G Protein Modulation of Voltage-Gated Calcium Channels

Pharmacological Reviews

Volumn 55, Issue 4, 2003, Pages 607-627

  Dolphin, Annette C ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA 2A ADRENERGIC RECEPTOR; BARIUM ION; CALCIUM CHANNEL; CALCIUM CHANNEL L TYPE; CALCIUM CHANNEL N TYPE; CALCIUM ION; CLONIDINE; DIHYDROPYRIDINE DERIVATIVE; DOPAMINE 2 RECEPTOR STIMULATING AGENT; G PROTEIN COUPLED RECEPTOR; GLUTATHIONE TRANSFERASE; GUANINE NUCLEOTIDE BINDING PROTEIN; HYBRID PROTEIN; OMEGA AGATOXIN IVA; OMEGA CONOTOXIN GVIA; PERTUSSIS TOXIN; QUINPIROLE; RECEPTOR SUBTYPE; SNX 482; UNCLASSIFIED DRUG; VOLTAGE GATED CALCIUM CHANNEL;

ANIMAL CELL; CALCIUM CURRENT; NERVE CELL; NONHUMAN; OOCYTE; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; XENOPUS;

ANIMALS; CALCIUM CHANNELS; GTP-BINDING PROTEINS; HUMANS; MOLECULAR BIOLOGY;

EID: 0344197075     PISSN: 00316997     EISSN: None     Source Type: Journal    
DOI: 10.1124/pr.55.4.3     Document Type: Review

References (194)

1. Baertschi AJ, Audigier Y, Lledo P-M, Israel J-M, Bockaert J, and Vincent J-D (1992) Dialysis of lactotropes with antisense oligonucleotides assigns guanine nucleotide binding protein subtypes to their channel effectors. Mol Endocrinol 6:2257-2265.
2. Barclay J, Balaguero N, Mione M, Ackerman SL, Letts VA, Brodbeck J, Canti C, Meir A, Page KM, Kusumi K, et al. (2001) Ducky mouse phenotype of epilepsy and ataxia is associated with mutations in the Cacna2d2 gene and decreased calcium channel current in cerebellar Purkinje cells. J Neurosci 21:6095-6104.
3. Bean BP (1989) Neurotransmitter inhibition of neuronal calcium currents by changes in channel voltage-dependence. Nature (Lond) 340:153-155.
4. v1.3) voltage-dependent calcium currents. J Neurophysiol 85:816-827.
5. Berrow NS, Brice NL, Tedder I, Page K, and Dolphin AC (1997) Properties of cloned rat α1A calcium channels transiently expressed in the COS-7 cell line. Eur J Neurosci 9:739-748.
6. Berrow NS, Campbell V, Fitzgerald EG, Brickley K, and Dolphin AC (1995) Antisense depletion of B-subunits modulates the biophysical and pharmacological properties of neuronal calcium channels. J Physiol (Lond) 482:481-491.
7. v2.2 calcium channels: probed by the use of receptor-Galpha tandems. Mol Pharmacol 63:832-843.
8. Bichet D, Cornet V, Geib S, Carlier E, Volsen S, Hoshi T, Mori Y, and De Waard M (2000) The I-II loop of the Ca2+ channel alpha(1) subunit contains an endoplasmic reticulum retention signal antagonized by the beta subunit. Neuron 25:177-190.
9. Birnbaumer L, Qin N, Olcese R, Tareilus E, Platano D, Costantin J, and Stefani E (1998) Structures and functions of calcium channel β subunits. J Bioenerg Biomembr 30:357-375.
10. Black JL and Lennon VA (1999) Identification and cloning of putative human neuronal voltage-gated calcium channel gamma-2 and gamma-3 subunits: neurologic implications. Mayo Clin Proc 74:357-361.
11. Bogdanov Y, Brice NL, Canti C, Page KM, Li M, Volsen SG, and Dolphin AC (2000) Acidic motif responsible for plasma membrane association of the voltage-dependent calcium channel B1b subunit. Eur J Neurosci 12:894-902.
12. Boland LM and Bean BP (1993) Modulation of N-type calcium channels in bullfrog sympathetic neurons by luteinizing hormone-releasing hormone: kinetics and voltage dependence. J Neurosci 13:516-533.
13. Bourinet E, Soong TW, Stea A, and Snutch TP (1996) Determinants of the G protein-dependent opioid modulation of neuronal calcium channels. Proc Natl Acad Sci USA 93:1486-1491.
14. Brice NL, Berrow NS, Campbell V, Page KM, Brickley K, Tedder I, and Dolphin AC (1997) Importance of the different β subunits in the membrane expression of the α1A and α2 calcium channel subunits: studies using a depolarisation-sensitive α1A antibody. Eur J Neurosci 9:749-759.
