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1
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Pham-Bui HA, Lee M. Germ granule-mediated mRNA storage and translational control. RNA Biol 2025; 22:1-11. [PMID: 39895378 PMCID: PMC11810088 DOI: 10.1080/15476286.2025.2462276] [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: 10/05/2024] [Revised: 12/24/2024] [Accepted: 01/28/2025] [Indexed: 02/04/2025] Open
Abstract
Germ cells depend on specialized post-transcriptional regulation for proper development and function, much of which is mediated by dynamic RNA granules. These membrane-less organelles form through the condensation of RNA and proteins, governed by multivalent biomolecular interactions. RNA granules compartmentalize cellular components, selectively enriching specific factors and modulating biochemical reactions. Over recent decades, various types of RNA granules have been identified in germ cells across species, with extensive studies uncovering their molecular roles and developmental significance. This review explores the mRNA regulatory mechanisms mediated by RNA granules in germ cells. We discuss the distinct spatial organization of specific granule components and the variations in material states of germ granules, which contribute to the regulation of mRNA storage and translation. Additionally, we highlight emerging research on how changes in these material states, during developmental stages, reflect the dynamic nature of germ granules and their critical role in development.
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Affiliation(s)
- Hoang-Anh Pham-Bui
- Soonchunhyang Institute of Medi-Bio Science, Soonchunhyang University, Cheonan-si, Korea
- Department of Integrated Biomedical Science, Soonchunhyang University, Cheonan-si, Korea
| | - Mihye Lee
- Soonchunhyang Institute of Medi-Bio Science, Soonchunhyang University, Cheonan-si, Korea
- Department of Integrated Biomedical Science, Soonchunhyang University, Cheonan-si, Korea
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2
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Maita H, Nakagawa S. Balancing RNA processing and innate immune response: Possible roles for SMN condensates in snRNP biogenesis. Biochim Biophys Acta Gen Subj 2025; 1869:130764. [PMID: 39826814 DOI: 10.1016/j.bbagen.2025.130764] [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: 10/31/2024] [Revised: 01/07/2025] [Accepted: 01/13/2025] [Indexed: 01/22/2025]
Abstract
Biomolecular condensates like U-bodies are specialized cellular structures formed through multivalent interactions among intrinsically disordered regions. U-bodies sequester small nuclear ribonucleoprotein complexes (snRNPs) in the cytoplasm, and their formation in mammalian cells depends on stress conditions. Because of their location adjacent to P-bodies, U-bodies have been considered potential sites for snRNP storage or turnover. SMN, a chaperone for snRNP biogenesis, forms condensates through its Tudor domain. In fly models, defects in SMN trigger innate immune responses similar to those observed with excess cytoplasmic snRNA during viral infection in mammalian cells. Additionally, spinal muscular atrophy (SMA), caused by SMN deficiency, is associated with inflammation. Therefore, SMN may help prevent innate immune aberrant activation due to defective snRNP biogenesis by forming U-bodies to sequester these molecules. Further studies on U-body functions may provide therapeutic insights for diseases related to RNA metabolism.
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Affiliation(s)
- Hiroshi Maita
- Graduate School of Life Science, Hokkaido University, Sapporo 060-0812, Japan; Faculty of Pharmaceutical Sciences, Hokkaido University, Sapporo 060-0812, Japan.
| | - Shinichi Nakagawa
- Graduate School of Life Science, Hokkaido University, Sapporo 060-0812, Japan; Faculty of Pharmaceutical Sciences, Hokkaido University, Sapporo 060-0812, Japan
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3
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Sekula M, Tworzydlo W, Bilinski SM. Balbiani body of basal insects is potentially involved in multiplication and selective elimination of mitochondria. Sci Rep 2024; 14:8263. [PMID: 38594333 PMCID: PMC11004008 DOI: 10.1038/s41598-024-58997-6] [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: 01/03/2024] [Accepted: 04/05/2024] [Indexed: 04/11/2024] Open
Abstract
Oocytes of both vertebrates and invertebrates often contain an intricate organelle assemblage, termed the Balbiani body (Bb). It has previously been suggested that this assemblage is involved in the delivery of organelles and macromolecules to the germ plasm, formation of oocyte reserve materials, and transfer of mitochondria to the next generation. To gain further insight into the function of the Bb, we performed a series of analyses and experiments, including computer-aided 3-dimensional reconstructions, detection of DNA (mtDNA) synthesis as well as immunolocalization studies. We showed that in orthopteran Meconema meridionale, the Bb comprises a network of mitochondria and perinuclear nuage aggregations. As oogenesis progresses, the network expands filling almost entire ooplasm, then partitions into several smaller entities, termed micro-networks, and ultimately into individual mitochondria. As in somatic cells, this process involves microfilaments and elements of endoplasmic reticulum. We showed also that at least some of the individual mitochondria are surrounded by phagophores and eliminated via mitophagy. These findings support the idea that the Bb is implicated in the multiplication and selective elimination of (defective) mitochondria and therefore may participate in the transfer of undamaged (healthy) mitochondria to the next generation.
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Affiliation(s)
- Malgorzata Sekula
- Department of Developmental Biology and Invertebrate Morphology, Institute of Zoology and Biomedical Research, Faculty of Biology, Jagiellonian University in Krakow, Gronostajowa 9, 30-387, Kraków, Poland.
| | - Waclaw Tworzydlo
- Department of Developmental Biology and Invertebrate Morphology, Institute of Zoology and Biomedical Research, Faculty of Biology, Jagiellonian University in Krakow, Gronostajowa 9, 30-387, Kraków, Poland
| | - Szczepan M Bilinski
- Department of Developmental Biology and Invertebrate Morphology, Institute of Zoology and Biomedical Research, Faculty of Biology, Jagiellonian University in Krakow, Gronostajowa 9, 30-387, Kraków, Poland.
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Abstract
A hallmark of all germ cells is the presence of germ granules: assemblies of proteins and RNA that lack a delineating membrane and are proposed to form via condensation. Germ granules across organisms share several conserved components, including factors required for germ cell fate determination and maintenance, and are thought to be linked to germ cell development. The molecular functions of germ granules, however, remain incompletely understood. In this Development at a Glance article, we survey germ granules across organisms and developmental stages, and highlight emerging themes regarding granule regulation, dynamics and proposed functions.
