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Helminth-Induced Alterations Of The Gut Microbiota Exacerbate Bacterial Colitis

Infection with the intestinal helminth parasite Heligmosomoides polygyrus exacerbates the colitis caused by the bacterial enteropathogen Citrobacter rodentium. To clarify the underlying mechanism, we analyzed fecal microbiota composition of control and helminth-infected mice and evaluated the functi...

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Autores principales: Su, Chienwen, Su, Libo, Li, Yali, Chang, Jeffrey, Zhang, Wei, Walker, W.A., Xavier, Ramnik J., Cherayil, Bobby J., Shi, Hai Ning
Formato: Online Artículo Texto
Lenguaje:English
Publicado: 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5620113/
https://www.ncbi.nlm.nih.gov/pubmed/28352104
http://dx.doi.org/10.1038/mi.2017.20
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author Su, Chienwen
Su, Libo
Li, Yali
Chang, Jeffrey
Zhang, Wei
Walker, W.A.
Xavier, Ramnik J.
Cherayil, Bobby J.
Shi, Hai Ning
author_facet Su, Chienwen
Su, Libo
Li, Yali
Chang, Jeffrey
Zhang, Wei
Walker, W.A.
Xavier, Ramnik J.
Cherayil, Bobby J.
Shi, Hai Ning
author_sort Su, Chienwen
collection PubMed
description Infection with the intestinal helminth parasite Heligmosomoides polygyrus exacerbates the colitis caused by the bacterial enteropathogen Citrobacter rodentium. To clarify the underlying mechanism, we analyzed fecal microbiota composition of control and helminth-infected mice and evaluated the functional role of compositional differences by microbiota transplantation experiments. Our results showed that infection of Balb/c mice with H. polygyrus resulted in significant changes in the composition of the gut microbiota, characterized by a marked increase in the abundance of Bacteroidetes and decreases in Firmicutes and Lactobacillales. Recipients of the gut microbiota from helminth-infected wide-type, but not STAT 6-deficient, Balb/c donors had increased fecal pathogen shedding and significant worsening of Citrobacter-induced colitis compared to recipients of microbiota from control donors. Recipients of helminth-altered microbiota also displayed increased regulatory T cells and IL-10 expression. Depletion of CD4(+)CD25(+) T cells and neutralization of IL-10 in recipients of helminth-altered microbiota led to reduced stool C. rodentium numbers and attenuated colitis. These results indicate that alteration of the gut microbiota is a significant contributor to the H. polygyrus-induced exacerbation of C. rodentium colitis. The helminth-induced alteration of the microbiota is Th2-dependent and acts by promoting regulatory T cells that suppress protective responses to bacterial enteropathogens.
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spelling pubmed-56201132017-12-21 Helminth-Induced Alterations Of The Gut Microbiota Exacerbate Bacterial Colitis Su, Chienwen Su, Libo Li, Yali Chang, Jeffrey Zhang, Wei Walker, W.A. Xavier, Ramnik J. Cherayil, Bobby J. Shi, Hai Ning Mucosal Immunol Article Infection with the intestinal helminth parasite Heligmosomoides polygyrus exacerbates the colitis caused by the bacterial enteropathogen Citrobacter rodentium. To clarify the underlying mechanism, we analyzed fecal microbiota composition of control and helminth-infected mice and evaluated the functional role of compositional differences by microbiota transplantation experiments. Our results showed that infection of Balb/c mice with H. polygyrus resulted in significant changes in the composition of the gut microbiota, characterized by a marked increase in the abundance of Bacteroidetes and decreases in Firmicutes and Lactobacillales. Recipients of the gut microbiota from helminth-infected wide-type, but not STAT 6-deficient, Balb/c donors had increased fecal pathogen shedding and significant worsening of Citrobacter-induced colitis compared to recipients of microbiota from control donors. Recipients of helminth-altered microbiota also displayed increased regulatory T cells and IL-10 expression. Depletion of CD4(+)CD25(+) T cells and neutralization of IL-10 in recipients of helminth-altered microbiota led to reduced stool C. rodentium numbers and attenuated colitis. These results indicate that alteration of the gut microbiota is a significant contributor to the H. polygyrus-induced exacerbation of C. rodentium colitis. The helminth-induced alteration of the microbiota is Th2-dependent and acts by promoting regulatory T cells that suppress protective responses to bacterial enteropathogens. 2017-03-29 2018-01 /pmc/articles/PMC5620113/ /pubmed/28352104 http://dx.doi.org/10.1038/mi.2017.20 Text en http://www.nature.com/authors/editorial_policies/license.html#terms Users may view, print, copy, and download text and data-mine the content in such documents, for the purposes of academic research, subject always to the full Conditions of use:http://www.nature.com/authors/editorial_policies/license.html#terms
spellingShingle Article
Su, Chienwen
Su, Libo
Li, Yali
Chang, Jeffrey
Zhang, Wei
Walker, W.A.
Xavier, Ramnik J.
Cherayil, Bobby J.
Shi, Hai Ning
Helminth-Induced Alterations Of The Gut Microbiota Exacerbate Bacterial Colitis
title Helminth-Induced Alterations Of The Gut Microbiota Exacerbate Bacterial Colitis
title_full Helminth-Induced Alterations Of The Gut Microbiota Exacerbate Bacterial Colitis
title_fullStr Helminth-Induced Alterations Of The Gut Microbiota Exacerbate Bacterial Colitis
title_full_unstemmed Helminth-Induced Alterations Of The Gut Microbiota Exacerbate Bacterial Colitis
title_short Helminth-Induced Alterations Of The Gut Microbiota Exacerbate Bacterial Colitis
title_sort helminth-induced alterations of the gut microbiota exacerbate bacterial colitis
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5620113/
https://www.ncbi.nlm.nih.gov/pubmed/28352104
http://dx.doi.org/10.1038/mi.2017.20
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