Coupling and cooperativity in voltage activation of a limited-state BK channel gating in saturating Ca2+

Journal of General Physiology

Volumn 135, Issue 5, 2010, Pages 461-480

  Shelley, Christopher ^a,b   Niu, Xiaowei ^a,c   Geng, Yanyan ^a   Magleby, Karl L ^a  

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

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c Columbia University ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; LARGE CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL;

ANIMAL; ARTICLE; CELL CULTURE; CHANNEL GATING; CHEMICAL STRUCTURE; CHEMISTRY; CYTOLOGY; GENETIC TRANSFECTION; GENETICS; HUMAN; KIDNEY; MOUSE; PATCH CLAMP; PHYSIOLOGY;

ANIMALS; CALCIUM; CELLS, CULTURED; HUMANS; ION CHANNEL GATING; KIDNEY; LARGE-CONDUCTANCE CALCIUM-ACTIVATED POTASSIUM CHANNELS; MICE; MODELS, MOLECULAR; PATCH-CLAMP TECHNIQUES; TRANSFECTION;

EID: 77951758133     PISSN: 00221295     EISSN: 15407748     Source Type: Journal    
DOI: 10.1085/jgp.200910331     Document Type: Article

References (74)

1. Adelman, J.P., K.Z. Shen, M.P. Kavanaugh, R.A. Warren, Y.N. Wu, A. Lagrutta, C.T. Bond, and R.A. North. 1992. Calcium-activated potassium channels expressed from cloned complementary DNAs. Neuron. 9:209-216. doi: 10.1016/0896-6273(92)90160-F
2. 8+ sensitivity. J. Gen. Physiol, 120:173-189. doi:10.1085/jgp.20028627
3. 8+ sensing. J. Gen. Physiol. 123:475-489. doi:10.1085/jgp.200409052
4. BarrettJ.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.
5. + channels. J. Gen. Physiol. 111:343-362. doi:10.1085/jgp.111.2.343
6. 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. doi:10.1126/ science.7687074
7. Colquhoun, D., and A.G. Hawkes. 1995. The principles of the stochastic, interpretation of ion-channel mechanisms. In Single Channel Recording. B. Sakmann and E. Neher, editors. Plenum Press, New York. 397-482.
8. + channel. J. Gen. Physiol 110:257-281. cloi:10.1085/jgp.110.3.257
9. 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. doi:10.1016/S0006-3495(90)82416-4
10. + channels. Biochemistry. 39:15612-15619. doi:10.1021/bi001509+
11. + channels. J. Gen. Physiol. 109:647-673. doi:10.1085/jgp.109.5.647
12. Cui, J., H. Yang, and U.S. Lee. 2009. Molecular mechanisms of BK channel activation. Cell. Mol Life Sci 66:852-875. doi: 10.1007/s00018-008-8609-x
13. + (hslo) channel from smooth muscle. J. Gen. Physiol, 107:399-407. doi: 10.1085/jgp.107.3.399
14. 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. doi: 10.1074/jbc.273.49.32430 (Pubitemid 28557615)
15. 2+ on gating ring stability. J. Biol. Chem. 280:41716-41724. doi:10.1074/jbc.M508144200
16. Fersht, A. 1985. Enzyme Structure and Mechanism. Second edition. W.H. Freeman and Company, New York. 149 pp.
17. Fredkin, D.R., M. Montai, 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 Advanced Books &: Software, Monterey, CA. 269-289.
18. Gagnon, D.G., and F. Bezanilla. 2009. A single charged voltage sensor is capable of gating the Shaker K channel. J. Gen, Physiol 133:467-483. doi: 10.1085/jgp.200810082
19. Gil, Z., K.L. Magleby, and S.D. Silberberg. 2001. Two-dimensional kinetic, analysis suggests nonsequential gating of mechanosensitive channels in Xenopus oocytes. Biophys. J. 81:2082-2099. doi: 10.1016/S0006-3495 (01) 75857-75862
20. Horn, R. 2009. Uncooperative voltage sensors. J. Gen. Physiol 133:463-466. doi:10.1085/jgp.200910236
21. Horn, R., and K Lange. 1983. Estimating kinetic constants from single channel data. Biophys. J. 43:207-223. doi:10.1016/S00063495(83)84341-0
22. 2+. J. Gen. Physiol, 114:305-336. doi:10 .1085/jgp.114.2.305
23. 2+ binding and channel opening in large conductance (BK) potassium channels. J. Gen. Physiol. 120:267-305. doi:10.1085/jgp.20028605
24. 2+ enhances voltage sensor/ gate coupling in BK channels. J. Gen. Physiol 131:13-32. doi:10 .1085/jgp.200709877
25. 2+. J.Gen. Physiol, 114:277-304. doi:10.1085/jgp.114.2.277
