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

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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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Figure 1 Cytopathic effect induced by E. coli live bacteria or protein extracts on epithelial cells at three-day post-infection. For CNF and CDT, the cytopathic effect is only observable with bacterial lysates. In contrast, for colibactin and CIF, a contact between bacteria and host cells is required. Colibactin, CDT and CIF induced cytopathic effects as seen by enlarged nuclei and cell distension (megalocytosis), while CNF induced multinucleation and enlargement of HeLa cells.CC BY · PubMed Central

Figure 2 Distribution of E. coli strains producing various cyclomodulins according to phylogroups and specimen origins. A, E. coli strains (n = 70) isolated from CRC samples (n = 38), and B, E. coli strains (n = 46) isolated from diverticulosis samples (n = 31).CC BY · PubMed Central

Figure 3 DNA damage was detected by the comet assay in HeLa cells exposed to E. coli for 3 h. DNA damage was not detected in HeLa cells infected with the E. coli strain IHE3034 ΔclbP harboring a defective pks island (A). Comet assay was positive in HeLa cells infected with the E. coli strain IHE3034 harboring pks island (B) or with E. coli devoid of known cyclomodulin-encoding genes (C).CC BY · PubMed Central

Figure 4 Adhesion ability of E. coli strains isolated from diverticulosis and CRC (proximal and distal) samples to Int-407 intestinal epithelial cells. A, adhesion ability according to the specimen origin and E. coli phylogroup. B, Adhesion ability of E. coli strains isolated from diverticulosis and CRC (proximal and distal) samples and belonging to A and D phylogroups according to their ability to produce or not a cyclomodulin/genotoxin. The results are expressed as number of adherent bacteria per cell after 3 h infection period. Data are means+/−SEM for at least 3 independent experiments.CC BY · PubMed Central

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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
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 › Immunology and Microbiology › Microbiology › 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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