BK_Ca channels as physiological regulators: a focused review

References

• Marty A. Ca-dependent K channels with large unitary conductance in chromaffin cell membranes. Nature. 1981;291(5815):497–500.
   Web of Science ®Google Scholar
• Chen L, Jeffries O, Rowe IC, et al. Membrane trafficking of large conductance calcium-activated potassium channels is regulated by alternative splicing of a transplantable, acidic trafficking motif in the RCK1-RCK2 linker. J Biol Chem. 2010;285(30):23265–23275.
   Web of Science ®Google Scholar
• Kim EY, Ridgway LD, Zou S, Chiu YH, Dryer SE. Alternatively spliced C-terminal domains regulate the surface expression of large conductance calcium-activated potassium channels. Neuroscience. 2007;146(4):1652–1661.
   Web of Science ®Google Scholar
• Ma D, Nakata T, Zhang G, Hoshi T, Li M, Shikano S. Differential trafficking of carboxyl isoforms of Ca2+-gated (Slo1) potassium channels. FEBS Lett. 2007;581(5):1000–1008.
   Web of Science ®Google Scholar
• Zarei MM, Eghbali M, Alioua A, et al. An endoplasmic reticulum trafficking signal prevents surface expression of a voltage- and Ca2+-activated K+ channel splice variant. Proc Natl Acad Sci U S A. 2004;101(27):10072–10077.
   Web of Science ®Google Scholar
• Zarei MM, Zhu N, Alioua A, Eghbali M, Stefani E, Toro L. A novel MaxiK splice variant exhibits dominant-negative properties for surface expression. J Biol Chem. 2001;276(19):16232–16239.
   Web of Science ®Google Scholar
• Singh H, Lu R, Bopassa JC, Meredith AL, Stefani E, Toro L. MitoBK(Ca) is encoded by the Kcnma1 gene, and a splicing sequence defines its mitochondrial location. Proc Natl Acad Sci U S A. 2013;110(26):10836–10841.
   Web of Science ®Google Scholar
• Faber ES, Sah P. Calcium-activated potassium channels: multiple contributions to neuronal function. Neuroscientist. 2003;9(3):181–194.
   Web of Science ®Google Scholar
• Lancaster B, Nicoll RA. Properties of two calcium-activated hyperpolarizations in rat hippocampal neurones. J Physiol. 1987;389:187–203.
   PubMed Web of Science ®Google Scholar
• Shao LR, Halvorsrud R, Borg-Graham L, Storm JF. 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.
   Google Scholar
• Hu H, Shao LR, Chavoshy S, et al. Presynaptic Ca2+-activated K+ channels in glutamatergic hippocampal terminals and their role in spike repolarization and regulation of transmitter release. J Neurosci. 2001;21(24):9585–9597.
   Web of Science ®Google Scholar
• Gu N, Vervaeke K, Storm JF. BK potassium channels facilitate high-frequency firing and cause early spike frequency adaptation in rat CA1 hippocampal pyramidal cells. J Physiol. 2007;580(Pt.3):859–882.
   Web of Science ®Google Scholar
• Filosa JA, Bonev AD, Straub SV, et al. Local potassium signaling couples neuronal activity to vasodilation in the brain. Nat Neurosci. 2006;9(11):1397–1403.
   PubMed Web of Science ®Google Scholar
• Hill MA, Yang Y, Ella SR, Davis MJ, Braun AP. Large conductance, Ca2+-activated K+ channels (BKCa) and arteriolar myogenic signaling. FEBS Lett. 2010;584(10):2033–2042.
   PubMed Web of Science ®Google Scholar
• Kim N, Chung J, Kim E, Han J. Changes in the Ca2+-activated K+ channels of the coronary artery during left ventricular hypertrophy. Circ Res. 2003;93(6):541–547.
   Web of Science ®Google Scholar
• Wu SN, Ho LL, Li HF, Chiang HT. Regulation of Ca(2+)-activated K+ currents by ciglitazone in rat pituitary GH3 cells. J Investig Med. 2000;48(4):259–269.
   Web of Science ®Google Scholar
• Matzkin ME, Lauf S, Spinnler K, et al. The Ca2+-activated, large conductance K+-channel (BKCa) is a player in the LH/hCG signaling cascade in testicular Leydig cells. Mol Cell Endocrinol. 2013;367(1–2):41–49.
   Web of Science ®Google Scholar
• Pluznick JL, Wei P, Carmines PK, Sansom SC. Renal fluid and electrolyte handling in BKCa-beta1-/- mice. Am J Physiol Renal Physiol. 2003;284(6):F1274–F1279.
   Web of Science ®Google Scholar
• Mantegazza M, Curia G, Biagini G, Ragsdale DS, Avoli M. Voltage-gated sodium channels as therapeutic targets in epilepsy and other neurological disorders. Lancet Neurol. 2010;9(4):413–424.
