Determinants of voltage-dependent gating and open-state stability in the S5 segment of Shaker potassium channels

Journal of General Physiology

Volumn 114, Issue 2, 1999, Pages 215-242

  Kanevsky, Max ^a   Aldrich, Richard W ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Activation; Gating current; Ion channel; Site directed mutagenesis

Indexed keywords

ALANINE; LEUCINE; PHENYLALANINE; POTASSIUM CHANNEL; VALINE;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; CHANNEL GATING; CONTROLLED STUDY; DROSOPHILA; KINETICS; MEMBRANE POTENTIAL; MODEL; NONHUMAN; OOCYTE; PATCH CLAMP; PHENOTYPE; POINT MUTATION; SITE DIRECTED MUTAGENESIS; STEADY STATE;

ALGORITHMS; ANIMALS; DROSOPHILA; DROSOPHILA PROTEINS; ELECTRIC STIMULATION; ELECTROPHYSIOLOGY; ION CHANNEL GATING; KINETICS; MEMBRANE POTENTIALS; MUTAGENESIS, SITE-DIRECTED; MUTATION; OOCYTES; PATCH-CLAMP TECHNIQUES; PHENYLALANINE; POTASSIUM CHANNELS; SHAKER SUPERFAMILY OF POTASSIUM CHANNELS; XENOPUS;

EID: 0032770402     PISSN: 00221295     EISSN: None     Source Type: Journal    
DOI: 10.1085/jgp.114.2.215     Document Type: Article

References (93)

