Cardiac H11 kinase/Hsp22 stimulates oxidative phosphorylation and modulates mitochondrial reactive oxygen species production: Involvement of a nitric oxide-dependent mechanism

Free Radic Biol Med. 2012 Jun;52(11-12):2168-76. doi: 10.1016/j.freeradbiomed.2012.03.001. Epub 2012 Apr 18.

Abstract

H11 kinase/Hsp22 (Hsp22), a small heat shock protein upregulated by ischemia/reperfusion, provides cardioprotection equal to ischemic preconditioning (IPC) through a nitric oxide (NO)-dependent mechanism. A main target of NO-mediated preconditioning is the mitochondria, where NO reduces O₂ consumption and reactive oxygen species (ROS) production during ischemia. Therefore, we tested the hypothesis that Hsp22 overexpression modulates mitochondrial function through an NO-sensitive mechanism. In cardiac mitochondria isolated from transgenic (TG) mice with cardiac-specific overexpression of Hsp22, mitochondrial basal, ADP-dependent, and uncoupled O₂ consumption was increased in the presence of either glucidic or lipidic substrates. This was associated with a decrease in the maximal capabilities of complexes I and III to generate superoxide anion in combination with an inhibition of superoxide anion production by the reverse electron flow. NO synthase expression and NO production were increased in mitochondria from TG mice. Hsp22-induced increase in O₂ consumption was abolished either by pretreatment of TG mice with the NO synthase inhibitor L-N(G)-nitroarginine methyl ester (L-NAME) or in isolated mitochondria by the NO scavenger phenyltetramethylimidazoline-1-oxyl-3-oxide. L-NAME pretreatment also restored the reverse electron flow. After anoxia, mitochondria from TG mice showed a reduction in both oxidative phosphorylation and H₂O₂ production, an effect partially reversed by L-NAME. Taken together, these results demonstrate that Hsp22 overexpression increases the capacity of mitochondria to produce NO, which stimulates oxidative phosphorylation in normoxia and decreases oxidative phosphorylation and reactive oxygen species production after anoxia. Such characteristics replicate those conferred by IPC, thereby placing Hsp22 as a potential tool for prophylactic protection of mitochondrial function during ischemia.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cells, Cultured
  • HSP20 Heat-Shock Proteins / genetics
  • HSP20 Heat-Shock Proteins / metabolism*
  • Heart* / drug effects
  • Heart* / physiopathology
  • Heat-Shock Proteins
  • Ischemia / metabolism
  • Mice
  • Mice, Transgenic
  • Mitochondria, Heart / metabolism*
  • Molecular Chaperones
  • Muscle Proteins / genetics
  • Muscle Proteins / metabolism*
  • NG-Nitroarginine Methyl Ester / administration & dosage
  • Nitric Oxide / metabolism*
  • Organ Specificity
  • Oxidative Phosphorylation / drug effects
  • Oxygen Consumption / drug effects
  • Oxygen Consumption / genetics
  • Reactive Oxygen Species / metabolism
  • Transgenes / genetics

Substances

  • HSP20 Heat-Shock Proteins
  • Heat-Shock Proteins
  • Hspb8 protein, mouse
  • Molecular Chaperones
  • Muscle Proteins
  • Reactive Oxygen Species
  • Nitric Oxide
  • NG-Nitroarginine Methyl Ester