Skip to main content
NCBI home page
Biophysical Journal logoLink to Biophysical Journal
. 1999 Dec;77(6):3060–3070. doi: 10.1016/S0006-3495(99)77137-7

K(+)-dependent composite gating of the yeast K(+) channel, Tok1.

S H Loukin 1, Y Saimi 1
PMCID: PMC1300577  PMID: 10585928

Abstract

TOK1 encodes an outwardly rectifying K(+) channel in the plasma membrane of the budding yeast Saccharomyces cerevisiae. It is capable of dwelling in two kinetically distinct impermeable states, a near-instantaneously activating R state and a set of related delayed activating C states (formerly called C(2) and C(1), respectively). Dwell in the R state is dependent on membrane potential and both internal and external K(+) in a manner consistent with the K(+) electrochemical potential being its determinant, where dwell in the C states is dependent on voltage and only external K(+). Whereas activation from the C states showed high temperature dependencies, typical of gating transitions in other Shaker-like channels, activation from the R state had a temperature dependence nearly as low as that of simple ionic diffusion. These findings lead us to conclude that although the C states reflect the activity of an internally oriented channel gate, the R state results from an intrinsic gating property of the channel filter region.

Full Text

The Full Text of this article is available as a PDF (162.4 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Alvarado F., Brot-Laroche E., L'Herminier M., Murer H., Stange G. The effect of harmaline on intestinal sodium transport and on sodium-dependent D-glucose transport in brush-border membrane vesicles from rabbit jejunum. Pflugers Arch. 1979 Oct;382(1):35–41. doi: 10.1007/BF00585901. [DOI] [PubMed] [Google Scholar]
  2. Baukrowitz T., Yellen G. Use-dependent blockers and exit rate of the last ion from the multi-ion pore of a K+ channel. Science. 1996 Feb 2;271(5249):653–656. doi: 10.1126/science.271.5249.653. [DOI] [PubMed] [Google Scholar]
  3. Beam K. G., Donaldson P. L. A quantitative study of potassium channel kinetics in rat skeletal muscle from 1 to 37 degrees C. J Gen Physiol. 1983 Apr;81(4):485–512. doi: 10.1085/jgp.81.4.485. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bertl A., Bihler H., Reid J. D., Kettner C., Slayman C. L. Physiological characterization of the yeast plasma membrane outward rectifying K+ channel, DUK1 (TOK1), in situ. J Membr Biol. 1998 Mar 1;162(1):67–80. doi: 10.1007/s002329900343. [DOI] [PubMed] [Google Scholar]
  5. Chen T. Y., Miller C. Nonequilibrium gating and voltage dependence of the ClC-0 Cl- channel. J Gen Physiol. 1996 Oct;108(4):237–250. doi: 10.1085/jgp.108.4.237. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Chiu S. Y., Mrose H. E., Ritchie J. M. Anomalous temperature dependence of the sodium conductance in rabbit nerve compared with frog nerve. Nature. 1979 May 24;279(5711):327–328. doi: 10.1038/279327a0. [DOI] [PubMed] [Google Scholar]
  7. Collins C. A., Rojas E. Temperature dependence of the sodium channel gating kinetics in the node of Ranvier. Q J Exp Physiol. 1982 Jan;67(1):41–55. doi: 10.1113/expphysiol.1982.sp002623. [DOI] [PubMed] [Google Scholar]
  8. Doyle D. A., Morais Cabral J., Pfuetzner R. A., Kuo A., Gulbis J. M., Cohen S. L., Chait B. T., MacKinnon R. The structure of the potassium channel: molecular basis of K+ conduction and selectivity. Science. 1998 Apr 3;280(5360):69–77. doi: 10.1126/science.280.5360.69. [DOI] [PubMed] [Google Scholar]
  9. Dudel J., Rüdel R. Voltage and time dependence of excitatory sodium current in cooled sheep Purkinje fibres. Pflugers Arch. 1970;315(2):136–158. doi: 10.1007/BF00586657. [DOI] [PubMed] [Google Scholar]
  10. FRANKENHAEUSER B., MOORE L. E. THE EFFECT OF TEMPERATURE ON THE SODIUM AND POTASSIUM PERMEABILITY CHANGES IN MYELINATED NERVE FIBRES OF XENOPUS LAEVIS. J Physiol. 1963 Nov;169:431–437. doi: 10.1113/jphysiol.1963.sp007269. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gustin M. C., Martinac B., Saimi Y., Culbertson M. R., Kung C. Ion channels in yeast. Science. 1986 Sep 12;233(4769):1195–1197. doi: 10.1126/science.2426783. [DOI] [PubMed] [Google Scholar]
