Cited by 85Inflammatory Bowel DiseaseGut microbiota and healthEscherichia coli research studies

Chronic intestinal inflammation induces stress-response genes in commensal Escherichia coli

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Patwa, Laura G., Fan, Ting–Jia, Tchaptchet, Sandrine, Liu, Yang, Lussier, Yves A., Sartor, R. Balfour, Hansen, Jonathan J.·2011·Gastroenterology

Abstract

Background & aims Intestinal microbes induce homeostatic mucosal immune responses, but can also cause inappropriate immune activation in genetically susceptible hosts. Although immune responses to bacterial products have been studied extensively, little is known about how intestinal inflammation affects functions of commensal luminal microbes.Methods Microarrays and real-time polymerase chain reaction were used to profile transcriptional changes in luminal bacteria from wild-type and IL-10(-/-) mice monoassociated with a nonpathogenic, murine isolate of Escherichia coli (NC101, which causes colitis in gnotobiotic IL-10(-/-) mice). Colonic inflammation and innate and adaptive immune responses were measured in wild-type and IL-10(-/-) mice monoassociated with mutant NC101 that lack selected, up-regulated genes, and in IL-10(-/-) mice that were colonized with a combination of mutant and parental NC101. We measured intracellular survival of bacteria within primary macrophages from mice and resulting production of tumor necrosis factor.Results Bacteria from IL-10(-/-) mice with colitis had significant up-regulation of the stress-response regulon, including the small heat shock proteins IbpA and IbpB that protect E coli from oxidative stress, compared to healthy, wild-type controls. In IL-10(-/-) mice, expression of ibpAB reduced histologic signs of colon inflammation, secretion of interleukin-12/23p40 in colonic explant cultures, serologic reactivity to NC101 antigens, and secretion of interferon-gamma by stimulated mesenteric lymph node cells. Infection of primary macrophages by bacteria that express ibpAB was associated with decreased intracellular survival and reduced secretion of tumor necrosis factor.Conclusions Chronic intestinal inflammation causes functional alterations in gene expression in commensal gut bacterium (E coli NC101). Further studies of these expression patterns might identify therapeutic targets for patients with inflammatory bowel diseases.

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Crossref · 10.1053/j.gastro.2011.06.064

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  • In a mouse model of colitis monocolonized with commensal E. coli, microarray measurements found several enzymes in the galactonate utilization pathway, including galactonate dehydratase, among the most strongly down-regulated compared with wild-type mice.

    “There, microarray-based measurements found a number of enzymes in the galactonate utilization pathway, including galactonate dehydratase, to be among the most strongly down-regulated in comparison with wild-type mice.”

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Authors
Patwa, L. G., Fan, T., Tchaptchet, S., Liu, Y., Lussier, Y. A., Sartor, R. B., & Hansen, J. J.
Affiliations
  • University of North Carolina at Chapel Hill (US)
  • University of Chicago (US)
Corresponding author
Hansen, Jonathan J.
Venue
Gastroenterology
Publisher
Elsevier BV
Published
2011-11
Volume
141
Issue
5
Pages
1842-1851.e10
ISSN
0016-5085 (ISSN-L)
OpenAlex
W1970279206
Cited by
85
References
39
Citations by year
2025: 4 · 2024: 4 · 2023: 5 · 2022: 6 · 2021: 6 · 2020: 3 · 2019: 12 · 2018: 8 · 2017: 3 · 2016: 6 · 2015: 7 · 2014: 7 · 2013: 8 · 2012: 5
FWCI
4.19
Type
journal article
Language
en
Open access
Locations
  • Gastroenterology (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
Funders
NIH (P30DK34987)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Inflammatory Bowel Disease
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Endocrinology › Escherichia coli research studies
Keywords
chronic intestinal inflammation, commensal Escherichia coli, stress response genes, small heat shock proteins, IbpA, IbpB, oxidative stress, IL-10 knockout mice, colitis, inflammatory bowel disease, bacterial gene expression, macrophage survival, TNF-α, interferon-gamma, mucosal immunity
MeSH terms
Animals, Cell Line, Chronic Disease, Colitis, Disease Models, Animal, Escherichia coli, Heat-Shock Proteins, Stress, Physiological, Tumor Necrosis Factor-alpha, Gene Expression Regulation, Bacterial, Interleukin-10, Mice, Knockout, Escherichia coli Proteins, Mice

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