Activation of Ras in the Vascular Endothelium Induces Brain Vascular Malformations and Hemorrhagic Stroke

Cell Rep. 2018 Sep 11;24(11):2869-2882. doi: 10.1016/j.celrep.2018.08.025.

Abstract

Cerebrovascular malformations (CVMs) affect approximately 3% of the population, risking hemorrhagic stroke, seizures, and neurological deficits. Recently Ras mutations have been identified in a majority of brain arterio-venous malformations. We generated an endothelial-specific, inducible HRASV12 mouse model, which results in dilated, proliferative blood vessels in the brain, blood-brain barrier breakdown, intracerebral hemorrhage, and rapid lethality. Organoid morphogenesis models revealed abnormal cessation of proliferation, abnormalities in expression of tip and stalk genes, and a failure to properly form elongating tubes. These defects were influenced by both hyperactive PI-3' kinase signaling and altered TGF-β signaling. Several phenotypic changes predicted by the in vitro morphogenesis analysis were validated in the mouse model. These data provide a model of brain vascular malformations induced by mutant Ras and reveal insights into intersecting molecular mechanisms in the pathogenesis of brain vascular malformations.

Keywords: ALK1; ALK5; ERK; HRAS; PI-3′ kinase; TGF-β; angiogenesis; endothelial; proliferation; vascular malformation.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Activin Receptors, Type II / metabolism
  • Animals
  • Brain / drug effects
  • Brain / metabolism
  • Cells, Cultured
  • Endothelial Cells / drug effects*
  • Endothelial Cells / metabolism*
  • Female
  • Fluorescent Antibody Technique
  • Imidazoles / pharmacology
  • Immunohistochemistry
  • Male
  • Mice
  • Mice, Transgenic
  • Pericytes / cytology
  • Pericytes / metabolism
  • Phosphatidylinositol 3-Kinases / metabolism*
  • Phosphoinositide-3 Kinase Inhibitors
  • Proto-Oncogene Proteins p21(ras) / genetics
  • Proto-Oncogene Proteins p21(ras) / metabolism*
  • Quinoxalines / pharmacology
  • Receptor, Transforming Growth Factor-beta Type I / metabolism
  • Reverse Transcriptase Polymerase Chain Reaction
  • Transforming Growth Factor beta / metabolism
  • Vascular Malformations / metabolism*

Substances

  • 6-(2-tert-butyl-5-(6-methylpyridin-2-yl)-1H-imidazol-4-yl)quinoxaline
  • Imidazoles
  • Phosphoinositide-3 Kinase Inhibitors
  • Quinoxalines
  • Transforming Growth Factor beta
  • Activin Receptors, Type II
  • Acvrl1 protein, mouse
  • Receptor, Transforming Growth Factor-beta Type I
  • Tgfbr1 protein, mouse
  • Hras protein, mouse
  • Proto-Oncogene Proteins p21(ras)