction of dental regeneration, coupled with the unique extension of the replacement dental units throughout the jaw, are primary contributors to the evolution and development of this unique beak-like dentition.
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31
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Chen D, Blom H, Sanchez S, Tafforeau P, Märss T, Ahlberg PE. Development of cyclic shedding teeth from semi-shedding teeth: the inner dental arcade of the stem osteichthyan Lophosteus. ROYAL SOCIETY OPEN SCIENCE 2017; 4:161084. [PMID: 28573003 PMCID: PMC5451804 DOI: 10.1098/rsos.161084] [Citation(s) in RCA: 7] [Impact Index Per Article: 0.9] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Figures] [Subscribe] [Scholar Register] [Received: 12/23/2016] [Accepted: 04/21/2017] [Indexed: 06/07/2023]
Abstract
The numerous cushion-shaped tooth-bearing plates attributed to the stem group osteichthyan Lophosteus superbus, which are argued here to represent an early form of the osteichthyan inner dental arcade, display a previously unknown and presumably primitive mode of tooth shedding by basal hard tissue resorption. They carry regularly spaced, recumbent, gently recurved teeth arranged in transverse tooth files that diverge towards the lingual margin of the cushion. Three-dimensional reconstruction from propagation phase-contrast synchrotron microtomography (PPC-SRµCT) reveals remnants of the first-generation teeth embedded in the basal plate, a feature never previously observed in any taxon. These teeth were shed by semi-basal resorption with the periphery of their bases retained as dentine rings. The rings are highly overlapped, which evidences tooth shedding prior to adding the next first-generation tooth at the growing edge of the plate. The first generation of teeth is thus diachronous. Successor teeth at the same sites underwent cyclical replacing and shedding through basal resorption, producing stacks of buried resorption surfaces separated by bone of attachment. The number and spatial arrangement of resorption surfaces elucidates that basal resorption of replacement teeth had taken place at the older tooth sites before the addition of the youngest first-generation teeth at the lingual margin. Thus, the replacement tooth buds cannot have been generated by a single permanent dental lamina at the lingual edge of the tooth cushion, but must have arisen either from successional dental laminae associated with the individual predecessor teeth, or directly from the dental epithelium of these teeth. The virtual histological dissection of these Late Silurian microfossils broadens our understanding of the development of the gnathostome dental systems and the acquisition of the osteichthyan-type of tooth replacement.
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Affiliation(s)
- Donglei Chen
- Department of Organismal Biology, Uppsala University, Norbyvägen 18A, 752 36, Uppsala, Sweden
| | - Henning Blom
- Department of Organismal Biology, Uppsala University, Norbyvägen 18A, 752 36, Uppsala, Sweden
| | - Sophie Sanchez
- Department of Organismal Biology, Uppsala University, Norbyvägen 18A, 752 36, Uppsala, Sweden
- SciLifeLab, Uppsala University, Norbyvägen 18A, 752 36, Uppsala, Sweden
| | - Paul Tafforeau
- European Synchrotron Radiation Facility, 6 rue Jules Horowitz, 38043 Grenoble Cedex, France
| | - Tiiu Märss
- Estonian Marine Institute, University of Tartu, Mäealuse Street 14, 12618 Tallinn, Estonia
| | - Per E. Ahlberg
- Department of Organismal Biology, Uppsala University, Norbyvägen 18A, 752 36, Uppsala, Sweden
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32
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Chalisserry EP, Nam SY, Park SH, Anil S. Therapeutic potential of dental stem cells. J Tissue Eng 2017; 8:2041731417702531. [PMID: 28616151 PMCID: PMC5461911 DOI: 10.1177/2041731417702531] [Citation(s) in RCA: 123] [Impact Index Per Article: 15.4] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/09/2017] [Accepted: 03/12/2017] [Indexed: 12/13/2022] Open
Abstract
Stem cell biology has become an important field in regenerative medicine and tissue engineering therapy since the discovery and characterization of mesenchymal stem cells. Stem cell populations have also been isolated from human dental tissues, including dental pulp stem cells, stem cells from human exfoliated deciduous teeth, stem cells from apical papilla, dental follicle progenitor cells, and periodontal ligament stem cells. Dental stem cells are relatively easily obtainable and exhibit high plasticity and multipotential capabilities. The dental stem cells represent a gold standard for neural-crest-derived bone reconstruction in humans and can be used for the repair of body defects in low-risk autologous therapeutic strategies. The bioengineering technologies developed for tooth regeneration will make substantial contributions to understand the developmental process and will encourage future organ replacement by regenerative therapies in a wide variety of organs such as the liver, kidney, and heart. The concept of developing tooth banking and preservation of dental stem cells is promising. Further research in the area has the potential to herald a new dawn in effective treatment of notoriously difficult diseases which could prove highly beneficial to mankind in the long run.
