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ISSN 2522-9028 (Print)
ISSN 2522-9036 (Online)
DOI: https://doi.org/10.15407/fz

Fiziologichnyi Zhurnal

is a scientific journal issued by the

Bogomoletz Institute of Physiology
National Academy of Sciences of Ukraine

Editor-in-chief: V.F. Sagach

The journal was founded in 1955 as
1955 – 1977 "Fiziolohichnyi zhurnal" (ISSN 0015 – 3311)
1978 – 1993 "Fiziologicheskii zhurnal" (ISSN 0201 – 8489)
1994 – 2016 "Fiziolohichnyi zhurnal" (ISSN 0201 – 8489)
2017 – "Fiziolohichnyi zhurnal" (ISSN 2522-9028)

Fiziol. Zh. 2016; 62(4): 84-94

VOLTAGE-GATED CALCIUM CHANNELS: CLASSIFICATION AND PHARMACOLOGICAL PROPERTIES (PART I)

O. Iegorova1, O. Maximyuk1,2, A. Fisyunov1, O. Krishtal1,2

  1. Bogomoletz Institute of Physiology National Academy of Sciences of Ukraine, Kyiv
  2. International Center for Molecular Physiology National Academy of Sciences of Ukraine, Kyiv
DOI: https://doi.org/10.15407/fz62.04.084

Abstract

Calcium influx though voltage-gated calcium channels mediate a huge amount of physiological events and cellular responses. Numerous scientific reports indicate that calcium channels are involved in synaptic transmission, neurotransmitter release, regulation of gene expression, cellular membrane voltage oscillations, pacemaker activity, secretion of specific substances from nerve and secretory cells, morphological differentiation, activation of calcium-dependent enzymes, etc. This review represents the modern classification, molecular structure, physiological and pharmacological properties of voltage-gated calcium channels expressed in mammalian cells.

Keywords: voltage-gated calcium channels, pharmacology, molecular structure.

Full text: (PDF, in Ukrainian)

