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Evaluating the effect of spaceflight on the host-pathogen interaction between human intestinal epithelial cells and Salmonella Typhimurium. NPJ Microgravity 2021; 7:9. [PMID: 33750813 PMCID: PMC7943786 DOI: 10.1038/s41526-021-00136-w] [Citation(s) in RCA: 14] [Impact Index Per Article: 3.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/27/2020] [Accepted: 02/03/2021] [Indexed: 01/31/2023] Open
Abstract
Spaceflight uniquely alters the physiology of both human cells and microbial pathogens, stimulating cellular and molecular changes directly relevant to infectious disease. However, the influence of this environment on host-pathogen interactions remains poorly understood. Here we report our results from the STL-IMMUNE study flown aboard Space Shuttle mission STS-131, which investigated multi-omic responses (transcriptomic, proteomic) of human intestinal epithelial cells to infection with Salmonella Typhimurium when both host and pathogen were simultaneously exposed to spaceflight. To our knowledge, this was the first in-flight infection and dual RNA-seq analysis using human cells.
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2
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Partrick KA, Rosenhauer AM, Auger J, Arnold AR, Ronczkowski NM, Jackson LM, Lord MN, Abdulla SM, Chassaing B, Huhman KL. Ingestion of probiotic (Lactobacillus helveticus and Bifidobacterium longum) alters intestinal microbial structure and behavioral expression following social defeat stress. Sci Rep 2021; 11:3763. [PMID: 33580118 PMCID: PMC7881201 DOI: 10.1038/s41598-021-83284-z] [Citation(s) in RCA: 33] [Impact Index Per Article: 8.3] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/28/2020] [Accepted: 01/28/2021] [Indexed: 02/08/2023] Open
Abstract
Social stress exacerbates anxious and depressive behaviors in humans. Similarly, anxiety- and depressive-like behaviors are triggered by social stress in a variety of non-human animals. Here, we tested whether oral administration of the putative anxiolytic probiotic strains Lactobacillus helveticus R0052 and Bifidobacterium longum R0175 reduces the striking increase in anxiety-like behavior and changes in gut microbiota observed following social defeat stress in Syrian hamsters. We administered the probiotic at two different doses for 21 days, and 16S rRNA gene amplicon sequencing revealed a shift in microbial structure following probiotic administration at both doses, independently of stress. Probiotic administration at either dose increased anti-inflammatory cytokines IL-4, IL-5, and IL-10 compared to placebo. Surprisingly, probiotic administration at the low dose, equivalent to the one used in humans, significantly increased social avoidance and decreased social interaction. This behavioral change was associated with a reduction in microbial richness in this group. Together, these results demonstrate that probiotic administration alters gut microbial composition and may promote an anti-inflammatory profile but that these changes may not promote reductions in behavioral responses to social stress.
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Affiliation(s)
- Katherine A Partrick
- Neuroscience Institute, Center for Behavioral Neuroscience, Georgia State University, PO Box 5030, Atlanta, GA, 30303-5030, USA
| | - Anna M Rosenhauer
- Neuroscience Institute, Center for Behavioral Neuroscience, Georgia State University, PO Box 5030, Atlanta, GA, 30303-5030, USA
| | - Jérémie Auger
- Rosell Institute for Microbiome and Probiotics, Montreal, QC, Canada
| | - Amanda R Arnold
- Neuroscience Institute, Center for Behavioral Neuroscience, Georgia State University, PO Box 5030, Atlanta, GA, 30303-5030, USA
| | - Nicole M Ronczkowski
- Neuroscience Institute, Center for Behavioral Neuroscience, Georgia State University, PO Box 5030, Atlanta, GA, 30303-5030, USA
| | - Lanaya M Jackson
- Neuroscience Institute, Center for Behavioral Neuroscience, Georgia State University, PO Box 5030, Atlanta, GA, 30303-5030, USA
| | - Magen N Lord
- Neuroscience Institute, Center for Behavioral Neuroscience, Georgia State University, PO Box 5030, Atlanta, GA, 30303-5030, USA
| | - Sara M Abdulla
- Neuroscience Institute, Center for Behavioral Neuroscience, Georgia State University, PO Box 5030, Atlanta, GA, 30303-5030, USA
| | - Benoit Chassaing
- Neuroscience Institute, Center for Behavioral Neuroscience, Georgia State University, PO Box 5030, Atlanta, GA, 30303-5030, USA.,INSERM U1016, Team "Mucosal Microbiota in Chronic Inflammatory Diseases", CNRS UMR 8104, Université de Paris, Paris, France.,Institute for Biomedical Sciences, Georgia State University, Atlanta, GA, USA
| | - Kim L Huhman
- Neuroscience Institute, Center for Behavioral Neuroscience, Georgia State University, PO Box 5030, Atlanta, GA, 30303-5030, USA.