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Affiliation(s)
- Laura Thomas
- HHMI and Department of Molecular Biology and Genetics, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA
| | - Andrea Putnam
- HHMI and Department of Molecular Biology and Genetics, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA
| | - Andrew Folkmann
- HHMI and Department of Molecular Biology and Genetics, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA
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5
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Sekula M, Tworzydlo W, Bilinski SM. Morphology and ultrastructure of the Balbiani body in the oocytes of closely related bush cricket species. Shared features reveal important aspect of functioning. ZOOLOGY 2022; 155:126051. [PMID: 36108419 DOI: 10.1016/j.zool.2022.126051] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/05/2021] [Revised: 08/29/2022] [Accepted: 09/05/2022] [Indexed: 01/25/2023]
Abstract
Balbiani bodies (Bbs) are female germline-specific organelle assemblages usually composed of mitochondria, Golgi complexes, elements of endoplasmic reticulum and accumulations of fine granular material, termed the nuage. Here we present results of morphological and ultrastructural analysis of the Bb of four bush crickets nested in four subfamilies of the family Tettigonidae. This study has revealed that Bbs of closely related species (belonging to the defined evolutionary line) are morphologically rather different. In two species (Meconema meridionale and Pholidoptera griseoaptera) the Bb has the form of a hollow hemisphere that covers a part of the germinal vesicle surface. In contrast, the Bb of Conocephalus fuscus and Leptophyes albovittata is less distinct and surrounds the whole or the majority of the germinal vesicle surface. Aside from this difference, the Bbs of all four studied species are built of identical sets of organelles and, most importantly, share one significant feature: close association of mitochondria and nuage accumulations. We show additionally that mitochondria remaining in direct contact with the nuage are characterized by distinct morphologies e.g. elongated, dumbbell shaped or bifurcated. In the light of our results and literature survey, the ancestral function of the Bb is discussed.
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Affiliation(s)
- Malgorzata Sekula
- Department of Developmental Biology and Invertebrate Morphology, Institute of Zoology and Biomedical Research, Faculty of Biology, Jagiellonian University in Krakow, Gronostajowa 9, 30-387 Krakow, Poland.
| | - Waclaw Tworzydlo
- Department of Developmental Biology and Invertebrate Morphology, Institute of Zoology and Biomedical Research, Faculty of Biology, Jagiellonian University in Krakow, Gronostajowa 9, 30-387 Krakow, Poland
| | - Szczepan M Bilinski
- Department of Developmental Biology and Invertebrate Morphology, Institute of Zoology and Biomedical Research, Faculty of Biology, Jagiellonian University in Krakow, Gronostajowa 9, 30-387 Krakow, Poland
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6
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Carro MDLM, Grimson A, Cohen PE. Small RNAs and their protein partners in animal meiosis. Curr Top Dev Biol 2022; 151:245-279. [PMID: 36681472 DOI: 10.1016/bs.ctdb.2022.06.001] [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] [Indexed: 01/25/2023]
Abstract
Meiosis is characterized by highly regulated transitions in gene expression that require diverse mechanisms of gene regulation. For example, in male mammals, transcription undergoes a global shut-down in early prophase I of meiosis, followed by increasing transcriptional activity into pachynema. Later, as spermiogenesis proceeds, the histones bound to DNA are replaced with transition proteins, which are themselves replaced with protamines, resulting in a highly condensed nucleus with repressed transcriptional activity. In addition, two specialized gene silencing events take place during prophase I: meiotic silencing of unsynapsed chromatin (MSUC), and the sex chromatin specific mechanism, meiotic sex chromosome inactivation (MSCI). Notably, conserved roles for the RNA binding protein (RBP) machinery that functions with small non-coding RNAs have been described as participating in these meiosis-specific mechanisms, suggesting that RNA-mediated gene regulation is critical for fertility in many species. Here, we review roles of small RNAs and their associated RBPs in meiosis-related processes such as centromere function, silencing of unpaired chromatin and meiotic recombination. We will discuss the emerging evidence of non-canonical functions of these components in meiosis.
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Affiliation(s)
- María de Las Mercedes Carro
- Department of Biomedical Sciences, Cornell University, Ithaca, NY, United States; Cornell Reproductive Sciences Center (CoRe), Cornell University, Ithaca, NY, United States
| | - Andrew Grimson
- Cornell Reproductive Sciences Center (CoRe), Cornell University, Ithaca, NY, United States; Department of Molecular Biology & Genetics, Cornell University, Ithaca, NY, United States.
| | - Paula E Cohen
- Department of Biomedical Sciences, Cornell University, Ithaca, NY, United States; Cornell Reproductive Sciences Center (CoRe), Cornell University, Ithaca, NY, United States.
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7
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Quarato P, Singh M, Bourdon L, Cecere G. Inheritance and maintenance of small RNA-mediated epigenetic effects. Bioessays 2022; 44:e2100284. [PMID: 35338497 DOI: 10.1002/bies.202100284] [Citation(s) in RCA: 4] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/06/2021] [Revised: 02/04/2022] [Accepted: 03/15/2022] [Indexed: 11/08/2022]
Abstract
Heritable traits are predominantly encoded within genomic DNA, but it is now appreciated that epigenetic information is also inherited through DNA methylation, histone modifications, and small RNAs. Several examples of transgenerational epigenetic inheritance of traits have been documented in plants and animals. These include even the inheritance of traits acquired through the soma during the life of an organism, implicating the transfer of epigenetic information via the germline to the next generation. Small RNAs appear to play a significant role in carrying epigenetic information across generations. This review focuses on how epigenetic information in the form of small RNAs is transmitted from the germline to the embryos through the gametes. We also consider how inherited epigenetic information is maintained across generations in a small RNA-dependent and independent manner. Finally, we discuss how epigenetic traits acquired from the soma can be inherited through small RNAs.
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Affiliation(s)
- Piergiuseppe Quarato
- Department of Developmental and Stem Cell Biology, Institut Pasteur, Université de Paris, CNRS UMR3738, Mechanisms of Epigenetic Inheritance, Paris, France
| | - Meetali Singh
- Department of Developmental and Stem Cell Biology, Institut Pasteur, Université de Paris, CNRS UMR3738, Mechanisms of Epigenetic Inheritance, Paris, France
| | - Loan Bourdon
- Department of Developmental and Stem Cell Biology, Institut Pasteur, Université de Paris, CNRS UMR3738, Mechanisms of Epigenetic Inheritance, Paris, France
| | - Germano Cecere
- Department of Developmental and Stem Cell Biology, Institut Pasteur, Université de Paris, CNRS UMR3738, Mechanisms of Epigenetic Inheritance, Paris, France
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8
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Chen Y, Fang X, Tian XQ, Cui Z, Feng HY, Qiu GF. Germ plasm and the origin of the primordial germ cells in the oriental river prawn Macrobrachium nipponense. Cell Tissue Res 2021; 386:559-569. [PMID: 34599688 DOI: 10.1007/s00441-021-03534-4] [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: 11/18/2020] [Accepted: 09/21/2021] [Indexed: 11/28/2022]
Abstract
Germ plasm is a special cytoplasmic component containing special RNAs and proteins, and is located in specific regions of oocytes and embryos. Only the blastomeres inheriting the germ plasm can develop into primordial germ cells (PGCs). By using Vasa mRNA as a germline marker, we previously demonstrated that germline specification followed the preformation mode in the prawn Macrobrachium nipponense. In this study, we raised the Vasa antibody to identify germ plasm in the oocyte and trace the origin and migration of PGCs. In previtellogenic oocytes, Vasa protein was detected in the perinuclear region, in which electron-dense granules associated with numerous mitochondria were mostly visualized under a transmission electron microscope. In mature oocytes, immunosignal was localized to a large granule under the plasma membrane. During early embryogenesis, the granule was inherited by a single blastomere from 1-cell to 16-cell stages, and thereafter was segregated into two daughter blastomeres at the 32-cell stage. In gastrula, the Vasa-positive cells were large with typical PGC characteristics, containing a big round nucleus and a prominent nucleolus. The immunosignal was localized to the perinuclear region again. In the zoea stage, the Vasa-positive cells migrated toward the genital ridge and clustered in the dorsomedial region close to the yolk portion. Accordingly, we concluded that the prawn PGCs could be specified from the 16-cell stage by inheriting the germplasm. To our knowledge, this is the first report on the identification of the prawn germ plasm and PGCs. The continuous expression of Vasa protein throughout oogenesis and embryogenesis suggests that Vasa protein could be an important factor in germ plasm that functions in early germ cell specification.
