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J Gen Physiol. Feb 1, 1994; 103(2): 279–319.
PMCID: PMC2216838

Shaker potassium channel gating. II: Transitions in the activation pathway

Abstract

Voltage-dependent gating behavior of Shaker potassium channels without N-type inactivation (ShB delta 6-46) expressed in Xenopus oocytes was studied. The voltage dependence of the steady-state open probability indicated that the activation process involves the movement of the equivalent of 12-16 electronic charges across the membrane. The sigmoidal kinetics of the activation process, which is maintained at depolarized voltages up to at least +100 mV indicate the presence of at least five sequential conformational changes before opening. The voltage dependence of the gating charge movement suggested that each elementary transition involves 3.5 electronic charges. The voltage dependence of the forward opening rate, as estimated by the single- channel first latency distribution, the final phase of the macroscopic ionic current activation, the ionic current reactivation and the ON gating current time course, showed movement of the equivalent of 0.3 to 0.5 electronic charges were associated with a large number of the activation transitions. The equivalent charge movement of 1.1 electronic charges was associated with the closing conformational change. The results were generally consistent with models involving a number of independent and identical transitions with a major exception that the first closing transition is slower than expected as indicated by tail current and OFF gating charge measurements.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Almers W. Gating currents and charge movements in excitable membranes. Rev Physiol Biochem Pharmacol. 1978;82:96–190. [PubMed]
  • Andersen OS, Koeppe RE., 2nd Molecular determinants of channel function. Physiol Rev. 1992 Oct;72(4 Suppl):S89–158. [PubMed]
  • Armstrong CM. Sodium channels and gating currents. Physiol Rev. 1981 Jul;61(3):644–683. [PubMed]
  • Armstrong CM, Bezanilla F. Charge movement associated with the opening and closing of the activation gates of the Na channels. J Gen Physiol. 1974 May;63(5):533–552. [PMC free article] [PubMed]
  • Ascher P, Marty A, Neild TO. Life time and elementary conductance of the channels mediating the excitatory effects of acetylcholine in Aplysia neurones. J Physiol. 1978 May;278:177–206. [PMC free article] [PubMed]
  • Bezanilla F, Perozo E, Papazian DM, Stefani E. Molecular basis of gating charge immobilization in Shaker potassium channels. Science. 1991 Nov 1;254(5032):679–683. [PubMed]
  • Cahalan MD, Chandy KG, DeCoursey TE, Gupta S. A voltage-gated potassium channel in human T lymphocytes. J Physiol. 1985 Jan;358:197–237. [PMC free article] [PubMed]
  • COLE KS, MOORE JW. Potassium ion current in the squid giant axon: dynamic characteristic. Biophys J. 1960 Sep;1:1–14. [PMC free article] [PubMed]
  • Durell SR, Guy HR. Atomic scale structure and functional models of voltage-gated potassium channels. Biophys J. 1992 Apr;62(1):238–250. [PMC free article] [PubMed]
  • Gautam M, Tanouye MA. Alteration of potassium channel gating: molecular analysis of the Drosophila Sh5 mutation. Neuron. 1990 Jul;5(1):67–73. [PubMed]
  • Gilly WF, Armstrong CM. Gating current and potassium channels in the giant axon of the squid. Biophys J. 1980 Mar;29(3):485–492. [PMC free article] [PubMed]
  • Gilly WF, Armstrong CM. Divalent cations and the activation kinetics of potassium channels in squid giant axons. J Gen Physiol. 1982 Jun;79(6):965–996. [PMC free article] [PubMed]
  • Greenblatt RE, Blatt Y, Montal M. The structure of the voltage-sensitive sodium channel. Inferences derived from computer-aided analysis of the Electrophorus electricus channel primary structure. FEBS Lett. 1985 Dec 2;193(2):125–134. [PubMed]
