A BK (Slo1) channel journey from molecule to physiology

Channels

Volumn 7, Issue 6, 2013, Pages

  Contreras, Gustavo F ^a   Castillo, Karen ^a   Enrique, Nicolás ^c   Carrasquel Ursulaez, Willy ^a   Castillo, Juan Pablo ^a,b   Milesi, Verónica ^c   Neely, Alan ^a   Alvarez, Osvaldo ^b   Ferreira, Gonzalo ^d   Gonzalez, Carlos ^a   Latorre, Ramon ^a  

^a UNIVERSIDAD DE VALPARAÍSO   (Chile)

^b UNIVERSITY OF CHILE   (Chile)

^c UNIVERSIDAD NACIONAL DE LA PLATA   (Argentina)

^d UNIVERSIDAD DE LA REPÚBLICA   (Uruguay)

Author keywords

Auxiliary subunits; BK channels; Diseases; Slo1; Smooth muscle; Voltage sensor

Indexed keywords

CALCIUM; LARGE CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL; LARGE CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL ALPHA SUBUNIT; LARGE CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL BETA SUBUNIT; SCORPION VENOM; POTASSIUM CHANNEL BLOCKING AGENT;

ALTERNATIVE RNA SPLICING; ASTHMA; CALCIUM CELL LEVEL; CELL FUNCTION; CHANNEL GATING; CRYSTAL STRUCTURE; DIABETES MELLITUS; HAIR CELL; HUMAN; HYPERTENSION; KIDNEY DISEASE; NEGATIVE FEEDBACK; NEOPLASM; NEUROLOGIC DISEASE; NONHUMAN; PATHOPHYSIOLOGY; PROTEIN DOMAIN; PROTEIN PROCESSING; PROTEIN STRUCTURE; REVIEW; SENSOR; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; VASCULAR SMOOTH MUSCLE; ANIMAL; ANTAGONISTS AND INHIBITORS; CHEMISTRY; DISEASES; GENETICS; METABOLISM;

ANIMALS; CALCIUM; DISEASE; HUMANS; ION CHANNEL GATING; LARGE-CONDUCTANCE CALCIUM-ACTIVATED POTASSIUM CHANNELS; POTASSIUM CHANNEL BLOCKERS;

EID: 84886994171     PISSN: 19336950     EISSN: 19336969     Source Type: Journal    
DOI: 10.4161/chan.26242     Document Type: Review

References (240)

