Akt/eNOS signaling and PLN S-sulfhydration are involved in H₂S-dependent cardiac effects in frog and rat

Am J Physiol Regul Integr Comp Physiol. 2013 Aug 15;305(4):R443-51. doi: 10.1152/ajpregu.00088.2013. Epub 2013 Jun 19.

Abstract

Hydrogen sulfide (H₂S) has recently emerged as an important mediator of mammalian cardiovascular homeostasis. In nonmammalian vertebrates, little is known about the cardiac effects of H₂S. This study aimed to evaluate, in the avascular heart of the frog, Rana esculenta, whether and to what extent H₂S affects the cardiac performance, and what is the mechanism of action responsible for the observed effects. Results were analyzed in relation to those obtained in the rat heart, used as the mammalian model. Isolated and perfused (working and Langendorff) hearts, Western blot analysis, and modified biotin switch (S-sulfhydration) assay were used. In the frog heart, NaHS (used as H₂S donor, 10⁻¹²/10⁻⁷ M) dose-dependently decreased inotropism. This effect was reduced by glibenclamide (KATP channels blocker), NG-monomethyl-L-arginine (NOS inhibitor), 1H-[1,2,4] oxadiazolo-[4,3-a]quinoxalin-1-one (guanylyl cyclase inhibitor), KT₅₈₂₃ (PKG inhibitor), and it was blocked by Akt1/2 (Akt inhibitor) and by detergent Triton X-100. In the rat, in addition to the classic negative inotropic effect, NaHS (10⁻¹²/10⁻⁷ M) exhibited negative lusitropism. In both frog and rat hearts, NaHS treatment induced Akt and eNOS phosphorylation and an increased cardiac protein S-sulfhydration that, in the rat heart, includes phospholamban. Our data suggest that H₂S represents a phylogenetically conserved cardioactive molecule. Results obtained on the rat heart extend the role of H₂S also to cardiac relaxation. H₂S effects involve KATP channels, the Akt/NOS-cGMP/PKG pathway, and S-sulfhydration of cardiac proteins.

Keywords: hydrogen sulfide; inotropism; lusitropism; nitric oxide synthase-cGMP/PKG pathway.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amphibian Proteins / metabolism*
  • Animals
  • Calcium-Binding Proteins / metabolism*
  • Cyclic GMP-Dependent Protein Kinases / antagonists & inhibitors
  • Cyclic GMP-Dependent Protein Kinases / metabolism
  • Detergents / pharmacology
  • Dose-Response Relationship, Drug
  • Enzyme Inhibitors / pharmacology
  • Female
  • Guanylate Cyclase / antagonists & inhibitors
  • Guanylate Cyclase / metabolism
  • Heart / drug effects*
  • Hydrogen Sulfide / metabolism
  • Hydrogen Sulfide / pharmacology*
  • KATP Channels / drug effects
  • KATP Channels / metabolism
  • Male
  • Myocardial Contraction / drug effects
  • Myocardium / enzymology*
  • Nitric Oxide Synthase Type III / antagonists & inhibitors
  • Nitric Oxide Synthase Type III / metabolism*
  • Potassium Channel Blockers / pharmacology
  • Protein Processing, Post-Translational
  • Proto-Oncogene Proteins c-akt / antagonists & inhibitors
  • Proto-Oncogene Proteins c-akt / metabolism*
  • Rana esculenta
  • Rats
  • Rats, Wistar
  • Signal Transduction / drug effects*
  • Sulfides / metabolism
  • Sulfides / pharmacology*
  • Time Factors

Substances

  • Amphibian Proteins
  • Calcium-Binding Proteins
  • Detergents
  • Enzyme Inhibitors
  • KATP Channels
  • Potassium Channel Blockers
  • Sulfides
  • phospholamban
  • Nitric Oxide Synthase Type III
  • Nos3 protein, rat
  • Akt1 protein, rat
  • Akt2 protein, rat
  • Proto-Oncogene Proteins c-akt
  • Cyclic GMP-Dependent Protein Kinases
  • Guanylate Cyclase
  • sodium sulfide
  • Hydrogen Sulfide