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The bacterial genotoxin colibactin promotes colon tumor growth by modifying the tumor microenvironment
Open accessAbstract
The gut microbiota is suspected to promote colorectal cancer (CRC). Escherichia coli are more frequently found in CCR biopsies than in healthy mucosa; furthermore, the majority of mucosa-associated E. coli isolated from CCR harbors the pks genomic island (pks+ E. coli) that is responsible for the synthesis of colibactin, a genotoxic compound. We have recently reported that transient contact of a few malignant cells with colibactin-producing E. coli increases tumor growth in a xenograft mouse model. Growth is sustained by cellular senescence that is accompanied by the production of growth factors. We demonstrated that cellular senescence is a consequence of the pks+ E. coli-induced alteration of p53 SUMOylation, an essential post-translational modification in eukaryotic cells. The underlying mechanisms for this process involve the induction of miR-20a-5p expression, which targets SENP1, a key protein in the regulation of the SUMOylation process. These results are consistent with the expression of SENP1, miR-20a-5p and growth factors that are observed in a CRC mouse model and in human CCR biopsies colonized by pks+ E. coli. Overall, the data reveal a new paradigm for carcinogenesis in which pks+ E. coli infection induces cellular senescence characterized by the production of growth factors that promote the proliferation of uninfected cells and, subsequently, tumor growth.
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TL;DR
Colibactin-producing *E. coli* (pks+ *E. coli*) induce cellular senescence in intestinal epithelial cells via a c-Myc/miR-20a-5p/SENP1 axis that increases SUMO-conjugated p53, and the resulting senescence-associated secretory phenotype (notably HGF) promotes proliferation of uninfected cells and tumor growth. The authors propose that pks+ *E. coli* modify the tumor microenvironment to favor colon tumor promotion.
Key findings
- Transient infection of HCT116 xenografts in nude mice at low MOI (20) increased tumor growth and Ki67-positive cells, whereas high MOI (100) decreased tumor growth, consistent with tumor dormancy from massive cell-cycle arrest (n = 5/group; *P* < 0.05).
- Conditioned medium from pks+ *E. coli*-infected cells increased proliferation of uninfected cells to a degree similar to medium with 10% fetal bovine serum; this was reproduced across Int-407, HCT8, Caco-2, HT-29, HCT116 and non-transformed IEC-6 cells.
- pks+ *E. coli* induced senescence (SA-β-gal, phospho-p53, p21^Cip, Rb accumulation, decreased E2F-1) with increased HGF, FGF and GM-CSF; tumors at day 10 post-implantation showed an ~3-fold increase in the percentage of senescent cells versus pks− controls.
- An HGF pathway inhibitor (and neutralizing antibodies) abrogated the pro-proliferative activity of conditioned medium and significantly blocked xenograft growth; mechanistically, pks+ *E. coli* induced c-Myc, which drove miR-20a-5p, which bound the SENP1 3′-UTR and reduced SENP1, increasing SUMO1-conjugated p53.
- In the AOM/DSS model, colonization with a clinical pks+ *E. coli* strain significantly increased colon tumor number versus the isogenic pks mutant, without affecting inflammatory score or tumor size; γH2Ax, miR-20a-5p, SA-β-gal, p21^Cip and HGF pathway activation were increased. Human colon adenocarcinoma biopsies colonized by pks+ *E. coli* showed the same signature (high γH2Ax, miR-20a-5p, senescence markers, HGF mRNA and activated HGF receptors; decreased SENP1-expressing cells), differentiating them from pks−-colonized tumors by redundancy analyses.
Methods
- Xenograft model: HCT116 cells (2 × 10⁶) subcutaneously injected into nude mice and infected for 3 hours with pks+ *E. coli* or isogenic pks− *E. coli* at MOI 20 or 100; tumor size monitored over time.
- In vitro assays: conditioned medium transfer to measure proliferation of uninfected cells across multiple intestinal epithelial lines; SA-β-gal, senescence protein profiles, growth factor expression, SUMOylation patterns, miR-20a-5p/SENP1 reporter and transfection experiments, and inhibitor/neutralizing antibody treatments.
- In vivo validation: AOM/DSS (azoxymethane/dextran sodium sulfate) CRC mouse model colonized with a clinical pks+ *E. coli* strain versus its isogenic pks mutant, plus analysis of human colon adenocarcinoma biopsies colonized by pks+ versus pks− *E. coli* (including redundancy analyses).
Limitations
- Stated: pks+ *E. coli*-induced senescence was also observed in p53−/− cells, suggesting pathways other than p53 signaling may be involved.
