Hypoxia and upregulation of hypoxia-inducible factor 1{alpha} stimulate venous thrombus recanalization

Arterioscler Thromb Vasc Biol. 2010 Dec;30(12):2443-51. doi: 10.1161/ATVBAHA.110.215038. Epub 2010 Oct 7.

Abstract

Objective: Angiogenic factors are expressed within thrombus during resolution, but the primary stimulus for neovascularization is unknown. Our aims were to determine whether (1) hypoxia and hypoxia-inducible factor 1α (HIF1α) are induced in resolving thrombus, (2) this stimulates angiogenic factor production, and (3) upregulating HIF1α enhances thrombus resolution and vein recanalization.

Methods and results: Oxygen tension in the thrombus was negatively correlated with HIF1α levels (Spearman correlation [RS] = -0.77, P<0.0001), whereas HIF1α levels positively correlated with vascular endothelial growth factor (VEGF) expression (Pearson correlation [R] = 0.85, P<0.0005), during resolution in a murine model. HIF1α (P<0.005), VEGF (P<0.005), and VEGF receptor 1 (VEGFR1) (P<0.05) expression was 2-fold greater in the thrombus of mice treated with the prolyl hydroxylase domain inhibitor L-mimosine compared with controls. The levels of 13 other HIF1-mediated angiogenic factors were also increased. Thrombus weight (P<0.001) and volume (P<0.05) were reduced by a third in l-mimosine-treated mice compared with controls, whereas vein recanalization (P<0.005) and thrombus neovascularization (P<0.001) were 2-fold greater, and this was associated with increased inflammatory cell content.

Conclusions: Hypoxia and HIF1α are induced in the naturally resolving thrombus and correlate with increased angiogenic factor expression. Upregulation of HIF1α enhances thrombus resolution and vein recanalization. HIF1α may represent a novel target for treatments that promote resolution and recanalization and reduce the incidence of post-thrombotic syndrome.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Hypoxia*
  • Cytokines / metabolism
  • Disease Models, Animal
  • Enzyme Inhibitors / pharmacology
  • Hypoxia-Inducible Factor 1, alpha Subunit / metabolism*
  • Macrophages / immunology
  • Male
  • Mice
  • Mice, Inbred BALB C
  • Mimosine / pharmacology
  • Neovascularization, Physiologic* / drug effects
  • Neutrophil Infiltration
  • Neutrophils / immunology
  • Oxygen / metabolism*
  • Procollagen-Proline Dioxygenase / antagonists & inhibitors
  • Procollagen-Proline Dioxygenase / metabolism
  • Time Factors
  • Up-Regulation
  • Vascular Endothelial Growth Factor A / metabolism
  • Vascular Endothelial Growth Factor Receptor-1 / metabolism
  • Vena Cava, Inferior / drug effects
  • Vena Cava, Inferior / immunology
  • Vena Cava, Inferior / metabolism*
  • Venous Thrombosis / immunology
  • Venous Thrombosis / metabolism*
  • Venous Thrombosis / physiopathology

Substances

  • Cytokines
  • Enzyme Inhibitors
  • Hif1a protein, mouse
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • VEGFA protein, human
  • Vascular Endothelial Growth Factor A
  • Mimosine
  • Procollagen-Proline Dioxygenase
  • Flt1 protein, mouse
  • Vascular Endothelial Growth Factor Receptor-1
  • Oxygen