Cytolethal Distending Toxin Modulates Cell Differentiation and Elicits Epithelial to Mesenchymal Transition

J Infect Dis. 2024 Jun 14;229(6):1688-1701. doi: 10.1093/infdis/jiae105.

Abstract

Background: The bacterial genotoxin, cytolethal distending toxin (CDT), causes DNA damage in host cells, a risk factor for carcinogenesis. Previous studies have shown that CDT induces phenotypes reminiscent of epithelial to mesenchymal transition (EMT), a process involved in cancer initiation and progression.

Methods: We investigated different steps of EMT in response to Helicobacter hepaticus CDT and its active CdtB subunit using in vivo and in vitro models.

Results: Most of the steps of the EMT process were induced by CDT/CdtB and observed throughout the study in murine and epithelial cell culture models. CdtB induced cell-cell junction disassembly, causing individualization of cells and acquisition of a spindle-like morphology. The key transcriptional regulators of EMT (SNAIL and ZEB1) and some EMT markers were upregulated at both RNA and protein levels in response to CDT/CdtB. CdtB increased the expression and proteolytic activity of matrix metalloproteinases, as well as cell migration. A range of these results were confirmed in Helicobacter hepaticus-infected and xenograft murine models. In addition, colibactin, a genotoxic metabolite produced by Escherichia coli, induced EMT-like effects in cell culture.

Conclusions: Overall, these data show that infection with genotoxin-producing bacteria elicits EMT process activation, supporting their role in tumorigenesis.

Keywords: Helicobacter hepaticus; SNAIL; ZEB1; cell-cell junctions; colibactin; cytolethal distending toxin; epithelial to mesenchymal transition; matrix metalloproteinases; migration.

MeSH terms

  • Animals
  • Bacterial Toxins* / metabolism
  • Bacterial Toxins* / toxicity
  • Cell Differentiation* / drug effects
  • Epithelial Cells / drug effects
  • Epithelial Cells / metabolism
  • Epithelial Cells / microbiology
  • Epithelial-Mesenchymal Transition* / drug effects
  • Female
  • Helicobacter Infections / microbiology
  • Helicobacter hepaticus
  • Humans
  • Mice
  • Snail Family Transcription Factors / genetics
  • Snail Family Transcription Factors / metabolism

Substances

  • cytolethal distending toxin
  • Bacterial Toxins
  • Snail Family Transcription Factors