Endothelial cell adhesion to the extracellular matrix induces c-Src-dependent VEGFR-3 phosphorylation without the activation of the receptor intrinsic kinase activity

Circ Res. 2010 Jun 25;106(12):1839-48. doi: 10.1161/CIRCRESAHA.109.206326. Epub 2010 Apr 29.

Abstract

Rationale: Integrins cooperate with growth factor receptors to promote downstream signaling for cell proliferation and migration. However, the mechanism of receptor activation is still unknown.

Objective: To analyze the mechanism of phosphorylation of the vascular endothelial growth factor receptor (VEGFR)-3 by cell adhesion.

Methods and results: We show that VEGFR-3 phosphorylation, induced by cell attachment to the extracellular matrix, is independent from the intrinsic kinase activity of the receptor, as evidenced from phosphorylation cell adhesion experiments with a mutant kinase dead receptor or in the presence of the specific kinase inhibitor MAZ 51. Cell adhesion experiments in the presence of the c-Src inhibitor PP2 or in fibroblast triple knockout for c-Src, Yes, and Fyn (SYF) demonstrate that VEGFR-3 phosphorylation, induced by extracellular matrix, is mediated by c-Src. Kinase assays in vitro with recombinant c-Src show that VEGFR-3 is a direct c-Src target and mass spectrometry analysis identified the sites phosphorylated by c-Src as tyrosine 830, 833, 853, 1063, 1333, and 1337, demonstrating that integrin-mediated receptor phosphorylation induces a phosphorylation pattern that is distinct from that induced by growth factors. Furthermore, pull-down assays show that integrin-mediated VEGFR-3 phosphorylation activates the recruitment to the receptor of the adaptor proteins CRKI/II and SHC inducing activation of JNK.

Conclusions: These data suggest that cell adhesion to extracellular matrix induces a downstream signaling using the tyrosine kinase receptor VEGFR-3 as scaffold.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • CSK Tyrosine-Protein Kinase
  • Cell Adhesion
  • Cell Line
  • Cells, Cultured
  • Collagen Type I / metabolism
  • Endothelium, Vascular / cytology*
  • Endothelium, Vascular / metabolism*
  • Extracellular Matrix / metabolism*
  • Humans
  • MAP Kinase Kinase 4 / metabolism
  • Mice
  • Mice, Knockout
  • Models, Animal
  • Phosphorylation
  • Protein-Tyrosine Kinases / metabolism*
  • Proto-Oncogene Proteins c-crk / metabolism
  • Proto-Oncogene Proteins c-fyn / genetics
  • Proto-Oncogene Proteins c-fyn / metabolism
  • Proto-Oncogene Proteins c-yes / genetics
  • Proto-Oncogene Proteins c-yes / metabolism
  • Shc Signaling Adaptor Proteins / metabolism
  • Vascular Endothelial Growth Factor Receptor-3 / metabolism*
  • src-Family Kinases

Substances

  • Collagen Type I
  • Proto-Oncogene Proteins c-crk
  • Shc Signaling Adaptor Proteins
  • Protein-Tyrosine Kinases
  • Vascular Endothelial Growth Factor Receptor-3
  • CSK Tyrosine-Protein Kinase
  • Proto-Oncogene Proteins c-fyn
  • Proto-Oncogene Proteins c-yes
  • src-Family Kinases
  • CSK protein, human
  • MAP Kinase Kinase 4