Ischemic preconditioning preserves mitochondrial membrane potential and limits reactive oxygen species production

J Surg Res. 2012 Nov;178(1):8-17. doi: 10.1016/j.jss.2012.05.090. Epub 2012 Jun 17.

Abstract

Background: Mitochondrial superoxide radical (O(2)(•¯)) production increases after cardiac ischemia/reperfusion (IR). Ischemic preconditioning (IPC) preserves mitochondrial function and attenuates O(2)(•¯) production, but the mechanism is unknown. Mitochondrial membrane potential (mΔΨ) is known to affect O(2)(•¯) production; mitochondrial depolarization decreases O(2)(•¯) formation. We examined the relationship between O(2)(•¯) production and mΔΨ during IR and IPC.

Materials/methods: Rat hearts were subjected to Control or IPC. Mitochondria were isolated at end equilibration (End EQ), end ischemia (End I), and end reperfusion (End RP). mΔΨ was measured using a tetraphenylphosphonium electrode. Mitochondrial O(2)(•¯) production was measured by electron paramagnetic resonance using DMPO spin trap. Cytochrome c levels were measured using high-pressure liquid chromatography.

Results: IPC preserved mΔΨ at End I (-156 ± 5 versus -131 ± 6 mV, P < 0.001) and End RP (-168 ± 2 versus -155 ± 2 mV, P < 0.05). At End RP, IPC attenuated O(2)(•¯) production (2527 ± 221 versus 3523 ± 250 AU/mg protein, P < 0.05). IPC preserved cytochrome c levels (351 ± 14 versus 269 ± 16 picomoles/mg protein, P < 0.05) at End RP, and decreased mitochondrial cristae disruption (10% ± 4% versus 33% ± 7%, P < 0.05) and amorphous density formation (18% ± 4% versus 28% ± 1%, P < 0.05).

Conclusion: We conclude that IPC preserves mΔΨ, possibly by limiting disruption of mitochondrial inner membrane. IPC also decreases mitochondrial O(2)(•¯) production and preserves mitochondrial ultrastructure after IR. While it was previously held that slight decreases in mΔΨ decrease O(2)(•¯) production, our results indicate that preservation of mΔΨ is associated with decreased O(2)(•¯) and preservation of cardiac function in IPC. These findings indicate that the mechanism of IPC may not involve mΔΨ depolarization, but rather preservation of mitochondrial electrochemical potential.

Publication types

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

MeSH terms

  • Animals
  • Cytochromes c / metabolism
  • Electron Spin Resonance Spectroscopy
  • Ischemic Preconditioning, Myocardial / methods*
  • Male
  • Membrane Potential, Mitochondrial / physiology*
  • Mitochondria / metabolism
  • Myocardium / metabolism*
  • Oxidative Stress / physiology*
  • Oxygen / metabolism
  • Rats
  • Rats, Sprague-Dawley
  • Reactive Oxygen Species / metabolism*
  • Sarcolemma / metabolism
  • Superoxides / metabolism

Substances

  • Reactive Oxygen Species
  • Superoxides
  • Cytochromes c
  • Oxygen