Hydrogen sulfide as an oxygen sensor/transducer in vertebrate hypoxic vasoconstriction and hypoxic vasodilation

Kenneth R. Olson, Ryan A. Dombkowski, Michael J. Russell, Meredith M. Doellman, Sally K. Head, Nathan L. Whitfield, Jane A. Madden

Research output: Contribution to journalArticle

192 Scopus citations

Abstract

How vertebrate blood vessels sense acute hypoxia and respond either by constricting (hypoxic vasoconstriction) or dilating (hypoxic vasodilation) has not been resolved. In the present study we compared the mechanical and electrical responses of select blood vessels to hypoxia and H2S, measured vascular H2S production, and evaluated the effects of inhibitors of H2S synthesis and addition of the H2S precursor, cysteine, on hypoxic vasoconstriction and hypoxic vasodilation. We found that: (1) in all vertebrate vessels examined to date, hypoxia and H 2S produce temporally and quantitatively identical responses even though the responses vary from constriction (lamprey dorsal aorta; IDA), to dilation (rat aorta; rA), to multiphasic (rat and bovine pulmonary arteries; rPA and bPA, respectively). (2) The responses of IDA, rA and bPA to hypoxia and H2S appear competitive; in the presence of one stimulus, the response to the other stimulus is substantially or completely eliminated. (3) Hypoxia and H2S produce the same degree of cell depolarization in bPA. (4) H2S is constitutively synthesized by IDA and bPA vascular smooth muscle. (5) Inhibition of H2S synthesis inhibits the hypoxic response of IDA, rA, rPA and bPA. (6) Addition of the H2S precursor, cysteine, doubles hypoxic contraction in IDA, prolongs contraction in bPA and alters the re-oxygenation response of rA. These studies suggest that H 2S may serve as an O2 sensor/transducer in the vascular responses to hypoxia. In this model, the concentration of vasoactive H 2S in the vessel is governed by the balance between endogenous H 2S production and its oxidation by available O2.

Original languageEnglish (US)
Pages (from-to)4011-4023
Number of pages13
JournalJournal of Experimental Biology
Volume209
Issue number20
DOIs
StatePublished - Oct 1 2006

Keywords

  • Cysteine metabolism
  • Hydrogen sulfide metabolism
  • Redox signaling
  • Vascular smooth muscle

ASJC Scopus subject areas

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

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    Olson, K. R., Dombkowski, R. A., Russell, M. J., Doellman, M. M., Head, S. K., Whitfield, N. L., & Madden, J. A. (2006). Hydrogen sulfide as an oxygen sensor/transducer in vertebrate hypoxic vasoconstriction and hypoxic vasodilation. Journal of Experimental Biology, 209(20), 4011-4023. https://doi.org/10.1242/jeb.02480