Gut Microbiota Are Associated With Psychological Stress-Induced Defections in Intestinal and Blood–Brain Barriers

Altered gut microbiota has been identified during psychological stress, which causes severe health issues worldwide. The integrity of the intestinal barrier and blood–brain barrier regulates the process of bacterial translocation and can supply the nervous system with real-time information about the...

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Main Authors: Shaohui Geng, Liping Yang, Feng Cheng, Zhumou Zhang, Jiangbo Li, Wenbo Liu, Yujie Li, Yukun Chen, Yu Bao, Lin Chen, Zihao Fei, Xinmin Li, Junlin Hou, Yuan Lin, Zhilin Liu, Shuai Zhang, Hengtao Wang, Qing Zhang, Honggang Wang, Xiaodan Wang, Jingtao Zhang
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-01-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2019.03067/full
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language English
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author Shaohui Geng
Liping Yang
Feng Cheng
Zhumou Zhang
Jiangbo Li
Wenbo Liu
Yujie Li
Yukun Chen
Yu Bao
Lin Chen
Zihao Fei
Xinmin Li
Junlin Hou
Yuan Lin
Zhilin Liu
Shuai Zhang
Hengtao Wang
Qing Zhang
Honggang Wang
Xiaodan Wang
Jingtao Zhang
spellingShingle Shaohui Geng
Liping Yang
Feng Cheng
Zhumou Zhang
Jiangbo Li
Wenbo Liu
Yujie Li
Yukun Chen
Yu Bao
Lin Chen
Zihao Fei
Xinmin Li
Junlin Hou
Yuan Lin
Zhilin Liu
Shuai Zhang
Hengtao Wang
Qing Zhang
Honggang Wang
Xiaodan Wang
Jingtao Zhang
Gut Microbiota Are Associated With Psychological Stress-Induced Defections in Intestinal and Blood–Brain Barriers
Frontiers in Microbiology
gut microbiota
dysbiosis
psychological stress
intestinal barrier
blood–brain barrier
tight junction
author_facet Shaohui Geng
Liping Yang
Feng Cheng
Zhumou Zhang
Jiangbo Li
Wenbo Liu
Yujie Li
Yukun Chen
Yu Bao
Lin Chen
Zihao Fei
Xinmin Li
Junlin Hou
Yuan Lin
Zhilin Liu
Shuai Zhang
Hengtao Wang
Qing Zhang
Honggang Wang
Xiaodan Wang
Jingtao Zhang
author_sort Shaohui Geng
title Gut Microbiota Are Associated With Psychological Stress-Induced Defections in Intestinal and Blood–Brain Barriers
title_short Gut Microbiota Are Associated With Psychological Stress-Induced Defections in Intestinal and Blood–Brain Barriers
title_full Gut Microbiota Are Associated With Psychological Stress-Induced Defections in Intestinal and Blood–Brain Barriers
title_fullStr Gut Microbiota Are Associated With Psychological Stress-Induced Defections in Intestinal and Blood–Brain Barriers
title_full_unstemmed Gut Microbiota Are Associated With Psychological Stress-Induced Defections in Intestinal and Blood–Brain Barriers
title_sort gut microbiota are associated with psychological stress-induced defections in intestinal and blood–brain barriers
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2020-01-01
description Altered gut microbiota has been identified during psychological stress, which causes severe health issues worldwide. The integrity of the intestinal barrier and blood–brain barrier regulates the process of bacterial translocation and can supply the nervous system with real-time information about the environment. However, the association of gut microbiota with psychological stress remains to be fully interpreted. In this study, we established a psychological stress model using an improved communication box and compared the expression of tight junction proteins in multiple regions of the intestinal (duodenum, jejunum, ileum) and blood–brain (amygdala, hippocampus) barriers between model and control rats. We also conducted fecal microbiota analysis using 16S rRNA gene sequencing. Expression levels of the stress-related indicators adrenocorticotropic hormone, NR3C1,2, and norepinephrine were increased in the model group compared to control group. Psychological stress reduced brain and intestinal levels of tight junction proteins, including claudin5, occludin, α-actin, and ZO-1. Microbiota analysis revealed elevated microbial diversity and fecal proportions of Intestinimonas, Catenisphaera, and Globicatella in the model group. Further analysis indicated a negative correlation of Allisonella and Odoribacter, as well as a positive correlation of norank_f__Peptococcaceae, Clostridium_sensu_stricto_1, and Coprococcus_2, with claudin5, occludin, α-actin, and ZO-1. Our use of a rodent model to explore the association between compromised intestinal and blood–brain barriers and altered fecal microbiota under psychological stress improves our understanding of the gut–brain axis. Here, cues converge to control basic developmental processes in the intestine and brain such as barrier function. This study provides new directions for investigating the pathogenesis of emotional disorders and the formulation of clinical treatment.