   PubMed Web of Science ®Google Scholar
• Vetri F, Xu H, Paisansathan C, Pelligrino DA. Impairment of neurovascular coupling in type 1 diabetes mellitus in rats is linked to PKC modulation of BK(Ca) and Kir channels. Am J Physiol Heart Circ Physiol. 2012;302(6):H1274–H1284.
   Web of Science ®Google Scholar
• Wilcock DM, Vitek MP, Colton CA. Vascular amyloid alters astrocytic water and potassium channels in mouse models and humans with Alzheimer’s disease. Neuroscience. 2009;159(3):1055–1069.
   PubMed Web of Science ®Google Scholar
• Koide M, Bonev AD, Nelson MT, Wellman GC. Inversion of neurovascular coupling by subarachnoid blood depends on large-conductance Ca2+-activated K+ (BK) channels. Proc Natl Acad Sci U S A. 2012;109(21):E1387–E1395.
   Web of Science ®Google Scholar
• Lehmann-Horn F, Jurkat-Rott K. Voltage-gated ion channels and hereditary disease. Physiol Rev. 1999;79(4):1317–1372.
   PubMed Web of Science ®Google Scholar
• Cheney JA, Weisser JD, Bareyre FM, et al. The maxi-K channel opener BMS-204352 attenuates regional cerebral edema and neurologic motor impairment after experimental brain injury. J Cereb Blood Flow Metab. 2001;21(4):396–403.
   PubMed Web of Science ®Google Scholar
• Yang Y, Li PY, Cheng J, et al. Function of BKCa channels is reduced in human vascular smooth muscle cells from Han Chinese patients with hypertension. Hypertension. 2013;61(2):519–525.
   Web of Science ®Google Scholar
• Lawson K. Potassium channel openers as potential therapeutic weapons in ion channel disease. Kidney Int. 2000;57(3):838–845.
   Web of Science ®Google Scholar
• Aydin M, Wang HZ, Zhang X, et al. Large-conductance calcium-activated potassium channel activity, as determined by whole-cell patch clamp recording, is decreased in urinary bladder smooth muscle cells from male rats with partial urethral obstruction. BJU Int. 2012;110(8 Pt B):E402–E408.
   Google Scholar
• Li L, Jiang C, Song B, Yan J, Pan J. Altered expression of calcium-activated K and Cl channels in detrusor overactivity of rats with partial bladder outlet obstruction. BJU Int. 2008;101(12):1588–1594.
   Web of Science ®Google Scholar
• Rüttiger L, Sausbier M, Zimmermann U, et al. Deletion of the Ca2+-activated potassium (BK) alpha-subunit but not the BKbeta1-subunit leads to progressive hearing loss. Proc Natl Acad Sci U S A. 2004;101(35):12922–12927.
   Web of Science ®Google Scholar
• Knaus HG, Eberhart A, Glossmann H, Munujos P, Kaczorowski GJ, Garcia ML. Pharmacology and structure of high conductance calcium-activated potassium channels. Cell Signal. 1994;6(8):861–870.
   Web of Science ®Google Scholar
• Tanaka Y, Meera P, Song M, Knaus HG, Toro L. Molecular constituents of maxi KCa channels in human coronary smooth muscle: predominant alpha + beta subunit complexes. J Physiol. 1997;502(Pt 3):545–557.
   Web of Science ®Google Scholar
• Ma Z, Lou XJ, Horrigan FT. Role of charged residues in the S1–S4 voltage sensor of BK channels. J Gen Physiol. 2006;127(3):309–328.
   Web of Science ®Google Scholar
• McManus OB, Helms LM, Pallanck L, Ganetzky B, Swanson R, Leonard RJ. Functional role of the beta subunit of high conductance calcium-activated potassium channels. Neuron. 1995;14(3):645–650.
   PubMed Web of Science ®Google Scholar
• Bao L, Cox DH. Gating and ionic currents reveal how the BKCa channel’s Ca2+ sensitivity is enhanced by its beta1 subunit. J Gen Physiol. 2005;126(4):393–412.
   Web of Science ®Google Scholar
• Brenner R, Peréz GJ, Bonev AD, et al. Vasoregulation by the beta1 subunit of the calcium-activated potassium channel. Nature. 2000;407(6806):870–876.
   PubMed Web of Science ®Google Scholar
• Sweet TB, Cox DH. Measurements of the BKCa channel’s high-affinity Ca2+ binding constants: effects of membrane voltage. J Gen Physiol. 2008;132(5):491–505.
   Web of Science ®Google Scholar
• Toro B, Cox N, Wilson RJ, et al. KCNMB1 regulates surface expression of a voltage and Ca2+-activated K+ channel via endocytic trafficking signals. Neuroscience. 2006;142(3):661–669.
