Hydrogen sulfide (H2S) and hypoxia inhibit salmonid gastrointestinal motility: Evidence for H2S as an oxygen sensor

Ryan A. Dombkowski, Marie G. Naylor, Emma Shoemaker, Michelle Smith, Eric R. DeLeon, Gilbrian F. Stoy, Yan Gao, Kenneth Olson

Research output: Contribution to journalArticle

21 Citations (Scopus)

Abstract

Hydrogen sulfide (H2S) has been shown to affect gastrointestinal (GI) motility and signaling in mammals and O2-dependent H 2S metabolism has been proposed to serve as an O2 'sensor' that couples hypoxic stimuli to effector responses in a variety of other O 2-sensing tissues. The low PO2 values and high H2S concentrations routinely encountered in the GI tract suggest that H2S might also be involved in hypoxic responses in these tissues. In the present study we examined the effect of H2S on stomach, esophagus, gallbladder and intestinal motility in the rainbow trout (Oncorhynchus mykiss) and coho salmon (Oncorhynchus kisutch) and we evaluated the potential for H2S in oxygen sensing by examining GI responses to hypoxia in the presence of known inhibitors of H2S biosynthesis and by adding the sulfide donor cysteine (Cys). We also measured H2S production by intestinal tissue in real time and in the presence and absence of oxygen. In tissues exhibiting spontaneous contractions, H2S inhibited contraction magnitude (area under the curve and amplitude) and frequency, and in all tissues it reduced baseline tension in a concentration-dependent relationship. Longitudinal intestinal smooth muscle was significantly more sensitive to H2S than other tissues, exhibiting significant inhibitory responses at 1-10μmol l-1 H2S. The effects of hypoxia were essentially identical to those of H2S in longitudinal and circular intestinal smooth muscle; of special note was a unique transient stimulatory effect upon application of both hypoxia and H2S. Inhibitors of enzymes implicated in H2S biosynthesis (cystathionine β-synthase and cystathionine γ-lyase) partially inhibited the effects of hypoxia whereas the hypoxic effects were augmented by the sulfide donor Cys. Furthermore, tissue production of H2S was inversely related to O2; addition of Cys to intestinal tissue homogenate stimulated H 2S production when the tissue was gassed with 100% nitrogen (∼0% O2), whereas addition of oxygen (∼10% O2) reversed this to net H2S consumption. This study shows that the inhibitory effects of H2S on the GI tract of a non-mammalian vertebrate are identical to those reported in mammals and they provide further evidence that H2S is a key mediator of the hypoxic response in a variety of O 2-sensitive tissues.

Original languageEnglish
Pages (from-to)4030-4040
Number of pages11
JournalJournal of Experimental Biology
Volume214
Issue number23
DOIs
StatePublished - Dec 2011

Fingerprint

gastrointestinal motility
Hydrogen Sulfide
Gastrointestinal Motility
hydrogen sulfide
motility
salmonid
hypoxia
Oxygen
sensor
oxygen
Oncorhynchus kisutch
Cystathionine
cystathionine
Cysteine
cysteine
Oncorhynchus mykiss
Sulfides
sulfides
smooth muscle
contraction

Keywords

  • Fish
  • Gastrointestinal system
  • HS
  • Hypoxia
  • Visceral smooth muscle

ASJC Scopus subject areas

  • Animal Science and Zoology
  • Ecology, Evolution, Behavior and Systematics
  • Molecular Biology
  • Physiology
  • Insect Science
  • Aquatic Science

Cite this

Hydrogen sulfide (H2S) and hypoxia inhibit salmonid gastrointestinal motility : Evidence for H2S as an oxygen sensor. / Dombkowski, Ryan A.; Naylor, Marie G.; Shoemaker, Emma; Smith, Michelle; DeLeon, Eric R.; Stoy, Gilbrian F.; Gao, Yan; Olson, Kenneth.

In: Journal of Experimental Biology, Vol. 214, No. 23, 12.2011, p. 4030-4040.

Research output: Contribution to journalArticle

Dombkowski, Ryan A. ; Naylor, Marie G. ; Shoemaker, Emma ; Smith, Michelle ; DeLeon, Eric R. ; Stoy, Gilbrian F. ; Gao, Yan ; Olson, Kenneth. / Hydrogen sulfide (H2S) and hypoxia inhibit salmonid gastrointestinal motility : Evidence for H2S as an oxygen sensor. In: Journal of Experimental Biology. 2011 ; Vol. 214, No. 23. pp. 4030-4040.
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