topic gut microbiota
dysbiosis
psychological stress
intestinal barrier
blood–brain barrier
tight junction
url https://www.frontiersin.org/article/10.3389/fmicb.2019.03067/full
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spelling doaj-b3da13d93264497a943deb8de630bdc92020-11-25T02:34:06ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2020-01-011010.3389/fmicb.2019.03067476330Gut Microbiota Are Associated With Psychological Stress-Induced Defections in Intestinal and Blood–Brain BarriersShaohui Geng0Liping Yang1Feng Cheng2Zhumou Zhang3Jiangbo Li4Wenbo Liu5Yujie Li6Yukun Chen7Yu Bao8Lin Chen9Zihao Fei10Xinmin Li11Junlin Hou12Yuan Lin13Zhilin Liu14Shuai Zhang15Hengtao Wang16Qing Zhang17Honggang Wang18Xiaodan Wang19Jingtao Zhang20First Clinical Medical College, Henan University of Chinese Medicine, Zhengzhou, ChinaBasic Medical College, Henan University of Chinese Medicine, Zhengzhou, ChinaFirst Clinical Medical College, Henan University of Chinese Medicine, Zhengzhou, ChinaFirst Clinical Medical College, Henan University of Chinese Medicine, Zhengzhou, ChinaFirst Clinical Medical College, Henan University of Chinese Medicine, Zhengzhou, ChinaFirst Clinical Medical College, Henan University of Chinese Medicine, Zhengzhou, ChinaBasic Medical College, Henan University of Chinese Medicine, Zhengzhou, ChinaFirst Clinical Medical College, Henan University of Chinese Medicine, Zhengzhou, ChinaFirst Clinical Medical College, Henan University of Chinese Medicine, Zhengzhou, ChinaFirst Clinical Medical College, Henan University of Chinese Medicine, Zhengzhou, ChinaRehabilitation Medical College, Henan University of Chinese Medicine, Zhengzhou, ChinaBasic Medical College, Henan University of Chinese Medicine, Zhengzhou, ChinaBasic Medical College, Henan University of Chinese Medicine, Zhengzhou, ChinaBasic Medical College, Henan University of Chinese Medicine, Zhengzhou, ChinaFirst Clinical Medical College, Henan University of Chinese Medicine, Zhengzhou, ChinaFirst Clinical Medical College, Henan University of Chinese Medicine, Zhengzhou, ChinaFirst Clinical Medical College, Henan University of Chinese Medicine, Zhengzhou, ChinaFirst Clinical Medical College, Henan University of Chinese Medicine, Zhengzhou, ChinaSchool of Pharmacy, Henan University of Chinese Medicine, Zhengzhou, ChinaAcupuncture and Massage College, Henan University of Chinese Medicine, Zhengzhou, ChinaFirst Clinical Medical College, Henan University of Chinese Medicine, Zhengzhou, ChinaAltered gut microbiota has been identified during psychological stress, which causes severe health issues worldwide. The integrity of the intestinal barrier and blood–brain barrier regulates the process of bacterial translocation and can supply the nervous system with real-time information about the environment. However, the association of gut microbiota with psychological stress remains to be fully interpreted. In this study, we established a psychological stress model using an improved communication box and compared the expression of tight junction proteins in multiple regions of the intestinal (duodenum, jejunum, ileum) and blood–brain (amygdala, hippocampus) barriers between model and control rats. We also conducted fecal microbiota analysis using 16S rRNA gene sequencing. Expression levels of the stress-related indicators adrenocorticotropic hormone, NR3C1,2, and norepinephrine were increased in the model group compared to control group. Psychological stress reduced brain and intestinal levels of tight junction proteins, including claudin5, occludin, α-actin, and ZO-1. Microbiota analysis revealed elevated microbial diversity and fecal proportions of Intestinimonas, Catenisphaera, and Globicatella in the model group. Further analysis indicated a negative correlation of Allisonella and Odoribacter, as well as a positive correlation of norank_f__Peptococcaceae, Clostridium_sensu_stricto_1, and Coprococcus_2, with claudin5, occludin, α-actin, and ZO-1. Our use of a rodent model to explore the association between compromised intestinal and blood–brain barriers and altered fecal microbiota under psychological stress improves our understanding of the gut–brain axis. Here, cues converge to control basic developmental processes in the intestine and brain such as barrier function. This study provides new directions for investigating the pathogenesis of emotional disorders and the formulation of clinical treatment.https://www.frontiersin.org/article/10.3389/fmicb.2019.03067/fullgut microbiotadysbiosispsychological stressintestinal barrierblood–brain barriertight junction