Bk Channel and Alcohol, a Complicated Affair

International Review of Neurobiology

Volumn 91, Issue C, 2010, Pages 321-338

  Martin, Gilles Erwan ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

Alcohol; Behavior; BK channel; Dendrites; Nucleus accumbens

Indexed keywords

ALCOHOL; CALCIUM; LARGE CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL; LARGE CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL BETA SUBUNIT;

ALCOHOL ABUSE; ALCOHOL CONSUMPTION; BEHAVIOR CHANGE; BOOK; BRAIN REGION; CALCIUM CELL LEVEL; CORPUS STRIATUM; DRINKING BEHAVIOR; ENZYME PHOSPHORYLATION; HUMAN; LIPID MEMBRANE; NERVE CELL MEMBRANE POTENTIAL; NERVE CELL STIMULATION; NEUROMODULATION; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SYNAPTIC TRANSMISSION;

EID: 77956143556     PISSN: 00747742     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0074-7742(10)91010-6     Document Type: Chapter

References (104)

1. Adams P.R., Constanti A., Brown D.A., Clark R.B. Intracellular Ca2+ activates a fast voltage-sensitive K+ current in vertebrate sympathetic neurones. Nature 1982, 296:746-749.
2. Adelman J.P., Shen K.Z., Kavanaugh M.P., Warren R.A., Wu Y.N., Lagrutta A., Bond C.T., North R.A. Calcium-activated potassium channels expressed from cloned complementary DNAs. Neuron 1992, 9:209-216.
3. Aroor A.R., Shukla S.D. MAP kinase signaling in diverse effects of ethanol. Life Sci. 2004, 74:2339-2364.
4. Atkinson N.S., Robertson G.A., Ganetzky B. A component of calcium-activated potassium channels encoded by the Drosophila slo locus. Science 1991, 253:551-555.
5. Backus K.H., Trube G. Single-channel activity in cultured cortical neurons of the rat in the presence of a toxic dose of glutamate. Eur. J. Neurosci. 1993, 5:174-185.
6. Behrens R., Nolting A., Reimann F., Schwarz M., Waldschutz R., Pongs O. hKCNMB3 and hKCNMB4, cloning and characterization of two members of the large-conductance calcium-activated potassium channel beta subunit family. FEBS Lett. 2000, 474:99-106.
7. Benhassine N., Berger T. Large-conductance calcium-dependent potassium channels prevent dendritic excitability in neocortical pyramidal neurons. Pflugers Arch. 2008, 457:1133-1145.
8. Benhassine N., Berger T. Homogeneous distribution of large-conductance calcium-dependent potassium channels on soma and apical dendrite of rat neocortical layer 5 pyramidal neurons. Eur. J. Neurosci. 2005, 21:914-926.
9. Bielefeldt K., Rotter J.L., Jackson M.B. Three potassium channels in rat posterior pituitary nerve terminals. J. Physiol. 1992, 458:41-67.
10. Boehm S.L., Peden L., Chang R., Harris R.A., Blednov Y.A. Deletion of the fyn-kinase gene alters behavioral sensitivity to ethanol. Alcohol. Clin. Exp. Res. 2003, 27:1033-1040.
11. Bowers B.J., Wehner J.M. Ethanol consumption and behavioral impulsivity are increased in protein kinase Cgamma null mutant mice. J. Neurosci. 2001, 21:RC180.
12. Brenner R., Chen Q.H., Vilaythong A., Toney G.M., Noebels J.L., Aldrich R.W. BK channel beta4 subunit reduces dentate gyrus excitability and protects against temporal lobe seizures. Nat. Neurosci. 2005, 8:1752-1759.
13. Brenner R., Jegla T.J., Wickenden A., Liu Y., Aldrich R.W. Cloning and functional characterization of novel large conductance calcium-activated potassium channel beta subunits, hKCNMB3 and hKCNMB4. J. Biol. Chem. 2000, 275:6453-6461.
14. Campanac E., Debanne D. Spike timing-dependent plasticity: A learning rule for dendritic integration in rat CA1 pyramidal neurons. J. Physiol. 2008, 586:779-793.
15. Chandler L.J., Harris R.A., Crews F.T. Ethanol tolerance and synaptic plasticity. Trends Pharmacol. Sci. 1998, 19:491-495.
