VEGF and inhibitors of TGFbeta type-I receptor kinase synergistically promote blood-vessel formation by inducing alpha5-integrin expression

J Cell Sci. 2009 Sep 15;122(Pt 18):3294-302. doi: 10.1242/jcs.048942. Epub 2009 Aug 25.

Abstract

Vascular endothelial growth factor (VEGF) and transforming growth factor-beta (TGFbeta) are potent regulators of angiogenesis. How VEGF and TGFbeta signaling pathways crosstalk is not well understood. Therefore, we analyzed the effects of the TGFbeta type-I-receptor inhibitors (SB-431542 and LY-2157299) and VEGF on endothelial cell (EC) function and angiogenesis. We show that SB-431542 dramatically enhances VEGF-induced formation of EC sheets from fetal mouse metatarsals. Sub-optimal doses of VEGF and SB-431542 synergistically induced EC migration and sprouting of EC spheroids, whereas overexpression of a constitutively active form of TGFbeta type-I receptor had opposite effects. Using quantitative PCR, we demonstrated that VEGF and SB-431542 synergistically upregulated the mRNA expression of genes involved in angiogenesis, including the integrins alpha5 and beta3. Specific downregulation of alpha5-integrin expression or functional blocking of alpha5 integrin with a specific neutralizing antibody inhibited the cooperative effect of VEGF and SB-431542 on EC sprouting. In vivo, LY-2157299 induced angiogenesis and enhanced VEGF- and basic-fibroblast-growth-factor-induced angiogenesis in a Matrigel-plug assay, whereas adding an alpha5-integrin-neutralizing antibody to the Matrigel selectively inhibited this enhanced response. Thus, induction of alpha5-integrin expression is a key determinant by which inhibitors of TGFbeta type-I receptor kinase and VEGF synergistically promote angiogenesis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Benzamides
  • Biological Assay
  • Cell Movement / drug effects
  • Collagen / metabolism
  • Dioxoles
  • Drug Combinations
  • Drug Synergism
  • Endothelial Cells / cytology
  • Endothelial Cells / drug effects
  • Endothelial Cells / metabolism
  • Fetus / blood supply
  • Fetus / drug effects
  • Gene Expression Profiling
  • Humans
  • Integrin alpha5 / metabolism*
  • Integrin beta3 / metabolism
  • Laminin / metabolism
  • Mice
  • Neovascularization, Physiologic / drug effects*
  • Neutralization Tests
  • Protein Kinase Inhibitors / pharmacology*
  • Protein Serine-Threonine Kinases / antagonists & inhibitors*
  • Proteoglycans / metabolism
  • Receptor, Transforming Growth Factor-beta Type I
  • Receptors, Transforming Growth Factor beta / antagonists & inhibitors*
  • Spheroids, Cellular / cytology
  • Spheroids, Cellular / drug effects
  • Spheroids, Cellular / metabolism
  • Vascular Endothelial Growth Factor A / pharmacology*

Substances

  • 4-(5-benzo(1,3)dioxol-5-yl-4-pyridin-2-yl-1H-imidazol-2-yl)benzamide
  • Benzamides
  • Dioxoles
  • Drug Combinations
  • Integrin alpha5
  • Integrin beta3
  • Laminin
  • Protein Kinase Inhibitors
  • Proteoglycans
  • Receptors, Transforming Growth Factor beta
  • Vascular Endothelial Growth Factor A
  • matrigel
  • Collagen
  • Protein Serine-Threonine Kinases
  • Receptor, Transforming Growth Factor-beta Type I