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Affiliation(s)
- Ying Chen
- Key Laboratory of Freshwater Aquatic Genetic Resources, Ministry of Agriculture; National Demonstration Center for Experimental Fisheries Science Education; Shanghai Engineering Research Center of Aquaculture, Shanghai Ocean University, 999 Hucheng Ring Road, Shanghai, 201306, China
| | - Xiang Fang
- Key Laboratory of Freshwater Aquatic Genetic Resources, Ministry of Agriculture; National Demonstration Center for Experimental Fisheries Science Education; Shanghai Engineering Research Center of Aquaculture, Shanghai Ocean University, 999 Hucheng Ring Road, Shanghai, 201306, China
| | - Xiao-Qing Tian
- Key Laboratory of Freshwater Aquatic Genetic Resources, Ministry of Agriculture; National Demonstration Center for Experimental Fisheries Science Education; Shanghai Engineering Research Center of Aquaculture, Shanghai Ocean University, 999 Hucheng Ring Road, Shanghai, 201306, China
| | - Zheng Cui
- Key Laboratory of Freshwater Aquatic Genetic Resources, Ministry of Agriculture; National Demonstration Center for Experimental Fisheries Science Education; Shanghai Engineering Research Center of Aquaculture, Shanghai Ocean University, 999 Hucheng Ring Road, Shanghai, 201306, China
| | - Hai-Yang Feng
- Key Laboratory of Freshwater Aquatic Genetic Resources, Ministry of Agriculture; National Demonstration Center for Experimental Fisheries Science Education; Shanghai Engineering Research Center of Aquaculture, Shanghai Ocean University, 999 Hucheng Ring Road, Shanghai, 201306, China
| | - Gao-Feng Qiu
- Key Laboratory of Freshwater Aquatic Genetic Resources, Ministry of Agriculture; National Demonstration Center for Experimental Fisheries Science Education; Shanghai Engineering Research Center of Aquaculture, Shanghai Ocean University, 999 Hucheng Ring Road, Shanghai, 201306, China.
- College of Fisheries and Life Science, Pudong New Area, Shanghai Ocean University, 999 Hucheng Ring Road, Shanghai, 201306, China.
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9
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Filimonova S. Female reproductive system and oogenesis in the mite Bakericheyla chanayi. ARTHROPOD STRUCTURE & DEVELOPMENT 2021; 62:101047. [PMID: 33770520 DOI: 10.1016/j.asd.2021.101047] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 09/02/2020] [Revised: 02/14/2021] [Accepted: 02/18/2021] [Indexed: 06/12/2023]
Abstract
The fine structure of the female reproductive system of a cheyletid mite Bakericheyla chanayi (Trombidiformes: Cheyletidae) is investigated for the first time. This system consists of an unpaired ovary, glandular oviduct, receptaculum seminis, long cuticle-lined vagina, and genital atrium terminating in the genital opening. A separate sperm access system has not been found. The receptaculum seminis opens into the distal oviduct region, where fertilization apparently takes place. The ovary contains clusters of oogonia (cystocytes), clustered early meiotic cells, a few growing previtellogenic oocytes, and 3 large nurse cells. The dorsal ovarian region is occupied by the clusters of bacteriocytes which harbor symbiotic bacteria. Oocytes undergo vitellogenesis in individual ovarian pouches, each connected to the corresponding nurse cell by an intercellular bridge. The fine structure of the bridge suggests transport between the interconnected cells in the course of vitellogenesis. The population of cystocytes was shown to be heterogenic. The electron-light cells enter meiosis and develop into the oocytes or nurse cells. The electron-dense cystocytes do not show meiotic transformation and probably give rise to the bacteriocytes. The early development of the nurse cells and oocytes is similar and accompanied by the blebbing of the nuclear envelope, appearance of nuage material and Balbiani bodies.
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Affiliation(s)
- Svetlana Filimonova
- Zoological Institute, Russian Academy of Sciences, Saint-Petersburg, Russia.
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Mukherjee N, Mukherjee C. Germ cell ribonucleoprotein granules in different clades of life: From insects to mammals. WILEY INTERDISCIPLINARY REVIEWS-RNA 2021; 12:e1642. [PMID: 33555143 DOI: 10.1002/wrna.1642] [Citation(s) in RCA: 14] [Impact Index Per Article: 3.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Subscribe] [Scholar Register] [Received: 07/12/2020] [Revised: 01/04/2021] [Accepted: 01/05/2021] [Indexed: 12/12/2022]
Abstract
Ribonucleoprotein (RNP) granules are no newcomers in biology. Found in all life forms, ranging across taxa, these membrane-less "organelles" have been classified into different categories based on their composition, structure, behavior, function, and localization. Broadly, they can be listed as stress granules (SGs), processing bodies (PBs), neuronal granules (NGs), and germ cell granules (GCGs). Keeping in line with the topic of this review, RNP granules present in the germ cells have been implicated in a wide range of cellular functions including cellular specification, differentiation, proliferation, and so forth. The mechanisms used by them can be diverse and many of them remain partly obscure and active areas of research. GCGs can be of different types in different organisms and at different stages of development, with multiple types coexisting in the same cell. In this review, the different known subcategories of GCGs have been studied with respect to five distinct model organisms, namely, Drosophila, Caenorhabditis elegans, Xenopus, Zebrafish, and mammals. Of them, the cytoplasmic polar granules in Drosophila, P granules in C. elegans, balbiani body in Xenopus and Zebrafish, and chromatoid bodies in mammals have been specifically emphasized upon. A descriptive account of the same has been provided along with insights into our current understanding of their functional significance with respect to cellular events relating to different developmental and reproductive processes. This article is categorized under: RNA Interactions with Proteins and Other Molecules > RNA-Protein Complexes RNA Export and Localization > RNA Localization RNA in Disease and Development > RNA in Disease.