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Affiliation(s)
- Elna Paul Chalisserry
- Interdisciplinary Program of Marine-Bio, Electrical & Mechanical Engineering, Pukyong National University, Busan, Korea
- Center for Marine-Integrated Biomedical Technology (BK21 Plus), Pukyong National University, Busan, Korea
| | - Seung Yun Nam
- Interdisciplinary Program of Marine-Bio, Electrical & Mechanical Engineering, Pukyong National University, Busan, Korea
- Center for Marine-Integrated Biomedical Technology (BK21 Plus), Pukyong National University, Busan, Korea
- Department of Biomedical Engineering, Pukyong National University, Busan, South Korea
| | - Sang Hyug Park
- Interdisciplinary Program of Marine-Bio, Electrical & Mechanical Engineering, Pukyong National University, Busan, Korea
- Center for Marine-Integrated Biomedical Technology (BK21 Plus), Pukyong National University, Busan, Korea
- Department of Biomedical Engineering, Pukyong National University, Busan, South Korea
| | - Sukumaran Anil
- Division of Periodontics, Department of Preventive Dental Sciences, College of Dentistry Prince Sattam Bin Abdulaziz University, Al-Kharj, Saudi Arabia
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33
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Sox2+ progenitors in sharks link taste development with the evolution of regenerative teeth from denticles. Proc Natl Acad Sci U S A 2016; 113:14769-14774. [PMID: 27930309 DOI: 10.1073/pnas.1612354113] [Citation(s) in RCA: 42] [Impact Index Per Article: 4.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/18/2022] Open
Abstract
Teeth and denticles belong to a specialized class of mineralizing epithelial appendages called odontodes. Although homology of oral teeth in jawed vertebrates is well supported, the evolutionary origin of teeth and their relationship with other odontode types is less clear. We compared the cellular and molecular mechanisms directing development of teeth and skin denticles in sharks, where both odontode types are retained. We show that teeth and denticles are deeply homologous developmental modules with equivalent underlying odontode gene regulatory networks (GRNs). Notably, the expression of the epithelial progenitor and stem cell marker sex-determining region Y-related box 2 (sox2) was tooth-specific and this correlates with notable differences in odontode regenerative ability. Whereas shark teeth retain the ancestral gnathostome character of continuous successional regeneration, new denticles arise only asynchronously with growth or after wounding. Sox2+ putative stem cells associated with the shark dental lamina (DL) emerge from a field of epithelial progenitors shared with anteriormost taste buds, before establishing within slow-cycling cell niches at the (i) superficial taste/tooth junction (T/TJ), and (ii) deep successional lamina (SL) where tooth regeneration initiates. Furthermore, during regeneration, cells from the superficial T/TJ migrate into the SL and contribute to new teeth, demonstrating persistent contribution of taste-associated progenitors to tooth regeneration in vivo. This data suggests a trajectory for tooth evolution involving cooption of the odontode GRN from nonregenerating denticles by sox2+ progenitors native to the oral taste epithelium, facilitating the evolution of a novel regenerative module of odontodes in the mouth of early jawed vertebrates: the teeth.
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34
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Sun Z, Yu W, Sanz Navarro M, Sweat M, Eliason S, Sharp T, Liu H, Seidel K, Zhang L, Moreno M, Lynch T, Holton NE, Rogers L, Neff T, Goodheart MJ, Michon F, Klein OD, Chai Y, Dupuy A, Engelhardt JF, Chen Z, Amendt BA. Sox2 and Lef-1 interact with Pitx2 to regulate incisor development and stem cell renewal. Development 2016; 143:4115-4126. [PMID: 27660324 PMCID: PMC5117215 DOI: 10.1242/dev.138883] [Citation(s) in RCA: 43] [Impact Index Per Article: 4.8] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/21/2016] [Accepted: 09/06/2016] [Indexed: 12/26/2022]
Abstract
Sox2 marks dental epithelial stem cells (DESCs) in both mammals and reptiles, and in this article we demonstrate several Sox2 transcriptional mechanisms that regulate dental stem cell fate and incisor growth. Conditional Sox2 deletion in the oral and dental epithelium results in severe craniofacial defects, including impaired dental stem cell proliferation, arrested incisor development and abnormal molar development. The murine incisor develops initially but is absorbed independently of apoptosis owing to a lack of progenitor cell proliferation and differentiation. Tamoxifen-induced inactivation of Sox2 demonstrates the requirement of Sox2 for maintenance of the DESCs in adult mice. Conditional overexpression of Lef-1 in mice increases DESC proliferation and creates a new labial cervical loop stem cell compartment, which produces rapidly growing long tusk-like incisors, and Lef-1 epithelial overexpression partially rescues the tooth arrest in Sox2 conditional knockout mice. Mechanistically, Pitx2 and Sox2 interact physically and regulate Lef-1, Pitx2 and Sox2 expression during development. Thus, we have uncovered a Pitx2-Sox2-Lef-1 transcriptional mechanism that regulates DESC homeostasis and dental development.
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Affiliation(s)
- Zhao Sun
- Department of Anatomy and Cell Biology, and the Craniofacial Anomalies Research Center, The University of Iowa, Iowa City, IA 52242, USA
| | - Wenjie Yu
- Department of Anatomy and Cell Biology, and the Craniofacial Anomalies Research Center, The University of Iowa, Iowa City, IA 52242, USA
| | - Maria Sanz Navarro
- Developmental Biology Program, Institute of Biotechnology, University of Helsinki, 00790 Helsinki, Finland
| | - Mason Sweat
- Department of Anatomy and Cell Biology, and the Craniofacial Anomalies Research Center, The University of Iowa, Iowa City, IA 52242, USA
| | - Steven Eliason
- Department of Anatomy and Cell Biology, and the Craniofacial Anomalies Research Center, The University of Iowa, Iowa City, IA 52242, USA
| | - Thad Sharp
- Department of Anatomy and Cell Biology, and the Craniofacial Anomalies Research Center, The University of Iowa, Iowa City, IA 52242, USA
| | - Huan Liu
- Department of Anatomy and Cell Biology, and the Craniofacial Anomalies Research Center, The University of Iowa, Iowa City, IA 52242, USA
