Modulation of the Intestinal Microbiota Alters Colitis-Associated Colorectal Cancer Susceptibility
Open accessAbstract
It is well established that the intestinal microbiota plays a key role in the pathogenesis of Crohn's disease (CD) and ulcerative colitis (UC) collectively referred to as inflammatory bowel disease (IBD). Epidemiological studies have provided strong evidence that IBD patients bear increased risk for the development of colorectal cancer (CRC). However, the impact of the microbiota on the development of colitis-associated cancer (CAC) remains largely unknown. In this study, we established a new model of CAC using azoxymethane (AOM)-exposed, conventionalized-Il10(-/-) mice and have explored the contribution of the host intestinal microbiota and MyD88 signaling to the development of CAC. We show that 8/13 (62%) of AOM-Il10(-/-) mice developed colon tumors compared to only 3/15 (20%) of AOM- wild-type (WT) mice. Conventionalized AOM-Il10(-/-) mice developed spontaneous colitis and colorectal carcinomas while AOM-WT mice were colitis-free and developed only rare adenomas. Importantly, tumor multiplicity directly correlated with the presence of colitis. Il10(-/-) mice mono-associated with the mildly colitogenic bacterium Bacteroides vulgatus displayed significantly reduced colitis and colorectal tumor multiplicity compared to Il10(-/-) mice. Germ-free AOM-treated Il10(-/-) mice showed normal colon histology and were devoid of tumors. Il10(-/-); Myd88(-/-) mice treated with AOM displayed reduced expression of Il12p40 and Tnfalpha mRNA and showed no signs of tumor development. We present the first direct demonstration that manipulation of the intestinal microbiota alters the development of CAC. The TLR/MyD88 pathway is essential for microbiota-induced development of CAC. Unlike findings obtained using the AOM/DSS model, we demonstrate that the severity of chronic colitis directly correlates to colorectal tumor development and that bacterial-induced inflammation drives progression from adenoma to invasive carcinoma.
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Several changes in microbiota composition are described in CRC: increased diversity in Clostridium leptum and Clostridium coccoides, while temporary instability and decreased complexity in composition are linked to colitis-associated CRC.
“An increased diversity in Clostridium leptum (C.leptum) and Clostridium coccoides is present, while temporary instability and decreased complexity in composition are linked to colitis-associated CRC [48,49] .”
From Intestinal microbiota in health and disease: Role of bifidobacteria in gut homeostasis (2014) · cites this paper as [49]
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- Authors
- Uronis, J. M., Mühlbauer, M., Herfarth, H. H., Rubinas, T. C., Jones, G. S., & Jobin, C.
- Affiliations
- University of North Carolina at Chapel Hill (US)
- Corresponding author
- Jobin, Christian
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2009-06-24
- Volume
- 4
- Issue
- 6
- Pages
- e6026
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC2696084
- OpenAlex
- W2008631743
- Cited by
- 425
- References
- 33
- Citations by year
- 2026: 3 · 2025: 6 · 2024: 15 · 2023: 19 · 2022: 23 · 2021: 28 · 2020: 27 · 2019: 27 · 2018: 33 · 2017: 30 · 2016: 30 · 2015: 25 · 2014: 28 · 2013: 43 · 2012: 36
- FWCI
- 11.80
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS ONE (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Carolina Digital Repository (University of North Carolina at Chapel Hill) (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- UNC Libraries
- Funders
- National Institutes of Health (NIH 5 T32, DK034987, DK 47700)
- University of North Carolina at Chapel Hill (DK034987, P30 DK034987)
- National Institute of Diabetes and Digestive and Kidney Diseases (R01 DK47700, R01 DK73338, R01DK047700, R01DK073338, P30DK034987, T32DK007737)
- National Center for Research Resources (P40RR018603)
- Center for Gastrointestinal Biology and Disease, School of Medicine, University of North Carolina at Chapel Hill (P30 DK 034987, NIH P30 DK034987)
- 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 › Epidemiology › Microscopic Colitis
- Keywords
- colitis-associated colorectal cancer, gut microbiota, MyD88 signaling, Toll-like receptor signaling, IL-10 knockout mice, azoxymethane, Bacteroides vulgatus, germ-free mice, inflammatory bowel disease, colitis, tumor multiplicity, adenoma-to-carcinoma progression, TNF-α
- MeSH terms
- Animals, Colitis, Immunohistochemistry, Inflammation, Intestines, Mice, Inbred C57BL, Mice, Transgenic, Time Factors, Colorectal Neoplasms, NF-kappa B, Disease Progression, Transgenes, Genetic Predisposition to Disease, Mice, Myeloid Differentiation Factor 88
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