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. 2001 May;80(5):2216–2220. doi: 10.1016/S0006-3495(01)76194-2

Revisiting the role of Ca2+ in Shaker K+ channel gating.

K H Hong 1, C M Armstrong 1, C Miller 1
PMCID: PMC1301413  PMID: 11325724

Abstract

Shaker K+ channels were expressed in outside-out macropatches excised from Xenopus oocytes, and the effects on gating of removal of extracellular Ca2+ were examined in the complete absence of intracellular divalent cations. Removal of extracellular Ca2+ by perfusion with EDTA-containing solution caused a small negative shift in the channel's voltage-activation curve and led to an increased nonselective leak, but did not otherwise alter or disrupt the channels. The results contradict the proposal that Ca2+ is an essential component required for maintenance of ion selectivity and proper gating of Kv-type K+ channels. The large nonselective leak in Ca2+-free conditions was found to be a patch-seal phenomenon related to F- ion in the recording pipette.

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Selected References

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  1. Armstrong C. M., Cota G. Calcium block of Na+ channels and its effect on closing rate. Proc Natl Acad Sci U S A. 1999 Mar 30;96(7):4154–4157. doi: 10.1073/pnas.96.7.4154. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Armstrong C. M. Distinguishing surface effects of calcium ion from pore-occupancy effects in Na+ channels. Proc Natl Acad Sci U S A. 1999 Mar 30;96(7):4158–4163. doi: 10.1073/pnas.96.7.4158. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Armstrong C. M. Interaction of tetraethylammonium ion derivatives with the potassium channels of giant axons. J Gen Physiol. 1971 Oct;58(4):413–437. doi: 10.1085/jgp.58.4.413. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Armstrong C. M., Lopez-Barneo J. External calcium ions are required for potassium channel gating in squid neurons. Science. 1987 May 8;236(4802):712–714. doi: 10.1126/science.2437654. [DOI] [PubMed] [Google Scholar]
  5. Armstrong C. M., Matteson D. R. The role of calcium ions in the closing of K channels. J Gen Physiol. 1986 May;87(5):817–832. doi: 10.1085/jgp.87.5.817. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Armstrong C. M., Miller C. Do voltage-dependent K+ channels require Ca2+? A critical test employing a heterologous expression system. Proc Natl Acad Sci U S A. 1990 Oct;87(19):7579–7582. doi: 10.1073/pnas.87.19.7579. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Campbell D. T., Hille B. Kinetic and pharmacological properties of the sodium channel of frog skeletal muscle. J Gen Physiol. 1976 Mar;67(3):309–323. doi: 10.1085/jgp.67.3.309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cha A., Snyder G. E., Selvin P. R., Bezanilla F. Atomic scale movement of the voltage-sensing region in a potassium channel measured via spectroscopy. Nature. 1999 Dec 16;402(6763):809–813. doi: 10.1038/45552. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. FRANKENHAEUSER B., HODGKIN A. L. The action of calcium on the electrical properties of squid axons. J Physiol. 1957 Jul 11;137(2):218–244. doi: 10.1113/jphysiol.1957.sp005808. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Goldstein S. A., Miller C. A point mutation in a Shaker K+ channel changes its charybdotoxin binding site from low to high affinity. Biophys J. 1992 Apr;62(1):5–7. doi: 10.1016/S0006-3495(92)81760-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Grissmer S., Cahalan M. D. Divalent ion trapping inside potassium channels of human T lymphocytes. J Gen Physiol. 1989 Apr;93(4):609–630. doi: 10.1085/jgp.93.4.609. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hoshi T., Zagotta W. N., Aldrich R. W. Biophysical and molecular mechanisms of Shaker potassium channel inactivation. Science. 1990 Oct 26;250(4980):533–538. doi: 10.1126/science.2122519. [DOI] [PubMed] [Google Scholar]
  14. Jiang Y., MacKinnon R. The barium site in a potassium channel by x-ray crystallography. J Gen Physiol. 2000 Mar;115(3):269–272. doi: 10.1085/jgp.115.3.269. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Liman E. R., Hess P., Weaver F., Koren G. Voltage-sensing residues in the S4 region of a mammalian K+ channel. Nature. 1991 Oct 24;353(6346):752–756. doi: 10.1038/353752a0. [DOI] [PubMed] [Google Scholar]
  16. Liu Y., Holmgren M., Jurman M. E., Yellen G. Gated access to the pore of a voltage-dependent K+ channel. Neuron. 1997 Jul;19(1):175–184. doi: 10.1016/s0896-6273(00)80357-8. [DOI] [PubMed] [Google Scholar]
  17. Schwarz T. L., Tempel B. L., Papazian D. M., Jan Y. N., Jan L. Y. Multiple potassium-channel components are produced by alternative splicing at the Shaker locus in Drosophila. Nature. 1988 Jan 14;331(6152):137–142. doi: 10.1038/331137a0. [DOI] [PubMed] [Google Scholar]
  18. Spires S., Begenisich T. Chemical properties of the divalent cation binding site on potassium channels. J Gen Physiol. 1992 Aug;100(2):181–193. doi: 10.1085/jgp.100.2.181. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Spires S., Begenisich T. Modulation of potassium channel gating by external divalent cations. J Gen Physiol. 1994 Oct;104(4):675–692. doi: 10.1085/jgp.104.4.675. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Yellen G. The moving parts of voltage-gated ion channels. Q Rev Biophys. 1998 Aug;31(3):239–295. doi: 10.1017/s0033583598003448. [DOI] [PubMed] [Google Scholar]

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