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Sekula M, Tworzydlo W, Bilinski SM. Morphogenesis of the Balbiani body in developing oocytes of an orthopteran, Metrioptera brachyptera, and multiplication of female germline mitochondria. J Morphol 2020; 281:1142-1151. [PMID: 32767591 DOI: 10.1002/jmor.21242] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/06/2020] [Revised: 06/19/2020] [Accepted: 07/17/2020] [Indexed: 12/23/2022]
Abstract
Balbiani body (Bb) is a female germline specific organelle complex. Although the morphology and morphogenesis of the Bb have been analyzed in numerous vertebrate and invertebrate species, the role and ultimate fate of this organelle assemblage are still under debate. As a result, various functions have been attributed to the Bb in given animal lineages or even species. Our analyses showed that in the bush cricket, Metrioptera brachyptera, the Bb is an elaborate and highly dynamic structure positioned at one side of the oocyte nucleus. It forms in early previtellogenic oocytes and consists of two compartments: perinuclear and cytoplasmic. In the cytoplasmic compartment, characteristic complexes of nuage and polymorphous mitochondria are present. Computer-aided 3D reconstructions revealed that mitochondria clustered around neighboring nuage accumulations remain in a physical contact and form an extensive, though dispersed network. As oogenesis progresses, nuage/mitochondria complexes are partitioned into progressively smaller entities that become separated from each other. Concurrently, the mitochondrial network splits into small individual mitochondria populating the whole ooplasm. Immunohistochemical analysis showed that the latter process involves dynamin-related protein 1 (Drp1). Collectively, our findings suggest that in basal insect species, the Bb might be responsible for the selection as well as multiplication of the oocyte mitochondria.
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Affiliation(s)
- Malgorzata Sekula
- Department of Developmental Biology and Invertebrate Morphology, Institute of Zoology and Biomedical Research, Faculty of Biology, Jagiellonian University in Krakow, Krakow, Poland
| | - Waclaw Tworzydlo
- Department of Developmental Biology and Invertebrate Morphology, Institute of Zoology and Biomedical Research, Faculty of Biology, Jagiellonian University in Krakow, Krakow, Poland
| | - Szczepan M Bilinski
- Department of Developmental Biology and Invertebrate Morphology, Institute of Zoology and Biomedical Research, Faculty of Biology, Jagiellonian University in Krakow, Krakow, Poland
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Hyjek‐Składanowska M, Bajczyk M, Gołębiewski M, Nuc P, Kołowerzo‐Lubnau A, Jarmołowski A, Smoliński DJ. Core spliceosomal Sm proteins as constituents of cytoplasmic mRNPs in plants. THE PLANT JOURNAL : FOR CELL AND MOLECULAR BIOLOGY 2020; 103:1155-1173. [PMID: 32369637 PMCID: PMC7540296 DOI: 10.1111/tpj.14792] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.2] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 12/04/2019] [Revised: 04/13/2020] [Accepted: 04/21/2020] [Indexed: 05/15/2023]
Abstract
In recent years, research has increasingly focused on the key role of post-transcriptional regulation of messenger ribonucleoprotein (mRNP) function and turnover. As a result of the complexity and dynamic nature of mRNPs, the full composition of a single mRNP complex remains unrevealed and mRNPs are poorly described in plants. Here we identify canonical Sm proteins as part of the cytoplasmic mRNP complex, indicating their function in the post-transcriptional regulation of gene expression in plants. Sm proteins comprise an evolutionarily ancient family of small RNA-binding proteins involved in pre-mRNA splicing. The latest research indicates that Sm could also impact on mRNA at subsequent stages of its life cycle. In this work we show that in the microsporocyte cytoplasm of Larix decidua, the European larch, Sm proteins accumulate within distinct cytoplasmic bodies, also containing polyadenylated RNA. To date, several types of cytoplasmic bodies involved in the post-transcriptional regulation of gene expression have been described, mainly in animal cells. Their role and molecular composition in plants remain less well established, however. A total of 222 mRNA transcripts have been identified as cytoplasmic partners for Sm proteins. The specific colocalization of these mRNAs with Sm proteins within cytoplasmic bodies has been confirmed via microscopic analysis. The results from this work support the hypothesis, that evolutionarily conserved Sm proteins have been adapted to perform a whole repertoire of functions related to the post-transcriptional regulation of gene expression in Eukaryota. This adaptation presumably enabled them to coordinate the interdependent processes of splicing element assembly, mRNA maturation and processing, and mRNA translation regulation, and its degradation.
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Affiliation(s)
- Malwina Hyjek‐Składanowska
- Department of Cellular and Molecular BiologyNicolaus Copernicus UniveristyLwowska 187‐100TorunPoland
- Centre For Modern Interdisciplinary TechnologiesNicolaus Copernicus UniversityWilenska 487‐100TorunPoland
- Present address:
Laboratory of Protein StructureInternational Institute of Molecular and Cell Biology4 Trojdena St.02‐109WarsawPoland
| | - Mateusz Bajczyk
- Department of Gene ExpressionInstitute of Molecular Biology and BiotechnologyAdam Mickiewicz UniversityUmultowska 89Poznan61‐614Poland
| | - Marcin Gołębiewski
- Centre For Modern Interdisciplinary TechnologiesNicolaus Copernicus UniversityWilenska 487‐100TorunPoland
- Department of Plant Physiology and BiotechnologyNicolaus Copernicus UniveristyLwowska 187‐100TorunPoland
| | - Przemysław Nuc
- Department of Gene ExpressionInstitute of Molecular Biology and BiotechnologyAdam Mickiewicz UniversityUmultowska 89Poznan61‐614Poland
| | - Agnieszka Kołowerzo‐Lubnau
- Department of Cellular and Molecular BiologyNicolaus Copernicus UniveristyLwowska 187‐100TorunPoland
- Centre For Modern Interdisciplinary TechnologiesNicolaus Copernicus UniversityWilenska 487‐100TorunPoland
| | - Artur Jarmołowski
- Department of Gene ExpressionInstitute of Molecular Biology and BiotechnologyAdam Mickiewicz UniversityUmultowska 89Poznan61‐614Poland
| | - Dariusz Jan Smoliński
- Department of Cellular and Molecular BiologyNicolaus Copernicus UniveristyLwowska 187‐100TorunPoland
- Centre For Modern Interdisciplinary TechnologiesNicolaus Copernicus UniversityWilenska 487‐100TorunPoland
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Tworzydlo W, Sekula M, Bilinski SM. Transmission of Functional, Wild-Type Mitochondria and the Fittest mtDNA to the Next Generation: Bottleneck Phenomenon, Balbiani Body, and Mitophagy. Genes (Basel) 2020; 11:E104. [PMID: 31963356 PMCID: PMC7016935 DOI: 10.3390/genes11010104] [Citation(s) in RCA: 11] [Impact Index Per Article: 2.2] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/09/2019] [Revised: 12/28/2019] [Accepted: 01/13/2020] [Indexed: 02/05/2023] Open
Abstract
The most important role of mitochondria is to supply cells with metabolic energy in the form of adenosine triphosphate (ATP). As synthesis of ATP molecules is accompanied by the generation of reactive oxygen species (ROS), mitochondrial DNA (mtDNA) is highly vulnerable to impairment and, consequently, accumulation of deleterious mutations. In most animals, mitochondria are transmitted to the next generation maternally, i.e., exclusively from female germline cells (oocytes and eggs). It has been suggested, in this context, that a specialized mechanism must operate in the developing oocytes enabling escape from the impairment and subsequent transmission of accurate (devoid of mutations) mtDNA from one generation to the next. Literature survey suggest that two distinct and irreplaceable pathways of mitochondria transmission may be operational in various animal lineages. In some taxa, the mitochondria are apparently selected: functional mitochondria with high inner membrane potential are transferred to the cells of the embryo, whereas those with low membrane potential (overloaded with mutations in mtDNA) are eliminated by mitophagy. In other species, the respiratory activity of germline mitochondria is suppressed and ROS production alleviated leading to the same final effect, i.e., transmission of undamaged mitochondria to offspring, via an entirely different route.
