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. 1997 Feb 1;498(Pt 3):649–662. doi: 10.1113/jphysiol.1997.sp021890

A novel oxygen-sensitive potassium current in rat carotid body type I cells.

K J Buckler 1
PMCID: PMC1159182  PMID: 9051577

Abstract

1. Hypoxic stimuli depolarize carotid body type I cells causing voltage-gated calcium influx. This study investigates the cause of this membrane depolarization. Isolated type I cells from neonatal (11-16 day) rat carotid bodies were used in the experiments. 2. Tetraethylammonium (TEA; 10 mM), 1 and 5 mM 4-aminopyridine (4-AP) and 20 nM charybdotoxin all failed to evoke a significant rise in [Ca2+]i. Similarly, in perforated patch whole-cell recordings, a combination of 10 mM TEA and 5 mM 4-AP failed to depolarize type I cells. 3. In type I cells voltage clamped at -70 mV, anoxia evoked a small inward current under control conditions, but had no effect in the absence of pipette and extracellular K+. 4. Anoxia decreased resting membrane conductance from 322 to 131 pS. The anoxia-sensitive current (measured using voltage ramps from -100 to -40 mV) had a reversal potential of -89 mV in 4.5 mM Ko+ and -66 mV in 20 mM Ko+, indicating that this current was carried principally by potassium ions. In contrast, 10 mM TEA + 5 mM 4-AP had little effect on the current-voltage relationship of the cells over the same range. 5. This O2-sensitive K+ conductance showed only mild outward rectification over the range -90 to +30 mV, which could be approximated by the Goldman-Hodgkin-Katz current equation. In addition, there was no time-dependent activation or inactivation of membrane currents elicited by voltage steps in the range -100 to -30 mV. 6. The O2-sensitive K+ conductance was inhibited by graded reductions in PO2 to 40 Torr and below, with a K1/2 of about 12 Torr. 7. The data suggest that hypoxia depolarizes type I cells principally through the inhibition of a small voltage-insensitive resting (or background) K+ conductance, and not through the inhibition of voltage-gated TEA and 4-AP-sensitive K+ channels (e.g. maxi-K or KO2 channels), as has been previously suggested.

