Cardioprotection by S-nitrosation of a cysteine switch on mitochondrial complex I

Nat Med. 2013 Jun;19(6):753-9. doi: 10.1038/nm.3212. Epub 2013 May 26.

Abstract

Oxidative damage from elevated production of reactive oxygen species (ROS) contributes to ischemia-reperfusion injury in myocardial infarction and stroke. The mechanism by which the increase in ROS occurs is not known, and it is unclear how this increase can be prevented. A wide variety of nitric oxide donors and S-nitrosating agents protect the ischemic myocardium from infarction, but the responsible mechanisms are unclear. Here we used a mitochondria-selective S-nitrosating agent, MitoSNO, to determine how mitochondrial S-nitrosation at the reperfusion phase of myocardial infarction is cardioprotective in vivo in mice. We found that protection is due to the S-nitrosation of mitochondrial complex I, which is the entry point for electrons from NADH into the respiratory chain. Reversible S-nitrosation of complex I slows the reactivation of mitochondria during the crucial first minutes of the reperfusion of ischemic tissue, thereby decreasing ROS production, oxidative damage and tissue necrosis. Inhibition of complex I is afforded by the selective S-nitrosation of Cys39 on the ND3 subunit, which becomes susceptible to modification only after ischemia. Our results identify rapid complex I reactivation as a central pathological feature of ischemia-reperfusion injury and show that preventing this reactivation by modification of a cysteine switch is a robust cardioprotective mechanism and hence a rational therapeutic strategy.

Publication types

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

MeSH terms

  • Animals
  • Cysteine / metabolism*
  • Electron Transport Complex I / metabolism*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mitochondria, Heart / metabolism*
  • Mitochondrial Proteins / metabolism*
  • Myocardial Reperfusion Injury / prevention & control*
  • Nitrosation
  • Protein Subunits
  • Rats
  • Reactive Oxygen Species / metabolism

Substances

  • Mitochondrial Proteins
  • Protein Subunits
  • Reactive Oxygen Species
  • Electron Transport Complex I
  • MT-ND3 protein, human
  • Cysteine