Recent advances in the molecular understanding of voltage-gated Ca2+ channels

Molecular and Cellular Neurosciences

Volumn 14, Issue 4-5, 1999, Pages 255-272

  Randall, Andrew ^a   Benham, Christopher D ^a  

^a GLAXOSMITHKLINE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CHANNEL; CALMODULIN; CYCLIC AMP DEPENDENT PROTEIN KINASE; DIHYDROPYRIDINE DERIVATIVE; GABAPENTIN; PHENYLALKYLAMINE; TOXIN; VOLTAGE GATED CHANNEL FORMING PROTEIN;

DRUG PROTEIN BINDING; GENE MUTATION; HUMAN; MIGRAINE; MOLECULAR BIOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PROTEIN INTERACTION; REVIEW;

EID: 0032729746     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1006/mcne.1999.0795     Document Type: Review

References (151)

1. Akaike N. T-type calcium channel in mammalian CNS neurones. Comp. Biochem. Physiol. Ser. C. 98:1991;31-40.
2. Ashcroft F. M., Proks P., Smith P. A., Ammala C., Bokvist K., Rorsman P. Stimulus-secretion coupling in pancreatic β cells. J. Cell. Biochem. 55:1994;54-65.
3. Ashcroft F. M., Stanfield P. R. Calcium inactivation in skeletal muscle fibres of the stick insect, Carausius morosus. J. Physiol. London. 330:1982;349-372.
4. Bechhansen N. T., Naylor M. J., Maybaum T. A., Pearce W. G., Koop B., Fishman G. A., Mets M., Musarella M. A., Boycott K. M. Loss of function mutations in a calcium-channel alpha(1)-subunit gene in XP11.23 cause incomplete X-linked congenital stationary night blindness. Nature Genet. 19:1998;264-267.
5. 1A calcium channels transiently expressed in the COS-7 cell line. Eur. J. Neurosci. 9:1997;739-748.
6. 2+-dependent regulation in neuronal gene expression. Curr. Opin. Neurobiol. 7:1997;419-429.
7. Black J. L., Lennon V. A. Identification and cloning of putative human neuronal voltage-gated calcium channel gamma-2 and gamma-3 subunits: Neurologic implications. Mayo Clinic Proc. 74:1999;357-361.
8. 2+ channels and insulin-containing secretory granules and its significance for the initiation of exocytosis in mouse pancreatic B-cells. EMBO J. 14:1995;50-57.
9. 1A subunit gene generates phenotypic variants of P- and Q-type calcium channels. Nature Neurosci. 2:1999;407-415.
10. 1E calcium channel exhibits permeation properties similar to the low-voltage-activated calcium channels. J. Neurosci. 16:1996;4983-4993.
11. Brehm P., Eckert R. Calcium entry leads to inactivation of calcium channel in Paramecium. Science. 202:1978;1203-1206.
12. 2+ channel subunit compositions in lethargic mouse brain. Mol. Cell. Neurosci. 13:1999;293-311.
13. 2+ channel β subunit gene Cchb4 is associated with ataxia and seizures in the lethargic (lh) mouse. Cell. 88:1997;385-392.
14. 2+ channel β subunits. Biochem. Soc. Trans. 22:1994;483-488.
15. Castellano A., Wei X., Birnbaumer L., Perez-Reyes E. Cloning and expression of a neuronal calcium channel β subunit. J. Biol. Chem. 268:1993a;12359-12366.
16. Castellano A., Wei X., Birnbaumer L., Perez-Reyes E. Cloning and expression of a third calcium channel β subunit. J. Biol. Chem. 268:1993b;3450-3455.
17. Catterall W. A. Structure and function of voltage-gated ion channels. Annu. Rev. Biochem. 64:1995;493-531.
18. Chad J., Eckert R., Ewald D. Kinetics of calcium-dependent inactivation of calcium current in voltage-clamped neurones of Aplysia californica. J. Physiol. Lond. 347:1984;279-300.
19. Chad J. E., Eckert R. Calcium domains associated with individual channels can account for anomalous voltage relations of Ca-dependent responses. Biophys. J. 45:1984;993-999.