   Web of Science ®Google Scholar
• Zarei MM, Song M, Wilson RJ, et al. Endocytic trafficking signals in KCNMB2 regulate surface expression of a large conductance voltage and Ca(2+)-activated K+ channel. Neuroscience. 2007;147(1):80–89.
   PubMed Web of Science ®Google Scholar
• Wang YW, Ding JP, Xia XM, Lingle CJ. Consequences of the stoichiometry of Slo1 alpha and auxiliary beta subunits on functional properties of large-conductance Ca2+-activated K+ channels. J Neurosci. 2002;22(5):1550–1561.
   PubMed Web of Science ®Google Scholar
• McCarron JG, Chalmers S, Bradley KN, MacMillan D, Muir TC. Ca2+ microdomains in smooth muscle. Cell Calcium. 2006;40(5–6):461–493.
   Web of Science ®Google Scholar
• Wang XL, Ye D, Peterson TE, et al. Caveolae targeting and regulation of large conductance Ca(2+)-activated K+ channels in vascular endothelial cells. J Biol Chem. 2005;280(12):11656–11664.
   Web of Science ®Google Scholar
• Alioua A, Mahajan A, Nishimaru K, Zarei MM, Stefani E, Toro L. Coupling of c-Src to large conductance voltage- and Ca2+-activated K+ channels as a new mechanism of agonist-induced vasoconstriction. Proc Natl Acad Sci U S A. 2002;99(22):14560–14565.
   Web of Science ®Google Scholar
• Sundivakkam PC, Kwiatek AM, Sharma TT, Minshall RD, Malik AB, Tiruppathi C. Caveolin-1 scaffold domain interacts with TRPC1 and IP3R3 to regulate Ca2+ store release-induced Ca2+ entry in endothelial cells. Am J Physiol Cell Physiol. 2009;296(3):C403–C413.
   PubMed Web of Science ®Google Scholar
• Minami K, Fukuzawa K, Nakaya Y. Protein kinase C inhibits the Ca(2+)-activated K+ channel of cultured porcine coronary artery smooth muscle cells. Biochem Biophys Res Commun. 1993;190(1):263–269.
   Web of Science ®Google Scholar
• Brainard AM, Miller AJ, Martens JR, England SK. Maxi-K channels localize to caveolae in human myometrium: a role for an actin-channel-caveolin complex in the regulation of myometrial smooth muscle K+ current. Am J Physiol Cell Physiol. 2005;289(1):C49–C57.
   Web of Science ®Google Scholar
• Earley S, Heppner TJ, Nelson MT, Brayden JE. TRPV4 forms a novel Ca2+ signaling complex with ryanodine receptors and BKCa channels. Circ Res. 2005;97(12):1270–1279.
   PubMed Web of Science ®Google Scholar
• Kwan HY, Shen B, Ma X, et al. TRPC1 associates with BK(Ca) channel to form a signal complex in vascular smooth muscle cells. Circ Res. 2009;104(5):670–678.
   Web of Science ®Google Scholar
• Brayden JE, Nelson MT. Regulation of arterial tone by activation of calcium-dependent potassium channels. Science. 1992;256(5056):532–525.
   PubMed Web of Science ®Google Scholar
• Plüger S, Faulhaber J, Fürstenau M, et al. Mice with disrupted BK channel beta1 subunit gene feature abnormal Ca(2+) spark/STOC coupling and elevated blood pressure. Circ Res. 2000;87(11):E53–E60.
   Web of Science ®Google Scholar
• Dimitropoulou C, Han G, Miller AW, et al. Potassium (BK(Ca)) currents are reduced in microvascular smooth muscle cells from insulin-resistant rats. Am J Physiol Heart Circ Physiol. 2002;282(3):H908–H917.
   Web of Science ®Google Scholar
• Zhao Q, Wang L, Yang W, et al. Interactions among genetic variants from contractile pathway of vascular smooth muscle cell in essential hypertension susceptibility of Chinese Han population. Pharmacogenet Genomics. 2008;18(6):459–466.
   Web of Science ®Google Scholar
• Howitt L, Sandow SL, Grayson TH, Ellis ZE, Morris MJ, Murphy TV. Differential effects of diet-induced obesity on BKCa {beta}1-subunit expression and function in rat skeletal muscle arterioles and small cerebral arteries. Am J Physiol Heart Circ Physiol. 2011;301(1):H29–H40.
   PubMed Web of Science ®Google Scholar
• Hald BO, Jacobsen JC, Braunstein TH, et al. BKCa and KV channels limit conducted vasomotor responses in rat mesenteric terminal arterioles. Pflugers Arch. 2012;463(2):279–295.
   PubMed Web of Science ®Google Scholar
• Nishimaru K, Eghbali M, Lu R, Marijic J, Stefani E, Toro L. Functional and molecular evidence of MaxiK channel beta1 subunit decrease with coronary artery ageing in the rat. J Physiol. 2004;559(Pt 3):849–862.
