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Acute Cold Water-Immersion Restraint Stress Induces Intestinal Injury and Reduces the Diversity of Gut Microbiota in Mice

Growing evidence has demonstrated that stress triggers gastrointestinal (GI) disorders. This study aimed to investigate how the acute cold water-immersion restraint (CWIR) stress affects intestinal injury and gut microbiota (GM) distribution. Male C57BL/6 mice were used to establish a CWIR animal mo...

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Autores principales: Zhang, Yuan, Wu, Shuwen, Liu, Yongming, Ma, Jingchang, Li, Wenpeng, Xu, Xuexue, Wang, Yuling, Luo, Yanling, Cheng, Kun, Zhuang, Ran
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8551804/
https://www.ncbi.nlm.nih.gov/pubmed/34722327
http://dx.doi.org/10.3389/fcimb.2021.706849
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author Zhang, Yuan
Wu, Shuwen
Liu, Yongming
Ma, Jingchang
Li, Wenpeng
Xu, Xuexue
Wang, Yuling
Luo, Yanling
Cheng, Kun
Zhuang, Ran
author_facet Zhang, Yuan
Wu, Shuwen
Liu, Yongming
Ma, Jingchang
Li, Wenpeng
Xu, Xuexue
Wang, Yuling
Luo, Yanling
Cheng, Kun
Zhuang, Ran
author_sort Zhang, Yuan
collection PubMed
description Growing evidence has demonstrated that stress triggers gastrointestinal (GI) disorders. This study aimed to investigate how the acute cold water-immersion restraint (CWIR) stress affects intestinal injury and gut microbiota (GM) distribution. Male C57BL/6 mice were used to establish a CWIR animal model. Hematoxylin–eosin and periodic acid–Schiff staining were performed to assess intestinal histopathological changes. Reverse transcription quantitative polymerase chain reaction (RT-qPCR) analysis and immunofluorescence staining were used to evaluate the expression of inflammatory cytokines and immune cell infiltration in the intestinal tissues. The gut permeability and intestinal occludin protein expression were determined through fluorescein isothiocyanate-dextran detection and western blot, respectively. GM profiles were analyzed via high-throughput sequencing of the fecal bacterial 16S rRNA genes. Results showed that CWIR induced more severe intestinal mucosal injury compared to the control, leading to a significant increase in tumor necrosis factor-α expression, but no infiltration of neutrophil and T cells. CWIR also resulted in GI disruption and increased the permeability of the intestinal mucosa. GM profiles showed that CWIR reduced GM diversity of mice compared with the control group. Specifically, aerobic and gram-negative bacteria significantly increased after CWIR, which was associated with the severity of gut injury under stress. Therefore, acute CWIR leads to severe intestinal damage with inflammation and disrupts the GM homeostasis, contributing to decreased GM diversity. Our findings provide the theoretical basis for the further treatment of intestinal disorders induced by CWIR.
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spelling pubmed-85518042021-10-29 Acute Cold Water-Immersion Restraint Stress Induces Intestinal Injury and Reduces the Diversity of Gut Microbiota in Mice Zhang, Yuan Wu, Shuwen Liu, Yongming Ma, Jingchang Li, Wenpeng Xu, Xuexue Wang, Yuling Luo, Yanling Cheng, Kun Zhuang, Ran Front Cell Infect Microbiol Cellular and Infection Microbiology Growing evidence has demonstrated that stress triggers gastrointestinal (GI) disorders. This study aimed to investigate how the acute cold water-immersion restraint (CWIR) stress affects intestinal injury and gut microbiota (GM) distribution. Male C57BL/6 mice were used to establish a CWIR animal model. Hematoxylin–eosin and periodic acid–Schiff staining were performed to assess intestinal histopathological changes. Reverse transcription quantitative polymerase chain reaction (RT-qPCR) analysis and immunofluorescence staining were used to evaluate the expression of inflammatory cytokines and immune cell infiltration in the intestinal tissues. The gut permeability and intestinal occludin protein expression were determined through fluorescein isothiocyanate-dextran detection and western blot, respectively. GM profiles were analyzed via high-throughput sequencing of the fecal bacterial 16S rRNA genes. Results showed that CWIR induced more severe intestinal mucosal injury compared to the control, leading to a significant increase in tumor necrosis factor-α expression, but no infiltration of neutrophil and T cells. CWIR also resulted in GI disruption and increased the permeability of the intestinal mucosa. GM profiles showed that CWIR reduced GM diversity of mice compared with the control group. Specifically, aerobic and gram-negative bacteria significantly increased after CWIR, which was associated with the severity of gut injury under stress. Therefore, acute CWIR leads to severe intestinal damage with inflammation and disrupts the GM homeostasis, contributing to decreased GM diversity. Our findings provide the theoretical basis for the further treatment of intestinal disorders induced by CWIR. Frontiers Media S.A. 2021-10-14 /pmc/articles/PMC8551804/ /pubmed/34722327 http://dx.doi.org/10.3389/fcimb.2021.706849 Text en Copyright © 2021 Zhang, Wu, Liu, Ma, Li, Xu, Wang, Luo, Cheng and Zhuang https://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 Cellular and Infection Microbiology
Zhang, Yuan
Wu, Shuwen
Liu, Yongming
Ma, Jingchang
Li, Wenpeng
Xu, Xuexue
Wang, Yuling
Luo, Yanling
Cheng, Kun
Zhuang, Ran
Acute Cold Water-Immersion Restraint Stress Induces Intestinal Injury and Reduces the Diversity of Gut Microbiota in Mice
title Acute Cold Water-Immersion Restraint Stress Induces Intestinal Injury and Reduces the Diversity of Gut Microbiota in Mice
title_full Acute Cold Water-Immersion Restraint Stress Induces Intestinal Injury and Reduces the Diversity of Gut Microbiota in Mice
title_fullStr Acute Cold Water-Immersion Restraint Stress Induces Intestinal Injury and Reduces the Diversity of Gut Microbiota in Mice
title_full_unstemmed Acute Cold Water-Immersion Restraint Stress Induces Intestinal Injury and Reduces the Diversity of Gut Microbiota in Mice
title_short Acute Cold Water-Immersion Restraint Stress Induces Intestinal Injury and Reduces the Diversity of Gut Microbiota in Mice
title_sort acute cold water-immersion restraint stress induces intestinal injury and reduces the diversity of gut microbiota in mice
topic Cellular and Infection Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8551804/
https://www.ncbi.nlm.nih.gov/pubmed/34722327
http://dx.doi.org/10.3389/fcimb.2021.706849
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