High Prevalence of Mucosa-Associated E. coli Producing Cyclomodulin and Genotoxin in Colon Cancer

Buc, Emmanuel; Dubois, Damien; Sauvanet, Pierre; Raisch, Jennifer; Delmas, Julien; Darfeuille-Michaud, Arlette; Pezet, Denis; Bonnet, Richard

doi:10.1371/journal.pone.0056964

Cited by 538Escherichia coli research studiesClostridium difficile and Clostridium perfringens researchBacterial Genetics and Biotechnology

High Prevalence of Mucosa-Associated E. coli Producing Cyclomodulin and Genotoxin in Colon Cancer

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Buc, Emmanuel, Dubois, Damien, Sauvanet, Pierre, Raisch, Jennifer, Delmas, Julien, Darfeuille-Michaud, Arlette, Pezet, Denis, Bonnet, Richard·2013·PLoS ONE

DOI 10.1371/journal.pone.0056964PMC PMC3572998

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Abstract

Some Escherichia coli strains produce toxins designated cyclomodulins (CMs) which interfere with the eukaryotic cell cycle of host cells, suggesting a possible link between these bacteria and cancers. There are relatively few data available concerning the colonization of colon tumors by cyclomodulin- and genotoxic-producing E. coli. We did a qualitative and phylogenetic analysis of mucosa-associated E. coli harboring cyclomodulin-encoding genes from 38 patients with colorectal cancer (CRC) and 31 with diverticulosis. The functionality of these genes was investigated on cell cultures and the genotoxic activity of strains devoid of known CM-encoding gene was investigated. Results showed a higher prevalence of B2 phylogroup E. coli harboring the colibatin-producing genes in biopsies of patients with CRC (55.3%) than in those of patients with diverticulosis (19.3%), (p<0.01). Likewise, a higher prevalence of B2 E. coli harboring the CNF1-encoding genes in biopsies of patients with CRC (39.5%) than in those of patients with diverticulosis (12.9%), (p = 0.01). Functional analysis revealed that the majority of these genes were functional. Analysis of the ability of E. coli to adhere to intestinal epithelial cells Int-407 indicated that highly adherent E. coli strains mostly belonged to A and D phylogroups, whatever the origin of the strains (CRC or diverticulosis), and that most E. coli strains belonging to B2 phylogroup displayed very low levels of adhesion. In addition, 27.6% (n = 21/76) E. coli strains devoid of known cyclomodulin-encoding genes induced DNA damage in vitro, as assessed by the comet assay. In contrast to cyclomodulin-producing E. coli, these strains mainly belonged to A or D E. coli phylogroups, and exhibited a non significant difference in the distribution of CRC and diverticulosis specimens (22% versus 32.5%, p = 0.91). In conclusion, cyclomodulin-producing E. coli belonging mostly to B2 phylogroup colonize the colonic mucosa of patients with CRC.

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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.
“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 [153]
The Results section (page unavailable) reports pks-positive E. coli in 55.3% of CRC specimens, reasonably approximating the claimed 60%. It reports 19.3% in diverticulosis specimens, not healthy individuals, and gives no pks-positive prevalence for patients with inflammatory bowel disease; the claimed 20% and 40% are therefore unsupported. (LLM, conf=0.88)
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Authors: Buc, E., Dubois, D., Sauvanet, P., Raisch, J., Delmas, J., Darfeuille-Michaud, A., Pezet, D., & Bonnet, R.
Affiliations: Inserm (FR)
Corresponding author: Bonnet, Richard
ORCID: Buc, Emmanuel
Dubois, Damien
Raisch, Jennifer
Delmas, Julien
Pezet, Denis
Bonnet, Richard
Venue: PLoS ONE
Publisher: Public Library of Science (PLoS)
Published: 2013-02-14
Volume: 8
Issue: 2
Pages: e56964
ISSN: 1932-6203 (ISSN-L)
DOI: 10.1371/journal.pone.0056964
PMC: PMC3572998
OpenAlex: W1996173530
Cited by: 535
References: 76
Citations by year: 2026: 20 · 2025: 42 · 2024: 62 · 2023: 44 · 2022: 62 · 2021: 83 · 2020: 49 · 2019: 49 · 2018: 31 · 2017: 21 · 2016: 25 · 2015: 17 · 2014: 20 · 2013: 8 · 2012: 1
FWCI: 16.57
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0/ (unspecified)
Locations: PLoS ONE (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, other-oa)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
HAL (submittedVersion, other-oa)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Figshare (submittedVersion, cc-by)
Funders: Institut National de la Santé et de la Recherche Médicale (USC-2018, U1071)
Ligue Contre le Cancer
Institut National de la Recherche Agronomique (U1071, USC-2018)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Endocrinology › Escherichia coli research studies
Health Sciences › Medicine › Infectious Diseases › Clostridium difficile and Clostridium perfringens research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
Keywords: Escherichia coli, cytotoxic necrotizing factor 1, colorectal cancer, diverticulosis, genotoxicity, DNA damage, bacterial adhesion, host cell cycle
MeSH terms: Adult, Aged, Aged, 80 and over, Bacterial Adhesion, Bacterial Toxins, Colonic Neoplasms, Escherichia coli, Humans, Intestinal Mucosa, Middle Aged, Mutagens, Phenotype, Prevalence

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High Prevalence of Mucosa-Associated E. coli Producing Cyclomodulin and Genotoxin in Colon Cancer

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