Mitochondrial thioredoxin reductase is essential for early postischemic myocardial protection

Circulation. 2011 Dec 20;124(25):2892-902. doi: 10.1161/CIRCULATIONAHA.111.059253. Epub 2011 Dec 5.

Abstract

Background: Excessive formation of reactive oxygen species contributes to tissue injury and functional deterioration after myocardial ischemia/reperfusion. Especially, mitochondrial reactive oxygen species are capable of opening the mitochondrial permeability transition pore, a harmful event in cardiac ischemia/reperfusion. Thioredoxins are key players in the cardiac defense against oxidative stress. Mutations in the mitochondrial thioredoxin reductase (thioredoxin reductase-2, Txnrd2) gene have been recently identified to cause dilated cardiomyopathy in patients. Here, we investigated whether mitochondrial thioredoxin reductase is protective against myocardial ischemia/reperfusion injury.

Methods and results: In mice, α-MHC-restricted Cre-mediated Txnrd2 deficiency, induced by tamoxifen (Txnrd2-/-ic), aggravated systolic dysfunction and cardiomyocyte cell death after ischemia (90 minutes) and reperfusion (24 hours). Txnrd2-/-ic was accompanied by a loss of mitochondrial integrity and function, which was resolved on pretreatment with the reactive oxygen species scavenger N-acetylcysteine and the mitochondrial permeability transition pore blocker cyclosporin A. Likewise, Txnrd2 deletion in embryonic endothelial precursor cells and embryonic stem cell-derived cardiomyocytes, as well as introduction of Txnrd2-shRNA into adult HL-1 cardiomyocytes, increased cell death on hypoxia and reoxygenation, unless N-acetylcysteine was coadministered.

Conclusions: We report that Txnrd2 exerts a crucial function during postischemic reperfusion via thiol regeneration. The efficacy of cyclosporin A in cardiac Txnrd2 deficiency may indicate a role for Txnrd2 in reducing mitochondrial reactive oxygen species, thereby preventing opening of the mitochondrial permeability transition pore.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acetylcysteine / pharmacology
  • Animals
  • Cell Death / drug effects
  • Cell Death / physiology
  • Cells, Cultured
  • Cyclosporine / pharmacology
  • Embryonic Stem Cells / cytology
  • Endothelial Cells / cytology
  • Enzyme Inhibitors / pharmacology
  • Free Radical Scavengers / pharmacology
  • Gene Expression Regulation, Enzymologic / physiology
  • Hematopoietic Stem Cells / cytology
  • Mice
  • Mice, Knockout
  • Mitochondria / enzymology*
  • Myocardial Reperfusion Injury / drug therapy
  • Myocardial Reperfusion Injury / metabolism*
  • Myocardial Reperfusion Injury / pathology
  • Myocardial Reperfusion Injury / physiopathology
  • Myocytes, Cardiac / cytology
  • Oxidative Stress / drug effects
  • Oxidative Stress / physiology*
  • Sulfhydryl Compounds / metabolism*
  • Thioredoxin Reductase 1 / genetics
  • Thioredoxin Reductase 1 / metabolism
  • Thioredoxin Reductase 2 / genetics
  • Thioredoxin Reductase 2 / metabolism*

Substances

  • Enzyme Inhibitors
  • Free Radical Scavengers
  • Sulfhydryl Compounds
  • Cyclosporine
  • Thioredoxin Reductase 1
  • Thioredoxin Reductase 2
  • Txnrd1 protein, mouse
  • Txnrd2 protein, mouse
  • Acetylcysteine