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Affiliation(s)
| | | | - Szczepan M. Bilinski
- Department of Developmental Biology and Invertebrate Morphology, Institute of Zoology and Biomedical Research, Faculty of Biology, Jagiellonian University in Krakow, Gronostajowa 9, 30-387 Krakow, Poland; (W.T.); (M.S.)
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14
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Ge DT, Wang W, Tipping C, Gainetdinov I, Weng Z, Zamore PD. The RNA-Binding ATPase, Armitage, Couples piRNA Amplification in Nuage to Phased piRNA Production on Mitochondria. Mol Cell 2019; 74:982-995.e6. [PMID: 31076285 PMCID: PMC6636356 DOI: 10.1016/j.molcel.2019.04.006] [Citation(s) in RCA: 66] [Impact Index Per Article: 11.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/03/2018] [Revised: 01/24/2019] [Accepted: 04/01/2019] [Indexed: 12/13/2022]
Abstract
PIWI-interacting RNAs (piRNAs) silence transposons in Drosophila ovaries, ensuring female fertility. Two coupled pathways generate germline piRNAs: the ping-pong cycle, in which the PIWI proteins Aubergine and Ago3 increase the abundance of pre-existing piRNAs, and the phased piRNA pathway, which generates strings of tail-to-head piRNAs, one after another. Proteins acting in the ping-pong cycle localize to nuage, whereas phased piRNA production requires Zucchini, an endonuclease on the mitochondrial surface. Here, we report that Armitage (Armi), an RNA-binding ATPase localized to both nuage and mitochondria, links the ping-pong cycle to the phased piRNA pathway. Mutations that block phased piRNA production deplete Armi from nuage. Armi ATPase mutants cannot support phased piRNA production and inappropriately bind mRNA instead of piRNA precursors. We propose that Armi shuttles between nuage and mitochondria, feeding precursor piRNAs generated by Ago3 cleavage into the Zucchini-dependent production of Aubergine- and Piwi-bound piRNAs on the mitochondrial surface.
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Affiliation(s)
- Daniel Tianfang Ge
- RNA Therapeutics Institute and Howard Hughes Medical Institute, University of Massachusetts Medical School, 368 Plantation Street, Worcester, MA 01605, USA
| | - Wei Wang
- RNA Therapeutics Institute and Howard Hughes Medical Institute, University of Massachusetts Medical School, 368 Plantation Street, Worcester, MA 01605, USA; Program in Bioinformatics and Integrative Biology, University of Massachusetts Medical School, Worcester, MA 01605, USA
| | - Cindy Tipping
- RNA Therapeutics Institute and Howard Hughes Medical Institute, University of Massachusetts Medical School, 368 Plantation Street, Worcester, MA 01605, USA
| | - Ildar Gainetdinov
- RNA Therapeutics Institute and Howard Hughes Medical Institute, University of Massachusetts Medical School, 368 Plantation Street, Worcester, MA 01605, USA
| | - Zhiping Weng
- Program in Bioinformatics and Integrative Biology, University of Massachusetts Medical School, Worcester, MA 01605, USA.
| | - Phillip D Zamore
- RNA Therapeutics Institute and Howard Hughes Medical Institute, University of Massachusetts Medical School, 368 Plantation Street, Worcester, MA 01605, USA.
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15
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Żelazowska M, Halajian A. Previtellogenic oocytes of South African largemouth bass Micropterus salmoides
Lacépède 1802 (Actinopterygii, Perciformes) - the Balbiani body, cortical alveoli and developing eggshell. J Morphol 2019; 280:360-369. [DOI: 10.1002/jmor.20948] [Citation(s) in RCA: 5] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/18/2018] [Revised: 12/14/2018] [Accepted: 12/23/2018] [Indexed: 01/07/2023]
Affiliation(s)
- Monika Żelazowska
- Department of Developmental Biology and Morphology of Invertebrates, Institute of Zoology and Biomedical Research; Jagiellonian University; Kraków Poland
| | - Ali Halajian
- Department of Biodiversity; University of Limpopo; Sovenga South Africa
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Bilinski SM, Jaglarz MK, Tworzydlo W. Organelle assemblages implicated in the transfer of oocyte components to the embryo: an insect perspective. CURRENT OPINION IN INSECT SCIENCE 2019; 31:1-7. [PMID: 31109662 DOI: 10.1016/j.cois.2018.05.004] [Citation(s) in RCA: 9] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 04/19/2018] [Accepted: 05/09/2018] [Indexed: 06/09/2023]
Abstract
Besides reserve materials (yolk spheres, lipid droplets), ribosomes and various mRNA species, insect oocytes contain large easily morphologically recognizable organelle assemblages: the Balbiani body and the oosome (pole plasm). These assemblages are implicated in the transfer of oocyte components (mitochondria, polar granules) to the embryo that is to offspring. Here, we review present knowledge of morphology, morphogenesis, molecular composition and function/s of these assemblages. We discuss also the morphogenesis and presumed function of unconventional organelle assemblages, dormant stacks of endoplasmic reticulum, recently described in the oocytes and early embryos of a viviparous dermapteran, Hemimerus talpoides.
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Affiliation(s)
- Szczepan M Bilinski
- Department of Developmental Biology and Invertebrate Morphology, Institute of Zoology and Biomedical Research, Jagiellonian University, Gronostajowa 9, 30-387 Krakow, Poland.
| | - Mariusz K Jaglarz
- Department of Developmental Biology and Invertebrate Morphology, Institute of Zoology and Biomedical Research, Jagiellonian University, Gronostajowa 9, 30-387 Krakow, Poland
| | - Waclaw Tworzydlo
- Department of Developmental Biology and Invertebrate Morphology, Institute of Zoology and Biomedical Research, Jagiellonian University, Gronostajowa 9, 30-387 Krakow, Poland
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17
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Bilinski SM, Kloc M, Tworzydlo W. Selection of mitochondria in female germline cells: is Balbiani body implicated in this process? J Assist Reprod Genet 2017; 34:1405-1412. [PMID: 28755153 PMCID: PMC5699987 DOI: 10.1007/s10815-017-1006-3] [Citation(s) in RCA: 40] [Impact Index Per Article: 5.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/16/2017] [Accepted: 07/21/2017] [Indexed: 11/13/2022] Open
Abstract
Early oocytes of nearly all animal species contain a transient organelle assemblage termed the Balbiani body. Structure and composition of this assemblage may vary even between closely related species. Despite this variability, the Balbiani body always comprises of numerous tightly clustered mitochondria and accumulations of nuage material. It has been suggested that the Balbiani body is an evolutionarily ancestral structure, which plays a role in various processes such as the localization of organelles and macromolecules to the germ plasm, lipidogenesis, as well as the selection/elimination of dysfunctional mitochondria from female germline cells. We suggest that the selection/elimination of mitochondria is a primary and evolutionarily ancestral function of Balbiani body, and that the other functions are secondary, evolutionarily derived additions. We propose a simple model explaining the role of the Balbiani body in the selection of mitochondria, i.e., in the mitochondrial DNA (mtDNA) bottleneck phenomenon.
