Relative transmembrane segment rearrangements during BK channel activation resolved by structurally assigned fluorophore-quencher pairing

Journal of General Physiology

Volumn 140, Issue 2, 2012, Pages 207-218

  Pantazis, Antonios ^a   Olcese, Riccardo ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FLUORESCENT DYE; KCNMA1 PROTEIN, HUMAN; LARGE CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL ALPHA SUBUNIT; POTASSIUM;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMAL; ARTICLE; CHANNEL GATING; CHEMICAL MODEL; CHEMISTRY; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; OOCYTE; PATCH CLAMP; PHOTOCHEMISTRY; PROTEIN CONFORMATION; SPECTROFLUOROMETRY; XENOPUS;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; FLUORESCENT DYES; HUMANS; ION CHANNEL GATING; LARGE-CONDUCTANCE CALCIUM-ACTIVATED POTASSIUM CHANNEL ALPHA SUBUNITS; MODELS, CHEMICAL; MOLECULAR SEQUENCE DATA; OOCYTES; PATCH-CLAMP TECHNIQUES; PHOTOCHEMICAL PROCESSES; POTASSIUM; PROTEIN CONFORMATION; SPECTROMETRY, FLUORESCENCE; XENOPUS;

EID: 84866161825     PISSN: 00221295     EISSN: 15407748     Source Type: Journal    
DOI: 10.1085/jgp.201210807     Document Type: Article

References (77)

1. Armstrong, C.M. 2003. Voltage-gated K channels. Sci. STKE. 2003: re10. http://dx.doi.org/10.1126/stke.2003.188.re10
2. 2+ sensitivity is enhanced by its β1 subunit. J. Gen. Physiol. 126:393-412. http://dx.doi.org/10.1085/jgp.200509346
3. 2+ sensing. J. Gen. Physiol. 123:475-489. http://dx.doi.org/10.1085/jgp.200409052
4. Bezanilla, F. 2008. How membrane proteins sense voltage. Nat. Rev. Mol. Cell Biol. 9:323-332. http://dx.doi.org/10.1038/nrm2376
5. 2+-dependent activation. Proc. Natl. Acad. Sci. USA. 98:4776-4781. http://dx.doi.org/10.1073/pnas.081072398
6. + channel with fluorescence. Neuron. 19:1127-1140. http://dx.doi.org/10.1016/S0896-6273(00)80403-1
7. Chanda, B., and F. Bezanilla. 2008. A common pathway for charge transport through voltage-sensing domains. Neuron. 57:345-351. http://dx.doi.org/10.1016/j.neuron.2008.01.015
8. Claydon, T.W., and D. Fedida. 2007. Voltage clamp fluorimetry studies of mammalian voltage-gated K(+) channel gating. Biochem. Soc. Trans. 35:1080-1082. http://dx.doi.org/10.1042/BST0351080
9. +
10. Cui, J., H. Yang, and U.S. Lee. 2009. Molecular mechanisms of BK channel activation. Cell. Mol. Life Sci. 66:852-875. http://dx.doi.org/10.1007/s00018-008-8609-x
11. Díaz, 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. http://dx.doi.org/10.1074/jbc.273.49.32430
12. Doose, S., H. Neuweiler, and M. Sauer. 2005. A close look at fluorescence quenching of organic dyes by tryptophan. ChemPhysChem. 6:2277-2285. http://dx.doi.org/10.1002/cphc.200500191
13. Doose, S., H. Neuweiler, and M. Sauer. 2009. Fluorescence quenching by photoinduced electron transfer: a reporter for conformational dynamics of macromolecules. ChemPhysChem. 10:1389-1398. http://dx.doi.org/10.1002/cphc.200900238
14. Gandhi, C.S., and R. Olcese. 2008. The voltage-clamp fluorometry technique. Methods Mol. Biol. 491:213-231. http://dx.doi.org/10.1007/978-1-59745-526-8_17
15. + conduction by external surface charge effect. J. Gen. Physiol. 124:173-184. http://dx.doi.org/10.1085/jgp.200308949
16. 2+ binding and channel opening in large conductance (BK) potassium channels. J. Gen. Physiol. 120:267-305. http://dx.doi.org/10.1085/jgp.20028605
17. 2+ enhances voltage sensor/gate coupling in BK channels. J. Gen. Physiol. 131:13-32. http://dx.doi.org/10.1085/jgp.200709877
18. Hou, S., S.H. Heinemann, and T. Hoshi. 2009. Modulation of BKCa channel gating by endogenous signaling molecules. Physiology (Bethesda). 24:26-35. http://dx.doi.org/10.1152/physiol.00032.2008
