Structural basis for calcium and magnesium regulation of a large conductance calcium-activated potassium channel with β1 subunits

Journal of Biological Chemistry

Volumn 289, Issue 24, 2014, Pages 16914-16923

  Liu, Hao Wen ^a   Hou, Pan Pan ^a   Guo, Xi Ying ^a   Zhao, Zhi Wen ^a   Hu, Bin ^a   Li, Xia ^a   Wang, Lu Yang ^b   Ding, Jiu Ping ^a   Wang, Sheng ^a  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; BIOLOGY;

CALCIUM AND MAGNESIUMS; CALCIUM-ACTIVATED POTASSIUM; HYDROPHOBIC SITES; PHYSIOLOGICAL ACTIVITY; SMOOTH MUSCLE CELLS; STRUCTURAL MODELING; UNDERLYING DYNAMICS; VOLTAGE-ACTIVATED POTASSIUM;

CALCIUM;

CALCIUM; LARGE CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL BETA 1 SUBUNIT; LARGE CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL BETA SUBUNIT; MAGNESIUM; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CONTROLLED STUDY; CRYSTAL STRUCTURE; HYDROPHOBICITY; MOLECULAR INTERACTION; PRIORITY JOURNAL; PROTEIN DOMAIN; REGULATORY MECHANISM; SENSITIVITY ANALYSIS; STATIC ELECTRICITY; STRUCTURAL HOMOLOGY; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS;

BK CHANNELS; ELECTROPHYSIOLOGY; MEMBRANE BIOPHYSICS; MOLECULAR BIOLOGY; POTASSIUM CHANNEL; PROTEIN STRUCTURE; Β1; Β2;

ACTION POTENTIALS; AMINO ACID SEQUENCE; BINDING SITES; CALCIUM; HEK293 CELLS; HUMANS; ICE; ION CHANNEL GATING; LARGE-CONDUCTANCE CALCIUM-ACTIVATED POTASSIUM CHANNEL ALPHA SUBUNITS; MAGNESIUM; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN SUBUNITS;

EID: 84902440204     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.557991     Document Type: Article

References (41)

