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. 1998 Jun;74(6):2953–2962. doi: 10.1016/S0006-3495(98)78002-6

The N-terminus of the K channel KAT1 controls its voltage-dependent gating by altering the membrane electric field.

I Marten 1, T Hoshi 1
PMCID: PMC1299636  PMID: 9635749

Abstract

Functional roles of different domains (pore region, S4 segment, N-terminus) of the KAT1 potassium channel in its voltage-dependent gating were electrophysiologically studied in Xenopus oocytes. The KAT1 properties did not depend on the extracellular K+ concentration or on residue H267, equivalent to one of the residues known to be important in C-type inactivation in Shaker channels, indicating that the hyperpolarization-induced KAT1 inward currents are related to the channel activation rather than to recovery from inactivation. Neutralization of a positively charged amino acid in the S4 domain (R176S) reduced the gating charge movement, suggesting that it acts as a voltage-sensing residue in KAT1. N-terminal deletions alone (e.g., delta20-34) did not affect the gating charge movement. However, the deletions paradoxically increased the voltage sensitivity of the R176S mutant channel, but not that of the wild-type channel. We propose a simple model in which the N-terminus determines the KAT1 voltage sensitivity by contributing to the electric field sensed by the voltage sensor.

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Selected References

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  1. Aldrich R. W. Potassium channels. New channel subunits are a turn-off. Curr Biol. 1994 Sep 1;4(9):839–840. doi: 10.1016/s0960-9822(00)00187-1. [DOI] [PubMed] [Google Scholar]
  2. Anderson J. A., Huprikar S. S., Kochian L. V., Lucas W. J., Gaber R. F. Functional expression of a probable Arabidopsis thaliana potassium channel in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1992 May 1;89(9):3736–3740. doi: 10.1073/pnas.89.9.3736. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Auld V. J., Goldin A. L., Krafte D. S., Catterall W. A., Lester H. A., Davidson N., Dunn R. J. A neutral amino acid change in segment IIS4 dramatically alters the gating properties of the voltage-dependent sodium channel. Proc Natl Acad Sci U S A. 1990 Jan;87(1):323–327. doi: 10.1073/pnas.87.1.323. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Choi K. L., Aldrich R. W., Yellen G. Tetraethylammonium blockade distinguishes two inactivation mechanisms in voltage-activated K+ channels. Proc Natl Acad Sci U S A. 1991 Jun 15;88(12):5092–5095. doi: 10.1073/pnas.88.12.5092. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Curran M. E., Splawski I., Timothy K. W., Vincent G. M., Green E. D., Keating M. T. A molecular basis for cardiac arrhythmia: HERG mutations cause long QT syndrome. Cell. 1995 Mar 10;80(5):795–803. doi: 10.1016/0092-8674(95)90358-5. [DOI] [PubMed] [Google Scholar]
  6. Daram P., Urbach S., Gaymard F., Sentenac H., Chérel I. Tetramerization of the AKT1 plant potassium channel involves its C-terminal cytoplasmic domain. EMBO J. 1997 Jun 16;16(12):3455–3463. doi: 10.1093/emboj/16.12.3455. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Dreyer I., Antunes S., Hoshi T., Müller-Röber B., Palme K., Pongs O., Reintanz B., Hedrich R. Plant K+ channel alpha-subunits assemble indiscriminately. Biophys J. 1997 May;72(5):2143–2150. doi: 10.1016/S0006-3495(97)78857-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. García J., Nakai J., Imoto K., Beam K. G. Role of S4 segments and the leucine heptad motif in the activation of an L-type calcium channel. Biophys J. 1997 Jun;72(6):2515–2523. doi: 10.1016/S0006-3495(97)78896-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Hoshi T. Regulation of voltage dependence of the KAT1 channel by intracellular factors. J Gen Physiol. 1995 Mar;105(3):309–328. doi: 10.1085/jgp.105.3.309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. 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]