16. Chang C.P., Dworetzky S.I., Wang J., Goldstein M.E. Differential expression of the alpha and beta subunits of the large-conductance calcium-activated potassium channel: Implication for channel diversity. Brain Res. Mol. Brain Res. 1997, 45:33-40.
17. Chen L., Tian L., MacDonald S.H., McClafferty H., Hammond M.S., Huibant J.M., Ruth P., Knaus H.G., Shipston M.J. Functionally diverse complement of large conductance calcium- and voltage-activated potassium channel (BK) alpha-subunits generated from a single site of splicing. J. Biol. Chem. 2005, 280:33599-33609.
18. Chrostek L., Szmitkowski M. Genetic evaluation of tolerance to alcohol. Postepy Hig Med Dosw 1998, 52:35-47.
19. Cowmeadow R.B., Krishnan H.R., Ghezzi A., Al'Hasan Y.M., Wang Y.Z., Atkinson N.S. Ethanol tolerance caused by slowpoke induction in Drosophila. Alcohol. Clin. Exp. Res. 2006, 30:745-753.
20. Cowmeadow R.B., Krishnan H.R., Atkinson N.S. The slowpoke gene is necessary for rapid ethanol tolerance in Drosophila. Alcohol. Clin. Exp. Res. 2005, 29:1777-1786.
21. Crews F.T., Morrow A.L., Criswell H., Breese G. Effects of ethanol on ion channels. Int. Rev. Neurobiol. 1996, 39:283-367.
22. Crowder C.M. Ethanol targets: A BK channel cocktail in C. elegans. Trends Neurosci. 2004, 27:579-582.
23. Crowley J.J., Treistman S.N., Dopico A.M. Cholesterol antagonizes ethanol potentiation of human brain BKCa channels reconstituted into phospholipid bilayers. Mol. Pharmacol. 2003, 64:365-372.
24. Crowley J.J., Treistman S.N., Dopico A.M. Distinct structural features of phospholipids differentially determine ethanol sensitivity and basal function of BK channels. Mol. Pharmacol. 2005, 68:4-10.
25. Dan Y., Poo M.M. Spike timing-dependent plasticity of neural circuits. Neuron 2004, 44:23-30.
26. Davies A.G., Pierce-Shimomura J.T., Kim H., VanHoven M.K., Thiele T.R., Bonci A., Bargmann C.I., McIntire S.L. A central role of the BK potassium channel in behavioral responses to ethanol in C. elegans. Cell 2003, 115:655-666.
27. Dopico A.M., Anantharam V., Treistman S.N. Ethanol increases the activity of Ca(++)-dependent K+ (mslo) channels: Functional interaction with cytosolic Ca++. J. Pharmacol. Exp. Ther. 1998, 284:258-268.
28. Dopico A.M., Lemos J.R., Treistman S.N. Ethanol increases the activity of large conductance, Ca(2+)-activated K+ channels in isolated neurohypophysial terminals. Mol. Pharmacol. 1996, 49:40-48.
29. Dopico A.M. Ethanol sensitivity of BK(Ca) channels from arterial smooth muscle does not require the presence of the beta 1-subunit. Am. J. Physiol. Cell. Physiol. 2003, 284:C1468-1480.
30. Edgerton J.R., Reinhart P.H. Distinct contributions of small and large conductance Ca2+-activated K+ channels to rat Purkinje neuron function. J. Physiol. 2003, 548:53-69.
31. Erwin V.G., McClearn G.E., Kuse A.R. Interrelationships of alcohol consumption, actions of alcohol, and biochemical traits. Pharmacol. Biochem. Behav. 1980, 13(Suppl 1):297-302.
32. Erxleben C., Everhart A.L., Romeo C., Florance H., Bauer M.B., Alcorta D.A., Rossie S., Shipston M.J., Armstrong D.L. Interacting effects of N-terminal variation and strex exon splicing on slo potassium channel regulation by calcium, phosphorylation, and oxidation. J. Biol. Chem. 2002, 277:27045-27052.
33. Faber E.S., Sah P. Physiological role of calcium-activated potassium currents in the rat lateral amygdala. J. Neurosci. 2002, 22:1618-1628.