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Affiliation(s)
- Szczepan M Bilinski
- Department of Developmental Biology and Invertebrate Morphology, Institute of Zoology and Biomedical Research, Jagiellonian University, Gronostajowa 9, 30-387, Krakow, Poland.
| | - Malgorzata Kloc
- The Houston Methodist Research Institute and The Houston Methodist Hospital, 6670 Bertner Ave, Houston, TX, 77030, USA
| | - Waclaw Tworzydlo
- Department of Developmental Biology and Invertebrate Morphology, Institute of Zoology and Biomedical Research, Jagiellonian University, Gronostajowa 9, 30-387, Krakow, Poland
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18
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Bilinski SM, Jaglarz MK, Tworzydlo W. The Pole (Germ) Plasm in Insect Oocytes. Results Probl Cell Differ 2017; 63:103-126. [PMID: 28779315 DOI: 10.1007/978-3-319-60855-6_5] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 02/17/2023]
Abstract
Animal germline cells are specified either through zygotic induction or cytoplasmic inheritance. Zygotic induction takes place in mid- or late embryogenesis and requires cell-to-cell signaling leading to the acquisition of germline fate de novo. In contrast, cytoplasmic inheritance involves formation of a specific, asymmetrically localized oocyte region, termed the germ (pole) plasm. This region contains maternally provided germline determinants (mRNAs, proteins) that are capable of inducing germline fate in a subset of embryonic cells. Recent data indicate that among insects, the zygotic induction represents an ancestral condition, while the cytoplasmic inheritance evolved at the base of Holometabola or in the last common ancestor of Holometabola and its sister taxon, Paraneoptera.In this chapter, we first describe subsequent stages of morphogenesis of the pole plasm and polar granules in the model organism, Drosophila melanogaster. Then, we present an overview of morphology and cytoarchitecture of the pole plasm in various holometabolan and paraneopteran insect species. Finally, we focus on phylogenetic hypotheses explaining the known distribution of two different strategies of germline specification among insects.
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Affiliation(s)
- Szczepan M Bilinski
- Department of Developmental Biology and Morphology of Invertebrates, Institute of Zoology and Biomedical Research, Jagiellonian University, Gronostajowa 9, 30-387, Krakow, Poland.
| | - Mariusz K Jaglarz
- Department of Developmental Biology and Morphology of Invertebrates, Institute of Zoology and Biomedical Research, Jagiellonian University, Gronostajowa 9, 30-387, Krakow, Poland
| | - Waclaw Tworzydlo
- Department of Developmental Biology and Morphology of Invertebrates, Institute of Zoology and Biomedical Research, Jagiellonian University, Gronostajowa 9, 30-387, Krakow, Poland
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Kot M, Büning J, Jankowska W, Drohojowska J, Szklarzewicz T. Development of ovary structures in the last larval and adult stages of psyllids (Insecta, Hemiptera, Sternorrhyncha: Psylloidea). ARTHROPOD STRUCTURE & DEVELOPMENT 2016; 45:389-398. [PMID: 27140505 DOI: 10.1016/j.asd.2016.04.004] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.2] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 03/14/2016] [Revised: 04/21/2016] [Accepted: 04/21/2016] [Indexed: 06/05/2023]
Abstract
The development and organization of the ovaries of ten species from four Psylloidea families (Psyllidae, Triozidae, Aphalaridae and Liviidae) have been investigated. The ovaries of the last larval stage (i.e. fifth instar) of all examined species are filled with numerous clusters of cystocytes which undergo synchronous incomplete mitotic division. Cystocytes of the given cluster are arranged into a rosette with polyfusome in the centre. These clusters are associated with single somatic cells. At the end of the fifth instar, the clusters begin to separate from each other, forming spherical ovarioles which are surrounded by a single layer of somatic cells. In the ovarioles of very young females all cystocytes enter the prophase of meiosis and differentiate shortly thereafter into oocytes and trophocytes (nurse cells). Meanwhile, somatic cells differentiate into cells of the inner epithelial sheath surrounding the trophocytes and into the prefollicular cells that encompass the oocytes. During this final differentiation, the trophocytes lose their cell membranes and become syncytial. Oocytes remain cellular and most of them (termed arrested oocytes) do not grow. In the ovarioles of older females, one oocyte encompassed by its follicle cells starts growing, still connected to the syncytial tropharium by a nutritive cord. After the short phase of previtellogenesis alone, the oocyte enters its vitellogenic the growth phase in the vitellarium. At that time, the second oocyte may enter the vitellarium and start its previtellogenic growth. In the light of the obtained results, the phylogeny of psyllids, as well as phylogenetic relationships between taxa of Hemiptera: Sternorrhyncha are discussed.
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Affiliation(s)
- Marta Kot
- Department of Developmental Biology and Morphology of Invertebrates, Institute of Zoology, Jagiellonian University, Gronostajowa 9, 30-387 Kraków, Poland
| | - Jürgen Büning
- Friedrich-Alexander University of Erlangen-Nuremberg, Department of Biology, Division of Developmental Biology, Staudtstr. 5, 91058 Erlangen, Germany
| | - Władysława Jankowska
- Department of Developmental Biology and Morphology of Invertebrates, Institute of Zoology, Jagiellonian University, Gronostajowa 9, 30-387 Kraków, Poland
| | - Jowita Drohojowska
- Department of Zoology, Faculty of Biology and Environmental Protection, University of Silesia, Bankowa 9, 40-007 Katowice, Poland
| | - Teresa Szklarzewicz
- Department of Developmental Biology and Morphology of Invertebrates, Institute of Zoology, Jagiellonian University, Gronostajowa 9, 30-387 Kraków, Poland.
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20
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Tworzydlo W, Kisiel E, Jankowska W, Witwicka A, Bilinski SM. Exclusion of dysfunctional mitochondria from Balbiani body during early oogenesis of Thermobia. Cell Tissue Res 2016; 366:191-201. [PMID: 27164893 PMCID: PMC5031756 DOI: 10.1007/s00441-016-2414-x] [Citation(s) in RCA: 34] [Impact Index Per Article: 3.8] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/27/2015] [Accepted: 04/12/2016] [Indexed: 01/08/2023]
Abstract
Oocytes of many invertebrate and vertebrate species contain a characteristic organelle complex known as the Balbiani body (Bb). Until now, three principal functions have been ascribed to this complex: delivery of germ cell determinants and localized RNAs to the vegetal cortex/posterior pole of the oocyte, transport of the mitochondria towards the germ plasm, and participation in the formation of lipid droplets. Here, we present the results of a computer-aided 3D reconstruction of the Bb in the growing oocytes of an insect, Thermobia domestica. Our analyses have shown that, in Thermobia, the central part of each fully developed Bb comprises a single intricate mitochondrial network. This “core” network is surrounded by several isolated bean-shaped mitochondrial units that display lowered membrane potential and clear signs of degeneration. In light of the above results and recent theoretical models of mitochondrial quality control, the role of the Bb is discussed. We suggest that, in addition to the aforementioned functions, the Bb is implicated in the selective elimination of dysfunctional mitochondria during oogenesis.
