Cytokine-induced nitric oxide production inhibits mitochondrial energy production and impairs contractile function in rat cardiac myocytes

J Am Coll Cardiol. 2000 Apr;35(5):1338-46. doi: 10.1016/s0735-1097(00)00526-x.

Abstract

Objectives: The present study examined whether nitric oxide (NO) produced by inducible nitric oxide synthase (iNOS) can directly inhibit aerobic energy metabolism and impair cell function in interleukin (IL)-1beta,-stimulated cardiac myocytes.

Background: Recent reports have indicated that excessive production of NO induced by cytokines can disrupt cellular energy balance through the inhibition of mitochondrial respiration in a variety of cells. However, it is still largely uncertain whether the NO-induced energy depletion affects myocardial contractility.

Methods: Primary cultures of rat neonatal cardiac myocytes were prepared, and NO2-/NO3- (NOx) in the culture media was measured using Griess reagent.

Results: Treatment with IL-1beta (10 ng/ml) increased myocyte production of NOx in a time-dependent manner. The myocytes showed a concomitant significant increase in glucose consumption, a marked increase in lactate production, and a significant decrease in cellular ATP (adenosine 5'-triphosphate). These metabolic changes were blocked by co-incubation with N(G)-monomethyl-L-arginine (L-NMMA), an inhibitor of NO synthesis. Sodium nitroprusside (SNP), a NO donor, induced similar metabolic changes in a dose-dependent manner, but 8-bromo-cyclic guanosine 3',5'-monophosphate (8-bromo-cGMP), a cGMP donor, had no effect on these parameters. The activities of the mitochondrial iron-sulfur enzymes, NADH-CoQreductase and succinate-CoQreductase, but not oligomycin-sensitive ATPase, were significantly inhibited in the IL-1beta, or SNP-treated myocytes. Both IL-1beta and SNP significantly elevated maximum diastolic potential, reduced peak calcium current (I(Ca)), and lowered contractility in the myocytes. KT5823, an inhibitor of cGMP-dependent protein kinase, did not block the electrophysiological and contractility effects.

Conclusions: These data suggest that IL-1beta-induced NO production in cardiac myocytes lowers energy production and myocardial contractility through a direct attack on the mitochondria, rather than through cGMP-mediated pathways.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Triphosphate / analysis
  • Adenosine Triphosphate / metabolism
  • Animals
  • Animals, Newborn
  • Cells, Cultured / physiology
  • Cyclic GMP / analogs & derivatives
  • Cyclic GMP / pharmacology
  • Disease Models, Animal
  • Dose-Response Relationship, Drug
  • Energy Metabolism / physiology*
  • Glucose / analysis
  • Glucose / metabolism
  • Glycolysis
  • Inflammation
  • Interleukin-1 / physiology*
  • Lactic Acid / analysis
  • Lactic Acid / metabolism
  • Mitochondria, Heart / metabolism*
  • Myocardial Contraction / physiology*
  • Myocardium / cytology*
  • Myocardium / metabolism*
  • Nitric Oxide / physiology*
  • Nitric Oxide Synthase / antagonists & inhibitors
  • Nitric Oxide Synthase / physiology*
  • Nitroprusside / pharmacology
  • Rats
  • omega-N-Methylarginine / pharmacology

Substances

  • Interleukin-1
  • Nitroprusside
  • omega-N-Methylarginine
  • 8-bromocyclic GMP
  • Nitric Oxide
  • Lactic Acid
  • Adenosine Triphosphate
  • Nitric Oxide Synthase
  • Cyclic GMP
  • Glucose