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. 1989 May 1;93(5):1001–1015. doi: 10.1085/jgp.93.5.1001

Low pO2 selectively inhibits K channel activity in chemoreceptor cells of the mammalian carotid body

PMCID: PMC2216240  PMID: 2738574

Abstract

The hypothesis that changes in environmental O2 tension (pO2) could affect the ionic conductances of dissociated type I cells of the carotid body was tested. Cells were subjected to whole-cell patch clamp and ionic currents were recorded in a control solution with normal pO2 (pO2 = 150 mmHg) and 3-5 min after exposure to the same solution with a lower pO2. Na and Ca currents were unaffected by lowering pO2 to 10 mmHg, however, in all cells studied (n = 42) exposure to hypoxia produced a reversible reduction of the K current. In 14 cells exposed to a pO2 of 10 mmHg peak K current amplitude decreased to 35 +/- 8% of the control value. The effect of low pO2 was independent of the internal Ca2+ concentration and was observed in the absence of internal exogenous nucleotides. Inhibition of K channel activity by hypoxia is a graded phenomenon and in the range between 70 and 120 mmHg, which includes normal pO2 values in arterial blood, it is directly correlated with pO2 levels. Low pO2 appeared to slow down the activation time course of the K current but deactivation kinetics seemed to be unaltered. Type I cells subjected to current clamp generate large Na- and Ca-dependent action potentials repetitively. Exposure to low pO2 produces a 4-10 mV increase in the action potential amplitude and a faster depolarization rate of pacemaker potentials, which leads to an increase in the firing frequency. Repolarization rate of individual action potentials is, however, unaffected, or slightly increased. The selective inhibition of K channel activity by low pO2 is a phenomenon without precedents in the literature that explains the chemoreceptive properties of type I cells. The nature of the interaction of molecular O2 with the K channel protein is unknown, however, it is argued that a hemoglobin-like O2 sensor, perhaps coupled to a G protein, could be involved.

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Selected References

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  1. Almaraz L., Gonzalez C., Obeso A. Effects of high potassium on the release of [3H]dopamine from the cat carotid body in vitro. J Physiol. 1986 Oct;379:293–307. doi: 10.1113/jphysiol.1986.sp016254. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Avenet P., Hofmann F., Lindemann B. Transduction in taste receptor cells requires cAMP-dependent protein kinase. Nature. 1988 Jan 28;331(6154):351–354. doi: 10.1038/331351a0. [DOI] [PubMed] [Google Scholar]
  3. Biscoe T. J., Purves M. J., Sampson S. R. The frequency of nerve impulses in single carotid body chemoreceptor afferent fibres recorded in vivo with intact circulation. J Physiol. 1970 May;208(1):121–131. doi: 10.1113/jphysiol.1970.sp009109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Brown A. M., Birnbaumer L. Direct G protein gating of ion channels. Am J Physiol. 1988 Mar;254(3 Pt 2):H401–H410. doi: 10.1152/ajpheart.1988.254.3.H401. [DOI] [PubMed] [Google Scholar]
  5. Connor J. A., Stevens C. F. Voltage clamp studies of a transient outward membrane current in gastropod neural somata. J Physiol. 1971 Feb;213(1):21–30. doi: 10.1113/jphysiol.1971.sp009365. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cota G. Calcium channel currents in pars intermedia cells of the rat pituitary gland. Kinetic properties and washout during intracellular dialysis. J Gen Physiol. 1986 Jul;88(1):83–105. doi: 10.1085/jgp.88.1.83. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Fernandez J. M., Fox A. P., Krasne S. Membrane patches and whole-cell membranes: a comparison of electrical properties in rat clonal pituitary (GH3) cells. J Physiol. 1984 Nov;356:565–585. doi: 10.1113/jphysiol.1984.sp015483. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Fesenko E. E., Kolesnikov S. S., Lyubarsky A. L. Induction by cyclic GMP of cationic conductance in plasma membrane of retinal rod outer segment. Nature. 1985 Jan 24;313(6000):310–313. doi: 10.1038/313310a0. [DOI] [PubMed] [Google Scholar]
  9. Fitzgerald R. S., Parks D. C. Effect of hypoxia on carotid chemoreceptor response to carbon dioxide in cats. Respir Physiol. 1971 Jun;12(2):218–229. doi: 10.1016/0034-5687(71)90054-5. [DOI] [PubMed] [Google Scholar]
  10. Forscher P., Oxford G. S. Modulation of calcium channels by norepinephrine in internally dialyzed avian sensory neurons. J Gen Physiol. 1985 May;85(5):743–763. doi: 10.1085/jgp.85.5.743. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hille B. Charges and potentials at the nerve surface. Divalent ions and pH. J Gen Physiol. 1968 Feb;51(2):221–236. doi: 10.1085/jgp.51.2.221. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kinnamon S. C., Roper S. D. Membrane properties of isolated mudpuppy taste cells. J Gen Physiol. 1988 Mar;91(3):351–371. doi: 10.1085/jgp.91.3.351. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kostyuk P. G. Metabolic control of ionic channels in the neuronal membrane. Neuroscience. 1984 Dec;13(4):983–989. doi: 10.1016/0306-4522(84)90282-3. [DOI] [PubMed] [Google Scholar]
  14. Lahiri S. Introductory remarks: oxygen linked response of carotid chemoreceptors. Adv Exp Med Biol. 1977;78:185–202. doi: 10.1007/978-1-4615-9035-4_15. [DOI] [PubMed] [Google Scholar]
  15. Levitan I. B. Phosphorylation of ion channels. J Membr Biol. 1985;87(3):177–190. doi: 10.1007/BF01871217. [DOI] [PubMed] [Google Scholar]
  16. Motais R., Garcia-Romeu F., Borgese F. The control of Na+/H+ exchange by molecular oxygen in trout erythrocytes. A possible role of hemoglobin as a transducer. J Gen Physiol. 1987 Aug;90(2):197–207. doi: 10.1085/jgp.90.2.197. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Nakamura T., Gold G. H. A cyclic nucleotide-gated conductance in olfactory receptor cilia. 1987 Jan 29-Feb 4Nature. 325(6103):442–444. doi: 10.1038/325442a0. [DOI] [PubMed] [Google Scholar]
  18. Neer E. J., Clapham D. E. Roles of G protein subunits in transmembrane signalling. Nature. 1988 May 12;333(6169):129–134. doi: 10.1038/333129a0. [DOI] [PubMed] [Google Scholar]
  19. Rigual R., Gonzalez E., Fidone S., Gonzalez C. Effects of low pH on synthesis and release of catecholamines in the cat carotid body in vitro. Brain Res. 1984 Aug 20;309(1):178–181. doi: 10.1016/0006-8993(84)91026-6. [DOI] [PubMed] [Google Scholar]
  20. Tonosaki K., Funakoshi M. Cyclic nucleotides may mediate taste transduction. Nature. 1988 Jan 28;331(6154):354–356. doi: 10.1038/331354a0. [DOI] [PubMed] [Google Scholar]
  21. Ureña J., López-López J., González C., López-Barneo J. Ionic currents in dispersed chemoreceptor cells of the mammalian carotid body. J Gen Physiol. 1989 May;93(5):979–999. doi: 10.1085/jgp.93.5.979. [DOI] [PMC free article] [PubMed] [Google Scholar]

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