Gating kinetics of single large-conductance Ca2+-activated K+ channels in high Ca2+ suggest a two-tiered allosteric gating mechanism

Journal of General Physiology

Volumn 114, Issue 1, 1999, Pages 93-124

  Rothberg, Brad S ^a   Magleby, Karl L ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

BK channel; Eigen; K(ca) channel; Markov; Monod Wyman Changeux

Indexed keywords

ANIMAL CELL; ARTICLE; BINDING SITE; CALCIUM CELL LEVEL; CALCIUM CONDUCTANCE; CHANNEL GATING; LIGAND BINDING; MEMBRANE DEPOLARIZATION; NEGATIVE FEEDBACK; NERVE EXCITABILITY; NONHUMAN; POTASSIUM TRANSPORT; PROTEIN EXPRESSION; RAT;

ANIMALS; CALCIUM; ELECTRIC CONDUCTIVITY; ION CHANNEL GATING; KINETICS; LARGE-CONDUCTANCE CALCIUM-ACTIVATED POTASSIUM CHANNELS; LIGANDS; MODELS, BIOLOGICAL; OSMOLAR CONCENTRATION; POTASSIUM CHANNELS; POTASSIUM CHANNELS, CALCIUM-ACTIVATED; RATS;

EID: 0033067095     PISSN: 00221295     EISSN: None     Source Type: Journal    
DOI: 10.1085/jgp.114.1.93     Document Type: Article

References (100)