  11. Hoshi T., Zagotta W. N., Aldrich R. W. Two types of inactivation in Shaker K+ channels: effects of alterations in the carboxy-terminal region. Neuron. 1991 Oct;7(4):547–556. doi: 10.1016/0896-6273(91)90367-9. [DOI] [PubMed] [Google Scholar]
  12. Jan L. Y., Jan Y. N. Cloned potassium channels from eukaryotes and prokaryotes. Annu Rev Neurosci. 1997;20:91–123. doi: 10.1146/annurev.neuro.20.1.91. [DOI] [PubMed] [Google Scholar]
  13. Larsson H. P., Baker O. S., Dhillon D. S., Isacoff E. Y. Transmembrane movement of the shaker K+ channel S4. Neuron. 1996 Feb;16(2):387–397. doi: 10.1016/s0896-6273(00)80056-2. [DOI] [PubMed] [Google Scholar]
  14. Levy D. I., Deutsch C. Recovery from C-type inactivation is modulated by extracellular potassium. Biophys J. 1996 Feb;70(2):798–805. doi: 10.1016/S0006-3495(96)79619-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Li M., Jan Y. N., Jan L. Y. Specification of subunit assembly by the hydrophilic amino-terminal domain of the Shaker potassium channel. Science. 1992 Aug 28;257(5074):1225–1230. doi: 10.1126/science.1519059. [DOI] [PubMed] [Google Scholar]
  16. López-Barneo J., Hoshi T., Heinemann S. H., Aldrich R. W. Effects of external cations and mutations in the pore region on C-type inactivation of Shaker potassium channels. Receptors Channels. 1993;1(1):61–71. [PubMed] [Google Scholar]
  17. Mannuzzu L. M., Moronne M. M., Isacoff E. Y. Direct physical measure of conformational rearrangement underlying potassium channel gating. Science. 1996 Jan 12;271(5246):213–216. doi: 10.1126/science.271.5246.213. [DOI] [PubMed] [Google Scholar]
  18. Marten I., Hoshi T. Voltage-dependent gating characteristics of the K+ channel KAT1 depend on the N and C termini. Proc Natl Acad Sci U S A. 1997 Apr 1;94(7):3448–3453. doi: 10.1073/pnas.94.7.3448. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. McCormack K., Tanouye M. A., Iverson L. E., Lin J. W., Ramaswami M., McCormack T., Campanelli J. T., Mathew M. K., Rudy B. A role for hydrophobic residues in the voltage-dependent gating of Shaker K+ channels. Proc Natl Acad Sci U S A. 1991 Apr 1;88(7):2931–2935. doi: 10.1073/pnas.88.7.2931. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Miller A. G., Aldrich R. W. Conversion of a delayed rectifier K+ channel to a voltage-gated inward rectifier K+ channel by three amino acid substitutions. Neuron. 1996 Apr;16(4):853–858. doi: 10.1016/s0896-6273(00)80105-1. [DOI] [PubMed] [Google Scholar]
  21. Ogielska E. M., Zagotta W. N., Hoshi T., Heinemann S. H., Haab J., Aldrich R. W. Cooperative subunit interactions in C-type inactivation of K channels. Biophys J. 1995 Dec;69(6):2449–2457. doi: 10.1016/S0006-3495(95)80114-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Papazian D. M., Shao X. M., Seoh S. A., Mock A. F., Huang Y., Wainstock D. H. Electrostatic interactions of S4 voltage sensor in Shaker K+ channel. Neuron. 1995 Jun;14(6):1293–1301. doi: 10.1016/0896-6273(95)90276-7. [DOI] [PubMed] [Google Scholar]
  23. Pardo L. A., Heinemann S. H., Terlau H., Ludewig U., Lorra C., Pongs O., Stühmer W. Extracellular K+ specifically modulates a rat brain K+ channel. Proc Natl Acad Sci U S A. 1992 Mar 15;89(6):2466–2470. doi: 10.1073/pnas.89.6.2466. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Pearson R. B., Kemp B. E. Protein kinase phosphorylation site sequences and consensus specificity motifs: tabulations. Methods Enzymol. 1991;200:62–81. doi: 10.1016/0076-6879(91)00127-i. [DOI] [PubMed] [Google Scholar]
