Campylobacter jejuni-derived cytolethal distending toxin promotes colorectal cancer metastasis

Cell Host Microbe. 2024 Dec 11;32(12):2080-2091.e6. doi: 10.1016/j.chom.2024.11.006. Epub 2024 Dec 2.

Abstract

Various forms of solid tumors harbor intracellular bacteria, but the physiological consequences of these microorganisms are poorly understood. We show that Campylobacter is significantly enriched in primary colorectal cancer (CRC) lesions from patients with metastasis. Campylobacter jejuni-derived cytolethal distending toxin (CDT) promotes CRC metastasis through JAK2-STAT3-MMP9 signaling in liver or pulmonary metastatic mice models, as confirmed in C. jejuni-infected human colonic tissue and CDT-treated colonic tumoroids from patients. Genetic deletion of cdtB (ΔcdtB) or purified CdtB protein demonstrates that the genotoxin is essential for C. jejuni's pro-metastatic property. In C.-jejuni-colonized mice, increased translocation of CDT-producing C. jejuni to extraintestinal implanted tumors potentially leads to accelerated metastasis of these tumors. Overall, these findings demonstrate that an intratumor-bacteria-derived genotoxin accelerates tumor metastasis, potentially opening a new diagnostic and therapeutic avenue for cancer management.

Keywords: Campylobacter jejuni; colorectal cancer; cytolethal distending toxin; metastasis.

MeSH terms

  • Animals
  • Bacterial Toxins* / genetics
  • Bacterial Toxins* / metabolism
  • Campylobacter Infections / microbiology
  • Campylobacter jejuni* / genetics
  • Campylobacter jejuni* / metabolism
  • Cell Line, Tumor
  • Colorectal Neoplasms* / microbiology
  • Colorectal Neoplasms* / pathology
  • Disease Models, Animal
  • Female
  • Humans
  • Janus Kinase 2 / genetics
  • Janus Kinase 2 / metabolism
  • Matrix Metalloproteinase 9 / metabolism
  • Mice
  • Neoplasm Metastasis*
  • STAT3 Transcription Factor* / metabolism
  • Signal Transduction

Substances

  • Bacterial Toxins
  • cytolethal distending toxin
  • STAT3 Transcription Factor
  • Janus Kinase 2
  • Matrix Metalloproteinase 9