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Akkermansia muciniphila exacerbates food allergy in fibre-deprived mice

Alterations in the gut microbiome, including diet-driven changes, are linked to the rising prevalence of food allergy. However, little is known about how specific gut bacteria trigger the breakdown of oral tolerance. Here we show that depriving specific-pathogen-free mice of dietary fibre leads to a...

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Autores principales: Parrish, Amy, Boudaud, Marie, Grant, Erica T., Willieme, Stéphanie, Neumann, Mareike, Wolter, Mathis, Craig, Sophie Z., De Sciscio, Alessandro, Cosma, Antonio, Hunewald, Oliver, Ollert, Markus, Desai, Mahesh S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10522492/
https://www.ncbi.nlm.nih.gov/pubmed/37696941
http://dx.doi.org/10.1038/s41564-023-01464-1
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author Parrish, Amy
Boudaud, Marie
Grant, Erica T.
Willieme, Stéphanie
Neumann, Mareike
Wolter, Mathis
Craig, Sophie Z.
De Sciscio, Alessandro
Cosma, Antonio
Hunewald, Oliver
Ollert, Markus
Desai, Mahesh S.
author_facet Parrish, Amy
Boudaud, Marie
Grant, Erica T.
Willieme, Stéphanie
Neumann, Mareike
Wolter, Mathis
Craig, Sophie Z.
De Sciscio, Alessandro
Cosma, Antonio
Hunewald, Oliver
Ollert, Markus
Desai, Mahesh S.
author_sort Parrish, Amy
collection PubMed
description Alterations in the gut microbiome, including diet-driven changes, are linked to the rising prevalence of food allergy. However, little is known about how specific gut bacteria trigger the breakdown of oral tolerance. Here we show that depriving specific-pathogen-free mice of dietary fibre leads to a gut microbiota signature with increases in the mucin-degrading bacterium Akkermansia muciniphila. This signature is associated with intestinal barrier dysfunction, increased expression of type 1 and 2 cytokines and IgE-coated commensals in the colon, which result in an exacerbated allergic reaction to food allergens, ovalbumin and peanut. To demonstrate the causal role of A. muciniphila, we employed a tractable synthetic human gut microbiota in gnotobiotic mice. The presence of A. muciniphila within the microbiota, combined with fibre deprivation, resulted in stronger anti-commensal IgE coating and innate type-2 immune responses, which worsened symptoms of food allergy. Our study provides important insights into how gut microbes can regulate immune pathways of food allergy in a diet-dependent manner.
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spelling pubmed-105224922023-09-28 Akkermansia muciniphila exacerbates food allergy in fibre-deprived mice Parrish, Amy Boudaud, Marie Grant, Erica T. Willieme, Stéphanie Neumann, Mareike Wolter, Mathis Craig, Sophie Z. De Sciscio, Alessandro Cosma, Antonio Hunewald, Oliver Ollert, Markus Desai, Mahesh S. Nat Microbiol Article Alterations in the gut microbiome, including diet-driven changes, are linked to the rising prevalence of food allergy. However, little is known about how specific gut bacteria trigger the breakdown of oral tolerance. Here we show that depriving specific-pathogen-free mice of dietary fibre leads to a gut microbiota signature with increases in the mucin-degrading bacterium Akkermansia muciniphila. This signature is associated with intestinal barrier dysfunction, increased expression of type 1 and 2 cytokines and IgE-coated commensals in the colon, which result in an exacerbated allergic reaction to food allergens, ovalbumin and peanut. To demonstrate the causal role of A. muciniphila, we employed a tractable synthetic human gut microbiota in gnotobiotic mice. The presence of A. muciniphila within the microbiota, combined with fibre deprivation, resulted in stronger anti-commensal IgE coating and innate type-2 immune responses, which worsened symptoms of food allergy. Our study provides important insights into how gut microbes can regulate immune pathways of food allergy in a diet-dependent manner. Nature Publishing Group UK 2023-09-11 2023 /pmc/articles/PMC10522492/ /pubmed/37696941 http://dx.doi.org/10.1038/s41564-023-01464-1 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/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/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Parrish, Amy
Boudaud, Marie
Grant, Erica T.
Willieme, Stéphanie
Neumann, Mareike
Wolter, Mathis
Craig, Sophie Z.
De Sciscio, Alessandro
Cosma, Antonio
Hunewald, Oliver
Ollert, Markus
Desai, Mahesh S.
Akkermansia muciniphila exacerbates food allergy in fibre-deprived mice
title Akkermansia muciniphila exacerbates food allergy in fibre-deprived mice
title_full Akkermansia muciniphila exacerbates food allergy in fibre-deprived mice
title_fullStr Akkermansia muciniphila exacerbates food allergy in fibre-deprived mice
title_full_unstemmed Akkermansia muciniphila exacerbates food allergy in fibre-deprived mice
title_short Akkermansia muciniphila exacerbates food allergy in fibre-deprived mice
title_sort akkermansia muciniphila exacerbates food allergy in fibre-deprived mice
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10522492/
https://www.ncbi.nlm.nih.gov/pubmed/37696941
http://dx.doi.org/10.1038/s41564-023-01464-1
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