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Affiliation(s)
- Waclaw Tworzydlo
- Department of Developmental Biology and Morphology of Invertebrates, Institute of Zoology, Jagiellonian University, Krakow, Poland.
| | - Elzbieta Kisiel
- Department of Developmental Biology and Morphology of Invertebrates, Institute of Zoology, Jagiellonian University, Krakow, Poland
| | - Wladyslawa Jankowska
- Department of Developmental Biology and Morphology of Invertebrates, Institute of Zoology, Jagiellonian University, Krakow, Poland
| | - Alicja Witwicka
- Department of Developmental Biology and Morphology of Invertebrates, Institute of Zoology, Jagiellonian University, Krakow, Poland
| | - Szczepan M Bilinski
- Department of Developmental Biology and Morphology of Invertebrates, Institute of Zoology, Jagiellonian University, Krakow, Poland
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21
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Yakovlev KV. Localization of germ plasm-related structures during sea urchin oogenesis. Dev Dyn 2015; 245:56-66. [PMID: 26385846 DOI: 10.1002/dvdy.24348] [Citation(s) in RCA: 9] [Impact Index Per Article: 0.9] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/22/2015] [Accepted: 09/12/2015] [Indexed: 12/31/2022] Open
Abstract
BACKGROUND Animal germ cells have specific organelles that are similar to ribonucleoprotein complex, called germ plasm, which is accumulated in eggs. Germ plasm is essential for inherited mechanism of germ line segregation in early embryogenesis. Sea urchins have early germ line segregation in early embryogenesis. Nevertheless, organization of germ plasm-related organelles and their molecular composition are still unclear. Another issue is whether maternally accumulated germ plasm exists in the sea urchin eggs. RESULTS I analyzed intracellular localization of germ plasm during oogenesis in sea urchin Strongylocentrotus intermedius by using morphological approach and immunocytochemical detection of Vasa, a germ plasm marker. All ovarian germ cells have germ plasm-related organelles in the form of germ granules, Balbiani bodies, and perinuclear nuage found previously in germ cells in other animals. Maternal germ plasm is accumulated in late oogenesis at the cell periphery. Cytoskeletal drug treatment showed an association of Vasa-positive granules with actin filaments in the egg cortex. CONCLUSIONS All female germ cells of sea urchins have germ plasm-related organelles. Eggs have a maternally accumulated germ plasm associated with cortical cytoskeleton. These findings correlate with early segregation of germ line in sea urchins.
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Affiliation(s)
- Konstantin V Yakovlev
- Laboratory of Cytotechnology, A.V. Zhirmunsky Institute of Marine Biology of the Far Eastern Branch of the Russian Academy of Sciences, Vladivostok, Russia
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22
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Reid WR, Zhang L, Liu N. Temporal Gene Expression Profiles of Pre Blood-Fed Adult Females Immediately Following Eclosion in the Southern House Mosquito Culex Quinquefasciatus. Int J Biol Sci 2015; 11:1306-13. [PMID: 26435696 PMCID: PMC4582154 DOI: 10.7150/ijbs.12829] [Citation(s) in RCA: 13] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/30/2015] [Accepted: 07/28/2015] [Indexed: 01/08/2023] Open
Abstract
Prior to acquisition of the first host blood meal, the anautogenous mosquito Culex quinquefasciatus requires a period of time in order to prepare for the blood feeding and, later, vitellogenesis. In the current study, we conducted whole transcriptome analyses of adult female Culex mosquitoes to identify genes that may be necessary for both taking of the blood meal, and processing of the blood meal in adult female mosquitoes Cx. quinquefasciatus. We examined temporal expression of genes for the periods of post eclosion and prior to the female freely taking a blood meal. We further evaluated the temporal expression of certain genes for the periods after the taking of a blood meal to identify genes that may be necessary for both the taking of the blood meal, and the processing of the blood meal. We found that adult females required a minimum of 48 h post-eclosion before they freely took their first blood meal. We hypothesized that gene expression signatures were altered in the mosquitoes before blood feeding in preparation for the acquisition of the blood meal through changes in multiple gene expression. To identify the genes involved in the acquisition of blood feeding, we quantified the gene expression levels of adult female Cx. quinquefasciatus using RNA Seq throughout a pre-blooding period from 2 to 72 h post eclosion at 12 h intervals. A total of 325 genes were determined to be differentially-expressed throughout the pre-blooding period, with the majority of differentially-expressed genes occurring between the 2 h and 12 h post-eclosion time points. Among the up-regulated genes were salivary proteins, cytochrome P450s, odorant-binding proteins, and proteases, while the majority of the down-regulated genes were hypothetical or cuticular genes. In addition, Trypsin was found to be up-regulated immediately following blood feeding, while trypsin and chymotrypsin were up-regulated at 48h and 60h post blood-feeding, respectively, suggesting that these proteases are likely involved in the digestion of the blood meal. Overall, this study reviewed multiple genes that might be involved in the adult female competency for blood meal acquisition in mosquitoes.
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Affiliation(s)
- William R Reid
- 1. Department of Entomology and Plant Pathology, Auburn University, Auburn, AL 36849, USA ; 2. Current address: UDSA-ARS Center for Medical Veterinary and Agricultural Entomology, Mosquito and Fly Research Unit, Gainesville, FL 32608, USA
| | - Lee Zhang
- 3. Genomics Laboratory, Auburn University, Auburn, AL 36849, USA
| | - Nannan Liu
- 1. Department of Entomology and Plant Pathology, Auburn University, Auburn, AL 36849, USA
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Abstract
Messenger ribonucleoprotein (mRNP) granules are dynamic, self-assembling structures that harbor non-translating mRNAs bound by various proteins that regulate mRNA translation, localization, and turnover. Their importance in gene expression regulation is far reaching, ranging from precise spatial-temporal control of mRNAs that drive developmental programs in oocytes and embryos, to similarly exquisite control of mRNAs in neurons that underpin synaptic plasticity, and thus, memory formation. Analysis of mRNP granules in their various contexts has revealed common themes of assembly, disassembly, and modes of mRNA regulation, yet new studies continue to reveal unexpected and important findings, such as links between aberrant mRNP granule assembly and neurodegenerative disease. Continued study of these enigmatic structures thus promises fascinating new insights into cellular function, and may also suggest novel therapeutic strategies in various disease states.