1. + channel. Neuron. 16: 1169-1177.
2. Alicata, D.A., M.D. Rayner, andJ.G. Starkus. 1990. Sodium channel activation mechanisms. Insights from deuterium oxide substitution. Biophys. J. 57:745-758.
3. Almers, W. 1978. Gating currents and charge movements in excitable membranes. Rev. Physiol. Biochem. Pharmacol. 82:96-190.
4. + channel gating. Neuron. 20:1283-1294.
5. Bezanilla, F., E. Perozo, D.M. Papazian, and E. Stefani. 1991. Molecular basis of gating change in Shaker potassium channels. Science. 254:679-683.
6. + channels: II. The components of gating currents and a model of channel activation. Biophys. J. 66:1011-1021.
7. Bezanilla, F., and E. Stefani. 1994. Voltage-dependent gating of ionic channels. Annu. Rev. Biophys. Biomol. Struct. 23:819-846.
8. + channel deactivation. J. Gen. Physiol. 110:87-100.
9. Cole, K.S., and J.W. Moore. 1960. Potassium ion current in the squid giant axon: dynamic characteristic. Biophys. J. 1:1-14.
10. + channel correlate with occupancy of the pore. Biophys. J. 61:639-648.
11. + conduction and selectivity. Science. 280:69-77.
12. Eriksson, A.E., W.A. Baase, and B.W. Matthews. 1993. Similar hydrophobic replacements of Leu99 and Phe153 within the core of T4 lysozyme have different structural and thermodynamic consequences. J. Mol. Biol. 229:747-769.
13. Flocco, M.M., and S.L. Mowbray. 1994. Planar stacking interactions of arginine and aromatic side-chains in proteins. J. Mol. Biol. 235: 709-717.
14. 5 mutation. Neuron. 5:67-73.
15. Hamill, O.P., A. Marty, E. Neher, B. Sakmann, and F.J. Sigworth. 1981. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers Arch. 391:85-100.
16. Hodgkin, A.L., and A.F. Huxley. 1952. A quantitative description of membrane current and its application to conduction and excitation in nerve. J. Physiol. 117:500-544.
17. Hoshi, T., W.N. Zagotta, and R.W. Aldrich. 1990. Biophysical and molecular mechanisms of Shaker potassium channel inactivation. Science. 250:533-538.
18. Hoshi, T., W.N. Zagotta, and R.W. Aldrich. 1994. Shaker potassium channel gating I: transitions near the open state. J. Gen. Physiol. 103:249-278.
19. Hurst, R.S., M.P. Kavanaugh, J. Yakel, J.P. Adelman, and R.A. North. 1992. Cooperative interactions among subunits of a voltage-dependent potassium channel. Evidence from expression of concatenated cDNAs. J Biol. Chem. 267:23742-23745.
20. Hurst. R.S., M.J. Roux. L. Toro, and E. Stefani. 1997. External barium influences the gating charge movement of Shaker potassium channels. Biophys. J. 72:77-84.
21. Kamb, A., L.E. Iverson, and M.A. Tanouye. 1987. Molecular characterization of Shaker, a Drosophila gene that encodes a potassium channel. Cell. 50:405-413.
22. Kanevsky, M. 1998. Role of the S5 Segment in Voltage Gating and Open State Stability of the Shaker Potassium Channel. Ph.D. Dissertation. Stanford University, Stanford, CA.
23. Kavanaugh, M.P., R.S. Hurst, J. Yakel, M.D. Varnum, J.P. Adelman, and R.A. North. 1992. Multiple subunits of a voltage-dependent potassium channel contribute to the binding site for tetraethylammonium. Neuron. 8:493-497.
24. Keynes, R.D., and F. Elinder. 1999. The screw-helical voltage gating of ion channels. Proc. R. Soc. Lond. B Biol. Sci. 266:843-852.
25. Koren, G., E.R. Liman, D.E. Logothetis, G.B. Nadal, and P. Hess. 1990. Gating mechanism of a cloned potassium channel expressed in frog oocytes and mammalian cells. Neuron. 4:39-51.
26. + channel S4. Neuron. 16:387-397.
27. Ledwell, J.L., and R.W. Aldrich. 1999. Mutations in the S4 region isolate the final cooperative step in Shaker potassium channel activation. J. Gen. Physiol 113:389-414.
28. Lichtinghagen, R., M. Stocker, R. Wittka, G. Boheim, W. Stühmer, A. Ferrus, and O. Pongs. 1990. Molecular basis of altered excitability in Shaker mutants of Drosaphila melanogaster. EMBO (Eur. Mol. Biol. Organ.) J. 9:4399-4407.
29. + channel. Nature. 353:752-756.
30. + channel determined by construction of multimeric cDNAs. Neuron. 9:861-871.
