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
- 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
- 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
- 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
- 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
- Erdemli G, Xu YZ, Krnjevic K. Potassium conductance causing hyperpolarization of CA1 hippocampal neurons during hypoxia. J Neurophysiol. 1998;80(5):2378–90.
PubMed
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- Plummer MR, Hess P. Reversible uncoupling of inactivation in N-type calcium channels. Nature. 1991; 351(6328):657–9.
CrossRef
PubMed
- 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
- 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
- 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
- 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
- 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
- Mintz IM, Adams ME, Bean BP. P-type calcium channels in rat central and peripheral neurons. Neuron. 1992;9(1):85–95.
CrossRef
- 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
- Chad JE, Eckert R. An enzymatic mechanism for calcium current inactivation in dialysed Helix neurones. J Physiol. 1986;378:31–51.
CrossRef
- 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
- Hagiwara S, Byerly L. Calcium channel. Annu Rev Neurosci. 1981;4:69–125.
CrossRef
PubMed
- 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
- 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
- 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.
- 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
- 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
- Huguenard JR. Low-threshold calcium currents in central nervous system neurons. Annu Rev Physiol. 1996;58: 329–48.
CrossRef
PubMed
- Kostyuk PG. Low-voltage activated calcium channels: achievements and problems. Neuroscience. 1999;92(4):1157–63.
CrossRef
- 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.
- 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
- Carbone E, Swandulla D. Neuronal calcium channels: kinetics, blockade and modulation. Prog Biophys Mol Biol. 1989;54(1):31–58.
CrossRef
- 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
- 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
- Swandulla D, Armstrong CM. Fast-deactivating calcium channels in chick sensory neurons. J Gen Physiol. 1988;92(2):197–218.
CrossRef
PubMed
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- Cohen CJ, McCarthy RT. Nimodipine block of calcium channels in rat anterior pituitary cells. J Physiol. 1987;387:195–225.
CrossRef
- 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
- Brown AM, Kunze DL, Yatani A. The agonist effect of dihydropyridines on Ca channels. Nature. 1984;311(5986):570–2.
CrossRef
PubMed
- 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
- 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
- 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
- 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
- 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
- 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
- Lacerda AE, Brown AM. Nonmodal gating of cardiac calcium channels as revealed by dihydropyridines. J GenPhysiol. 1989;93(6):1243–73.
CrossRef
PubMed
- 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
- 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
- Boll W, Lux HD. Action of organic antagonists on neuronal calcium currents. Neurosci Lett. 1985;56(3):335–9.
CrossRef
- 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
- Gray WR, Olivera BM, Cruz LJ. Peptide toxins from venomous Conus snails. Annu Rev Biochem. 1988;57: 665–700.
CrossRef
PubMed
- Cruz LJ, Olivera BM. Calcium channel antagonists. Omega-conotoxin defines a new high affinity site. J Biol Chem. 1986;261(14):6230–3.
PubMed
- 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
- Kerr LM, Yoshikami D. A venom peptide with a novel presynaptic blocking action. Nature. 1984;308(5956):282–4.
CrossRef
- 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
- 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
- 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
- Saccomano NA, Ahlijanian MK. Calcium channel toxins: tools to study channel structure and function. Drug Development Reseach. 1994;33:319–43.
CrossRef
- 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
- 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
- Mynlieff M, Beam KG. Characterization of voltagedependent calcium currents in mouse motoneurons. J Neurophysiol. 1992;68(1):85–92.
PubMed
- 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
- 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
- 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
- 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
- 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
- Stoehr SJ, Dooley DJ. Characteristics of [125I]omegaconotoxin MVIIA binding to rat neocortical membranes. Neurosci Lett. 1993;161(1):113–6.
CrossRef
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- Mintz IM, Bean BP. Block of calcium channels in rat neurons by synthetic omega-Aga-IVA. Neuropharmacology. 1993;32(11):1161–9.
CrossRef
- 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.
- 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
- 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
- Luebke JI, Dunlap K, Turner TJ. Multiple calcium channel types control glutamatergic synaptic transmission in the hippocampus. Neuron. 1993;11(5):895–902.
CrossRef
|