26. + channel and demonstration of its presence in the human BK channel. Neuron. 29:593-601. doi: 10.1016/S0896-6273(01)00236-7
27. Jiang, Y., A. Lee, J. Chen, M. Cadene, B.T. Chait, and R. MacKinnon. 2002. Crystal structure and mechanism of a calcium-gated potassium channel. Nature. 417:515-522. doi:10.1038/417515a (Pubitemid 34595912)
28. Kahlig, K.M., S.N. Misra, and A.L. George Jr. 2006. Impaired inactivation gate stabilization predicts increased persistent current for an epilepsy-associated SCN1A mutation. J. Neurosd. 26:10958-10966. doi: 10.1523/JNEUROSCI.3378-06.2006
29. Koehler, A.B.,20and E.H. Murphree. 1988. A comparison of the Akaike and Schwarz Criteria for selecting model order. Appl Stat. 37:187-195. doi:10.2307/2347338
30. Lape, R., D. Colquhoun, and L.G. Sivilotti. 2008. On the nature of partial agonism in the nicotinic receptor superfamily. Nature. 454:722-727.
31. 2+ and voltage. Biol Res. 39:385-401.doi:10.4067/S0716- 97602006000300003
32. Lingle, C.J. 2007. Gating rings formed by RCK domains: keys to gate opening. J. Gen. Physiol. 129:101-107. doi:10.1085/jgp.200709739
33. + channel. Science. 309:897-903. doi: 10.1126/science.1116269
34. Long, S.B., E.B. Campbell, and R. Mackinnon. 2005b. Voltage sensor of Kv1.2: structural basis of electromechanical coupling. Science. 309:903-908. doi: 10.1126/science. 1116270
35. Lu, R., A. Alioua, Y. Kumar, M. Eghbali, E. Stefani, and L. Toro. 2006. MaxiK channel partners: physiological impact. J. Physiol, 570:65-72. doi:10.1113/jphysio1.2005.098913
36. Ma, Z., X.J. Lou, and F.T Horrigan. 2006. Role of charged residues in the S1-S4 voltage sensor of BK channels. J. Gen, Physiol 127:309-328. doi:10.1085/jgp.200509421 (Pubitemid 43312207)
37. Magleby, K.L. 2003. Gating mechanism of BK (Slol) channels: so near, yet so far. J. Gen. Physiol 121:81-96. doi:10.1085/jgp.20028721
38. Magleby, K.L., and L. Song. 1992. Dependency plots suggest the kinetic structure of ion channels. Proc. R. Soc. Land. B Biol. Sci. 249: 133-142. doi: 10.1098/rspb.1992.0095
39. Marks, T.N., and S.W. Jones. 1992. Calcium currents in the A7r5 smooth muscle-derived cell line. An allosteric model for calcium channel activation and dihydropyridine agonist action. J. Gen. Physiol. 99:367-390. doi:10.1085/jgp.99.3.367
40. + channels. Neuron. 12:301-315. doi:10.1016/ 0896-6273(94)90273-90279
41. 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.
42. 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. doi:10.1085/jgp.94.6.1037
43. + channels in rat skeletal muscle. J. Physiol. 443:739-777.
44. + channel, a distinct member of voltage-dependent ion channels with seven N-terminal transmembrane segments (S0-S6), an extracellular N terminus, and an intracellular (S9-S10) C terminus. Proc. Natl, Acad. Sci. USA. 94:14066-14071. doi:10.1073/pnas.94.25.14066
45. Monod, J., J. Wyman, and J.P. Changeux. 1965. On the nature of allosteric transitions: a plausible model. J. Mol, Biol 12:88-118. doi: 10.1016/S0022-2836 (65) 80285-80286
46. Mukhtasimova, N., WY Lee, H.L. Wang, and S.M. Sine. 2009. Detection and trapping of intermediate states priming nicotinic receptor channel opening. Nature. 459:451-454. doi:10.1038/nature07923
47. 2+-activated potassium channels by retaining the gating in the bursting states. J. Gen, Physiol, 113:425-440. doi:10.1085/jgp.113.3.425
48. Niu, X., and K.L. Magleby. 2002. Stepwise contribution of each subunit, to the cooperative activation of BKchannels lay Ca2+. Proc. Natl. Acad. Sci USA. 99:11441-11446. doi: 10.1073/pnas. 172254699 (Pubitemid 34920944)
49. 2+-activated potassium channel. Neuron. 42:745-756.
50. Piskorowski, R.A., and R.W. Aldrich. 2006. Relationship between pore occupancy and gating in BK potassium channels. J. Gen. Physiol. 127:557-576. doi:10.1085/jgp.200509482
51. Purohit, P., and A. Auerbach. 2007. Acetylcholine receptor gating at extracellular transmembrane domain interface: the "pre-M1" linker. J. Gen. Physiol 130:559-568. doi:10.1085/jgp.200709857
