Reactive oxygen species trigger Parkin/PINK1 pathway-dependent mitophagy by inducing mitochondrial recruitment of Parkin

J Biol Chem. 2017 Oct 6;292(40):16697-16708. doi: 10.1074/jbc.M117.787739. Epub 2017 Aug 28.

Abstract

Defective mitophagy linked to dysfunction in the proteins Parkin and PTEN-induced putative kinase 1 (PINK1) is implicated in the pathogenesis of Parkinson's disease. Although the mechanism by which Parkin mediates mitophagy in a PINK1-dependent manner is becoming clearer, the triggers for this mitophagy pathway remain elusive. Reactive oxygen species (ROS) have been suggested as such triggers, but this proposal remains controversial because ROS scavengers fail to retard mitophagy. Here we demonstrate that the role of ROS in mitophagy has been underappreciated as a result of the inefficiency of ROS scavengers to control ROS bursts after high-dose treatment with carbonyl cyanide m-chlorophenylhydrazone. Supporting this, combinatorial treatment with N-acetyl-l-cysteine and catalase substantially inhibited the ROS upsurge and PINK1-dependent Parkin translocation to mitochondria in response to carbonyl cyanide m-chlorophenylhydrazone treatment. In addition to the chemical mitophagy inducer, overexpression of voltage-dependent anion channel 1 (VDAC1) induced Parkin translocation to mitochondria, presumably by stimulating ROS generation. Similarly, combined N-acetyl-l-cysteine and catalase treatment also suppressed VDAC1-induced redistribution of Parkin. Alongside these observations, we also found that the elevated protein level of PINK1 was not necessary for Parkin translocation to mitochondria. Thus, our data suggest that ROS may act as a trigger for the induction of Parkin/PINK1-dependent mitophagy. In addition, our study casts doubt on the importance of protein quantity of PINK1 in the recruitment of Parkin to mitochondria.

Keywords: PTEN-induced putative kinase 1 (PINK1); VDAC1; mitochondria; mitophagy; parkin; reactive oxygen species (ROS).

MeSH terms

  • Acetylcysteine / pharmacology
  • Free Radical Scavengers / pharmacology
  • HeLa Cells
  • Humans
  • Mitochondria / genetics
  • Mitochondria / metabolism*
  • Mitophagy / drug effects
  • Mitophagy / physiology*
  • Protein Kinases / genetics
  • Protein Kinases / metabolism*
  • Protein Transport / drug effects
  • Protein Transport / genetics
  • Reactive Oxygen Species / metabolism*
  • Ubiquitin-Protein Ligases / genetics
  • Ubiquitin-Protein Ligases / metabolism*

Substances

  • Free Radical Scavengers
  • Reactive Oxygen Species
  • Ubiquitin-Protein Ligases
  • parkin protein
  • Protein Kinases
  • PTEN-induced putative kinase
  • Acetylcysteine