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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. 2017; 63(3): 49-57


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

O. Iegorova, O. Maximyuk, A. Fisyunov, O. Krishtal

    Bogomoletz Institute of Physiology NAS of Ukraine, Kyiv
DOI: https://doi.org/10.15407/fz63.03.049

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

References

  1. Romanin C, Grosswagen P, Schindler H. Calpastatin and nucleotides stabilize cardiac calcium channel activity in excised patches. Pflugers Arch. 1991;418(1–2):86–92. CrossRef PubMed
  2.  
  3. Iegorova O, O. M, Fisyunov A, Krishtal O. Voltage-gated calcium channels: classification and pharmacological properties (part I). Fiziol Zh. 2016;62(4):84–94. CrossRef  
  4. Fedulova SA, Kostyuk PG, Veselovsky NS. Calcium channels in the somatic membrane of the rat dorsal root ganglion neurons, effect of cAMP. Brain Res.1981;214(1):210–4. CrossRef  
  5. Fedulova SA, Kostyuk PG, Veselovsky NS. Two types of calcium channels in the somatic membrane of new-born rat dorsal root ganglion neurones. J Physiol. 1985;359:431–46. CrossRef PubMed PubMedCentral
  6.  
  7. Erdemli G, Xu YZ, Krnjevic K. Potassium conductance causing hyperpolarization of CA1 hippocampal neurons during hypoxia. J Neurophysiol. 1998;80(5):2378–90. PubMed
  8.  
  9. Osterrieder W, Brum G, Hescheler J, Trautwein W, Flockerzi V, Hofmann F. Injection of subunits of cyclic AMP-dependent protein kinase into cardiac myocytes modulates Ca2+ current. Nature. 1982;298(5874):576–8. CrossRef PubMed
  10.  
  11. Brum G, Flockerzi V, Hofmann F, Osterrieder W, Trautwein W. Injection of catalytic subunit of cAMPdependent protein kinase into isolated cardiac myocytes. Pflugers Arch. 1983;398(2):147–54. CrossRef PubMed
  12.  
  13. Trautwein W, Cavalie A, Flockerzi V, Hofmann F, Pelzer D. Modulation of calcium channel function by phosphorylation in guinea pig ventricular cells and phospholipid bilayer membranes. Circ Res. 1987;61(4 Pt 2):I17–23. PubMed
  14.  
  15. Kostyuk PG, Lukyanetz EA, Doroshenko PA. Effects of serotonin and cAMP on calcium currents in different neurones of Helix pomatia. Pflugers Arch. 1992;420(1): 9–15. CrossRef PubMed
  16.  
  17. McCarron JG, McGeown JG, Reardon S, Ikebe M, Fay FS, Walsh JV, Jr. Calcium-dependent enhancement of calcium current in smooth muscle by calmodulin-dependent protein kinase II. Nature. 1992;357(6373):74–7. CrossRef PubMed
  18.  
  19. Egorova O, Fisyunov O, Maksymyuk O, Kryshtal O. Mechanisms Underlying Positive Modulation of a Current through P-Type Calcium Channels in Purkinje Neurons by an Agonist of Opioid Receptors. Neurophysiology. 2016;48(4):230–7. CrossRef  
  20. Albillos A, Artalejo AR, Lopez MG, Gandia L, Garcia AG, Carbone E. Calcium channel subtypes in cat chromaffin cells. J Physiol. 1994;477(Pt 2):197–213. CrossRef PubMed PubMedCentral
  21.  
  22. Rane SG, Dunlap K. Kinase C activator 1,2-oleoylacetylglycerol attenuates voltage-dependent calcium current in sensory neurons. Proc Natl Acad Sci U S A. 1986;83(1):184–8. CrossRef  
  23. Harris KM, Kongsamut S, Miller RJ. Protein kinase C mediated regulation of calcium channels in PC- 12 pheochromocytoma cells. Biochem Biophys Res Commun. 1986;134(3):1298–305. CrossRef  
  24. DeRiemer SA, Strong JA, Albert KA, Greengard P, Kaczmarek LK. Enhancement of calcium current in Aplysia neurones by phorbol ester and protein kinase C. Nature. 1985;313(6000):313–6. CrossRef PubMed
  25.  
  26. Fischmeister R, Hartzell HC. Mechanism of action of acetylcholine on calcium current in single cells from frog ventricle. J Physiol. 1986;376:183–202. CrossRef PubMed PubMedCentral
  27.  
  28. Mironov SL, Langohr K, Haller M, Richter DW. Hypoxia activates ATP-dependent potassium channels in inspiratory neurones of neonatal mice. J Physiol. 1998;509 (Pt 3):755–66. CrossRef PubMed PubMedCentral
  29.  
