Endoglin prevents vascular malformation by regulating flow-induced cell migration and specification through VEGFR2 signalling

Nat Cell Biol. 2017 Jun;19(6):639-652. doi: 10.1038/ncb3534. Epub 2017 May 22.

Abstract

Loss-of-function (LOF) mutations in the endothelial cell (EC)-enriched gene endoglin (ENG) cause the human disease hereditary haemorrhagic telangiectasia-1, characterized by vascular malformations promoted by vascular endothelial growth factor A (VEGFA). How ENG deficiency alters EC behaviour to trigger these anomalies is not understood. Mosaic ENG deletion in the postnatal mouse rendered Eng LOF ECs insensitive to flow-mediated venous to arterial migration. Eng LOF ECs retained within arterioles acquired venous characteristics and secondary ENG-independent proliferation resulting in arteriovenous malformation (AVM). Analysis following simultaneous Eng LOF and overexpression (OE) revealed that ENG OE ECs dominate tip-cell positions and home preferentially to arteries. ENG knockdown altered VEGFA-mediated VEGFR2 kinetics and promoted AKT signalling. Blockage of PI(3)K/AKT partly normalized flow-directed migration of ENG LOF ECs in vitro and reduced the severity of AVM in vivo. This demonstrates the requirement of ENG in flow-mediated migration and modulation of VEGFR2 signalling in vascular patterning.

Publication types

  • Video-Audio Media

MeSH terms

  • Animals
  • Arteriovenous Malformations / genetics
  • Arteriovenous Malformations / metabolism
  • Arteriovenous Malformations / pathology
  • Arteriovenous Malformations / prevention & control*
  • Cell Lineage
  • Cell Proliferation
  • Cells, Cultured
  • Disease Models, Animal
  • Endoglin / deficiency
  • Endoglin / genetics
  • Endoglin / metabolism*
  • Endothelial Cells / metabolism*
  • Endothelial Cells / pathology
  • Genetic Predisposition to Disease
  • Humans
  • Kinetics
  • Mice, Knockout
  • Neovascularization, Pathologic*
  • Neovascularization, Physiologic*
  • Phenotype
  • Phosphatidylinositol 3-Kinase / metabolism
  • Proto-Oncogene Proteins c-akt / metabolism
  • RNA Interference
  • Signal Transduction*
  • Stress, Mechanical
  • Telangiectasia, Hereditary Hemorrhagic / genetics
  • Telangiectasia, Hereditary Hemorrhagic / metabolism
  • Telangiectasia, Hereditary Hemorrhagic / pathology
  • Telangiectasia, Hereditary Hemorrhagic / prevention & control*
  • Tissue Culture Techniques
  • Transfection
  • Vascular Endothelial Growth Factor A / metabolism
  • Vascular Endothelial Growth Factor Receptor-2 / genetics
  • Vascular Endothelial Growth Factor Receptor-2 / metabolism*

Substances

  • Endoglin
  • Eng protein, mouse
  • Vascular Endothelial Growth Factor A
  • vascular endothelial growth factor A, mouse
  • Phosphatidylinositol 3-Kinase
  • Kdr protein, mouse
  • Vascular Endothelial Growth Factor Receptor-2
  • Proto-Oncogene Proteins c-akt