19. Islas, L.D., and W.N. Zagotta. 2006. Short-range molecular rearrangements in ion channels detected by tryptophan quenching of bimane fluorescence. J. Gen. Physiol. 128:337-346. http://dx.doi.org/10.1085/jgp.200609556
20. 2+-dependent potassium channel (BK) gating ring apparatus. J. Biol. Chem. 286:20701-20709. http://dx.doi.org/10.1074/jbc.M111.235234
21. Jeffries, O., N. Geiger, I.C. Rowe, L. Tian, H. McClafferty, L. Chen, D. Bi, H.G. Knaus, P. Ruth, and M.J. Shipston. 2010. Palmitoylation of the S0-S1 linker regulates cell surface expression of voltage- and calcium-activated potassium (BK) channels. J. Biol. Chem. 285:33307-33314. http://dx.doi.org/10.1074/jbc.M110.153940
22. Koval, O.M., Y. Fan, and B.S. Rothberg. 2007. A role for the S0 transmembrane segment in voltage-dependent gating of BK channels. J. Gen. Physiol. 129:209-220. http://dx.doi.org/10.1085/jgp.200609662
23. 2+ and voltage. Biol. Res. 39:385-401. http://dx.doi.org/10.4067/S0716-97602006000300003
24. Latorre, R., and C. Miller. 1983. Conduction and selectivity in potassium channels. J. Membr. Biol. 71:11-30. http://dx.doi.org/10.1007/BF01870671
25. 2+-activated (BK) channel. J. Physiol. 588:3141-3148. http://dx.doi.org/10.1113/jphysiol.2010.191999
26. Lee, U.S., and J. Cui. 2010. BK channel activation: structural and functional insights. Trends Neurosci. 33:415-423. http://dx.doi.org/10.1016/j.tins.2010.06.004
27. Lee, U.S., J. Shi, and J. Cui. 2010. Modulation of BK channel gating by the β2 subunit involves both membrane-spanning and cytoplasmic domains of Slo1. J. Neurosci. 30:16170-16179. http://dx.doi.org/10.1523/JNEUROSCI.2323-10.2010
28. Liu, G., S.I. Zakharov, L. Yang, R.S. Wu, S.X. Deng, D.W. Landry, A. Karlin, and S.O. Marx. 2008. Locations of the beta1 transmembrane helices in the BK potassium channel. Proc. Natl. Acad. Sci. USA. 105:10727-10732. http://dx.doi.org/10.1073/pnas.0805212105
29. Liu, G., X. Niu, R.S. Wu, N. Chudasama, Y. Yao, X. Jin, R. Weinberg, S.I. Zakharov, H. Motoike, S.O. Marx, and A. Karlin. 2010. Location of modulatory β subunits in BK potassium channels. J. Gen. Physiol. 135:449-459. http://dx.doi.org/10.1085/jgp.201010417
30. + channel. Science. 309:897-903. http://dx.doi.org/10.1126/science.1116269
31. + channel in a lipid membrane-like environment. Nature. 450:376-382. http://dx.doi.org/10.1038/nature06265
32. Lu, R., A. Alioua, Y. Kumar, M. Eghbali, E. Stefani, and L. Toro. 2006. MaxiK channel partners: physiological impact. J. Physiol. 570: 65-72. http://dx.doi.org/10.1113/jphysiol.2005.098913
33. 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. http://dx.doi.org/10.1085/jgp.200509421
34. Magleby, K.L. 2003. Gating mechanism of BK (Slo1) channels: so near, yet so far. J. Gen. Physiol. 121:81-96. http://dx.doi.org/10.1085/jgp.20028721
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. http://dx.doi.org/10.1126/science.271.5246.213
36. Mansoor, S.E., H.S. McHaourab, and D.L. Farrens. 2002. Mapping proximity within proteins using fluorescence spectroscopy. A study of T4 lysozyme showing that tryptophan residues quench bimane fluorescence. Biochemistry. 41:2475-2484. http://dx.doi.org/10.1021/bi011198i
37. Mansoor, S.E., M.A. Dewitt, and D.L. Farrens. 2010. Distance mapping in proteins using fluorescence spectroscopy: the tryptophaninduced quenching (TrIQ) method. Biochemistry. 49:9722-9731. http://dx.doi.org/10.1021/bi100907m
38. + 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. http://dx.doi.org/10.1073/pnas.94.25.14066
39. Morera, F.J., A. Alioua, P. Kundu, M. Salazar, C. Gonzales, A.D. Martinez, E. Stefani, L. Toro, and R. Latorre. 2012. The first transmembrane domain (TM1) of β2-subunit binds to the transmembrane domain S1 of α-subunit in BK potassium channels. FEBS Lett. In press.
