Effect of pharmacologic plasminogen activator inhibitor-1 inhibition on cell motility and tumor angiogenesis

J Thromb Haemost. 2006 Dec;4(12):2710-5. doi: 10.1111/j.1538-7836.2006.02244.x. Epub 2006 Oct 2.

Abstract

Background: Plasminogen activator inhibitor-1 (PAI-1) is integrally involved in tumorigenesis by impacting on both proteolytic activity and cell migration during angiogenesis.

Objectives: We hypothesized that an orally active small molecule inhibitor of PAI-1 (PAI-039; tiplaxtinin) could affect smooth muscle cell (SMC) attachment and migration in vitro on a vitronectin matrix, and exhibit antiangiogenic activity in vivo.

Methods: In vitro assays were used to assess the mechanism of inhibition of PAI-1 by PAI-039 using wild-type PAI-1 in the presence or absence of vitronectin and wild-type PAI-1 and specific PAI-1 mutants in SMC adhesion and migration assays. An in vivo tumor angiogenesis model was used to assess the effect of PAI-039 administration on neovascularization in a Matrigel implant.

Results: PAI-039 dose-dependently inhibited soluble, but not vitronectin-bound, PAI-1. Cell adhesion assays using PAI-1 mutants unable to bind vitronectin (PAI-1K) or inactivate proteases (PAI-1R) further suggested that PAI-039 inactivated PAI-1 by binding near its vitronectin domain. In a tumor angiogenesis model, PAI-039 treatment of wild-type mice dose-dependently decreased hemoglobin concentration and endothelial cell staining within the Matrigel implant, indicating reduced angiogenesis, but exhibited no in vivo efficacy in PAI-1 null mice.

Conclusions: Administration of an orally active PAI-1 inhibitor prevented angiogenesis in a Matrigel implant. The lack of activity of PAI-039 against wild-type PAI-1 bound to vitronectin and PAI-1K suggests PAI-039 binding near the vitronectin-binding site. Our studies further substantiate a role for PAI-1 in cellular motility and tumor angiogenesis, and suggest for the first time that these effects can be modulated pharmacologically.

MeSH terms

  • Angiogenesis Inhibitors / pharmacology*
  • Angiogenesis Inhibitors / therapeutic use
  • Animals
  • Aorta
  • Cell Adhesion / drug effects
  • Cell Movement / drug effects*
  • Cells, Cultured
  • Collagen
  • Dose-Response Relationship, Drug
  • Drug Combinations
  • Endothelial Cells / drug effects
  • Endothelial Cells / metabolism
  • Humans
  • Indoleacetic Acids / pharmacology*
  • Indoleacetic Acids / therapeutic use
  • Laminin
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Muscle, Smooth, Vascular / cytology
  • Muscle, Smooth, Vascular / drug effects*
  • Muscle, Smooth, Vascular / metabolism
  • Mutation
  • Myocytes, Smooth Muscle / drug effects
  • Myocytes, Smooth Muscle / metabolism
  • Neoplasms / blood supply
  • Neoplasms / drug therapy
  • Neovascularization, Pathologic / metabolism
  • Neovascularization, Pathologic / prevention & control*
  • Plasminogen Activator Inhibitor 1 / genetics
  • Plasminogen Activator Inhibitor 1 / metabolism*
  • Protein Binding
  • Proteoglycans
  • Vitronectin / metabolism

Substances

  • Angiogenesis Inhibitors
  • Drug Combinations
  • Indoleacetic Acids
  • Laminin
  • Plasminogen Activator Inhibitor 1
  • Proteoglycans
  • Vitronectin
  • tiplaxtinin
  • matrigel
  • Collagen