34. Faber E.S., Sah P. Ca2+-activated K+ (BK) channel inactivation contributes to spike broadening during repetitive firing in the rat lateral amygdala. J. Physiol. 2003, 552:483-497.
35. Fakler B., Adelman J.P. Control of K(Ca) channels by calcium nano/microdomains. Neuron 2008, 59:873-881.
36. Feinberg-Zadek P.L., Treistman S.N. Beta-subunits are important modulators of the acute response to alcohol in human BK channels. Alcohol. Clin. Exp. Res. 2007, 31:737-744.
37. Fillmore M.T., Marczinski C.A., Bowman A.M. Acute tolerance to alcohol effects on inhibitory and activational mechanisms of behavioral control. J. Stud. Alcohol 2005, 66:663-672.
38. Fuenzalida M., Fernandez de Sevilla D., Couve A., Buno W. Role of AMPA and NMDA receptors and back-propagating action potentials in spike timing-dependent plasticity. J. Neurophysiol. 2010, 103:47-54.
39. Fukao M., Mason H.S., Britton F.C., Kenyon J.L., Horowitz B., Keef K.D. Cyclic GMP-dependent protein kinase activates cloned BKCa channels expressed in mammalian cells by direct phosphorylation at serine 1072. J. Biol. Chem. 1999, 274:10927-10935.
40. Fury M., Marx S.O., Marks A.R. Molecular BKology: The study of splicing and dicing. Sci. STKE 2002, 2002:PE12.
41. Gandhi C.R., Ross D.H. Influence of ethanol on calcium, inositol phospholipids and intracellular signalling mechanisms. Experientia 1989, 45:407-413.
42. Goldberg J.A., Wilson C.J. Control of spontaneous firing patterns by the selective coupling of calcium currents to calcium-activated potassium currents in striatal cholinergic interneurons. J. Neurosci. 2005, 25:10230-10238.
43. 2+ ]: Homogeneity and dependence on the alpha 1-subunit. Am. J. Physiol 1996, 271:C842-C850.
44. Gong L.W., Gao T.M., Huang H., Zhou K.X., Tong Z. ATP modulation of large conductance Ca(2+)-activated K(+) channels via a functionally associated protein kinase A in CA1 pyramidal neurons from rat hippocampus. Brain Res. 2002, 951:130-134.
45. Gruss M., Henrich M., Konig P., Hempelmann G., Vogel W., Scholz A. Ethanol reduces excitability in a subgroup of primary sensory neurons by activation of BK(Ca) channels. Eur. J. Neurosci. 2001, 14:1246-1256.
46. Ha T.S., Jeong S.Y., Cho S.W., Jeon H., Roh G.S., Choi W.S., Park C.S. Functional characteristics of two BKCa channel variants differentially expressed in rat brain tissues. Eur. J. Biochem. 2000, 267:910-918.
47. Hall S.K., Armstrong D.L. Conditional and unconditional inhibition of calcium-activated potassium channels by reversible protein phosphorylation. J. Biol. Chem. 2000, 275:3749-3754.
48. Heath A.C., Madden P.A., Bucholz K.K., Dinwiddie S.H., Slutske W.S., Bierut L.J., Rohrbaugh J.W., Statham D.J., Dunne M.P., Whitfield J.B., Martin N.G. Genetic differences in alcohol sensitivity and the inheritance of alcoholism risk. Psychol. Med. 1999, 29:1069-1081.
49. Isaacson J.S., Murphy G.J. Glutamate-mediated extrasynaptic inhibition: Direct coupling of NMDA receptors to Ca(2+)-activated K+ channels. Neuron 2001, 31:1027-1034.
50. Kamouchi M., Trouet D., De Greef C., Droogmans G., Eggermont J., Nilius B. Functional effects of expression of hslo Ca2+ activated K+ channels in cultured macrovascular endothelial cells. Cell Calcium 1997, 22:497-506.
51. Kang J., Huguenard J.R., Prince D.A. Two types of BK channels in immature rat neocortical pyramidal neurons. J. Neurophysiol. 1996, 76:4194-4197.