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2. Krnjevic K, Lisiewicz A. Injections of calcium ions into spinal motoneurones. J Physiol 1972; 225:363-90; PMID:5074394
3. Heyer CB, Lux HD. Control of the delayed outward potassium currents in bursting pace-maker neurones of the snail, Helix pomatia. J Physiol 1976; 262:349-82; PMID:994042
4. Meech RW, Standen NB. Potassium activation in Helix aspersa neurones under voltage clamp: a component mediated by calcium influx. J Physiol 1975; 249:211-39; PMID:1177091
5. Brown AM, Ellory JC, Young JD, Lew VL. A calcium-activated potassium channel present in foetal red cells of the sheep but absent from reticulocytes and mature red cells. Biochim Biophys Acta 1978; 511:163-75; PMID:354695; http://dx.doi.org/10.1016/0005-2736(78)90311-5 (Pubitemid 8383459)
6. Hotson JR, Prince DA. A calcium-activated hyperpolarization follows repetitive firing in hippocampal neurons. J Neurophysiol 1980; 43:409-19; PMID:6247461 (Pubitemid 10098370)
7. Pallotta BS, Magleby KL, Barrett JN. Single channel recordings of Ca2+-activated K+ currents in rat muscle cell culture. Nature 1981; 293:471-4; PMID:6273730; http://dx.doi.org/10.1038/293471a0 (Pubitemid 12193176)
8. Marty A. Ca-dependent K channels with large unitary conductance in chromaffin cell membranes. Nature 1981; 291:497-500; PMID:6262657; http://dx.doi.org/10.1038/291497a0 (Pubitemid 11093668)
9. Latorre R, Vergara C, Hidalgo C. Reconstitution in planar lipid bilayers of a Ca2+-dependent K+ channel from transverse tubule membranes isolated from rabbit skeletal muscle. Proc Natl Acad Sci U S A 1982; 79:805-9; PMID:6278496; http://dx.doi.org/10.1073/pnas.79.3.805 (Pubitemid 12160319)
10. Latorre R, Miller C. Conduction and selectivity in potassium channels. J Membr Biol 1983; 71:11-30; PMID:6300405; http://dx.doi.org/10.1007/BF01870671 (Pubitemid 13156990)
11. Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch 1981; 391:85-100; PMID:6270629; http://dx.doi.org/10.1007/BF00656997 (Pubitemid 11012976)
12. Rink TJ, Deutsch C. Calcium-activated potassium channels in lymphocytes. Cell Calcium 1983; 4:463-73; PMID:6323008; http://dx.doi.org/10.1016/0143- 4160(83)90022-2 (Pubitemid 14154090)
13. Jenkinson DH, Haylett DG, Cook NS. Calcium-activated potassium channels in liver cells. Cell Calcium 1983; 4:429-37; PMID:6323005; http://dx.doi.org/10. 1016/0143-4160(83)90019-2 (Pubitemid 14154087)
14. Hunter M, Lopes AG, Boulpaep EL, Giebisch GH. Single channel recordings of calcium-activated potassium channels in the apical membrane of rabbit cortical collecting tubules. Proc Natl Acad Sci U S A 1984; 81:4237-9; PMID:6330754; http://dx.doi.org/10.1073/pnas.81.13.4237 (Pubitemid 14054556)
15. Trautmann A, Marty A. Activation of Ca-dependent K channels by carbamoylcholine in rat lacrimal glands. Proc Natl Acad Sci U S A 1984; 81:611-5; PMID:6320199; http://dx.doi.org/10.1073/pnas.81.2.611 (Pubitemid 14186615)
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18. Orio P, Rojas P, Ferreira G, Latorre R. New disguises for an old channel: MaxiK channel beta-subunits. News Physiol Sci 2002; 17:156-61; PMID:12136044
19. Salkoff L, Butler A, Ferreira G, Santi C, Wei A. High-conductance potassium channels of the SLO family. Nat Rev Neurosci 2006; 7:921-31; PMID:17115074; http://dx.doi.org/10.1038/nrn1992
20. Miller C, Moczydlowski E, Latorre R, Phillips M. Charybdotoxin, a protein inhibitor of single Ca2+-activated K+ channels from mammalian skeletal muscle. Nature 1985; 313:316-8; PMID:2578618; http://dx.doi.org/10.1038/313316a0 (Pubitemid 15151987)