15. Brody DL and Yue DT (2000) Relief of G-protein inhibition of calcium channels and short-term synaptic facilitation in cultured hippocampal neurons. J Neurosci 20:889-898.
16. o in rat frontal cortex. FEBS Lett 370:135-140.
17. o: antisense oligonucleotide studies. J Physiol (Lond) 470:1-11.
18. o with calcium channels by the calcium channel B-subunit in rat neurones. J Physiol (Lond) 485:365-372.
19. Canti C, Bogdanov Y, and Dolphin AC (2000) Interaction between G proteins and accessory β subunits in the regulation of α1B calcium channels in Xenopus oocytes. J Physiol (Lond) 527:419-432.
20. Canti C, Davies A, Berrow NS, Butcher AJ, Page KM, and Dolphin AC (2001) Evidence for two concentration-dependent processes for β subunit effects on α1B calcium channels. Biophys J 81:1439-1451.
21. v2.2 currents triggered by D2 dopamine receptor activation. Neuropharmacology, 45:814-827.
22. Canti C, Page KM, Stephens GJ, and Dolphin AC (1999) Identification of residues in the N-terminus of α1B critical for inhibition of the voltage-dependent calcium channel by Gβγ. J Neurosci 19:6855-6864.
23. Carbone E and Lux HD (1984) A low voltage-activated, fully inactivating Ca channel in vertebrate sensory neurones. Nature (Lond) 310:501-502.
24. Castellano A, Wei X, Birnbaumer L, and Perez-Reyes E (1993a) Cloning and expression of a neuronal calcium channel β subunit. J Biol Chem 268:12359-12366.
25. Castellano A, Wei X, Birnbaumer L, and Perez-Reyes E (1993b) Cloning and expression of a third calcium channel β subunit. J Biol Chem 268:3450-3455.
26. 2+ channels. Annu Rev Cell Dev Biol 16:521-555.
27. Cens T, Restituito S, Galas S, and Charnet P (1999) Voltage and calcium use the same molecular determinants to inactivate calcium channels. J Biol Chem 274:5483-5490.
28. Chang FC and Hosey MM (1988) Dihydropyridine and phenylalkylamine receptors associated with cardiac and skeletal muscle calcium channels are structurally different. J Biol Chem 263:18929-18937.
29. Chen J, DeVivo M, Dingus J, Harry A, Li J, Sui J, Carty DJ, Blank JL, Exton JH, Stoffel RH, et al. (1995) A region of adenylyl cyclase 2 critical for regulation by G protein Bgamma subunits. Science (Wash DC) 268:1166-1169.
30. 2a subunit and effects on channel function. J Biol Chem 271:26465-26469.
31. Chien AJ and Hosey MM (1998) Post-translational modifications of β subunits of voltage-dependent calcium channels. J Bioenerg Biomembr 30:377-386.
32. 2+ channels. J Biol Chem 270:30036-30044.
33. Clapham DE and Neer EJ (1993) New roles for G-protein β gamma dimers in transmembrane signalling. Nature (Lond) 365:403-406.
34. Cooper CB, Arnot MI, Feng ZP, Jarvis SE, Hamid J, and Zamponi GW (2000) Cross-talk between G-protein and protein kinase C modulation of N-type calcium channels is dependent on the G-protein β subunit isoform. J Biol Chem 275:40777-40781.
35. 0 heterotrimer couples somatostatin receptors to voltage-gated calcium channels in RINm5F cells. FEBS Lett 380:137-141.
36. Delcour AH, Lipscombe D, and Tsien RW (1993) Multiple modes of N-type calcium channel activity distinguished by differences in gating kinetics. J Neurosci 13:181-194.
37. Delcour AH and Tsien RW (1993) Altered prevalence of gating modes in neurotransmitter inhibition of N-type calcium channels. Science (Wash DC) 259:980-984.
38. Delmas P, Abogadie FC, Buckley NJ, and Brown DA (2000) Calcium channel gating and modulation by transmitters depend on cellular compartmentalization. Nat Neurosci 3:670-678.
39. Delmas P, Abogadie FC, Milligan G, Buckley NJ, and Brown DA (1999) Beta gamma dimers derived from G(o) and G(i) proteins contribute different components of adrenergic inhibition of Ca2+ channels in rat sympathetic neurones. J Physiol (Lond) 518:23-36.
40. De Waard M, Liu HY, Walker D, Scott VES, Gurnett CA, and Campbell KP (1997) Direct binding of G-protein Bgamma complex to voltage-dependent calcium channels. Nature (Lond) 385:446-450.
41. 2+ channel regulation by a conserved β subunit domain. Neuron 13:495-503.