  30. Plummer MR, Logothetis DE, Hess P. Elementary properties and pharmacological sensitivities of calcium channels in mammalian peripheral neurons. Neuron. 1989;2(5):1453–63. CrossRef  
  31. Plummer MR, Hess P. Reversible uncoupling of inactivation in N-type calcium channels. Nature. 1991; 351(6328):657–9. CrossRef PubMed
  32.  
  33. Scott RH, Dolphin AC. The agonist effect of Bay K 8644 on neuronal calcium channel currents is promoted by Gprotein activation. Neurosci Lett. 1988;89(2):170–5. CrossRef  
  34. Yatani A, Imoto Y, Codina J, Hamilton SL, Brown AM, Birnbaumer L. The stimulatory G protein of adenylyl cyclase, Gs, also stimulates dihydropyridine-sensitive Ca2+ channels. Evidence for direct regulation independent of phosphorylation by cAMP-dependent protein kinase or stimulation by a dihydropyridine agonist. J Biol Chem. 1988;263(20):9887–95. PubMed
  35.  
  36. Hamilton SL, Codina J, Hawkes MJ, Yatani A, Sawada T, Strickland FM, et al. Evidence for direct interaction of Gs alpha with the Ca2+ channel of skeletal muscle. J Biol Chem. 1991;266(29):19528–35. PubMed
  37.  
  38. Kostyuk PG, Martynyuk AE, Pogorelaya N. Effects of intracellular administration of L-tyrosine and Lphenylalanine on voltage-operated calcium conductance in PC12 pheochromocytoma cells. Brain Res. 1991; 550(1):11–4. CrossRef  
  39. Bosma MM, Bernheim L, Leibowitz MD, Pfaffinger PJ, Hille B. Modulation of M current in frog sympathetic ganglion cells. Soc Gen Physiol Ser. 1990;45:43–59. PubMed
  40.  
  41. Mintz IM, Adams ME, Bean BP. P-type calcium channels in rat central and peripheral neurons. Neuron. 1992;9(1):85–95. CrossRef  
  42. Sullivan JM, Lasater EM. Sustained and transient calcium currents in horizontal cells of the white bass retina. J Gen Physiol. 1992;99(1):85–107. CrossRef  
  43. Chad JE, Eckert R. An enzymatic mechanism for calcium current inactivation in dialysed Helix neurones. J Physiol. 1986;378:31–51. CrossRef  
  44. Kostyuk PG, Lukyanetz EA. Mechanisms of antagonistic action of internal Ca2+ on serotonin-induced potentiation of Ca2+ currents in Helix neurones. Pflugers Arch. 1993;424(1):73–83. CrossRef  
  45. Hagiwara S, Byerly L. Calcium channel. Annu Rev Neurosci. 1981;4:69–125. CrossRef PubMed
  46.  
  47. Fox AP, Nowycky MC, Tsien RW. Kinetic and pharmacological properties distinguishing three types of calcium currents in chick sensory neurones. J Physiol. 1987;394:149–72. CrossRef PubMed PubMedCentral
  48.  
  49. Crunelli V, Lightowler S, Pollard CE. A T-type Ca2+ current underlies low-threshold Ca2+ potentials in cells of the cat and rat lateral geniculate nucleus. J Physiol. 1989;413:543–61. CrossRef PubMed PubMedCentral
  50.  
  51. Boland LM, Dingledine R. Multiple components of both transient and sustained barium currents in a rat dorsal root ganglion cell line. J Physiol (Lond). 1990;420:223– 45:223–45.
  52.  
  53. Carbone E, Lux HD. Kinetics and selectivity of a lowvoltage- activated calcium current in chick and rat sensory neurones. J Physiol. 1987;386:547–70. CrossRef PubMed PubMedCentral
  54.  
  55. Carbone E, Lux HD. Single low-voltage-activated calcium channels in chick and rat sensory neurones. J Physiol. 1987;386:571–601. CrossRef PubMed PubMedCentral
  56.  
  57. Huguenard JR. Low-threshold calcium currents in central nervous system neurons. Annu Rev Physiol. 1996;58: 329–48. CrossRef PubMed
  58.  
  59. Kostyuk PG. Low-voltage activated calcium channels: achievements and problems. Neuroscience. 1999;92(4):1157–63. CrossRef  
  60. Tarasenko AN, Kostyuk PG, Eremin AV, Isaev DS. Two types of low-voltage-activated Ca2+ channels in neurones of rat laterodorsal thalamic nucleus. J Physiol. 1997;499 ( Pt 1)(Pt 1):77–86.