- State Key Laboratory Breeding Base of Basic Science of Stomatology (Hubei-MOST) and Key Laboratory for Oral Biomedicine of Ministry of Education, School and Hospital of Stomatology, Wuhan University, Wuhan 430079, P.R.China
| | - Kerstin Seidel
- Department of Orofacial Sciences and Program in Craniofacial Biology, UCSF, San Francisco, CA 94143-0442, USA
| | - Li Zhang
- State Key Laboratory Breeding Base of Basic Science of Stomatology (Hubei-MOST) and Key Laboratory for Oral Biomedicine of Ministry of Education, School and Hospital of Stomatology, Wuhan University, Wuhan 430079, P.R.China
| | - Myriam Moreno
- Department of Anatomy and Cell Biology, and the Craniofacial Anomalies Research Center, The University of Iowa, Iowa City, IA 52242, USA
| | - Thomas Lynch
- Department of Anatomy and Cell Biology, and the Craniofacial Anomalies Research Center, The University of Iowa, Iowa City, IA 52242, USA
| | - Nathan E Holton
- Iowa Institute for Oral Health Research, College of Dentistry, The University of Iowa, Iowa City, IA 52242, USA
| | - Laura Rogers
- Department of Anatomy and Cell Biology, and the Craniofacial Anomalies Research Center, The University of Iowa, Iowa City, IA 52242, USA
| | - Traci Neff
- Department of Anatomy and Cell Biology, and the Craniofacial Anomalies Research Center, The University of Iowa, Iowa City, IA 52242, USA
| | - Michael J Goodheart
- Department of Obstetrics and Gynecology, The University of Iowa, Iowa City, IA 52242, USA
| | - Frederic Michon
- Developmental Biology Program, Institute of Biotechnology, University of Helsinki, 00790 Helsinki, Finland
| | - Ophir D Klein
- Department of Orofacial Sciences and Program in Craniofacial Biology, UCSF, San Francisco, CA 94143-0442, USA
| | - Yang Chai
- Center for Craniofacial Molecular Biology, Ostrow School of Dentistry, University of Southern California, Los Angeles, CA 90033, USA
| | - Adam Dupuy
- Department of Anatomy and Cell Biology, and the Craniofacial Anomalies Research Center, The University of Iowa, Iowa City, IA 52242, USA
| | - John F Engelhardt
- Department of Anatomy and Cell Biology, and the Craniofacial Anomalies Research Center, The University of Iowa, Iowa City, IA 52242, USA
| | - Zhi Chen
- State Key Laboratory Breeding Base of Basic Science of Stomatology (Hubei-MOST) and Key Laboratory for Oral Biomedicine of Ministry of Education, School and Hospital of Stomatology, Wuhan University, Wuhan 430079, P.R.China
| | - Brad A Amendt
- Department of Anatomy and Cell Biology, and the Craniofacial Anomalies Research Center, The University of Iowa, Iowa City, IA 52242, USA
- Iowa Institute for Oral Health Research, College of Dentistry, The University of Iowa, Iowa City, IA 52242, USA
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35
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Underwood C, Johanson Z, Smith MM. Cutting blade dentitions in squaliform sharks form by modification of inherited alternate tooth ordering patterns. ROYAL SOCIETY OPEN SCIENCE 2016; 3:160385. [PMID: 28018617 PMCID: PMC5180115 DOI: 10.1098/rsos.160385] [Citation(s) in RCA: 16] [Impact Index Per Article: 1.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Subscribe] [Scholar Register] [Received: 05/31/2016] [Accepted: 11/04/2016] [Indexed: 05/25/2023]
Abstract
The squaliform sharks represent one of the most speciose shark clades. Many adult squaliforms have blade-like teeth, either on both jaws or restricted to the lower jaw, forming a continuous, serrated blade along the jaw margin. These teeth are replaced as a single unit and successor teeth lack the alternate arrangement present in other elasmobranchs. Micro-CT scans of embryos of squaliforms and a related outgroup (Pristiophoridae) revealed that the squaliform dentition pattern represents a highly modified version of tooth replacement seen in other clades. Teeth of Squalus embryos are arranged in an alternate pattern, with successive tooth rows containing additional teeth added proximally. Asynchronous timing of tooth production along the jaw and tooth loss prior to birth cause teeth to align in oblique sets containing teeth from subsequent rows; these become parallel to the jaw margin during ontogeny, so that adult Squalus has functional tooth rows comprising obliquely stacked teeth of consecutive developmental rows. In more strongly heterodont squaliforms, initial embryonic lower teeth develop into the oblique functional sets seen in adult Squalus, with no requirement to form, and subsequently lose, teeth arranged in an initial alternate pattern.
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Affiliation(s)
- Charlie Underwood
- Department of Earth and Planetary Sciences, Birkbeck, University of London, London, UK
- Department of Earth Sciences, Natural History Museum, London, UK
| | - Zerina Johanson
- Department of Earth and Planetary Sciences, Birkbeck, University of London, London, UK
| | - Moya Meredith Smith
- Department of Earth and Planetary Sciences, Birkbeck, University of London, London, UK
- Dental Institute, Craniofacial Development, King's College London, London, UK
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36
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The stem osteichthyan Andreolepis and the origin of tooth replacement. Nature 2016; 539:237-241. [PMID: 27750278 DOI: 10.1038/nature19812] [Citation(s) in RCA: 19] [Impact Index Per Article: 2.1] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/16/2015] [Accepted: 08/25/2016] [Indexed: 02/02/2023]
Abstract
The teeth of gnathostomes (jawed vertebrates) show rigidly patterned, unidirectional replacement that may or may not be associated with a shedding mechanism. These mechanisms, which are critical for the maintenance of the dentition, are incongruently distributed among extant gnathostomes. Although a permanent tooth-generating dental lamina is present in all chondrichthyans, many tetrapods and some teleosts, it is absent in the non-teleost actinopterygians. Tooth-shedding by basal hard tissue resorption occurs in most osteichthyans (including tetrapods) but not in chondrichthyans. Here we report a three-dimensional virtual dissection of the dentition of a 424-million-year-old stem osteichthyan, Andreolepis hedei, using propagation phase-contrast synchrotron microtomography, with a reconstruction of its growth history. Andreolepis, close to the common ancestor of all extant osteichthyans, shed its teeth by basal resorption but probably lacked a permanent dental lamina. This is the earliest documented instance of resorptive tooth shedding and may represent the primitive osteichthyan mode of tooth replacement.