42. 2+ channels. FEBS Lett 380:272-276.
43. 2+ channels. J Biol Chem 270:12056-12064.
44. Diversé-Pierluissi M and Dunlap K (1993) Distinct, convergent second messenger pathways modulate neuronal calcium currents. Neuron 10:753-760.
45. Diversé-Pierluissi M, Goldsmith PK, and Dunlap K (1995) Transmitter-mediated inhibition of N-type calcium channels in sensory neurons involves multiple GTP-binding proteins and subunits. Neuron 14:191-200.
46. Dohlman HG and Thorner J (1997) RGS proteins and signaling by heterotrimeric G proteins. J Biol Chem 272:3871-3874.
47. Dolphin AC (1991) Regulation of calcium channel activity by GTP binding proteins and second messengers. Biochim Biophys Acta 1091:68-80.
48. Dolphin AC (1998) Mechanisms of modulation of voltage-dependent calcium channels by G proteins. J Physiol (Lond) 506:3-11.
49. Dolphin AC (1999) L-type calcium channel modulation. Adv Second Messenger Phosphoprotein Res 33:153-177.
50. Dolphin AC (2003) β subunits of voltage-gated calcium channels. J Bioenerg Biomembr, in press.
51. Dolphin AC, Forda SR, and Scott RH (1986) Calcium-dependent currents in cultured rat dorsal root ganglion neurones are inhibited by an adenosine analogue. J Physiol (Lond) 373:47-61.
52. Dolphin AC and Prestwich SA (1985) Pertussis toxin reverses adenosine inhibition of neuronal glutamate release. Nature (Lond) 316:148-150.
53. Dolphin AC and Scott RH (1987) Calcium channel currents and their inhibition by (-)-baclofen in rat sensory neurones: modulation by guanine nucleotides. J Physiol (Lond) 386:1-17.
54. Dolphin AC and Scott RH (1990) Modulation of neuronal calcium currents by G protein activation, in G Proteins and Signal Transduction (Nathanson N ed) pp 12-27, Rockefeller University Press, New York, NY.
55. Dolphin AC, Wootton JF, Scott RH, and Trentham DR (1988) Photoactivation of intracellular guanosine triphosphate analogues reduces the amplitude and slows the kinetics of voltage-activated calcium channel currents in sensory neurones. Pflueg Arch Eur J Physiol 411:628-636.
56. Dubel SJ, Starr TVB, Hell J, Ahlijanian MK, Enyeart JJ, Catterall WA, and Snutch TP (1992) Molecular cloning of the α-1 subunit of an ω-conotoxin-sensitive calcium channel. Proc Natl Acad Sci USA 89:5058-5062.
57. Dunlap K and Fischbach GD (1978) Neurotransmitters decrease the calcium component of sensory neurone action potentials. Nature (Lond) 276:837-839.
58. Dunlap K and Fischbach GD (1981) Neurotransmitters decrease the calcium conductance activated by depolarization of embryonic chick sensory neurones. J Physiol (Lond) 317:519-535.
59. Dunlap KL and Ikeda SR (1998) Receptor-mediated pathways that modulate calcium channels. Semin Neurosci 9:198-208.
60. 2 subunits of a DHP-sensitive calcium channel. Science (Wash DC) 241:1661-1664.
61. Elmslie KS and Jones SW (1994) Concentration dependence of neurotransmitter effects on calcium current kinetics in frog sympathetic neurones. J Physiol (Lond) 481:35-46.
62. Elmslie KS, Zhou W, and Jones SW (1990) LHRH and GTPyS modify calcium current activation in bullfrog sympathetic neurons. Neuron 5:75-80.
63. Ertel EA, Campbell KP, Harpold MM, Hofmann F, Mori Y, Perez-Reyes E, Schwartz A, Snutch TP, Tanabe T, Birnbaumer L, et al. (2000) Nomenclature of voltage-gated calcium channels. Neuron 25:533-535.
64. 2+ channels in rat dorsal root ganglion neurons in vitro. Neuron 2:1185-1193.
65. Fatt P and Katz B (1953) The electrical properties of crustacean muscle fibres. J Physiol (Lond) 120:171-204.
66. 5 subunit interacts selectively with the Gq α subunit. J Biol Chem 273:636-644.
67. Flockerzi V, Oeken H-J, Hofmann F, Pelzer D, Cavalié A, and Trautwein W (1986) Purified dihydropyridine-binding site from skeletal muscle T-tubules is a functional calcium channel. Nature (Lond) 323:66-68.
68. Forscher P, Oxford GS, and Schulz D (1986) Noradrenaline modulates calcium channels in avian dorsal root ganglion cells through tight receptor-channel coupling. J Physiol (Lond) 379:131-144.