  • Guy HR, Seetharamulu P. Molecular model of the action potential sodium channel. Proc Natl Acad Sci U S A. 1986 Jan;83(2):508–512. [PMC free article] [PubMed]
  • Hill TL, Chen YD. On the theory of ion transport across the nerve membrane. 3. Potassium ion kinetics and cooperativity (with x=4,6,9). Proc Natl Acad Sci U S A. 1971 Oct;68(10):2488–2492. [PMC free article] [PubMed]
  • Hill TL, Chen YD. On the theory of ion transport across the nerve membrane. II. Potassium ion kinetics and cooperativity (with x = 4). Proc Natl Acad Sci U S A. 1971 Aug;68(8):1711–1715. [PMC free article] [PubMed]
  • HODGKIN AL, HUXLEY AF. A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol. 1952 Aug;117(4):500–544. [PMC free article] [PubMed]
  • Hoshi T, Zagotta WN, Aldrich RW. Shaker potassium channel gating. I: Transitions near the open state. J Gen Physiol. 1994 Feb;103(2):249–278. [PMC free article] [PubMed]
  • Hurst RS, Kavanaugh MP, Yakel J, Adelman JP, North RA. Cooperative interactions among subunits of a voltage-dependent potassium channel. Evidence from expression of concatenated cDNAs. J Biol Chem. 1992 Nov 25;267(33):23742–23745. [PubMed]
  • Iverson LE, Tanouye MA, Lester HA, Davidson N, Rudy B. A-type potassium channels expressed from Shaker locus cDNA. Proc Natl Acad Sci U S A. 1988 Aug;85(15):5723–5727. [PMC free article] [PubMed]
  • Kamb A, Tseng-Crank J, Tanouye MA. Multiple products of the Drosophila Shaker gene may contribute to potassium channel diversity. Neuron. 1988 Jul;1(5):421–430. [PubMed]
  • Koren G, Liman ER, Logothetis DE, Nadal-Ginard B, Hess P. Gating mechanism of a cloned potassium channel expressed in frog oocytes and mammalian cells. Neuron. 1990 Jan;4(1):39–51. [PubMed]
  • Lichtinghagen R, Stocker M, Wittka R, Boheim G, Stühmer W, Ferrus A, Pongs O. Molecular basis of altered excitability in Shaker mutants of Drosophila melanogaster. EMBO J. 1990 Dec;9(13):4399–4407. [PMC free article] [PubMed]
  • Liman ER, 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. [PubMed]
  • Liman ER, Tytgat J, Hess P. Subunit stoichiometry of a mammalian K+ channel determined by construction of multimeric cDNAs. Neuron. 1992 Nov;9(5):861–871. [PubMed]
  • Lopez GA, Jan YN, Jan LY. Hydrophobic substitution mutations in the S4 sequence alter voltage-dependent gating in Shaker K+ channels. Neuron. 1991 Aug;7(2):327–336. [PubMed]
  • MacKinnon R. Determination of the subunit stoichiometry of a voltage-activated potassium channel. Nature. 1991 Mar 21;350(6315):232–235. [PubMed]
  • Marchais D, Marty A. Interaction of permeant ions with channels activated by acetylcholine in Aplysia neurones. J Physiol. 1979 Dec;297(0):9–45. [PMC free article] [PubMed]
  • Matteson DR, Swenson RP., Jr External monovalent cations that impede the closing of K channels. J Gen Physiol. 1986 May;87(5):795–816. [PMC free article] [PubMed]
  • McCormack K, Tanouye MA, Iverson LE, Lin JW, Ramaswami M, McCormack T, Campanelli JT, Mathew MK, 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. [PMC free article] [PubMed]
  • Noda M, Ikeda T, Suzuki H, Takeshima H, Takahashi T, Kuno M, Numa S. Expression of functional sodium channels from cloned cDNA. Nature. 322(6082):826–828. [PubMed]
  • Oxford GS. Some kinetic and steady-state properties of sodium channels after removal of inactivation. J Gen Physiol. 1981 Jan;77(1):1–22. [PMC free article] [PubMed]
  • Papazian DM, Timpe LC, Jan YN, Jan LY. Alteration of voltage-dependence of Shaker potassium channel by mutations in the S4 sequence. Nature. 1991 Jan 24;349(6307):305–310. [PubMed]
  • Perozo E, Papazian DM, Stefani E, Bezanilla F. Gating currents in Shaker K+ channels. Implications for activation and inactivation models. Biophys J. 1992 Apr;62(1):160–171. [PMC free article] [PubMed]
  • Pongs O, Kecskemethy N, Müller R, Krah-Jentgens I, Baumann A, Kiltz HH, Canal I, Llamazares S, Ferrus A. Shaker encodes a family of putative potassium channel proteins in the nervous system of Drosophila. EMBO J. 1988 Apr;7(4):1087–1096. [PMC free article] [PubMed]
