Hydrogen sulfide as endothelium-derived hyperpolarizing factor sulfhydrates potassium channels

Circ Res. 2011 Nov 11;109(11):1259-68. doi: 10.1161/CIRCRESAHA.111.240242. Epub 2011 Oct 6.

Abstract

Rationale: Nitric oxide, the classic endothelium-derived relaxing factor (EDRF), acts through cyclic GMP and calcium without notably affecting membrane potential. A major component of EDRF activity derives from hyperpolarization and is termed endothelium-derived hyperpolarizing factor (EDHF). Hydrogen sulfide (H(2)S) is a prominent EDRF, since mice lacking its biosynthetic enzyme, cystathionine γ-lyase (CSE), display pronounced hypertension with deficient vasorelaxant responses to acetylcholine.

Objective: The purpose of this study was to determine if H(2)S is a major physiological EDHF.

Methods and results: We now show that H(2)S is a major EDHF because in blood vessels of CSE-deleted mice, hyperpolarization is virtually abolished. H(2)S acts by covalently modifying (sulfhydrating) the ATP-sensitive potassium channel, as mutating the site of sulfhydration prevents H(2)S-elicited hyperpolarization. The endothelial intermediate conductance (IK(Ca)) and small conductance (SK(Ca)) potassium channels mediate in part the effects of H(2)S, as selective IK(Ca) and SK(Ca) channel inhibitors, charybdotoxin and apamin, inhibit glibenclamide-insensitive, H(2)S-induced vasorelaxation.

Conclusions: H(2)S is a major EDHF that causes vascular endothelial and smooth muscle cell hyperpolarization and vasorelaxation by activating the ATP-sensitive, intermediate conductance and small conductance potassium channels through cysteine S-sulfhydration. Because EDHF activity is a principal determinant of vasorelaxation in numerous vascular beds, drugs influencing H(2)S biosynthesis offer therapeutic potential.

Publication types

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

MeSH terms

  • Acetylcholine / pharmacology
  • Animals
  • Aorta / cytology
  • Aorta / metabolism
  • Cells, Cultured / drug effects
  • Cells, Cultured / metabolism
  • Charybdotoxin / pharmacology
  • Cystathionine gamma-Lyase / deficiency
  • Cystathionine gamma-Lyase / genetics
  • Endothelium, Vascular / metabolism*
  • Endothelium-Dependent Relaxing Factors / metabolism
  • Female
  • Glyburide / pharmacology
  • Hydrogen Sulfide / metabolism*
  • Hypertension / metabolism
  • KATP Channels / metabolism*
  • Male
  • Membrane Potentials / drug effects
  • Mesenteric Arteries / injuries
  • Mesenteric Arteries / metabolism
  • Mesenteric Arteries / pathology
  • Mice
  • Mice, Inbred C57BL
  • Phenylephrine / pharmacology
  • Potassium Chloride / pharmacology
  • Rats
  • Rats, Wistar
  • Vasodilation / drug effects
  • Vasodilation / physiology*

Substances

  • Endothelium-Dependent Relaxing Factors
  • KATP Channels
  • uK-ATP-1 potassium channel
  • Charybdotoxin
  • Phenylephrine
  • Potassium Chloride
  • Cystathionine gamma-Lyase
  • Acetylcholine
  • Glyburide
  • Hydrogen Sulfide