Upregulation of hypoxia-inducible factor (HIF)-1alpha and HIF-2alpha in leptomeningeal vascular malformations of Sturge-Weber syndrome

J Neuropathol Exp Neurol. 2007 Jan;66(1):86-97. doi: 10.1097/nen.0b013e31802d9011.

Abstract

Cutaneous and leptomeningeal vascular malformations are hallmarks of the Sturge-Weber Syndrome (SWS), resulting in chronic ischemic tissue damage. The mechanisms underlying the pathobiology of these progressive lesions are unknown. Aberrant expression of angiogenic factors has been implicated in the genesis and maintenance of vascular malformations. To assess the role of angiogenesis in SWS vascular lesions we determined the expression of key angiogenic factors by immunohistochemistry and in situ hybridization in 8 SWS patients (age: 8 months to 18 years). We observed increased expression of vascular endothelial growth factor (VEGF), its cognate receptors VEGFR-1, VEGFR-2, and neuropilin (NP)-1 as well as Tie2 in leptomeningeal SWS blood vessels. Intriguingly, these factors are known to be transcriptionally induced by hypoxia-inducible factor (HIF). The HIF system has emerged as the key regulatory system of responses to hypoxia. Immunohistochemical analysis demonstrated markedly elevated nuclear HIF-1alpha and HIF-2alpha protein levels in SWS vessels. Concomitantly, SWS vessels revealed signs of enhanced endothelial cell (EC) turnover as evidenced by increased EC proliferation and apoptosis. Thus, in terms of angiogenesis, vascular malformations in SWS are not static lesions but constitute dynamic structures. Our observation of a dysregulated HIF-alpha expression in SWS vessels are in agreement with recent findings that EC-specific HIF activation provides a setting which supports and sustains angiogenesis and could be of potential use for developing therapeutic strategies to treat these currently incurable lesions.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • Adult
  • Angiogenic Proteins / genetics
  • Angiogenic Proteins / metabolism
  • Basic Helix-Loop-Helix Transcription Factors
  • Blood Vessels / abnormalities
  • Blood Vessels / metabolism*
  • Blood Vessels / ultrastructure
  • Child
  • Child, Preschool
  • Endothelial Cells / metabolism
  • Female
  • Humans
  • Hypoxia-Inducible Factor 1, alpha Subunit / metabolism*
  • Immunohistochemistry / methods
  • In Situ Hybridization / methods
  • In Situ Nick-End Labeling / methods
  • Male
  • Meninges*
  • Microscopy, Electron, Transmission / methods
  • Middle Aged
  • Models, Biological
  • Neuropilins / genetics
  • Neuropilins / metabolism
  • Sturge-Weber Syndrome / metabolism
  • Sturge-Weber Syndrome / pathology*
  • Sturge-Weber Syndrome / physiopathology
  • Transcription Factors / metabolism*
  • Up-Regulation / physiology*
  • Vascular Endothelial Growth Factor A / metabolism

Substances

  • Angiogenic Proteins
  • Basic Helix-Loop-Helix Transcription Factors
  • HIF1A protein, human
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Neuropilins
  • Transcription Factors
  • VEGFA protein, human
  • Vascular Endothelial Growth Factor A
  • endothelial PAS domain-containing protein 1