  12. HODGKIN A. L., KATZ B. The effect of temperature on the electrical activity of the giant axon of the squid. J Physiol. 1949 Aug;109(1-2):240–249. doi: 10.1113/jphysiol.1949.sp004388. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Ketchum K. A., Joiner W. J., Sellers A. J., Kaczmarek L. K., Goldstein S. A. A new family of outwardly rectifying potassium channel proteins with two pore domains in tandem. Nature. 1995 Aug 24;376(6542):690–695. doi: 10.1038/376690a0. [DOI] [PubMed] [Google Scholar]
  14. Kiss L., Immke D., LoTurco J., Korn S. J. The interaction of Na+ and K+ in voltage-gated potassium channels. Evidence for cation binding sites of different affinity. J Gen Physiol. 1998 Feb;111(2):195–206. doi: 10.1085/jgp.111.2.195. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kiss L., Korn S. J. Modulation of C-type inactivation by K+ at the potassium channel selectivity filter. Biophys J. 1998 Apr;74(4):1840–1849. doi: 10.1016/S0006-3495(98)77894-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Lesage F., Guillemare E., Fink M., Duprat F., Lazdunski M., Romey G., Barhanin J. A pH-sensitive yeast outward rectifier K+ channel with two pore domains and novel gating properties. J Biol Chem. 1996 Feb 23;271(8):4183–4187. doi: 10.1074/jbc.271.8.4183. [DOI] [PubMed] [Google Scholar]
  17. Loukin S. H., Vaillant B., Zhou X. L., Spalding E. P., Kung C., Saimi Y. Random mutagenesis reveals a region important for gating of the yeast K+ channel Ykc1. EMBO J. 1997 Aug 15;16(16):4817–4825. doi: 10.1093/emboj/16.16.4817. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Miosga T., Witzel A., Zimmermann F. K. Sequence and function analysis of a 9.46 kb fragment of Saccharomyces cerevisiae chromosome X. Yeast. 1994 Jul;10(7):965–973. doi: 10.1002/yea.320100712. [DOI] [PubMed] [Google Scholar]
  19. Moore L. E. Effect of temperature and calcium ions on rate constants of myelinated nerve. Am J Physiol. 1971 Jul;221(1):131–137. doi: 10.1152/ajplegacy.1971.221.1.131. [DOI] [PubMed] [Google Scholar]
  20. Reid J. D., Lukas W., Shafaatian R., Bertl A., Scheurmann-Kettner C., Guy H. R., North R. A. The S. cerevisiae outwardly-rectifying potassium channel (DUK1) identifies a new family of channels with duplicated pore domains. Receptors Channels. 1996;4(1):51–62. [PubMed] [Google Scholar]
  21. Schauf C. L. Temperature dependence of the ionic current kinetics of Myxicola giant axons. J Physiol. 1973 Nov;235(1):197–205. doi: 10.1113/jphysiol.1973.sp010384. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Schreibmayer W., Lester H. A., Dascal N. Voltage clamping of Xenopus laevis oocytes utilizing agarose-cushion electrodes. Pflugers Arch. 1994 Mar;426(5):453–458. doi: 10.1007/BF00388310. [DOI] [PubMed] [Google Scholar]
  23. Starkus J. G., Kuschel L., Rayner M. D., Heinemann S. H. Ion conduction through C-type inactivated Shaker channels. J Gen Physiol. 1997 Nov;110(5):539–550. doi: 10.1085/jgp.110.5.539. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Starkus J. G., Kuschel L., Rayner M. D., Heinemann S. H. Macroscopic Na+ currents in the "Nonconducting" Shaker potassium channel mutant W434F. J Gen Physiol. 1998 Jul;112(1):85–93. doi: 10.1085/jgp.112.1.85. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Vergani P., Miosga T., Jarvis S. M., Blatt M. R. Extracellular K+ and Ba2+ mediate voltage-dependent inactivation of the outward-rectifying K+ channel encoded by the yeast gene TOK1. FEBS Lett. 1997 Apr 1;405(3):337–344. doi: 10.1016/s0014-5793(97)00211-1. [DOI] [PubMed] [Google Scholar]
  26. Zhou X. L., Vaillant B., Loukin S. H., Kung C., Saimi Y. YKC1 encodes the depolarization-activated K+ channel in the plasma membrane of yeast. FEBS Lett. 1995 Oct 9;373(2):170–176. doi: 10.1016/0014-5793(95)01035-d. [DOI] [PubMed] [Google Scholar]

Articles from Biophysical Journal are provided here courtesy of The Biophysical Society

RESOURCES