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Voltage-Gated Calcium Channels

  • M. Wakamori
  • K. Imoto
Reference work entry

Abstract

Voltage-gated calcium channels (VGCCs) are membrane proteins and mediate Ca2+ influx in response to membrane depolarization to evoke a wide spectrum of cellular responses, which include neurotransmitter release and activation of Ca2+-dependent enzymes. Molecularly, VGCCs are composed of multiple subunits, and their channel properties are primarily determined by the α1 subunits, which form the channel pore and various binding sites for associated proteins and drugs. There are ten genes encoding the α1 subunits. CaV2.1 (P/Q type) and CaV2.2 (N-type) are two major VGCCs in the brain, and are involved in neurotransmitter release. Recent studies revealed differences between them, for example in G-protein mediated modulation and in developmental changes. CaV1 (L-type) VGCCs are involved also in inducing changes in gene expression. CaV3 (T-type) VGCCs activate at subthreshold potentials, and for example play an important role in generating rhythmic activity.

Keywords

Neurotransmitter Release CaV2 Channel Congenital Stationary Night Blindness Layer Versus Pyramidal Neuron Thalamic Reticular Nucleus Neuron 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

List of Abbreviations

AID

α1 interacting domain

CCAT

channel-associated transcriptional regulator

cDNA

complementary DNA

CGRP

calcitonin gene-related peptide

ChIs

cholinergic interneurons

GID

G-protein interaction domain

HVA

high-voltage activated

LVA

low-voltage activated

MSNs

medium spiny neurons

NALCN

sodium leak channel

NSCaTE

N-terminal spatial Ca2+ transforming element

PKC

protein kinase C

RIM1

Rab3-interacting molecule 1

TARP

transmembrane AMPA receptor regulatory protein

VGCC

voltage-gated calcium channels

References

  1. Ahlijanian MK, Ruth E, Westenbroek RE, Catterall WA. 1990. Subunit structure and localization of dihydropyridine-sensitive calcium channels in mammalian brain, spinal cord, and retina. Neuron 4: 819–832.PubMedCrossRefGoogle Scholar
  2. Almers W, McCleskey EW. 1984. Non-selective conductance in calcium channels of frog muscle: Calcium selectivity in a single-file pore. J Physiol 353: 585–608.PubMedGoogle Scholar
  3. Andrade A, Sandoval A, Oviedo N, DeWaard M, Elias D, et al. 2007. Proteolytic cleavage of the voltage-gated Ca2+ channel α2δ subunit: Structural and functional features. Eur J Neurosci 25: 1705–1710.PubMedCrossRefGoogle Scholar
  4. Aosaki T, Kasai H. 1989. Characterization of two kinds of high-voltage-activated Ca-channel currents in chick sensory neurons. Differential sensitivity to dihydropyridines and ω-conotoxin GVIA. Pflügers Arch 414: 150–156.PubMedCrossRefGoogle Scholar
  5. Bading H, Ginty DD, Greenberg ME. 1993. Regulation of gene expression in hippocampal neurons by distinct calcium signaling pathways. Science 260: 181–186.PubMedCrossRefGoogle Scholar
  6. Bean BP. 1989. Neurotransmitter inhibition of neuronal calcium currents by changes in channel voltage dependence. Nature 340: 153–156.PubMedCrossRefGoogle Scholar
  7. Bean BP. 2007. The action potential in mammalian central neurons. Nat Rev Neurosci 8: 451–465.PubMedCrossRefGoogle Scholar
  8. Bech-Hansen NT, Naylor MJ, Maybaum TA, Pearce WG, Koop B, et al. 1998. Loss of function mutations in a calcium-channel alpha-1 subunit gene in Xp11.23 cause incomplete X-linked congenital stationary night blindness. Nat Genet 19: 264–267.PubMedCrossRefGoogle Scholar
  9. Berkefeld H, Sailer CA, Bildl W, Rohde V, Thumfart JO, et al. 2006. BKCa-CaV channel complexes mediate rapid and localized Ca2+-activated K+ signaling. Science 314: 615–620.PubMedCrossRefGoogle Scholar