20. Chaudhari N. A single nucleotide deletion in the skeletal muscle-specific calcium channel transcript of muscular dysgenesis (mdg) mice. J. Biol. Chem. 267:1992;25636-25639.
21. Chin H. Molecular biology of neuronal voltage-gated calcium channels. Exp. Mol. Med. 30:1998;123-130.
22. Craig P. J., McAinsh A. D., McCormack A. L., Smith W., Beattie R. E., Priestley J. V., Yip J. L., Averill S., Longbottom E. R., Volsen S. G. Distribution of the voltage-dependent calcium channel alpha(1A) subunit throughout the mature rat brain and its relationship to neurotransmitter pathways. J. Comp. Neurol. 397:1998;251-267.
23. 2+ channel gene family. Circ. Res. 83:1998;103-109.
24. Dasgupta M., Honeycutt T., Blumenthal D. K. The gamma-subunit of skeletal muscle phosphorylase kinase contains two noncontiguous domains that act in concert to bind calmodulin. J. Biol. Chem. 264:1989;17156-17163.
25. 1E voltage-dependent calcium channel subunits in the human hippocampus and parahippocampal gyrus. Neuroscience. 71:1996;1013-1024.
26. 1 subunits at the human and rat neuromuscular junction. J. Neurosci. 17:1997;6226-6235.
27. 2+ channels. Science. 270:1995;1502-1506.
28. 2+ channel expressed in Xenopus oocytes. J. Physiol. London. 485:1995;619-634.
29. 2+ channel regulation by a conserved β subunit domain. Neuron. 13:1994;495-503.
30. Deisseroth K., Bito H., Tsien R. W. Signaling from synapse to nucleus: postsynaptic CREB phosphorylation during multiple forms of hippocampal synaptic plasticity. Neuron. 16:1996;89-101.
31. 2+ channel conductance. Biophys. J. 73:1997;1402-1409.
32. Dolphin A. C. Mechanisms of modulation of voltage-dependent calcium channels by G proteins. J. Physiol. 506:1998;3-11.
33. 2δ and other accessory subunits on the expression and properties of the calcium channel α1G. J. Physiol. 519:1999;35-46.
34. Dove L. S., Abbott L. C., Griffith W. H. Whole-cell and single-channel analysis of P-type calcium currents in cerebellar Purkinje cells of leaner mutant mice. J. Neurosci. 18:1998;7687-7699.
35. Doyle J., Ren X., Lennon G., Stubbs L. Mutations in the Cacn11a4 calcium channel gene are associated with seizures, cerebellar degeneration, and ataxia in tottering and leaner mutant mice. Mammalian Genome. 8:1997;113-120.
36. 1 subunit of an omega-conotoxin-sensitive calcium channel. Proc. Natl. Acad. Sci. USA. 89:1992;5058-5062.
37. 2+ channels in mammalian central neurons. Trends Neurosci. 18:1995;89-98.
38. Eckert R., Chad J. E. Inactivation of Ca channels. Prog. Biophys. Mol. Biol. 44:1984;215-267.
39. Elbaz A., Vale-Santos J., Jurkat-Rott K., Lapie P., Ophoff R. A., Bady B., Links T. P., Piussan C., Vila A., Monnier N. Hypokalemic periodic paralysis and the dihydropyridine receptor (CACNL1A3): Genotype/phenotype correlations for two predominant mutations and evidence for the absence of a founder effect in 16 caucasian families. Am. J. Human Genet. 56:1995;374-380.
40. Ellinor P. T., Zhang J. F., Horne W. A., Tsien R. W. Structural determinants of the blockade of N-type calcium channels by a peptide neurotoxin. Nature. 372:1994;272-275.
41. 2 subunits of a DHP-sensitive calcium channel. Science. 241:1988;1661-1664.
42. Fletcher C. F., Lutz C. M., O'Sullivan T. N., Shaughnessy J. D. J., Hawkes R., Frankel W. N., Copeland N. G., Jenkins N. A. Absence epilepsy in tottering mutant mice is associated with calcium channel defects. Cell. 87:1996;607-617.