1. Adelman, J.P., E. Shen, M.P. Kavanaugh, R.A. Warren, Y. Wu, A. Lagrutta, C. Bond, and R.A. North. 1992. Calcium-activated potassium channels expressed from cloned complementary DNAs. Neuron. 9:209-216.
2. Akaike, H. 1974. A new look at the statistical model identification. IEEE (Inst. Electr. Electron. Eng.) Trans. Auto. Control 19:716-723.
3. Art, J.J., Y.-C. Wu, and R. Fettiplace. 1995. The calcium-activated potassium channels of turtle hair cells. J. Gen. Physiol. 105:49-72.
4. Atkinson, N.S., G.A. Robertson, and B. Ganetzky. 1991. A component of calcium-activated potassium channels encoded by the Drosophila slo locus. Science. 253:551-555.
5. Barrett, J.N., K.L. Magleby, and B.S. Pallotta. 1982. Properties of single calcium-activated potassium channels in cultured rat muscle. J. Physiol. 331:211-230.
6. Bauer, R.J., B.F. Bowman, and J.L. Kenyon. 1987. Theory of the kinetic analysis of patch clamp data. Biophys. J. 52: 961-978.
7. + channels. J. Gen. Physiol. 111: 343-362.
8. + channels: II. The components of gating currents and a model of channel activation. Biophys. J. 66:1011-1021.
9. Blatz, A.L., and K.L. Magleby. 1986. Correcting single channel data for missed events. Biophys. J. 49:967-980.
10. Butler, A., S. Tsunoda, D.P. McCobb, A. Wei, and L. Salkoff. 1993. mSlo, a complex mouse gene encoding "maxi" calcium-activated potassium channels. Science. 261:221-224.
11. + channel with fluorescence. Neuron. 19:1127-1140.
12. Chang, C.-P., S.I. Dworetzky, J. Wang, and M.E. Goldstein. 1997. Differential expression of the α and β subunits of the large-conductance calcium-activated potassium channel: implication for channel diversity. Mol. Brain Res. 45:33-40.
13. Colquhoun, D. 1973. The relation between classical and cooperative models for drug action. In Drug Receptors. H.P. Rang, editor. University Park Press, London. 149-182.
14. Colquhoun, D., and A.G. Hawkes. 1981. On the stochastic properties of single ion channels. Proc. R. Soc. Lond. B Biol. Sci. 211:205-235.
15. Colquhoun, D., and A.G. Hawkes. 1987. A note on correlations in single ion channel records. Proc. R. Soc. Lond. B Biol. Sci. 230: 1-52.
16. Colquhoun, D., and A.G. Hawkes. 1995a. The principles of the stochastic interpretation of ion-channel mechanisms. In Single-Channel Recording. B. Sakmann and E. Neher, editors. Plenum Publishing Corp., New York. 397-482.
17. Colquhoun, D., and A.G. Hawkes. 1995b. A Q-matrix cookbook. In Single-Channel Recording. B. Sakmann and E. Neher, editors. Plenum Publishing Corp., New York, 589-633.
18. Colquhoun, D., and F.J. Sigworth. 1995. Fitting and statistical analysis of single-channel records. In Single-Channel Recording. B. Sakmann and E. Neher, editors. Plenum Publishing Corp., New York. 483-587.
19. Conley, E.C. 1996. The ion channel facts book. II. Intracellular ligand-gated channels. Academic Press, New York. 607-720.
20. Crouzy, S.C., and F.J. Sigworth. 1990. Yet another approach to the dwell-time omission problem of single-channel analysis. Biophys. J. 58:731-743.
21. + channels. J. Gen. Physiol. 109:633-646.
22. + channel. J. Gen. Physiol. 110: 257-281.
23. + channels. J. Gen. Physiol. 109:647-673.
24. + channel correlates with occupancy of the pore. Biophys. J. 61:639-648.
25. Diaz, L., P. Meera, J. Amigo, E. Stefani, O. Alvarez, L. Toro, and R. Latorre. 1998. Role of the S4 segment in a voltage-dependent calcium-sensitive potassium (hSlo) channel. J. Biol. Chem. 273: 32430-32436.
26. + channels. J. Physiol. 489:403-418.
27. Dworetzky, S.I., C.G. Boissard, J.T. Lum-Ragan, M.C. McKay, D.J. Post-Munson, J.T. Trojnacki, C.-P. Chang, and V.K. Gribkoff, 1996. Phenotypic alteration of a human BK (hSlo) channel by hSloβ subunit coexpression: changes in blocker sensitivity, activation/relaxation and inactivation kinetics, and protein kinase A modulation. J. Neurosci. 16:4543-4550.
28. Eigen, M. 1968. New looks and outlooks on physical enzymology. Q. Rev. Biophys. 1:3-33.
29. + channel in rat skeletal muscle. J. Gen. Physiol. 98:163-181.
30. Ferguson, W.B., O.B. McManus, and K.L. Magleby. 1993. Opening and closing transitions for BK channels often occur in two steps via sojourns through a brief lifetime subconductance state, Biophys. J. 65:702-714.
31. Fersht, A. 1985. Enzyme Structure and Mechanism. W.H. Freeman Co., San Francisco, CA. 263-278.
32. Fredkin, D.R., M. Montal, and J.A. Rice. 1985. Identification of aggregated Markovian models: application to the nicotinic acetylcholine receptor. In Proceedings of the Berkeley Conference in Honor of Jerzy Neyman and Jack Kiefer. L.M. LeCam, and R.A. Olshen, editors. Wadsworth Publishing Co., Belmont, CA. 269-289.
33. + channels from mammalian skeletal muscle. J. Exp. Biol. 124:5-13.