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3
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Sun L, Tian W, Guo X, Zhang Y, Liu X, Li X, Tian Y, Man C, Jiang Y. Lactobacillus gasseri JM1 with potential probiotic characteristics alleviates inflammatory response by activating the PI3K/Akt signaling pathway in vitro. J Dairy Sci 2020; 103:7851-7864. [DOI: 10.3168/jds.2020-18187] [Citation(s) in RCA: 13] [Impact Index Per Article: 2.6] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/11/2020] [Accepted: 04/19/2020] [Indexed: 12/18/2022]
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4
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Jeffrey MP, MacPherson CW, Mathieu O, Tompkins TA, Green-Johnson JM. Secretome-Mediated Interactions with Intestinal Epithelial Cells: A Role for Secretome Components from Lactobacillus rhamnosus R0011 in the Attenuation of Salmonella enterica Serovar Typhimurium Secretome and TNF-α-Induced Proinflammatory Responses. THE JOURNAL OF IMMUNOLOGY 2020; 204:2523-2534. [PMID: 32238458 DOI: 10.4049/jimmunol.1901440] [Citation(s) in RCA: 15] [Impact Index Per Article: 3.0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Subscribe] [Scholar Register] [Received: 12/04/2019] [Accepted: 02/26/2020] [Indexed: 12/13/2022]
Abstract
Recent evidence suggests that lactic acid bacteria communicate with host cells via secretome components to influence immune responses but less is known about gut-pathogen secretomes, impact of lactic acid bacteria secretomes on host-pathogen interactions, and the mechanisms underlying these interactions. Genome-wide microarrays and cytokine profiling were used to interrogate the impact of the Lactobacillus rhamnosus R0011 secretome (LrS) on TNF-α and Salmonella enterica subsp. enterica serovar Typhimurium secretome (STS)-induced outcomes in human intestinal epithelial cells. The LrS attenuated both TNF-α- and STS-induced gene expression involved in NF-κB and MAPK activation, as well as expression of genes involved in other immune-related signaling pathways. Specifically, the LrS induced the expression of dual specificity phosphatase 1 (DUSP1), activating transcription factor 3 (ATF3), and tribbles pseudokinase 3 (TRIB3), negative regulators of innate immune signaling, in HT-29 intestinal epithelial cells challenged with TNF-α or STS. TNF-α- and STS-induced acetylation of H3 and H4 histones was attenuated by the LrS, as was the production of TNF-α- and STS-induced proinflammatory cytokines and chemokines. Interestingly, the LrS induced production of macrophage migration inhibitory factor (MIF), a cytokine involved in host-microbe interactions at the gut interface. We propose that the LrS attenuates proinflammatory mediator expression through increased transcription of negative regulators of innate immune activity and changes in global H3 and H4 histone acetylation. To our knowledge, these findings provide novel insights into the complex multifaceted mechanisms of action behind secretome-mediated interdomain communication at the gut-mucosal interface.
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Affiliation(s)
- Michael P Jeffrey
- Applied Bioscience Graduate Program and the Faculty of Science, Ontario Technical University, Oshawa, Ontario L1G 0C5, Canada; and
| | - Chad W MacPherson
- Rosell Institute for Microbiome and Probiotics, Montreal, Quebec H4P 2R2, Canada
| | - Olivier Mathieu
- Rosell Institute for Microbiome and Probiotics, Montreal, Quebec H4P 2R2, Canada
| | - Thomas A Tompkins
- Rosell Institute for Microbiome and Probiotics, Montreal, Quebec H4P 2R2, Canada
| | - Julia M Green-Johnson
- Applied Bioscience Graduate Program and the Faculty of Science, Ontario Technical University, Oshawa, Ontario L1G 0C5, Canada; and
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5
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Gomez DE, Galvão KN, Rodriguez-Lecompte JC, Costa MC. The Cattle Microbiota and the Immune System: An Evolving Field. Vet Clin North Am Food Anim Pract 2019; 35:485-505. [PMID: 31590899 DOI: 10.1016/j.cvfa.2019.08.002] [Citation(s) in RCA: 28] [Impact Index Per Article: 4.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/13/2022] Open
Abstract
New insights into the host-microbiota relationship have recently emerged with the advancement of molecular technologies such as next-generation sequencing. This article presents the current knowledge regarding the interaction between bacteria and the immune system of the gut, the uterus, and the mammary gland of cattle.
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Affiliation(s)
- Diego E Gomez
- Department of Large Animal Clinical Sciences, College of Veterinary Medicine, University of Florida, 2015 Southwest 16th Avenue, Gainesville, FL 32608, USA.
