Microbial genomic analysis reveals the essential role of inflammation in bacteria-induced colorectal cancer
Open accessAbstract
Enterobacteria, especially Escherichia coli, are abundant in patients with inflammatory bowel disease or colorectal cancer (CRC). However, it is unclear whether cancer is promoted by inflammation-induced expansion of E. coli and/or changes in expression of specific microbial genes. Here we use longitudinal (2, 12 and 20 weeks) 16S rRNA sequencing of luminal microbiota from ex-germ-free mice to show that inflamed Il10(-/-) mice maintain a higher abundance of Enterobacteriaceae than healthy wild-type mice. Experiments with mono-colonized Il10(-/-) mice reveal that host inflammation is necessary for E. coli cancer-promoting activity. RNA-sequence analysis indicates significant changes in E. coli gene catalogue in Il10(-/-) mice, with changes mostly driven by adaptation to the intestinal environment. Expression of specific genes present in the tumour-promoting E. coli pks island are modulated by inflammation/CRC development. Thus, progression of inflammation in Il10(-/-) mice supports Enterobacteriaceae and alters a small subset of microbial genes important for tumour development.
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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 [126]
The Results (‘E. coli requires inflammation to promote AOM-initiated CRC’; page unavailable) report greater tumor burden in two inflamed mouse groups colonized with E. coli NC101 than in the non-inflamed group. The Discussion identifies NC101’s pks island as linked to colibactin and cancer promotion, but says that whether other pks-bearing strains behave similarly requires further experiments. This paper therefore supports a cancer-promoting effect in these mouse models, not the claim about multiple other E. coli strains. (LLM, conf=0.85)
Experimental — accuracy not yet measuredpks-positive E. coli strains have been detected in approximately 20% of healthy individuals, 40% of patients with inflammatory bowel disease, and 60% of patients with CRC.
“These pks-positive E. coli strains have been detected in approximately 20% of healthy individuals, 40% of patients with inflammatory bowel disease, and 60% of patients with CRC”
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 [126]
The Introduction (page unavailable) reports a high abundance of pks-encoding E. coli in patients with IBD and CRC. It does not give the claimed 20%, 40%, and 60% detection rates or a rate for healthy individuals; searches for those percentages and for prevalence in healthy controls found no such passage. (LLM, conf=0.86)
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- Authors
- Arthur, J. C., Gharaibeh, R. Z., Mühlbauer, M., Perez-Chanona, E., Uronis, J. M., McCafferty, J., Fodor, A. A., & Jobin, C.
- Affiliations
- University of North Carolina at Chapel Hill (US)
- University of North Carolina at Charlotte (US)
- University of Florida Health (US)
- Corresponding author
- Fodor, Anthony A.
- Jobin, Christian
- ORCID
- Venue
- Nature Communications
- Published
- 2014-09-03
- Volume
- 5
- Issue
- 1
- Pages
- 4724-4724
- ISSN
- 2041-1723 (ISSN-L)
- PMC
- PMC4155410
- OpenAlex
- W2011411661
- Cited by
- 392
- References
- 66
- Citations by year
- 2026: 18 · 2025: 38 · 2024: 28 · 2023: 34 · 2022: 45 · 2021: 39 · 2020: 43 · 2019: 36 · 2018: 36 · 2017: 29 · 2016: 20 · 2015: 22 · 2014: 4
- FWCI
- 10.24
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Nature Communications (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Carolina Digital Repository (University of North Carolina at Chapel Hill) (submittedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- UNC Libraries
- Funders
- National Institutes of Health (NIH-R01, DK034987, P40OD010995)
- University of North Carolina at Charlotte
- National Cancer Institute (P30CA016086)
- National Institute of Diabetes and Digestive and Kidney Diseases (R01 DK47700, R01 DK73338, R01DK047700, R01DK073338, R01DK053347, P30DK034987)
- Center for Gastrointestinal Biology and Disease, School of Medicine, University of North Carolina at Chapel Hill (P30 DK 034987)
- Topics
- 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
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biotechnology › Cancer Research and Treatments
- Keywords
- colorectal cancer, intestinal inflammation, Escherichia coli, Enterobacteriaceae, IL-10 knockout mice, germ-free mice, microbial gene expression, pks island, inflammatory bowel disease, host-microbe interactions
- MeSH terms
- Animals, Escherichia coli, Escherichia coli Infections, Female, Genes, Bacterial, Inflammation, Male, RNA, Ribosomal, 16S, Colorectal Neoplasms, Gene Expression, Genome, Bacterial, Interleukin-10, Mice, Knockout, Genomic Islands, Mice, Host-Pathogen Interactions, Microbiota
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