References

  1. Kostyuk P. Calcium ions in nerve cell function. Oxford:Oxford University Press; 1992.
    2.  
  2. Hodgkin AL, Huxley AF. A quantitative description ofmembrane current and its application to conduction andexcitation in nerve. J Physiol. 1952;117(4):500-44. CrossRef  
  3. Fatt P, Katz B. The electrical properties of crustaceanmuscle fibres. J Physiol. 1953;120(1-2):171-204. CrossRef PubMed PubMedCentral
    4.  
  4. Fatt P, Ginsborg BL. The ionic requirements for theproduction of action potentials in crustacean muscle fibres.J Physiol. 1958;142(3):516-43. CrossRef PubMed PubMedCentral
    5.  
  5. Hagiwara S, Nakajima S. Effects of the intracellular Caion concentration upon the excitability of the muscle fibermembrane of a barnacle. J Gen Physiol. 1966;49(4):807-18. CrossRef PubMed PubMedCentral
    6.  
  6. Reuter H. The dependence of slow inward current inPurkinje fibres on the extracellular calcium-concentration.J Physiol. 1967;192(2):479-92. CrossRef PubMed PubMedCentral
    7.  
  7. Reuter H. Divalent cations as charge carriers in excitablemembranes. Prog Biophys Mol Biol. 1973;26:1-43. CrossRef  
  8. Birnbaumer L, Campbell KP, Catterall WA, Harpold MM,Hofmann F, Horne WA, et al. The naming of voltage-gatedcalcium channels. Neuron. 1994;13(3):505-6. CrossRef  
  9. Kostyuk PG, Krishtal OA, Doroshenko PA. Calciumcurrents in snail neurones. I. Identification of calciumcurrent. Pflugers Arch. 1974;348(2):83-93. CrossRef PubMed
    10.  
  10. Trautwein W, McDonald TF, Tripathi O. Calciumconductance and tension in mammalian ventricular muscle.Pflugers Arch. 1975;354(1):55-74. CrossRef PubMed
    11.  
  11. Doroshenko PA, Kostiuk PG, Kryshtal OA. [Action ofcalcium on the somatic membrane of the giant neuronsof molluscs]. Neirofiziologiia. 1973;5(6):621-7.[Articlein Russian] PubMed
    12.  
  12. Kostyuk PG, Krishtal OA, Pidoplichko VI. Intracellularperfusion. J Neurosci Methods. 1981;4(3):201-10. CrossRef  
  13. Kostyuk PG, Krishtal OA, Shakhovalov YA. Separationof sodium and calcium currents in the somatic membraneof mollusc neurones. J Physiol. 1977;270(3):545-68. CrossRef PubMed PubMedCentral
    14.  
  14. Reuter H. Localization of beta adrenergic receptors, andeffects of noradrenaline and cyclic nucleotides on actionpotentials, ionic currents and tension in mammaliancardiac muscle. J Physiol. 1974;242(2):429-51. CrossRef PubMed PubMedCentral
    15.  
  15. Tsien RW. Adrenaline-like effects of intracellulariontophoresis of cyclic AMP in cardiac Purkinje fibres.Nat New Biol. 1973;245(143):120-2. CrossRef PubMed
    16.  
  16. Fedulova SA, Kostyuk PG, Veselovsky NS. Calciumchannels in the somatic membrane of the rat dorsalroot ganglion neurons, effect of cAMP. Brain Res.1981;214(1):210-4. CrossRef  
  17. Neher E, Sakmann B. Single-channel currents recordedfrom membrane of denervated frog muscle fibres. Nature.1976;260(5554):799-802. CrossRef PubMed
    18.  
  18. Hosey MM, Chang FC, O'Callahan CM, Ptasienski J.L-type calcium channels in cardiac and skeletal muscle.Purification and phosphorylation. Ann N Y Acad Sci.1989;560:27-38. CrossRef PubMed
    19.  
  19. Stea A, Soong TW, Snutch TP. The voltage-gated calciumchannels. In: North R, editor. Handbook of Receptors andChannels; Ligand- and Voltage-Gated Ion Channels: BocaRaton, Florida:CRC Press Inc.; 1995. p. 113-52. PubMed
    20.  
  20. Perez-Reyes E, Cribbs LL, Daud A, Lacerda AE, BarclayJ, Williamson MP, et al. Molecular characterization of aneuronal low-voltage-activated T-type calcium channel.Nature. 1998;391(6670):896-900. CrossRef PubMed
    21.  
  21. Catterall WA. Voltage-gated calcium channels. ColdSpring Harb Perspect Biol. 2011;3(8). CrossRef PubMed PubMedCentral
    22.  
  22. Dolphin AC. The G.L. Brown Prize Lecture. Voltagedependentcalcium channels and their modulationby neurotransmitters and G-proteins. Exp Physiol.1995;80(1):1-36. CrossRef  
  23. Carbone E, Lux HD. A low voltage-activated calciumconductance in embryonic chick sensory neurons. BiophysJ. 1984;46(3):413-8. CrossRef  
