15(S)-hydroxyeicosatetraenoic acid-induced angiogenesis requires Src-mediated Egr-1-dependent rapid induction of FGF-2 expression

Blood. 2010 Mar 11;115(10):2105-16. doi: 10.1182/blood-2009-09-241802. Epub 2010 Jan 6.

Abstract

To understand the mechanisms underlying 15(S)-hydroxyeicosatetraenoic acid [15(S)-HETE]-induced angiogenesis, we studied the role of Egr-1. 15(S)-HETE induced Egr-1 expression in a time-dependent manner in human dermal microvascular endothelial cells (HDMVECs). Blockade of Egr-1 via forced expression of its dominant-negative mutant attenuated 15(S)-HETE-induced HDMVEC migration and tube formation as well as Matrigel plug angiogenesis. 15(S)-HETE-induced Egr-1 expression requires Src activation. In addition, adenovirus-mediated expression of dominant-negative mutant of Src blocked 15(S)-HETE's effects on migration and tube formation of HDMVECs and Matrigel plug angiogenesis. 15(S)-HETE induced fibroblast growth factor-2 (FGF-2) expression rapidly via Src-mediated production of Egr-1. Cloning and mutational analysis of FGF-2 promoter revealed that Egr-1 binding site proximal to transcription start site is required for 15(S)-HETE-induced FGF-2 expression. Neutralizing antibody-mediated suppression of FGF-2 function also attenuated the effects of 15(S)-HETE on HDMVEC migration and tube formation as well as Matrigel plug angiogenesis. Furthermore, in contrast to wild-type mice, 12/15-LOX(-/-) mice exhibited decreased Matrigel plug angiogenesis in response to AA, which was rescued by 15(S)-HETE. On the basis of these observations, we conclude that 15(S)-HETE-induced angiogenesis requires Src-mediated Egr-1-dependent rapid induction of FGF-2. These findings may suggest that 15(S)-HETE could be a potential endogenous regulator of pathologic angiogenesis associated with atherosclerosis and restenosis.

Publication types

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

MeSH terms

  • Animals
  • Arachidonate 12-Lipoxygenase / genetics
  • Arachidonate 15-Lipoxygenase / genetics
  • Base Sequence
  • Cells, Cultured
  • Early Growth Response Protein 1 / metabolism
  • Early Growth Response Protein 1 / physiology*
  • Fibroblast Growth Factor 2 / genetics*
  • Fibroblast Growth Factor 2 / metabolism
  • Gene Expression Regulation / drug effects
  • Humans
  • Hydroxyeicosatetraenoic Acids / pharmacology*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Molecular Sequence Data
  • Neovascularization, Physiologic / drug effects*
  • Neovascularization, Physiologic / genetics
  • Proto-Oncogene Proteins pp60(c-src) / physiology*
  • Time Factors
  • Up-Regulation / drug effects

Substances

  • 12-15-lipoxygenase
  • EGR1 protein, human
  • Early Growth Response Protein 1
  • Hydroxyeicosatetraenoic Acids
  • Fibroblast Growth Factor 2
  • 15-hydroxy-5,8,11,13-eicosatetraenoic acid
  • Arachidonate 12-Lipoxygenase
  • Arachidonate 15-Lipoxygenase
  • Proto-Oncogene Proteins pp60(c-src)