VEGF-induced endothelial cell migration requires urokinase receptor (uPAR)-dependent integrin redistribution

Cardiovasc Res. 2012 Apr 1;94(1):125-35. doi: 10.1093/cvr/cvs017. Epub 2012 Jan 26.

Abstract

Aims: Vascular endothelial growth factor (VEGF)-initiated angiogenesis requires coordinated proteolytic degradation of extracellular matrix provided by the urokinase plasminogen activator/urokinase receptor (uPA/uPAR) system and regulation of cell migration provided by integrin-matrix interaction. In this study, we investigated the mechanisms underlying the uPAR-dependent modulation of VEGF-induced endothelial migration.

Methods and results: We used flow cytometry to quantify integrins at the cell surface. Stimulation of human and murine endothelial cells with VEGF resulted in internalization of α5β1-integrins. Micropatterning and immunocytochemistry revealed co-clustering of uPAR and α5β1-integrins and retrieval via clathrin-coated vesicles. It was also contingent on receptors of the low-density lipoprotein receptor (LDL-R) family. VEGF-induced integrin redistribution was inhibited by elimination of uPAR from the endothelial cell surface or by inhibitory peptides that block the uPAR-integrin interaction. Under these conditions, the migratory response of endothelial cells upon VEGF stimulation was impaired both in vitro and in vivo.

Conclusions: The observations indicate that uPAR is an essential component of the network through which VEGF controls endothelial cell migration. uPAR is a bottleneck through which the VEGF-induced signal must be funnelled for both focused proteolytic activity at the leading edge and for redistribution of integrins.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Movement*
  • Cells, Cultured
  • Clathrin-Coated Vesicles / metabolism
  • Endocytosis
  • Endothelial Cells / metabolism*
  • Flow Cytometry
  • Human Umbilical Vein Endothelial Cells / metabolism
  • Humans
  • Immunohistochemistry
  • Integrin alpha5beta1 / metabolism*
  • Mice
  • Mice, Knockout
  • Neovascularization, Physiologic*
  • Protein Transport
  • RNA Interference
  • Receptors, LDL / metabolism
  • Receptors, Urokinase Plasminogen Activator / deficiency
  • Receptors, Urokinase Plasminogen Activator / genetics
  • Receptors, Urokinase Plasminogen Activator / metabolism*
  • Recombinant Proteins / metabolism
  • Signal Transduction
  • Transfection
  • Vascular Endothelial Growth Factor A / metabolism*

Substances

  • Integrin alpha5beta1
  • PLAUR protein, human
  • Plaur protein, mouse
  • Receptors, LDL
  • Receptors, Urokinase Plasminogen Activator
  • Recombinant Proteins
  • Vascular Endothelial Growth Factor A
  • vascular endothelial growth factor A, mouse