Annexin 2 regulates endothelial morphogenesis by controlling AKT activation and junctional integrity

J Biol Chem. 2010 Dec 24;285(52):40624-34. doi: 10.1074/jbc.M110.157271. Epub 2010 Oct 13.

Abstract

Sprouting angiogenesis is a multistep process that involves endothelial cell activation, basement membrane degradation, proliferation, lumen formation, and stabilization. In this study, we identified annexin 2 as a regulator of endothelial morphogenesis using a three-dimensional in vitro model where sprouting angiogenesis was driven by sphingosine 1-phosphate and angiogenic growth factors. We observed that sphingosine 1-phosphate triggered annexin 2 translocation from the cytosol to the plasma membrane and its association with vascular endothelial (VE)-cadherin. In addition, annexin 2 depletion attenuated Akt activation, which was associated with increased phosphorylation of VE-cadherin and endothelial barrier leakage. Disrupting homotypic VE-cadherin interactions with EGTA, antibodies to the extracellular domain of VE-cadherin, or gene silencing all resulted in decreased Akt (but not Erk1/2) activation. Furthermore, expression of constitutively active Akt restored reduced endothelial sprouting responses observed with annexin 2 and VE-cadherin knockdown. Collectively, we report that annexin 2 regulates endothelial morphogenesis through an adherens junction-mediated pathway upstream of Akt.

Publication types

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

MeSH terms

  • Annexin A2 / genetics
  • Annexin A2 / metabolism*
  • Antigens, CD / genetics
  • Antigens, CD / metabolism
  • Cadherins / genetics
  • Cadherins / metabolism
  • Cytosol / metabolism*
  • Endothelial Cells / cytology
  • Endothelial Cells / metabolism*
  • Enzyme Activation / physiology
  • Gene Knockdown Techniques
  • HEK293 Cells
  • Humans
  • Intercellular Junctions / genetics
  • Intercellular Junctions / metabolism*
  • Lysophospholipids / genetics
  • Lysophospholipids / metabolism
  • Mitogen-Activated Protein Kinase 1 / genetics
  • Mitogen-Activated Protein Kinase 1 / metabolism
  • Mitogen-Activated Protein Kinase 3 / genetics
  • Mitogen-Activated Protein Kinase 3 / metabolism
  • Neovascularization, Physiologic / physiology*
  • Protein Transport / physiology
  • Proto-Oncogene Proteins c-akt / genetics
  • Proto-Oncogene Proteins c-akt / metabolism*
  • Sphingosine / analogs & derivatives
  • Sphingosine / genetics
  • Sphingosine / metabolism

Substances

  • ANXA2 protein, human
  • Annexin A2
  • Antigens, CD
  • Cadherins
  • Lysophospholipids
  • cadherin 5
  • sphingosine 1-phosphate
  • Proto-Oncogene Proteins c-akt
  • MAPK1 protein, human
  • Mitogen-Activated Protein Kinase 1
  • Mitogen-Activated Protein Kinase 3
  • Sphingosine