Integrin-Linked Kinase Links Integrin Activation to Invadopodia Function and Invasion via the p(T567)-Ezrin/NHERF1/NHE1 Pathway

Int J Mol Sci. 2021 Feb 22;22(4):2162. doi: 10.3390/ijms22042162.

Abstract

Tumor cell invasion depends largely on degradation of the extracellular matrix (ECM) by protease-rich structures called invadopodia, whose formation and activity requires the convergence of signaling pathways engaged in cell adhesion, actin assembly, membrane regulation and ECM proteolysis. It is known that β1-integrin stimulates invadopodia function through an invadopodial p(T567)-ezrin/NHERF1/NHE1 signal complex that regulates NHE1-driven invadopodia proteolytic activity and invasion. However, the link between β1-integrin and this signaling complex is unknown. In this study, in metastatic breast (MDA-MB-231) and prostate (PC-3) cancer cells, we report that integrin-linked kinase (ILK) integrates β1-integrin with this signaling complex to regulate invadopodia activity and invasion. Proximity ligation assay experiments demonstrate that, in invadopodia, ILK associates with β1-integrin, NHE1 and the scaffold proteins p(T567)-ezrin and NHERF1. Activation of β1-integrin increased both invasion and invadopodia activity, which were specifically blocked by inhibition of either NHE1 or ILK. We conclude that ILK integrates β1-integrin with the ECM proteolytic/invasion signal module to induce NHE1-driven invadopodial ECM proteolysis and cell invasion.

Keywords: breast cancer; integrin signaling; invadopodia; invasion; pH; prostate cancer.

MeSH terms

  • Cell Line, Tumor
  • Cytoskeletal Proteins / metabolism
  • Extracellular Matrix / metabolism
  • Humans
  • Integrin beta1 / metabolism*
  • Male
  • PC-3 Cells
  • Phosphoproteins / metabolism
  • Podosomes / metabolism*
  • Podosomes / pathology*
  • Protein Serine-Threonine Kinases / metabolism*
  • Sodium-Hydrogen Exchanger 1 / metabolism
  • Sodium-Hydrogen Exchangers / metabolism

Substances

  • Cytoskeletal Proteins
  • Integrin beta1
  • Itgb1 protein, human
  • Phosphoproteins
  • SLC9A1 protein, human
  • Sodium-Hydrogen Exchanger 1
  • Sodium-Hydrogen Exchangers
  • ezrin
  • sodium-hydrogen exchanger regulatory factor
  • integrin-linked kinase
  • Protein Serine-Threonine Kinases