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First published online October 5, 2006
Journal of Experimental Biology 209, 4011-4023 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02480

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

Kenneth R. Olson^1,*, Ryan A. Dombkowski^1,2,, Michael J. Russell^1,, Meredith M. Doellman², Sally K. Head², Nathan L. Whitfield^1,2 and Jane A. Madden^3,4

¹ Indiana University School of Medicine-South Bend, 1234 Notre Dame Avenue, South Bend, IN 46617, USA
² Department of Biological Sciences, University of Notre Dame, Notre Dame, IN 46556, USA
³ Department of Neurology, The Medical College of Wisconsin, Milwaukee 53226, WI, USA
⁴ Research Service, Zablocki Veterans Affairs Medical Center, Milwaukee, WI 53295, USA

^* Author for correspondence (e-mail: kolson{at}nd.edu)

Accepted 1 August 2006

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 H₂S produce temporally and quantitatively identical responses even though the responses vary from constriction (lamprey dorsal aorta; lDA), to dilation (rat aorta; rA), to multi-phasic (rat and bovine pulmonary arteries; rPA and bPA, respectively). (2) The responses of lDA, 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 lDA and bPA vascular smooth muscle. (5) Inhibition of H₂S synthesis inhibits the hypoxic response of lDA, rA, rPA and bPA. (6) Addition of the H₂S precursor, cysteine, doubles hypoxic contraction in lDA, prolongs contraction in bPA and alters the re-oxygenation response of rA. These studies suggest that H₂S may serve as an O₂ sensor/transducer in the vascular responses to hypoxia. In this model, the concentration of vasoactive H₂S in the vessel is governed by the balance between endogenous H₂S production and its oxidation by available O₂.

Key words: vascular smooth muscle, hydrogen sulfide metabolism, cysteine metabolism, redox signaling

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