  24. Kostyuk PG, Shuba Ya M, Savchenko AN. Three typesof calcium channels in the membrane of mouse sensoryneurons. Pflugers Arch. 1988;411(6):661-9. CrossRef PubMed
    25.  
  25. Nowycky MC, Fox AP, Tsien RW. Three types of neuronalcalcium channel with different calcium agonist sensitivity.Nature. 1985;316(6027):440-3. CrossRef PubMed
    26.  
  26. Olivera BM, Gray WR, Zeikus R, McIntosh JM, Varga J,Rivier J, et al. Peptide neurotoxins from fish-hunting conesnails. Science. 1985;230(4732):1338-43. CrossRef PubMed
    27.  
  27. Aosaki T, Kasai H. Characterization of two kinds of highvoltage-activatedCa-channel currents in chick sensoryneurons. Differential sensitivity to dihydropyridines and w-conotoxin GVIA. Pflugers Arch. 1989;414(2):150-6. CrossRef PubMed
    28.  
  28. Ferroni A, Mancinelli E, Camagni S, Wanke E. Twohigh voltage-activated calcium currents are present inisolation in adult rat spinal neurons. Biochem BiophysRes Commun. 1989;159(2):379-84. CrossRef  
  29. Llinas R, Sugimori M, Lin JW, Cherksey B. Blocking andisolation of a calcium channel from neurons in mammalsand cephalopods utilizing a toxin fraction (FTX) fromfunnel-web spider poison. Proc Natl Acad Sci U S A.1989;86(5):1689-93. CrossRef PubMed PubMedCentral
    30.  
  30. Snutch TP, Reiner PB. Ca2+ channels: diversity of formand function. Curr Opin Neurobiol. 1992;2(3):247-53. CrossRef  
  31. Ertel EA, Campbell KP, Harpold MM, Hofmann F, MoriY, Perez-Reyes E, et al. Nomenclature of voltage-gatedcalcium channels. Neuron. 2000;25(3):533-5. CrossRef  
  32. Tsien RW, Ellinor PT, Horne WA. Molecular diversity ofvoltage-dependent Ca2+ channels. Trends Pharmacol Sci.1991;12(9):349-54. CrossRef  
  33. Albillos A, Artalejo AR, Lopez MG, Gandia L, Garcia AG,Carbone E. Calcium channel subtypes in cat chromaffincells. J Physiol. 1994;477(Pt 2):197-213. CrossRef PubMed PubMedCentral
    34.  
  34. Fedulova SA, Kostyuk PG, Veselovsky NS. Two types ofcalcium channels in the somatic membrane of new-born ratdorsal root ganglion neurones. J Physiol. 1985;359:431-46. CrossRef PubMed PubMedCentral
    35.  
  35. Fenwick EM, Marty A, Neher E. Sodium and calciumchannels in bovine chromaffin cells. J Physiol. 1982;331:599-635. CrossRef PubMed PubMedCentral
    36.  
  36. Carbone E, Lux HD. Kinetics and selectivity of a lowvoltage-activatedcalcium current in chick and rat sensoryneurones. J Physiol. 1987;386:547-70. CrossRef PubMed PubMedCentral
    37.  
  37. Matteson DR, Armstrong CM. Properties of two types ofcalcium channels in clonal pituitary cells. J Gen Physiol.1986;87(1):161-82. CrossRef  
  38. Lux HD, Carbone E, Zucker H. Na+ currents throughlow-voltage-activated Ca2+ channels of chick sensoryneurones: block by external Ca2+ and Mg2+. J Physiol.1990;430:159-88. CrossRef PubMed PubMedCentral
    39.  
  39. Fox AP, Nowycky MC, Tsien RW. Kinetic and pharmacologicalproperties distinguishing three types ofcalcium currents in chick sensory neurones. J Physiol.1987;394:149-72. CrossRef PubMed PubMedCentral
    40.  
  40. Bean BP. Two kinds of calcium channels in canineatrial cells. Differences in kinetics, selectivity, andpharmacology. J Gen Physiol. 1985;86(1):1-30. CrossRef PubMed
    41.  
  41. Carbone E, Lux HD. Single low-voltage-activated calciumchannels in chick and rat sensory neurones. J Physiol.1987;386:571-601. CrossRef PubMed PubMedCentral
    42.  
  42. Narahashi T, Tsunoo A, Yoshii M. Characterization of twotypes of calcium channels in mouse neuroblastoma cells.J Physiol. 1987;383:231-49. CrossRef PubMed PubMedCentral
    43.  
  43. Akaike N, Kostyuk PG, Osipchuk YV. Dihydropyridinesensitivelow-threshold calcium channels in isolated rathypothalamic neurones. J Physiol. 1989;412:181-95. CrossRef PubMed PubMedCentral
    44.  
  44. Tang CM, Presser F, Morad M. Amiloride selectivelyblocks the low threshold (T) calcium channel. Science.1988;240(4849):213-5. CrossRef PubMed
    45.  
  45. Yaari Y, Hamon B, Lux HD. Development of two typesof calcium channels in cultured mammalian hippocampalneurons. Science. 1987;235(4789):680-2. CrossRef PubMed
    46.  