34. Green, W.N., and O.S. Andersen. 1991. Surface charges and ion channel function. Annu. Rev. Physiol. 53:341-359.
35. 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.
36. Hawkes, A.G., A. Jalali, and D. Colquhoun. 1992. Asymptotic distributions of apparent open times and shut times in a single channel record allowing for the omission of brief events. Philos. Trans. R. Soc. Lond. B Biol. Sci. 337:383-404.
37. Hille, B., A.M. Woodhull, and B.I. Shapiro. 1975. Negative surface charge near sodium channels of nerve: divalent ions, monovalent ions, and pH. Phil. Trans. R. Soc. Lond. B Biol. Sci. 170: 301-318.
38. Horn, R. 1987. Statistical methods for model discrimination: application to gating kinetics and permeation of the acetylcholine receptor channel. Biophys. J. 51:255-263.
39. Horn, R., and K. Lange. 1983. Estimating kinetic constants from single channel data. Biophys. J. 43:207-223.
40. + channels. Biophys. J. 74:A218.
41. 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.
42. Kienker, P. 1989. Equivalence of aggregated Markov models of ion-channel gating. Proc. R. Soc. Lond. B Biol. Sci. 236:269-309.
43. Lagrutta, A., K.R.A. Shen, R.A. North, and J.P. Adelman. 1994. Functional differences among alternatively spliced variants of slowpoke, a Drosophila calcium-activated potassium channel. J. Biol. Chem. 269:20347-203511.
44. + channels. In Handbook of Membrane Channels: Molecular and Cellular Physiology. C. Peracchia, editor. Academic Press, Inc., New York. 79-102.
45. Magleby, K.L. 1992. Preventing artifacts and reducing errors in single-channel analysis. Methods Enzymol. 207:763-791.
46. Magleby, K.L., and B.S. Pallotta. 1983. Burst kinetics of single calcium-activated potassium channels in cultured rat skeletal muscle. J. Physiol. 344:605-623.
47. Magleby, K.L., and L. Song. 1992. Dependency plots suggest the kinetic structure of ion channels. Proc. R. Soc. Lond. B Biol Sci. 249: 133-142.
48. Magleby, K.L., and D.S. Weiss. 1990a. Estimating kinetic parameters for single channels with simulation. A general method that resolves the missed event problem and accounts for noise. Biophys. J. 58:1411-1426.
49. Magleby, K.L., and D.S. Weiss. 1990b. Identifying kinetic gating mechanisms for ion channels by using two-dimensional distributions of simulated dwell times. Proc. R. Soc. Lond. B Biol. Sci. 241: 220-228.
50. Marty, A. 1989. The physiological role of calcium-dependent channels. Trends Neurosci. 12:420-424.
51. McManus, O.B. 1991. Calcium-activated potassium channels: regulation by calcium. J. Bioenerg. Biomembr. 23:537-560.
52. McManus, O.B., A.L. Blatz, and K.L. Magleby. 1985. Inverse relationship of the durations of adjacent open and shut intervals for Cl and K channels. Nature. 317:625-628.
53. McManus, O.B., A.L. Blatz, and K.L. Magleby. 1987. Sampling, log binning, fitting, and plotting durations of open and shut intervals from single channels and the effects of noise. Pflügers Arch. 410:530-553.
54. McManus, O.B., L.M.H. Helms, L. Pallanck, B. Ganetzky, R. Swanson, and R.J. Leonard. 1995. Functional role of the beta subunit of high-conductance calcium-activated potassium channels. Natron. 14:645-650.
55. McManus, O.B., and K.L. Magleby. 1988. Kinetic states and modes of single large-conductance calcium-activated potassium channels in cultured rat skeletal muscle. J. Physiol. 402:79-120.
56. McManus, O.B., and K.L. Magleby. 1989. Kinetic time constants independent of previous single-channel activity suggest Markov gating for a large-conductance Ca-activated K channel. J. Gen. Physiol. 94:1037-1070.
57. + channels in rat skeletal muscle. J. Physiol. 443:739-777.
58. Meera, P., M. Wallner, Z. Jiang, and L. Toro. 1996. A calcium switch for the functional coupling between α (hslo) and β subunits (K, Caβ) of maxi K channels. FEBS Lett. 382:84-88.
59. Mendenhall, W., R.L. Scheaffer, and D.D. Wackerly. 1990. Mathematical statistics with applications. PWS-Kent Publishing Co., Boston. 650-655.
60. + channels. Biophys. J. 70:778-785.
61. Miller, C. 1987. Trapping single ions inside single ion channels. Biophys. J. 52:123-126.
62. + channel in planar lipid bilayers. J. Membr. Biol. 83:273-282.
63. 2+ binding reactions. J. Gen. Physiol. 82:511-542.
64. Monod, J., J. Wyman, andJ.-P. Changeux. 1965. On the nature of allosteric transitions: a plausible model. J. Mol. Biol. 12:88-118.
65. + (BK) channel. Biophys. J. 76:3099-3117.
66. 2+ indicators in smooth muscle cells. Biophys. J. 75: 1774-1782.
67. 2+-activated potassium channels by retaining the gating in the bursting states. J. Gen. Physiol. 113:425-439.