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Affiliation(s)
- J Ross Buchan
- a Department of Molecular and Cellular Biology ; University of Arizona ; Tucson , AZ USA
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24
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Dorn DC, Dorn A. Stem cell autotomy and niche interaction in different systems. World J Stem Cells 2015; 7:922-944. [PMID: 26240680 PMCID: PMC4515436 DOI: 10.4252/wjsc.v7.i6.922] [Citation(s) in RCA: 7] [Impact Index Per Article: 0.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 07/20/2014] [Accepted: 05/27/2015] [Indexed: 02/06/2023] Open
Abstract
The best known cases of cell autotomy are the formation of erythrocytes and thrombocytes (platelets) from progenitor cells that reside in special niches. Recently, autotomy of stem cells and its enigmatic interaction with the niche has been reported from male germline stem cells (GSCs) in several insect species. First described in lepidopterans, the silkmoth, followed by the gipsy moth and consecutively in hemipterans, foremost the milkweed bug. In both, moths and the milkweed bug, GSCs form finger-like projections toward the niche, the apical cells (homologs of the hub cells in Drosophila). Whereas in the milkweed bug the projection terminals remain at the surface of the niche cells, in the gipsy moth they protrude deeply into the singular niche cell. In both cases, the projections undergo serial retrograde fragmentation with progressing signs of autophagy. In the gipsy moth, the autotomized vesicles are phagocytized and digested by the niche cell. In the milkweed bug the autotomized vesicles accumulate at the niche surface and disintegrate. Autotomy and sprouting of new projections appears to occur continuously. The significance of the GSC-niche interactions, however, remains enigmatic. Our concept on the signaling relationship between stem cell-niche in general and GSC and niche (hub cells and cyst stem cells) in particular has been greatly shaped by Drosophila melanogaster. In comparing the interactions of GSCs with their niche in Drosophila with those in species exhibiting GSC autotomy it is obvious that additional or alternative modes of stem cell-niche communication exist. Thus, essential signaling pathways, including niche-stem cell adhesion (E-cadherin) and the direction of asymmetrical GSC division - as they were found in Drosophila - can hardly be translated into the systems where GSC autotomy was reported. It is shown here that the serial autotomy of GSC projections shows remarkable similarities with Wallerian axonal destruction, developmental axon pruning and dying-back degeneration in neurodegenerative diseases. Especially the hypothesis of an existing evolutionary conserved “autodestruction program” in axons that might also be active in GSC projections appears attractive. Investigations on the underlying signaling pathways have to be carried out. There are two other well known cases of programmed cell autotomy: the enucleation of erythroblasts in the process of erythrocyte maturation and the segregation of thousands of thrombocytes (platelets) from one megakaryocyte. Both progenitor cell types - erythroblasts and megakaryocytes - are associated with a niche in the bone marrow, erythroblasts with a macrophage, which they surround, and the megakaryocytes with the endothelial cells of sinusoids and their extracellular matrix. Although the regulatory mechanisms may be specific in each case, there is one aspect that connects all described processes of programmed cell autotomy and neuronal autodestruction: apoptotic pathways play always a prominent role. Studies on the role of male GSC autotomy in stem cell-niche interaction have just started but are expected to reveal hitherto unknown ways of signal exchange. Spermatogenesis in mammals advance our understanding of insect spermatogenesis. Mammal and insect spermatogenesis share some broad principles, but a comparison of the signaling pathways is difficult. We have intimate knowledge from Drosophila, but of almost no other insect, and we have only limited knowledge from mammals. The discovery of stem cell autotomy as part of the interaction with the niche promises new general insights into the complicated stem cell-niche interdependence.
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Kloc M, Jedrzejowska I, Tworzydlo W, Bilinski SM. Balbiani body, nuage and sponge bodies--term plasm pathway players. ARTHROPOD STRUCTURE & DEVELOPMENT 2014; 43:341-8. [PMID: 24398038 DOI: 10.1016/j.asd.2013.12.003] [Citation(s) in RCA: 65] [Impact Index Per Article: 5.9] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 10/10/2013] [Revised: 11/28/2013] [Accepted: 12/18/2013] [Indexed: 05/14/2023]
Abstract
In many animal species, germ cells are specified by maternally provided, often asymmetrically localized germ cell determinant, termed the germ plasm. It has been shown that in model organisms such as Xenopus laevis, Danio rerio and Drosophila melanogaster germ plasm components (various proteins, mRNAs and mitochondria) are delivered to the proper position within the egg cell by germline specific organelles, i.e. Balbiani bodies, nuage accumulations and/or sponge bodies. In the present article, we review the current knowledge on morphology, molecular composition and functioning of these organelles in main lineages of arthropods and different ovary types on the backdrop of data derived from the studies of the model vertebrate species.
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Affiliation(s)
- Malgorzata Kloc
- The Houston Methodist Hospital, The Houston Methodist Hospital Research Institute, Houston, TX, USA
| | - Izabela Jedrzejowska
- Department of Animal Developmental Biology, Institute of Experimental Biology, University of Wroclaw, Wroclaw, Poland
| | - Waclaw Tworzydlo
- Department of Developmental Biology and Morphology of Invertebrates, Institute of Zoology, Jagiellonian University, Krakow, Poland
| | - Szczepan M Bilinski
- Department of Developmental Biology and Morphology of Invertebrates, Institute of Zoology, Jagiellonian University, Krakow, Poland.
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26
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Tworzydlo W, Kisiel E, Jankowska W, Bilinski SM. Morphology and ultrastructure of the germarium in panoistic ovarioles of a basal “apterygotous” insect, Thermobia domestica. ZOOLOGY 2014; 117:200-6. [DOI: 10.1016/j.zool.2014.01.002] [Citation(s) in RCA: 24] [Impact Index Per Article: 2.2] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/29/2013] [Revised: 01/10/2014] [Accepted: 01/20/2014] [Indexed: 02/06/2023]
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28
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The Bic-C family of developmental translational regulators. Comp Funct Genomics 2012; 2012:141386. [PMID: 22611335 PMCID: PMC3352585 DOI: 10.1155/2012/141386] [Citation(s) in RCA: 20] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/24/2012] [Accepted: 02/18/2012] [Indexed: 12/14/2022] Open
Abstract
Regulation of mRNA translation is especially important during cellular and developmental processes. Many evolutionarily conserved proteins act in the context of multiprotein complexes and modulate protein translation both at the spatial and the temporal levels. Among these, Bicaudal C constitutes a family of RNA binding proteins whose founding member was first identified in Drosophila and contains orthologs in vertebrates. We discuss recent advances towards understanding the functions of these proteins in the context of the cellular and developmental biology of many model organisms and their connection to human disease.
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29
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Buckingham M, Liu JL. U bodies respond to nutrient stress in Drosophila. Exp Cell Res 2011; 317:2835-44. [DOI: 10.1016/j.yexcr.2011.09.001] [Citation(s) in RCA: 18] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/06/2011] [Revised: 09/01/2011] [Accepted: 09/04/2011] [Indexed: 10/17/2022]
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30
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Abstract
"Germ granules" are cytoplasmic, nonmembrane-bound organelles unique to germline. Germ granules share components with the P bodies and stress granules of somatic cells, but also contain proteins and RNAs uniquely required for germ cell development. In this review, we focus on recent advances in our understanding of germ granule assembly, dynamics, and function. One hypothesis is that germ granules operate as hubs for the posttranscriptional control of gene expression, a function at the core of the germ cell differentiation program.
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Affiliation(s)
- Ekaterina Voronina
- Department of Molecular Biology and Genetics and Howard Hughes Medical Institute, Center for Cell Dynamics, Johns Hopkins University School of Medicine, Baltimore, Maryland, USA.
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