| | - Klibs N Galvão
- Department of Large Animal Clinical Sciences, College of Veterinary Medicine, University of Florida, 2015 Southwest 16th Avenue, Gainesville, FL 32608, USA
| | - Juan C Rodriguez-Lecompte
- Department of Pathology and Microbiology, Atlantic Veterinary College, University of Prince Edward Island, 550 University Avenue, Charlottetown, Prince Edward Island C1A 4P3, Canada
| | - Marcio C Costa
- Department of Veterinary Biomedicine, University of Montreal, 3200 Rue Sicotte, Saint-Hyacinthe, Quebec J2S 2M2, Canada
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6
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Hou Y, Li X, Liu X, Zhang Y, Zhang W, Man C, Jiang Y. Transcriptomic responses of Caco-2 cells to Lactobacillus rhamnosus GG and Lactobacillus plantarum J26 against oxidative stress. J Dairy Sci 2019; 102:7684-7696. [PMID: 31255276 DOI: 10.3168/jds.2019-16332] [Citation(s) in RCA: 20] [Impact Index Per Article: 3.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/18/2019] [Accepted: 04/20/2019] [Indexed: 12/12/2022]
Abstract
Oxidative stress is the basic reason for aging and age-related diseases. In this study, we investigated the protective effect of 2 strains of lactic acid bacteria (LAB), Lactobacillus rhamnosus GG and L. plantarum J26, against oxidative stress in Caco-2 cells, and gave an overview of the mechanisms of lactic acid bacteria antioxidant activity using digital gene expression profiling. The 2 LAB strains provided significant protection against hydrogen peroxide (H2O2)-induced reduction in superoxide dismutase activity and increase in glutathione peroxidase activity in Caco-2 cells. However, inactive bacteria had little effect on alleviating oxidation stress in Caco-2 cells. Eight genes related to oxidative stress-FOSB, TNF, PPP1R15A, NUAK2, ATF3, TNFAIP3, EGR2, and FBN2-were significantly upregulated in H2O2-induced Caco-2 cells compared with untreated Caco-2 cells. After incubation of the H2O2-induced Caco-2 cells with L. rhamnosus GG and L. plantarum J26, 5 genes (TNF, EGR2, NUAK2, FBN2, and TNFAIP3) and 2 genes (NUAK2 and FBN2) were downregulated, respectively. In addition, the Kyoto Encyclopedia of Genes and Genomes indicated that some signaling pathways associated with inflammation, immune response, and apoptosis, such as Janus kinase/signal transducers and activators of transcription (Jak-STAT), mitogen-activated protein kinase (MAPK), nuclear factor-κB, and tumor necrosis factor, were all negatively modulated by the 2 strains, especially L. rhamnosus GG. In this paper, we reveal the mechanism of LAB in relieving oxidative stress and provide a theoretical basis for the rapid screening and evaluation of new LAB resources.
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Affiliation(s)
- Yichao Hou
- Key Laboratory of Dairy Science, Ministry of Education, Department of Food Science, Northeast Agricultural University, Harbin, China, 150030
| | - Xuesong Li
- Key Laboratory of Dairy Science, Ministry of Education, Department of Food Science, Northeast Agricultural University, Harbin, China, 150030
| | - Xinyu Liu
- Key Laboratory of Dairy Science, Ministry of Education, Department of Food Science, Northeast Agricultural University, Harbin, China, 150030
| | - Yashuo Zhang
- Key Laboratory of Dairy Science, Ministry of Education, Department of Food Science, Northeast Agricultural University, Harbin, China, 150030
| | - Wei Zhang
- Key Laboratory of Dairy Science, Ministry of Education, Department of Food Science, Northeast Agricultural University, Harbin, China, 150030
| | - Chaoxin Man
- Key Laboratory of Dairy Science, Ministry of Education, Department of Food Science, Northeast Agricultural University, Harbin, China, 150030.
| | - Yujun Jiang
- Key Laboratory of Dairy Science, Ministry of Education, Department of Food Science, Northeast Agricultural University, Harbin, China, 150030.
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7
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Jeffrey MP, Strap JL, Jones Taggart H, Green-Johnson JM. Suppression of Intestinal Epithelial Cell Chemokine Production by Lactobacillus rhamnosus R0011 and Lactobacillus helveticus R0389 Is Mediated by Secreted Bioactive Molecules. Front Immunol 2018; 9:2639. [PMID: 30524427 PMCID: PMC6262363 DOI: 10.3389/fimmu.2018.02639] [Citation(s) in RCA: 21] [Impact Index Per Article: 3.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/27/2018] [Accepted: 10/26/2018] [Indexed: 12/21/2022] Open
Abstract
Host intestinal epithelial cells (IEC) present at the gastrointestinal interface are exposed to pathogenic and non-pathogenic bacteria and their products. Certain probiotic lactic acid bacteria (LAB) have been associated with a range of host-immune modulatory activities including down-regulation of pro-inflammatory gene expression and cytokine production by IEC, with growing evidence suggesting that these bacteria secrete bioactive molecules with immunomodulatory activity. The aim of this study was to determine whether two lactobacilli with immunomodulatory activity [Lactobacillus rhamnosus R0011 (Lr) and Lactobacillus helveticus R0389 (Lh)], produce soluble mediators able to influence IEC responses to Pattern Recognition Receptor (PRR) ligands and pro-inflammatory cytokines [Tumor Necrosis Factor α (TNFα), Interleukin-1β (IL-1β)], signals inducing IEC chemokine production during infection. To this end, the effects of cell-free supernatants (CFS) from Lr and Lh on IEC production of the pro-inflammatory chemokines interleukin (IL)-8 and cytokine-induced neutrophil chemoattractant 1 (CINC-1) induced by a range of host- or pathogen-derived pro-inflammatory stimuli were determined, and the impact on human HT-29 IEC and a primary IEC line (rat IEC-6) was compared. The Lr-CFS and Lh-CFS did not significantly modulate basal IL-8 production from HT-29 IECs or CINC-1 production from IEC-6 cells. However, both Lr-CFS and Lh-CFS significantly down-regulated IL-8 production from HT-29 IECs challenged with varied PRR ligands. Lr-CFS and Lh-CFS had differential effects on PRR-induced CINC-1 production by rat IEC-6 IECs, with no significant down-regulation of CINC-1 observed from IEC-6 IECs cultured with Lh-CFS. Further analysis of the Lr-CFS revealed down-regulation of IL-8 production induced by the pro-inflammatory cytokines IL-1β and TNFα Preliminary characterization of the bioactive constituent(s) of the Lr-CFS indicates that it is resistant to treatment with DNase, RNase, and an acidic protease, but is sensitive to alterations in pH. Taken together, these results indicate that these lactobacilli secrete bioactive molecules of low molecular weight that may modulate host innate immune activity through interactions with IEC.