- Stated: no increase in tumor size was observed with pks+ *E. coli* in the AOM/DSS model in immunocompetent mice, possibly because senescent tumors generate an immune response that constrains expansion; the authors note the promoting effect on intestinal tumor size may be difficult to observe.
- Stated: the study focused on colibactin as the sole toxin affecting the cell cycle, but clinical pks+ *E. coli* frequently also produce CNF1, whose impact on CRC remains to be explored; overall understanding of the cancer-promoting potential of pks+ *E. coli* remains limited and clinical consequences need clarification.
- Evident from the text: several supporting results are described as "unpublished data" (e.g., high-MOI growth decrease, SUMOylation patterns, anacardic acid and SENP1 overexpression effects), and the role of the dormancy-type interaction in intestinal tumors "remains to be assessed."
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“In addition, using a reporter assay, we demonstrated that miR-20a-5p binds to the SENP1 mRNA 3'-UTR.”
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In the paper
“pksC E. coli-infected cells displayed a modified pattern of SUMO-conjugated proteins compared with pks-E.coliinfected cells or uninfected cells (unpublished data).”
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In the paper
“pksC E. coli, in contrast to pks-E.coli, induced a time- dependent and dose-dependent increase in SA-b-gal activity.”
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In the paper
“Of note, the expression levels of FGF, GM-CSF and HGF were also increased in xenografts at 10 d post-pksC E. coli infection compared to xenografts infected with pks-E.coli.”
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes- Rests on an assumption: The subcutaneous xenograft model in immunodeficient mice is a valid model for the effect of pksC E. coli on human colon tumor growth.
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In the paper
“Interestingly, pksC E. coli-infected cells expressed significantly higher levels of the growth factors HGF, FGF, and GM-CSF than pks-E.coli-infected cells.”
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In the paper
“Furthermore, transfection of cells with mature miR-20a-5p decreased SENP1 expression at both the mRNA and protein levels.”
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In the paper
“Interestingly, over-expression of SENP1, unlike overexpression of an inactive SENP1, significantly decreased the number of senescent cells induced by pksC E. coli infection, confirming the role of SENP1 in pksC E. coli-induced senescence.”
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In the paper
“In this model, a single and transient exposure of xenografts to pksC E. coli at a multiplicity of infection (MOI) of 20 was associated with an increase in tumor growth and Ki67positive cell numbers, suggesting that pksC E. coli enhance cell proliferation (Fig. 1A).”
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes- Rests on an assumption: The subcutaneous xenograft model in immunodeficient mice is a valid model for the effect of pksC E. coli on human colon tumor growth.
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In the paper
“An HGF pathway inhibitor, in contrast to vehicle or other growth factor inhibitors abrogated the pro-proliferative activity of CM in vitro.”
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In the paper
“Furthermore, an anti-miR-20a-5p abrogated pksC E. coli-induced accumulation of SUMO1-conjugated p53 and, consequently, cellular senescence.”
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In the paper
“pksC E. coli did not affect the inflammatory score or the size of the tumors.”
Strength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passesIt may state two separate claims as one.
- Rests on an assumption: The AOM/DSS mouse model is a valid model for human colorectal cancer promotion by pksC E. coli.
In the paper
“pksC E. coli-infected cells exhibited an accumulation of phospho-p53, p21 Cip , and Retinoblastoma protein as well as a decrease in E2F-1 expression at day 5 post-infection, which correspond to a protein expression profile characteristic of senescent cells.12”
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- Not checked yetcites [12] source
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“As observed upon pksC E. coli infection, cells transfected with miR-20a-5p produced significant levels of HGF, and their CM induced the proliferation of untransfected cells.”
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In the paper
“Accordingly, we observed an accumulation of SUMO1-conjugated p53, which is known to drive cellular senescence.17 This accumulation was associated with a decrease in SENP1 expression, a key enzyme involved in the control of the SUMOylation process.17”
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- Not checked yetcites [17] source
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In the paper
“Accordingly, we observed that pksC E. coli infection, which is known to induce DNA damage, 9,10 induced c-Myc expression and its binding to the miR-20a-5p promoter.”
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“Finally, time-course experiments showed that pksC E. coli induced c-Myc expression 3 d after infection, followed by modifications of miR-20a-5p and SENP1 expression levels 2 d later.”
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“Transfection of pksC E. coli-infected cells with c-Myc siRNA strongly reduced the expression of miR20a-5p, increased the expression of SENP1, reduced the level of SUMO-conjugated p53, decreased the number of pksC E. coli-induced senescent cells and consequently abolished the pro-proliferative effect of the CM derived from those cells.”
