Locoregional Effects of Microbiota in a Preclinical Model of Colon Carcinogenesis
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Abstract
Inflammation and microbiota are critical components of intestinal tumorigenesis. To dissect how the microbiota contributes to tumor distribution, we generated germ-free (GF) ApcMin/+and ApcMin/+;Il10−/− mice and exposed them to specific-pathogen-free (SPF) or colorectal cancer-associated bacteria. We found that colon tumorigenesis significantly correlated with inflammation in SPF-housed ApcMin/+;Il10−/−, but not in ApcMin/+mice. In contrast, small intestinal neoplasia development significantly correlated with age in both ApcMin/+;Il10−/− and ApcMin/+ mice. GF ApcMin/+;Il10−/− mice conventionalized by an SPF microbiota had significantly more colon tumors compared with GF mice. Gnotobiotic studies revealed that while Fusobacterium nucleatum clinical isolates with FadA and Fap2 adhesins failed to induce inflammation and tumorigenesis, pks+Escherichia coli promoted tumorigenesis in the ApcMin/+;Il10−/− model in a colibactin-dependent manner, suggesting colibactin is a driver of carcinogenesis. Our results suggest a distinct etiology of cancers in different locations of the gut, where colon cancer is primarily driven by inflammation and the microbiome, while age is a driving force for small intestine cancer. Cancer Res; 77(10); 2620–32. ©2017 AACR.
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In several mouse models, other colibactin-producing E. coli have been observed to promote the development of colorectal cancer.
“in several mouse models, other colibactin-producing E. coli have been observed to promote the development of colorectal cancer [125–131]”
From Selection, Comparative Genomics, and Potential Probiotic Features of Escherichia coli 5C, a pks-Negative Strain Isolated from Healthy Infant Donor Feces (2026) · cites this paper as [127]
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- Authors
- Tomkovich, S., Yang, Y., Winglee, K., Gauthier, J., Mühlbauer, M., Sun, X., Mohamadzadeh, M., Liu, X., Martin, P., Wang, G. P., Oswald, E., Fodor, A. A., & Jobin, C.
- Affiliations
- University of North Carolina at Chapel Hill (US)
- University of Florida (US)
- University of North Carolina at Charlotte (US)
- 1Department of Medicine, University of Florida, Gainesville, Florida.
- 6IRSD, Université de Toulouse, INSERM, INRA, ENVT, UPS, Toulouse, France.
- University of Florida Health (US)
- Corresponding author
- Jobin, Christian
- ORCID
- Venue
- Cancer Research
- Published
- 2017-05-14
- Volume
- 77
- Issue
- 10
- Pages
- 2620-2632
- ISSN
- 0008-5472 (ISSN-L)
- 1538-7445
- PMC
- PMC5468752
- OpenAlex
- W2606691626
- Cited by
- 252
- References
- 49
- Citations by year
- 2026: 10 · 2025: 22 · 2024: 17 · 2023: 19 · 2022: 44 · 2021: 49 · 2020: 29 · 2019: 24 · 2018: 26 · 2017: 12
- FWCI
- 10.17
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- other-oa
- Locations
- Cancer Research (publishedVersion, other-oa)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- HAL (submittedVersion, cc-by-sa)
- Funders
- NIH (R01DK047700, R01DK073338, and R21 CA195226)
- CCFA (409472)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biotechnology › Cancer Research and Treatments
- Health Sciences › Medicine › Pathology and Forensic Medicine › Genetic factors in colorectal cancer
- Keywords
- gut microbiota, colon carcinogenesis, colorectal cancer, inflammation, ApcMin/+ mice, germ-free mice, Fusobacterium nucleatum, colibactin, Escherichia coli, tumor location, age-related cancer, carcinogenesis
- MeSH terms
- Gastrointestinal Microbiome, Animals, Bacteria, Cell Transformation, Neoplastic, Disease Models, Animal, Inflammation, Mice, Transgenic, Colorectal Neoplasms, Interleukin-10, Mice, Knockout, Adenomatous Polyposis Coli Protein, Mice
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