Peptostreptococcus stomatis promotes colonic tumorigenesis and receptor tyrosine kinase inhibitor resistance by activating ERBB2-MAPK

Cell Host Microbe. 2024 Aug 14;32(8):1365-1379.e10. doi: 10.1016/j.chom.2024.07.001. Epub 2024 Jul 25.

Abstract

Peptostreptococcus stomatis (P. stomatis) is enriched in colorectal cancer (CRC), but its causality and translational implications in CRC are unknown. Here, we show that P. stomatis accelerates colonic tumorigenesis in ApcMin/+ and azoxymethane/dextran sodium sulfate (AOM-DSS) models by inducing cell proliferation, suppressing apoptosis, and impairing gut barrier function. P. stomatis adheres to CRC cells through its surface protein fructose-1,6-bisphosphate aldolase (FBA) that binds to the integrin α6/β4 receptor on CRC cells, leading to the activation of ERBB2 and the downstream MEK-ERK-p90 cascade. Blockade of the FBA-integrin α6/β4 abolishes ERBB2-mitogen-activated protein kinase (MAPK) activation and the protumorigenic effect of P. stomatis. P. stomatis-driven ERBB2 activation bypasses receptor tyrosine kinase (RTK) blockade by EGFR inhibitors (cetuximab, erlotinib), leading to drug resistance in xenograft and spontaneous CRC models of KRAS-wild-type CRC. P. stomatis also abrogates BRAF inhibitor (vemurafenib) efficacy in BRAFV600E-mutant CRC xenografts. Thus, we identify P. stomatis as an oncogenic bacterium and a contributory factor for non-responsiveness to RTK inhibitors in CRC.

Keywords: Peptostreptococcus Stomatis; colorectal cancer; drug resistance; host-microbe interaction; receptor tyrosine kinase inhibitor.

MeSH terms

  • Animals
  • Apoptosis / drug effects
  • Carcinogenesis*
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Colorectal Neoplasms* / drug therapy
  • Colorectal Neoplasms* / microbiology
  • Colorectal Neoplasms* / pathology
  • Drug Resistance, Neoplasm*
  • Fructose-Bisphosphate Aldolase / genetics
  • Fructose-Bisphosphate Aldolase / metabolism
  • Humans
  • MAP Kinase Signaling System / drug effects
  • Mice
  • Mitogen-Activated Protein Kinases / genetics
  • Mitogen-Activated Protein Kinases / metabolism
  • Peptostreptococcus*
  • Receptor, ErbB-2* / genetics
  • Receptor, ErbB-2* / metabolism
  • Tyrosine Kinase Inhibitors* / pharmacology

Substances

  • ERBB2 protein, human
  • Fructose-Bisphosphate Aldolase
  • Mitogen-Activated Protein Kinases
  • Receptor, ErbB-2
  • Tyrosine Kinase Inhibitors