   Web of Science ®Google Scholar
• Faehling M, Koch ED, Raithel J, Trischler G, Waltenberger J. Vascular endothelial growth factor-A activates Ca2+-activated K+ channels in human endothelial cells in culture. Int J Biochem Cell Biol. 2001;33(4):337–346.
   Web of Science ®Google Scholar
• Kuhlmann CR, Wu Y, Li F, et al. bFGF activates endothelial Ca2+-activated K+ channels involving G-proteins and tyrosine kinases. Vascul Pharmacol. 2004;41(6):181–186.
   Web of Science ®Google Scholar
• Wrzosek A. Endothelium as target for large-conductance calcium-activated potassium channel openers. Acta Biochim Pol. 2009;56(3):393–404.
   Web of Science ®Google Scholar
• Wrzosek A, Łukasiak A, Gwóźdź P, et al. Large-conductance K+ channel opener CGS7184 as a regulator of endothelial cell function. Eur J Pharmacol. 2009;602(1):105–111.
   Web of Science ®Google Scholar
• Simon A, Harrington EO, Liu GX, Koren G, Choudhary G. Mechanism of C-type natriuretic peptide-induced endothelial cell hyperpolarization. Am J Physiol Lung Cell Mol Physiol. 2009;296(2):L248–L256.
   Web of Science ®Google Scholar
• Ledoux J, Werner ME, Brayden JE, Nelson MT. Calcium-activated potassium channels and the regulation of vascular tone. Physiology (Bethesda). 2006;21:69–78.
   PubMed Web of Science ®Google Scholar
• Félétou M. Calcium-activated potassium channels and endothelial dysfunction: therapeutic options? Br J Pharmacol. 2009;156(4):545–562.
   PubMed Web of Science ®Google Scholar
• Félétou M, Vanhoutte PM. Endothelial dysfunction: a multifaceted disorder (The Wiggers Award Lecture). Am J Physiol Heart Circ Physiol. 2006;291(3):H985–H1002.
   PubMed Web of Science ®Google Scholar
• Félétou M, Vanhoutte PM. Endothelium-derived hyperpolarizing factor: where are we now? Arterioscler Thromb Vasc Biol. 2006;26(6):1215–1225.
   Web of Science ®Google Scholar
• Hughes JM, Riddle MA, Paffett ML, Gonzalez Bosc LV, Walker BR. Novel role of endothelial BKCa channels in altered vasoreactivity following hypoxia. Am J Physiol Heart Circ Physiol. 2010;299(5):H1439–H1450.
   Web of Science ®Google Scholar
• Riddle MA, Hughes JM, Walker BR. Role of caveolin-1 in endothelial BKCa channel regulation of vasoreactivity. Am J Physiol Cell Physiol. 2011;301(6):C1404–C1414.
   Web of Science ®Google Scholar
• Node K, Kitakaze M, Kosaka H, Minamino T, Hori M. Bradykinin mediation of Ca(2+)-activated K+ channels regulates coronary blood flow in ischemic myocardium. Circulation. 1997;95(6):1560–1567.
   Web of Science ®Google Scholar
• Node K, Kitakaze M, Kosaka H, et al. Roles of NO and Ca2+-activated K+ channels in coronary vasodilation induced by 17beta-estradiol in ischemic heart failure. FASEB J. 1997;11(10):793–799.
   Web of Science ®Google Scholar
• Node K, Kitakaze M, Kosaka H, Minamino T, Funaya H, Hori M. Amelioration of ischemia- and reperfusion-induced myocardial injury by 17beta-estradiol: role of nitric oxide and calcium-activated potassium channels. Circulation. 1997;96(6):1953–1963.
   Web of Science ®Google Scholar
• Miura H, Liu Y, Gutterman DD. Human coronary arteriolar dilation to bradykinin depends on membrane hyperpolarization: contribution of nitric oxide and Ca2+-activated K+ channels. Circulation. 1999;99(24):3132–3138.
   Web of Science ®Google Scholar
• Bychkov R, Gollasch M, Steinke T, Ried C, Luft FC, Haller H. Calcium-activated potassium channels and nitrate-induced vasodilation in human coronary arteries. J Pharmacol Exp Ther. 1998;285(1):293–298.
   Web of Science ®Google Scholar
• Khan SA, Higdon NR, Meisheri KD. Coronary vasorelaxation by nitroglycerin: involvement of plasmalemmal calcium-activated K+ channels and intracellular Ca++ stores. J Pharmacol Exp Ther. 1998;284(3):838–846.
   Web of Science ®Google Scholar
• Price JM, Hellermann A. Inhibition of cGMP mediated relaxation in small rat coronary arteries by block of CA++ activated K+ channels. Life Sci. 1997;61(12):1185–1192.