  10. Bezprozvanny I, Scheller RH, Tsien RW. 1995. Functional impact of syntaxin on gating of N-type and Q-type calcium channels. Nature 378: 623–626.PubMedCrossRefGoogle Scholar
  11. Bichet D, Cornet V, Geib S, Carlier E, Volsen S, et al. 2000. The I-II loop of the Ca2+ channel α1 subunit contains an endoplasmic reticulum retention signal antagonized by the β subunit. Neuron 25: 177–190.PubMedCrossRefGoogle Scholar
  12. Bourinet E, Soong TW, Sutton K, Slaymaker S, Mathews E, et al. 1999. Splicing of α1A subunit gene generates phenotypic variants of P- and Q-type calcium channels. Nat Neurosci 2: 407–415.PubMedCrossRefGoogle Scholar
  13. Breustedt J, Vogt KE, Miller RJ, Nicoll RA, Schmitz D. 2003. α1E-containing Ca2+ channels are involved in synaptic plasticity. Proc Natl Acad Sci USA 100: 12450–12455.PubMedCrossRefGoogle Scholar
  14. Carbone E, Lux HD. 1984. A low voltage-activated, fully inactivating Calcium channel in vertebrate sensory neurones. Nature 310: 501–502.PubMedCrossRefGoogle Scholar
  15. Catterall WA, Perez-Reyes E, Snutch TP, Striessnig J. 2005. International Union of Pharmacology. XLVIII. nomenclature and structure-function relationships of voltage-gated calcium channels. Pharmacol Rev 57: 411–425.PubMedCrossRefGoogle Scholar
  16. Chen L, Chetkovich DM, Petralia RS, Sweeney NT, Kawasaki Y, et al. 2000. Stargazin regulates synaptic targeting of AMPA receptors by two distinct mechanisms. Nature 408: 936–943.PubMedCrossRefGoogle Scholar
  17. Chen S, Ren YQ, Bing R, Hillman, DE. 2000. Alpha-1E subunit of the R-type calcium channel is associated with myelinogenesis. J Neurocytol 29: 719–728.PubMedCrossRefGoogle Scholar
  18. Chuang RSI, Jaffe H, Cribbs L, Perez-Reyes E, Swartz KJ. 1998. Inhibition of T-type voltage-gated calcium channels by a new scorpion toxin. Nat Neurosci 1: 668–674.PubMedCrossRefGoogle Scholar
  19. D'Ascenzo M, Vairano M, Andreassi C, Navarra P, Azzena GB, et al. 2003. Electrophysiological and molecular evidence of L- (CaV1), N- (CaV2.2), and R- (CaV2.3) type Ca2+ channels in rat cortical astrocytes. Glia 45: 354–363.CrossRefGoogle Scholar
  20. Davies A, Hendrich J, VanMinh AT, Wratten J, Douglas L, et al. 2007. Functional biology of the α2δ subunits of voltage-gated calcium channels. Trends Pharmacol Sci 28: 220–228.PubMedCrossRefGoogle Scholar
  21. De Jongh KS, Warner C, Catterall WA. 1990. Subunits of purified calcium channels. α2 and δ are encoded by the same gene. J Biol Chem 265: 14738–14741.PubMedGoogle Scholar
  22. De Waard M, Hering J, Neiss N, Feltz A. 2005. How do G proteins directly control neuronal Ca2+ channel function? Trends Pharmacol Sci 26: 427–436.Google Scholar
  23. Dick IE, Tadross MR, Liang H, Tay LH, Yang W, et al. 2008. A modular switch for spatial Ca2+ selectivity in the calmodulin regulation of CaV channels. Nature 451: 830–834.PubMedCrossRefGoogle Scholar
  24. Dietrich D, Kirschstein T, Kukley M, Pereverzev A, VonDerBrelie, et al. 2003. Functional specialization of presynaptic CaV2.3 Ca2+ channels. Neuron 39: 483–496.PubMedCrossRefGoogle Scholar
  25. Dodge FA Jr, Rahamimoff R. 1967. Co-operative action of calcium ions in transmitter release at the neuromuscular junction. J Physiol 193: 419–432.PubMedGoogle Scholar
  26. Dolmetsch RE, Pajvani U, Fife K, Spotts JM, Greenberg ME. 2001. Signaling to the nucleus by an L-type calcium channel-calmodulin complex through the MAP kinase pathway. Science 294: 333–339.PubMedCrossRefGoogle Scholar
  27. Dolphin AC. 2003. β subunits of voltage-gated calcium channels. J Bioenerg Biomembr 35: 599–620.PubMedCrossRefGoogle Scholar
  28. Dunlap K, Fischbach GD. 1981. Neurotransmitters decrease the calcium conductance activated by depolarization of embryonic chick sensory neurones. J Physiol 317: 519–535.PubMedGoogle Scholar
  29. Eckert R, Chad JE. 1984. Inactivation of Ca channels. Prog Biophys Mol Biol 44: 215–267.PubMedCrossRefGoogle Scholar