69. Furukawa T, Miura R, Mori Y, Strobeck M, Suzuki K, Ogihara Y, Asano T, Morishita R, Hashii M, Higashida H, et al. (1998a) Differential interactions of the C terminus and the cytoplasmic I-II loop of neuronal Ca2+ channels with G-protein alpha and beta gamma subunits. II. Evidence for direct binding. J Biol Chem 273:17595-17603.
70. Furukawa T, Nukada T, Mori Y, Wakamori M, Fujita Y, Ishida H, Fukuda K, Kato S, and Yoshii M (1998b) Differential interactions of the C terminus and the cytoplasmic I-II loop of neuronal Ca2+ channels with G-protein alpha and beta gamma subunits. I. Molecular determination. J Biol Chem 273:17585-17594.
71. 2+ channels. J Neurosci 18:9163-9170.
72. García-Palomero E, Renart J, Andrés-Mateos E, Solís-Garrido L, Matute C, Herrero CJ, García AG, and Montiel C (2001) Differential expression of calcium channel subtypes in the bovine adrenal medulla. Neuroendocrinology 74:251-261.
73. Golard A, Role L, and Siegelbaum SA (1994) Substance P potentiates calcium channel modulation by somatostatin in chick sympathetic ganglia. J Neurophysiol 72:2683-2690.
74. Hagiwara S and Takahashi K (1967) Surface density of calcium ions and calcium spikes in the barnacle muscle fiber membrane. J Gen Physiol 50:583-601.
75. Hamid J, Nelson D, Spaetgens R, Dubel SJ, Snutch TP, and Zamponi GW (1999) Identification of an integration center for cross-talk between protein kinase C and G protein modulation of N-type calcium channels. J Biol Chem 274:6195-6202.
76. 2+ channel β subunit as a basis for understanding its functional properties. FEBS Lett 445:366-370.
77. 2+ channels by G-protein βgamma subunits. Nature (Lond) 380:258-262.
78. 1A subunit. Proc Natl Acad Sci USA 94:1512-1516.
79. o, regulates neuronal calcium channels. Nature (Lond) 325:445-447.
80. Hess P, Lansman JB, and Tsien RW (1984) Different modes of Ca channel gating behaviour favoured by dihydropyridine Ca agonists and antagonists. Nature (Lond) 311:538-544.
81. 2+ channel β4 subunit. Proc Natl Acad Sci USA 100:307-312.
82. Hille B (1992) G protein-coupled mechanisms and nervous signaling. Neuron 9:187-195.
83. Hille B (2001) Ion Channels of Excitable Membranes, Sinauer Associates Inc, Sunderland, MA.
84. Hillman D, Chen S, Aung TT, Cherksey B, Sugimori M, and Llinás R (1991) Localization of P-type calcium channels in the central nervous system. Proc Natl Acad Sci USA 88:7076-7080.
85. Holz GGI, Rane SG, and Dunlap K (1986) GTP-binding proteins mediate transmitter inhibition of voltage-dependent calcium channels. Nature (Lond) 319:670-672.
86. Hosey MM, Barhanin J, Schmid A, Vandaele S, Ptasienski J, O'Callahan C, Cooper C, and Lazdunski M (1987) Photoaffinity labelling and phosphorylation of a 165 kilodalton peptide associated with dihydropyridine and phenylalkylamine-sensitive calcium channels. Biochem Biophys Res Commun 147:1137-1145.
87. Huang CL, Feng S, and Hilgemann DW (1998) Direct activation of inward rectifier potassium channels by PIP2 and its stabilization by Gbetagamma. Nature (Lond) 391:803-806.
88. Hullin R, Khan IFY, Wirtz S, Mohacsi P, Varadi G, Schwartz A, and Herzig S (2003) Cardiac L-type calcium channel β-subunits expressed in human heart have differential effects on single channel characteristics. J Biol Chem 2003:21623-21630.
89. Hymel L, Striessnig J, Glossmann H, and Schindler H (1988) Purified skeletal muscle 1,4-dihydropyridine receptor forms phosphorylation-dependent oligomeric calcium channels in planar bilayers. Proc Natl Acad Sci USA 85:4290-4294.
90. Ikeda SR (1991) Double-pulse calcium channel current facilitation in adult rat sympathetic neurones. J Physiol (Lond) 439:181-214.
91. Ikeda SR (1996) Voltage-dependent modulation of N-type calcium channels by G protein βgamma subunits. Nature (Lond) 380:255-258.
92. Ikeda SR and Schofield GG (1989) Somatostatin blocks a calcium current in rat sympathetic ganglion neurones. J Physiol (Lond) 409:221-240.