   Web of Science ®Google Scholar
• Pataricza J, Toth GK, Penke B, Hohn J, Papp JG. Effect of selective inhibition of potassium channels on vasorelaxing response to cromakalim, nitroglycerin and nitric oxide of canine coronary arteries. J Pharm Pharmacol. 1995;47(11):921–925.
   Web of Science ®Google Scholar
• Weston AH, Félétou M, Vanhoutte PM, Falck JR, Campbell WB, Edwards G. Bradykinin-induced, endothelium-dependent responses in porcine coronary arteries: involvement of potassium channel activation and epoxyeicosatrienoic acids. Br J Pharmacol. 2005;145(6):775–784.
   Web of Science ®Google Scholar
• Wellman GC, Brayden JE, Nelson MT. A proposed mechanism for the cardioprotective effect of oestrogen in women: enhanced endothelial nitric oxide release decreases coronary artery reactivity. Clin Exp Pharmacol Physiol. 1996;23(3):260–266.
   Web of Science ®Google Scholar
• Li PL, Zou AP, Campbell WB. Regulation of potassium channels in coronary arterial smooth muscle by endothelium-derived vasodilators. Hypertension. 1997;29(1 Pt 2):262–267.
   Web of Science ®Google Scholar
• Minami K, Hirata Y, Tokumura A, Nakaya Y, Fukuzawa K. Protein kinase C-independent inhibition of the Ca(2+)-activated K+ channel by angiotensin II and endothelin-1. Biochem Pharmacol. 1995;49(8):1051–1056.
   Web of Science ®Google Scholar
• Toro L, Amador M, Stefani E. ANG II inhibits calcium-activated potassium channels from coronary smooth muscle in lipid bilayers. Am J Physiol. 1990;258(3 Pt 2):H912–H915.
   Google Scholar
• Hu SL, Kim HS, Jeng AY. Dual action of endothelin-1 on the Ca2(+)-activated K+ channel in smooth muscle cells of porcine coronary artery. Eur J Pharmacol. 1991;194(1):31–36.
   Web of Science ®Google Scholar
• Scornik FS, Toro L. U46619, a thromboxane A2 agonist, inhibits KCa channel activity from pig coronary artery. Am J Physiol. 1992;262(3 Pt 1):C708–C713.
   Google Scholar
• Borbouse L, Dick GM, Payne GA, et al. Metabolic syndrome reduces the contribution of K+ channels to ischemic coronary vasodilation. Am J Physiol Heart Circ Physiol. 2010;298(4):H1182–H1189.
   Web of Science ®Google Scholar
• Merkus D, Sorop O, Houweling B, Hoogteijling BA, Duncker DJ. KCa+ channels contribute to exercise-induced coronary vasodilation in swine. Am J Physiol Heart Circ Physiol. 2006;291(5):H2090–H2097.
   Web of Science ®Google Scholar
• Troncoso Brindeiro CM, Fallet RW, Lane PH, Carmines PK. Potassium channel contributions to afferent arteriolar tone in normal and diabetic rat kidney. Am J Physiol Renal Physiol. 2008;295(1):F171–F178.
   Web of Science ®Google Scholar
• Liu Y, Gutterman DD. The coronary circulation in diabetes: influence of reactive oxygen species on K+ channel-mediated vasodilation. Vascul Pharmacol. 2002;38(1):43–49.
   Web of Science ®Google Scholar
• Wiecha J, Schläger B, Voisard R, Hannekum A, Mattfeldt T, Hombach V. Ca(2+)-activated K+ channels in human smooth muscle cells of coronary atherosclerotic plaques and coronary media segments. Basic Res Cardiol. 1997;92(4):233–239.
   Web of Science ®Google Scholar
• Knaus HG, Schwarzer C, Koch RO, et al. Distribution of high-conductance Ca(2+)-activated K+ channels in rat brain: targeting to axons and nerve terminals. J Neurosci. 1996;16(3):955–963.
   Web of Science ®Google Scholar
• Womack MD, Chevez C, Khodakhah K. Calcium-activated potassium channels are selectively coupled to P/Q-type calcium channels in cerebellar Purkinje neurons. J Neurosci. 2004;24(40):8818–8822.
   Web of Science ®Google Scholar
• Womack MD, Khodakhah K. Dendritic control of spontaneous bursting in cerebellar Purkinje cells. J Neurosci. 2004;24(14):3511–3521.
   Web of Science ®Google Scholar
• Bond CT, Herson PS, Strassmaier T, et al. Small conductance Ca2+-activated K+ channel knock-out mice reveal the identity of calcium-dependent afterhyperpolarization currents. J Neurosci. 2004;24(23):5301–5306.
   Web of Science ®Google Scholar
• Isaacson JS, Murphy GJ. Glutamate-mediated extrasynaptic inhibition: direct coupling of NMDA receptors to Ca(2+)-activated K+ channels. Neuron. 2001;31(6):1027–1034.
