Cited by 486Escherichia coli research studiesBacterial Cancer TherapyGut microbiota and health

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Bacterial genotoxin colibactin promotes colon tumour growth by inducing a senescence-associated secretory phenotype

Cougnoux, Antony, Dalmasso, Guillaume, Martinez, Ruben, Buc, Emmanuel, Delmas, Julien, Gibold, Lucie, Sauvanet, Pierre, Darcha, Claude, Déchelotte, Pierre, Bonnet, Mathilde, Pezet, Denis, Wodrich, Harald, Darfeuille-Michaud, Arlette, Bonnet, Richard·2014·Gut

DOI 10.1136/gutjnl-2013-305257

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Abstract

Background: Escherichia coli strains harbouring the pks island ( pks + E. coli ) are often seen in human colorectal tumours and have a carcinogenic effect independent of inflammation in an AOM/IL-10 −/− (azoxymethane/interleukin) mouse model. Objective: To investigate the mechanism sustaining pks + E. coli -induced carcinogenesis. Method: Underlying cell processes were investigated in vitro and in vivo (xenograft model) using intestinal epithelial cells infected by pks + E. coli or by an isogenic mutant defective for pks ( pks − E. coli ). The results were supported by data obtained from an AOM/DSS (azoxymethane/dextran sodium sulphate) colon cancer mouse model and from human colon cancer biopsy specimens colonised by pks + E. coli or pks− E. coli . Results: Colibactin-producing E. coli enhanced tumour growth in both xenograft and AOM/DSS models. Growth was sustained by cellular senescence (a direct consequence of small ubiquitin-like modifier (SUMO)-conjugated p53 accumulation), which was accompanied by the production of hepatocyte growth factor (HGF). The underlying mechanisms involve microRNA-20a-5p, which targets SENP1, a key protein regulating p53 deSUMOylation. These results are consistent with the expression of SENP1, microRNA-20a-5p, HGF and phosphorylation of HGF receptor found in human and mouse colon cancers colonised by pks + E. coli . Conclusion: These data reveal a new paradigm for carcinogenesis, in which colibactin-induced senescence has an important role.

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Authors: Cougnoux, A., Dalmasso, G., Martinez, R., Buc, E., Delmas, J., Gibold, L., Sauvanet, P., Darcha, C., Déchelotte, P., Bonnet, M., Pezet, D., Wodrich, H., Darfeuille-Michaud, A., & Bonnet, R.
Affiliations: Inserm (FR)
Centre National de la Recherche Scientifique (FR)
Centre Hospitalier Universitaire de Clermont-Ferrand (FR)
Clermont Université, UMR 1071 Inserm/Université d'Auvergne, Clermont-Ferrand, France
Corresponding author: Bonnet, Richard
ORCID: Cougnoux, Antony
Dalmasso, Guillaume
Martinez, Ruben
Buc, Emmanuel
Delmas, Julien
Darcha, Claude
Bonnet, Mathilde
Pezet, Denis
Wodrich, Harald
Bonnet, Richard
Venue: Gut
Publisher: BMJ
Published: 2014-03-21
Volume: 63
Issue: 12
Pages: 1932-1942
ISSN: 0017-5749 (ISSN-L)
1468-3288
DOI: 10.1136/gutjnl-2013-305257
OpenAlex: W2111725588
Semantic Scholar: 15f9aae86af823cd6aad2d6681907d71cc828598
Cited by: 486
References: 44
Citations by year: 2026: 34 · 2025: 35 · 2024: 43 · 2023: 46 · 2022: 54 · 2021: 68 · 2020: 50 · 2019: 37 · 2018: 35 · 2017: 27 · 2016: 25 · 2015: 22 · 2014: 10
FWCI: 19.73
Type: journal article
Language: en
Open access: closed
Locations: Gut (publishedVersion)
PubMed (publishedVersion)
HAL (submittedVersion)
HighWire Press Open Archive (submittedVersion)
Funders: Institut National de la Santé et de la Recherche Médicale
Ligue Contre le Cancer
Institut National de la Recherche Agronomique
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, pks island, colorectal cancer, tumor growth, cellular senescence, senescence-associated secretory phenotype, hepatocyte growth factor, SENP1, SUMOylation, bacterial carcinogenesis, AOM/DSS model, xenograft models
MeSH terms: Animals, Colonic Neoplasms, Cysteine Endopeptidases, Escherichia coli, Humans, Mutagens, Mutation, Neoplasms, Experimental, Nuclear Proteins, Endopeptidases, Peptides, Cellular Senescence, Hepatocyte Growth Factor, Proto-Oncogene Proteins c-met, Mice, Polyketides, Carcinogenesis

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Bacterial genotoxin colibactin promotes colon tumour growth by inducing a senescence-associated secretory phenotype

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