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In the paper
“The DNA damage marker gH2Ax, the miR-20a-5p expression level and senescence markers (SA-b-gal activity and p21 cip expression) were significantly increased in tumors isolated from mice colonized by the clinical pksC E. coli strain compared with those isolated from mice colonized by the corresponding isogenic mutant.”
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- Rests on an assumption: The AOM/DSS mouse model is a valid model for human colorectal cancer promotion by pksC E. coli.
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In the paper
“As observed in the AOM/DSS mouse model, human biopsies colonized by pksC E. coli harbored high expression levels of gH2Ax, miR-20a-5p, senescence markers (SA-b-gal, p21 cip ), and HGF mRNA and activated HGF receptors, as well as a decrease in the number of SENP1-expressing cells.”
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In the paper
“pksC E. coli activate the miR-20a-5p/SENP1/senescence/HGF pathway (Fig. 1B) in human and murine colon adenocarcinomas and therefore may contribute to CCR development.”
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In the paper
“Our findings suggest that colibactin-producing E. coli modulate the tumor microenvironment by inducing the secretion of several growth factors from senescent cells, which can promote tumor growth.”
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
- Rests on an assumption: The subcutaneous xenograft model in immunodeficient mice is a valid model for the effect of pksC E. coli on human colon tumor growth.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Consequently, colibactinproducing bacteria can modulate the tumor microenvironment to favor the emergence of senescent cells, which may also affects tumor promotion and cancer progression via the secretion of growth factors.”
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The paper relies on this without support.
The pks genomic island is responsible for the synthesis of colibactin, a genotoxic compound.
“the majority of mucosa-associated E. coli isolated from CCR harbors the pks genomic island (pksC E. coli) that is responsible for the synthesis of colibactin, a genotoxic compound.”
The paper relies on this without support.
The subcutaneous xenograft model in immunodeficient mice is a valid model for the effect of pksC E. coli on human colon tumor growth.
“The promotion of tumor growth was clearly observed in the subcutaneous xenograft model using immunodeficient mice.”
The paper relies on this without support.
The AOM/DSS mouse model is a valid model for human colorectal cancer promotion by pksC E. coli.
“To confirm the reliability of our findings, we explored the impact of a clinical pksC E. coli strain in an AOM/DSS (azoxymethane/dextran sodium sulfate) CRC mouse model.”
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In the citing paper
“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 [129]
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Metadata
- Authors
- Dalmasso, G., Cougnoux, A., Delmas, J., Darfeuille-Michaud, A., & Bonnet, R.
- Affiliations
- Inserm (FR)
- Corresponding author
- Bonnet, Richard
- Venue
- Gut Microbes
- Publisher
- Informa UK Limited
- Published
- 2014-09-03
- Volume
- 5
- Issue
- 5
- Pages
- 675-680
- ISSN
- 1949-0976 (ISSN-L)
- 1949-0984
- PMC
- PMC4615906
- OpenAlex
- W1964485249
- Semantic Scholar
- 10b0e7d77ac0c96917fb9e7be28852f987ee6021
- Cited by
- 296
- References
- 30
- Citations by year
- 2026: 22 · 2025: 32 · 2024: 27 · 2023: 31 · 2022: 35 · 2021: 39 · 2020: 35 · 2019: 24 · 2018: 18 · 2017: 16 · 2016: 11 · 2015: 5
- FWCI
- 7.51
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Gut Microbes (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion, other-oa)
- Funders
- Institut National de la Santé et de la Recherche Médicale (USC-2018, U1071)
- Ligue Contre le Cancer
- Centre National de la Recherche Scientifique
- Institut National de la Recherche Agronomique (U1071, USC-2018)
- Centre Hospitalier Universitaire de Clermont-Ferrand
- Topics
- Life Sciences › Immunology and Microbiology › Microbiology › Escherichia coli research studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biotechnology › Bacterial Cancer Therapy
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Keywords
- colibactin, Escherichia coli, colorectal cancer, tumor microenvironment, cellular senescence, SENP1, miR-20a-5p, growth factors, gut microbiota, carcinogenesis, xenograft mouse model
- MeSH terms
- Animals, Colonic Neoplasms, Cysteine Endopeptidases, Escherichia coli, Models, Biological, Mutagens, Endopeptidases, Peptides, Tumor Suppressor Protein p53, MicroRNAs, Mice, Sumoylation, Tumor Microenvironment, Polyketides
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