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Beneficial effect of butyrate‐producing Lachnospiraceae on stress‐induced visceral hypersensitivity in rats

BACKGROUND AND AIM: Emerging evidence indicates that psychological stress is involved in the pathogenesis of irritable bowel syndrome, which is characterized by visceral hypersensitivity and may be accompanied by gut dysbiosis. However, how such stress contributes to the development of visceral hype...

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Autores principales: Zhang, Jindong, Song, Lijin, Wang, Yujing, Liu, Chang, Zhang, Lu, Zhu, Shiwei, Liu, Shuangjiang, Duan, Liping
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7379616/
https://www.ncbi.nlm.nih.gov/pubmed/30402954
http://dx.doi.org/10.1111/jgh.14536
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author Zhang, Jindong
Song, Lijin
Wang, Yujing
Liu, Chang
Zhang, Lu
Zhu, Shiwei
Liu, Shuangjiang
Duan, Liping
author_facet Zhang, Jindong
Song, Lijin
Wang, Yujing
Liu, Chang
Zhang, Lu
Zhu, Shiwei
Liu, Shuangjiang
Duan, Liping
author_sort Zhang, Jindong
collection PubMed
description BACKGROUND AND AIM: Emerging evidence indicates that psychological stress is involved in the pathogenesis of irritable bowel syndrome, which is characterized by visceral hypersensitivity and may be accompanied by gut dysbiosis. However, how such stress contributes to the development of visceral hypersensitivity is incompletely understood. Here, we aimed to investigate the influence that stress‐induced microbial changes exert on visceral sensitivity, as well as the possible underlying mechanisms associated with this effect. METHODS: Male Sprague–Dawley rats underwent chronic water avoidance stress (WAS) to induce visceral hypersensitivity. Visceral sensitivity, colonic tight junction protein expression, and short‐chain fatty acids of cecal contents were measured. Fecal samples were collected to characterize microbiota profiles. In a separate study, oral gavage of Roseburia in WAS rats was conducted to verify its potential role in the effectiveness on visceral hypersensitivity. RESULTS: Repeated WAS caused visceral hypersensitivity, altered fecal microbiota composition and function, and decreased occludin expression in the colon. Stressed rats exhibited reduced representation of pathways involved in the metabolism of butyrate and reduced abundance of several operational taxonomic units associated with butyrate‐producing bacteria, such as Lachnospiraceae. Consistently, supplementation with Roseburia hominis, a species belonging to Lachnospiraceae, significantly increased cecal butyrate content. Moreover, Roseburia supplementation alleviated visceral hypersensitivity and prevented the decreased expression of occludin. CONCLUSIONS: Reduction in the abundance of butyrate‐producing Lachnospiraceae, which is beneficial for the intestinal barrier, was involved in the formation of visceral hypersensitivity. R. hominis is a potential probiotic for treating stress‐induced visceral hypersensitivity.
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spelling pubmed-73796162020-07-24 Beneficial effect of butyrate‐producing Lachnospiraceae on stress‐induced visceral hypersensitivity in rats Zhang, Jindong Song, Lijin Wang, Yujing Liu, Chang Zhang, Lu Zhu, Shiwei Liu, Shuangjiang Duan, Liping J Gastroenterol Hepatol Experimental Gastroenterology BACKGROUND AND AIM: Emerging evidence indicates that psychological stress is involved in the pathogenesis of irritable bowel syndrome, which is characterized by visceral hypersensitivity and may be accompanied by gut dysbiosis. However, how such stress contributes to the development of visceral hypersensitivity is incompletely understood. Here, we aimed to investigate the influence that stress‐induced microbial changes exert on visceral sensitivity, as well as the possible underlying mechanisms associated with this effect. METHODS: Male Sprague–Dawley rats underwent chronic water avoidance stress (WAS) to induce visceral hypersensitivity. Visceral sensitivity, colonic tight junction protein expression, and short‐chain fatty acids of cecal contents were measured. Fecal samples were collected to characterize microbiota profiles. In a separate study, oral gavage of Roseburia in WAS rats was conducted to verify its potential role in the effectiveness on visceral hypersensitivity. RESULTS: Repeated WAS caused visceral hypersensitivity, altered fecal microbiota composition and function, and decreased occludin expression in the colon. Stressed rats exhibited reduced representation of pathways involved in the metabolism of butyrate and reduced abundance of several operational taxonomic units associated with butyrate‐producing bacteria, such as Lachnospiraceae. Consistently, supplementation with Roseburia hominis, a species belonging to Lachnospiraceae, significantly increased cecal butyrate content. Moreover, Roseburia supplementation alleviated visceral hypersensitivity and prevented the decreased expression of occludin. CONCLUSIONS: Reduction in the abundance of butyrate‐producing Lachnospiraceae, which is beneficial for the intestinal barrier, was involved in the formation of visceral hypersensitivity. R. hominis is a potential probiotic for treating stress‐induced visceral hypersensitivity. John Wiley and Sons Inc. 2018-12-16 2019-08 /pmc/articles/PMC7379616/ /pubmed/30402954 http://dx.doi.org/10.1111/jgh.14536 Text en © 2018 The Authors. Journal of Gastroenterology and Hepatology published by Journal of Gastroenterology and Hepatology Foundation and John Wiley & Sons Australia, Ltd This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes.
spellingShingle Experimental Gastroenterology
Zhang, Jindong
Song, Lijin
Wang, Yujing
Liu, Chang
Zhang, Lu
Zhu, Shiwei
Liu, Shuangjiang
Duan, Liping
Beneficial effect of butyrate‐producing Lachnospiraceae on stress‐induced visceral hypersensitivity in rats
title Beneficial effect of butyrate‐producing Lachnospiraceae on stress‐induced visceral hypersensitivity in rats
title_full Beneficial effect of butyrate‐producing Lachnospiraceae on stress‐induced visceral hypersensitivity in rats
title_fullStr Beneficial effect of butyrate‐producing Lachnospiraceae on stress‐induced visceral hypersensitivity in rats
title_full_unstemmed Beneficial effect of butyrate‐producing Lachnospiraceae on stress‐induced visceral hypersensitivity in rats
title_short Beneficial effect of butyrate‐producing Lachnospiraceae on stress‐induced visceral hypersensitivity in rats
title_sort beneficial effect of butyrate‐producing lachnospiraceae on stress‐induced visceral hypersensitivity in rats
topic Experimental Gastroenterology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7379616/
https://www.ncbi.nlm.nih.gov/pubmed/30402954
http://dx.doi.org/10.1111/jgh.14536
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