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Affiliation(s)
- Michael P Jeffrey
- Applied Bioscience Graduate Program, University of Ontario Institute of Technology, Oshawa, ON, Canada
| | - Janice L Strap
- Applied Bioscience Graduate Program, University of Ontario Institute of Technology, Oshawa, ON, Canada.,Faculty of Science, University of Ontario Institute of Technology, Oshawa, ON, Canada
| | - Holly Jones Taggart
- Applied Bioscience Graduate Program, University of Ontario Institute of Technology, Oshawa, ON, Canada.,Faculty of Health Sciences, University of Ontario Institute of Technology, Oshawa, ON, Canada
| | - Julia M Green-Johnson
- Applied Bioscience Graduate Program, University of Ontario Institute of Technology, Oshawa, ON, Canada.,Faculty of Science, University of Ontario Institute of Technology, Oshawa, ON, Canada
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8
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MacPherson CW, Shastri P, Mathieu O, Tompkins TA, Burguière P. Genome-Wide Immune Modulation of TLR3-Mediated Inflammation in Intestinal Epithelial Cells Differs between Single and Multi-Strain Probiotic Combination. PLoS One 2017; 12:e0169847. [PMID: 28099447 PMCID: PMC5242491 DOI: 10.1371/journal.pone.0169847] [Citation(s) in RCA: 28] [Impact Index Per Article: 3.5] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/27/2016] [Accepted: 12/22/2016] [Indexed: 12/27/2022] Open
Abstract
Genome-wide transcriptional analysis in intestinal epithelial cells (IEC) can aid in elucidating the impact of single versus multi-strain probiotic combinations on immunological and cellular mechanisms of action. In this study we used human expression microarray chips in an in vitro intestinal epithelial cell model to investigate the impact of three probiotic bacteria, Lactobacillus helveticus R0052 (Lh-R0052), Bifidobacterium longum subsp. infantis R0033 (Bl-R0033) and Bifidobacterium bifidum R0071 (Bb-R0071) individually and in combination, and of a surface-layer protein (SLP) purified from Lh-R0052, on HT-29 cells' transcriptional profile to poly(I:C)-induced inflammation. Hierarchical heat map clustering, Set Distiller and String analyses revealed that the effects of Lh-R0052 and Bb-R0071 diverged from those of Bl-R0033 and Lh-R0052-SLP. It was evident from the global analyses with respect to the immune, cellular and homeostasis related pathways that the co-challenge with probiotic combination (PC) vastly differed in its effect from the single strains and Lh-R0052-SLP treatments. The multi-strain PC resulted in a greater reduction of modulated genes, found through functional connections between immune and cellular pathways. Cytokine and chemokine analyses based on specific outcomes from the TNF-α and NF-κB signaling pathways revealed single, multi-strain and Lh-R0052-SLP specific attenuation of the majority of proteins measured (TNF-α, IL-8, CXCL1, CXCL2 and CXCL10), indicating potentially different mechanisms. These findings indicate a synergistic effect of the bacterial combinations relative to the single strain and Lh-R0052-SLP treatments in resolving toll-like receptor 3 (TLR3)-induced inflammation in IEC and maintaining cellular homeostasis, reinforcing the rationale for using multi-strain formulations as a probiotic.
