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Cited by 362Gastrointestinal motility and disordersMast cells and histamineInflammatory Bowel Disease

Chronic stress induces mast cell-dependent bacterial adherence and initiates mucosal inflammation in rat intestine

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Söderholm, Johan D., Yang, Ping–Chang, Ceponis, Peter, Vohra, Angeli, Riddell, Robert, Sherman, Philip M., Perdue, Mary H.·2002·Gastroenterology
DOI 10.1053/gast.2002.36019
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Abstract

Background & aims Chronic psychological stress is an important factor in relapses of intestinal disorders, but it remains unclear if stress can induce primary gut inflammation in a previously healthy host.Methods Mast cell-deficient (Ws/Ws) rats and wild-type control (+/+) rats were submitted to water avoidance stress or sham stress (1 h/day) for 10 consecutive days, as a model of ongoing life stress.Results Both rat groups had similar systemic responses to stress, as assessed by changes in weight, corticosterone levels, and defecation. In +/+ rats, chronic stress induced barrier dysfunction in the ileum and colon (increased macromolecular permeability and depletion of mucus) and ultrastructural changes in epithelial cells (enlarged mitochondria and presence of autophagosomes) associated with bacterial adhesion and penetration into enterocytes. Moreover, hyperplasia and activation of mast cells, infiltration of neutrophils and mononuclear cells, and increased myeloperoxidase (MPO) activity were documented in the mucosa. In intestine of Ws/Ws rats, epithelial function and morphology were unchanged by chronic stress, bacterial-epithelial cell interaction was not demonstrated, and there was no evidence of inflammatory cell infiltration.Conclusions These findings suggest that chronic psychological stress can be an initiating factor in intestinal inflammation by impairing mucosal defenses against luminal bacteria and highlight the importance of mast cells in this process.

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  • Animal models of chronic stress demonstrate altered intestinal physiology and gut microbiota composition, with an increased secretory state and permeability.

    “Animal models of chronic stress demonstrate altered intestinal physiology and GM composition, with an increased secretory state and permeability (352–355).”

    From Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis (2023) · cites this paper as [352]

  • In mast cell-deficient rats, intestinal epithelial function and morphology are not damaged, and there is no evidence of inflammatory cell infiltration, highlighting the regulatory role played by mast cells.

    “In contrast, the intestinal epithelial function and morphology are not damaged in mast cell-deficient rats, and there is no evidence of inflammatory cell infiltration, which highlights the regulatory role played by mast cells (32).”

    From Stress triggers flare of inflammatory bowel disease in children and adults (2019) · cites this paper as [32]

  • In wild-type rats, chronic stress can induce intestinal barrier dysfunction, inflammatory cell infiltration, ultrastructural changes in epithelial cells, and mast cell proliferation and activation.

    “In wild-type rats, chronic stress can induce intestinal barrier dysfunction, inflammatory cell infiltration, ultrastructural changes in epithelial cells, and mast cell proliferation and activation.”

    From Stress triggers flare of inflammatory bowel disease in children and adults (2019) · cites this paper as [32]

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Research works printed but not linked: 1

  1. Pothoulakis C, Lamont JT. Microbes and microbial toxins: para- digms for microbial-mucosal interactions II. The integrated re- sponse of the intestine to Clostridium difficile toxins. Am J Physiol 2001;280:G178 -G183.

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Authors
Söderholm, J. D., Yang, P., Ceponis, P., Vohra, A., Riddell, R., Sherman, P. M., & Perdue, M. H.
Affiliations
  • McMaster University (CA)
  • University of Toronto (CA)
  • Mount Sinai Hospital (CA)
ORCID
Venue
Gastroenterology
Publisher
Elsevier BV
Published
2002-10
Volume
123
Issue
4
Pages
1099-1108
ISSN
0016-5085 (ISSN-L)
DOI
10.1053/gast.2002.36019
OpenAlex
W2084407626
Cited by
362
References
50
Citations by year
2026: 6 · 2025: 4 · 2024: 8 · 2023: 18 · 2022: 16 · 2021: 13 · 2020: 13 · 2019: 18 · 2018: 14 · 2017: 12 · 2016: 14 · 2015: 10 · 2014: 19 · 2013: 15 · 2012: 15
FWCI
12.31
Type
journal article
Language
en
Open access
Licence
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations
  • Gastroenterology (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • AstraZeneca
  • Canadian Association of Gastroenterology
  • Medical Research Council
Topics
  • Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
  • Life Sciences › Immunology and Microbiology › Immunology › Mast cells and histamine
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Inflammatory Bowel Disease
Keywords
chronic psychological stress, mast cells, bacterial adhesion, intestinal inflammation, mucosal barrier dysfunction, epithelial permeability, water avoidance stress, myeloperoxidase, neutrophil infiltration, autophagy, enterocyte ultrastructure, gut microbiota
MeSH terms
Animals, Bacterial Adhesion, Chronic Disease, Enteritis, Female, Intestinal Mucosa, Male, Mast Cells, Microscopy, Electron, Rats, Mutant Strains, Stress, Psychological, Goblet Cells, Enterocytes, Rats

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