Cited by 35Gut microbiota and healthInflammatory Bowel DiseaseGastrointestinal motility and disorders

Chronic psychological stress disrupted the composition of the murine colonic microbiota and accelerated a murine model of inflammatory bowel disease

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Watanabe, Yohei, Arase, Sohei, Nagaoka, Noriko, Kawai, Mitsuhisa, Matsumoto, Satoshi·2016·PLoS ONE

Abstract

The effect of psychological stress on the gastrointestinal microbiota is widely recognized. Chronic psychological stress may be associated with increased disease activity in inflammatory bowel disease, but the relationships among psychological stress, the gastrointestinal microbiota, and the severity of colitis is not yet fully understood. Here, we examined the impact of 12-week repeated water-avoidance stress on the microbiota of two inbred strains of T cell receptor alpha chain gene knockout mouse (background, BALB/c and C57BL/6) by means of next-generation sequencing of bacterial 16S rRNA genes. In both mouse strains, knockout of the T cell receptor alpha chain gene caused a loss of gastrointestinal microbial diversity and stability. Chronic exposure to repeated water-avoidance stress markedly altered the composition of the colonic microbiota of C57BL/6 mice, but not of BALB/c mice. In C57BL/6 mice, the relative abundance of genus Clostridium, some members of which produce the toxin phospholipase C, was increased, which was weakly positively associated with colitis severity, suggesting that expansion of specific populations of indigenous pathogens may be involved in the exacerbation of colitis. However, we also found that colitis was not exacerbated in mice with a relatively diverse microbiota even if their colonic microbiota contained an expanded phospholipase C-producing Clostridium population. Exposure to chronic stress also altered the concentration of free immunoglobulin A in colonic contents, which may be related to both the loss of bacterial diversity in the colonic microbiota and the severity of the colitis exacerbation. Together, these results suggest that long-term exposure to psychological stress induces dysbiosis in the immunodeficient mouse in a strain-specific manner and also that alteration of microbial diversity, which may be related to an altered pattern of immunoglobulin secretion in the gastrointestinal tract, might play a crucial role in the development of chronic stress-induced colitis.

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  • Stress-induced flora disturbance has a vital impact on IBD by influencing host-microbiota crosstalk and regulating the neuro-immune-endocrine system.

    “It has been shown that stress-induced flora disturbance has a vital impact on IBD by influencing host-microbiota crosstalk and regulating the neuro-immune-endocrine system (49–51).”
  • Twelve weeks of WAS significantly increased the relative abundance of the Clostridium genus, which produces the toxin phospholipase C, in C57BL/6 mice.

    “Additionally, 12 weeks of WAS significantly increased the relative abundance of the Clostridium genus, which produces the toxin phospholipase C in C57BL/6 mice.”

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Authors
Watanabe, Y., Arase, S., Nagaoka, N., Kawai, M., & Matsumoto, S.
Affiliations
Yakult Central Institute (JP)
Corresponding author
Watanabe, Yohei
Venue
PLoS ONE
Published
2016-03-07
Volume
11
Issue
3
Pages
e0150559
ISSN
1932-6203 (ISSN-L)
OpenAlex
W2296541423
Cited by
35
References
49
Citations by year
2026: 3 · 2025: 3 · 2024: 5 · 2023: 1 · 2022: 4 · 2021: 2 · 2020: 1 · 2019: 6 · 2018: 1 · 2017: 7 · 2016: 2
FWCI
2.77
Type
journal article
Language
en
Open access
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
  • Figshare (submittedVersion, cc-by)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Inflammatory Bowel Disease
  • Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
Keywords
chronic psychological stress, colonic microbiota, inflammatory bowel disease, colitis, water avoidance stress, strain differences, microbial diversity, Clostridium, phospholipase C, immunoglobulin A, dysbiosis
MeSH terms
Animals, Avoidance Learning, Clostridium, Colon, Disease Models, Animal, Immunoglobulin A, Type C Phospholipases, Stress, Psychological, Inflammatory Bowel Diseases, Receptors, Antigen, T-Cell, alpha-beta, Mice, Gene Knockout Techniques, Microbiota

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