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Affiliation(s)
- Chad W. MacPherson
- Lallemand Health Solutions Inc., 6100 avenue Royalmount, Montreal, QC, Canada
- * E-mail:
| | - Padmaja Shastri
- University of Ontario Institute of Technology, Oshawa, Canada
| | - Olivier Mathieu
- Lallemand Health Solutions Inc., 6100 avenue Royalmount, Montreal, QC, Canada
| | - Thomas A. Tompkins
- Lallemand Health Solutions Inc., 6100 avenue Royalmount, Montreal, QC, Canada
| | - Pierre Burguière
- Lallemand Health Solutions Inc., 6100 avenue Royalmount, Montreal, QC, Canada
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9
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Cousin FJ, Jouan-Lanhouet S, Théret N, Brenner C, Jouan E, Le Moigne-Muller G, Dimanche-Boitrel MT, Jan G. The probiotic Propionibacterium freudenreichii as a new adjuvant for TRAIL-based therapy in colorectal cancer. Oncotarget 2016; 7:7161-78. [PMID: 26771233 PMCID: PMC4872776 DOI: 10.18632/oncotarget.6881] [Citation(s) in RCA: 53] [Impact Index Per Article: 5.9] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/02/2015] [Accepted: 01/03/2016] [Indexed: 12/31/2022] Open
Abstract
TNF-Related Apoptosis-Inducing Ligand (TRAIL) is a well-known apoptosis inducer, which activates the extrinsic death pathway. TRAIL is pro-apoptotic on colon cancer cells, while not cytotoxic towards normal healthy cells. However, its clinical use is limited by cell resistance to cell death which occurs in approximately 50% of cancer cells. Short Chain Fatty Acids (SCFA) are also known to specifically induce apoptosis of cancer cells. In accordance, we have shown that food grade dairy propionibacteria induce intrinsic apoptosis of colon cancer cells, via the production and release of SCFA (propionate and acetate) acting on mitochondria. Here, we investigated possible synergistic effect between Propionibacterium freudenreichii and TRAIL. Indeed, we hypothesized that acting on both extrinsic and intrinsic death pathways may exert a synergistic pro-apoptotic effect. Whole transcriptomic analysis demonstrated that propionibacterial supernatant or propionibacterial metabolites (propionate and acetate), in combination with TRAIL, increased pro-apoptotic gene expression (TRAIL-R2/DR5) and decreased anti-apoptotic gene expression (FLIP, XIAP) in HT29 human colon cancer cells. The revealed synergistic pro-apoptotic effect, depending on both death receptors (TRAIL-R1/DR4, TRAIL-R2/DR5) and caspases (caspase-8, -9 and -3) activation, was lethal on cancer cells but not on normal human intestinal epithelial cells (HIEC), and was inhibited by Bcl-2 expression. Finally, milk fermented by P. freudenreichii induced HT29 cells apoptosis and enhanced TRAIL cytotoxic activity, as did P. freudenreichii DMEM culture supernatants or its SCFA metabolites. These results open new perspectives for food grade P. freudenreichii-containing products in order to potentiate TRAIL-based cancer therapy in colorectal cancer.
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Affiliation(s)
- Fabien J Cousin
- INRA, UMR1253 STLO, Science et Technologie du Lait et de l'Œuf, Rennes F-35042, France.,AGROCAMPUS OUEST, UMR1253 STLO, Rennes F-35042, France.,CNIEL/Syndifrais, Paris 09 F-75314, France.,Current address: Research Unit Aliments Bioprocédés Toxicologie Environnements (UR ABTE) EA 4651, Université de Caen Normandie, Caen F-14032, France
| | - Sandrine Jouan-Lanhouet
- INSERM, UMR1085, Institut de Recherche sur la Santé, l'Environnement et le Travail, Rennes F-35043, France.,Biosit UMS3080, Université de Rennes 1, Rennes F-35043, France.,Current address: Department for Biomedical Molecular Biology, University of Ghent, VIB Inflammation Research Center, Ghent B-9052, Belgium
| | - Nathalie Théret
- INSERM, UMR1085, Institut de Recherche sur la Santé, l'Environnement et le Travail, Rennes F-35043, France.,Biosit UMS3080, Université de Rennes 1, Rennes F-35043, France.,INRIA, UMR6074 IRISA, Rennes F-35042, France
| | - Catherine Brenner
- INSERM, UMRS1180, LabEx LERMIT, Châtenay-Malabry F-92290, France.,Université de Paris Sud, Faculté de Pharmacie, Châtenay-Malabry F-92290, France
| | - Elodie Jouan
- INSERM, UMR1085, Institut de Recherche sur la Santé, l'Environnement et le Travail, Rennes F-35043, France.,Biosit UMS3080, Université de Rennes 1, Rennes F-35043, France
| | - Gwénaëlle Le Moigne-Muller
- INSERM, UMR1085, Institut de Recherche sur la Santé, l'Environnement et le Travail, Rennes F-35043, France.,Biosit UMS3080, Université de Rennes 1, Rennes F-35043, France
| | - Marie-Thérèse Dimanche-Boitrel
- INSERM, UMR1085, Institut de Recherche sur la Santé, l'Environnement et le Travail, Rennes F-35043, France.,Biosit UMS3080, Université de Rennes 1, Rennes F-35043, France
| | - Gwénaël Jan
- INRA, UMR1253 STLO, Science et Technologie du Lait et de l'Œuf, Rennes F-35042, France.,AGROCAMPUS OUEST, UMR1253 STLO, Rennes F-35042, France
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10
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Panwar H, Calderwood D, Gillespie AL, Wylie AR, Graham SF, Grant IR, Grover S, Green BD. Identification of lactic acid bacteria strains modulating incretin hormone secretion and gene expression in enteroendocrine cells. J Funct Foods 2016. [DOI: 10.1016/j.jff.2016.02.040] [Citation(s) in RCA: 16] [Impact Index Per Article: 1.8] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/25/2022] Open
