Enrichment of colibactin-associated mutational signatures in unexplained colorectal polyposis patients

BMC Cancer. 2024 Jan 18;24(1):104. doi: 10.1186/s12885-024-11849-y.

Abstract

Background: Colibactin, a genotoxin produced by polyketide synthase harboring (pks+) bacteria, induces double-strand breaks and chromosome aberrations. Consequently, enrichment of pks+Escherichia coli in colorectal cancer and polyposis suggests a possible carcinogenic effect in the large intestine. Additionally, specific colibactin-associated mutational signatures; SBS88 and ID18 in the Catalogue of Somatic Mutations in Cancer database, are detected in colorectal carcinomas. Previous research showed that a recurrent APC splice variant perfectly fits SBS88.

Methods: In this study, we explore the presence of colibactin-associated signatures and fecal pks in an unexplained polyposis cohort. Somatic targeted Next-Generation Sequencing (NGS) was performed for 379 patients. Additionally, for a subset of 29 patients, metagenomics was performed on feces and mutational signature analyses using Whole-Genome Sequencing (WGS) on Formalin-Fixed Paraffin Embedded (FFPE) colorectal tissue blocks.

Results: NGS showed somatic APC variants fitting SBS88 or ID18 in at least one colorectal adenoma or carcinoma in 29% of patients. Fecal metagenomic analyses revealed enriched presence of pks genes in patients with somatic variants fitting colibactin-associated signatures compared to patients without variants fitting colibactin-associated signatures. Also, mutational signature analyses showed enrichment of SBS88 and ID18 in patients with variants fitting these signatures in NGS compared to patients without.

Conclusions: These findings further support colibactins ability to mutagenize colorectal mucosa and contribute to the development of colorectal adenomas and carcinomas explaining a relevant part of patients with unexplained polyposis.

Keywords: Bacterial pathogenesis; Colorectal adenomas; Intestinal microbiology; Polyposis.

MeSH terms

  • Adenoma* / genetics
  • Carcinoma*
  • Colorectal Neoplasms* / genetics
  • Colorectal Neoplasms* / microbiology
  • Escherichia coli / genetics
  • Humans
  • Mutation
  • Peptides / genetics
  • Polyketides*

Substances

  • colibactin
  • Peptides
  • Polyketides