Differential regulation of metabolism by nitric oxide and S-nitrosothiols in endothelial cells

Am J Physiol Heart Circ Physiol. 2011 Sep;301(3):H803-12. doi: 10.1152/ajpheart.00210.2011. Epub 2011 Jun 17.

Abstract

S-nitrosation of thiols in key proteins in cell signaling pathways is thought to be an important contributor to nitric oxide (NO)-dependent control of vascular (patho)physiology. Multiple metabolic enzymes are targets of both NO and S-nitrosation, including those involved in glycolysis and oxidative phosphorylation. Thus it is important to understand how these metabolic pathways are integrated by NO-dependent mechanisms. Here, we compared the effects of NO and S-nitrosation on both glycolysis and oxidative phosphorylation in bovine aortic endothelial cells using extracellular flux technology to determine common and unique points of regulation. The compound S-nitroso-L-cysteine (L-CysNO) was used to initiate intracellular S-nitrosation since it is transported into cells and results in stable S-nitrosation in vitro. Its effects were compared with the NO donor DetaNONOate (DetaNO). DetaNO treatment caused only a decrease in the reserve respiratory capacity; however, L-CysNO impaired both this parameter and basal respiration in a concentration-dependent manner. In addition, DetaNO stimulated extracellular acidification rate (ECAR), a surrogate marker of glycolysis, whereas L-CysNO stimulated ECAR at low concentrations and inhibited it at higher concentrations. Moreover, a temporal relationship between NO- and S-nitrosation-mediated effects on metabolism was identified, whereby NO caused a rapid impairment in mitochondrial function, which was eventually overwhelmed by S-nitrosation-dependent processes. Taken together, these results suggest that severe pharmacological nitrosative stress may differentially regulate metabolic pathways through both intracellular S-nitrosation and NO-dependent mechanisms. Moreover, these data provide insight into the role of NO and related compounds in vascular (patho)physiology.

Publication types

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

MeSH terms

  • Adenine Nucleotides / metabolism
  • Animals
  • Cattle
  • Cells, Cultured
  • Cysteine / analogs & derivatives
  • Cysteine / pharmacology
  • Dose-Response Relationship, Drug
  • Endothelial Cells / drug effects
  • Endothelial Cells / metabolism*
  • Glycolysis* / drug effects
  • Hydrogen-Ion Concentration
  • Mitochondria / drug effects
  • Mitochondria / metabolism
  • Nitric Oxide / metabolism*
  • Nitric Oxide Donors / pharmacology
  • Nitrosation
  • Nitroso Compounds / pharmacology
  • Oxidative Phosphorylation* / drug effects
  • S-Nitrosothiols / metabolism*
  • S-Nitrosothiols / pharmacology
  • Stress, Physiological* / drug effects
  • Time Factors

Substances

  • Adenine Nucleotides
  • Nitric Oxide Donors
  • Nitroso Compounds
  • S-Nitrosothiols
  • 2,2'-(hydroxynitrosohydrazono)bis-ethanamine
  • Nitric Oxide
  • S-nitrosocysteine
  • Cysteine