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11
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Lin Q, Mathieu O, Tompkins TA, Buckley ND, Green-Johnson JM. Modulation of the TNFα-induced gene expression profile of intestinal epithelial cells by soy fermented with lactic acid bacteria. J Funct Foods 2016. [DOI: 10.1016/j.jff.2016.02.047] [Citation(s) in RCA: 7] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/16/2022] Open
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12
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Gnauck A, Lentle RG, Kruger MC. The Characteristics and Function of Bacterial Lipopolysaccharides and Their Endotoxic Potential in Humans. Int Rev Immunol 2015; 35:189-218. [PMID: 26606737 DOI: 10.3109/08830185.2015.1087518] [Citation(s) in RCA: 65] [Impact Index Per Article: 6.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/25/2023]
Abstract
Cross-talk between enteral microbiota and human host is essential for the development and maintenance of the human gastrointestinal and systemic immune systems. The presence of lipopolysaccharides (LPS) lysed from the cell membrane of Gram-negative bacteria in the gut lumen is thought to promote the development of a balanced gut immune response whilst the entry of the same LPS into systemic circulation may lead to a deleterious pro-inflammatory systemic immune response. Recent data suggest that chronically low levels of circulating LPS may be associated with the development of metabolic diseases such as insulin resistance, type 2 diabetes, atherosclerosis and cardiovascular disease. This review focuses on the cross-talk between enteral commensal bacteria and the human immune system via LPS. We explain the structural characterisation of the LPS molecule and its function in the bacteria. We then examine how LPS is recognised by various elements of the human immune system and the signalling pathways that are activated by the structure of the LPS molecule and the effect of various concentrations. Further, we discuss the sequelae of this signalling in the gut-associated and systemic immune systems i.e. the neutralisation of LPS and the development of tolerance to LPS.
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Affiliation(s)
- Anne Gnauck
- a School of Food and Nutrition, College of Health , Massey University , Palmerston North , New Zealand
| | - Roger G Lentle
- a School of Food and Nutrition, College of Health , Massey University , Palmerston North , New Zealand
| | - Marlena C Kruger
- a School of Food and Nutrition, College of Health , Massey University , Palmerston North , New Zealand
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13
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Chen J, Tellez G, Richards JD, Escobar J. Identification of Potential Biomarkers for Gut Barrier Failure in Broiler Chickens. Front Vet Sci 2015; 2:14. [PMID: 26664943 PMCID: PMC4672187 DOI: 10.3389/fvets.2015.00014] [Citation(s) in RCA: 147] [Impact Index Per Article: 14.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/19/2015] [Accepted: 05/08/2015] [Indexed: 01/10/2023] Open
Abstract
The objective of the present study was to identify potential biomarkers for gut barrier failure in chickens. A total of 144 day-of-hatch Ross 308 male broiler chickens were housed in 24 battery cages with six chicks per cage. Cages were randomly assigned to either a control group (CON) or gut barrier failure (GBF) group. During the first 13 days, birds in CON or GBF groups were fed a common corn–soy starter diet. On day 14, CON chickens were switched to a corn grower diet, and GBF chickens were switched to rye–wheat–barley grower diet. In addition, on day 21, GBF chickens were orally challenged with a coccidiosis vaccine. At days 21 and 28, birds were weighed by cage and feed intake was recorded to calculate feed conversion ratio. At day 28, one chicken from each cage was euthanized to collect intestinal samples for morphometric analysis, blood for serum, and intestinal mucosa scrapings for gene expression. Overall performance and feed efficiency was severely affected (P < 0.05) by a GBF model when compared with CON group at days 21 and 28. Duodenum of GBF birds had wider villi, longer crypt depth, and higher crypt depth/villi height ratio than CON birds. Similarly, GBF birds had longer crypt depth in jejunum and ileum when compared with CON birds. Protein levels of endotoxin and α1-acid glycoprotein (AGP) in serum, as well as mRNA levels of interleukin (IL)-8, IL-1β, transforming growth factor (TGF)-β4, and fatty acid-binding protein (FABP) 6 were increased (P < 0.05) in GBF birds compared to CON birds; however, mRNA levels of FABP2, occludin, and mucin 2 (MUC2) were reduced by 34% (P < 0.05), 24% (P = 0.107), and 29% (P = 0.088), respectively, in GBF birds compared to CON birds. The results from the present study suggest that serum endotoxin and AGP, as well as, gene expression of FABP2, FABP6, IL-8, IL-1β, TGF-β4, occludin, and MUC2 in mucosa may work as potential biomarkers for gut barrier health in chickens.