  30. Ellinor PT, Zhang JF, Randall AD, Zhou M, Schwarz TL, et al. 1993. Functional expression of a rapidly inactivating neuronal calcium channel. Nature 363: 455–458.PubMedCrossRefGoogle Scholar
  31. Ellis SB, Williams ME, Ways NR, Brenner R, Sharp AH, et al. 1988. Sequence and expression of mRNAs encoding the α, and α2 subunits of a DHP-sensitive calcium channel. Science 241: 1661–1664.PubMedCrossRefGoogle Scholar
  32. Elmslie KS, Zhou W, Jones SW. 1990. LHRH and GTP-γ-S modify calcium current activation in bullfrog sympathetic neurons. Neuron 5: 75–80.PubMedCrossRefGoogle Scholar
  33. Ertel EA, Campbell KP, Harpold MM, Hofmann F, Mori Y, et al. 2000. Nomenclature of voltage-gated calcium channels. Neuron 25: 533–535.PubMedCrossRefGoogle Scholar
  34. Fatt P, Ginsbor BL. 1958. The ionic requirements for the production of action potentials in crustacean muscle fibres. J Physiol 142: 516–543.PubMedGoogle Scholar
  35. Fletcher CF, Lutz CM, OSullivan, TN, Shaughnessy JD Jr, Hawkes R, et al. 1996. Absence epilepsy in tottering mutant mice is associated with calcium channel defects. Cell 87: 607–617.PubMedCrossRefGoogle Scholar
  36. Freise D, Held B, Wissenbach U, Pfeifer A, Trost C, et al. 2000. Absence of the γ subunit of the skeletal muscle dihydropyridine receptor increased L-type Ca2+ currents and alters channel inactivation properties. J Biol Chem 275: 14476–14481.PubMedCrossRefGoogle Scholar
  37. Fujii S, Kameyama K, Hosono M, Hayashi Y, Kitamura, K. 1997. Effect of cilnidipine, a novel dihydropyridine Ca2+-channel antagonist, on N-type Ca2+ channel in rat dorsal root ganglion neurons. J Pharmacol Exp Ther 280: 1184–1191.PubMedGoogle Scholar
  38. Fujita Y, Mynlieff M, Dirksen RT, Kim MS, Niidome T, et al. 1993. Primary structure and functional expression of the ω-conotoxin-sensitive N-type calcium channel from rabbit brain. Neuron 10: 585–598.PubMedCrossRefGoogle Scholar
  39. Gomez-Ospina N, Tsuruta F, Barreto-Chang O, Hu L, Dolmetsch R. 2006. The C-terminus of the L-type voltage-gated calcium channel CaV1.2 encodes a transcription factor. Cell 127: 591–606.PubMedCrossRefGoogle Scholar
  40. Grabsch H, Pereverzev A, Weiergraber M, Schramm M, Henry M, et al. 1999. Immunohistochemical detection of alpha-1E voltage-gated Ca2+ channel isoforms in cerebellum, INS-1 cells, and neuroendocrine cells of the digestive system. J Histochem Cytochem 47: 981–994.PubMedGoogle Scholar
  41. Green EM, Barrett CF, Bultynck G, Shamah SM, Dolmetsch RE. 2007. The tumor suppressor elF3e mediates calcium-dependent internalization of the L-type calcium channel CaV1.2. Neuron 55: 615–632.PubMedCrossRefGoogle Scholar
  42. Hagiwara S, Byerly L. 1981. Calcium channel. Annu Rev Neurosci 4: 69–125.PubMedCrossRefGoogle Scholar
  43. Hagiwara S, Ozawa S, Sand O. 1975. Voltage clamp analysis of two inward current mechanisms in the egg cell membrane of a starfish. J Gen Physiol 65: 617–644.PubMedCrossRefGoogle Scholar
  44. Hanlon MR, Berrow NS, Dolphin AC, Wallace BA. 1999. Modelling of a voltage-dependent Ca2+ channel β subunit as a basis for understanding its functional properties. FEBS Lett 445: 366–370.PubMedCrossRefGoogle Scholar
  45. Hansen JP, Chen RS, Larsen JK, Chu PJ, Janes DM., et al. 2004. Calcium channel γ6 subunits are unique modulators of low voltage-activated (CaV3.1) calcium current. J Mol Cell Caradiol 37: 1147–1158.CrossRefGoogle Scholar
  46. Hatakeyama S, Wakamori M, Ino M, Miyamoto N, Takahashi E, et al. 2001. Differential nociceptive responses in mice lacking the α1B subunit of N-type Ca2+ channels. Neuroreport 12: 2423–2427.PubMedCrossRefGoogle Scholar
  47. Hefft S, Jonas, P. 2005. Asynchronous GABA release generate long-lasting inhibition at a hippocampal interneuron-principal neuron synapse. Nat Neurosci 8: 1319–1328.PubMedCrossRefGoogle Scholar
