An allosteric inhibitor of RhoGAP class-IX myosins suppresses the metastatic features of cancer cells

Nat Commun. 2024 Nov 16;15(1):9947. doi: 10.1038/s41467-024-54181-6.

Abstract

Aberrant Ras homologous (Rho) GTPase signalling is a major driver of cancer metastasis, and GTPase-activating proteins (GAPs), the negative regulators of RhoGTPases, are considered promising targets for suppressing metastasis, yet drug discovery efforts have remained elusive. Here, we report the identification and characterization of adhibin, a synthetic allosteric inhibitor of RhoGAP class-IX myosins that abrogates ATPase and motor function, suppressing RhoGTPase-mediated modes of cancer cell metastasis. In human and murine adenocarcinoma and melanoma cell models, including three-dimensional spheroid cultures, we reveal anti-migratory and anti-adhesive properties of adhibin that originate from local disturbances in RhoA/ROCK-regulated signalling, affecting actin-dynamics and actomyosin-based cell-contractility. Adhibin blocks membrane protrusion formation, disturbs remodelling of cell-matrix adhesions, affects contractile ring formation, and disrupts epithelial junction stability; processes severely impairing single/collective cell migration and cytokinesis. Combined with the non-toxic, non-pathological signatures of adhibin validated in organoids, mouse and Drosophila models, this mechanism of action provides the basis for developing anti-metastatic cancer therapies.

MeSH terms

  • Allosteric Regulation / drug effects
  • Animals
  • Cell Adhesion / drug effects
  • Cell Line, Tumor
  • Cell Movement* / drug effects
  • Drosophila
  • Female
  • GTPase-Activating Proteins* / genetics
  • GTPase-Activating Proteins* / metabolism
  • Humans
  • Melanoma / drug therapy
  • Melanoma / genetics
  • Melanoma / metabolism
  • Melanoma / pathology
  • Mice
  • Myosins / metabolism
  • Neoplasm Metastasis*
  • Organoids / drug effects
  • Organoids / metabolism
  • Signal Transduction / drug effects
  • rho-Associated Kinases / antagonists & inhibitors
  • rho-Associated Kinases / metabolism
  • rhoA GTP-Binding Protein / metabolism

Substances

  • GTPase-Activating Proteins
  • rho GTPase-activating protein
  • rhoA GTP-Binding Protein
  • Myosins
  • rho-Associated Kinases