Modulation of mitochondrial dysfunction-related oxidative stress in fibroblasts of patients with Leigh syndrome by inhibition of prooxidative p66Shc pathway

Mitochondrion. 2017 Nov:37:62-79. doi: 10.1016/j.mito.2017.07.002. Epub 2017 Jul 21.

Abstract

The mitochondrial respiratory chain, and in particular, complex I, is a major source of reactive oxygen species (ROS) in cells. Elevated levels of ROS are associated with an imbalance between the rate of ROS formation and the capacity of the antioxidant defense system. Increased ROS production may lead to oxidation of DNA, lipids and proteins and thus can affect fundamental cellular processes. The aim of this study was to investigate the magnitude of intracellular oxidative stress in fibroblasts of patients with Leigh syndrome with defined mutations in complex I. Moreover, we hypothesized that activation of the p66Shc protein (phosphorylation of p66Shc at Ser36 by PKCβ), being part of the oxidative stress response pathway, is partially responsible for the increased ROS production in cells with dysfunctional complex I. Characterization of bioenergetic parameters and ROS production showed that the cellular model of Leigh syndrome is described by increased intracellular oxidative stress and oxidative damage to DNA and proteins, which correlate with increased p66Shc phosphorylation at Ser36. Treatment of patients' fibroblasts with hispidin (an inhibitor of the protein kinase PKCβ), in addition to decreasing ROS production and intracellular oxidative stress, resulted in restoration of complex I activity.

Keywords: Complex I deficiency; Hispidin; Leigh syndrome; Mitochondrial dysfunction; Reactive oxygen species.

MeSH terms

  • Cells, Cultured
  • Electron Transport Complex I / genetics
  • Enzyme Inhibitors / metabolism
  • Fibroblasts / metabolism*
  • Humans
  • Leigh Disease / physiopathology*
  • Mitochondria / metabolism*
  • Mutation
  • Oxidative Stress*
  • Pyrones / metabolism
  • Reactive Oxygen Species / metabolism*
  • Src Homology 2 Domain-Containing, Transforming Protein 1 / antagonists & inhibitors*
  • Src Homology 2 Domain-Containing, Transforming Protein 1 / metabolism*

Substances

  • Enzyme Inhibitors
  • Pyrones
  • Reactive Oxygen Species
  • SHC1 protein, human
  • Src Homology 2 Domain-Containing, Transforming Protein 1
  • Electron Transport Complex I
  • hispidin