Robo4 maintains vessel integrity and inhibits angiogenesis by interacting with UNC5B

Dev Cell. 2011 Jan 18;20(1):33-46. doi: 10.1016/j.devcel.2010.12.001.

Abstract

Robo4 is an endothelial cell-specific member of the Roundabout axon guidance receptor family. To identify Robo4 binding partners, we performed a protein-protein interaction screen with the Robo4 extracellular domain. We find that Robo4 specifically binds to UNC5B, a vascular Netrin receptor, revealing unexpected interactions between two endothelial guidance receptors. We show that Robo4 maintains vessel integrity by activating UNC5B, which inhibits signaling downstream of vascular endothelial growth factor (VEGF). Function-blocking monoclonal antibodies against Robo4 and UNC5B increase angiogenesis and disrupt vessel integrity. Soluble Robo4 protein inhibits VEGF-induced vessel permeability and rescues barrier defects in Robo4(-/-) mice, but not in mice treated with anti-UNC5B. Thus, Robo4-UNC5B signaling maintains vascular integrity by counteracting VEGF signaling in endothelial cells, identifying a novel function of guidance receptor interactions in the vasculature.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antibodies, Blocking / pharmacology
  • Blood Vessels / drug effects
  • Blood Vessels / enzymology
  • Blood Vessels / metabolism*
  • Blood Vessels / pathology*
  • Capillary Permeability / drug effects
  • Enzyme Activation / drug effects
  • Humans
  • Ligands
  • Mice
  • Models, Biological
  • Neovascularization, Pathologic / metabolism*
  • Nerve Tissue Proteins / metabolism*
  • Netrin Receptors
  • Protein Binding / drug effects
  • Receptors, Cell Surface / metabolism*
  • Receptors, Immunologic / metabolism*
  • Retinal Vessels / drug effects
  • Retinal Vessels / metabolism
  • Retinal Vessels / pathology
  • Signal Transduction / drug effects
  • Sus scrofa
  • Vascular Endothelial Growth Factor A / metabolism
  • src-Family Kinases / metabolism

Substances

  • Antibodies, Blocking
  • Ligands
  • Nerve Tissue Proteins
  • Netrin Receptors
  • Receptors, Cell Surface
  • Receptors, Immunologic
  • Robo4 protein, mouse
  • Vascular Endothelial Growth Factor A
  • src-Family Kinases