93. Jeong SW and Ikeda SR (1999) Sequestration of G-protein beta gamma subunits by different G-protein alpha subunits blocks voltage-dependent modulation of Ca2+ channels in rat sympathetic neurons. J Neurosci 19:4755-4761.
94. Jeong SW and Ikeda SR (2000) Endogenous regulator of G-protein signaling proteins modify N-type calcium channel modulation in rat sympathetic neurons. J Neurosci 20:4489-4496.
95. Jones LP, Patil PG, Snutch TP, and Yue DT (1997) G-protein modulation of N-type calcium channel gating current in human embryonic kidney cells (HEK 293). J Physiol (Lond) 498:601-610.
96. 1E calcium channels. J Gen Physiol 112:125-143.
97. Jones SW and Elmslie KS (1997) Transmitter modulation of neuronal calcium channels. J Membr Biol 155:1-10.
98. 2+ channels. Biophys J 70:1285-1293.
99. Kammermeier PJ, Ruiz-Velasco V, and Ikeda SR (2000) A voltage-independent calcium current inhibitory pathway activated by muscarinic agonists in rat sympathetic neurons requires both Galpha Q/11 and Gbeta gamma. J Neurosci 20:5623-5629.
100. 2+ channels. J Biol Chem 276:32917-32924.
101. 2+ channel current by an adenosine analog mediated by a GTP-binding protein in chick sensory neurons. Pflueg Arch Eur J Physiol 414:145-149.
102. Kinoshita M, Nukada T, Asano T, Mori Y, Akaike A, Satoh M, and Kaneko S (2001) Binding of Galpha(o) N terminus is responsible for the voltage-resistant inhibition of alpha (1A) (P/Q-type, Ca(v)2.1) Ca(2+) channels. J Biol Chem 276:28731-28738.
103. Kleuss C, Hescheler J, Ewel C, Rosenthal W, Schultz G, and Wittig B (1991) Assignment of G-protein subtypes to specific receptors inducing inhibition of calcium currents. Nature (Lond) 353:43-48.
104. Klugbauer N, Dai SP, Specht V, Lacinová L, Marais E, Bohn G, and Hofmann F (2000) A family of gamma-like calcium channel subunits. FEBS Lett 470:189-197.
105. Klugbauer N, Lacinova L, Marais E, Hobom M, and Hofmann F (1999) Molecular diversity of the calcium channel α2-δ subunit. J Neurosci 19:684-691.
106. Koh DS and Hille B (1997) Modulation by neurotransmitters of catecholamine secretion from sympathetic ganglion neurons detected by amperometry. Proc Natl Acad Sci USA 94:1506-1511.
107. + channels by low concentrations of βγ subunits of rat brain G protein. Pflueg Arch Eur J Physiol 413:325-327.
108. Lee HK and Elmslie KS (2000) Reluctant gating of single N-type calcium channels during neurotransmitter-induced inhibition in bullfrog sympathetic neurons. J Neurosci 20:3115-3128.
109. 2+ channel gamma subunit. Nat Genet 19:340-347.
110. 2+ channel. J Biol Chem 271:13804-13810.
111. + channel in heart. Nature (Lond) 325:321-326.
112. + channels through phosphatidylinositol 4,5-bisphosphate. J Physiol (Lond) 520:630.
113. MacKinnon R, Aldrich RW, and Lee AW (1993) Functional stoichiometry of Shaker potassium channel inactivation. Science (Wash DC) 262:757-759.
114. Man-Son-Hing H, Zoran MJ, Lukowiak K, and Haydon PG (1989) A neuromodulator of synaptic transmission acts on the secretory apparatus as well as on ion channels. Nature (Lond) 341:237-239.
115. McCleskey EW, Fox AP, Feldman DH, Cruz LJ, Olivera BM, Tsien RW, and Yoshickami D (1987) Omega-conotoxin: direct and persistent blockade of specific types of calcium channels in neurons but not muscle. Proc Natl Acad Sci USA 84:4327-4331.
116. o, antagonize noradrenaline-induced calcium current inhibition in NG108-15 hybrid cells. Neuron 3:177-182.
117. Meir A, Bell DC, Stephens GJ, Page KM, and Dolphin AC (2000) Calcium channel β subunit promotes voltage-dependent modulation of α1B by Gβγ. Biophys J 79:731-746.
118. Meir A and Dolphin AC (1998) Known calcium channel α1 subunits can form low threshold, small conductance channels, with similarities to native T type channels. Neuron 20:341-351.
119. Meir A and Dolphin AC (2002) Kinetics and Gbetagamma modulation of Ca(v)2.2 channels with different auxiliary beta subunits. Pflueg Arch Eur J Physiol 444:263-275.
