Hydrogen sulfide mediates hypoxia-induced relaxation of trout urinary bladder smooth muscle

Ryan A. Dombkowski, Meredith M. Doellman, Sally K. Head, Kenneth R. Olson

Research output: Contribution to journalArticle

52 Scopus citations

Abstract

Hydrogen sulfide (H2S) is a recently identified gasotransmitter that may mediate hypoxic responses in vascular smooth muscle. H2S also appears to be a signaling molecule in mammalian non-vascular smooth muscle, but its existence and function in non-mammalian non-vascular smooth muscle have not been examined. In the present study we examined H2S production and its physiological effects in urinary bladder from steelhead and rainbow trout (Oncorhynchus mykiss) and evaluated the relationship between H 2S and hypoxia. H2S was produced by trout bladders, and its production was sensitive to inhibitors of cystathionine β-synthase and cystathionine γ-lyase. H2S produced a dose-dependent relaxation in unstimulated and carbachol pre-contracted bladders and inhibited spontaneous contractions. Bladders pre-contracted with 80 mmol l-1 KCl were less sensitive to H2S than bladders contracted with either 80 mmol l -1 KC2H3O2 (KAc) or carbachol, suggesting that some of the H2S effects are mediated through an ion channel. However, H2S relaxation of bladders was not affected by the potassium channel inhibitors, apamin, charybdotoxin, 4-aminopyridine, and glybenclamide, or by chloride channel/exchange inhibitors 4,4′- Diisothiocyanatostilbene-2,2′-disulfonic acid disodium salt, tamoxifen and glybenclamide, or by the presence or absence of extracellular HCO 3-. Inhibitors of neuronal mechanisms, tetrodotoxin, strychnine and N-vanillylnonanamide were likewise ineffective. Hypoxia (aeration with N2) also relaxed bladders, was competitive with H2S for relaxation, and it was equally sensitive to KCl, and unaffected by neuronal blockade or the presence of extracellular HCO3-. Inhibitors of H 2S synthesis also inhibited hypoxic relaxation. These experiments suggest that H2S is a phylogenetically ancient gasotransmitter in non-mammalian non-vascular smooth muscle and that it serves as an oxygen sensor/transducer, mediating the effects of hypoxia.

Original languageEnglish (US)
Pages (from-to)3234-3240
Number of pages7
JournalJournal of Experimental Biology
Volume209
Issue number16
DOIs
StatePublished - Aug 1 2006

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Keywords

  • HS
  • Hypoxia
  • Smooth muscle
  • Trout
  • Urinary bladder

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Agricultural and Biological Sciences (miscellaneous)

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