52. Kaufmann W.A., Ferraguti F., Fukazawa Y., Kasugai Y., Shigemoto R., Laake P., Sexton J.A., Ruth P., Wietzorrek G., Knaus H.G., Storm J.F., Ottersen O.P. Large-conductance calcium-activated potassium channels in Purkinje cell plasma membranes are clustered at sites of hypolemmal microdomains. J. Comp. Neurol. 2009, 515:215-230.
53. Knaus H.G., Schwarzer C., Koch R.O., Eberhart A., Kaczorowski G.J., Glossmann H., Wunder F., Pongs O., Garcia M.L., Sperk G. Distribution of high-conductance Ca(2+)-activated K+ channels in rat brain: Targeting to axons and nerve terminals. J. Neurosci. 1996, 16:955-963.
54. Lancaster B., Nicoll R.A. Properties of two calcium-activated hyperpolarizations in rat hippocampal neurones. J. Physiol. 1987, 389:187-203.
55. 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, 79:805-809.
56. Lee J., Ueda A., Wu C.F. Pre- and post-synaptic mechanisms of synaptic strength homeostasis revealed by slowpoke and shaker K(+) channel mutations in Drosophila. Neuroscience 2008, 154:1283-1296.
57. Liu J., Asuncion-Chin M., Liu P., Dopico A.M. CaM kinase II phosphorylation of slo Thr107 regulates activity and ethanol responses of BK channels. Nat. Neurosci. 2006, 9:41-49.
58. Liu X., Chang Y., Reinhart P.H., Sontheimer H., Chang Y. Cloning and characterization of glioma BK, a novel BK channel isoform highly expressed in human glioma cells. J. Neurosci. 2002, 22:1840-1849.
59. Livy D.J., Miller E.K., Maier S.E., West J.R. Fetal alcohol exposure and temporal vulnerability: Effects of binge-like alcohol exposure on the developing rat hippocampus. Neurotoxicol. Teratol. 2003, 25:447-458.
60. Loane D.J., Lima P.A., Marrion N.V. Co-assembly of N-type Ca2+ and BK channels underlies functional coupling in rat brain. J. Cell Sci. 2007, 120:985-995.
61. Markram H., Lubke J., Frotscher M., Sakmann B. Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science 1997, 275:213-215.
62. Marrion N.V., Tavalin S.J. Selective activation of Ca2+-activated K+ channels by co-localized Ca2+ channels in hippocampal neurons. Nature 1998, 395:900-905.
63. Martin G., Puig S., Pietrzykowski A., Zadek P., Emery P., Treistman S. Somatic localization of a specific large-conductance calcium-activated potassium channel subtype controls compartmentalized ethanol sensitivity in the nucleus accumbens. J. Neurosci. 2004, 24:6563-6572.
64. Martin G.E., Treistman S.N. BK channel: Mediator and model for alcohol tolerance. Trends in Neurosci 2009, 32:629-637.
65. Martin G.E., Hendrickson L.M., Penta K.L., Friesen R.M., Pietrzykowski A.Z., Tapper A.R., Treistman S.N Identification of a BK channel auxiliary protein controlling molecular and behavioral tolerance to alcohol. P.N.A.S. 2008, 105:17543-17548.
66. Marty A. Ca-dependent K channels with large unitary conductance in chromaffin cell membranes. Nature 1981, 291:497-500.
67. McCobb D.P., Fowler N.L., Featherstone T., Lingle C.J., Saito M., Krause J.E., Salkoff L. A human calcium-activated potassium channel gene expressed in vascular smooth muscle. Am. J. Physiol. 1995, 269:H767-777.
68. Miki T., Harris S.J., Wilce P., Takeuchi Y., Bedi K.S. Neurons in the hilus region of the rat hippocampus are depleted in number by exposure to alcohol during early postnatal life. Hippocampus 2000, 10:284-295.
69. Misonou H., Menegola M., Buchwalder L., Park E.W., Meredith A., Rhodes K.J., Aldrich R.W., Trimmer J.S. Immunolocalization of the Ca2+-activated K+ channel Slo1 in axons and nerve terminals of mammalian brain and cultured neurons. J. Comp. Neurol. 2006, 496:289-302.
70. Nara M., Dhulipala P.D., Ji G.J., Kamasani U.R., Wang Y.X., Matalon S., Kotlikoff M.I. Guanylyl cyclase stimulatory coupling to K(Ca) channels. Am. J. Physiol. Cell Physiol. 2000, 279:C1938-1945.
