Akkermansia muciniphila Protects Against Psychological Disorder-Induced Gut Microbiota-Mediated Colonic Mucosal Barrier Damage and Aggravation of Colitis

Psychological disorders are associated with increased risk of severe inflammatory bowel disease (IBD) by causing gut microbiota dysbiosis and colonic mucosal barrier damage. However, the interaction between chronic restraint stress (CRS), gut microbiota composition, and colonic mucus remains unclear...

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Main Authors: Tuo Chen, Rong Wang, Zhenglan Duan, Xiaomin Yuan, Yang Ding, Zeyu Feng, Fan Bu, Li Liu, Qiong Wang, Jinyong Zhou, Lei Zhu, Qing Ni, Guoping Shi, Yugen Chen
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-10-01
Series:Frontiers in Cellular and Infection Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fcimb.2021.723856/full
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author Tuo Chen
Rong Wang
Zhenglan Duan
Xiaomin Yuan
Yang Ding
Zeyu Feng
Fan Bu
Li Liu
Qiong Wang
Jinyong Zhou
Lei Zhu
Qing Ni
Guoping Shi
Yugen Chen
author_facet Tuo Chen
Rong Wang
Zhenglan Duan
Xiaomin Yuan
Yang Ding
Zeyu Feng
Fan Bu
Li Liu
Qiong Wang
Jinyong Zhou
Lei Zhu
Qing Ni
Guoping Shi
Yugen Chen
author_sort Tuo Chen
collection DOAJ
description Psychological disorders are associated with increased risk of severe inflammatory bowel disease (IBD) by causing gut microbiota dysbiosis and colonic mucosal barrier damage. However, the interaction between chronic restraint stress (CRS), gut microbiota composition, and colonic mucus remains unclear. We demonstrated that mice under CRS conditions exhibited alterations in microbiota composition, disruption of colonic mucus, and aggravation of colitis. In addition, the abundance of Akkermansia muciniphila was significantly decreased in mice under CRS and UC patients with depression, and positively associated with the expression of MUC2. After antibiotic treatment, the recipient mice colonized with CRS microbiota showed barrier defects and severe colitis. Administration of Akkermansia muciniphila was found to restore colonic mucus and modify the gut microbiota. We confirm that CRS-mediated gut microbiota dysbiosis results in colonic mucosal barrier damage and aggravation of colitis. Our results suggest that A. muciniphila is expected to be a potential probiotic to protect and treat colonic mucus that is involved in IBD with psychological disorders.
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spelling doaj.art-53b4a8cb71c44c60b855ef5520abfb322022-12-21T18:22:36ZengFrontiers Media S.A.Frontiers in Cellular and Infection Microbiology2235-29882021-10-011110.3389/fcimb.2021.723856723856Akkermansia muciniphila Protects Against Psychological Disorder-Induced Gut Microbiota-Mediated Colonic Mucosal Barrier Damage and Aggravation of ColitisTuo Chen0Rong Wang1Zhenglan Duan2Xiaomin Yuan3Yang Ding4Zeyu Feng5Fan Bu6Li Liu7Qiong Wang8Jinyong Zhou9Lei Zhu10Qing Ni11Guoping Shi12Yugen Chen13Department of General Surgery, Affiliated Hospital of Yangzhou University, Yangzhou, ChinaDepartment of Colorectal Surgery, Affiliated Hospital of Nanjing University of Chinese Medicine, Nanjing, ChinaDepartment of Colorectal Surgery, Affiliated Hospital of Nanjing University of Chinese Medicine, Nanjing, ChinaDepartment of Colorectal Surgery, Affiliated Hospital of Nanjing University of Chinese Medicine, Nanjing, ChinaDepartment of Colorectal Surgery, Affiliated Hospital of Nanjing University of Chinese Medicine, Nanjing, ChinaDepartment of Colorectal Surgery, Affiliated Hospital of Nanjing University of Chinese Medicine, Nanjing, ChinaDepartment of Colorectal Surgery, Affiliated Hospital of Nanjing University of Chinese Medicine, Nanjing, China Glycomics and Glycan Bioengineering Research