  48. Heinemann SH, Terlau H, Stühmer W, Imoto K, Numa S. 1992. Calcium channel characteristics conferred on the sodium channel by single mutations. Nature 356: 441–443.PubMedCrossRefGoogle Scholar
  49. Herlitze S, Garcia DE, Mackie K, Hille B, Scheuer T, et al. 1996. Modulation of Ca2+ channels by G-protein βγ subunits. Nature 380: 258–262.PubMedCrossRefGoogle Scholar
  50. Hess P, Tsien RW. 1984. Mechanism of ion permeation through calcium channels. Nature 309: 453–456.PubMedCrossRefGoogle Scholar
  51. Hidalgo P, Neely A. 2007. Multiplicity of protein interactions and functions of the voltage-gated calcium channel β-subunit. Cell calcium 42: 389–396.PubMedCrossRefGoogle Scholar
  52. Hildebrand M, David LS, Hamid J, Mulatz K, Garcia E, et al. 2007. Selective inhibition of CaV3.3 T-type calcium channels by Gαq/11-coupled muscarinic acetylcholine receptors. J Biol Chem 282: 21043–21055.PubMedCrossRefGoogle Scholar
  53. Hille B. 2001. Ion channels of excitable membranes, 3rd edition. Sinauer Associates, Sunderland, MA.Google Scholar
  54. Hille B. 1994. Modulation of ion-channel function by G-protein-coupled receptors. Trends in Neurosci 17: 531–536.CrossRefGoogle Scholar
  55. Holz GGT, Dunlap K, Kream RM. 1988. Characterization of the electrically evoked release of substance P from dorsal root ganglion neurons: Methods and dihydropyridine sensitivity. J Neurosci 8: 463–471.PubMedGoogle Scholar
  56. Iftinca M, Hamid J, Chen L, Varela D, Tadayonnejad R, et al. 2007. Regulation of T-type calcium channels by Rho-associated kinase. Nat Neurosci 10: 854–860.PubMedCrossRefGoogle Scholar
  57. Ikeda SR. 1996. Voltage-dependent modulation of N-type calcium channels by G-protein βγ subunits. Nature 380: 255–258.PubMedCrossRefGoogle Scholar
  58. Ino M, Yoshinaga T, Wakamori M, Miyamoto N, Takahashi E, et al. 2001. Functional disorders of the sympathetic nervous system in mice lacking the α1B subunit (CaV 2.2) of N-type calcium channels. Proc Natl Acad Sci USA 98: 5323–5328.PubMedCrossRefGoogle Scholar
  59. Iwasaki S, Momiyama A, Uchitel OD., Takahashi T. 2000. Developmental changes in calcium channel types mediating central synaptic transmission. J Neurosci 20: 59–65.PubMedGoogle Scholar
  60. Iwasaki S, Takahashi T. 1998. Developmental changes in calcium channel types mediating synaptic transmission in rat auditory brainstem. J Physiol 509: 419–423.PubMedCrossRefGoogle Scholar
  61. Jahnsen H, Llinás R. 1984. Ionic basis for the electro-responsiveness and oscillatory properties of guinea-pig thalamic neurones in vitro. J Physiol 349: 227–427.PubMedGoogle Scholar
  62. Jing X, Li DQ, Olofsson CS, Salehi A, Surve VV, et al. 2005. CaV2.3 calcium channels control second-phase insulin release. J Clin Invest 115: 146–154.PubMedGoogle Scholar
  63. Jones SW, Marks TN. 1989. Calcium currents in bullfrog sympathetic neurons. II. Inactivation J Gen Physiol 94: 169–182.PubMedCrossRefGoogle Scholar
  64. Jun K, Piedras-Rentería ES, Smith SM, Wheeler DB, Lee, SB, et al. 1999. Ablation of P/Q-type Ca2+ channel currents, altered synaptic transmission, and progressive ataxia in mice lacking the α1A subunit. Proc Natl Acad Sci USA 96: 15245–15250.PubMedCrossRefGoogle Scholar
  65. Kang HW, Park JY, Jeong SW, Kim JA, Moon HJ, et al. 2006. A molecular determinant of nickel inhibition in CaV3.2 T-type calcium channels. J Biol Chem 281: 4823–4830.PubMedCrossRefGoogle Scholar
  66. Kerr LM, Filloux F, Olivera BM, Jackson H, Wamsley JK. 1988. Autoradiographic localization of calcium channels with [125I]ω-conotoxin in rat brain. Eur J Pharmacol 146: 181–183.PubMedCrossRefGoogle Scholar
  67. Kim MS, Morii T, Sun LX, Imoto K, Mori Y. 1993. Structural determinants of ion selectivity in brain calcium channel. FEBS Lett 318: 145–148.PubMedCrossRefGoogle Scholar