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37
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Tsai S, Abdelhamid A, Khan MK, Elkarargy A, Widelitz RB, Chuong CM, Wu P. The Molecular Circuit Regulating Tooth Development in Crocodilians. J Dent Res 2016; 95:1501-1510. [PMID: 27872325 DOI: 10.1177/0022034516667724] [Citation(s) in RCA: 5] [Impact Index Per Article: 0.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/28/2023] Open
Abstract
Alligators have robust regenerative potential for tooth renewal. In contrast, extant mammals can either renew their teeth once (diphyodont dentition, as found in humans) or not at all (monophyodont dentition, present in mice). Previously, the authors used multiple mitotic labeling to map putative stem cells in alligator dental laminae, which contain quiescent odontogenic progenitors. The authors demonstrated that alligator tooth cycle initiation is related to β-catenin/Wnt pathway activity in the dental lamina bulge. However, the molecular circuitry underlying the developmental progression of polyphyodont teeth remains elusive. Here, the authors used transcriptomic analyses to examine the additional molecular pathways related to the process of alligator tooth development. The authors collected juvenile alligator dental laminae at different developmental stages and performed RNA-seq. This data shows that Wnt, bone morphogenetic protein (BMP), and fibroblast growth factor (FGF) pathways are activated at the transition from pre-initiation stage (bud) to initiation stage (cap). Intriguingly, the activation of Wnt ligands, receptors and co-activators accompanies the inactivation of Wnt antagonists. In addition, the authors identified the molecular circuitry at different stages of tooth development. The authors conclude that multiple pathways are associated with specific stages of tooth development in the alligator. This data shows that Wnt pathway activation may play the most important role in the initiation of tooth development. This result may offer insight into ways to modulate the genetic controls involved in mammalian tooth renewal.
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Affiliation(s)
- S Tsai
- Department of Pathology, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA.,Ostrow School of Dentistry, University of Southern California, Los Angeles, CA, USA.,Graduate School of Clinical Dentistry, National Taiwan University, Taipei, Taiwan.,Research Center for Developmental Biology and Regenerative Medicine, National Taiwan University, Taipei, Taiwan
| | - A Abdelhamid
- Qassim College of Dentistry, Qassim University, Saudi Arabia
| | - M K Khan
- Qassim College of Dentistry, Qassim University, Saudi Arabia
| | - A Elkarargy
- Qassim College of Dentistry, Qassim University, Saudi Arabia
| | - R B Widelitz
- Department of Pathology, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA
| | - C M Chuong
- Department of Pathology, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA.,Research Center for Developmental Biology and Regenerative Medicine, National Taiwan University, Taipei, Taiwan.,Integrative Stem Cell Center, China Medical University Hospital, China Medical University, Taichung, Taiwan
| | - P Wu
- Department of Pathology, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA
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38
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Mitsiadis TA, Orsini G. Editorial: A New Era in Dentistry: Stem Cell-Based Approaches for Tooth and Periodontal Tissue Regeneration. Front Physiol 2016; 7:357. [PMID: 27594843 PMCID: PMC4990556 DOI: 10.3389/fphys.2016.00357] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/15/2016] [Accepted: 08/04/2016] [Indexed: 11/13/2022] Open
Affiliation(s)
- Thimios A Mitsiadis
- Orofacial Development and Regeneration, Centre for Dental Medicine, Institute of Oral Biology, University of Zurich Zurich, Switzerland
| | - Giovanna Orsini
- Department of Clinical Sciences and Stomatology, Polytechnic University of Marche Ancona, Italy
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39
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Ellis NA, Donde NN, Miller CT. Early development and replacement of the stickleback dentition. J Morphol 2016; 277:1072-83. [PMID: 27145214 PMCID: PMC5298556 DOI: 10.1002/jmor.20557] [Citation(s) in RCA: 9] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/09/2016] [Revised: 04/12/2016] [Accepted: 04/17/2016] [Indexed: 11/09/2022]
Abstract
Teeth have long served as a model system to study basic questions about vertebrate organogenesis, morphogenesis, and evolution. In nonmammalian vertebrates, teeth typically regenerate throughout adult life. Fish have evolved a tremendous diversity in dental patterning in both their oral and pharyngeal dentitions, offering numerous opportunities to study how morphology develops, regenerates, and evolves in different lineages. Threespine stickleback fish (Gasterosteus aculeatus) have emerged as a new system to study how morphology evolves, and provide a particularly powerful system to study the development and evolution of dental morphology. Here, we describe the oral and pharyngeal dentitions of stickleback fish, providing additional morphological, histological, and molecular evidence for homology of oral and pharyngeal teeth. Focusing on the ventral pharyngeal dentition in a dense developmental time course of lab-reared fish, we describe the temporal and spatial consensus sequence of early tooth formation. Early in development, this sequence is highly stereotypical and consists of seventeen primary teeth forming the early tooth field, followed by the first tooth replacement event. Comparing this detailed morphological and ontogenetic sequence to that described in other fish reveals that major changes to how dental morphology arises and regenerates have evolved across different fish lineages. J. Morphol. 277:1072-1083, 2016. © 2016 Wiley Periodicals, Inc.
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Affiliation(s)
- Nicholas A. Ellis
- Department of Molecular and Cell Biology, University of California-Berkeley, Berkeley CA, 94720, USA
| | - Nikunj N. Donde
- Department of Molecular and Cell Biology, University of California-Berkeley, Berkeley CA, 94720, USA
| | - Craig T. Miller
- Department of Molecular and Cell Biology, University of California-Berkeley, Berkeley CA, 94720, USA
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40
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Popa EM, Anthwal N, Tucker AS. Complex patterns of tooth replacement revealed in the fruit bat (Eidolon helvum). J Anat 2016; 229:847-856. [PMID: 27444818 DOI: 10.1111/joa.12522] [Citation(s) in RCA: 12] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Accepted: 06/21/2016] [Indexed: 12/17/2022] Open
Abstract
How teeth are replaced during normal growth and development has long been an important question for comparative and developmental anatomy. Non-standard model animals have become increasingly popular in this field due to the fact that the canonical model laboratory mammal, the mouse, develops only one generation of teeth (monophyodonty), whereas the majority of mammals possess two generations of teeth (diphyodonty). Here we used the straw-coloured fruit bat (Eidolon helvum), an Old World megabat, which has two generations of teeth, in order to observe the development and replacement of tooth germs from initiation up to mineralization stages. Our morphological study uses 3D reconstruction of histological sections to uncover differing arrangements of the first and second-generation tooth germs during the process of tooth replacement. We show that both tooth germ generations develop as part of the dental lamina, with the first generation detaching from the lamina, leaving the free edge to give rise to a second generation. This separation was particularly marked at the third premolar locus, where the primary and replacement teeth become positioned side by side, unconnected by a lamina. The position of the replacement tooth, with respect to the primary tooth, varied within the mouth, with replacements forming posterior to or directly lingual to the primary tooth. Development of replacement teeth was arrested at some tooth positions and this appeared to be linked to the timing of tooth initiation and the subsequent rate of development. This study adds an additional species to the growing body of non-model species used in the study of tooth replacement, and offers a new insight into the development of the diphyodont condition.
