Testosterone induces cytoprotection by activating ATP-sensitive K+ channels in the cardiac mitochondrial inner membrane

Circulation. 2004 Nov 9;110(19):3100-7. doi: 10.1161/01.CIR.0000146900.84943.E0. Epub 2004 Nov 1.

Abstract

Background: Whereas in the past, androgens were mainly believed to exert adverse effects on the cardiovascular system, recent experimental data postulate a benefit of testosterone for recovery of myocardial function after ischemia/reperfusion injury. Thus, we examined whether testosterone might improve myocardial tolerance to ischemia due to activation of mitochondrial (mitoK(ATP)) and/or sarcoplasmatic (sarcK(ATP)) K(ATP) channels.

Methods and results: In a cellular model of ischemia, testosterone significantly decreased the rate of ischemia-induced death of cardiomyocytes that could be prevented by 5-hydroxydecainoic acid but was unaffected by the sarcK(ATP) blocker HMR1098 and the testosterone receptor antagonist flutamide. To index mitoK(ATP), mitochondrial flavoprotein fluorescence was measured. Testosterone induced a highly significant increase in mitochondrial flavoprotein fluorescence in intact myocytes and isolated mitoplasts that could be abolished by 5-hydroxydecainoic acid. Testosterone-mediated flavoprotein oxidation of mitoplasts was K+ dependent and ATP sensitive. In mitoplast-attached single-channel recordings, testosterone directly activated an ATP-sensitive K+ channel of the inner mitochondrial membrane. Addition of the K(ATP) channel opener diazoxide and pinacidil to the cytosolic solution activated the ATP-sensitive K+ current comparable to testosterone, whereas 5-hydroxydecainoic acid and glibenclamide inhibited the testosterone-induced current. Patch-clamp experiments of intact myocytes in whole-cell configuration did not demonstrate any effect of testosterone on sarcK(ATP) channels.

Conclusions: Our results provide direct evidence for the existence of cardiac mitoK(ATP) and a link between testosterone-induced cytoprotection and activation of mitoK(ATP). Endogenous testosterone might play a more important role in recovery after myocardial infarction than is currently assumed.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Triphosphate / pharmacology
  • Androgen Receptor Antagonists
  • Androstenedione / pharmacology
  • Animals
  • Biological Transport, Active / drug effects
  • Cells, Cultured / drug effects
  • Cells, Cultured / metabolism
  • Diazoxide / pharmacology
  • Flutamide / pharmacology
  • G Protein-Coupled Inwardly-Rectifying Potassium Channels
  • Ion Transport / drug effects
  • Male
  • Membrane Proteins / drug effects*
  • Membrane Proteins / metabolism
  • Mitochondria, Heart / drug effects*
  • Mitochondria, Heart / metabolism
  • Mitochondrial Membrane Transport Proteins / drug effects*
  • Mitochondrial Membrane Transport Proteins / metabolism
  • Myocardial Ischemia / drug therapy
  • Myocardial Ischemia / pathology
  • Myocardial Ischemia / prevention & control*
  • Myocytes, Cardiac / drug effects*
  • Myocytes, Cardiac / metabolism
  • Patch-Clamp Techniques
  • Pinacidil / pharmacology
  • Potassium / metabolism
  • Potassium Channels / drug effects
  • Potassium Channels / metabolism
  • Potassium Channels, Inwardly Rectifying / drug effects
  • Potassium Channels, Inwardly Rectifying / metabolism
  • Rats
  • Rats, Sprague-Dawley
  • Sarcoplasmic Reticulum / drug effects
  • Sarcoplasmic Reticulum / metabolism
  • Testosterone / pharmacology*

Substances

  • Androgen Receptor Antagonists
  • G Protein-Coupled Inwardly-Rectifying Potassium Channels
  • KCNJ5 protein, human
  • Membrane Proteins
  • Mitochondrial Membrane Transport Proteins
  • Potassium Channels
  • Potassium Channels, Inwardly Rectifying
  • mitochondrial K(ATP) channel
  • Testosterone
  • Androstenedione
  • Flutamide
  • Pinacidil
  • Adenosine Triphosphate
  • Diazoxide
  • Potassium