  46. Carbone E, Swandulla D. Neuronal calcium channels:kinetics, blockade and modulation. Prog Biophys MolBiol. 1989;54(1):31-58. CrossRef  
  47. Bean BP. Classes of calcium channels in vertebrate cells.Annu Rev Physiol. 1989;51:367-84. CrossRef PubMed
    48.  
  48. Lopez MG, Villarroya M, Lara B, Martinez Sierra R,Albillos A, Garcia AG, et al. Q- and L-type Ca2+ channelsdominate the control of secretion in bovine chromaffincells. FEBS Lett. 1994;349(3):331-7. CrossRef  
  49. Plant TD. Properties and calcium-dependent inactivationof calcium currents in cultured mouse pancreatic B-cells.J Physiol. 1988;404:731-47. CrossRef PubMed PubMedCentral
    50.  
  50. Madison DV, Nicoll RA. Control of the repetitive dischargeof rat CA 1 pyramidal neurones in vitro. J Physiol.1984;354:319-31. CrossRef  
  51. Platzer J, Engel J, Schrott-Fischer A, Stephan K, BovaS, Chen H, et al. Congenital deafness and sinoatrial nodedysfunction in mice lacking class D L-type Ca2+ channels.Cell. 2000;102(1):89-97. CrossRef  
  52. Bech-Hansen NT, Naylor MJ, Maybaum TA, Pearce WG,Koop B, Fishman GA, et al. Loss-of-function mutations ina calcium-channel alpha1-subunit gene in Xp11.23 causeincomplete X-linked congenital stationary night blindness.Nat Genet. 1998;19(3):264-7. CrossRef PubMed
    53.  
  53. Striessnig J, Bolz HJ, Koschak A. Channelopathies inCav1.1, Cav1.3, and Cav1.4 voltage-gated L-type Ca2+channels. Pflugers Arch. 2010;460(2):361-74. CrossRef PubMed PubMedCentral
    54.  
  54. Swandulla D, Armstrong CM. Fast-deactivating calciumchannels in chick sensory neurons. J Gen Physiol.1988;92(2):197-218. CrossRef PubMed
    55.  
  55. Eckert R, Chad JE. Inactivation of Ca channels. ProgBiophys Mol Biol. 1984;44(3):215-67. CrossRef  
  56. Durroux T, Gallo-Payet N, Payet MD. Three componentsof the calcium current in cultured glomerulosa cells fromrat adrenal gland. J Physiol. 1988;404:713-29. CrossRef PubMed PubMedCentral
    57.  
  57. Konnerth A, Dreessen J, Augustine GJ. Brief dendriticcalcium signals initiate long-lasting synaptic depressionin cerebellar Purkinje cells. Proc Natl Acad Sci U S A.1992;89(15):7051-5. CrossRef PubMed PubMedCentral
    58.  
  58. Lee KS, Tsien RW. Mechanism of calcium channel blockadeby verapamil, D600, diltiazem and nitrendipine in singledialysed heart cells. Nature. 1983;302(5911):790-4. CrossRef  
  59. Kostyuk PG, Krishtal OA, Pidoplichko VI. Calciuminward current and related charge movements in themembrane of snail neurones. J Physiol. 1981;310:403-21. CrossRef PubMed PubMedCentral
    60.  
  60. Kostyuk PG. Calcium channels in the neuronal membrane.Biochim Biophys Acta. 1981;650(2-3):128-50. CrossRef  
  61. Hirning LD, Fox AP, McCleskey EW, Olivera BM,Thayer SA, Miller RJ, et al. Dominant role of N-typeCa2+ channels in evoked release of norepinephrine fromsympathetic neurons. Science. 1988;239(4835):57-61. CrossRef PubMed
    62.  
  62. Regan LJ, Sah DW, Bean BP. Ca2+ channels in rat centraland peripheral neurons: high-threshold current resistantto dihydropyridine blockers and w-conotoxin. Neuron.1991;6(2):269-80. CrossRef  
  63. Carbone E, Sher E, Clementi F. Ca currents in humanneuroblastoma IMR32 cells: kinetics, permeability andpharmacology. Pflugers Arch. 1990; 416(1-2):170-9. CrossRef PubMed
    64.  
  64. Dupont JL, Bossu JL, Feltz A. Effect of internal calciumconcentration on calcium currents in rat sensory neurones.Pflugers Arch. 1986; 406(4):433-5. CrossRef PubMed
    65.  
  65. Wanke E, Ferroni A, Malgaroli A, Ambrosini A, PozzanT, Meldolesi J. Activation of a muscarinic receptorselectively inhibits a rapidly inactivated Ca2+ currentin rat sympathetic neurons. Proc Natl Acad Sci U S A.1987;84(12):4313-7. CrossRef PubMed PubMedCentral
    66.  
  66. Williams ME, Feldman DH, McCue AF, Brenner R,Velicelebi G, Ellis SB, et al. Structure and functionalexpression of alpha 1, alpha 2, and beta subunits of anovel human neuronal calcium channel subtype. Neuron.1992;8(1):71-84. CrossRef  
  67. Plummer MR, Logothetis DE, Hess P. Elementaryproperties and pharmacological sensitivities of calciumchannels in mammalian peripheral neurons. Neuron.1989;2(5):1453-63. CrossRef  