43. Fontaine B., Vale-Santos J., Jurkat-Rott K., Reboul J., Plassart E., Rime C. S., Elbaz A., Heine R., Guimaraes J., Weissenbach J. Mapping of the hypokalaemic periodic paralysis (HypoPP) locus to chromosome 1q31-32 in three European families. Nature Genet. 6:1994;267-272.
44. Fox A. P., Nowycky M. C., Tsien R. W. Kinetic and pharmacological properties distinguishing three types of calcium currents in chick sensory neurones. J. Physiol. London. 394:1987;149-172.
45. Garcia J., Nakai J., Imoto K., Beam K. G. Role of S4 segments and the leucine heptad motif in the activation of an L-type calcium channel. Biophys. J. 72:1997;2515-2523.
46. 2δ subunit of a calcium channel. J. Biol. Chem. 271:1996;5768-5776.
47. 2+ molecules. Nature. 341:1989;65-68.
48. Haan J., Terwindt G. M., Bos P. L., Ophoff R. A., Frants R. R., Ferrari M. D. Familial hemiplegic migraine in The Netherlands. Dutch Migraine Genetics Research Group. Clin. Neurol. Neurosurg. 96:1994;244-249.
49. 1A calcium channel subunit linked to familial hemiplegic migraine. J. Neurosci. 19:1999;1610-1619.
50. Hering S., Aczel S., Grabner M., Doring F., Berjukow S., Mitterdorfer J., Sinnegger M. J., Striessnig J., Degtiar V. E., Wang Z., Glossmann H. Transfer of high sensitivity for benzothiazepines from L-type to class A (BI) calcium channels. J. Biol. Chem. 271:1996;24471-24475.
51. Hess E. J. Migraines in mice. Cell. 87:1996;1149-1151.
52. Hille B. Ionic Channels of Excitable Membranes. 1992;Sinauer, Sunderland.
53. 2+ channels with a Hill coefficient of approximately 1 and an inhibition constant of approximately 4 microM by reducing channel's open probability. Biophys. J. 73:1997;1857-1865.
54. 2+ channel diversity. Annu. Rev. Neurosci. 17:1994;399-418.
55. Huguenard J. R. Low-threshold calcium currents in central nervous system neurons. Annu. Rev. Physiol. 58:1996;329-348.
56. Hullin R., Singer L. D., Freichel M., Biel M., Dascal N., Hofmann F., Flockerzi V. Calcium channel β subunit heterogeneity: functional expression of cloned cDNA from heart, aorta and brain. EMBO J. 11:1992;885-890.
57. Iles D. E., Lehmann H., Scherer S. W., Tsui L. C., Olde W., Suijkerbuijk R. F., Heytens L., Mikala G., Schwartz A., Ellis F. R. Localization of the gene encoding the alpha2/delta-subunits of the L-type voltage-dependent calcium channel to chromosome 7q and analysis of the segregation of flanking markers in malignant hyperthermia susceptible families. Hum. Mol. Genet. 3:1994;969-975.
58. 2+ channels. Neuron. 9:1992;197-207.
59. 2+ channels. Neuron. 12:1994;1301-1318.
60. Jay S. D., Ellis S. B., McCue A. F., Williams M. E., Vedvick T. S., Harpold M. M., Campbell K. P. Primary structure of the gamma subunit of the DHP-sensitive calcium channel from skeletal muscle. Science. 248:1990;490-492.
61. Jen J. Calcium channelopathies in the central nervous system. Curr. Opin. Neurobiol. 9:1999a;274-280.
62. Jen J., Yue Q., Nelson S. F., Yu H., Litt M., Nutt J., Baloh R. W. A novel nonsense mutation in CACNA1A causes episodic ataxia and hemiplegia. Neurology. 53:1999b;34-37.
