Elevated endothelial Sox2 causes lumen disruption and cerebral arteriovenous malformations

J Clin Invest. 2019 Jun 24;129(8):3121-3133. doi: 10.1172/JCI125965.

Abstract

Lumen integrity in vascularization requires fully differentiated endothelial cells (ECs). Here, we report that endothelial-mesenchymal transitions (EndMTs) emerged in ECs of cerebral arteriovenous malformation (AVMs) and caused disruption of the lumen or lumen disorder. We show that excessive Sry-box 2 (Sox2) signaling was responsible for the EndMTs in cerebral AVMs. EC-specific suppression of Sox2 normalized endothelial differentiation and lumen formation and improved the cerebral AVMs. Epigenetic studies showed that induction of Sox2 altered the cerebral-endothelial transcriptional landscape and identified jumonji domain-containing protein 5 (JMJD5) as a direct target of Sox2. Sox2 interacted with JMJD5 to induce EndMTs in cerebral ECs. Furthermore, we utilized a high-throughput system to identify the β-adrenergic antagonist pronethalol as an inhibitor of Sox2 expression. Treatment with pronethalol stabilized endothelial differentiation and lumen formation, which limited the cerebral AVMs.

Keywords: Cardiovascular disease; Vascular Biology.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Cell Differentiation*
  • Endothelial Cells / metabolism*
  • Endothelial Cells / pathology
  • Ethanolamines / pharmacology
  • Gene Expression Regulation / drug effects
  • Histone Demethylases / biosynthesis
  • Histone Demethylases / genetics
  • Humans
  • Intracranial Arteriovenous Malformations / drug therapy
  • Intracranial Arteriovenous Malformations / genetics
  • Intracranial Arteriovenous Malformations / metabolism*
  • Intracranial Arteriovenous Malformations / pathology
  • Jumonji Domain-Containing Histone Demethylases / biosynthesis
  • Jumonji Domain-Containing Histone Demethylases / genetics
  • Mice
  • Mice, Knockout
  • SOXB1 Transcription Factors / biosynthesis*
  • SOXB1 Transcription Factors / genetics
  • Transcription, Genetic / drug effects

Substances

  • Ethanolamines
  • SOX2 protein, human
  • SOXB1 Transcription Factors
  • Sox2 protein, mouse
  • Histone Demethylases
  • Jmjd5 protein, mouse
  • Jumonji Domain-Containing Histone Demethylases
  • KDM8 protein, human
  • pronethalol