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Affiliation(s)
- Juxing Chen
- Novus International, Inc. , St. Charles, MO , USA
| | - Guillermo Tellez
- Department of Poultry Science, University of Arkansas , Fayetteville, AR , USA
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14
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Guo S, Guo Y, Ergun A, Lu L, Walker WA, Ganguli K. Secreted Metabolites of Bifidobacterium infantis and Lactobacillus acidophilus Protect Immature Human Enterocytes from IL-1β-Induced Inflammation: A Transcription Profiling Analysis. PLoS One 2015; 10:e0124549. [PMID: 25906317 PMCID: PMC4407962 DOI: 10.1371/journal.pone.0124549] [Citation(s) in RCA: 34] [Impact Index Per Article: 3.4] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/17/2014] [Accepted: 03/06/2015] [Indexed: 01/28/2023] Open
Abstract
Combination regimens of Bifidobacterium infantis and Lactobacillus acidophilus have been demonstrated to prevent necrotizing enterocolitis (NEC) in clinical trials. However, the molecular mechanisms responsible for this protective effect are not well understood. Additionally, conditioned media from individual cultures of these two probiotics show strain specific modulation of inflammation using in vitro human intestinal NEC models. Here we report a transcription profiling analysis of gene expression in immature human fetal intestinal epithelial cells (H4 cells) pretreated with conditioned media from B. infantis (BCM) or L. acidophilus (LCM) prior to IL-1β stimulation. Compared with control media, the two probiotic-conditioned media (PCM) treatments altered the expression of hundreds of genes involved in the immune response, apoptosis and cell survival, cell adhesion, the cell cycle, development and angiogenesis. In IL-1β-stimulated cells, PCM treatment decreased the upregulation of genes in the NF-κB activation pathway and downregulated genes associated with extracellular matrix (ECM) remodeling. Compared with LCM, BCM showed more significant modulatory effects on ECM remodeling, reflected by a lower p value. IL-6 and IL-8 production was significantly reduced in IL-1β-stimulated cells pretreated with PCM (p<0.05), which was consistent with their altered gene expression. Western blot analysis showed that compared with IL-1β stimulation alone, PCM treatment attenuated the decrease of cytoplasmic IκBα and NF-κB p65 levels as well as the increase of nuclear NF-κB p65 levels in the stimulated cells (p<0.05). In conclusion, PCM treatment exerted anti-inflammatory effects in immature human fetal enterocytes primarily by modulating genes in the NF-κB signaling and ECM remodeling pathways. Additionally, some components of these signaling pathways, particularly the ECM remodeling pathway, were more profoundly affected by BCM than LCM.
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Affiliation(s)
- Shuangshuang Guo
- State Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural University, Beijing, China
- Mucosal Immunology and Biology Research Center, Massachusetts General Hospital for Children and Harvard Medical School, Charlestown, Massachusetts, United States of America
| | - Yuming Guo
- State Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural University, Beijing, China
| | - Ayla Ergun
- Department of Molecular Biology, Massachusetts General Hospital, Boston, Massachusetts, United States of America
| | - Lei Lu
- Section of Neonatology, Department of Pediatrics, The University of Chicago, Chicago, Illinois, United States of America
| | - W. Allan Walker
- Mucosal Immunology and Biology Research Center, Massachusetts General Hospital for Children and Harvard Medical School, Charlestown, Massachusetts, United States of America
- * E-mail: (WAW); (KG)
| | - Kriston Ganguli
- Mucosal Immunology and Biology Research Center, Massachusetts General Hospital for Children and Harvard Medical School, Charlestown, Massachusetts, United States of America
- * E-mail: (WAW); (KG)
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15
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Plaza-Diaz J, Gomez-Llorente C, Fontana L, Gil A. Modulation of immunity and inflammatory gene expression in the gut, in inflammatory diseases of the gut and in the liver by probiotics. World J Gastroenterol 2014; 20:15632-15649. [PMID: 25400447 PMCID: PMC4229528 DOI: 10.3748/wjg.v20.i42.15632] [Citation(s) in RCA: 132] [Impact Index Per Article: 12.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 02/28/2014] [Revised: 05/04/2014] [Accepted: 06/21/2014] [Indexed: 02/06/2023] Open
Abstract
The potential for the positive manipulation of the gut microbiome through the introduction of beneficial microbes, as also known as probiotics, is currently an active area of investigation. The FAO/WHO define probiotics as live microorganisms that confer a health benefit to the host when administered in adequate amounts. However, dead bacteria and bacterial molecular components may also exhibit probiotic properties. The results of clinical studies have demonstrated the clinical potential of probiotics in many pathologies, such as allergic diseases, diarrhea, inflammatory bowel disease and viral infection. Several mechanisms have been proposed to explain the beneficial effects of probiotics, most of which involve gene expression regulation in specific tissues, particularly the intestine and liver. Therefore, the modulation of gene expression mediated by probiotics is an important issue that warrants further investigation. In the present paper, we performed a systematic review of the probiotic-mediated modulation of gene expression that is associated with the immune system and inflammation. Between January 1990 to February 2014, PubMed was searched for articles that were published in English using the MeSH terms "probiotics" and "gene expression" combined with "intestines", "liver", "enterocytes", "antigen-presenting cells", "dendritic cells", "immune system", and "inflammation". Two hundred and five original articles matching these criteria were initially selected, although only those articles that included specific gene expression results (77) were later considered for this review and separated into three major topics: the regulation of immunity and inflammatory gene expression in the gut, in inflammatory diseases of the gut and in the liver. Particular strains of Bifidobacteria, Lactobacilli, Escherichia coli, Propionibacterium, Bacillus and Saccharomyces influence the gene expression of mucins, Toll-like receptors, caspases, nuclear factor-κB, and interleukins and lead mainly to an anti-inflammatory response in cultured enterocytes. In addition, the interaction of commensal bacteria and probiotics with the surface of antigen-presenting cells in vitro results in the downregulation of pro-inflammatory genes that are linked to inflammatory signaling pathways, whereas other anti-inflammatory genes are upregulated. The effects of probiotics have been extensively investigated in animal models ranging from fish to mice, rats and piglets. These bacteria induce a tolerogenic and hyporesponsive immune response in which many genes that are related to the immune system, in particular those genes expressing anti-inflammatory cytokines, are upregulated. By contrast, information related to gene expression in human intestinal cells mediated by the action of probiotics is scarce. There is a need for further clinical studies that evaluate the mechanism of action of probiotics both in healthy humans and in patients with chronic diseases. These types of clinical studies are necessary for addressing the influence of these microorganisms in gene expression for different pathways, particularly those that are associated with the immune response, and to better understand the role that probiotics might have in the prevention and treatment of disease.
