The GAS6-AXL signaling pathway triggers actin remodeling that drives membrane ruffling, macropinocytosis, and cancer-cell invasion

Proc Natl Acad Sci U S A. 2021 Jul 13;118(28):e2024596118. doi: 10.1073/pnas.2024596118.

Abstract

AXL, a member of the TAM (TYRO3, AXL, MER) receptor tyrosine kinase family, and its ligand, GAS6, are implicated in oncogenesis and metastasis of many cancer types. However, the exact cellular processes activated by GAS6-AXL remain largely unexplored. Here, we identified an interactome of AXL and revealed its associations with proteins regulating actin dynamics. Consistently, GAS6-mediated AXL activation triggered actin remodeling manifested by peripheral membrane ruffling and circular dorsal ruffles (CDRs). This further promoted macropinocytosis that mediated the internalization of GAS6-AXL complexes and sustained survival of glioblastoma cells grown under glutamine-deprived conditions. GAS6-induced CDRs contributed to focal adhesion turnover, cell spreading, and elongation. Consequently, AXL activation by GAS6 drove invasion of cancer cells in a spheroid model. All these processes required the kinase activity of AXL, but not TYRO3, and downstream activation of PI3K and RAC1. We propose that GAS6-AXL signaling induces multiple actin-driven cytoskeletal rearrangements that contribute to cancer-cell invasion.

Keywords: GAS6-AXL; TAM receptors; actin; macropinocytosis; membrane ruffles.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actin Cytoskeleton / metabolism
  • Actins / metabolism*
  • Axl Receptor Tyrosine Kinase
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Cell Surface Extensions / metabolism*
  • Enzyme Activation / drug effects
  • Focal Adhesions / drug effects
  • Focal Adhesions / metabolism
  • Glioblastoma / pathology
  • Glutamine / pharmacology
  • HEK293 Cells
  • Humans
  • Intercellular Signaling Peptides and Proteins / metabolism*
  • Models, Biological
  • Neoplasm Invasiveness
  • Neoplasms / metabolism*
  • Neoplasms / pathology*
  • Phosphatidylinositol 3-Kinases / metabolism
  • Pinocytosis*
  • Protein Binding
  • Proto-Oncogene Proteins / metabolism*
  • Receptor Protein-Tyrosine Kinases / metabolism*
  • Signal Transduction*
  • rac1 GTP-Binding Protein / metabolism

Substances

  • Actins
  • Intercellular Signaling Peptides and Proteins
  • Proto-Oncogene Proteins
  • growth arrest-specific protein 6
  • Glutamine
  • Receptor Protein-Tyrosine Kinases
  • rac1 GTP-Binding Protein
  • Axl Receptor Tyrosine Kinase
  • AXL protein, human