  61.  
  62. Zhuravleva SO, Kostyuk PG, Shuba YM. Divalent cation selectivity of the subtypes of low voltage-activated Ca2+ channels in thalamic neurons. Neuroreport. 1999;10(3):651–7. CrossRef PubMed
  63.  
  64. Carbone E, Swandulla D. Neuronal calcium channels: kinetics, blockade and modulation. Prog Biophys Mol Biol. 1989;54(1):31–58. CrossRef  
  65. Byerly L, Chase PB, Stimers JR. Permeation and interaction of divalent cations in calcium channels of snail neurons. J Gen Physiol. 1985;85(4):491–518. CrossRef PubMed
  66.  
  67. Lansman JB, Hess P, Tsien RW. Blockade of current through single calcium channels by Cd2+, Mg2+, and Ca2+. Voltage and concentration dependence of calcium entry into the pore. J Gen Physiol. 1986;88(3):321–47. CrossRef PubMed
  68.  
  69. Swandulla D, Armstrong CM. Fast-deactivating calcium channels in chick sensory neurons. J Gen Physiol. 1988;92(2):197–218. CrossRef PubMed
  70.  
  71. Carbone E, Clementi F, Formenti A, Pollo A, Sher E. Action of Ca2+ agonists/antagonists in mammalian peripheral neurons. Cell Biol Int Rep. 1989;13(12): 1155–64. CrossRef  
  72. Glossmann H, Ferry DR, Boschek CB. Purification of the putative calcium channel from skeletal muscle with the aid of [3H]-nimodipine binding. Naunyn Schmiedebergs Arch Pharmacol. 1983;323(1):1–11. CrossRef PubMed
  73.  
  74. Borsotto M, Barhanin J, Norman RI, Lazdunski M. Purification of the dihydropyridine receptor of the voltagedependent Ca2+ channel from skeletal muscle transverse tubules using (+) [3H]PN 200-110. Biochem Biophys Res Commun. 1984;122(3):1357–66. CrossRef  
  75. Curtis BM, Catterall WA. Purification of the calcium antagonist receptor of the voltage-sensitive calcium channel from skeletal muscle transverse tubules. Biochemistry. 1984;23(10):2113–8. CrossRef  
  76. Campbell KP, Leung AT, Sharp AH. The biochemistry and molecular biology of the dihydropyridine-sensitive calcium channel. Trends Neurosci. 1988;11(10):425–30. CrossRef  
  77. Ahlijanian MK, Westenbroek RE, Catterall WA. Subunit structure and localization of dihydropyridine-sensitive calcium channels in mammalian brain, spinal cord, and retina. Neuron. 1990;4(6):819–32. CrossRef  
  78. Tanabe T, Takeshima H, Mikami A, Flockerzi V, Takahashi H, Kangawa K, et al. Primary structure of the receptor for calcium channel blockers from skeletal muscle. Nature. 1987;328(6128):313–8. CrossRef PubMed
  79.  
  80. Bean BP. Nitrendipine block of cardiac calcium channels: high-affinity binding to the inactivated state. Proc Natl Acad Sci U S A. 1984;81(20):6388–92. CrossRef PubMed PubMedCentral
  81.  
  82. Sanguinetti MC, Krafte DS, Kass RS. Voltage-dependent modulation of Ca channel current in heart cells by Bay K8644. J Gen Physiol. 1986;88(3):369–92. CrossRef PubMed
  83.  
  84. Rane SG, Holz GGt, Dunlap K. Dihydropyridine inhibition of neuronal calcium current and substance P release. Pflugers Arch. 1987;409(4–5):361–6. CrossRef PubMed PubMedCentral
  85.  
  86. Cohen CJ, McCarthy RT. Nimodipine block of calcium channels in rat anterior pituitary cells. J Physiol. 1987;387:195–225. CrossRef  
  87. Reuter H, Porzig H, Kokubun S, Prod'hom B. 1,4-Dihydropyridines as tools in the study of Ca2+ channels. TrendsNeurosci. 1985;8:396–400. CrossRef  
  88. Brown AM, Kunze DL, Yatani A. The agonist effect of dihydropyridines on Ca channels. Nature. 1984;311(5986):570–2. CrossRef PubMed
  89.  
  90. Kokubun S, Prod'hom B, Becker C, Porzig H, Reuter H. Studies on Ca channels in intact cardiac cells: voltage-dependent effects and cooperative interactions of dihydropyridine enantiomers. Mol Pharmacol. 1986;30(6):571–84. PubMed
  91.  