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Selected References

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  1. Archer S. L., Huang J. M., Reeve H. L., Hampl V., Tolarová S., Michelakis E., Weir E. K. Differential distribution of electrophysiologically distinct myocytes in conduit and resistance arteries determines their response to nitric oxide and hypoxia. Circ Res. 1996 Mar;78(3):431–442. doi: 10.1161/01.res.78.3.431. [DOI] [PubMed] [Google Scholar]
  2. Biscoe T. J., Duchen M. R. Responses of type I cells dissociated from the rabbit carotid body to hypoxia. J Physiol. 1990 Sep;428:39–59. doi: 10.1113/jphysiol.1990.sp018199. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Buckler K. J., Vaughan-Jones R. D. Effects of acidic stimuli on intracellular calcium in isolated type I cells of the neonatal rat carotid body. Pflugers Arch. 1993 Oct;425(1-2):22–27. doi: 10.1007/BF00374499. [DOI] [PubMed] [Google Scholar]
  4. Buckler K. J., Vaughan-Jones R. D. Effects of hypercapnia on membrane potential and intracellular calcium in rat carotid body type I cells. J Physiol. 1994 Jul 1;478(Pt 1):157–171. doi: 10.1113/jphysiol.1994.sp020239. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Buckler K. J., Vaughan-Jones R. D. Effects of hypoxia on membrane potential and intracellular calcium in rat neonatal carotid body type I cells. J Physiol. 1994 May 1;476(3):423–428. doi: 10.1113/jphysiol.1994.sp020143. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cheng P. M., Donnelly D. F. Relationship between changes of glomus cell current and neural response of rat carotid body. J Neurophysiol. 1995 Nov;74(5):2077–2086. doi: 10.1152/jn.1995.74.5.2077. [DOI] [PubMed] [Google Scholar]
  7. Delpiano M. A., Hescheler J. Evidence for a PO2-sensitive K+ channel in the type-I cell of the rabbit carotid body. FEBS Lett. 1989 Jun 5;249(2):195–198. doi: 10.1016/0014-5793(89)80623-4. [DOI] [PubMed] [Google Scholar]
  8. Doyle T. P., Donnelly D. F. Effect of Na+ and K+ channel blockade on baseline and anoxia-induced catecholamine release from rat carotid body. J Appl Physiol (1985) 1994 Dec;77(6):2606–2611. doi: 10.1152/jappl.1994.77.6.2606. [DOI] [PubMed] [Google Scholar]
  9. Duchen M. R., Biscoe T. J. Relative mitochondrial membrane potential and [Ca2+]i in type I cells isolated from the rabbit carotid body. J Physiol. 1992 May;450:33–61. doi: 10.1113/jphysiol.1992.sp019115. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Duchen M. R., Caddy K. W., Kirby G. C., Patterson D. L., Ponte J., Biscoe T. J. Biophysical studies of the cellular elements of the rabbit carotid body. Neuroscience. 1988 Jul;26(1):291–311. doi: 10.1016/0306-4522(88)90146-7. [DOI] [PubMed] [Google Scholar]
  11. Franco-Obregón A., López-Barneo J. Differential oxygen sensitivity of calcium channels in rabbit smooth muscle cells of conduit and resistance pulmonary arteries. J Physiol. 1996 Mar 1;491(Pt 2):511–518. doi: 10.1113/jphysiol.1996.sp021235. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Ganfornina M. D., López-Barneo J. Potassium channel types in arterial chemoreceptor cells and their selective modulation by oxygen. J Gen Physiol. 1992 Sep;100(3):401–426. doi: 10.1085/jgp.100.3.401. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Ganfornina M. D., López-Barneo J. Single K+ channels in membrane patches of arterial chemoreceptor cells are modulated by O2 tension. Proc Natl Acad Sci U S A. 1991 Apr 1;88(7):2927–2930. doi: 10.1073/pnas.88.7.2927. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. González C., Almaraz L., Obeso A., Rigual R. Oxygen and acid chemoreception in the carotid body chemoreceptors. Trends Neurosci. 1992 Apr;15(4):146–153. doi: 10.1016/0166-2236(92)90357-e. [DOI] [PubMed] [Google Scholar]
  15. Koyano K., Tanaka K., Kuba K. A patch-clamp study on the muscarine-sensitive potassium channel in bullfrog sympathetic ganglion cells. J Physiol. 1992 Aug;454:231–246. doi: 10.1113/jphysiol.1992.sp019262. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Lahiri S., Rumsey W. L., Wilson D. F., Iturriaga R. Contribution of in vivo microvascular PO2 in the cat carotid body chemotransduction. J Appl Physiol (1985) 1993 Sep;75(3):1035–1043. doi: 10.1152/jappl.1993.75.3.1035. [DOI] [PubMed] [Google Scholar]
  17. López-López J. R., De Luis D. A., Gonzalez C. Properties of a transient K+ current in chemoreceptor cells of rabbit carotid body. J Physiol. 1993 Jan;460:15–32. doi: 10.1113/jphysiol.1993.sp019456. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. López-López J., González C., Ureña J., López-Barneo J. Low pO2 selectively inhibits K channel activity in chemoreceptor cells of the mammalian carotid body. J Gen Physiol. 1989 May;93(5):1001–1015. doi: 10.1085/jgp.93.5.1001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Montoro R. J., Ureña J., Fernández-Chacón R., Alvarez de Toledo G., López-Barneo J. Oxygen sensing by ion channels and chemotransduction in single glomus cells. J Gen Physiol. 1996 Jan;107(1):133–143. doi: 10.1085/jgp.107.1.133. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Peers C. Hypoxic suppression of K+ currents in type I carotid body cells: selective effect on the Ca2(+)-activated K+ current. Neurosci Lett. 1990 Nov 13;119(2):253–256. doi: 10.1016/0304-3940(90)90846-2. [DOI] [PubMed] [Google Scholar]
  21. Shen K. Z., North R. A., Surprenant A. Potassium channels opened by noradrenaline and other transmitters in excised membrane patches of guinea-pig submucosal neurones. J Physiol. 1992 Jan;445:581–599. doi: 10.1113/jphysiol.1992.sp018941. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Shuster M. J., Siegelbaum S. A. Pharmacological characterization of the serotonin-sensitive potassium channel of Aplysia sensory neurons. J Gen Physiol. 1987 Oct;90(4):587–608. doi: 10.1085/jgp.90.4.587. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Siegelbaum S. A., Camardo J. S., Kandel E. R. Serotonin and cyclic AMP close single K+ channels in Aplysia sensory neurones. Nature. 1982 Sep 30;299(5882):413–417. doi: 10.1038/299413a0. [DOI] [PubMed] [Google Scholar]
  24. Stea A., Nurse C. A. Whole-cell and perforated-patch recordings from O2-sensitive rat carotid body cells grown in short- and long-term culture. Pflugers Arch. 1991 Mar;418(1-2):93–101. doi: 10.1007/BF00370457. [DOI] [PubMed] [Google Scholar]
  25. 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]
  26. Wyatt C. N., Peers C. Ca(2+)-activated K+ channels in isolated type I cells of the neonatal rat carotid body. J Physiol. 1995 Mar 15;483(Pt 3):559–565. doi: 10.1113/jphysiol.1995.sp020606. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Wyatt C. N., Wright C., Bee D., Peers C. O2-sensitive K+ currents in carotid body chemoreceptor cells from normoxic and chronically hypoxic rats and their roles in hypoxic chemotransduction. Proc Natl Acad Sci U S A. 1995 Jan 3;92(1):295–299. doi: 10.1073/pnas.92.1.295. [DOI] [PMC free article] [PubMed] [Google Scholar]

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