120. B-receptor modulation of N-type calcium channels in cultured dorsal root ganglion nNeurons. Pflueg Arch Eur J Physiol 425:335-343.
121. Meza U and Adams B (1998) G-protein-dependent facilitation of neuronal alpha1A, alpha1B and alpha1E Ca channels. J Neurosci 18:5240-5252.
122. Mikami A, Imoto K, Tanabe T, Niidome T, Mori Y, Takeshima H, Narumiya S, and Numa S (1989) Primary structure and functional expression of the cardiac dihydropyridine-sensitive calcium channel. Nature (Lond) 340:230-233.
123. Mintz IM, Venema VJ, Swiderek KM, Lee TD, Bean BP, and Adams ME (1992) P-type calcium channels blocked by the spider toxin ω-Aga-IVA. Nature (Lond) 355:827-829.
124. 2+ channels. Neuron 17:781-788.
125. Mori Y, Friedrich T, Kim M-S, Mikami A, Nakai J, Ruth P, Bosse E, Hofmann F, Flockerzi V, Furuichi T, et al. (1991) Primary structure and functional expression from complementary DNA of a brain calcium channel. Nature (Lond) 350:398-402.
126. v2.2 calcium channel expression. EMBO J 21:1514-1523.
127. Nasuhoglu C, Feng S, Mao Y, Shammat I, Yamamato M, Earnest S, Lemmon M, and Hilgemann DW (2002) Modulation of cardiac PIP2 by cardioactive hormones and other physiologically relevant interventions. Am J Physiol Cell Physiol 283:C223-C234.
128. Neely A, Wei X, Olcese R, Birnbaumer L, and Stefani E (1993) Potentiation by the β subunit of the ratio of the ionic current to the charge movement in the cardiac calcium channel. Science (Wash DC) 262:575-578.
129. Nowycky MC, Fox AP, and Tsien RW (1985a) Long-opening mode of gating of neuronal calcium channels and its promotion by the dihydropyridine calcium agonist Bay K 8644. Proc Natl Acad Sci USA 82:2178-2182.
130. Nowycky MC, Fox AP, and Tsien RW (1985b) Three types of neuronal calcium channel with different calcium agonist sensitivity. Nature (Lond) 316:440-446.
131. Nunoki K, Florio V, and Catterall WA (1989) Activation of purified calcium channels by stoichiometric protein phosphorylation. Proc Natl Acad Sci USA 86:6816-6820.
132. Olcese R, Qin N, Schneider T, Neely A, Wei X, Stefani E, and Birnbaumer L (1994) The amino terminus of a calcium channel β subunit sets rates of channel inactivation independently of the subunit's effect on activation. Neuron 13:1433-1438.
133. 2+ channel α1 subunits α1B and α1E as an essential determinant of G protein modulation. J Neurosci 18:4815-4824.
134. Page KM, Stephens GJ, Berrow NS, and Dolphin AC (1997) The intracellular loop between domains I and II of the B type calcium channel confers aspects of G protein sensitivity to the E type calcium channel. J Neurosci 17:1330-1338.
135. Patil PG, De Leon M, Reed RR, Dubel S, Snutch TP, and Yue DT (1996) Elementary events underlying voltage-dependent G-protein inhibition of N-type calcium channels. Biophys J 71:2509-2521.
136. Perez-Reyes E, Castellano A, Kim HS, Bertrand P, Baggstrom E, Lacerda AE, Wei X, and Birnbaumer L (1992) Cloning and expression of a cardiac/brain β subunit of the L-type calcium channel. J Biol Chem 267:1792-1797.
137. Piedras-Rentería ES and Tsien RW (1998) Antisense oligonucleotides against alpha1E reduce R-type calcium currents in cerebellar granule cells. Proc Natl Acad Sci USA 95:7760-7765.
138. 1-subunit. Nature (Lond) 368:67-70.
139. 2+ channel subunit caused by palmitoylation. Proc Natl Acad Sci USA 95:4690-4695.
140. Qin N, Platano D, Olcese R, Stefani E, and Birnbaumer L (1997) Direct interaction of Gβgamma with a C terminal Gβgamma binding domain of the calcium channel α1 subunit is responsible for channel inhibition by G protein coupled receptors. Proc Natl Acad Sci USA 94:8866-8871.
141. 2δ-4 subunit. Mol Pharmacol 62:485-496.
142. 2+ channel currents in rat cerebellar granule neurons. J Neurosci 15:2995-3012.
143. Restituito S, Cens T, Barrere C, Geib S, Galas S, De Waard M, and Charnet P (2000) The beta(2a) subunit is a molecular groom for the Ca2+ channel inactivation gate. J Neurosci 20:9046-9052.
