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Deficiency of Dietary Fiber Modulates Gut Microbiota Composition, Neutrophil Recruitment and Worsens Experimental Colitis

Ulcerative colitis is an inflammatory disease of the colon that is associated with colonic neutrophil accumulation. Recent evidence indicates that diet alters the composition of the gut microbiota and influences host–pathogen interactions. Specifically, bacterial fermentation of dietary fiber produc...

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Autores principales: Shen, Sj, Prame Kumar, Kathryn, Wen, Shu Wen, Shim, Raymond, Wanrooy, Brooke J., Stanley, Dragana, Moore, Robert J., Van, Thi Thu Hao, Robert, Remy, Hickey, Michael J., Wong, Connie H. Y.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7940676/
https://www.ncbi.nlm.nih.gov/pubmed/33708211
http://dx.doi.org/10.3389/fimmu.2021.619366
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author Shen, Sj
Prame Kumar, Kathryn
Wen, Shu Wen
Shim, Raymond
Wanrooy, Brooke J.
Stanley, Dragana
Moore, Robert J.
Van, Thi Thu Hao
Robert, Remy
Hickey, Michael J.
Wong, Connie H. Y.
author_facet Shen, Sj
Prame Kumar, Kathryn
Wen, Shu Wen
Shim, Raymond
Wanrooy, Brooke J.
Stanley, Dragana
Moore, Robert J.
Van, Thi Thu Hao
Robert, Remy
Hickey, Michael J.
Wong, Connie H. Y.
author_sort Shen, Sj
collection PubMed
description Ulcerative colitis is an inflammatory disease of the colon that is associated with colonic neutrophil accumulation. Recent evidence indicates that diet alters the composition of the gut microbiota and influences host–pathogen interactions. Specifically, bacterial fermentation of dietary fiber produces metabolites called short-chain fatty acids (SCFAs), which have been shown to protect against various inflammatory diseases. However, the effect of fiber deficiency on the key initial steps of inflammation, such as leukocyte–endothelial cell interactions, is unknown. Moreover, the impact of fiber deficiency on neutrophil recruitment under basal conditions and during inflammation in vivo is unknown. Herein, we hypothesized that a fiber-deficient diet promotes an inflammatory state in the colon at baseline and predisposes the host to more severe colitis pathology. Mice fed a no-fiber diet for 14 days showed significant changes in the gut microbiota and exhibited increased neutrophil-endothelial interactions in the colonic microvasculature. Although mice fed a no-fiber diet alone did not have observable colitis-associated symptoms, these animals were highly susceptible to low dose (0.5%) dextran sodium sulphate (DSS)-induced model of colitis. Supplementation of the most abundant SCFA, acetate, prevented no-fiber diet-mediated enrichment of colonic neutrophils and colitis pathology. Therefore, dietary fiber, possibly through the actions of acetate, plays an important role in regulating neutrophil recruitment and host protection against inflammatory colonic damage in an experimental model of colitis.
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spelling pubmed-79406762021-03-10 Deficiency of Dietary Fiber Modulates Gut Microbiota Composition, Neutrophil Recruitment and Worsens Experimental Colitis Shen, Sj Prame Kumar, Kathryn Wen, Shu Wen Shim, Raymond Wanrooy, Brooke J. Stanley, Dragana Moore, Robert J. Van, Thi Thu Hao Robert, Remy Hickey, Michael J. Wong, Connie H. Y. Front Immunol Immunology Ulcerative colitis is an inflammatory disease of the colon that is associated with colonic neutrophil accumulation. Recent evidence indicates that diet alters the composition of the gut microbiota and influences host–pathogen interactions. Specifically, bacterial fermentation of dietary fiber produces metabolites called short-chain fatty acids (SCFAs), which have been shown to protect against various inflammatory diseases. However, the effect of fiber deficiency on the key initial steps of inflammation, such as leukocyte–endothelial cell interactions, is unknown. Moreover, the impact of fiber deficiency on neutrophil recruitment under basal conditions and during inflammation in vivo is unknown. Herein, we hypothesized that a fiber-deficient diet promotes an inflammatory state in the colon at baseline and predisposes the host to more severe colitis pathology. Mice fed a no-fiber diet for 14 days showed significant changes in the gut microbiota and exhibited increased neutrophil-endothelial interactions in the colonic microvasculature. Although mice fed a no-fiber diet alone did not have observable colitis-associated symptoms, these animals were highly susceptible to low dose (0.5%) dextran sodium sulphate (DSS)-induced model of colitis. Supplementation of the most abundant SCFA, acetate, prevented no-fiber diet-mediated enrichment of colonic neutrophils and colitis pathology. Therefore, dietary fiber, possibly through the actions of acetate, plays an important role in regulating neutrophil recruitment and host protection against inflammatory colonic damage in an experimental model of colitis. Frontiers Media S.A. 2021-02-23 /pmc/articles/PMC7940676/ /pubmed/33708211 http://dx.doi.org/10.3389/fimmu.2021.619366 Text en Copyright © 2021 Shen, Prame Kumar, Wen, Shim, Wanrooy, Stanley, Moore, Van, Robert, Hickey and Wong http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Immunology
Shen, Sj
Prame Kumar, Kathryn
Wen, Shu Wen
Shim, Raymond
Wanrooy, Brooke J.
Stanley, Dragana
Moore, Robert J.
Van, Thi Thu Hao
Robert, Remy
Hickey, Michael J.
Wong, Connie H. Y.
Deficiency of Dietary Fiber Modulates Gut Microbiota Composition, Neutrophil Recruitment and Worsens Experimental Colitis
title Deficiency of Dietary Fiber Modulates Gut Microbiota Composition, Neutrophil Recruitment and Worsens Experimental Colitis
title_full Deficiency of Dietary Fiber Modulates Gut Microbiota Composition, Neutrophil Recruitment and Worsens Experimental Colitis
title_fullStr Deficiency of Dietary Fiber Modulates Gut Microbiota Composition, Neutrophil Recruitment and Worsens Experimental Colitis
title_full_unstemmed Deficiency of Dietary Fiber Modulates Gut Microbiota Composition, Neutrophil Recruitment and Worsens Experimental Colitis
title_short Deficiency of Dietary Fiber Modulates Gut Microbiota Composition, Neutrophil Recruitment and Worsens Experimental Colitis
title_sort deficiency of dietary fiber modulates gut microbiota composition, neutrophil recruitment and worsens experimental colitis
topic Immunology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7940676/
https://www.ncbi.nlm.nih.gov/pubmed/33708211
http://dx.doi.org/10.3389/fimmu.2021.619366
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