   Web of Science ®Google Scholar
• Chavis P, Ango F, Michel JM, Bockaert J, Fagni L. Modulation of big K+ channel activity by ryanodine receptors and L-type Ca2+ channels in neurons. Eur J Neurosci. 1998;10(7):2322–2327.
   Web of Science ®Google Scholar
• Sausbier M, Hu H, Arntz C, et al. Cerebellar ataxia and Purkinje cell dysfunction caused by Ca2+-activated K+ channel deficiency. Proc Natl Acad Sci U S A. 2004;101(25):9474–9478.
   PubMed Web of Science ®Google Scholar
• Prakriya M, Lingle CJ. Activation of BK channels in rat chromaffin cells requires summation of Ca(2+) influx from multiple Ca(2+) channels. J Neurophysiol. 2000;84(3):1123–1135.
   Web of Science ®Google Scholar
• Prakriya M, Solaro CR, Lingle CJ. [Ca2+]i elevations detected by BK channels during Ca2+ influx and muscarine-mediated release of Ca2+ from intracellular stores in rat chromaffin cells. J Neurosci. 1996;16(14):4344–4359.
   Web of Science ®Google Scholar
• Eunson LH, Rea R, Zuberi SM, et al. Clinical, genetic, and expression studies of mutations in the potassium channel gene KCNA1 reveal new phenotypic variability. Ann Neurol. 2000;48(4):647–656.
   Web of Science ®Google Scholar
• Du W, Bautista JF, Yang H, et al. Calcium-sensitive potassium channelopathy in human epilepsy and paroxysmal movement disorder. Nat Genet. 2005;37(7):733–738.
   PubMed Web of Science ®Google Scholar
• Turnbull J, Lohi H, Kearney JA, et al. Sacred disease secrets revealed: the genetics of human epilepsy. Hum Mol Genet. 2005;14 Spec No. 2: 2491–2500.
   Google Scholar
• Wallner M, Meera P, Toro L. Molecular basis of fast inactivation in voltage and Ca2+-activated K+ channels: a transmembrane beta-subunit homolog. Proc Natl Acad Sci U S A. 1999;96(7):4137–4142.
   PubMed Web of Science ®Google Scholar
• Wang B, Rothberg BS, Brenner R. Mechanism of increased BK channel activation from a channel mutation that causes epilepsy. J Gen Physiol. 2009;133(3):283–294.
   PubMed Web of Science ®Google Scholar
• Douglas RM, Lai JC, Bian S, Cummins L, Moczydlowski E, Haddad GG. The calcium-sensitive large-conductance potassium channel (BK/MAXI K) is present in the inner mitochondrial membrane of rat brain. Neuroscience. 2006;139(4):1249–1261.
   Web of Science ®Google Scholar
• Cavalleri GL, Weale ME, Shianna KV, et al. Multicentre search for genetic susceptibility loci in sporadic epilepsy syndrome and seizure types: a case-control study. Lancet Neurol. 2007;6(11):970–980.
   Web of Science ®Google Scholar
• Siemen D, Loupatatzis C, Borecky J, Gulbins E, Lang F. Ca2+-activated K channel of the BK-type in the inner mitochondrial membrane of a human glioma cell line. Biochem Biophys Res Commun. 1999;257(2):549–554.
   Web of Science ®Google Scholar
• Xu W, Liu Y, Wang S, et al. Cytoprotective role of Ca2+-activated K+ channels in the cardiac inner mitochondrial membrane. Science. 2002;298(5595):1029–1033.
   Web of Science ®Google Scholar
• Piwonska M, Wilczek E, Szewczyk A, Wilczynski GM. Differential distribution of Ca2+-activated potassium channel beta4 subunit in rat brain: immunolocalization in neuronal mitochondria. Neuroscience. 2008;153(2):446–460.
   Web of Science ®Google Scholar
• Skalska J, Bednarczyk P, Piwońska M, et al. Calcium ions regulate K+ uptake into brain mitochondria: the evidence for a novel potassium channel. Int J Mol Sci. 2009;10(3):1104–1120.
   Web of Science ®Google Scholar
• Paisansathan C, Xu H, Vetri F, Hernandez M, Pelligrino DA. Interactions between adenosine and K+ channel-related pathways in the coupling of somatosensory activation and pial arteriolar dilation. Am J Physiol Heart Circ Physiol. 2010;299(6):H2009–H2017.
   Web of Science ®Google Scholar
• Girouard H, Bonev AD, Hannah RM, Meredith A, Aldrich RW, Nelson MT. Astrocytic endfoot Ca2+ and BK channels determine both arteriolar dilation and constriction. Proc Natl Acad Sci U S A. 2010;107(8):3811–3816.
   PubMed Web of Science ®Google Scholar
• Wang Y, Zhang HT, Su XL, et al. Experimental diabetes mellitus down-regulates large-conductance Ca2+-activated K+ channels in cerebral artery smooth muscle and alters functional conductance. Curr Neurovasc Res. 2010;7(2):75–84.