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Affiliation(s)
- Elena M Popa
- Department of Craniofacial Development and Stem Cell Biology, King's College London, Guy's Hospital, London, UK
| | - Neal Anthwal
- Department of Craniofacial Development and Stem Cell Biology, King's College London, Guy's Hospital, London, UK
| | - Abigail S Tucker
- Department of Craniofacial Development and Stem Cell Biology, King's College London, Guy's Hospital, London, UK
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41
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Grieco TM, Hlusko LJ. Insight from Frogs: Sonic Hedgehog Gene Expression and a Re-evaluation of the Vertebrate Odontogenic Band. Anat Rec (Hoboken) 2016; 299:1099-109. [DOI: 10.1002/ar.23378] [Citation(s) in RCA: 5] [Impact Index Per Article: 0.6] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/14/2014] [Revised: 03/26/2016] [Accepted: 03/30/2016] [Indexed: 02/04/2023]
Affiliation(s)
- Theresa M. Grieco
- Department of Oral Health Sciences; Life Sciences Institute, University of British Columbia; Vancouver British Columbia Canada
| | - Leslea J. Hlusko
- Department of Integrative Biology; University of California Berkeley; Berkeley California
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42
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Vandenplas S, Vandeghinste R, Boutet A, Mazan S, Huysseune A. Slow cycling cells in the continuous dental lamina of Scyliorhinus canicula: new evidence for stem cells in sharks. Dev Biol 2016; 413:39-49. [DOI: 10.1016/j.ydbio.2016.03.004] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/15/2015] [Revised: 02/29/2016] [Accepted: 03/07/2016] [Indexed: 01/06/2023]
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43
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Vandenplas S, Willems M, Witten PE, Hansen T, Fjelldal PG, Huysseune A. Epithelial Label-Retaining Cells Are Absent during Tooth Cycling in Salmo salar and Polypterus senegalus. PLoS One 2016; 11:e0152870. [PMID: 27049953 PMCID: PMC4822771 DOI: 10.1371/journal.pone.0152870] [Citation(s) in RCA: 8] [Impact Index Per Article: 0.9] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/25/2015] [Accepted: 03/21/2016] [Indexed: 01/17/2023] Open
Abstract
The Atlantic salmon (Salmo salar) and African bichir (Polypterus senegalus) are both actinopterygian fish species that continuously replace their teeth without the involvement of a successional dental lamina. Instead, they share the presence of a middle dental epithelium: an epithelial tier enclosed by inner and outer dental epithelium. It has been hypothesized that this tier could functionally substitute for a successional dental lamina and might be a potential niche to house epithelial stem cells involved in tooth cycling. Therefore, in this study we performed a BrdU pulse chase experiment on both species to (1) determine the localization and extent of proliferating cells in the dental epithelial layers, (2) describe cell dynamics and (3) investigate if label-retaining cells are present, suggestive for the putative presence of stem cells. Cells proliferate in the middle dental epithelium, outer dental epithelium and cervical loop at the lingual side of the dental organ to form a new tooth germ. Using long chase times, both in S. salar (eight weeks) and P. senegalus (eight weeks and twelve weeks), we could not reveal the presence of label-retaining cells in the dental organ. Immunostaining of P. senegalus dental organs for the transcription factor Sox2, often used as a stem cell marker, labelled cells in the zone of outer dental epithelium which grades into the oral epithelium (ODE transition zone) and the inner dental epithelium of a successor only. The location of Sox2 distribution does not provide evidence for epithelial stem cells in the dental organ and, more specifically, in the middle dental epithelium. Comparison of S. salar and P. senegalus reveals shared traits in tooth cycling and thus advances our understanding of the developmental mechanism that ensures lifelong replacement.
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Affiliation(s)
- Sam Vandenplas
- Evolutionary Developmental Biology, Ghent University, Ghent, Belgium
| | - Maxime Willems
- Pharmaceutical technology, Ghent University, Ghent, Belgium
| | - P. Eckhard Witten
- Evolutionary Developmental Biology, Ghent University, Ghent, Belgium
| | - Tom Hansen
- Institute of Marine Research (IMR), Matre Research Station, Matredal, Norway
| | - Per Gunnar Fjelldal
- Institute of Marine Research (IMR), Matre Research Station, Matredal, Norway
| | - Ann Huysseune
- Evolutionary Developmental Biology, Ghent University, Ghent, Belgium
- * E-mail:
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44
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Rasch LJ, Martin KJ, Cooper RL, Metscher BD, Underwood CJ, Fraser GJ. An ancient dental gene set governs development and continuous regeneration of teeth in sharks. Dev Biol 2016; 415:347-370. [PMID: 26845577 DOI: 10.1016/j.ydbio.2016.01.038] [Citation(s) in RCA: 70] [Impact Index Per Article: 7.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/30/2015] [Revised: 01/11/2016] [Accepted: 01/29/2016] [Indexed: 12/20/2022]
Abstract
The evolution of oral teeth is considered a major contributor to the overall success of jawed vertebrates. This is especially apparent in cartilaginous fishes including sharks and rays, which develop elaborate arrays of highly specialized teeth, organized in rows and retain the capacity for life-long regeneration. Perpetual regeneration of oral teeth has been either lost or highly reduced in many other lineages including important developmental model species, so cartilaginous fishes are uniquely suited for deep comparative analyses of tooth development and regeneration. Additionally, sharks and rays can offer crucial insights into the characters of the dentition in the ancestor of all jawed vertebrates. Despite this, tooth development and regeneration in chondrichthyans is poorly understood and remains virtually uncharacterized from a developmental genetic standpoint. Using the emerging chondrichthyan model, the catshark (Scyliorhinus spp.), we characterized the expression of genes homologous to those known to be expressed during stages of early dental competence, tooth initiation, morphogenesis, and regeneration in bony vertebrates. We have found that expression patterns of several genes from Hh, Wnt/β-catenin, Bmp and Fgf signalling pathways indicate deep conservation over ~450 million years of tooth development and regeneration. We describe how these genes participate in the initial emergence of the shark dentition and how they are redeployed during regeneration of successive tooth generations. We suggest that at the dawn of the vertebrate lineage, teeth (i) were most likely continuously regenerative structures, and (ii) utilised a core set of genes from members of key developmental signalling pathways that were instrumental in creating a dental legacy redeployed throughout vertebrate evolution. These data lay the foundation for further experimental investigations utilizing the unique regenerative capacity of chondrichthyan models to answer evolutionary, developmental, and regenerative biological questions that are impossible to explore in classical models.