68. Nonner, W., and B. Eisenberg. 1998. Ion permeation and glutamate residues linked by Poisson-Nernst-Plank theory in L-type calcium channels. Biophys. J. 75:1287-1305.
69. + channel from skeletal muscle membrane. J. Gen. Physiol. 92:67-86.
70. Pallanck, L., and B. Ganetzky. 1994. Cloning and characterization of human and mouse homologs of the Drosophila calcium-activated potassium channel gene, slowpoke. Hum. Mol. Genet. 3:1239-1243.
71. Pallotta, B.S. 1985. N-Bromoacetamide removes a calcium-dependent component of channel opening from calcium-activated potassium channels in rat skeletal muscle. J. Gen. Physiol. 86:601-611.
72. Petracchi, D., M. Barbi, M. Pellegrini, M. Pellegrino, and A. Simoni. 1991. Use of conditioned distributions in the analysis of ion channel recordings. Eur. Biophys. J. 20:31-39.
73. Reinhart, PH., S. Chung, and I.B. Levitan. 1989. A family of calcium-dependent potassium channels from rat brain. Neuron. 2:1031-1041.
74. Rothberg, B.S., R.A. Bell, and K.L. Magleby. 1997. Two-dimensional components and hidden dependencies provide insight into ion channel gating mechanisms. Biophys. J. 72:2524-2544.
75. 2+-independent long shut intervals in BK channels from rat muscle. J. Physiol. 493:673-689.
76. Rothberg, B.S., and K.L. Magleby. 1996. Gating of BK channels can be independent of calcium or voltage. Soc. Neurosci. Abstr. 22: 1443.
77. + channels suggests that the gating includes transitions through intermediate or secondary states. A mechanism for flickers. J. Gen. Physiol 111:751-780.
78. Rothberg, B.S., and K.L. Magleby. 1999. Voltage-dependent steps in the gating of single BK channels. Biophys. J. 76:A333.
79. Roux, B., and R. Sauve. 1985. A general solution for the time interval omission problem applied to single channel analysis. Biophys. J. 48:149-158.
80. Rudy, B. 1988. Diversity and ubiquity of K channels. Neuroscience. 25:729-749.
81. Schoppa, N.E., and F.J. Sigworth. 1998. Activation of Shaker potassium channels. III. An activation gating model for wild-type and V2 mutant channels. J. Gen. Physiol. 111:313-342.
82. Schreiber, M., and L. Salkoff. 1997. A novel calcium-sensing domain in the BK channel. Biophys. J. 73:1355-1363.
83. Schwarz, G. 1978. Estimating the dimension of a model. Annals of Statistics. 6:461-464.
84. Shen, K.-Z., A. Lagrutta, N.W. Davies, N.B. Standen, J.P. Adelman, and R.A. North. 1994. Tetraethylammonium block of slowpoke calcium-activated potassium channels expressed in Xenopus oocytes: evidence for tetrameric channel formation. Pflügers Arch. 426: 440-445.
85. Sigworth, F.J., and S.M. Sine. 1987. Data transformations for improved display and fitting of single-channel dwell time histograms. Biophys. J. 52:1047-1054.
86. Solaro, C.R., J.P. Ding, Z.W. Li, and C.J. Lingle. 1997. The cytosolic inactivation domains of BK channels in rat chromaffin cells do not behave like simple, open-channel blockers. Biophys. J. 73: 819-830.
87. + channels using two-dimensional dwell-time distributions. Biophys. J. 67:91-104.
88. + channel (hslo). Proc. Natl. Acad. Sci. USA. 94:5427-5431.
89. Talukder, G., and R.W. Aldrich. 1998. Intermediate states in the gating of single mSLO calcium activated potassium channels in the absence of calcium. Biophys. J. 74:A217. (Abstr.)
90. Ca channels in human coronary smooth muscle: predominant alpha + beta subunit complexes. J. Physiol. 502:545-557.
91. Ca, a unique member of the voltage-gated K channel superfamily. News Physiol. Sci. 13:112-117.
92. + channel β-subunit from human brain. Proc. Natl. Acad. Sci. USA. 93:9200-9205.
93. Van der Kloot, W.G., and I. Cohen. 1979. Membrane surface potendal changes may alter drug interactions: an example, acetylcholine and curare. Science. 203:1351-1353.
94. 2+ blockade. J. Gen. Physiol. 82: 543-568.
95. Waller, M., P. Meera, and L. Toro. 1999. A novel beta subunit leads to inactivating maxi K currents. Biophys. J. 76:A267. (Abstr.)
96. Weiss, D.S., and K.L. Magleby. 1992. Voltage-dependent gating mechanism for single fast chloride channels from rat skeletal muscle. J. Physiol. 453:279-306.
97. Wong, B.S., H. Lecar, and M. Adler. 1982. Single calcium-dependent potassium channels in clonal anterior pituitary cells. Biophys. J. 39:313-317.
98. Wu, Y.-C., J.J. Art, M.B. Goodman, and R. Fettiplace. 1995. A kinetic description of the calcium-activated potassium channel and its application to electrical tuning of hair cells. Prog. Biophys. Mol. Biol. 63:131-158.
99. Zagotta, W.N., T. Hoshi, and R.W. Aldrich. 1994. Shaker potassium channel gating. III: Evaluation of kinetic models for activation. J. Gen. Physiol. 103:321-362.
100. Zheng, J., and F.J. Sigworth. 1998. Intermediate conductances during deactivation of heteromultimeric Shaker potassium channels. J. Gen. Physiol. 112:457-474.