  68. Kiyonaka S, Wakamori M, Miki T, Uriu Y, Nonaka M, et al. 2007. RIM1 confers sustained activity and neurotransmitter vesicle anchoring to presynaptic Ca2+ channels. Nat Neurosci 10: 691–701.PubMedCrossRefGoogle Scholar
  69. Klöckner U, Lee JH, Cribbs LL, Daud A, Hescheler J, et al. 1999. Comparison of the Ca2+ currents induced by expression of three cloned α1 subunits, α1G, α1H and α1I, of low-voltage-activated T-type Ca2+ channels. Eur J Neurosci 11: 4171–4178.PubMedCrossRefGoogle Scholar
  70. Klöckner U, Pereverzev A, Leroy J, Krieger A, Vajna R, et al. 2004. The cytosolic II-III loop of CaV2.3 provides an essential determinant for the phorbol ester-mediated stimulation of E-type Ca2+ channel activity. Eur J Neurosci 19: 2659–2668.PubMedCrossRefGoogle Scholar
  71. Konda T, Enomoto A, Matsushita J, Takahara A, Moriyama T. 2005. The N- and L-type calcium channel blocker cilnidipine suppresses renal injury in dahl rats fed a high-sucrose diet, an experimental model of metabolic syndrome. Nephron Physiol 101: 1–13.CrossRefGoogle Scholar
  72. Kubota M, Murakoshi T, Saegusa H, Kazuno A, Zong S, et al. 2001. Intact LTP and fear memory but impaired spatial memory in mice lacking Cav2.3 (α1E) channel. Biochem Biophys Res Commun 282: 242–248.PubMedCrossRefGoogle Scholar
  73. Kulik A, Nakadate K, Hagiwara A, Fukazawa Y, Luján R, et al. 2004. Immunocytochemical localization of the α1A subunit of the P/Q-type calcium channel in the rat cerebellum. Eur J Neurosci 19: 2169–2178.PubMedCrossRefGoogle Scholar
  74. Kuzmiski JB, Barr W, Zamponi GW, Macvicar BA. 2005. Topiramate inhibits the initiation of plateau potentials in CA1 neurons by depressing R-type calcium channels. Epilepsia 46: 481–489.PubMedCrossRefGoogle Scholar
  75. Larkum ME, Kaiser MM, Sakmann B. 1999. Calcium electrogenesis in distal apical dendrites of layer five pyramidal cells at a critical frequency of back-propagating action potentials. Proc Natl Acad Sci USA 96: 14600–14604.PubMedCrossRefGoogle Scholar
  76. Lee JH, Cribbs LL, Perez-Reyes E. 1999. Cloning of a novel four repeat protein related to voltage-gated sodium and calcium channels. FEBS Lett 445: 231–236.PubMedCrossRefGoogle Scholar
  77. Lee SC, Choi S, Lee T, Kim HL, Chin H, et al. 2002. Molecular basis of R-type calcium channels in central amygdala neurons of the mouse. Proc Natl Acad Sci USA 99: 3276–3281.PubMedCrossRefGoogle Scholar
  78. Leroy J, Pereverzev A, Vajna R, Qin N, Pfitzer G, et al. 2003. Ca2+-sensitive regulation of E-type Ca2+ channel activity depends on an arginine-rich region in the cytosolic II-III loop. Eur J Neurosci 18: 841–855.PubMedCrossRefGoogle Scholar
  79. Letts VA, Felix R, Biddlecome GH, Arikkath J, Mahaffey CL, et al. 1998. The mouse stargazer gene encodes a neuronal Ca2+-channel γ subunit. Nat Genetics 19: 340–347.CrossRefGoogle Scholar
  80. Liang, H, Demaria CD, Erickson MG, Mori MX, Alseikhan BA, et al. 2003. Unified mechanisms of Ca2+ regulation across the Ca2+ channel family. Neuron 39: 951–960.PubMedCrossRefGoogle Scholar
  81. Llinás R, Sugimori M, Lin JW, Cherksey B. 1989. Blocking and isolation of a calcium channel from neurons in mammals and cephalopods utilizing a toxin fraction (FTX) from funnel-web spider poison. Proc Natl Acad Sci USA 86: 1689–1693.PubMedCrossRefGoogle Scholar
  82. Lu B, Su Y, Das S, Liu J, Xia J, et al. 2007. The neuronal channel NALCN contributes resting sodium permeability and is required for normal respiratory rhythm. Cell 129: 371–383.PubMedCrossRefGoogle Scholar
  83. Lu ZJ, Pereverzev A, Liu HL, Weiergraber M, Henry M, et al. 2004. Arrhythmia in isolated prenatal hearts after ablation of the Cav2.3 (α1E) subunit of voltage-gated Ca2+ channels. Cell Physiol Biochem 14: 11–22.PubMedCrossRefGoogle Scholar