71. Newton P.M., Messing R.O. Intracellular signaling pathways that regulate behavioral responses to ethanol. Pharmacol. Ther. 2006, 109:227-237.
72. Olive M.F., Mehmert K.K., Messing R.O., Hodge C.W. Reduced operant ethanol self-administration and in vivo mesolimbic dopamine responses to ethanol in PKCepsilon-deficient mice. Eur. J. Neurosci. 2000, 12:4131-4140.
73. Pallotta B.S., Magleby K.L., Barrett J.N. Single channel recordings of Ca2+-activated K+ currents in rat muscle cell culture. Nature 1981, 293:471-474.
74. Park W.S., Son Y.K., Kim N., Youm J.B., Warda M., Ko J.H., Ko E.A., Kang S.H., Kim E., Earm Y.E., Han J. Direct modulation of Ca(2+)-activated K(+) current by H-89 in rabbit coronary arterial smooth muscle cells. Vascul. Pharmacol. 2007, 46:105-113.
75. Pietrzykowski A.Z., Friesen R.M., Martin G.E., Puig S.I., Nowak C.L., Wynne P.M., Siegelmann H.T., Treistman S.N. Posttranscriptional regulation of BK channel splice variant stability by miR-9 underlies neuroadaptation to alcohol. Neuron 2008, 59:274-287.
76. Quirk J.C., Reinhart P.H. Identification of a novel tetramerization domain in large conductance K(ca) channels. Neuron 2001, 32:13-23.
77. Rhodes J.S., et al. Evaluation of a simple model of ethanol drinking to intoxication in C57BL/6J mice. Physiol. Behav. 2005, 84:53-63.
78. Rhodes J.S., et al. Mouse inbred strain differences in ethanol drinking to intoxication. Genes Brain Behav 2007, 6:1-18.
79. Robitaille R., Charlton M.P. Presynaptic calcium signals and transmitter release are modulated by calcium-activated potassium channels. J. Neurosci. 1992, 12:297-305.
80. Sailer C.A., Kaufmann W.A., Kogler M., Chen L., Sausbier U., Ottersen O.P., Ruth P., Shipston M.J., Knaus H.G. Immunolocalization of BK channels in hippocampal pyramidal neurons. Eur. J. Neurosci. 2006, 24:442-454.
81. Sausbier U., Sausbier M., Sailer C.A., Arntz C., Knaus H.G., Neuhuber W., Ruth P. Ca2+-activated K+ channels of the BK-type in the mouse brain. Histochem. Cell Biol. 2006, 125:725-741.
82. Scholz A., Gruss M., Vogel W. Properties and functions of calcium-activated K+ channels in small neurones of rat dorsal root ganglion studied in a thin slice preparation. J. Physiol. 1998, 513:55-69.
83. Schreiber M., Salkoff L. A novel calcium-sensing domain in the BK channel. Biophys. J. 1997, 73:1355-1363.
84. Schubert R., Noack T., Serebryakov V.N. Protein kinase C reduces the KCa current of rat tail artery smooth muscle cells. Am. J. Physiol. 1999, 276:C648-658.
85. Schuckit M.A. Low level of response to alcohol as a predictor of future alcoholism. Am. J. Psychiatry 1994, 151:184-189.
86. Shah M.M., Haylett D.G. K+ currents generated by NMDA receptor activation in rat hippocampal pyramidal neurons. J. Neurophysiol. 2002, 87:2983-2989.
87. Shao L.R., Halvorsrud R., Borg-Graham L., Storm J.F. The role of BK-type Ca2+-dependent K+ channels in spike broadening during repetitive firing in rat hippocampal pyramidal cells. J. Physiol. 1999, 521(Pt 1):135-146.
88. Shen K.Z., Lagrutta A., Davies N.W., Standen N.B., Adelman J.P., North R.A. Tetraethylammonium block of Slowpoke calcium-activated potassium channels expressed in Xenopus oocytes: Evidence for tetrameric channel formation. Pflugers Arch. 1994, 426:440-445.
89. Stork O., Kojima N., Stork S., Kume N., Obata K. Resistance to alcohol withdrawal-induced behaviour in Fyn transgenic mice and its reversal by ifenprodil. Brain Res. Mol. Brain Res. 2002, 105:126-135.