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Affiliation(s)
- Liam J Rasch
- Department of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, United Kingdom
| | - Kyle J Martin
- Department of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, United Kingdom
| | - Rory L Cooper
- Department of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, United Kingdom
| | - Brian D Metscher
- Department of Theoretical Biology, University of Vienna, Vienna A-1090, Austria
| | - Charlie J Underwood
- Department of Earth and Planetary Sciences, Birkbeck, University of London, London WC1E 7HX, United Kingdom
| | - Gareth J Fraser
- Department of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, United Kingdom.
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45
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Gaete M, Fons JM, Popa EM, Chatzeli L, Tucker AS. Epithelial topography for repetitive tooth formation. Biol Open 2015; 4:1625-34. [PMID: 26538639 PMCID: PMC4736031 DOI: 10.1242/bio.013672] [Citation(s) in RCA: 17] [Impact Index Per Article: 1.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/20/2022] Open
Abstract
During the formation of repetitive ectodermally derived organs such as mammary glands, lateral line and teeth, the tissue primordium iteratively initiates new structures. In the case of successional molar development, new teeth appear sequentially in the posterior region of the jaw from Sox2+ cells in association with the posterior aspect of a pre-existing tooth. The sequence of molar development is well known, however, the epithelial topography involved in the formation of a new tooth is unclear. Here, we have examined the morphology of the molar dental epithelium and its development at different stages in the mouse in vivo and in molar explants. Using regional lineage tracing we show that within the posterior tail of the first molar the primordium for the second and third molar are organized in a row, with the tail remaining in connection with the surface, where a furrow is observed. The morphology and Sox2 expression of the tail retains characteristics reminiscent of the earlier stages of tooth development, such that position along the A-P axes of the tail correlates with different temporal stages. Sox9, a stem/progenitor cell marker in other organs, is expressed mainly in the suprabasal epithelium complementary with Sox2 expression. This Sox2 and Sox9 expressing molar tail contains actively proliferating cells with mitosis following an apico-basal direction. Snail2, a transcription factor implicated in cell migration, is expressed at high levels in the tip of the molar tail while E-cadherin and laminin are decreased. In conclusion, our studies propose a model in which the epithelium of the molar tail can grow by posterior movement of epithelial cells followed by infolding and stratification involving a population of Sox2+/Sox9+ cells. Summary: This study proposes a model for repetitive tooth formation in which the epithelium can grow by the movement of epithelial cells followed by infolding and stratification of Sox2/Sox9 positive cells.
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Affiliation(s)
- Marcia Gaete
- Department of Craniofacial Development and Stem Cell Biology, King's College London, London SE1 9RT, UK Department of Anatomy, Faculty of Medicine, Pontificia Universidad Católica de Chile, Santiago 8331150, Chile
| | - Juan Manuel Fons
- Department of Craniofacial Development and Stem Cell Biology, King's College London, London SE1 9RT, UK
| | - Elena Mădălina Popa
- Department of Craniofacial Development and Stem Cell Biology, King's College London, London SE1 9RT, UK
| | - Lemonia Chatzeli
- Department of Craniofacial Development and Stem Cell Biology, King's College London, London SE1 9RT, UK
| | - Abigail S Tucker
- Department of Craniofacial Development and Stem Cell Biology, King's College London, London SE1 9RT, UK
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46
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Yu T, Volponi AA, Babb R, An Z, Sharpe PT. Stem Cells in Tooth Development, Growth, Repair, and Regeneration. Curr Top Dev Biol 2015; 115:187-212. [PMID: 26589926 DOI: 10.1016/bs.ctdb.2015.07.010] [Citation(s) in RCA: 43] [Impact Index Per Article: 4.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/21/2022]
Abstract
Human teeth contain stem cells in all their mesenchymal-derived tissues, which include the pulp, periodontal ligament, and developing roots, in addition to the support tissues such as the alveolar bone. The precise roles of these cells remain poorly understood and most likely involve tissue repair mechanisms but their relative ease of harvesting makes teeth a valuable potential source of mesenchymal stem cells (MSCs) for therapeutic use. These dental MSC populations all appear to have the same developmental origins, being derived from cranial neural crest cells, a population of embryonic stem cells with multipotential properties. In rodents, the incisor teeth grow continuously throughout life, a feature that requires populations of continuously active mesenchymal and epithelial stem cells. The discrete locations of these stem cells in the incisor have rendered them amenable for study and much is being learnt about the general properties of these stem cells for the incisor as a model system. The incisor MSCs appear to be a heterogeneous population consisting of cells from different neural crest-derived tissues. The epithelial stem cells can be traced directly back in development to a Sox10(+) population present at the time of tooth initiation. In this review, we describe the basic biology of dental stem cells, their functions, and potential clinical uses.