52. Qian, X., X. Niu, and K.L. Magleby. 2006. Intra- and intersubunit cooperativity in activation of BKchannels by Ca2+. J. Gen. Physiol. 128:389-404. doi:10.1085/jgp.200609486 (Pubitemid 44455098)
53. Ríos, E., M. Karhanek, J. Ma, and A. González. 1993. An allosteric model of the molecular interactions of excitation-contraction coupling in skeletal muscle. J. Gen. Physiol 102:449-481. doi:10 .1085/jgp.102.3.449
54. +channels suggests that the gating includes transitions through intermediate or secondary states. A mechanism for flickers. J. Gen. Physiol, 111:751-780. doi: 10 .1085/jgp.111.6.751
55. 2+ suggest a two-tiered allosteric, gating mechanism. J. Gen. Physiol. 114:93-124. doi:10.1085/jgp.114.1.93
56. + channels described by a two-tiered allosteric, gating mechanism. J. Gen. Physiol. 116:75-99. doi:10.1085/jgp.116.1.75
57. Rothberg, B.S., RA. Bello, and K.L. Magleby. 1997. Two-dimensional components and hidden dependencies provide insight into ion channel gating mechanisms. Biophys. J. 72:2524-2544. doi:10 .1016/S0006-3495(97)78897-0
58. Salkoff, L., A. Butler, G. Ferreira, C. Santi, and A. Wei. 2006. Highconductance potassium channels of the SLO family. Nat. Rev. Neurosd, 7:921-931. doi:10.1038/nm1992
59. +) channel, revealed by voltage-clamp fluorometry. Proc Natl, Acad Sci. USA. 103:12619-12624, doi:10.1073/pnas.0601176103
60. 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. doi:10.1085/jgp.111.2.313 (Pubitemid 28113080)
61. Schreiber, M., and L. Salkoff. 1997. A novel calcium-sensing domain in the BK channel Biophys. J. 73:1355-1363. doi: 10 .1016/S0006-3495(97)78168-2
62. Schroeder, I., and U.P. Hansen. 2007. Saturation and microsecond gating of current indicate depletion-induced instability of the MaxiK selectivity filter. J. Gen. Physiol. 130:83-97. doi:10.1085/ jgp.200709802 (Pubitemid 47007660)
63. +-induced micros gating of current indicates instability of the MaxiK selectivity filter as caused by ion/pore interaction. J. Gen, Physiol. 131:365-378. doi: 10.1085/jgp.200809956
64. Shi, J., G. Krishnamoorthy, Y. Yang, L. Hu, N. Chaturvedi, D. Harilal, J. Qin, and J. Cui. 2002. Mechanism of magnesium activation of calcium-activated potassium channels. Nature. 418:876-880. doi:10.1038/nature00941 (Pubitemid 34966306)
65. + channels using two-dimensional dwell-time distributions. Biophys. J. 67:91-104. doi:10.1016/ S0006-3495(94)80458-80468
66. + channel (hslo). Proc. Natl. Acad. Sci, USA, 94:5427-5431. doi:10.1073/pnas.94.10.5427
67. Tombola, E, M.M. Pathak, and E.Y Isacoff. 2006. How does voltage open an ion channel? Annu. Rev. Cell Dm Biol, 22:23-52. doi:10.1146/annurev.cellBio.21. 020404.145837
68. Wilkens, C.M., and R.W. Aldrich. 2006. State-independent block of BK channels by an intracellular quaternary ammonium. J. Gen. Physiol 128:347-364. doi:10.1085/jgp.20()609579
69. Wu, Y., Y. Xiong, S. Wang, H. Yi, H. Li, N. Pan, F.T. Horrigan, Y. Wu, and J. Ding. 2009. Intersubunit coupling in the pore of BK channels. J. Biol. Chem. 284:23353-23363.
70. Xia, X.M., X. Zeng, and C.J. Lingle. 2002. Multiple regulatory sites in large-conductance calcium-activated potassium channels. Nature. 418:880-884. doi:10.1038/nature00956
71. 2+ coordinated between the voltage sensor and RCK1 domains. Nat. Struct. Mol Biol 15:1152-1159. doi:10.1038/nsmb.1507
72. Ye, S., Y. Li, L. Chen, and Y.Jiang. 2006. Crystal structures of aligandfree MthKgating ring: insights into the ligand gating mechanism of K+channels. Cell 126:1161-1173. doi:10.1016/j.cell.2006.08.029 (Pubitemid 44380293)
73. 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. doi:10.1085/jgp.103.2.321 (Pubitemid 24068562)
74. Zeng, X.H., X.M. Xia, and C.J. Lingle. 2005. Divalent cation sensitivity of BK channel activation supports the existence of three distinct binding sites.J. Gen. Physiol. 125:273-286. doi:10.1085/ jgp.200409239