Center, College of Food Science and Technology, Nanjing Agricultural University, Nanjing, ChinaBasic Pharmacology Laboratory, Affiliated Hospital of Nanjing University of Chinese Medicine, Nanjing, ChinaCentral Laboratory, Affiliated Hospital of Nanjing University of Chinese Medicine, Nanjing, ChinaCollaborative Innovation Center for Cancer Medicine, Affiliated Hospital of Nanjing University of Chinese Medicine, Nanjing, ChinaDepartment of General Surgery, Affiliated Hospital of Yangzhou University, Yangzhou, ChinaCollaborative Innovation Center for Cancer Medicine, Affiliated Hospital of Nanjing University of Chinese Medicine, Nanjing, ChinaDepartment of Colorectal Surgery, Affiliated Hospital of Nanjing University of Chinese Medicine, Nanjing, ChinaPsychological disorders are associated with increased risk of severe inflammatory bowel disease (IBD) by causing gut microbiota dysbiosis and colonic mucosal barrier damage. However, the interaction between chronic restraint stress (CRS), gut microbiota composition, and colonic mucus remains unclear. We demonstrated that mice under CRS conditions exhibited alterations in microbiota composition, disruption of colonic mucus, and aggravation of colitis. In addition, the abundance of Akkermansia muciniphila was significantly decreased in mice under CRS and UC patients with depression, and positively associated with the expression of MUC2. After antibiotic treatment, the recipient mice colonized with CRS microbiota showed barrier defects and severe colitis. Administration of Akkermansia muciniphila was found to restore colonic mucus and modify the gut microbiota. We confirm that CRS-mediated gut microbiota dysbiosis results in colonic mucosal barrier damage and aggravation of colitis. Our results suggest that A. muciniphila is expected to be a potential probiotic to protect and treat colonic mucus that is involved in IBD with psychological disorders.https://www.frontiersin.org/articles/10.3389/fcimb.2021.723856/fullchronic restraint stresscolitiscolonic mucusfecal microbiota transplantationAkkermansia muciniphila
spellingShingle Tuo Chen
Rong Wang
Zhenglan Duan
Xiaomin Yuan
Yang Ding
Zeyu Feng
Fan Bu
Li Liu
Qiong Wang
Jinyong Zhou
Lei Zhu
Qing Ni
Guoping Shi
Yugen Chen
Akkermansia muciniphila Protects Against Psychological Disorder-Induced Gut Microbiota-Mediated Colonic Mucosal Barrier Damage and Aggravation of Colitis
Frontiers in Cellular and Infection Microbiology
chronic restraint stress
colitis
colonic mucus
fecal microbiota transplantation
Akkermansia muciniphila
title Akkermansia muciniphila Protects Against Psychological Disorder-Induced Gut Microbiota-Mediated Colonic Mucosal Barrier Damage and Aggravation of Colitis
title_full Akkermansia muciniphila Protects Against Psychological Disorder-Induced Gut Microbiota-Mediated Colonic Mucosal Barrier Damage and Aggravation of Colitis
title_fullStr Akkermansia muciniphila Protects Against Psychological Disorder-Induced Gut Microbiota-Mediated Colonic Mucosal Barrier Damage and Aggravation of Colitis
title_full_unstemmed Akkermansia muciniphila Protects Against Psychological Disorder-Induced Gut Microbiota-Mediated Colonic Mucosal Barrier Damage and Aggravation of Colitis
title_short Akkermansia muciniphila Protects Against Psychological Disorder-Induced Gut Microbiota-Mediated Colonic Mucosal Barrier Damage and Aggravation of Colitis
title_sort akkermansia muciniphila protects against psychological disorder induced gut microbiota mediated colonic mucosal barrier damage and aggravation of colitis
topic chronic restraint stress
colitis
colonic mucus
fecal microbiota transplantation
Akkermansia muciniphila
url https://www.frontiersin.org/articles/10.3389/fcimb.2021.723856/full
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