Bevacizumab promotes venous thromboembolism through the induction of PAI-1 in a mouse xenograft model of human lung carcinoma

Mol Cancer. 2015 Jul 29:14:140. doi: 10.1186/s12943-015-0418-x.

Abstract

Background: An increased incidence of venous thromboembolism (VTE) is associated with anti-vascular endothelial growth factor (VEGF) treatment in cancer. However, the mechanism underlying this effect remains elusive. In this study, we examined the effect of bevacizumab, a humanized monoclonal antibody against VEGF-A, on VTE in a murine xenograft A549 cell tumor model.

Methods: Inferior vena cava stenosis model and FeCl3-induced saphenous vein thrombosis model were performed in a mouse xenograft models of human lung adenocarcinoma.

Results: We found that treatment with bevacizumab significantly increased the thrombotic response to inferior vena cava obstruction and femoral vein injury. Plasminogen activator inhibitor (PAI-1) expression in tumors, plasma, and thrombi was significantly increased by bevacizumab. However, bevacizumab did not enhance VTE in PAI-1-deficient mice, suggesting that PAI-1 is a major mediator of bevacizumab's prothrombotic effect. VEGF inhibited expression of PAI-1 by A549 cells, and this effect was neutralized by bevacizumab, suggesting that bevacizumab increases PAI-1 expression in vivo by blocking the inhibitory effect of VEGF on PAI-1 expression by tumor cells. Pharmacological inhibition of PAI-1 with PAI-039 blocked bevacizumab-induced venous thrombosis.

Conclusion: Collectively, these findings indicate that PAI-1 plays a role in VTE associated with antiangiogenic therapy and the inhibition of PAI-1 shows efficacy as a therapeutic strategy for the prevention of bevacizumab-associated VTE.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenocarcinoma / complications
  • Adenocarcinoma / drug therapy
  • Adenocarcinoma / pathology*
  • Adenocarcinoma of Lung
  • Animals
  • Bevacizumab / administration & dosage
  • Bevacizumab / adverse effects*
  • Carcinoma, Non-Small-Cell Lung / complications
  • Carcinoma, Non-Small-Cell Lung / drug therapy
  • Carcinoma, Non-Small-Cell Lung / pathology*
  • Cell Line, Tumor
  • Disease Models, Animal
  • Gene Expression Regulation, Neoplastic / drug effects
  • Humans
  • Lung Neoplasms / complications
  • Lung Neoplasms / drug therapy
  • Lung Neoplasms / pathology*
  • Mice
  • Plasminogen Activator Inhibitor 1 / biosynthesis*
  • Plasminogen Activator Inhibitor 1 / genetics
  • Vascular Endothelial Growth Factor A / antagonists & inhibitors
  • Venous Thromboembolism / chemically induced
  • Venous Thromboembolism / etiology
  • Venous Thromboembolism / pathology*
  • Xenograft Model Antitumor Assays

Substances

  • Plasminogen Activator Inhibitor 1
  • SERPINE1 protein, human
  • VEGFA protein, human
  • Vascular Endothelial Growth Factor A
  • Bevacizumab