  92. Hoshi T, Smith SJ. Large depolarization induces long openings of voltage-dependent calcium channels in adrenal chromaffin cells. J Neurosci. 1987;7(2):571–80. PubMed
  93.  
  94. Hess P, Lansman JB, Tsien RW. Different modes of Ca channel gating behaviour favoured by dihydropyridine Ca agonists and antagonists. Nature. 1984;311(5986):538–44. CrossRef PubMed
  95.  
  96. Markwardt F, Nilius B. Modulation of calcium channel currents in guinea-pig single ventricular heart cells by the dihydropyridine Bay K 8644. J Physiol. 1988;399:559–75. CrossRef PubMed PubMedCentral
  97.  
  98. Carbone E, Formenti A, Pollo A. Multiple actions of Bay K 8644 on high-threshold Ca channels in adult rat sensory neurons. Neurosci Lett. 1990;111(3):315–20. CrossRef  
  99. Kokubun S, Reuter H. Dihydropyridine derivatives prolong the open state of Ca channels in cultured cardiac cells. Proc Natl Acad Sci U S A. 1984;81(15):4824–7. CrossRef PubMed PubMedCentral
  100.  
  101. Lacerda AE, Brown AM. Nonmodal gating of cardiac calcium channels as revealed by dihydropyridines. J GenPhysiol. 1989;93(6):1243–73. CrossRef PubMed
  102.  
  103. Dolphin AC, Scott RH. Calcium channel currents and their inhibition by (-)-baclofen in rat sensory neurones: modulation by guanine nucleotides. J Physiol (Lond). 1987;386:1–17. CrossRef  
  104. Jones SW, Marks TN. Calcium currents in bullfrog sympathetic neurons. I. Activation kinetics and pharmacology. J Gen Physiol. 1989;94(1):151–67. CrossRef PubMed
  105.  
  106. Boll W, Lux HD. Action of organic antagonists on neuronal calcium currents. Neurosci Lett. 1985;56(3):335–9. CrossRef  
  107. Gray WR, Luque A, Olivera BM, Barrett J, Cruz LJ. Peptide toxins from Conus geographus venom. J Biol Chem. 1981;256(10):4734–40. PubMed
  108.  
  109. Gray WR, Olivera BM, Cruz LJ. Peptide toxins from venomous Conus snails. Annu Rev Biochem. 1988;57: 665–700. CrossRef PubMed
  110.  
  111. Cruz LJ, Olivera BM. Calcium channel antagonists. Omega-conotoxin defines a new high affinity site. J Biol Chem. 1986;261(14):6230–3. PubMed
  112.  
  113. Olivera BM, Rivier J, Clark C, Ramilo CA, Corpuz GP, Abogadie FC, et al. Diversity of Conus neuropeptides. Science. 1990;249(4966):257–63. CrossRef PubMed
  114.  
  115. Kerr LM, Yoshikami D. A venom peptide with a novel presynaptic blocking action. Nature. 1984;308(5956):282–4. CrossRef
  116. Olivera BM, McIntosh JM, Cruz LJ, Luque FA, Gray WR. Purification and sequence of a presynaptic peptide toxin from Conus geographus venom. Biochemistry. 1984;23(22):5087–90. CrossRef PubMed
  117.  
  118. Hillyard DR, Monje VD, Mintz IM, Bean BP, Nadasdi L, Ramachandran J, et al. A new Conus peptide ligand for mammalian presynaptic Ca2+ channels. Neuron. 1992;9(1):69–77. CrossRef  
  119. Monje VD, Haack JA, Naisbitt SR, Miljanich G, Ramachandran J, Nasdasdi L, et al. A new Conus peptide ligand for Ca channel subtypes. Neuropharmacology. 1993;32(11):1141–9. CrossRef  
  120. Saccomano NA, Ahlijanian MK. Calcium channel toxins: tools to study channel structure and function. Drug Development Reseach. 1994;33:319–43. CrossRef  
  121. Aosaki T, Kasai H. Characterization of two kinds of highvoltage- activated Ca-channel currents in chick sensory neurons. Differential sensitivity to dihydropyridines and -conotoxin GVIA. Pflugers Arch. 1989;414(2):150–6. CrossRef PubMed
  122.  
  123. Regan LJ, Sah DW, Bean BP. Ca2+ channels in rat central and peripheral neurons: high-threshold current resistant to dihydropyridine blockers and  -conotoxin. Neuron. 1991;6(2):269–80. CrossRef  
  124. Mynlieff M, Beam KG. Characterization of voltagedependent calcium currents in mouse motoneurons. J Neurophysiol. 1992;68(1):85–92. PubMed
  125.  