  84. Maggi CA, Tramontana M, Cecconi R, Santicioli P. 1990. Neurochemical evidence for the involvement of N-type calcium channels in transmitter secretion from peripheral endings of sensory nerves in guinea pigs. Neurosci Lett 114: 203–206.PubMedCrossRefGoogle Scholar
  85. Markrum H, Helm PJ, Sakmann, B. 1995. Dendritic calcium transients evoked by single back-propagating action potentials in rat neocortical pyramidal neurons. J Physiol 485: 1–20.Google Scholar
  86. Martella G, Spadoni F, Sciamanna G, Tassone A, Bernardi G, et al. 2008. Age-related functional changes of high-voltage-activated calcium channels in different neuronal subtypes of mouse striatum. Neurosci 152: 469–476.Google Scholar
  87. Melzer W, Andronache Z, Urse D. 2006. Functional roles of the gamma subunit of the skeletal muscle DHP-receptor. J Muscle Res Cell Motil 27: 307–314.PubMedCrossRefGoogle Scholar
  88. Metz AE, Jarsky T, Martina M, Spruston N. 2005. R-type calcium channels contribute to afterdepolarization and bursting in hippocampal CA1 pyramidal neurons. J Neurosci 25: 5763–5773.PubMedCrossRefGoogle Scholar
  89. Mintz IM, Venema VJ, Swiderek KM, Lee TD, Bean BP, et al. 1992. P-type calcium channels blocked by the spider toxin ω-Aga-IVA. Nature 355: 827–829.PubMedCrossRefGoogle Scholar
  90. Mori Y, Friedrich T, Kim MS, Mikami A, Nakai J, et al. 1991. Primary structure and functional expression from complementary DNA of a brain calcium channel. Nature 350: 398–402.PubMedCrossRefGoogle Scholar
  91. Mori Y, Wakamori M, Oda S, Fletcher CF, Sekiguchi N, et al. 2000. Reduced voltage sensitivity of activation of P/Q-type Ca2+ channels is associated with the ataxic mouse mutation rolling Nagoya (tgrol). J Neurosci 20: 5654–5662.PubMedGoogle Scholar
  92. Moss FJ, Viard P, Davies A, Bertaso F, Page KM., et al. 2002. The novel product of five-exon stargazin-related gene abolishes CaV2.2calcium channel expression. EMBO J 21: 1514–1523.PubMedCrossRefGoogle Scholar
  93. Newcomb R, Szoke B, Palma A, Wang G, Chen X, et al. 1998. Selective peptide antagonist of the class-E calcium channel from the venom of the tarantula Hysterocrates gigas. Biochem 37: 15353–15362.CrossRefGoogle Scholar
  94. Nilius B, Talavera K, Verkhratsky A. 2006. T-type calcium channels: The never ending story. Cell calcium 40: 81–88.PubMedCrossRefGoogle Scholar
  95. Noebels JL, Sidman, RL. 1979. Inherited epilepsy: Spike-wave and focal motor seizures in the mutant mouse tottering. Science 204: 1334–1336.PubMedCrossRefGoogle Scholar
  96. Nowycky MC, Fox AP, Tsien RW. 1985. Three types of neuronal calcium channel with different calcium agonist sensitivity. Nature 316: 440–443PubMedCrossRefGoogle Scholar
  97. Oliveria SF, DellAcqua ML, Sather WA. 2007. AKAP79/150 anchoring of calcineurin controls neuronal L-type Ca2+ channel activity and nuclear signaling. Neuron 55: 261–275.PubMedCrossRefGoogle Scholar
  98. Opatowsky Y, Che CC, Campbell KP, Hirsch JA. 2004. Structural analysis of the voltage-dependent calcium channel β subunit functional core and its complex with the α1 interaction domain. Neuron 42: 387–399.PubMedCrossRefGoogle Scholar
  99. Pereverzev A, Mikhna M, Vajna R, Gissel C, Henry M, et al. 2002. Disturbances in glucose-tolerance, insulin-release, and stress-induced hyperglycemia upon disruption of the Cav2.3 (α1E) subunit of voltage-gated Ca2+ channels. Mol Endocrinol 16: 884–895.PubMedCrossRefGoogle Scholar
  100. Perez-Reyes E. 2006. Molecular characterization of T-type calcium channels. Cell calcium 40: 89–96.PubMedCrossRefGoogle Scholar
  101. Perez-Reyes E, Cribbs LL, Daud A, Lacerda AE, Barclay J, et al. 1998. Molecular characterization of a neuronal low-voltage-activated T-type calcium channel. Nature 391: 896–900.PubMedCrossRefGoogle Scholar