63. Jodice C., Mantuano E., Veneziano L., Trettel F., Sabbadini G., Calandriello L., Francia A., Spadaro M., Pierelli F., Salvi F., Ophoff R. A., Frants R. R., Frontali M. Episodic ataxia type 2 (EA2) and spinocerebellar ataxia type 6 (SCA6) due to CAG repeat expansion in the CACNA1A gene on chromosome 19p. Hum. Mol. Genet. 6:1997;1973-1978.
64. Jones S. W., Marks T. N. Calcium currents in bullfrog sympathetic neurons. II Inactivation. J. Gen. Physiol. 94:1989;169-182.
65. Joutel A., Bousser M. G., Biousse V., Labauge P., Chabriat H., Nibbio A., Maciazek J., Meyer B., Bach M. A., Weissenbach J. A gene for familial hemiplegic migraine maps to chromosome 19. Nature Genet. 5:1993;40-45.
66. Jurkat-Rott K., Lehmann-Horn F., Elbaz A., Heine R., Gregg R. G., Hogan K., Powers P. A., Lapie P., Vale-Santos J. E., Weissenbach J. A calcium channel mutation causing hypokalemic periodic paralysis. Hum. Mol. Genet. 3:1994;1415-1419.
67. 1G subunit mRNA of T-type voltage-dependent calcium channel in adult rat central nervous system. Neurosci. Lett. 268:1999;77-80.
68. Kim J. S., Yue Q., Jen J. C., Nelson S. F., Baloh R. W. Familial migraine with vertigo: No mutations found in CACNA1A. Am. J. Med. Genet. 79:1998;148-151.
69. 2δ subunit. J. Neurosci. 19:1999a;684-691.
70. Klugbauer N., Marais E., Lacinova L., Hofmann F. A T-type calcium channel from mouse brain. Pflugers Arch. Eur. J. Physiol. 437:1999b;710-715.
71. 1 subunit of the dihydropyridine receptor in mice with muscular dysgenesis. J. Biol. Chem. 264:1989;1345-1348.
72. Kostyuk P. G. Low-voltage activated calcium channels: Achievements and problems. Neuroscience. 92:1999;1157-1163.
73. 2+ channel kinetics. J. Biol. Chem. 273:1998;5586-5590.
74. 2δ subunits. J. Physiol. 516:1999;639-645.
75. 2+/calmodulin binds to and modulates P/Q-type calcium channels. Nature. 399:1999;155-159.
76. Lee J. H., Cribbs L. L., Daud A., Perez-Reyes E. Permeation and block of cloned T-type calcium channels. Soc. Neurosci. Abs. 24:1999a;1823.
77. Lee, J. H, Daud, A. N, Cribbs, L. L, Lacerda, A. E, Pereverzev, A, Klockner, U, Schneider, T, and, Perez-Reyes, E. 1999b, Cloning and expression of a.
78. Luebke J. I., Dunlap K., Turner T. J. Multiple calcium channel types control glutamatergic synaptic transmission in the hippocampus. Neuron. 11:1993;895-902.
79. McDonald T. F., Pelzer S., Trautwein W., Pelzer D. J. Regulation and modulation of calcium channels in cardiac, skeletal, and smooth muscle cells. Physiol. Reviews. 74:1994;365-507.
80. 1 subunits can form low threshold small conductance channels with similarities to native T-type channels. Neuron. 20:1998;341-351.
81. Meisler M. H., Sprunger L. K., Plummer N. W., Escayg A., Jones J. M. Ion channel mutations in mouse models of inherited neurological disease. Ann. Med. 29:1997;569-574.
82. Mennerick S., Matthews G. Rapid calcium-current kinetics in synaptic terminals of goldfish retinal bipolar neurons. Visual Neurosci. 15:1998;1051-1056.
83. Mikami A., Imoto K., Tanabe T., Niidome T., Mori Y., Takeshima H., Narumiya S., Numa S. Primary structure and functional expression of the cardiac dihydropyridine-sensitive calcium channel. Nature. 340:1989;230-233.
84. Mintz I. M., Adams M. E., Bean B. P. P-type calcium channels in rat central and peripheral neurons. Neuron. 9:1992;85-95.
85. 2+ channels. J. Bioenerg. Biomemb. 30:1998;319-334.