40. Morrow, J.P., S.I. Zakharov, G. Liu, L. Yang, A.J. Sok, and S.O. Marx. 2006. Defining the BK channel domains required for beta1-subunit modulation. Proc. Natl. Acad. Sci. USA. 103:5096-5101. http://dx.doi.org/10.1073/pnas.0600907103
41. Nelson, R.D., G. Kuan, M.H. Saier Jr., and M. Montal. 1999. Modular assembly of voltage-gated channel proteins: a sequence analysis and phylogenetic study. J. Mol. Microbiol. Biotechnol. 1:281-287.
42. Orio, P., and R. Latorre. 2005. Differential effects of β1 and β2 subunits on BK channel activity. J. Gen. Physiol. 125:395-411. http://dx.doi.org/10.1085/jgp.200409236
43. Orio, P., P. Rojas, G. Ferreira, and R. Latorre. 2002. New disguises for an old channel: MaxiK channel beta-subunits. News Physiol. Sci. 17:156-161.
44. + channel. Proc. Natl. Acad. Sci. USA. 107:4459-4464. http://dx.doi.org/10.1073/pnas.0911959107
45. Ca channel. J. Gen. Physiol. 136:645-657. http://dx.doi.org/10.1085/jgp.201010503
46. + channels described by a two-tiered allosteric gating mechanism. J. Gen. Physiol. 116:75-99. http://dx.doi.org/10.1085/jgp.116.1.75
47. Salkoff, L., A. Butler, G. Ferreira, C. Santi, and A. Wei. 2006. Highconductance potassium channels of the SLO family. Nat. Rev. Neurosci. 7:921-931. http://dx.doi.org/10.1038/nrn1992
48. Savalli, N., A. Kondratiev, L. Toro, and R. Olcese. 2006. Voltagedependent conformational changes in human Ca(2+)- and voltageactivated K(+) channel, revealed by voltage-clamp fluorometry. Proc. Natl. Acad. Sci. USA. 103:12619-12624. http://dx.doi.org/10.1073/pnas.0601176103
49. Savalli, N., A. Kondratiev, S.B. de Quintana, L. Toro, and R. Olcese. 2007. Modes of operation of the BKCa channel beta2 subunit. J. Gen. Physiol. 130:117-131. http://dx.doi.org/10.1085/jgp.200709803
50. Savalli, N., A. Pantazis, T. Yusifov, D. Sigg, and R. Olcese. 2012. The contribution of RCK domains to human BK channel allosteric activation. J. Biol. Chem. 287:21741-21750. http://dx.doi.org/10.1074/jbc.M112.346171
51. Schreiber, M., and L. Salkoff. 1997. A novel calcium-sensing domain in the BK channel. Biophys. J. 73:1355-1363. http://dx.doi.org/10.1016/S0006-3495(97)78168-2
52. Semenova, N.P., K. Abarca-Heidemann, E. Loranc, and B.S. Rothberg. 2009. Bimane fluorescence scanning suggests secondary structure near the S3-S4 linker of BK channels. J. Biol. Chem. 284:10684-10693. http://dx.doi.org/10.1074/jbc.M808891200
53. 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. Pflugers Arch. 426:440-445. http://dx.doi.org/10.1007/BF00388308
54. Stefani, E., and F. Bezanilla. 1998. Cut-open oocyte voltage-clamp technique. Methods Enzymol. 293:300-318. http://dx.doi.org/10.1016/S0076-6879(98)93020-8
55. +channel (hslo). Proc. Natl. Acad. Sci. USA. 94:5427-5431. http://dx.doi.org/10.1073/pnas.94.10.5427
56. Sun, X., M.A. Zaydman, and J. Cui. 2012. Regulation of voltageactivated K(+) channel gating by transmembrane β subunits. Front Pharmacol. 3:63.
