Human disease modeling reveals integrated transcriptional and epigenetic mechanisms of NOTCH1 haploinsufficiency

Cell. 2015 Mar 12;160(6):1072-86. doi: 10.1016/j.cell.2015.02.035.

Abstract

The mechanisms by which transcription factor haploinsufficiency alters the epigenetic and transcriptional landscape in human cells to cause disease are unknown. Here, we utilized human induced pluripotent stem cell (iPSC)-derived endothelial cells (ECs) to show that heterozygous nonsense mutations in NOTCH1 that cause aortic valve calcification disrupt the epigenetic architecture, resulting in derepression of latent pro-osteogenic and -inflammatory gene networks. Hemodynamic shear stress, which protects valves from calcification in vivo, activated anti-osteogenic and anti-inflammatory networks in NOTCH1(+/+), but not NOTCH1(+/-), iPSC-derived ECs. NOTCH1 haploinsufficiency altered H3K27ac at NOTCH1-bound enhancers, dysregulating downstream transcription of more than 1,000 genes involved in osteogenesis, inflammation, and oxidative stress. Computational predictions of the disrupted NOTCH1-dependent gene network revealed regulatory nodes that, when modulated, restored the network toward the NOTCH1(+/+) state. Our results highlight how alterations in transcription factor dosage affect gene networks leading to human disease and reveal nodes for potential therapeutic intervention.

Publication types

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

MeSH terms

  • Endothelial Cells / metabolism
  • Epigenesis, Genetic*
  • Female
  • Gene Regulatory Networks*
  • Haploinsufficiency
  • Histone Code
  • Humans
  • Induced Pluripotent Stem Cells / metabolism
  • Inflammation / metabolism
  • Male
  • Osteogenesis
  • Pedigree
  • Receptor, Notch1 / genetics*
  • Receptor, Notch1 / metabolism
  • Stress, Mechanical
  • Transcription, Genetic

Substances

  • NOTCH1 protein, human
  • Receptor, Notch1