21. Galvez A, Gimenez-Gallego G, Reuben JP, Roy-Contancin L, Feigenbaum P, Kaczorowski GJ, Garcia ML. Purification and characterization of a unique, potent, peptidyl probe for the high conductance calcium-activated potassium channel from venom of the scorpion Buthus tamulus. J Biol Chem 1990; 265:11083-90; PMID:1694175
22. Elkins T, Ganetzky B, Wu CF. A Drosophila mutation that eliminates a calcium-dependent potassium current. Proc Natl Acad Sci U S A 1986; 83:8415-9; PMID:2430288; http://dx.doi.org/10.1073/pnas.83.21.8415 (Pubitemid 17182511)
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24. Adelman JP, Shen KZ, Kavanaugh MP, Warren RA, Wu YN, Lagrutta A, Bond CT, North RA. Calcium-activated potassium channels expressed from cloned complementary DNAs. Neuron 1992; 9:209-16; PMID:1497890; http://dx.doi.org/10. 1016/0896-6273(92)90160-F
25. Butler A, Tsunoda S, McCobb DP, Wei A, Salkoff L. mSlo, a complex mouse gene encoding "maxi" calcium-activated potassium channels. Science 1993; 261:221-4; PMID:7687074; http://dx.doi.org/10.1126/science.7687074 (Pubitemid 23265401)
26. Berkefeld H, Fakler B, Schulte U. Ca2+-activated K+ channels: from protein complexes to function. Physiol Rev 2010; 90:1437-59; PMID:20959620; http://dx.doi.org/10.1152/physrev.00049.2009
27. Wallner M, Meera P, Toro L. Determinant for beta-subunit regulation in high-conductance voltage-activated and Ca(2+)-sensitive K+ channels: an additional transmembrane region at the N terminus. Proc Natl Acad Sci U S A 1996; 93:14922-7; PMID:8962157; http://dx.doi.org/10.1073/pnas.93.25.14922
28. Schreiber M, Wei A, Yuan A, Gaut J, Saito M, Salkoff L. Slo3, a novel pH-sensitive K+ channel from mammalian spermatocytes. J Biol Chem 1998; 273:3509-16; PMID:9452476; http://dx.doi.org/10.1074/jbc.273.6.3509 (Pubitemid 28109773)
29. Quirk JC, Reinhart PH. Identification of a novel tetramerization domain in large conductance K(ca) channels. Neuron 2001; 32:13-23; PMID:11604135; http://dx.doi.org/10.1016/S0896-6273(01)00444-5 (Pubitemid 32995886)
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31. Díaz L, Meera P, Amigo J, Stefani E, Alvarez O, Toro L, Latorre R. Role of the S4 segment in a voltage-dependent calcium-sensitive potassium (hSlo) channel. J Biol Chem 1998; 273:32430-6; PMID:9829973; http://dx.doi.org/10.1074/jbc.273.49.32430 (Pubitemid 28557615)
32. McManus OB, Magleby KL. Accounting for the Ca(2+)-dependent kinetics of single large-conductance Ca(2+)-activated K+ channels in rat skeletal muscle. J Physiol 1991; 443:739-77; PMID:1822543
33. Cox DH, Cui J, Aldrich RW. Allosteric gating of a large conductance Ca-activated K+ channel. J Gen Physiol 1997; 110:257-81; PMID:9276753; http://dx.doi.org/10.1085/jgp.110.3.257 (Pubitemid 27388118)
34. Lee US, Cui J. BK channel activation: structural and functional insights. Trends Neurosci 2010; 33:415-23; PMID:20663573; http://dx.doi.org/10.1016/j. tins.2010.06.004
35. Pérez GJ, Bonev AD, Nelson MT. Micromolar Ca(2+) from sparks activates Ca(2+)-sensitive K(+) channels in rat cerebral artery smooth muscle. Am J Physiol Cell Physiol 2001; 281:C1769-75; PMID:11698234
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45. Krnjevic K, Lisiewicz A. Injections of calcium ions into spinal motoneurones. J Physiol 1972; 225:363-90; PMID:5074394
46. Heyer CB, Lux HD. Control of the delayed outward potassium currents in bursting pace-maker neurones of the snail, Helix pomatia. J Physiol 1976; 262:349-82; PMID:994042
47. Meech RW, Standen NB. Potassium activation in Helix aspersa neurones under voltage clamp: a component mediated by calcium influx. J Physiol 1975; 249:211-39; PMID:1177091
