Reciprocal integrin/integrin antagonism through kindlin-2 and Rho GTPases regulates cell cohesion and collective migration

Matrix Biol. 2020 Nov:93:60-78. doi: 10.1016/j.matbio.2020.05.005. Epub 2020 May 23.

Abstract

Collective cell behaviour during embryogenesis and tissue repair requires the coordination of intercellular junctions, cytoskeleton-dependent shape changes controlled by Rho GTPases, and integrin-dependent cell-matrix adhesion. Many different integrins are simultaneously expressed during wound healing, embryonic development, and sprouting angiogenesis, suggesting that there is extensive integrin/integrin cross-talk to regulate cell behaviour. Here, we show that fibronectin-binding β1 and β3 integrins do not act synergistically, but rather antagonize each other during collective cell processes in neuro-epithelial cells, placental trophoblasts, and endothelial cells. Reciprocal β1/β3 antagonism controls RhoA activity in a kindlin-2-dependent manner, balancing cell spreading, contractility, and intercellular adhesion. In this way, reciprocal β1/β3 antagonism controls cell cohesion and cellular plasticity to switch between extreme and opposing states, including epithelial versus mesenchymal-like phenotypes and collective versus individual cell migration. We propose that integrin/integrin antagonism is a universal mechanism to effectuate social cellular interactions, important for tissue morphogenesis, endothelial barrier function, trophoblast invasion, and sprouting angiogenesis.

Keywords: Collective cell migration; Epithelial-to-mesenchymal transition; Fibronectin; Inhibition of integrin function; Kindlin-2; Rho GTPases.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cell Movement
  • Cell Plasticity
  • Cytoplasm / metabolism
  • Embryonic Development
  • HEK293 Cells
  • Human Umbilical Vein Endothelial Cells
  • Humans
  • Integrin beta1 / metabolism*
  • Integrin beta3 / metabolism*
  • Membrane Proteins / metabolism*
  • Neoplasm Proteins / metabolism*
  • Neuroepithelial Cells / cytology*
  • Neuroepithelial Cells / metabolism
  • Phenotype
  • rhoA GTP-Binding Protein / metabolism*

Substances

  • FERMT3 protein, human
  • ITGB3 protein, human
  • Integrin beta1
  • Integrin beta3
  • Itgb1 protein, human
  • Membrane Proteins
  • Neoplasm Proteins
  • RHOA protein, human
  • rhoA GTP-Binding Protein