S-Nitrosylation of Prostacyclin Synthase Instigates Nitrate Cross-Tolerance In Vivo

Clin Pharmacol Ther. 2019 Jan;105(1):201-209. doi: 10.1002/cpt.1094. Epub 2018 Aug 1.

Abstract

Development of nitrate tolerance is a major drawback to nitrate therapy. Prostacyclin (PGI2) is a powerful vasodilator produced from prostaglandin (PGH2) by prostacyclin synthase (PGIS) in endothelial cells. This study aimed to determine the role of PGIS S-nitrosylation in nitrate tolerance induced by nitroglycerin (GTN). In endothelial cells, GTN increased PGIS S-nitrosylation and disturbed PGH2 metabolism, which were normalized by mutants of PGIS cysteine 231/441 to alanine (C231/441A). Clearance of nitric oxide by carboxy-PTIO or inhibition of S-nitrosylation by N-acetyl-cysteine decreased GTN-induced PGIS S-nitrosylation. Enforced expression of mutated PGIS with C231/441A markedly abolished GTN-induced PGIS S-nitrosylation and nitrate cross-tolerance in Apoe-/- mice. Inhibition of cyclooxygenase 1 by aspirin, supplementation of PGI2 by beraprost, and inhibition of PGIS S-nitrosylation by N-acetyl-cysteine improved GTN-induced nitrate cross-tolerance in rats. In patients, increased PGIS S-nitrosylation was associated with nitrate tolerance. In conclusion, GTN induces nitrate cross-tolerance through PGIS S-nitrosylation at cysteine 231/441.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aged
  • Aged, 80 and over
  • Amino Acid Sequence
  • Animals
  • Cattle
  • Cricetinae
  • Cytochrome P-450 Enzyme System / genetics
  • Cytochrome P-450 Enzyme System / metabolism*
  • Dose-Response Relationship, Drug
  • Drug Tolerance / physiology*
  • Female
  • Human Umbilical Vein Endothelial Cells
  • Humans
  • Intramolecular Oxidoreductases / genetics
  • Intramolecular Oxidoreductases / metabolism*
  • Male
  • Mice
  • Mice, Knockout
  • Middle Aged
  • Nitrates / metabolism*
  • Nitric Oxide / metabolism*
  • Nitroglycerin / pharmacology*
  • Rats
  • Rats, Sprague-Dawley
  • Vasodilator Agents / pharmacology

Substances

  • Nitrates
  • Vasodilator Agents
  • Nitric Oxide
  • Cytochrome P-450 Enzyme System
  • Intramolecular Oxidoreductases
  • prostacyclin synthetase
  • Nitroglycerin