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Affiliation(s)
- Tian Yu
- Craniofacial Development and Stem Cell Biology, Dental Institute, Kings College London, London, United Kingdom
| | - Ana Angelova Volponi
- Craniofacial Development and Stem Cell Biology, Dental Institute, Kings College London, London, United Kingdom
| | - Rebecca Babb
- Craniofacial Development and Stem Cell Biology, Dental Institute, Kings College London, London, United Kingdom
| | - Zhengwen An
- Craniofacial Development and Stem Cell Biology, Dental Institute, Kings College London, London, United Kingdom
| | - Paul T Sharpe
- Craniofacial Development and Stem Cell Biology, Dental Institute, Kings College London, London, United Kingdom.
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47
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Welten M, Smith MM, Underwood C, Johanson Z. Evolutionary origins and development of saw-teeth on the sawfish and sawshark rostrum (Elasmobranchii; Chondrichthyes). ROYAL SOCIETY OPEN SCIENCE 2015; 2:150189. [PMID: 26473044 PMCID: PMC4593678 DOI: 10.1098/rsos.150189] [Citation(s) in RCA: 11] [Impact Index Per Article: 1.1] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Subscribe] [Scholar Register] [Received: 05/06/2015] [Accepted: 08/06/2015] [Indexed: 05/31/2023]
Abstract
A well-known characteristic of chondrichthyans (e.g. sharks, rays) is their covering of external skin denticles (placoid scales), but less well understood is the wide morphological diversity that these skin denticles can show. Some of the more unusual of these are the tooth-like structures associated with the elongate cartilaginous rostrum 'saw' in three chondrichthyan groups: Pristiophoridae (sawsharks; Selachii), Pristidae (sawfish; Batoidea) and the fossil Sclerorhynchoidea (Batoidea). Comparative topographic and developmental studies of the 'saw-teeth' were undertaken in adults and embryos of these groups, by means of three-dimensional-rendered volumes from X-ray computed tomography. This provided data on development and relative arrangement in embryos, with regenerative replacement in adults. Saw-teeth are morphologically similar on the rostra of the Pristiophoridae and the Sclerorhynchoidea, with the same replacement modes, despite the lack of a close phylogenetic relationship. In both, tooth-like structures develop under the skin of the embryos, aligned with the rostrum surface, before rotating into lateral position and then attaching through a pedicel to the rostrum cartilage. As well, saw-teeth are replaced and added to as space becomes available. By contrast, saw-teeth in Pristidae insert into sockets in the rostrum cartilage, growing continuously and are not replaced. Despite superficial similarity to oral tooth developmental organization, saw-tooth spatial initiation arrangement is associated with rostrum growth. Replacement is space-dependent and more comparable to that of dermal skin denticles. We suggest these saw-teeth represent modified dermal denticles and lack the 'many-for-one' replacement characteristic of elasmobranch oral dentitions.
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Affiliation(s)
- Monique Welten
- Department of Earth Sciences, Natural History Museum, London, UK
| | - Moya Meredith Smith
- Department of Earth Sciences, Natural History Museum, London, UK
- Dental Institute, Tissue Engineering and Biophotonics, King's College London, University of London, London, UK
| | - Charlie Underwood
- Department of Earth and Planetary Sciences, Birkbeck, University of London, London, UK
| | - Zerina Johanson
- Department of Earth Sciences, Natural History Museum, London, UK
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48
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Ellis NA, Glazer AM, Donde NN, Cleves PA, Agoglia RM, Miller CT. Distinct developmental genetic mechanisms underlie convergently evolved tooth gain in sticklebacks. Development 2015; 142:2442-51. [PMID: 26062935 DOI: 10.1242/dev.124248] [Citation(s) in RCA: 36] [Impact Index Per Article: 3.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/11/2015] [Accepted: 06/02/2015] [Indexed: 12/14/2022]
Abstract
Teeth are a classic model system of organogenesis, as repeated and reciprocal epithelial and mesenchymal interactions pattern placode formation and outgrowth. Less is known about the developmental and genetic bases of tooth formation and replacement in polyphyodonts, which are vertebrates with continual tooth replacement. Here, we leverage natural variation in the threespine stickleback fish Gasterosteus aculeatus to investigate the genetic basis of tooth development and replacement. We find that two derived freshwater stickleback populations have both convergently evolved more ventral pharyngeal teeth through heritable genetic changes. In both populations, evolved tooth gain manifests late in development. Using pulse-chase vital dye labeling to mark newly forming teeth in adult fish, we find that both high-toothed freshwater populations have accelerated tooth replacement rates relative to low-toothed ancestral marine fish. Despite the similar evolved phenotype of more teeth and an accelerated adult replacement rate, the timing of tooth number divergence and the spatial patterns of newly formed adult teeth are different in the two populations, suggesting distinct developmental mechanisms. Using genome-wide linkage mapping in marine-freshwater F2 genetic crosses, we find that the genetic basis of evolved tooth gain in the two freshwater populations is largely distinct. Together, our results support a model whereby increased tooth number and an accelerated tooth replacement rate have evolved convergently in two independently derived freshwater stickleback populations using largely distinct developmental and genetic mechanisms.