31. + channels are due to the specific charge content of their respective S4 regions. Neuron. 10:1121-1129.
32. + channel result in corresponding decreases in gating charge. Neuron. 8:531-540.
33. + channels. Neuron. 7:327-336.
34. MacKinnon, R. 1991. Determination of the subunit stoichiometry of a voltage-activated potassium channel. Nature. 350:232-235.
35. Mannuzzu, L.M., M.M. Moronne, and E.Y. Isacoff. 1996. Direct physical measure of conformational rearrangement underlying potassium channel gating. Science. 271:213-216.
36. Marchais, D., and A. Marty. 1979. Interaction of permeant ions with channels activated by acetylcholine in Aplysia neurones. J. Physiol. 297:9-45.
37. Matteson, D.R., and R.P.J. Swenson. 1986. External monovalent cations that impede the closing of K channels. J. Gen. Physiol. 87: 795-816.
38. + channels. Neuron. 12:301-315.
39. + channels during gating and assembly. Biophys. J. 65:1740-1748.
40. + channels. Proc. Natl. Acad. Sci. USA. 88: 2931-2935.
41. + channel. J. Gen. Physiol. 90:427-449.
42. Moore, J.W., and S.H. Young. 1981. Dynamics of potassium ion currents in squid axon membrane. A re-examination. Biophys. J. 36: 715-722.
43. + channel. J. Gen. Physiol. 92:569-586.
44. + channels. J. Gen. Physiol. 97:641-665.
45. 2+ channels. J. Gen. Physiol. 108:143-155.
46. Papazian, D.M., T.L. Schwarz, B.L. Tempel, Y.N. Jan, and L.Y Jan. 1987. Cloning of genomic and complementary DNA from Shaker, a putative potassium channel gene from Drosophila. Science. 237: 749-753.
47. + channel. Neuron. 14:1293-1301.
48. Papazian, D.M., L.C. Timpe, Y.N. Jan, and L.Y. Jan. 1991. Alteration of voltage-dependence of Shaker potassium channel by mutations in the S4 sequence. Nature. 349:305-310.
49. + channels. Neuron. 11:353-358.
50. + channels. Implications for activation and inactivation models. Biophys. J. 62:160-168.
51. Perozo, E., T.L. Santacruz, E. Stefani, F. Bezanilla, and D.M. Papazian. 1994. S4 mutations alter gating currents of Shaker K channels. Biophys. J. 66:345-354.
52. Pongs, O., N. Kecskemethy, R. Muller, J.I. Krah, A. Baumann, H.H. Kiltz, I. Canal, S. Llamazares, and A. Ferrus. 1988. Shaker encodes a family of putative potassium channel proteins in the nervous system of Drosophila. EMBO (Eur. Mol. Biol. Organ.) J. 7:1087-1096.
53. Rayner, M.D., J.G. Starkus, P.C. Ruben, and D.A. Alicata. 1992. Voltage-sensitive and solvent-sensitive processes in ion channel gating. Kinetic effects of hyperosmolar media on activation and deactivation of sodium channels. Biophys. J. 61:96-108.
54. +. J. Gen. Physiol. 98:535-554.
55. Salkoff, L. 1983. Generic and voltage-clamp analysis of a Drosophila potassium channel. Cold Spring Harbor Symp. Quant. Biol. 1:221-231.
56. Sanger, F., S. Nicklen, and A.R. Coulson. 1977. DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA. 74: 5463-5467.
57. Schauf, C.L., and J.O. Bullock. 1979. Modifications of sodium channel gating in Myxicola giant axons by deuterium oxide, temperature, and internal cations. Biophys. J. 27:193-208.
58. 2O on some components of membrane conductance. Biophys. J. 30: 295-305.
59. Schoppa, N.E., K. McCormack, M.A. Tanouye, and F.J. Sigworth. 1992. The size of gating charge in wild-type and mutant Shaker potassium channels. Science. 255:1712-1715.
60. Schoppa, N.E., and F.J. Sigworth 1998a. Activation of Shaker potassium channels. I. Characterization of voltage-dependent transitions. J. Gen. PhysioL 111:271-294.
61. Schoppa, N.E., and F.J. Sigworth. 1998b. Activation of Shaker potassium channels. II. Kinetics of the V2 mutant channel. J. Gen. Physiol. 111:295-311.
62. Schoppa, N.E., and F.J. Sigworth 1998c. Activation of Shaker potassium channels. III. An activation gating model for wild-type and V2 mutant channels. J. Gen. Physiol. 111:313-342.
63. Schulz, G.E., and R.H. Schirmer. 1979. Principles of Protein Structure. Springer-Verlag, New York. 314 pp.
64. + channel. Neuron. 16:1159-1167.
65. + channels. Neuron. 11:343-352.
66. + channels. J. Gen. Physiol. 109:767-778.