48. Brown AM, Ellory JC, Young JD, Lew VL. A calcium-activated potassium channel present in foetal red cells of the sheep but absent from reticulocytes and mature red cells. Biochim Biophys Acta 1978; 511:163-75; PMID:354695; http://dx.doi.org/10.1016/0005-2736(78)90311-5 (Pubitemid 8383459)
49. Hotson JR, Prince DA. A calcium-activated hyperpolarization follows repetitive firing in hippocampal neurons. J Neurophysiol 1980; 43:409-19; PMID:6247461 (Pubitemid 10098370)
50. Pallotta BS, Magleby KL, Barrett JN. Single channel recordings of Ca2+-activated K+ currents in rat muscle cell culture. Nature 1981; 293:471-4; PMID:6273730; http://dx.doi.org/10.1038/293471a0 (Pubitemid 12193176)
51. Marty A. Ca-dependent K channels with large unitary conductance in chromaffin cell membranes. Nature 1981; 291:497-500; PMID:6262657; http://dx.doi.org/10.1038/291497a0 (Pubitemid 11093668)
52. Latorre R, Vergara C, Hidalgo C. Reconstitution in planar lipid bilayers of a Ca2+-dependent K+ channel from transverse tubule membranes isolated from rabbit skeletal muscle. Proc Natl Acad Sci U S A 1982; 79:805-9; PMID:6278496; http://dx.doi.org/10.1073/pnas.79.3.805 (Pubitemid 12160319)
53. Latorre R, Miller C. Conduction and selectivity in potassium channels. J Membr Biol 1983; 71:11-30; PMID:6300405; http://dx.doi.org/10.1007/BF01870671 (Pubitemid 13156990)
54. Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch 1981; 391:85-100; PMID:6270629; http://dx.doi.org/10.1007/BF00656997 (Pubitemid 11012976)
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56. Jenkinson DH, Haylett DG, Cook NS. Calcium-activated potassium channels in liver cells. Cell Calcium 1983; 4:429-37; PMID:6323005; http://dx.doi.org/10. 1016/0143-4160(83)90019-2 (Pubitemid 14154087)
57. Hunter M, Lopes AG, Boulpaep EL, Giebisch GH. Single channel recordings of calcium-activated potassium channels in the apical membrane of rabbit cortical collecting tubules. Proc Natl Acad Sci U S A 1984; 81:4237-9; PMID:6330754; http://dx.doi.org/10.1073/pnas.81.13.4237 (Pubitemid 14054556)
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59. Berger W, Grygorcyk R, Schwarz W. Single K+ channels in membrane evaginations of smooth muscle cells. Pflugers Arch 1984; 402:18-23; PMID:6095176; http://dx.doi.org/10.1007/BF00584826 (Pubitemid 14046390)
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63. Miller C, Moczydlowski E, Latorre R, Phillips M. Charybdotoxin, a protein inhibitor of single Ca2+-activated K+ channels from mammalian skeletal muscle. Nature 1985; 313:316-8; PMID:2578618; http://dx.doi.org/10.1038/313316a0 (Pubitemid 15151987)
64. Galvez A, Gimenez-Gallego G, Reuben JP, Roy-Contancin L, Feigenbaum P, Kaczorowski GJ, Garcia ML. Purification and characterization of a unique, potent, peptidyl probe for the high conductance calcium-activated potassium channel from venom of the scorpion Buthus tamulus. J Biol Chem 1990; 265:11083-90; PMID:1694175
65. Elkins T, Ganetzky B, Wu CF. A Drosophila mutation that eliminates a calcium-dependent potassium current. Proc Natl Acad Sci U S A 1986; 83:8415-9; PMID:2430288; http://dx.doi.org/10.1073/pnas.83.21.8415 (Pubitemid 17182511)
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67. Adelman JP, Shen KZ, Kavanaugh MP, Warren RA, Wu YN, Lagrutta A, Bond CT, North RA. Calcium-activated potassium channels expressed from cloned complementary DNAs. Neuron 1992; 9:209-16; PMID:1497890; http://dx.doi.org/10. 1016/0896-6273(92)90160-F
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72. Quirk JC, Reinhart PH. Identification of a novel tetramerization domain in large conductance K(ca) channels. Neuron 2001; 32:13-23; PMID:11604135; http://dx.doi.org/10.1016/S0896-6273(01)00444-5 (Pubitemid 32995886)