57. Swartz, K.J. 2004. Towards a structural view of gating in potassium channels. Nat. Rev. Neurosci. 5:905-916. http://dx.doi.org/10.1038/nrn1559
58. Swartz, K.J. 2008. Sensing voltage across lipid membranes. Nature. 456:891-897. http://dx.doi.org/10.1038/nature07620
59. 2+ binding constants: effects of membrane voltage. J. Gen. Physiol. 132:491-505. http://dx.doi.org/10.1085/jgp.200810094
60. Tombola, F., M.M. Pathak, and E.Y. Isacoff. 2006. How does voltage open an ion channel? Annu. Rev. Cell Dev. Biol. 22:23-52. http://dx.doi.org/10.1146/annurev.cellbio.21.020404.145837
61. Toro, L., M. Wallner, P. Meera, and Y. Tanaka. 1998. Maxi-K(Ca), a unique member of the voltage-gated K channel superfamily. News Physiol. Sci. 13:112-117.
62. Unnerståle, S., J. Lind, E. Papadopoulos, and L. Mäler. 2009. Solution structure of the HsapBK K+ channel voltage-sensor paddle sequence. Biochemistry. 48:5813-5821. http://dx.doi.org/10.1021/bi9004599
63. Wallner, M., P. Meera, M. Ottolia, G.J. Kaczorowski, R. Latorre, M.L. Garcia, E. Stefani, and L. Toro. 1995. Characterization of and modulation by a beta-subunit of a human maxi KCa channel cloned from myometrium. Receptors Channels. 3:185-199.
64. + channels: an additional transmembrane region at the N terminus. Proc. Natl. Acad. Sci. USA. 93:14922-14927. http://dx.doi.org/10.1073/pnas.93.25.14922
65. Wang, L., and F.J. Sigworth. 2009. Structure of the BK potassium channel in a lipid membrane from electron cryomicroscopy. Nature. 461:292-295. http://dx.doi.org/10.1038/nature08291
66. Wei, A., C. Solaro, C. Lingle, and L. Salkoff. 1994. Calcium sensitivity of BK-type KCa channels determined by a separable domain. Neuron. 13:671-681. http://dx.doi.org/10.1016/0896-6273(94)90034-5
67. Wu, R.S., and S.O. Marx. 2010. The BK potassium channel in the vascular smooth muscle and kidney: α- and β-subunits. Kidney Int. 78:963-974. http://dx.doi.org/10.1038/ki.2010.325
68. Wu, R.S., N. Chudasama, S.I. Zakharov, D. Doshi, H. Motoike, G. Liu, Y. Yao, X. Niu, S.X. Deng, D.W. Landry, et al. 2009. Location of the beta 4 transmembrane helices in the BK potassium channel. J. Neurosci. 29:8321-8328. http://dx.doi.org/10.1523/JNEUROSCI.6191-08.2009
69. Wu, Y., Y. Yang, S. Ye, and Y. Jiang. 2010. Structure of the gating ring from the human large-conductance Ca(2+)-gated K(+) channel. Nature. 466:393-397. http://dx.doi.org/10.1038/nature09252
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. http://dx.doi.org/10.1038/nature00956
71. 2+ coordinated between the voltage sensor and RCK1 domains. Nat. Struct. Mol. Biol. 15:1152-1159. http://dx.doi.org/10.1038/nsmb.1507
72. 2+-activation apparatus at 3.0 A resolution. Science. 329:182-186. http://dx.doi.org/10.1126/science.1190414
73. + channel. Nature. 481:94-97. http://dx.doi.org/10.1038/nature10670
74. Yusifov, T., N. Savalli, C.S. Gandhi, M. Ottolia, and R. Olcese. 2008. The RCK2 domain of the human BKCa channel is a calcium sensor. Proc. Natl. Acad. Sci. USA. 105:376-381. http://dx.doi.org/10.1073/pnas.0705261105
75. 2+ binding into structural rearrangements. J. Gen. Physiol. 136: 189-202. http://dx.doi.org/10.1085/jgp.200910374
76. 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. http://dx.doi.org/10.1085/jgp.200409239
77. Zhang, G., S.Y. Huang, J. Yang, J. Shi, X. Yang, A. Moller, X. Zou, and J. Cui. 2010. Ion sensing in the RCK1 domain of BK channels. Proc. Natl. Acad. Sci. USA. 107:18700-18705. http://dx.doi.org/10.1073/pnas.1010124107