Notch3 signaling promotes the development of pulmonary arterial hypertension

Nat Med. 2009 Nov;15(11):1289-97. doi: 10.1038/nm.2021. Epub 2009 Oct 25.

Abstract

Notch receptor signaling is implicated in controlling smooth muscle cell proliferation and in maintaining smooth muscle cells in an undifferentiated state. Pulmonary arterial hypertension is characterized by excessive vascular resistance, smooth muscle cell proliferation in small pulmonary arteries, leading to elevation of pulmonary vascular resistance, right ventricular failure and death. Here we show that human pulmonary hypertension is characterized by overexpression of NOTCH3 in small pulmonary artery smooth muscle cells and that the severity of disease in humans and rodents correlates with the amount of NOTCH3 protein in the lung. We further show that mice with homozygous deletion of Notch3 do not develop pulmonary hypertension in response to hypoxic stimulation and that pulmonary hypertension can be successfully treated in mice by administration of N-[N-(3,5-difluorophenacetyl)-L-alanyl]-S-phenylglycine t-butyl ester (DAPT), a gamma-secretase inhibitor that blocks activation of Notch3 in smooth muscle cells. We show a mechanistic link from NOTCH3 receptor signaling through the Hairy and enhancer of Split-5 (HES-5) protein to smooth muscle cell proliferation and a shift to an undifferentiated smooth muscle cell phenotype. These results suggest that the NOTCH3-HES-5 signaling pathway is crucial for the development of pulmonary arterial hypertension and provide a target pathway for therapeutic intervention.

Publication types

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

MeSH terms

  • Animals
  • Basic Helix-Loop-Helix Transcription Factors / metabolism
  • Cell Proliferation / drug effects
  • Dipeptides / pharmacology
  • Dipeptides / therapeutic use
  • Disease Models, Animal
  • Enzyme Inhibitors / pharmacology
  • Enzyme Inhibitors / therapeutic use
  • Gene Expression Regulation / drug effects
  • Gene Expression Regulation / physiology
  • Humans
  • Hypertension, Pulmonary / drug therapy
  • Hypertension, Pulmonary / metabolism*
  • Hypertension, Pulmonary / pathology*
  • Hypoxia / drug therapy
  • Hypoxia / physiopathology
  • In Vitro Techniques
  • Lung / metabolism
  • Lung / pathology
  • Mice
  • Mice, Knockout
  • Microscopy, Electron, Transmission / methods
  • Myocytes, Smooth Muscle
  • Pulmonary Artery / metabolism
  • Pulmonary Artery / pathology
  • Pulmonary Artery / physiopathology*
  • Pulmonary Artery / ultrastructure
  • RNA, Messenger / metabolism
  • Rats
  • Receptor, Notch3
  • Receptors, Notch / deficiency
  • Receptors, Notch / metabolism*
  • Repressor Proteins / metabolism
  • Signal Transduction / drug effects
  • Signal Transduction / genetics
  • Signal Transduction / physiology*
  • Time Factors

Substances

  • Basic Helix-Loop-Helix Transcription Factors
  • Dipeptides
  • Enzyme Inhibitors
  • N-(N-(3,5-difluorophenacetyl)alanyl)phenylglycine tert-butyl ester
  • NOTCH3 protein, human
  • RNA, Messenger
  • Receptor, Notch3
  • Receptors, Notch
  • Repressor Proteins
  • HES5 protein, human