73. Wang L, Sigworth FJ. Structure of the BK potassium channel in a lipid membrane from electron cryomicroscopy. Nature 2009; 461:292-5; PMID:19718020; http://dx.doi.org/10.1038/nature08291
74. Díaz L, Meera P, Amigo J, Stefani E, Alvarez O, Toro L, Latorre R. Role of the S4 segment in a voltage-dependent calcium-sensitive potassium (hSlo) channel. J Biol Chem 1998; 273:32430-6; PMID:9829973; http://dx.doi.org/10.1074/jbc.273.49.32430 (Pubitemid 28557615)
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76. Cox DH, Cui J, Aldrich RW. Allosteric gating of a large conductance Ca-activated K+ channel. J Gen Physiol 1997; 110:257-81; PMID:9276753; http://dx.doi.org/10.1085/jgp.110.3.257 (Pubitemid 27388118)
77. Lee US, Cui J. BK channel activation: structural and functional insights. Trends Neurosci 2010; 33:415-23; PMID:20663573; http://dx.doi.org/10.1016/j. tins.2010.06.004
78. Pérez GJ, Bonev AD, Nelson MT. Micromolar Ca(2+) from sparks activates Ca(2+)-sensitive K(+) channels in rat cerebral artery smooth muscle. Am J Physiol Cell Physiol 2001; 281:C1769-75; PMID:11698234
79. Roberts WM, Jacobs RA, Hudspeth AJ. Colocalization of ion channels involved in frequency selectivity and synaptic transmission at presynaptic active zones of hair cells. J Neurosci 1990; 10:3664-84; PMID:1700083
80. Issa NP, Hudspeth AJ. Clustering of Ca2+ channels and Ca(2+)-activated K+ channels at fluorescently labeled presynaptic active zones of hair cells. Proc Natl Acad Sci U S A 1994; 91:7578-82; PMID:8052623; http://dx.doi.org/10.1073/ pnas.91.16.7578
81. Berkefeld H, Sailer CA, Bildl W, Rohde V, Thumfart JO, Eble S, Klugbauer N, Reisinger E, Bischofberger J, Oliver D, et al. BKCa-Cav channel complexes mediate rapid and localized Ca2+-activated K+ signaling. Science 2006; 314:615-20; PMID:17068255; http://dx.doi.org/10.1126/science.1132915 (Pubitemid 44646378)
82. Horrigan FT, Aldrich RW. Coupling between voltage sensor activation, Ca2+ binding and channel opening in large conductance (BK) potassium channels. J Gen Physiol 2002; 120:267-305; PMID:12198087; http://dx.doi.org/10.1085/jgp. 20028605 (Pubitemid 35014730)
83. Barrett JN, Magleby KL, Pallotta BS. Properties of single calcium-activated potassium channels in cultured rat muscle. J Physiol 1982; 331:211-30; PMID:6296366 (Pubitemid 12002600)
84. Schreiber M, Salkoff L. A novel calcium-sensing domain in the BK channel. Biophys J 1997; 73:1355-63; PMID:9284303; http://dx.doi.org/10.1016/S0006- 3495(97)78168-2 (Pubitemid 27360725)
85. Bao L, Rapin AM, Holmstrand EC, Cox DH. Elimination of the BK(Ca) channel's high-affinity Ca(2+) sensitivity. J Gen Physiol 2002; 120:173-89; PMID:12149279; http://dx.doi.org/10.1085/jgp.20028627 (Pubitemid 34857967)
86. Bao L, Kaldany C, Holmstrand EC, Cox DH. Mapping the BKCa channel's "Ca2+ bowl": side-chains essential for Ca2+ sensing. J Gen Physiol 2004; 123:475-89; PMID:15111643; http://dx.doi.org/10.1085/jgp.200409052 (Pubitemid 38590853)
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103. Bai JP, Surguchev A, Navaratnam D. β4-subunit increases Slo responsiveness to physiological Ca2+ concentrations and together with β1 reduces surface expression of Slo in hair cells. Am J Physiol Cell Physiol 2011; 300:C435-46; PMID:21178105; http://dx.doi.org/10.1152/ajpcell.00449.2010
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112. Hoshi T, Tian Y, Xu R, Heinemann SH, Hou S. Mechanism of the modulation of BK potassium channel complexes with different auxiliary subunit compositions by the omega-3 fatty acid DHA. Proc Natl Acad Sci U S A 2013; 110:4822-7; PMID:23487786; http://dx.doi.org/10.1073/pnas.1222003110
