Natural angiogenesis inhibitor signals through Erk5 activation of peroxisome proliferator-activated receptor gamma (PPARgamma)

J Biol Chem. 2010 Apr 30;285(18):13517-24. doi: 10.1074/jbc.M110.117374. Epub 2010 Feb 25.

Abstract

Erk-5, a member of the MAPK superfamily, has a catalytic domain similar to Erk1/2 and a unique C-terminal domain enabling binding with transcription factors. Aberrant vascularization in the Erk5-null mice suggested a link to angiogenesis. Ectopic expression of constitutively active Erk5 blocks endothelial cell morphogenesis and causes HIF1-alpha destabilization/degradation. However the mechanisms by which endogenous Erk5 regulates angiogenesis remain unknown. We show that Erk5 and its activating kinase MEK5 are the upstream mediators of the anti-angiogenic signal by the natural angiogenesis inhibitor, pigment epithelial-derived factor (PEDF). We demonstrate that Erk5 phosphorylation allows activation of PPARgamma transcription factor by displacement of SMRT co-repressor. PPARgamma, in turn is critical for NFkappaB activation, PEDF-dependent apoptosis, and anti-angiogenesis. The dominant negative MEK5 mutant and Erk5 shRNA diminished PEDF-dependent apoptosis, inhibition of the endothelial cell chemotaxis, and angiogenesis. This is the first evidence of Erk5-dependent transduction of signals by endogenous angiogenesis inhibitors.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Angiogenesis Inhibitors / metabolism*
  • Angiogenesis Inhibitors / pharmacology
  • Animals
  • Apoptosis / drug effects
  • Apoptosis / physiology
  • Endothelial Cells / metabolism*
  • Enzyme Activation / drug effects
  • Enzyme Activation / physiology
  • Eye Proteins / genetics
  • Eye Proteins / metabolism*
  • Female
  • Humans
  • MAP Kinase Kinase 5 / genetics
  • MAP Kinase Kinase 5 / metabolism
  • MAP Kinase Signaling System / genetics
  • MAP Kinase Signaling System / physiology*
  • Mice
  • Mice, Nude
  • Mitogen-Activated Protein Kinase 7 / genetics
  • Mitogen-Activated Protein Kinase 7 / metabolism*
  • Mutation
  • NF-kappa B / genetics
  • NF-kappa B / metabolism
  • Neovascularization, Physiologic / drug effects
  • Neovascularization, Physiologic / physiology*
  • Nerve Growth Factors / genetics
  • Nerve Growth Factors / metabolism*
  • Nuclear Receptor Co-Repressor 2 / genetics
  • Nuclear Receptor Co-Repressor 2 / metabolism
  • PPAR gamma / genetics
  • PPAR gamma / metabolism*
  • Phosphorylation / drug effects
  • Phosphorylation / physiology
  • Serpins / genetics
  • Serpins / metabolism*

Substances

  • Angiogenesis Inhibitors
  • Eye Proteins
  • NCOR2 protein, human
  • NF-kappa B
  • Ncor2 protein, mouse
  • Nerve Growth Factors
  • Nuclear Receptor Co-Repressor 2
  • PPAR gamma
  • Serpins
  • pigment epithelium-derived factor
  • Mitogen-Activated Protein Kinase 7
  • MAP Kinase Kinase 5
  • MAP2K5 protein, human