Hydrogen sulfide as an oxygen sensor in trout gill chemoreceptors

Kenneth Olson, Michael J. Healy, Zhaohong Qin, Nini Skovgaard, Branka Vulesevic, Douglas W. Duff, Nathan L. Whitfield, Guangdong Yang, Rui Wang, Steve F. Perry

Research output: Contribution to journalArticle

98 Citations (Scopus)

Abstract

O2 chemoreceptors elicit cardiorespiratory reflexes in all vertebrates, but consensus on O2-sensing signal transduction mechanism(s) is lacking. We recently proposed that hydrogen sulfide (H2S) metabolism is involved in O2 sensing in vascular smooth muscle. Here, we examined the possibility that H2S is an O2 sensor in trout chemoreceptors where the first pair of gills is a primary site of aquatic O2 sensing and the homolog of the mammalian carotid body. Intrabuccal injection of H2S in unanesthetized trout produced a dose-dependent bradycardia and increased ventilatory frequency and amplitude similar to the hypoxic response. Removal of the first, but not second, pair of gills significantly inhibited H2S-mediated bradycardia, consistent with the loss of aquatic chemoreceptors. mRNA for H2S-synthesizing enzymes, cystathionine β-synthase and cystathionine γ-lyase, was present in branchial tissue. Homogenized gills produced H2S enzymatically, and H2S production was inhibited by O2, whereas mitochondrial H2S consumption was O2 dependent. Ambient hypoxia did not affect plasma H2S in unanesthetized trout, but produced a PO 2-dependent increase in a sulfide moiety suggestive of increased H2S production. In isolated zebrafish neuroepithelial cells, the putative chemoreceptive cells of fish, both hypoxia and H2S, produced a similar ∼10-mV depolarization. These studies are consistent with H 2S involvement in O2 sensing/signal transduction pathway(s) in chemoreceptive cells, as previously demonstrated in vascular smooth muscle. This novel mechanism, whereby H2S concentration ([H2S]) is governed by the balance between constitutive production and oxidation, tightly couples tissue [H2S] to PO2 and may provide an exquisitely sensitive, yet simple, O2 sensor in a variety of tissues.

Original languageEnglish
JournalAmerican Journal of Physiology - Regulatory Integrative and Comparative Physiology
Volume295
Issue number2
DOIs
StatePublished - Aug 2008

Fingerprint

Hydrogen Sulfide
Trout
Chemoreceptor Cells
Cystathionine
Bradycardia
Oxygen
Vascular Smooth Muscle
Signal Transduction
Neuroepithelial Cells
Carotid Body
Lyases
Sulfides
Zebrafish
Reflex
Vertebrates
Consensus
Fishes
Messenger RNA
Injections
Enzymes

Keywords

  • Hydrogen sulfide concentration

ASJC Scopus subject areas

  • Physiology
  • Physiology (medical)

Cite this

Hydrogen sulfide as an oxygen sensor in trout gill chemoreceptors. / Olson, Kenneth; Healy, Michael J.; Qin, Zhaohong; Skovgaard, Nini; Vulesevic, Branka; Duff, Douglas W.; Whitfield, Nathan L.; Yang, Guangdong; Wang, Rui; Perry, Steve F.

In: American Journal of Physiology - Regulatory Integrative and Comparative Physiology, Vol. 295, No. 2, 08.2008.

Research output: Contribution to journalArticle

Olson, K, Healy, MJ, Qin, Z, Skovgaard, N, Vulesevic, B, Duff, DW, Whitfield, NL, Yang, G, Wang, R & Perry, SF 2008, 'Hydrogen sulfide as an oxygen sensor in trout gill chemoreceptors', American Journal of Physiology - Regulatory Integrative and Comparative Physiology, vol. 295, no. 2. https://doi.org/10.1152/ajpregu.00807.2007
Olson, Kenneth ; Healy, Michael J. ; Qin, Zhaohong ; Skovgaard, Nini ; Vulesevic, Branka ; Duff, Douglas W. ; Whitfield, Nathan L. ; Yang, Guangdong ; Wang, Rui ; Perry, Steve F. / Hydrogen sulfide as an oxygen sensor in trout gill chemoreceptors. In: American Journal of Physiology - Regulatory Integrative and Comparative Physiology. 2008 ; Vol. 295, No. 2.
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