Nitrative inactivation of thioredoxin-1 and its role in postischemic myocardial apoptosis

Circulation. 2006 Sep 26;114(13):1395-402. doi: 10.1161/CIRCULATIONAHA.106.625061. Epub 2006 Sep 11.

Abstract

Background: Intracellular proteins involved in oxidative stress and apoptosis are nitrated in diseased tissues but not in normal tissues; definitive evidence to support a causative link between a specific protein that is nitratively modified with tissue injury in a specific disease is limited, however. The aims of the present study were to determine whether thioredoxin (Trx), a novel antioxidant and antiapoptotic molecule, is susceptible to nitrative inactivation and to establish a causative link between Trx nitration and postischemic myocardial apoptosis.

Methods and results: In vitro exposure of human Trx-1 to 3-morpholinosydnonimine resulted in significant Trx-1 nitration and almost abolished Trx-1 activity. 3-morpholinosydnonimine-induced nitrative Trx-1 inactivation was completely blocked by MnTE-2-PyP(5+) (a superoxide dismutase mimetic) and markedly attenuated by PTIO (a nitric oxide scavenger). Administration of either reduced or oxidized Trx-1 in vivo attenuated myocardial ischemia/reperfusion injury (>50% reduction in apoptosis and infarct size, P<0.01). However, administration of nitrated Trx-1 failed to exert a cardioprotective effect. In cardiac tissues obtained from ischemic/reperfused heart, significant Trx-1 nitration was detected, Trx activity was markedly inhibited, Trx-1/ASK1 (apoptosis signal-regulating kinase-1) complex formation was abolished, and apoptosis signal-regulating kinase-1 activity was increased. Treatment with either FP15 (a peroxynitrite decomposition catalyst) or MnTE-2-PyP(5+) 10 minutes before reperfusion blocked nitrative Trx inactivation, attenuated apoptosis signal-regulating kinase-1 activation, and reduced postischemic myocardial apoptosis.

Conclusions: These results strongly suggest that nitrative inactivation of Trx plays a proapoptotic role under those pathological conditions in which production of reactive nitrogen species is increased and that antinitrating treatment may have therapeutic value in those diseases, such as myocardial ischemia/reperfusion, in which pathological apoptosis is increased.

Publication types

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

MeSH terms

  • Amino Acid Substitution
  • Animals
  • Apoptosis / physiology*
  • Cardiotonic Agents / antagonists & inhibitors
  • Cardiotonic Agents / pharmacology
  • Cardiotonic Agents / therapeutic use
  • Cyclic N-Oxides / pharmacology
  • Free Radical Scavengers / pharmacology
  • Humans
  • Imidazoles / pharmacology
  • MAP Kinase Kinase Kinase 5 / metabolism
  • MAP Kinase Signaling System / drug effects
  • Male
  • Metalloporphyrins / pharmacology
  • Metalloporphyrins / therapeutic use
  • Mice
  • Molsidomine / analogs & derivatives*
  • Molsidomine / antagonists & inhibitors
  • Molsidomine / pharmacology
  • Mutagenesis, Site-Directed
  • Myocardial Ischemia / metabolism*
  • Myocardial Ischemia / pathology
  • Myocardial Reperfusion Injury / drug therapy
  • Myocardium / pathology*
  • NADP / metabolism
  • Oxidation-Reduction
  • Oxidative Stress
  • Peroxynitrous Acid / pharmacology
  • Thioredoxins / antagonists & inhibitors*
  • Thioredoxins / therapeutic use
  • p38 Mitogen-Activated Protein Kinases / metabolism

Substances

  • Cardiotonic Agents
  • Cyclic N-Oxides
  • FeCl tetrakis-2-(triethyleneglycolmonomethylether)pyridylporphyrin
  • Free Radical Scavengers
  • Imidazoles
  • Metalloporphyrins
  • TXN protein, human
  • manganese (III) meso-tetrakis(N-ethylpyridinium-2-yl)porphyrin
  • Peroxynitrous Acid
  • 2-phenyl-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide
  • Thioredoxins
  • NADP
  • linsidomine
  • Molsidomine
  • p38 Mitogen-Activated Protein Kinases
  • MAP Kinase Kinase Kinase 5