A human colonic commensal promotes colon tumorigenesis via activation of T helper type 17 T cell responses
Open accessAbstract
The intestinal flora may promote colon tumor formation. Here we explore immunologic mechanisms of colonic carcinogenesis by a human colonic bacterium, enterotoxigenic Bacteroides fragilis (ETBF). ETBF that secretes B. fragilis toxin (BFT) causes human inflammatory diarrhea but also asymptomatically colonizes a proportion of the human population. Our results indicate that whereas both ETBF and nontoxigenic B. fragilis (NTBF) chronically colonize mice, only ETBF triggers colitis and strongly induces colonic tumors in multiple intestinal neoplasia (Min) mice. ETBF induces robust, selective colonic signal transducer and activator of transcription-3 (Stat3) activation with colitis characterized by a selective T helper type 17 (T(H)17) response distributed between CD4+ T cell receptor-alphabeta (TCRalphabeta)+ and CD4-8-TCRgammadelta+ T cells. Antibody-mediated blockade of interleukin-17 (IL-17) as well as the receptor for IL-23, a key cytokine amplifying T(H)17 responses, inhibits ETBF-induced colitis, colonic hyperplasia and tumor formation. These results show a Stat3- and T(H)17-dependent pathway for inflammation-induced cancer by a common human commensal bacterium, providing new mechanistic insight into human colon carcinogenesis.
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Enterotoxigenic Bacteroides fragilis-derived toxin, which triggers colitis and induces colonic tumors in mice, activates the STAT3 and Th17 response.
“Indeed, a human colonic bacterium, enterotoxigenic Bacteroides fragilis (ETBF)-derived toxin, which triggers colitis and induces colonic tumors in mice, activates the STAT3 and Th17 response (326).”
From IL-6 in inflammation, autoimmunity and cancer (2021) · cites this paper as [326]
The Results report that ETBF colonization caused colitis and colonic tumors in Min mice and activated colonic Stat3 and TH17 responses. The Discussion suggests that ETBF’s toxin, BFT, has a central role, but the reported mouse findings concern colonization by the toxin-producing bacterium, not an isolated-toxin experiment; the claim attributes those effects more directly to the toxin than the paper establishes. (LLM, conf=0.86)
Experimental — accuracy not yet measuredBacteroides fragilis and Streptococcus bovis could be linked to the development of CRC by activating immune cells to release pro-mitogenic and proangiogenic cytokines, mostly Interleukin-17 (IL-17).
“In this regard, Bacteroides fragilis (B.fragilis) and Streptococcus bovis (S. bovis) could be linked to the development of CRC by activating immune cells to release pro-mitogenic and proangiogenic cytokines, mostly Interleukin-17 (IL-17) [46] .”
From Intestinal microbiota in health and disease: Role of bifidobacteria in gut homeostasis (2014) · cites this paper as [46]
A small number of specific pathobionts have now been linked with adenomas and colorectal cancer, including Streptococcus gallolyticus, Enterococcus faecalis and B. fragilis.
“a small number of specific pathobionts have now been linked with adenomas and CRC including Streptococcus gallolyticus,94 Enterococcus faecalis95 and B. fragilis.84”
From The gut microbiota and host health: a new clinical frontier (2016) · cites this paper as [84]
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- Authors
- Wu, S., Rhee, K.-J., Albesiano, E., Rabizadeh, S., Wu, X., Yen, H.-R., Huso, D. L., Brancati, F. L., Wick, E., McAllister, F., Housseau, F., Pardoll, D. M., & Sears, C. L.
- Affiliations
- Johns Hopkins University (US)
- Corresponding author
- Housseau, Franck
- Sears, Cynthia L
- ORCID
- Venue
- Nature Medicine
- Published
- 2009-08-23
- Volume
- 15
- Issue
- 9
- Pages
- 1016-1022
- ISSN
- 1078-8956 (ISSN-L)
- 1546-170X
- PMC
- PMC3034219
- OpenAlex
- W1987375206
- Cited by
- 1,812
- References
- 44
- Citations by year
- 2026: 123 · 2025: 105 · 2024: 106 · 2023: 134 · 2022: 152 · 2021: 151 · 2020: 127 · 2019: 114 · 2018: 116 · 2017: 92 · 2016: 93 · 2015: 92 · 2014: 98 · 2013: 94 · 2012: 67
- FWCI
- 28.69
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Medicine (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health (5r24dk064388-07)
- National Cancer Institute (P50CA062924, CA 62924)
- National Institute of General Medical Sciences (T32GM066691)
- National Institute of Allergy and Infectious Diseases (R01AI089830)
- National Institute of Diabetes and Digestive and Kidney Diseases (R24 DK64388, F32DK079509, R24DK-064388, R01DK045496, R01DK080817, R01 DK 45496)
- National Center for Research Resources (RR 00171, K26RR000171)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (5 T32 HD44355, T32HD044355)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Endocrinology › Escherichia coli research studies
- Keywords
- enterotoxigenic Bacteroides fragilis, colon carcinogenesis, STAT3 signaling, IL-17, IL-23, colitis-associated colorectal cancer, γδ T cells, Bacteroides fragilis toxin, ApcMin/+ mice
- MeSH terms
- Animals, Bacterial Toxins, Bacteroides fragilis, Bacteroides Infections, Colitis, Colon, Colonic Neoplasms, Enterotoxins, T-Lymphocytes, Helper-Inducer, Humans, Lymphocyte Activation, Metalloendopeptidases, Mice, Mutant Strains, Neutralization Tests, T-Lymphocyte Subsets, Mice, Knockout, Interleukin-17, STAT3 Transcription Factor, Mice
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