86. Mittman S., Guo J., Emerick M. C., Agnew W. S. Structure and alternative splicing of the gene encoding alpha(1I), a human brain T calcium channel alpha(1) subunit. Neurosci. Lett. 269:1999;121-124.
87. Moreno H., Rudy B., Llinas R. β subunits influence the biophysical and pharmacological differences between P- and Q-type calcium currents expressed in a mammalian cell line. Proc. Natl. Acad. Sci. USA. 94:1997;14042-14047.
88. Morgan J. I., Curran T. Calcium as a modulator of the immediate-early gene cascade in neurons. Cell Calcium. 9:1988;303-311.
89. Mori Y. Primary structure and functional expression from complimentary DNA of a brain calcium channel. Nature. 350:1991;398-402.
90. Nakai J., Adams B. A., Imoto K., Beam K. G. Critical roles of the S3 segment and S3-S4 linker of repeat I in activation of L-type calcium channels. Proc. Natl. Acad. Sci. USA. 91:1994;1014-1018.
91. 1C) expressed in Xenopus oocytes. Biophys. J. 66:1994;1895-1903.
92. Niidome T. Stable expression of the neuronal BI (Class A) calcium channel in baby hamster kidney cells. Biochem. Biophys. Res. Commun. 203:1994;1821-1827.
93. Noble S., Shimoni Y. The calcium and frequency dependence of the slow inward current 'staircase' in frog atrium. J. Physiol. 310:1981;57-75.
94. Nowycky M. C., Fox A. P., Tsien R. W. Three types of neuronal calcium channel with different calcium agonist sensitivity. Nature. 316:1985;440-443.
95. 2+ channels. Hist. Histopath. 13:1998;827-836.
96. 2+ channel gene CACNL1A4. Cell. 87:1996;543-552.
97. Perez-Reyes E., Castellano A., Kim H. S., Bertrand P., Baggstrom E., Lacerda A. E., Wei X. Y., Birnbaumer L. Cloning and expression of a cardiac/brain β subunit of the L-type calcium channel. J. Biol. Chem. 267:1992;1792-1797.
98. Perez-Reyes E., Cribbs L. L., Daud A., Lacerda A. E., Barclay J., Williamson M. P., Fox M., Rees M., Lee J. H. Molecular characterization of a neuronal low-voltage-activated T-type calcium channel. Nature. 391:1998;896-900.
99. 2+-dependent inactivation of L-type calcium channels. Neuron. 22:1999;549-558.
100. Pragnell M., De Waard M., Mori Y., Tanabe T., Snutch T. P., Campbell K. P. Calcium channel β-subunit binds to a conserved motif in the I-II cytoplasmic linker of the α1-subunit. Nature. 368:1994;67-70.
101. Ptacek L. J., Tawil R., Griggs R. C., Engel A. G., Layzer R. B., Kwiecinski H., McManis P. G., Santiago L., Moore M., Fouad G. Dihydropyridine receptor mutations cause hypokalemic periodic paralysis. Cell. 77:1994;863-868.
102. 2+ channel currents in rat cerebellar granule neurons. J. Neurosci. 15:1995;2995-3012.
103. 2+ channel diversity: Is it time for T. J. Membr. Biol. 161:1997;207-213.
104. Randall A. D., Tsien R. W. Contrasting biophysical and pharmacological properties of T-type and R-type calcium channels. Neuropharmacology. 36:1997;879-893.
105. Regan L. J. Voltage Dependent Calcium Currents in Purkinje Cells from Rat Cerebellar Vermis. J. Neurosci. 11:1991;2259-2269.
106. 1A-voltage-dependent calcium channel gene. Hum. Mol. Genet. 6:1997;1289-1293.
107. Ruth P., Rohrkasten A., Biel M., Bosse E., Regulla S., Meyer H. E., Flockerzi V., Hofmann F. Primary structure of the β subunit of the DHP-sensitive calcium channel from skeletal muscle. Science. 245:1989;1115-1118.
108. 1 subunits. Neuron. 11:1993;291-303.