   Web of Science ®Google Scholar
• Pelucchi B, Grimaldi A, Moriondo A. Vertebrate rod photoreceptors express both BK and IK calcium-activated potassium channels, but only BK channels are involved in receptor potential regulation. J Neurosci Res. 2008;86(1):194–201.
   Web of Science ®Google Scholar
• Xu JW, Slaughter MM. Large-conductance calcium-activated potassium channels facilitate transmitter release in salamander rod synapse. J Neurosci. 2005;25(33):7660–7668.
   Web of Science ®Google Scholar
• Yagi T, Macleish PR. Ionic conductances of monkey solitary cone inner segments. J Neurophysiol. 1994;71(2):656–665.
   Web of Science ®Google Scholar
• Nemargut JP, Zhu J, Savoie BT, Wang GY. Differential effects of charybdotoxin on the activity of retinal ganglion cells in the dark- and light-adapted mouse retina. Vision Res. 2009;49(3):388–397.
   Web of Science ®Google Scholar
• Nelson MT, Cheng H, Rubart M, et al. Relaxation of arterial smooth muscle by calcium sparks. Science. 1995;270(5236):633–637.
   Web of Science ®Google Scholar
• McGahon MK, Dash DP, Arora A, et al. Diabetes downregulates large-conductance Ca2+-activated potassium beta 1 channel subunit in retinal arteriolar smooth muscle. Circ Res. 2007;100(5):703–711.
   Web of Science ®Google Scholar
• Mori A, Suzuki S, Sakamoto K, Nakahara T, Ishii K. BMS-191011, an opener of large-conductance Ca2+-activated potassium channels, dilates rat retinal arterioles in vivo. Biol Pharm Bull. 2011;34(1):150–152.
   PubMed Web of Science ®Google Scholar
• Jaggar JH, Porter VA, Lederer WJ, Nelson MT. Calcium sparks in smooth muscle. Am J Physiol Cell Physiol. 2000;278(2):C235–C256.
   PubMed Web of Science ®Google Scholar
• Jaggar JH, Nelson MT. Differential regulation of Ca(2+) sparks and Ca(2+) waves by UTP in rat cerebral artery smooth muscle cells. Am J Physiol Cell Physiol. 2000;279(5):C1528–C15239.
   Web of Science ®Google Scholar
• Herrera GM, Heppner TJ, Nelson MT. Regulation of urinary bladder smooth muscle contractions by ryanodine receptors and BK and SK channels. Am J Physiol Regul Integr Comp Physiol. 2000;279(1):R60–R68.
   Web of Science ®Google Scholar
• Fallet RW, Bast JP, Fujiwara K, Ishii N, Sansom SC, Carmines PK. Influence of Ca(2+)-activated K(+) channels on rat renal arteriolar responses to depolarizing agonists. Am J Physiol Renal Physiol. 2001;280(4):F583–F591.
   Web of Science ®Google Scholar
• Stockand JD, Sansom SC. Large Ca(2+)-activated K+ channels responsive to angiotensin II in cultured human mesangial cells. Am J Physiol. 1994;267(4 Pt 1):C1080–C1086.
   Google Scholar
• Stockand JD, Sansom SC. Glomerular mesangial cells: electrophysiology and regulation of contraction. Physiol Rev. 1998;78(3):723–744.
   Web of Science ®Google Scholar
• Guggino SE, Guggino WB, Green N, Sacktor B. Ca2+-activated K+ channels in cultured medullary thick ascending limb cells. Am J Physiol. 1987;252(2 Pt 1):C121–C127.
   Google Scholar
• Belfodil R, Barrière H, Rubera I, et al. CFTR-dependent and -independent swelling-activated K+ currents in primary cultures of mouse nephron. Am J Physiol Renal Physiol. 2003;284(4):F812–F828.
   Web of Science ®Google Scholar
• Stoner LC, Morley GE. Effect of basolateral or apical hyposmolarity on apical maxi K channels of everted rat collecting tubule. Am J Physiol. 1995;268(4 Pt 2):F569–F580.
   Google Scholar
• Rieg T, Vallon V, Sausbier M, et al. The role of the BK channel in potassium homeostasis and flow-induced renal potassium excretion. Kidney Int. 2007;72(5):566–573.
   Web of Science ®Google Scholar
• Pluznick JL, Wei P, Grimm PR, Sansom SC. BK-{beta}1 subunit: immunolocalization in the mammalian connecting tubule and its role in the kaliuretic response to volume expansion. Am J Physiol Renal Physiol. 2005;288(4):F846–F854.
   Web of Science ®Google Scholar
• Kudlacek PE, Pluznick JL, Ma R, Padanilam B, Sansom SC. Role of hbeta1 in activation of human mesangial BK channels by cGMP kinase. Am J Physiol Renal Physiol. 2003;285(2):F289–F294.