144. Reuter H (1987) Calcium channel modulation by β-adrenergic neurotransmitters in the heart. Experientia (Basel)43:1173-1175.
145. Roche JP and Treistman SN (1998) The calcium channel β3 subunit enhances voltage-dependent relief of G protein inhibition induced by muscarinic receptor activation and Gβgamma. J Neurosci 18:4883-4890.
146. Ruiz-Velasco V and Ikeda SR (2000) Multiple G-protein βgamma combinations produce voltage-dependent inhibition of N-type calcium channels in rat superior cervical ganglion neurons. J Neurosci 20:2183-2191.
147. Ruth P, Röhrkasten A, Biel M, Bosse E, Regulla S, Meyer HE, Flockerzi V, and Hofmann F (1989) Primary structure of the β subunit of the DHP-sensitive calcium channel from skeletal muscle. Science (Wash DC) 245:1115-1118.
148. + channel by G-protein α-subunits, Nature (Lond) 380:624-627.
149. Scott RH and Dolphin AC (1986) Regulation of calcium currents by a GTP analogue: potentiation of (-)-baclofen-mediated inhibition. Neurosci Lett 69:59-64,
150. 2+ channels. J Biol Chem 271:3207-3212.
151. Shapiro MS and Hille B (1993) Substance P and somatostatin inhibit calcium channels in rat sympathetic neurons via different G protein pathways. Neuron 10:11-20.
152. Simen AA, Lee CC, Simen BB, Bindokas VP, and Miller RJ (2001) The C terminus of the Ca channel alpha1B subunit mediates selective inhibition by G-protein-coupled receptors. J Neurosci 21:7587-7597.
153. Singer D, Biel M, Loten I, Flockerzi V, Hofmann F, and Dascal N (1991) The roles of the subunits in the function of the calcium channel. Science (Wash DC) 253:1553-1557.
154. 5 subunits. Proc Natl Acad Sci USA 95:13307-13312.
155. Soong TW, Stea A, Hodson CD, Dubel SJ, Vincent SR, and Snutch TP (1993) Structure and functional expression of a member of the low voltage-activated calcium channel family. Science (Wash DC) 260:1133-1136.
156. 1E calcium channels. J Biol Chem 274:22428-22436.
157. Stanley EF and Atrakchi AH (1990) Calcium currents recorded from a vertebrate presynaptic nerve terminal are resistant to the dihydropyridine nifedipine. Proc Natl Acad Sci USA 87:9683-9687.
158. Stea A, Soong TW, and Snutch TP (1995) Determinants of PKC-dependent modulation of a family of neuronal calcium channels. Neuron 15:929-940.
159. Stephens GJ, Brice NL, Berrow NS, and Dolphin AC (1998a) Facilitation of rabbit α1B calcium channels: involvement of endogenous Gβgamma subunits. J Physiol (Lond) 509:15-27.
160. 2+ channel al subunits in G protein modulation. J Physiol (Lond) 509:163-169.
161. Stephens GJ, Page KM, Bogdanov Y, and Dolphin AC (2000) The α1B calcium channel amino terminus contributes determinants for β subunit mediated voltage-dependent inactivation properties. J Physiol (Lond) 525:377-390.
162. Stephens GJ, Page KM, Burley JR, Berrow NS, and Dolphin AC (1997) Functional expression of rat brain cloned α1E calcium channels in COS-7 cells. Pflueg Arch Eur J Physiol 433:523-532.
163. Stotz SC, Hamid J, Spaetgens RL, Jarvis SE, and Zamponi GW (2000) Fast inactivation of voltage-dependent calcium channels. A hinged-lid mechanism? J Biol Chem 275:24575-24582.
164. Surprenant A, Shen K-Z, North RA, and Tatsumi H (1990) Inhibition of
165. Takahashi M, Seager MJ, Jones JF, Reber BFX, and Catterall WA (1987) Subunit structure of dihydropyridine-sensitive calcium channels from skeletal muscle. Proc Natl Acad Sci USA 84:5478-5482.
166. Takahashi T, Kajikawa Y, and Tsujimoto T (1998) G-protein-coupled modulation of presynaptic calcium currents and transmitter release by a GABAB receptor. J Neurosci 18:3138-3146.
167. Takahashi T and Momiyama A (1993) Different types of calcium channels mediate central synaptic transmission. Nature (Lond) 366:156-158.
168. Tanabe T, Takeshima H, Mikami A, Flockerzi V, Takahashi H, Kangawa K, Kojima M, Matsuo H, Hirose T, and Numa S (1987) Primary structure of the receptor for calcium channel blockers from skeletal muscle. Nature (Lond) 328:313-318.