  102. Plummer MR, Hess, P. 1991. Reversible uncoupling of inactivation in N-type calcium channels. Nature 351: 657–659.PubMedCrossRefGoogle Scholar
  103. Poncer JC, McKinney RA, Gähwiler BH, Thompson SM. 1997. Either N- or P-type calcium channels mediate GABA release at distinct hippocampal inhibitory synapses. Neuron 18: 463–472.PubMedCrossRefGoogle Scholar
  104. Puopolo M, Raviola E, Bean BP. 2007. Roles of subthreshold calcium current and sodium current in spontaneous firing of mouse midbrain dopamine neurons. J Neurosci 27: 645–656.PubMedCrossRefGoogle Scholar
  105. Raingo J, Castiglioni AJ, Lipscombe D. 2007. Alternative splicing controls G protein-dependent inhibition of N-type calcium channels in nociceptors. Nat Neurosci 10: 285–292.PubMedCrossRefGoogle Scholar
  106. Randall A, Tsien, RW. 1995. Pharmacological dissection of multiple types of Ca2+ channel currents in rat cerebellar granule neurons. J Neurosci 15: 2995–3012.PubMedGoogle Scholar
  107. Reid CA, Bekkers JM, Clements JD. 2003. Presynaptic Ca2+ channels: A functional patchwork. Trends Neurosci 26: 683–687.PubMedCrossRefGoogle Scholar
  108. Rosato Siri MD, Uchitel OD. 1999. Calcium channels coupled to neurotransmitter release at neonatal rat neuromuscular junctions. J Physiol 514: 533–540.PubMedCrossRefGoogle Scholar
  109. Sabatini BL, Svoboda K. 2000. Analysis of calcium channels in single spines using optical fluctuation analysis. Nature 408: 589–593.PubMedCrossRefGoogle Scholar
  110. Saegusa H, Kurihara T, Zong S, Minowa O, Kazuno A, et al. 2000. Altered pain responses in mice lacking alpha 1E subunit of the voltage- dependent Ca2+ channel. Proc Natl Acad Sci USA 97: 6132–6137.PubMedCrossRefGoogle Scholar
  111. Santicioli P, Del Bianco E, Tramontana M, Geppetti P, Maggi CA. 1992. Release of calcitonin gene-related peptide like-immunoreactivity induced by electrical field stimulation from rat spinal afferents is mediated by conotoxin-sensitive calcium channels. Neurosci Lett 136: 161–164.PubMedCrossRefGoogle Scholar
  112. Scroggs RS, Fox AP. 1991. Distribution of dihydropyridine and ω-conotoxin-sensitive calcium currents in acutely isolated rat and frog sensory neuron somata: Diameter-dependent L channel expression in frog. J Neurosci 11: 1334–1346.PubMedGoogle Scholar
  113. Sidach SS, Mintz IM. 2002. Kurtoxin, a gating modifier of neuronal high- and low-threshold Ca channels. J Neurosci 22: 2023–2034.PubMedGoogle Scholar
  114. Soong TW, Stea A, Hodson CD, Dubel SJ, Vincent SR, et al. 1993. Structure and functional expression of a member of the low voltage-activated calcium channel family. Science 260: 1133–1136.PubMedCrossRefGoogle Scholar
  115. Stea A, Tomlinson WJ, Soong TW, Bourinet E, Dubel SJ, et al. 1994. 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: 10576–10580.PubMedCrossRefGoogle Scholar
  116. Takahashi M, Seagar MJ, Jones JF, Reber BF, Catterall WA. 1987. Subunit structure of dihydropyridine-sensitive calcium channels from skeletal muscle. Proc Natl Acad Sci USA 84: 5478–5482.PubMedCrossRefGoogle Scholar
  117. Talley EM, Cribbs LL, Lee JH, Daud A, Perez-Reyes E, et al. 1999. Differential distribution of three members of a gene family encoding low voltage-activated (T-type) calcium channels. J Neurosci 19: 1895–1911.PubMedGoogle Scholar
  118. Tanabe T, Takeshima H, Mikami A, Flockerzi V, Takahashi H, et al. 1987. Primary structure of the receptor for calcium channel blockers from skeletal muscle. Nature 328: 313–318.PubMedCrossRefGoogle Scholar
  119. Toriyama H, Wang L, Saegusa H, Zong S, Osanai M, et al. 2002. Role of Cav 2.3 (α1E) Ca2+ channel in ischemic neuronal injury. Neuroreport 13: 261–265.PubMedCrossRefGoogle Scholar