   Web of Science ®Google Scholar
• Bailey MA, Cantone A, Yan Q, et al. Maxi-K channels contribute to urinary potassium excretion in the ROMK-deficient mouse model of Type II Bartter’s syndrome and in adaptation to a high-K diet. Kidney Int. 2006;70(1):51–59.
   Web of Science ®Google Scholar
• Najjar F, Zhou H, Morimoto T, et al. Dietary K+ regulates apical membrane expression of maxi-K channels in rabbit cortical collecting duct. Am J Physiol Renal Physiol. 2005;289(4):F922–F932.
   Web of Science ®Google Scholar
• Wein AJ, Rackley RR. Overactive bladder: a better understanding of pathophysiology, diagnosis and management. J Urol. 2006;175(3 Pt 2):S5–S10.
   PubMed Web of Science ®Google Scholar
• Petkov GV, Nelson MT. Differential regulation of Ca2+-activated K+ channels by beta-adrenoceptors in guinea pig urinary bladder smooth muscle. Am J Physiol Cell Physiol. 2005;288(6):C1255–C1263.
   Web of Science ®Google Scholar
• Shruti S, Urban-Ciecko J, Fitzpatrick JA, Brenner R, Bruchez MP, Barth AL. The brain-specific Beta4 subunit downregulates BK channel cell surface expression. PLoS One. 2012;7(3):e33429.
   Web of Science ®Google Scholar
• Schubert R, Nelson MT. Protein kinases: tuners of the BKCa channel in smooth muscle. Trends Pharmacol Sci. 2001;22(10):505–512.
   PubMed Web of Science ®Google Scholar
• Shipston MJ. Ion channel regulation by protein palmitoylation. J Biol Chem. 2011;286(11):8709–8716.
   PubMed Web of Science ®Google Scholar
• Shipston MJ. Alternative splicing of potassium channels: a dynamic switch of cellular excitability. Trends Cell Biol. 2001;11(9):353–358.
   Web of Science ®Google Scholar
• Candia S, Garcia ML, Latorre R. Mode of action of iberiotoxin, a potent blocker of the large conductance Ca(2+)-activated K+ channel. Biophys J. 1992;63(2):583–590.
   Web of Science ®Google Scholar
• Behrens R, Nolting A, Reimann F, Schwarz M, Waldschütz 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(1):99–106.
   PubMed Web of Science ®Google Scholar
• Meera P, Wallner M, Toro L. A neuronal beta subunit (KCNMB4) makes the large conductance, voltage- and Ca2+-activated K+ channel resistant to charybdotoxin and iberiotoxin. Proc Natl Acad Sci U S A. 2000;97(10):5562–5567.
   PubMed Web of Science ®Google Scholar
• Hu H, Shao LR, Chavoshy S, et al. Presynaptic Ca2+-activated K+ channels in glutamatergic hippocampal terminals and their role in spike repolarization and regulation of transmitter release. J Neurosci. 2001;21(24):9585–9597.
   Web of Science ®Google Scholar
• Dalziel JE, Finch SC, Dunlop J. The fungal neurotoxin lolitrem B inhibits the function of human large conductance calcium-activated potassium channels. Toxicol Lett. 2005;155(3):421–426.
   Web of Science ®Google Scholar
• Imlach WL, Finch SC, Dunlop J, Meredith AL, Aldrich RW, Dalziel JE. The molecular mechanism of “ryegrass staggers,” a neurological disorder of K+ channels. J Pharmacol Exp Ther. 2008;327(3):657–664.
   Web of Science ®Google Scholar
• Imlach WL, Finch SC, Dunlop J, Dalziel JE. Structural determinants of lolitrems for inhibition of BK large conductance Ca2+-activated K+ channels. Eur J Pharmacol. 2009;605(1–3):36–45.
   Web of Science ®Google Scholar
• Miles CO, Munday SC, Wilkins AL, Ede RM, Towers NR. Large-scale isolation of lolitrem B and structure determination of lolitrem E. J Agric Food Chem. 1994;42:1488–1492.
   Web of Science ®Google Scholar
• Munday-Finch SC, Miles CO, Wilkins AL, Hawkes AD. Isolation and structure elucidation of lolitrem A, a tremorgenic mycotoxin from perennial ryegrass infected with Acremonium lolii. J Agric Food Chem. 1995;43:1283–1288.
   Web of Science ®Google Scholar
• Munday-Finch SC, Wilkins AL, Miles CO, Ede RM, Thomson RA. Structure elucidation of lolitrem F, a naturally occurring stereoisomer of the tremorgenic mycotoxin lolitrem B, isolated from Lolium perenne infected with Acremonium lolii. J Agric Food Chem. 1996;44:2782–2788.
   Web of Science ®Google Scholar