169. Tareilus E, Roux M, Qin N, Olcese R, Zhou JM, Stefani E, and Birnbaumer L (1997) A Xenopus oocyte β subunit: evidence for a role in the assembly/expression of voltage-gated calcium channels that is separate from its role as a regulatory subunit. Proc Natl Acad Sci USA 94:1703-1708.
170. Tomita S, Chen L, Kawasaki Y, Petralia RS, Wenthold RJ, Nicoll RA, and Bredt DS (2003) Functional studies and distribution define a family of transmembrane AMPA receptor regulatory proteins. J Cell Biol 161:805-816.
171. Toth PT, Bindokas VP, Bleakman D, Colmers WF, and Miller RJ (1993) Mechanism of presynaptic inhibition by neuropeptide Y at sympathetic nerve terminals. Nature (Lond) 364:635-639.
172. Wakamori M, Mikala G, and Mori Y (1999) Auxiliary subunits operate as a molecular switch in determining gating behaviour of the unitary N-type Ca2+ channel current in Xenopus oocytes. J Physiol (Lond) 517:659-672.
173. 1A subunit. J Biol Chem 273:2361-2367.
174. 2+ channel activation. J Biol Chem 274:12383-12390.
175. Walker D and De Waard M (1998) Subunit interaction sites in voltage-dependent Ca2+ channels: role in channel function. Trends Neurosci 21:148-154.
176. Watson N, Linder ME, Druey KM, Kehrl JH, and Blumer KJ (1996) RGS family members: GTPase-activating proteins for heterotrimeric G-protein a-subunits. Nature (Lond) 383:172-175.
177. Wickman K, Iniguez-Lluhl JA, Davenport PA, Taussig R, Krapivinsky GB, Linder ME, Gilman AG, and Clapham DE (1994) Recombinant G protein β gamma subunits activate the muscarinic-gated atrial potassium channel. Nature (Lond) 368:255-257.
178. Williams S, Serafin M, Mühlethaler M, and Bernheim L (1997) Facilitation of N-type calcium current is dependent on the frequency of action potential-like depolarizations in dissociated cholinergic basal forebrain neurons of the guinea pig. J Neurosci 17:1625-1632.
179. 2+ channel complex purified from brain. Science (Wash DC) 261:486-489.
180. Wolfe JT, Wang H, Howard J, Garrison JC, and Barrett PQ (2003) T-type calcium channel regulation by specific G-protein betagamma subunits. Nature (Lond) 424:209-213.
181. 2. Nature (Lond) 419:947-952,
182. + channels are activated by βgamma subunits and inhibited by the GDP bound form of the a subunit of transducin. Biochem Biophys Res Commun 200:1484-1490.
183. 3 cells. Biochem Biophys Res Commun 220:453-458.
184. Yatani A, Codina J, Brown AM, and Birnbaumer L (1987) Direct activation of mammalian atrial muscarinic potassium channels by GTP regulatory protein Gk. Science (Wash DC) 235:207-211.
185. 1 subunit. Nature (Lond) 385:442-446.
186. βgamma subunit. Proc Natl Acad Sci USA 95:4035-4039.
187. Zhang H, He C, Yan X, Mirshahi T, and Logothetis DE (1999) Activation of inwardly rectifying K+ channels by distinct PtdIns(4,5)P2 interactions. Nat Cell Biol 1:183-188.
188. Zhang J-F, Ellinor PT, Aldrich RW, and Tsien RW (1994) Molecular determinants of voltage-dependent inactivation in calcium channels. Nature (Lond) 372:97-100.
189. 2+ channels support their inhibition by G proteins. Neuron 17:991-1003.
190. Zhao X, Varnai P, Tuymetova G, Balla A, Toth ZE, Oker-Blom C, Roder J, Jeromin A, and Balla T (2001) Interaction of neuronal calcium sensor-1 (NCS-1) with phosphatidylinositol 4-kinase beta stimulates lipid kinase activity and affects membrane trafficking in COS-7 cells. J Biol Chem 276:40183-40189.
191. Zhong H, Li B, Scheuer T, and Catterall WA (2001) Control of gating mode by a single amino acid residue in transmembrane segment IS3 of the N-type Ca2+ channel. Proc Natl Acad Sci USA 98:4705-4709.
192. Zhou J, Shapiro M, and Hille B (1997) Speed of calcium channel modulation by neurotransmitters in rat sympathetic neurons. J Neurophysiol 77:2040-2048.
193. Zhou JY, Siderovski DP, and Miller RJ (2000) Selective regulation of N-type Ca channels by different combinations of G-protein β/gamma subunits and RGS proteins. J Neurosci 20:7143-7148.
194. 2+ channels of sympathetic neurons via a pertussis toxin-insensitive but cholera toxin-sensitive pathway. Neuron 13:657-669.