  120. Tsujimoto T, Jeromin A, Saitoh N, Roder JC, Takahashi T. 2002. Neuronal calcium sensor 1 and activity-dependent facilitation of P/Q-type calcium currents at presynaptic nerve terminals. Science 295: 2276–2279.PubMedCrossRefGoogle Scholar
  121. Tunemi T, Saegusa H, Ishikawa K, Nagayama S, Murakoshi T., et al. 2002. Novel CaV2.1 splice variants isolated from Purkinje cells do not generate P-type Ca2+ current. J Biol Chem 277: 7214–7221.CrossRefGoogle Scholar
  122. Uchitel OD, Protti DA, Sanchez V, Cherksey BD, Sugimori M, et al. 1992. P-type voltage-dependent calcium channel mediates presynaptic calcium influx and transmitter release in mammalian synapses. Proc Natl Acad Sci USA 89: 3330–3333.PubMedCrossRefGoogle Scholar
  123. Vanegas H, Schaible H. 2000. Effects of antagonists to high-threshold calcium channels upon spinal mechanisms of pain, hyperalgesia and allodynia. Pain 85: 9–18.PubMedCrossRefGoogle Scholar
  124. Vendel AC, Rithner CD, Lyons BA, Horne WA. 2006. Solution structure of the N-terminal A domain of the human voltage-gated Ca2+ channel β4a subunit. Protein Sci 15: 378–383.PubMedCrossRefGoogle Scholar
  125. Wakamori M, Niidome T, Furutama D, Furuichi T, Mikoshiba K, et al. 1994. Distinctive functional properties of the neuronal BII (class E) calcium channel. Receptors Channels 2: 303–314.PubMedGoogle Scholar
  126. Wakamori M, Yamazaki K, Matsunodaira H, Teramoto T, Tanaka I, et al. 1998. Single tottering mutations responsible for the neuropathic phenotype of the P-type calcium channel. J Biol Chem 273: 34857–34867.PubMedCrossRefGoogle Scholar
  127. Weiergraber M, Henry M, Krieger A, Kamp M, Radhakrishnan K, et al. 2006. Altered seizure susceptibility in mice lacking the Cav2.3 E-type Ca2+ channel. Epilepsia 47: 839–850.PubMedCrossRefGoogle Scholar
  128. Weiergraber M, Henry M, Sudkamp M, DeVivie ER, Hescheler J, et al. 2005. Ablation of Cav2.3/E-type voltage-gated calcium channel results in cardiac arrhythmia and altered autonomic control within the murine cardiovascular system. Basic Res Cardiol 100: 1–13.PubMedCrossRefGoogle Scholar
  129. Weiss N, Arnoult C, DeWaard M. 2006. Contribution of the kinetics of G protein dissociation to the characteristic modifications of N-type calcium channel activity. Neurosci Res 56: 332–343.PubMedCrossRefGoogle Scholar
  130. Westenbroek RE, Babcock DF. 1999. Discrete regional distributions suggest diverse functional roles of calcium channel alpha1 subunits in sperm. Dev Biol 207: 457–469.PubMedCrossRefGoogle Scholar
  131. Wheeler DB, Randall A, Tsien RW. 1994. Roles of N-type and Q-type Ca2+ channels in supporting hippocampal synaptic transmission. Science 264: 107–111.PubMedCrossRefGoogle Scholar
  132. Wilson SM, Toth PT, Oh SB, Gillard SE, Volsen S, et al. 2000. The status of voltage-dependent calcium channel in α1E knock-out mice. J Neurosci 20: 8566–8571.PubMedGoogle Scholar
  133. Wu LG, Westenbroek RE, Borst JGG, Catterall WA, Sakmann B. 1999. Calcium channel types with distinct presynaptic localization couple differentially to transmitter release in single calyx-type synapses. J Neurosci 19: 726–736.PubMedGoogle Scholar
  134. Xu J, Clancy CE. 2008. Ionic mechanisms of endogenous bursting in CA3 hippocampal pyramidal neurons: A model study. PloS ONE 3: e2056.PubMedCrossRefGoogle Scholar
  135. Zaitsev AV, Povysheva DA, Lewis DA., Krimer LS. 2007. P/Q-type, but not N-type, calcium channels mediate GABA release from fast-spiking interneurons to pyramidal cells in rat prefrontal cortex. J Neurophysiol 97: 3567–3573.PubMedCrossRefGoogle Scholar
  136. Zhong H, Yokoyama CT, Scheuer T, Catterall WA. 1999. Reciprocal regulation of P/Q-type Ca2+ channels by SNAP-25, syntaxin and synaptotagmin. Nat Neurosci 2: 939–941.PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  • M. Wakamori
  • K. Imoto

There are no affiliations available

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