Loss of Estrogen-Related Receptor Alpha Facilitates Angiogenesis in Endothelial Cells

Mol Cell Biol. 2019 Feb 15;39(5):e00411-18. doi: 10.1128/MCB.00411-18. Print 2019 Mar 1.

Abstract

Estrogen-related receptors (ERRs) have emerged as major metabolic regulators in various tissues. However, their expression and function in the vasculature remains unknown. Here, we report the transcriptional program and cellular function of ERRα in endothelial cells (ECs), a cell type with a multifaceted role in vasculature. Of the three ERR subtypes, ECs exclusively express ERRα. Gene expression profiling of ECs lacking ERRα revealed that ERRα predominantly acts as a transcriptional repressor, targeting genes linked with angiogenesis, cell migration, and cell adhesion. ERRα-deficient ECs exhibit decreased proliferation but increased migration and tube formation. ERRα depletion increased basal as well as vascular endothelial growth factor A (VEGFA)- and ANG1/2-stimulated angiogenic sprouting in endothelial spheroids. Moreover, retinal angiogenesis is enhanced in ERRα knockout mice compared to that in wild-type mice. Surprisingly, ERRα is dispensable for the regulation of its classic targets, such as metabolism, mitochondrial biogenesis, and cellular respiration in the ECs. ERRα is enriched at the promoters of angiogenic, migratory, and cell adhesion genes. Further, VEGFA increased ERRα recruitment to angiogenesis-associated genes and simultaneously decreased their expression. Despite increasing its gene occupancy, proangiogenic stimuli decrease ERRα expression in ECs. Our work shows that endothelial ERRα plays a repressive role in angiogenesis and potentially fine-tunes growth factor-mediated angiogenesis.

Keywords: angiogenesis; endothelial cell; estrogen-related receptors; nuclear receptor; regulation of gene expression.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Angiogenesis Inducing Agents / metabolism
  • Animals
  • Cell Adhesion / genetics
  • Cell Movement / genetics
  • ERRalpha Estrogen-Related Receptor
  • Endothelial Cells / metabolism*
  • Energy Metabolism / physiology
  • Gene Expression Regulation, Neoplastic / genetics
  • Human Umbilical Vein Endothelial Cells
  • Humans
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Neovascularization, Physiologic / physiology
  • Organelle Biogenesis
  • Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha / metabolism
  • Receptors, Estrogen / genetics*
  • Receptors, Estrogen / metabolism*
  • Signal Transduction / physiology
  • Transcription Factors / metabolism
  • Vascular Endothelial Growth Factor A / metabolism

Substances

  • Angiogenesis Inducing Agents
  • Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha
  • Receptors, Estrogen
  • Transcription Factors
  • Vascular Endothelial Growth Factor A