90. Storm J.F. Potassium currents in hippocampal pyramidal cells. Prog. Brain Res. 1990, 83:161-187.
91. Swayze R.D., Braun A.P. A catalytically inactive mutant of type I cGMP-dependent protein kinase prevents enhancement of large conductance, calcium-sensitive K+ channels by sodium nitroprusside and cGMP. J. Biol. Chem. 2001, 276:19729-19737.
92. Thiele T.E., Willis B., Stadler J., Reynolds J.G., Bernstein I.L., McKnight G.S. High ethanol consumption and low sensitivity to ethanol-induced sedation in protein kinase A-mutant mice. J. Neurosci. 2000, 20:RC75.
93. Tian L., Coghill L.S., McClafferty H., MacDonald S.H., Antoni F.A., Ruth P., Knaus H.G., Shipston M.J. Distinct stoichiometry of BKCa channel tetramer phosphorylation specifies channel activation and inhibition by cAMP-dependent protein kinase. Proc. Natl. Acad. Sci. U S A. 2004, 101:11897-11902.
94. Tian L., Duncan R.R., Hammond M.S., Coghill L.S., Wen H., Rusinova R., Clark A.G., Levitan I.B., Shipston M.J. Alternative splicing switches potassium channel sensitivity to protein phosphorylation. J. Biol. Chem. 2001, 276:7717-7720.
95. Urakubo H., Honda M., Froemke R.C., Kuroda S. Requirement of an allosteric kinetics of NMDA receptors for spike timing-dependent plasticity. J. Neurosci. 2008, 28:3310-3323.
96. Wanner S.G., Koch R.O., Koschak A., Trieb M., Garcia M.L., Kaczorowski G.J., Knaus H.G. High-conductance calcium-activated potassium channels in rat brain: Pharmacology, distribution, and subunit composition. Biochemistry 1999, 38:5392-5400.
97. Weiger T.M., Holmqvist M.H., Levitan I.B., Clark F.T., Sprague S., Huang W.J., Ge P., Wang C., Lawson D., Jurman M.E., Glucksmann M.A., Silos-Santiago I., DiStefano P.S., Curtis R. A novel nervous system beta subunit that downregulates human large conductance calcium-dependent potassium channels. J. Neurosci. 2000, 20:3563-3570.
98. White R.E., Lee A.B., Shcherbatko A.D., Lincoln T.M., Schonbrunn A., Armstrong D.L. Potassium channel stimulation by natriuretic peptides through cGMP-dependent dephosphorylation. Nature 1993, 361:263-266.
99. Widmer H., Lemos J.R., Treistman S.N. Ethanol reduces the duration of single evoked spikes by a selective inhibition of voltage-gated calcium currents in acutely dissociated supraoptic neurons of the rat. J. Neuroendocrinol. 1998, 10:399-406.
100. Woodward J.J., Ron D., Winder D., Roberto M. From blue states to up states: A regional view of NMDA-ethanol interactions. Alcohol. Clin. Exp. Res. 2006, 30:359-367.
101. Wynne P.M., Puig S.I., Martin G.E., Treistman S.N. Compartmentalized beta subunit distribution determines characteristics and ethanol sensitivity of somatic, dendritic, and terminal large-conductance calcium-activated potassium channels in the rat central nervous system. J. Pharmacol. Exp. Ther. 2009, 329:978-986.
102. Yaka R., Phamluong K., Ron D. Scaffolding of Fyn kinase to the NMDA receptor determines brain region sensitivity to ethanol. J. Neurosci. 2003, 23:3623-3632.
103. Yuan C., O'Connell R.J., Wilson A., Pietrzykowski A.Z., Treistman S.N. Acute alcohol tolerance is intrinsic to the BKCa protein, but is modulated by the lipid environment. J. Biol. Chem. 2008, 283:5090-5098.
104. Zhang X.Y., Wang S., Yan Z., Wan Y., Wang W., Cui G.B., Du P., Ma K.J., Han W., Zhang Y.Q., Wei J.G. Molecular cloning, tissue distribution and bioinformatics analyses of the rabbit BK channel beta1 subunit gene. Mol. Biol. Rep. 2008, 35:649-655.