109. Simmons M. L., Terman G. W., Gibbs S. M., Chavkin C. L-type calcium channels mediate dynorphin neuropeptide release from dendrites but not axons of hippocampal granule cells. Neuron. 14:1995;1265-1272.
110. 2+ channels: Diversity of form and function. Curr. Opin. Neurobiol. 2:1992;247-253.
111. 2+ dependence of inactivation. J. Biol. Chem. 272:1997;3560-3566.
112. Soong T. W., Stea A., Hodson C. D., Dubel S. J., Vincent S. R., Snutch T. P. Structure and functional expression of a member of the low voltage-activated calcium channel family. Science. 260:1993;1133-1136.
113. Starr T. V., Prystay W., Snutch T. P. Primary structure of a calcium channel that is highly expressed in the rat cerebellum. Proc. Natl. Acad. Sci. USA. 88:1991;5621-5625.
114. Stea A., Tomlinson W. J., Soong T. W., Bourinet E., Dubel S. J., Vincent S. R., Snutch T. P. Localization and functional properties of a rat brain α1A calcium channel reflect similarities to neuronal Q- and P-type channels. Proc. Natl. Acad. Sci. USA. 91:1994;10576-10580.
115. 2+ channels. Trends Pharmacol. Sci. 19:1998;108-115.
116. Strom T. M., Nyakatura G., Apfelstedtsylla E., Hellebrand H., Lorenz B., Weber B. H. F., Wutz K., Gutwillinger N., Ruther K., Drescher B., Sauer C., Zrenner E., Meitinger T., Rosenthal A., Meindl A. An L-type calcium-channel gene mutated in incomplete X-linked congenital stationary night blindness. Nature Genet. 19:1998;260-263.
117. Szepetowski P., Rochette J., Berquin P., Piussan C., Lathrop G. M., Monaco A. P. Familial infantile convulsions and paroxysmal choreoathetosis: A new neurological syndrome linked to the pericentromeric region of human chromosome 16. Am. J. Hum. Genet. 61:1997;889-898.
118. Takahashi T., Momiyama A. Different types of calcium channels mediate central synaptic transmission. Nature. 366:1993;156-158.
119. Talley E. M., Cribbs L. L., Lee J. H., Daud A., Perez-Reyes E., Bayliss D. A. Differential distribution of three members of a gene family encoding low voltage-activated (T-type) calcium channels. J. Neurosci. 19:1999;1895-1911.
120. Tanabe T., Mikami A., Niidome T., Numa S., Adams B. A., Beam K. G. Structure and function of voltage-dependent calcium channels from muscle. Ann. N.Y. Acad. Sci. 707:1993;81-86.
121. Tanabe T., Takeshima H., Mikami A., Flockerzi V., Takahshi H., Kangawa K., Kojima M., Matsuo H., Hirose T., Numa S. Primary structure of the receptor for calcium channel blockers from skeletal muscle. Nature. 328:1987;313-318.
122. 2+ channels in neurones of rat laterodorsal thalamic nucleus. J. Physiol. 499:1997;77-86.
123. Terwindt G. M., Ophoff R. A., Haan J., Sandkuijl L. A., Frants R. R., Ferrari M. D. Migraine, ataxia and epilepsy: A challenging spectrum of genetically determined calcium channelopathies. Dutch Migraine Genetics Research Group. Eur. J. Hum. Genet. 6:1998a;297-307.
124. Terwindt G. M., Ophoff R. A., Haan J., Vergouwe M. N., van Eijk R., Frants R. R., Ferrari M. D. Variable clinical expression of mutations in the P/Q-type calcium channel gene in familial hemiplegic migraine. Dutch Migraine Genetics Research Group. Neurology. 50:1998b;1105-1110.
125. Tsien R. W., Clozel J. P., Nargeot J. (Eds.). Low-Voltage-Activated T-Type Calcium Channels. 1998;Adis International, Tattenhall.
126. Tsien R. W., Wheeler D. B. Voltage-gated calcium channels. Carafoli E., Klee C. B. Intracellular Calcium. 1999.
127. Usowicz M. M., Sugimori M., Cherksey B., Llinas R. P-type calcium channels in the somata and dendrites of adult cerebellar Purkinje cells. Neuron. 9:1992;1185-1199.
