Regulation of mitochondrial oxidative stress by β-arrestins in cultured human cardiac fibroblasts

Dis Model Mech. 2015 Dec;8(12):1579-89. doi: 10.1242/dmm.019968. Epub 2015 Oct 8.

Abstract

Oxidative stress in cardiac fibroblasts (CFs) promotes transformation to myofibroblasts and collagen synthesis leading to myocardial fibrosis, a precursor to heart failure (HF). NADPH oxidase 4 (Nox4) is a major source of cardiac reactive oxygen species (ROS); however, mechanisms of Nox4 regulation are unclear. β-arrestins are scaffold proteins that signal in G-protein-dependent and -independent pathways; for example, in ERK activation. We hypothesize that β-arrestins regulate oxidative stress in a Nox4-dependent manner and increase fibrosis in HF. CFs were isolated from normal and failing adult human left ventricles. Mitochondrial ROS/superoxide production was quantitated using MitoSox. β-arrestin and Nox4 expressions were manipulated using adenoviral overexpression or short interfering RNA (siRNA)-mediated knockdown. Mitochondrial oxidative stress and Nox4 expression in CFs were significantly increased in HF. Nox4 knockdown resulted in inhibition of mitochondrial superoxide production and decreased basal and TGF-β-stimulated collagen and α-SMA expression. CF β-arrestin expression was upregulated fourfold in HF. β-arrestin knockdown in failing CFs decreased ROS and Nox4 expression by 50%. β-arrestin overexpression in normal CFs increased mitochondrial superoxide production twofold. These effects were prevented by inhibition of either Nox or ERK. Upregulation of Nox4 seemed to be a primary mechanism for increased ROS production in failing CFs, which stimulates collagen deposition. β-arrestin expression was upregulated in HF and plays an important and newly identified role in regulating mitochondrial superoxide production via Nox4. The mechanism for this effect seems to be ERK-mediated. Targeted inhibition of β-arrestins in CFs might decrease oxidative stress as well as pathological cardiac fibrosis.

Keywords: Cardiac fibroblast; Collagen; Heart failure; Myocardial fibrosis; NADPH oxidase; Oxidative stress; β-arrestin.

Publication types

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

MeSH terms

  • Arrestins / metabolism*
  • Cell Line, Transformed
  • Cells, Cultured
  • Collagen / biosynthesis
  • Extracellular Signal-Regulated MAP Kinases / metabolism
  • Fibroblasts / drug effects
  • Fibroblasts / enzymology
  • Fibroblasts / metabolism*
  • Heart Failure / pathology
  • Humans
  • Mitochondria / drug effects
  • Mitochondria / metabolism*
  • Myocardium / pathology*
  • Myofibroblasts / drug effects
  • Myofibroblasts / metabolism
  • NADPH Oxidase 4
  • NADPH Oxidases / metabolism
  • Oxidative Stress* / drug effects
  • Superoxides / metabolism
  • Transforming Growth Factor beta / pharmacology
  • Up-Regulation / drug effects
  • beta-Arrestins

Substances

  • Arrestins
  • Transforming Growth Factor beta
  • beta-Arrestins
  • Superoxides
  • Collagen
  • NADPH Oxidase 4
  • NADPH Oxidases
  • NOX4 protein, human
  • Extracellular Signal-Regulated MAP Kinases