Role of tyrosine phosphatase SHP-1 in the mechanism of endorepellin angiostatic activity

Blood. 2009 Nov 26;114(23):4897-906. doi: 10.1182/blood-2009-02-207134. Epub 2009 Sep 29.

Abstract

Endorepellin, the C-terminal domain of perlecan, is a powerful angiogenesis inhibitor. To dissect the mechanism of endorepellin-mediated endothelial silencing, we used an antibody array against multiple tyrosine kinase receptors. Endorepellin caused a widespread reduction in phosphorylation of key receptors involved in angiogenesis and a concurrent increase in phosphatase activity in endothelial cells and tumor xenografts. These effects were efficiently hampered by function-blocking antibodies against integrin alpha2beta1, the functional endorepellin receptor. The Src homology-2 protein phosphatase-1 (SHP-1) coprecipitated with integrin alpha2 and was phosphorylated in a dynamic fashion after endorepellin stimulation. Genetic evidence was provided by lack of an endorepellin-evoked phosphatase response in microvascular endothelial cells derived from integrin alpha2beta1(-/-) mice and by response to endorepellin in cells genetically engineered to express the alpha2beta1 integrin, but not in cells either lacking this receptor or expressing a chimera harboring the integrin alpha2 ectodomain fused to the alpha1 intracellular domain. siRNA-mediated knockdown of integrin alpha2 caused a dose-dependent reduction of SHP-1. Finally, the levels of SHP-1 and its enzymatic activity were substantially reduced in multiple organs from alpha2beta1(-/-) mice. Our results show that SHP-1 is an essential mediator of endorepellin activity and discover a novel functional interaction between the integrin alpha2 subunit and SHP-1.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Carcinoma, Lewis Lung / blood supply
  • Cell Adhesion / drug effects
  • Endothelium, Vascular / physiology
  • Heparan Sulfate Proteoglycans / pharmacology
  • Heparan Sulfate Proteoglycans / physiology*
  • Humans
  • Integrin alpha1 / genetics
  • Integrin alpha2beta1 / chemistry
  • Integrin alpha2beta1 / deficiency
  • Integrin alpha2beta1 / genetics
  • Integrin alpha2beta1 / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Neovascularization, Pathologic / drug therapy
  • Neovascularization, Physiologic / physiology*
  • Peptide Fragments / pharmacology
  • Peptide Fragments / physiology*
  • Phosphorylation / drug effects
  • Phosphotyrosine / analysis
  • Protein Interaction Mapping
  • Protein Processing, Post-Translational / drug effects
  • Protein Structure, Tertiary
  • Protein Tyrosine Phosphatase, Non-Receptor Type 6 / chemistry
  • Protein Tyrosine Phosphatase, Non-Receptor Type 6 / deficiency
  • Protein Tyrosine Phosphatase, Non-Receptor Type 6 / metabolism
  • Protein Tyrosine Phosphatase, Non-Receptor Type 6 / physiology*
  • Receptor Protein-Tyrosine Kinases / antagonists & inhibitors
  • Receptor Protein-Tyrosine Kinases / physiology
  • Recombinant Fusion Proteins / physiology
  • Xenograft Model Antitumor Assays

Substances

  • Heparan Sulfate Proteoglycans
  • Integrin alpha1
  • Integrin alpha2beta1
  • Peptide Fragments
  • Recombinant Fusion Proteins
  • perlecan
  • Phosphotyrosine
  • Receptor Protein-Tyrosine Kinases
  • PTPN6 protein, human
  • Protein Tyrosine Phosphatase, Non-Receptor Type 6
  • Ptpn6 protein, mouse