  126. Williams ME, Brust PF, Feldman DH, Patthi S, Simerson S, Maroufi A, et al. Structure and functional expression of an omega-conotoxin-sensitive human N-type calcium channel. Science. 1992;257(5068):389–95. CrossRef PubMed
  127.  
  128. Boland LM, Morrill JA, Bean BP. omega-Conotoxin block of N-type calcium channels in frog and rat sympathetic neurons. J Neurosci. 1994;14(8):5011–27. PubMed
  129.  
  130. McCleskey EW, Fox AP, Feldman DH, Cruz LJ, Olivera BM, Tsien RW, et al. Omega-conotoxin: direct and persistent blockade of specific types of calcium channels in neurons but not muscle. Proc Natl Acad Sci U S A. 1987;84(12):4327–31. CrossRef PubMed PubMedCentral
  131.  
  132. Kuo CC, Hess P. Ion permeation through the L-type Ca2+ channel in rat phaeochromocytoma cells: two sets of ion binding sites in the pore. J Physiol (Lond). 1993;466:629–55. PubMed PubMedCentral
  133.  
  134. McIntosh M, Cruz LJ, Hunkapiller MW, Gray WR, Olivera BM. Isolation and structure of a peptide toxin from the marine snail Conus magus. Arch Biochem Biophys. 1982;218(1):329–34. CrossRef  
  135. Stoehr SJ, Dooley DJ. Characteristics of [125I]omegaconotoxin MVIIA binding to rat neocortical membranes. Neurosci Lett. 1993;161(1):113–6. CrossRef  
  136. Zhang JF, Randall AD, Ellinor PT, Horne WA, Sather WA, Tanabe T, et al. Distinctive pharmacology and kinetics of cloned neuronal Ca2+ channels and their possible counterparts in mammalian CNS neurons. Neuropharmacology. 1993;32(11):1075–88. CrossRef  
  137. Sather WA, Tanabe T, Zhang JF, Mori Y, Adams ME, Tsien RW. Distinctive biophysical and pharmacological properties of class A (BI) calcium channel 1 subunits. Neuron. 1993;11(2):291–303. CrossRef  
  138. Grantham CJ, Bowman D, Bath CP, Bell DC, Bleakman D. Omega-conotoxin MVIIC reversibly inhibits a human N-type calcium channel and calcium influx into chick synaptosomes. Neuropharmacology. 1994;33(2):255–8. CrossRef  
  139. Wheeler DB, Randall A, Tsien RW. Roles of N-type and Q-type Ca2+ channels in supporting hippocampal synaptic transmission. Science. 1994;264(5155):107–11. CrossRef PubMed
  140.  
  141. Mintz IM, Venema VJ, Swiderek KM, Lee TD, Bean BP, Adams ME. P-type calcium channels blocked by the spider toxin -Aga-IVA. Nature. 1992;355(6363):827–9. CrossRef PubMed
  142.  
  143. Mintz IM, Venema VJ, Adams ME, Bean BP. Inhibition of N- and L-type Ca2+ channels by the spider venom toxin omega-Aga-IIIA. Proc Natl Acad Sci U S A. 1991;88(15):6628–31. CrossRef PubMed PubMedCentral
  144.  
  145. Mintz IM. Block of Ca channels in rat central neurons by the spider toxin omega-Aga-IIIA. J Neurosci. 1994;14(5 Pt 1):2844–53. PubMed
  146.  
  147. Mintz IM, Bean BP. Block of calcium channels in rat neurons by synthetic omega-Aga-IVA. Neuropharmacology. 1993;32(11):1161–9. CrossRef  
  148. Bean BP, Mintz IM, Boland LM, Sah DW, Morrill JA. Pharmacology of voltage-dependent calcium channels. In: Soria B, Cena V, editors. Ion channel pharmacology: United States by Oxford University; 1988.
  149.  
  150. Turner TJ, Adams ME, Dunlap K. Calcium channels coupled to glutamate release identified by omega-Aga- IVA. Science. 1992;258(5080):310–3. CrossRef PubMed
  151.  
  152. Turner TJ, Adams ME, Dunlap K. Multiple Ca2+ channel types coexist to regulate synaptosomal neurotransmitter release. Proc Natl Acad Sci U S A. 1993;90(20):9518–22. CrossRef PubMed PubMedCentral
  153.  
  154. Luebke JI, Dunlap K, Turner TJ. Multiple calcium channel types control glutamatergic synaptic transmission in the hippocampus. Neuron. 1993;11(5):895–902. CrossRef  

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