1. Petersen, O. H., and Maruyama, Y. (1984) Calcium-activated potassium channels and their role in secretion. Nature 307, 693-696 (Pubitemid 14133937)
2. Brayden, J. E., and Nelson, M. T. (1992) Regulation of arterial tone by activation of calcium-dependent potassium channels. Science 256, 532-535
3. Fuchs, P. A., and Murrow, B. W. (1992) Cholinergic inhibition of short (outer) hair cells of the chick's cochlea. J. Neurosci. 12, 800-809
4. Robitaille, R., and Charlton, M. P. (1992) Presynaptic calcium signals and transmitter release are modulated by calcium-activated potassium channels. J. Neurosci. 12, 297-305
5. Wu, Y. C., Ricci, A. J., and Fettiplace, R. (1999) Two components of transducer adaptation in auditory hair cells. J. Neurophysiol. 82, 2171-2181
6. + channels in rat skeletal muscle. J. Physiol. 443, 739-777
7. 2+ coordinated between the voltage sensor and RCK1 domains. Nat. Struct. Mol. Biol. 15, 1152-1159
8. Schreiber, M., and Salkoff, L. (1997) A novel calcium-sensing domain in the BK channel. Biophys. J. 73, 1355-1363 (Pubitemid 27360725)
9. Xia, X. M., Zeng, X., and Lingle, C. J. (2002) Multiple regulatory sites in large-conductance calcium-activated potassium channels. Nature 418, 880-884 (Pubitemid 34966307)
10. Shi, J., Krishnamoorthy, G., Yang, Y., Hu, L., Chaturvedi, N., Harilal, D., Qin, J., and Cui, J. (2002) Mechanism of magnesium activation of calcium-activated potassium channels. Nature 418, 876-880 (Pubitemid 34966306)
11. Tanaka, Y., Meera, P., Song, M., Knaus, H. G., and Toro, L. (1997) Molecular constituents of maxi KCa channels in human coronary smooth muscle: predominant α + β subunit complexes. J. Physiol. 502, 545-557 (Pubitemid 27365820)
12. Brenner, R., Peréz, G. J., Bonev, A. D., Eckman, D. M., Kosek, J. C., Wiler, S. W., Patterson, A. J., Nelson, M. T., and Aldrich, R. W. (2000) Vasoregulation by the beta1 subunit of the calcium-activated potassium channel. Nature 407, 870-876
13. 2+ spark/STOC coupling and elevated blood pressure. Circ. Res. 87, E53-E60
14. Behrens, R., Nolting, A., Reimann, F., Schwarz, M., Waldschütz, R., and Pongs, O. (2000) hKCNMB3 and hKCNMB4, cloning and characterization of two members of the large-conductance calcium-activated potassium channel beta subunit family. FEBS Lett. 474, 99-106 (Pubitemid 30320840)
15. Brenner, R., Jegla, T. J., Wickenden, A., Liu, Y., and Aldrich, R. W. (2000) Cloning and functional characterization of novel large conductance calcium-activated potassium channel β subunits, hKCNMB3 and hKCNMB4. J. Biol. Chem. 275, 6453-6461 (Pubitemid 30129943)
16. + channel resistant to charybdotoxin and iberiotoxin. Proc. Natl. Acad. Sci. U.S.A. 97, 5562-5567
17. Uebele, V. N., Lagrutta, A., Wade, T., Figueroa, D. J., Liu, Y., McKenna, E., Austin, C. P., Bennett, P. B., and Swanson, R. (2000) Cloning and functional expression of two families of β-subunits of the large conductance calcium-activated K+ channel. J. Biol. Chem. 275, 23211-23218 (Pubitemid 30646218)
18. + channels. Proc. Natl. Acad. Sci. U.S.A. 100, 10488-10493
19. Ding, J. P., Li, Z. W., and Lingle, C. J. (1998) Inactivating BK channels in rat chromaffin cells may arise from heteromultimeric assembly of distinct inactivation-competent and noninactivating subunits. Biophys. J. 74, 268-289
20. Wang, Y. W., Ding, J. P., Xia, X. M., and Lingle, C. J. (2002) Consequences of the stoichiometry of Slo1 α and auxiliary beta subunits on functional properties of large-conductance Ca2+-activated K+ channels. J. Neurosci. 22, 1550-1561 (Pubitemid 35386274)
21. Lee, U. S., and Cui, J. (2010) BK channel activation: structural and functional insights. Trends Neurosci. 33, 415-423
22. 2+, activating mechanisms. Proc. Natl. Acad. Sci. U.S.A. 100, 10061-10066
23. + channels is involved in β subunit modulation of gating. J. Neurosci. 33, 11253-11261
24. Zeng, X. H., Xia, X. M., and Lingle, C. J. (2003) Redox-sensitive extracellular gates formed by auxiliary β subunits of calcium-activated potassium channels. Nat. Struct. Biol. 10, 448-454
25. Chen, M., Gan, G., Wu, Y., Wang, L., Wu, Y., and Ding, J. (2008) Lysinerich extracellular rings formed by hβ2 subunits confer the outward rectification of BK channels. PLoS One 3, e2114
26. Hou, P., Zeng, W., Gan, G., Lv, C., Guo, X., Zhang, Z., Liu, H., Wu, Y., Yao, J., Wei, A. D., Wang, S., and Ding, J. (2013) Inter-α/β subunits coupling mediating pre-inactivation and augmented activation of BKCa(β2). Sci. Rep. 3, 1666
27. + channels: an additional transmembrane region at the N terminus. Proc. Natl. Acad. Sci. U.S.A. 93, 14922-14927
28. Morrow, J. P., Zakharov, S. I., Liu, G., Yang, L., Sok, A. J., and Marx, S. O. (2006) Defining the BK channel domains required for β1-subunit modulation. Proc. Natl. Acad. Sci. U.S.A. 103, 5096-5101
29. Liu, G., Zakharov, S. I., Yang, L., Wu, R. S., Deng, S. X., Landry, D. W., Karlin, A., and Marx, S. O. (2008) Locations of the β1 transmembrane helices in the BK potassium channel. Proc. Natl. Acad. Sci. U.S.A. 105, 10727-10732
30. + (BK) channel. J. Gen. Physiol. 127, 191-204
31. + channel. Nature 466, 393-397
32. 2+-activation apparatus at 3.0 Å resolution. Science 329, 182-186
33. Case, D. A., Darden, T. A., Cheatham, T. E., 3rd, Simmerling, C. L., Wang, J., Duke, R. E., Luo, R., Walker, R. C., Zhang, W., Merz, K. M., Roberts, B., Hayik, S., Roitberg, A., Seabra, G., Swails, J., Goetz, A. W., Kolossváry, I., Wong, K. F., Paesani, F., Vanicek, J., Wolf, R. M., Liu, J., Wu, X., Brozell, S. R., Steinbrecher, T., Gohlke, H., Cai, Q., Ye, X., Wang, J., Hsieh, M. J., Cui, G., Roe, D. R., Mathews, D. H., Seetin, M. G., Salomon-Ferrer, R., Sagui, C., Babin, V., Luchko, T., Gusarov, S., Kovalenko, A., and Kollman, P. A. (2012) AMBER, University of California, San Francisco
34. McManus, O. B., Helms, L. M., Pallanck, L., Ganetzky, B., Swanson, R., and Leonard, R. J. (1995) Functional role of the β subunit of high conductance calcium-activated potassium channels. Neuron 14, 645-650
35. 2+-activated potassium channels by retaining the gating in the bursting states. J. Gen. Physiol. 113, 425-440
36. 2+- and voltage-dependent BK channels in adrenal chromaffin cells and rat insulinoma tumor cells. J. Neurosci. 19, 5255-5264
37. 2+-activated K+ channels: a transmembrane β-subunit homolog. Proc. Natl. Acad. Sci. U.S.A. 96, 4137-4142
38. Carter, P. J., Winter, G., Wilkinson, A. J., and Fersht, A. R. (1984) The use of double mutants to detect structural changes in the active site of the tyrosyl-tRNA synthetase (Bacillus stearothermophilus). Cell 38, 835-840
39. Serrano, L., Horovitz, A., Avron, B., Bycroft, M., and Fersht, A. R. (1990) Estimating the contribution of engineered surface electrostatic interactions to protein stability by using double-mutant cycles. Biochemistry 29, 9343-9352 (Pubitemid 20329069)
40. + channel. Cell 111, 231-239
41. + channel. Proc. Natl. Acad. Sci. U.S.A. 104, 19813-19818