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16
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Finelli C, Tarantino G. Non-alcoholic fatty liver disease, diet and gut microbiota. EXCLI JOURNAL 2014; 13:461-490. [PMID: 26417275 PMCID: PMC4464355 DOI: pmid/26417275] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Download PDF] [Figures] [Subscribe] [Scholar Register] [Received: 03/12/2013] [Accepted: 03/31/2014] [Indexed: 02/07/2023]
Abstract
Non-alcoholic fatty liver disease (NAFLD) is a severe liver disease that is increasing in prevalence with the worldwide epidemic of obesity and its related insulin-resistance state. Evidence for the role of the gut microbiota in energy storage and the subsequent development of obesity and some of its related diseases is now well established. More recently, a new role of gut microbiota has emerged in NAFLD. The gut microbiota is involved in gut permeability, low-grade inflammation and immune balance, it modulates dietary choline metabolism, regulates bile acid metabolism and produces endogenous ethanol. All of these factors are molecular mechanisms by which the microbiota can induce NAFLD or its progression toward overt non-alcoholic steatohepatitis. Modification of the gut microbiota composition and/or its biochemical capacity by specific dietary or pharmacological interventions may advantageously affect host metabolism. Large-scale intervention trials, investigating the potential benefit of prebiotics and probiotics in improving cardiometabolic health in high-risk populations, are fervently awaited.
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Affiliation(s)
- Carmine Finelli
- Center of Obesity and Eating Disorders, Stella Maris Mediterraneum Foundation, Potenza, Italy
| | - Giovanni Tarantino
- Department of Clinical Medicine and Surgery, Federico II University Medical School of Naples, Italy
- National Cancer Institute "Foundation G. Pascale" -IRCS- 83013 Mercogliano (Av), Italy
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17
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Multistrain probiotic modulation of intestinal epithelial cells' immune response to a double-stranded RNA ligand, poly(i·c). Appl Environ Microbiol 2013; 80:1692-700. [PMID: 24375132 DOI: 10.1128/aem.03411-13] [Citation(s) in RCA: 31] [Impact Index Per Article: 2.6] [Reference Citation Analysis] [Abstract] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/31/2022] Open
Abstract
A commercially available product containing three probiotic bacterial strains (Lactobacillus helveticus R0052, Bifidobacterium longum subsp. infantis R0033, and Bifidobacterium bifidum R0071) was previously shown in animal trials to modulate both TH1 and TH2 immune responses. Clinical studies on this combination of bacteria have also shown positive health effects against seasonal winter diseases and rotavirus infection. The goal of this study was to use a well-established in vitro intestinal epithelial (HT-29) cell model that has been shown to constitutively express double-stranded RNA (dsRNA) sensors (Toll-like receptor 3 [TLR3], retinoic acid-inducible gene I, melanoma differentiation-associated gene 5, and dsRNA-activated protein kinase). By using the HT-29 cell model, we wanted to evaluate whether or not this combination of three bacteria had the capacity to immune modulate the host cell response to a dsRNA ligand, poly(I·C). Using a custom-designed, two-color expression microarray targeting genes of the human immune system, we investigated the response of HT-29 cells challenged with poly(I·C) both in the presence and in the absence of the three probiotic bacteria. We observed that the combination of the three bacteria had a major impact on attenuating the expression of genes connected to proinflammatory TH1 and antiviral innate immune responses compared to that obtained by the poly(I·C)-only challenge. Major pathways through which the multistrain combination may be eliciting its immune-modulatory effect include the TLR3 domain-containing adapter-inducing beta interferon (TRIF), mitogen-activated protein kinase, and NF-κB signaling pathways. Such a model may be useful for selecting potential biomarkers for the design of future clinical trials.
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18
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Affiliation(s)
- David Gurwitz
- Department of Human Molecular Genetics and Biochemistry; Sackler Faculty of Medicine; Tel-Aviv University; Tel-Aviv; Israel
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