Endothelial NADPH oxidase-2 promotes interstitial cardiac fibrosis and diastolic dysfunction through proinflammatory effects and endothelial-mesenchymal transition

J Am Coll Cardiol. 2014 Jun 24;63(24):2734-41. doi: 10.1016/j.jacc.2014.02.572. Epub 2014 Mar 26.

Abstract

Objectives: This study sought to investigate the effect of endothelial dysfunction on the development of cardiac hypertrophy and fibrosis.

Background: Endothelial dysfunction accompanies cardiac hypertrophy and fibrosis, but its contribution to these conditions is unclear. Increased nicotinamide adenine dinucleotide phosphate oxidase-2 (NOX2) activation causes endothelial dysfunction.

Methods: Transgenic mice with endothelial-specific NOX2 overexpression (TG mice) and wild-type littermates received long-term angiotensin II (AngII) infusion (1.1 mg/kg/day, 2 weeks) to induce hypertrophy and fibrosis.

Results: TG mice had systolic hypertension and hypertrophy similar to those seen in wild-type mice but developed greater cardiac fibrosis and evidence of isolated left ventricular diastolic dysfunction (p < 0.05). TG myocardium had more inflammatory cells and VCAM-1-positive vessels than did wild-type myocardium after AngII treatment (both p < 0.05). TG microvascular endothelial cells (ECs) treated with AngII recruited 2-fold more leukocytes than did wild-type ECs in an in vitro adhesion assay (p < 0.05). However, inflammatory cell NOX2 per se was not essential for the profibrotic effects of AngII. TG showed a higher level of endothelial-mesenchymal transition (EMT) than did wild-type mice after AngII infusion. In cultured ECs treated with AngII, NOX2 enhanced EMT as assessed by the relative expression of fibroblast versus endothelial-specific markers.

Conclusions: AngII-induced endothelial NOX2 activation has profound profibrotic effects in the heart in vivo that lead to a diastolic dysfunction phenotype. Endothelial NOX2 enhances EMT and has proinflammatory effects. This may be an important mechanism underlying cardiac fibrosis and diastolic dysfunction during increased renin-angiotensin activation.

Keywords: NADPH (nicotinamide adenine dinucleotide phosphate) oxidase; angiotensin II; diastolic dysfunction; endothelial-mesenchymal transition; endothelium.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cardiomegaly / enzymology*
  • Cardiomegaly / genetics
  • Cardiomegaly / pathology
  • Cells, Cultured
  • Endothelium, Vascular / enzymology*
  • Endothelium, Vascular / pathology
  • Fibrosis / enzymology
  • Fibrosis / genetics
  • Fibrosis / pathology
  • Heart Failure, Diastolic / enzymology
  • Heart Failure, Diastolic / genetics
  • Heart Failure, Diastolic / pathology
  • Humans
  • Inflammation Mediators / physiology*
  • Male
  • Membrane Glycoproteins / genetics
  • Membrane Glycoproteins / physiology*
  • Mesenchymal Stem Cells / enzymology*
  • Mesenchymal Stem Cells / pathology
  • Mice
  • Mice, Transgenic
  • NADPH Oxidase 2
  • NADPH Oxidases / genetics
  • NADPH Oxidases / physiology*
  • Ventricular Dysfunction, Left / enzymology*
  • Ventricular Dysfunction, Left / genetics
  • Ventricular Dysfunction, Left / pathology

Substances

  • Inflammation Mediators
  • Membrane Glycoproteins
  • Cybb protein, mouse
  • NADPH Oxidase 2
  • NADPH Oxidases