128. 2+ channels in GH3 cells: Direct evidence against dephosphorylation by calcineurin. J. Membr. Biol. 156:1997;53-61.
129. Volsen S. G., Day N. C., McCormack A. L., Smith W., Craig P. J., Beattie R. E., Smith D., Ince P. G., Shaw P. J., Ellis S. B., Mayne N., Burnett J. P., Gillespie A., Harpold M. M. The expression of voltage-dependent calcium channel β subunits in human cerebellum. Neuroscience. 80:1997;161-174.
130. Wakamori M., Niidome T., Furutama D., Furuichi T., Mikoshiba K., Fujita Y., Tanaka I., Katayama K., Yatani A., Schwartz A., Mori Y. Distinctive functional properties of the neuronal BII (class E) calcium channel. Receptors Channels. 2:1994;303-314.
131. 2+ channels: Role in channel function. Trends Neurosci. 21:1998;148-154.
132. 1A subunits of brain calcium channels. J. Neurosci. 15:1995;6403-6418.
133. 2+ channels in supporting hippocampal synaptic transmission. Science. 264:1994;107-111.
134. 2+ channels in rat hippocampus. J. Neurosci. 16:1996;2226-2237.
135. Whitty C. W. M. Familial hemiplegic migraine. Handbook Clin. Neurol. 4:1986;141-153.
136. Williams M. E., Brust P. F., Feldman D. H., Patthi S., Simerson S., Maroufi A., McCue A. F., Velicelebi G., Ellis S. B., Harpold M. M. Structure and functional expression of an omega-conotoxin-sensitive human N-type calcium channel. Science. 257:1992a;389-395.
137. 2, and β subunits of a novel human neuronal calcium channel subtype. Neuron. 8:1992b;71-84.
138. 1E calcium channel subtypes. J. Biol. Chem. 269:1994;22347-22357.
139. Williams M. E., Washburn M. S., Hans M., Urrutia A., Brust P. F., Prodanovich P., Harpold M. M., Stauderman K. A. Structure and functional characterization of a novel human low-voltage activated calcium channel. J. Neurochem. 72:1999;791-799.
140. 2+ currents evoke transmitter release at a rat central synapse. Proc. Natl. Acad. Sci. USA. 95:1998;4720-4725.
141. 2+ channels. Nature. 366:1993;158-161.
142. Yue D. T., Backx P. H., Imredy J. P. Calcium-sensitive inactivation in the gating of single calcium channels. Science. 250:1990;1735-1738.
143. Yue Q., Jen J. C., Nelson S. F., Baloh R. W. Progressive ataxia due to a missense mutation in a calcium-channel gene. Am. J. Hum. Genet. 61:1997;1078-1087.
144. Yue Q., Jen J. C., Thwe M. M., Nelson S. F., Baloh R. W. De novo mutation in CACNA1A caused acetazolamide-responsive episodic ataxia. Am. J. Med. Genet. 77:1998;298-301.
145. Zhang J. F., Ellinor P. T., Aldrich R. W., Tsien R. W. Molecular determinants of voltage-dependent inactivation in calcium channels. Nature. 372:1994;97-100.
146. 2+ channels and their possible counterparts in mammalian CNS neurons. Neuropharmacology. 32:1993;1075-1088.
147. 1A-voltage-dependent calcium channel. Nature Genet. 15:1997;62-69.
148. 2+ channels in thalamic neurons. Neuroreport. 10:1999;651-657.
149. Zuhlke R. D., Pitt G. S., Deisseroth K., Tsien R. W., Reuter H. Calmodulin supports both inactivation and facilitation of L-type calcium channels. Nature. 399:1999;159-162.
150. 1C subunit. Proc. Natl. Acad. Sci. USA. 95:1998;3287-3294.
151. Zygmunt A. C., Maylie J. Stimulation-dependent facilitation of the high threshold calcium current in guinea-pig ventricular myocytes. J. Physiol. 428:1990;653-671.