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135. Zhou XB, Wang GX, Huneke B, Wieland T, Korth M. Pregnancy switches adrenergic signal transduction in rat and human uterine myocytes as probed by BKCa channel activity. J Physiol 2000; 524:339-52; PMID:10766916; http://dx.doi.org/10.1111/j.1469-7793.2000.t01-1-00339.x (Pubitemid 30229501)
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139. Yan J, Olsen JV, Park KS, Li W, Bildl W, Schulte U, Aldrich RW, Fakler B, Trimmer JS. Profiling the phospho-status of the BKCa channel alpha subunit in rat brain reveals unexpected patterns and complexity. Mol Cell Proteomics 2008; 7:2188-98; PMID:18573811; http://dx.doi.org/10.1074/mcp. M800063-MCP200
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142. Bai JP, Surguchev A, Navaratnam D. β4-subunit increases Slo responsiveness to physiological Ca2+ concentrations and together with β1 reduces surface expression of Slo in hair cells. Am J Physiol Cell Physiol 2011; 300:C435-46; PMID:21178105; http://dx.doi.org/10.1152/ajpcell.00449.2010
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144. Wu RS, Liu G, Zakharov SI, Chudasama N, Motoike H, Karlin A, Marx SO. Positions of β2 and β3 subunits in the large-conductance calcium-and voltage-activated BK potassium channel. J Gen Physiol 2013; 141:105-17; PMID:23277477; http://dx.doi.org/10.1085/jgp.201210891
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146. Morera FJ, Alioua A, Kundu P, Salazar M, Gonzalez C, Martinez AD, Stefani E, Toro L, Latorre R. The first transmembrane domain (TM1) of β2-subunit binds to the transmembrane domain S1 of α-subunit in BK potassium channels. FEBS Lett 2012; 586:2287-93; PMID:22710124; http://dx.doi.org/10.1016/ j.febslet.2012.05.066
147. Orio P, Latorre R. Differential effects of beta 1 and beta 2 subunits on BK channel activity. J Gen Physiol 2005; 125:395-411; PMID:15767297; http://dx.doi.org/10.1085/jgp.200409236
148. Cox DH, Aldrich RW. Role of the beta1 subunit in large-conductance Ca(2+)-activated K(+) channel gating energetics. Mechanisms of enhanced Ca(2+) sensitivity. J Gen Physiol 2000; 116:411-32; PMID:10962017; http://dx.doi.org/ 10.1085/jgp.116.3.411
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150. Valverde MA, Rojas P, Amigo J, Cosmelli D, Orio P, Bahamonde MI, Mann GE, Vergara C, Latorre R. Acute activation of Maxi-K channels (hSlo) by estradiol binding to the beta subunit. Science 1999; 285:1929-31; PMID:10489376; http://dx.doi.org/10.1126/science.285.5435.1929
151. Hoshi T, Tian Y, Xu R, Heinemann SH, Hou S. Mechanism of the modulation of BK potassium channel complexes with different auxiliary subunit compositions by the omega-3 fatty acid DHA. Proc Natl Acad Sci U S A 2013; 110:4822-7; PMID:23487786; http://dx.doi.org/10.1073/pnas.1222003110
152. Dworetzky SI, Boissard CG, Lum-Ragan JT, McKay MC, Post-Munson DJ, Trojnacki JT, Chang CP, Gribkoff VK. Phenotypic alteration of a human BK (hSlo) channel by hSlobeta subunit coexpression: changes in blocker sensitivity, activation/relaxation and inactivation kinetics, and protein kinase A modulation. J Neurosci 1996; 16:4543-50; PMID:8764643 (Pubitemid 26251051)
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157. Xia XM, Ding JP, Lingle CJ. Inactivation of BK channels by the NH2 terminus of the beta2 auxiliary subunit: an essential role of a terminal peptide segment of three hydrophobic residues. J Gen Physiol 2003; 121:125-48; PMID:12566540; http://dx.doi.org/10.1085/jgp.20028667 (Pubitemid 36255342)
158. Benzinger GR, Xia XM, Lingle CJ. Direct observation of a preinactivated, open state in BK channels with beta2 subunits. J Gen Physiol 2006; 127:119-31; PMID:16418401; http://dx.doi.org/10.1085/jgp.200509425 (Pubitemid 43177135)
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