  • Rojas E, Keynes RD. On the relation between displacement currents and activation of the sodium conductance in the squid giant axon. Philos Trans R Soc Lond B Biol Sci. 1975 Jun 10;270(908):459–482. [PubMed]
  • Sala S, Matteson DR. Voltage-dependent slowing of K channel closing kinetics by Rb+. J Gen Physiol. 1991 Sep;98(3):535–554. [PMC free article] [PubMed]
  • Schoppa NE, McCormack K, Tanouye MA, Sigworth FJ. The size of gating charge in wild-type and mutant Shaker potassium channels. Science. 1992 Mar 27;255(5052):1712–1715. [PubMed]
  • Shapiro MS, DeCoursey TE. Permeant ion effects on the gating kinetics of the type L potassium channel in mouse lymphocytes. J Gen Physiol. 1991 Jun;97(6):1251–1278. [PMC free article] [PubMed]
  • Shapiro MS, DeCoursey TE. Selectivity and gating of the type L potassium channel in mouse lymphocytes. J Gen Physiol. 1991 Jun;97(6):1227–1250. [PMC free article] [PubMed]
  • Spruce AE, Standen NB, Stanfield PR. Rubidium ions and the gating of delayed rectifier potassium channels of frog skeletal muscle. J Physiol. 1989 Apr;411:597–610. [PMC free article] [PubMed]
  • Stühmer W, Conti F, Stocker M, Pongs O, Heinemann SH. Gating currents of inactivating and non-inactivating potassium channels expressed in Xenopus oocytes. Pflugers Arch. 1991 May;418(4):423–429. [PubMed]
  • Stühmer W, Conti F, Suzuki H, Wang XD, Noda M, Yahagi N, Kubo H, Numa S. Structural parts involved in activation and inactivation of the sodium channel. Nature. 1989 Jun 22;339(6226):597–603. [PubMed]
  • Swenson RP, Jr, Armstrong CM. K+ channels close more slowly in the presence of external K+ and Rb+. Nature. 1981 Jun 4;291(5814):427–429. [PubMed]
  • Taglialatela M, Kirsch GE, VanDongen AM, Drewe JA, Hartmann HA, Joho RH, Stefani E, Brown AM. Gating currents from a delayed rectifier K+ channel with altered pore structure and function. Biophys J. 1992 Apr;62(1):34–36. [PMC free article] [PubMed]
  • Taglialatela M, Toro L, Stefani E. Novel voltage clamp to record small, fast currents from ion channels expressed in Xenopus oocytes. Biophys J. 1992 Jan;61(1):78–82. [PMC free article] [PubMed]
  • Taylor RE, Bezanilla F. Sodium and gating current time shifts resulting from changes in initial conditions. J Gen Physiol. 1983 Jun;81(6):773–784. [PMC free article] [PubMed]
  • Tempel BL, Papazian DM, Schwarz TL, Jan YN, Jan LY. Sequence of a probable potassium channel component encoded at Shaker locus of Drosophila. Science. 1987 Aug 14;237(4816):770–775. [PubMed]
  • Timpe LC, Jan YN, Jan LY. Four cDNA clones from the Shaker locus of Drosophila induce kinetically distinct A-type potassium currents in Xenopus oocytes. Neuron. 1988 Oct;1(8):659–667. [PubMed]
  • Tytgat J, Hess P. Evidence for cooperative interactions in potassium channel gating. Nature. 1992 Oct 1;359(6394):420–423. [PubMed]
  • Vandenberg CA, Bezanilla F. A sodium channel gating model based on single channel, macroscopic ionic, and gating currents in the squid giant axon. Biophys J. 1991 Dec;60(6):1511–1533. [PMC free article] [PubMed]
  • White MM, Bezanilla F. Activation of squid axon K+ channels. Ionic and gating current studies. J Gen Physiol. 1985 Apr;85(4):539–554. [PMC free article] [PubMed]
  • Zagotta WN, Aldrich RW. Alterations in activation gating of single Shaker A-type potassium channels by the Sh5 mutation. J Neurosci. 1990 Jun;10(6):1799–1810. [PubMed]
  • Zagotta WN, Aldrich RW. Voltage-dependent gating of Shaker A-type potassium channels in Drosophila muscle. J Gen Physiol. 1990 Jan;95(1):29–60. [PMC free article] [PubMed]
  • Zagotta WN, Hoshi T, Aldrich RW. Shaker potassium channel gating. III: Evaluation of kinetic models for activation. J Gen Physiol. 1994 Feb;103(2):321–362. [PMC free article] [PubMed]

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