  68. McCleskey EW, Fox AP, Feldman DH, Cruz LJ, OliveraBM, Tsien RW, et al. Omega-conotoxin: direct andpersistent blockade of specific types of calcium channelsin neurons but not muscle. Proc Natl Acad Sci U S A.1987;84(12):4327-31. CrossRef PubMed PubMedCentral
    69.  
  69. Tsien RW, Lipscombe D, Madison DV, Bley KR, FoxAP. Multiple types of neuronal calcium channels and theirselective modulation. Trends Neurosci. 1988;11(10):431-8. CrossRef  
  70. Mintz IM, Adams ME, Bean BP. P-type calciumchannels in rat central and peripheral neurons. Neuron.1992;9(1):85-95. CrossRef  
  71. Wakamori M, Yamazaki K, Matsunodaira H, TeramotoT, Tanaka I, Niidome T, et al. Single tottering mutationsresponsible for the neuropathic phenotype of the P-typecalcium channel. J Biol Chem. 1998; 273(52):34857-67. CrossRef PubMed
    72.  
  72. Regan LJ. Voltage-dependent calcium currents inPurkinje cells from rat cerebellar vermis. J Neurosci.1991;11(7):2259-69. PubMed
    73.  
  73. Usowicz MM, Sugimori M, Cherksey B, Llinas R. P-typecalcium channels in the somata and dendrites of adultcerebellar Purkinje cells. Neuron. 1992;9(6):1185-99. CrossRef  
  74. Sather WA, Tanabe T, Zhang JF, Mori Y, Adams ME,Tsien RW. Distinctive biophysical and pharmacologicalproperties of class A (BI) calcium channel a1 subunits.Neuron. 1993;11(2):291-303. CrossRef  
  75. Randall A, Tsien RW. Pharmacological dissection ofmultiple types of Ca2+ channel currents in rat cerebellargranule neurons. J Neurosci. 1995;15(4):2995-3012. PubMed
    76.  
  76. Zhang JF, Randall AD, Ellinor PT, Horne WA, SatherWA, Tanabe T, et al. Distinctive pharmacology andkinetics of cloned neuronal Ca2+ channels and theirpossible counterparts in mammalian CNS neurons.Neuropharmacology. 1993;32(11):1075-88. CrossRef  
  77. Wheeler DB, Randall A, Tsien RW. Roles of N-type andQ-type Ca2+ channels in supporting hippocampal synaptictransmission. Science. 1994;264(5155):107-11. CrossRef PubMed
    78.  
  78. Ellinor PT, Zhang JF, Randall AD, Zhou M, SchwarzTL, Tsien RW, et al. Functional expression of arapidly inactivating neuronal calcium channel. Nature.1993;363(6428):455-8. CrossRef PubMed
    79.  
  79. Toro-Castillo C, Thapliyal A, Gonzalez-Ochoa H, AdamsBA, Meza U. Muscarinic modulation of Cav2.3 (R-type)calcium channels is antagonized by RGS3 and RGS3T.Am J Physiol Cell Physiol. 2007;292(1):C573-80. CrossRef PubMed
    80.  
  80. Randall AD, Tsien RW. Contrasting biophysical andpharmacological properties of T-type and R-type calciumchannels. Neuropharmacology. 1997;36(7):879-93. CrossRef  
  81. Williams ME, Marubio LM, Deal CR, Hans M, BrustPF, Philipson LH, et al. Structure and functionalcharacterization of neuronal a1E calcium channel subtypes.J Biol Chem. 1994;269(35):22347-57. PubMed
    82.  
  82. Schneider T, Wei X, Olcese R, Costantin JL, NeelyA, Palade P, et al. Molecular analysis and functionalexpression of the human type E neuronal Ca2+ channelalpha 1 subunit. Recept Channels. 1994;2(4):255-70. PubMed
    83.  
  83. Soong TW, Stea A, Hodson CD, Dubel SJ, Vincent SR,Snutch TP. Structure and functional expression of amember of the low voltage-activated calcium channelfamily. Science. 1993;260(5111):1133-6. CrossRef PubMed
    84.  
  84. Day NC, Shaw PJ, McCormack AL, Craig PJ, SmithW, Beattie R, et al. Distribution of a1A, a1B and a1Evoltage-dependent calcium channel subunits in the humanhippocampus and parahippocampal gyrus. Neuroscience.1996;71(4):1013-24. CrossRef  
  85. Elliott EM, Malouf AT, Catterall WA. Role of calciumchannel subtypes in calcium transients in hippocampalCA3 neurons. J Neurosci. 1995;15(10):6433-44. PubMed
    86.  
  86. Ikeda SR. Voltage-dependent modulation of N-typecalcium channels by G-protein bg subunits. Nature.1996;380(6571):255-8. CrossRef PubMed
    87.  
  87. Martin-Moutot N, Charvin N, Leveque C, Sato K, NishikiT, Kozaki S, et al. Interaction of SNARE complexes withP/Q-type calcium channels in rat cerebellar synaptosomes.J Biol Chem. 1996;271(12):6567-70. CrossRef PubMed
    88.  

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