  25. Rettig J., Heinemann S. H., Wunder F., Lorra C., Parcej D. N., Dolly J. O., Pongs O. Inactivation properties of voltage-gated K+ channels altered by presence of beta-subunit. Nature. 1994 May 26;369(6478):289–294. doi: 10.1038/369289a0. [DOI] [PubMed] [Google Scholar]
  26. Sanguinetti M. C., Jiang C., Curran M. E., Keating M. T. A mechanistic link between an inherited and an acquired cardiac arrhythmia: HERG encodes the IKr potassium channel. Cell. 1995 Apr 21;81(2):299–307. doi: 10.1016/0092-8674(95)90340-2. [DOI] [PubMed] [Google Scholar]
  27. Schachtman D. P., Schroeder J. I., Lucas W. J., Anderson J. A., Gaber R. F. Expression of an inward-rectifying potassium channel by the Arabidopsis KAT1 cDNA. Science. 1992 Dec 4;258(5088):1654–1658. doi: 10.1126/science.8966547. [DOI] [PubMed] [Google Scholar]
  28. Schlief T., Schönherr R., Heinemann S. H. Modification of C-type inactivating Shaker potassium channels by chloramine-T. Pflugers Arch. 1996 Feb;431(4):483–493. doi: 10.1007/BF02191894. [DOI] [PubMed] [Google Scholar]
  29. Schönherr R., Heinemann S. H. Molecular determinants for activation and inactivation of HERG, a human inward rectifier potassium channel. J Physiol. 1996 Jun 15;493(Pt 3):635–642. doi: 10.1113/jphysiol.1996.sp021410. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Seoh S. A., Sigg D., Papazian D. M., Bezanilla F. Voltage-sensing residues in the S2 and S4 segments of the Shaker K+ channel. Neuron. 1996 Jun;16(6):1159–1167. doi: 10.1016/s0896-6273(00)80142-7. [DOI] [PubMed] [Google Scholar]
  31. Sigworth F. J. Voltage gating of ion channels. Q Rev Biophys. 1994 Feb;27(1):1–40. doi: 10.1017/s0033583500002894. [DOI] [PubMed] [Google Scholar]
  32. Smith P. L., Baukrowitz T., Yellen G. The inward rectification mechanism of the HERG cardiac potassium channel. Nature. 1996 Feb 29;379(6568):833–836. doi: 10.1038/379833a0. [DOI] [PubMed] [Google Scholar]
  33. Spector P. S., Curran M. E., Zou A., Keating M. T., Sanguinetti M. C. Fast inactivation causes rectification of the IKr channel. J Gen Physiol. 1996 May;107(5):611–619. doi: 10.1085/jgp.107.5.611. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Terlau H., Heinemann S. H., Stühmer W., Pongs O., Ludwig J. Amino terminal-dependent gating of the potassium channel rat eag is compensated by a mutation in the S4 segment. J Physiol. 1997 Aug 1;502(Pt 3):537–543. doi: 10.1111/j.1469-7793.1997.537bj.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Tiwari-Woodruff S. K., Schulteis C. T., Mock A. F., Papazian D. M. Electrostatic interactions between transmembrane segments mediate folding of Shaker K+ channel subunits. Biophys J. 1997 Apr;72(4):1489–1500. doi: 10.1016/S0006-3495(97)78797-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Trudeau M. C., Warmke J. W., Ganetzky B., Robertson G. A. HERG, a human inward rectifier in the voltage-gated potassium channel family. Science. 1995 Jul 7;269(5220):92–95. doi: 10.1126/science.7604285. [DOI] [PubMed] [Google Scholar]
  37. Véry A. A., Gaymard F., Bosseux C., Sentenac H., Thibaud J. B. Expression of a cloned plant K+ channel in Xenopus oocytes: analysis of macroscopic currents. Plant J. 1995 Feb;7(2):321–332. doi: 10.1046/j.1365-313x.1995.7020321.x. [DOI] [PubMed] [Google Scholar]
  38. Warmke J. W., Ganetzky B. A family of potassium channel genes related to eag in Drosophila and mammals. Proc Natl Acad Sci U S A. 1994 Apr 12;91(8):3438–3442. doi: 10.1073/pnas.91.8.3438. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Zagotta W. N., Hoshi T., Dittman J., Aldrich R. W. Shaker potassium channel gating. II: Transitions in the activation pathway. J Gen Physiol. 1994 Feb;103(2):279–319. doi: 10.1085/jgp.103.2.279. [DOI] [PMC free article] [PubMed] [Google Scholar]

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