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Perturbation of the gut microbiome by Prevotella spp. enhances host susceptibility to mucosal inflammation

Diverse microbial signatures within the intestinal microbiota have been associated with intestinal and systemic inflammatory diseases, but whether these candidate microbes actively modulate host phenotypes or passively expand within the altered microbial ecosystem is frequently not known. Here we de...

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Autores principales: Iljazovic, Aida, Roy, Urmi, Gálvez, Eric J. C., Lesker, Till R., Zhao, Bei, Gronow, Achim, Amend, Lena, Will, Sabine E., Hofmann, Julia D., Pils, Marina C., Schmidt-Hohagen, Kerstin, Neumann-Schaal, Meina, Strowig, Till
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group US 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7790746/
https://www.ncbi.nlm.nih.gov/pubmed/32433514
http://dx.doi.org/10.1038/s41385-020-0296-4
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author Iljazovic, Aida
Roy, Urmi
Gálvez, Eric J. C.
Lesker, Till R.
Zhao, Bei
Gronow, Achim
Amend, Lena
Will, Sabine E.
Hofmann, Julia D.
Pils, Marina C.
Schmidt-Hohagen, Kerstin
Neumann-Schaal, Meina
Strowig, Till
author_facet Iljazovic, Aida
Roy, Urmi
Gálvez, Eric J. C.
Lesker, Till R.
Zhao, Bei
Gronow, Achim
Amend, Lena
Will, Sabine E.
Hofmann, Julia D.
Pils, Marina C.
Schmidt-Hohagen, Kerstin
Neumann-Schaal, Meina
Strowig, Till
author_sort Iljazovic, Aida
collection PubMed
description Diverse microbial signatures within the intestinal microbiota have been associated with intestinal and systemic inflammatory diseases, but whether these candidate microbes actively modulate host phenotypes or passively expand within the altered microbial ecosystem is frequently not known. Here we demonstrate that colonization of mice with a member of the genus Prevotella, which has been previously associated to colitis in mice, exacerbates intestinal inflammation. Our analysis revealed that Prevotella intestinalis alters composition and function of the ecosystem resulting in a reduction of short-chain fatty acids, specifically acetate, and consequently a decrease in intestinal IL-18 levels during steady state. Supplementation of IL-18 to Prevotella-colonized mice was sufficient to reduce intestinal inflammation. Hence, we conclude that intestinal Prevotella colonization results in metabolic changes in the microbiota, which reduce IL-18 production and consequently exacerbate intestinal inflammation, and potential systemic autoimmunity.
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spelling pubmed-77907462021-01-15 Perturbation of the gut microbiome by Prevotella spp. enhances host susceptibility to mucosal inflammation Iljazovic, Aida Roy, Urmi Gálvez, Eric J. C. Lesker, Till R. Zhao, Bei Gronow, Achim Amend, Lena Will, Sabine E. Hofmann, Julia D. Pils, Marina C. Schmidt-Hohagen, Kerstin Neumann-Schaal, Meina Strowig, Till Mucosal Immunol Article Diverse microbial signatures within the intestinal microbiota have been associated with intestinal and systemic inflammatory diseases, but whether these candidate microbes actively modulate host phenotypes or passively expand within the altered microbial ecosystem is frequently not known. Here we demonstrate that colonization of mice with a member of the genus Prevotella, which has been previously associated to colitis in mice, exacerbates intestinal inflammation. Our analysis revealed that Prevotella intestinalis alters composition and function of the ecosystem resulting in a reduction of short-chain fatty acids, specifically acetate, and consequently a decrease in intestinal IL-18 levels during steady state. Supplementation of IL-18 to Prevotella-colonized mice was sufficient to reduce intestinal inflammation. Hence, we conclude that intestinal Prevotella colonization results in metabolic changes in the microbiota, which reduce IL-18 production and consequently exacerbate intestinal inflammation, and potential systemic autoimmunity. Nature Publishing Group US 2020-05-20 2021 /pmc/articles/PMC7790746/ /pubmed/32433514 http://dx.doi.org/10.1038/s41385-020-0296-4 Text en © The Author(s) 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Iljazovic, Aida
Roy, Urmi
Gálvez, Eric J. C.
Lesker, Till R.
Zhao, Bei
Gronow, Achim
Amend, Lena
Will, Sabine E.
Hofmann, Julia D.
Pils, Marina C.
Schmidt-Hohagen, Kerstin
Neumann-Schaal, Meina
Strowig, Till
Perturbation of the gut microbiome by Prevotella spp. enhances host susceptibility to mucosal inflammation
title Perturbation of the gut microbiome by Prevotella spp. enhances host susceptibility to mucosal inflammation
title_full Perturbation of the gut microbiome by Prevotella spp. enhances host susceptibility to mucosal inflammation
title_fullStr Perturbation of the gut microbiome by Prevotella spp. enhances host susceptibility to mucosal inflammation
title_full_unstemmed Perturbation of the gut microbiome by Prevotella spp. enhances host susceptibility to mucosal inflammation
title_short Perturbation of the gut microbiome by Prevotella spp. enhances host susceptibility to mucosal inflammation
title_sort perturbation of the gut microbiome by prevotella spp. enhances host susceptibility to mucosal inflammation
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7790746/
https://www.ncbi.nlm.nih.gov/pubmed/32433514
http://dx.doi.org/10.1038/s41385-020-0296-4
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