67. Sigg, D., and F. Bezanilla. 1997. Total charge movement per channel. The relation between gating charge displacement and the voltage sensitivity of activation. J. Gen. Physiol. 109:27-39.
68. Sigg, D., E. Stefani, and F. Bezanilla. 1994. Gating current noise produced by elementary transitions in Shaker potassium channels. Science. 264:578-582.
69. Sigworth, F.J. 1994. Voltage gating of ion channels. Q. Rev. Biophys. 27:1-40.
70. Smith-Maxwell, C.J., J.L. Ledwell, and R.W. Aldrich. 1998a. Role of the S4 in cooperativity of voltage-dependent potassium channel activation. J. Gen. Physiol. 111:399-420.
71. Smith-Maxwell, C.J., J.L. Ledwell, and R.W. Aldrich. 1998b. Uncharged S4 residues and cooperativity in voltage-dependent potassium channel activation. J. Gen. Physiol. 111:421-439.
72. Spruce, A.E., N.B. Standen, and P.R. Stanfield. 1989. Rubidium ions and the gating of delayed rectifier potassium channels of frog skeletal muscle. J. Physiol. 411:597-610.
73. Starkus, J.G., T. Schlief, M.D. Rayner, and S.H. Heinemann. 1995. Unilateral exposure of Shaker B potassium channels to hyperosmolar solutions. Biophys. J. 69:860-872.
74. + channels: I. Ionic and gating currents. Biophys. J. 66:996-1010.
75. +. Nature. 291: 427-429.
76. Taglialatela, M., L. Toro, and E. Stefani. 1992. Novel voltage clamp to record small, fast currents from ion channels expressed in Xenopusoocytes. Biophys. J. 61:78-82.
77. Tanouye, M.A., and A. Ferrus. 1985. Action potentials in normal and Shaker mutant Drosophila. J. Neurogenet. 2:253-271.
78. Tanouye, M.A., A. Ferrus, and S.C. Fujita. 1981. Abnormal action potentials associated with the Shaker complex locus of Drosophila. Proc. Natl Acad. Sci. USA. 78:6548-6552.
79. Tempel, B.L., D.M. Papazian, T.L. Schwarz, Y.N. Jan, and L.Y. Jan. 1987. Sequence of a probable potassium channel component encoded at Shaker locus of Drosophila. Science. 237:770-775.
80. Tytgat, J., and P. Hess. 1992. Evidence for cooperative interactions in potassium channel gating. Nature. 359:420-423.
81. Wu, C.F., and F.N. Haugland. 1985. Voltage clamp analysis of membrane currents in larval muscle fibers of Drosophila: alteration of potassium currents in Shaker mutants. J. Neurosci. 5:2626-2640.
82. Xu, J., W. Yu, J.M. Wright, R.W. Raab, and M. Li. 1998. Distinct functional stoichiometry of potassium channel beta subunits. Proc. Natl. Acad. Sci. USA. 95:1846-1851.
83. Yang, N., A.J. George, and R. Horn. 1996. Molecular basis of charge movement in voltage-gated sodium channels. Neuron. 16:113-122.
84. Yang, N., and R. Horn. 1995. Evidence for voltage-dependent S4 movement in sodium channels. Neuron. 15:213-218.
85. Yang, Y., Y. Yan, and F.J. Sigworth. 1997. How does the W434F mutation block current in Shaker potassium channels? J. Gen. Physiol. 109:779-789.
86. Yusaf, S.P., D. Wray, and A. Sivaprasadarao. 1996. Measurement of the movement of the S4 segment during the activation of a voltage-gated potassium channel. Pflügers Arch. 433:91-97.
87. Zagotta, W.N., and R.W. Aldrich. 1990a. Voltage-dependent gating of Shaker A-type potassium channels in Drosophila muscle. J. Gen. Physiol. 95:29-60.
88. 5 mutation. J. Neurosci. 10:1799-1810.
89. Zagotta, W.N., T. Hoshi, and R.W. Aldrich. 1994b. Shaker potassium channel gating. III: Evaluation of kinetic models for activation. J. Gen. Physiol. 103:321-362.
90. Zagotta, W.N., T. Hoshi, J. Dittman, and R.W. Aldrich. 1994a. Shaker potassium channel gating. II: Transitions in the activation pathway. J. Gen. Physiol. 103:279-319.
91. Zimmerberg, J., F. Bezanilla, and V.A. Parsegian. 1990. Solute inaccessible aqueous volume changes during opening of the potassium channel of the squid giant axon. Biophys. J. 57:1049-1064.
92. Zimmerberg, J., and V.A. Parsegian. 1986. Polymer inaccessible volume changes during opening and closing of a voltage-dependent ionic channel. Nature. 323:36-39.
93. Zimmerberg, J., and V.A. Parsegian. 1987. Water movement during channel opening and closing. J. Bioenerg. Biomembr. 19:351-358.