Endothelial Nox1 oxidase assembly in human pulmonary arterial hypertension; driver of Gremlin1-mediated proliferation

Clin Sci (Lond). 2017 Jul 16;131(15):2019-2035. doi: 10.1042/CS20160812. Print 2017 Aug 1.

Abstract

Pulmonary arterial hypertension (PAH) is a rapidly degenerating and devastating disease of increased pulmonary vessel resistance leading to right heart failure. Palliative modalities remain limited despite recent endeavors to investigate the mechanisms underlying increased pulmonary vascular resistance (PVR), i.e. aberrant vascular remodeling and occlusion. However, little is known of the molecular mechanisms responsible for endothelial proliferation, a root cause of PAH-associated vascular remodeling. Lung tissue specimens from PAH and non-PAH patients and hypoxia-exposed human pulmonary artery endothelial cells (ECs) (HPAEC) were assessed for mRNA and protein expression. Reactive oxygen species (ROS) were measured using cytochrome c and Amplex Red assays. Findings demonstrate for the first time an up-regulation of NADPH oxidase 1 (Nox1) at the transcript and protein level in resistance vessels from PAH compared with non-PAH patients. This coincided with an increase in ROS production and expression of bone morphogenetic protein (BMP) antagonist Gremlin1 (Grem1). In HPAEC, hypoxia induced Nox1 subunit expression, assembly, and oxidase activity leading to elevation in sonic hedgehog (SHH) and Grem1 expression. Nox1 gene silencing abrogated this cascade. Moreover, loss of either Nox1, SHH or Grem1 attenuated hypoxia-induced EC proliferation. Together, these data support a Nox1-SHH-Grem1 signaling axis in pulmonary vascular endothelium that is likely to contribute to pathophysiological endothelial proliferation and the progression of PAH. These findings also support targeting of Nox1 as a viable therapeutic option to combat PAH.

Keywords: NADPH oxidase; endothelial cells; gremlin1; hedgehog; pulmonary hypertension; reactive oxygen species.

MeSH terms

  • Adult
  • Aged
  • Cell Proliferation*
  • Endothelial Cells / cytology
  • Endothelial Cells / metabolism
  • Female
  • Hedgehog Proteins / genetics
  • Hedgehog Proteins / metabolism
  • Humans
  • Hypertension, Pulmonary / enzymology*
  • Hypertension, Pulmonary / genetics
  • Hypertension, Pulmonary / metabolism
  • Hypertension, Pulmonary / physiopathology
  • Intercellular Signaling Peptides and Proteins / genetics
  • Intercellular Signaling Peptides and Proteins / metabolism*
  • Male
  • Middle Aged
  • NADPH Oxidase 1
  • NADPH Oxidases / genetics
  • NADPH Oxidases / metabolism*
  • Pulmonary Artery / enzymology
  • Reactive Oxygen Species / metabolism
  • Signal Transduction

Substances

  • GREM1 protein, human
  • Hedgehog Proteins
  • Intercellular Signaling Peptides and Proteins
  • Reactive Oxygen Species
  • SHH protein, human
  • NADPH Oxidase 1
  • NADPH Oxidases
  • NOX1 protein, human