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Affiliation(s)
- Nicholas A Ellis
- Department of Molecular and Cell Biology, University of California-Berkeley, Berkeley, CA 94720, USA
| | - Andrew M Glazer
- Department of Molecular and Cell Biology, University of California-Berkeley, Berkeley, CA 94720, USA
| | - Nikunj N Donde
- Department of Molecular and Cell Biology, University of California-Berkeley, Berkeley, CA 94720, USA
| | - Phillip A Cleves
- Department of Molecular and Cell Biology, University of California-Berkeley, Berkeley, CA 94720, USA
| | - Rachel M Agoglia
- Department of Molecular and Cell Biology, University of California-Berkeley, Berkeley, CA 94720, USA
| | - Craig T Miller
- Department of Molecular and Cell Biology, University of California-Berkeley, Berkeley, CA 94720, USA
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49
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Dosedělová H, Dumková J, Lesot H, Glocová K, Kunová M, Tucker AS, Veselá I, Krejčí P, Tichý F, Hampl A, Buchtová M. Fate of the molar dental lamina in the monophyodont mouse. PLoS One 2015; 10:e0127543. [PMID: 26010446 PMCID: PMC4444311 DOI: 10.1371/journal.pone.0127543] [Citation(s) in RCA: 26] [Impact Index Per Article: 2.6] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/04/2014] [Accepted: 04/16/2015] [Indexed: 11/19/2022] Open
Abstract
The successional dental lamina (SDL) plays an essential role in the development of replacement teeth in diphyodont and polyphyodont animals. A morphologically similar structure, the rudimental successional dental lamina (RSDL), has been described in monophyodont (only one tooth generation) lizards on the lingual side of the developing functional tooth. This rudimentary lamina regresses, which has been proposed to play a role in preventing the formation of future generations of teeth. A similar rudimentary lingual structure has been reported associated with the first molar in the monophyodont mouse, and we show that this structure is common to all murine molars. Intriguingly, a lingual lamina is also observed on the non-replacing molars of other diphyodont mammals (pig and hedgehog), initially appearing very similar to the successional dental lamina on the replacing teeth. We have analyzed the morphological as well as ultrastructural changes that occur during the development and loss of this molar lamina in the mouse, from its initiation at late embryonic stages to its disappearance at postnatal stages. We show that loss appears to be driven by a reduction in cell proliferation, down-regulation of the progenitor marker Sox2, with only a small number of cells undergoing programmed cell death. The lingual lamina was associated with the dental stalk, a short epithelial connection between the tooth germ and the oral epithelium. The dental stalk remained in contact with the oral epithelium throughout tooth development up to eruption when connective tissue and numerous capillaries progressively invaded the dental stalk. The buccal side of the dental stalk underwent keratinisation and became part of the gingival epithelium, while most of the lingual cells underwent programmed cell death and the tissue directly above the erupting tooth was shed into the oral cavity.
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Affiliation(s)
- Hana Dosedělová
- Department of Anatomy, Histology and Embryology, Faculty of Veterinary Medicine, University of Veterinary and Pharmaceutical Sciences, Brno, Czech Republic
- Institute of Animal Physiology and Genetics, v.v.i., Academy of Sciences of the Czech Republic, Brno, Czech Republic
| | - Jana Dumková
- Department of Histology and Embryology, Faculty of Medicine, Masaryk University, Brno, Czech Republic
| | - Hervé Lesot
- INSERM UMR1109, Team "Osteoarticular and Dental Regenerative NanoMedicine", Université de Strasbourg, Strasbourg, France
- Faculté de Chirurgie Dentaire, Université de Strasbourg, Strasbourg, France
| | - Kristýna Glocová
- Department of Anatomy, Histology and Embryology, Faculty of Veterinary Medicine, University of Veterinary and Pharmaceutical Sciences, Brno, Czech Republic
| | - Michaela Kunová
- Department of Biology, Faculty of Medicine, Masaryk University, Brno, Czech Republic
| | - Abigail S. Tucker
- Department of Craniofacial Development and Stem Cell Biology, King´s College London, London, United Kingdom
- Department of Orthodontics, King´s College London Dental Institute, London, United Kingdom
| | - Iva Veselá
- Department of Anatomy, Histology and Embryology, Faculty of Veterinary Medicine, University of Veterinary and Pharmaceutical Sciences, Brno, Czech Republic
- Institute of Animal Physiology and Genetics, v.v.i., Academy of Sciences of the Czech Republic, Brno, Czech Republic
| | - Pavel Krejčí
- Department of Biology, Faculty of Medicine, Masaryk University, Brno, Czech Republic
| | - František Tichý
- Department of Anatomy, Histology and Embryology, Faculty of Veterinary Medicine, University of Veterinary and Pharmaceutical Sciences, Brno, Czech Republic
| | - Aleš Hampl
- Department of Histology and Embryology, Faculty of Medicine, Masaryk University, Brno, Czech Republic
| | - Marcela Buchtová
- Department of Anatomy, Histology and Embryology, Faculty of Veterinary Medicine, University of Veterinary and Pharmaceutical Sciences, Brno, Czech Republic
- Institute of Animal Physiology and Genetics, v.v.i., Academy of Sciences of the Czech Republic, Brno, Czech Republic
- Department of Experimental Biology, Faculty of Science, Masaryk University, Brno, Czech Republic
- * E-mail:
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Distinctive genetic activity pattern of the human dental pulp between deciduous and permanent teeth. PLoS One 2014; 9:e102893. [PMID: 25047033 PMCID: PMC4105481 DOI: 10.1371/journal.pone.0102893] [Citation(s) in RCA: 17] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/18/2014] [Accepted: 06/23/2014] [Indexed: 11/19/2022] Open
Abstract
Human deciduous and permanent teeth exhibit different developmental processes, morphologies, histological characteristics and life cycles. In addition, their pulp tissues react differently to external stimuli, such as the pulp sensitivity test, dental trauma and pulp therapy materials. These suggest differences in gene expression and regulation, and in this study we compared gene-expression profiles of the human dental pulp from deciduous and permanent teeth. Pulp tissues from permanent premolars and deciduous molars aged 11–14 years were extirpated and mRNA was isolated for cDNA microarray analysis, and quantitative real-time PCR (qPCR). Other teeth were used for immunohistochemical analysis (IHC). Microarray analysis identified 263 genes with a twofold or greater difference in expression level between the two types of pulp tissue, 43 and 220 of which were more abundant in deciduous and permanent pulp tissues, respectively. qPCR analysis was conducted for eight randomly selected genes, and the findings were consistent with the cDNA microarray results. IHC confirmed that insulin-like growth factor 2 mRNA-binding protein 1 (IGF2BP1) was broadly expressed in deciduous dental pulp tissue, but minimally expressed in permanent dental pulp tissue. Immunohistochemical analysis showed that calbindin 1 (CALB1), leucine-rich repeat-containing G-protein-coupled receptor 5 (LGR5), and gamma-aminobutyric acid A receptor beta 1 (GABRB1) were abundantly expressed in permanent predentin/odontoblasts, but only minimally expressed in deciduous dental pulp tissue. These results show that deciduous and permanent pulp tissues have different characteristics and gene expression, suggesting that they may have different functions and responses to therapies focused on pulp or dentin regeneration.
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