Zn2+ slows down CaV3.3 gating kinetics: Implications for thalamocortical activity

Journal of Neurophysiology

Volumn 98, Issue 4, 2007, Pages 2274-2284

  Cataldi, M ^a   Lariccia, V ^a   Marzaioli, V ^a   Cavaccini, A ^a   Curia, G ^b   Viggiano, D ^a   Canzoniero, L M T ^a   Di Renzo, G ^a   Avoli, M ^b,c   Annunziato, L ^a,d  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b MCGILL UNIVERSITY   (Canada)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

^d Divisione di Gastroenterologia   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOPYRIDINE; CALCIUM; VOLTAGE GATED POTASSIUM CHANNEL; VOLTAGE GATED SODIUM CHANNEL; ZINC;

ARTICLE; BRAIN FUNCTION; CELL MEMBRANE PERMEABILITY; CELL STRAIN HEK293; CHANNEL GATING; CHELATION; EMBRYO; EVOKED RESPONSE; HUMAN; HUMAN CELL; PATCH CLAMP; PRIORITY JOURNAL; RETICULUM CELL; STEADY STATE; THALAMOCORTICAL TRACT; THALAMUS; WHOLE CELL;

4-AMINOPYRIDINE; ACTION POTENTIALS; ALGORITHMS; ANIMALS; CALCIUM CHANNELS, T-TYPE; CELL LINE; CEREBRAL CORTEX; CHELATING AGENTS; DATA INTERPRETATION, STATISTICAL; EPILEPSY; HUMANS; ION CHANNEL GATING; KINETICS; MALE; MEMBRANE POTENTIALS; MEMBRANE TRANSPORT PROTEINS; PATCH-CLAMP TECHNIQUES; POTASSIUM CHANNEL BLOCKERS; RATS; RATS, SPRAGUE-DAWLEY; THALAMUS; TRANSFECTION; ZINC;

EID: 35348836597     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00889.2006     Document Type: Article

References (64)

1. Abbas SY, Ying SW, Goldstein PA. Compartmental distribution of hyperpolarization-activated cyclic-nucleotide-gated channel 2 and hyperpolarization-activated cyclic-nucleotide-gated channel 4 in thalamic reticular and thalamocortical relay neurons. Neuroscience 141: 1811-1825, 2006.
2. Agmon A, Connors BW. Thalamocortical responses of mouse somatosensory (barrel) cortex in vitro. Neuroscience 41: 365-379, 1991.
3. Armstrong CM, Cota G. Modification of sodium channel gating by lanthanum. Some effects that cannot be explained by surface charge theory. J Gen Physiol 96: 1129-1140, 1990.
4. Biagini G, D'Antuono M, Tancredi V, Motalli R, Louvel J, D'Arcangelo G, Pumain R, Warren RA, Avoli M. Thalamocortical connectivity in a rat brain slice preparation: participation of the ventrobasal complex to synchronous activities. Thalamus Related Syst 310: 169-179, 2001.
5. Brown CE, Dyck RH. Retrograde tracing of the subset of afferent connections in mouse barrel cortex provided by zincergic neurons. J Comp Neurol 486: 48-60, 2005.
6. 2+ channel in vertebrate sensory neurons. Nature 310: 501-502, 1984.
7. Casanovas-Aguilar C, Miro-Bernie N, Perez-Clausell J. Zinc-rich neurons in the rat visual cortex give rise to two laminar segregated systems of connections. Neuroscience. 110: 445-458, 2002.
8. Casanovas-Aguilar C, Reblet C, Pérez-Clausell J, Bueno-López JL. Zincrich afferents to the rat neocortex: projections to the visual cortex traced with intracerebral selenite injections. J Chem Neuroanat 15: 97-109, 1998.
9. Cataldi M, Gaudino A, Lariccia V, Russo M, Amoroso S, di Renzo G, Annunziato L. Imatinib-mesylate blocks recombinant T-type calcium channels expressed in human embryonic kidney-293 cells by a protein tyrosine kinase-independent mechanism. J Pharmacol Exp Ther 309: 208-215, 2004.
10. 2+ channels. J Biol Chem 277: 45969-45976, 2002.
11. Coulter DA, Huguenard JR, Prince DA. Calcium currents in rat thalamocortical relay neurons: kinetic properties of the transient, low-threshold current. J Physiol 414: 587-604, 1989.
12. 2+ channel gene family. Circ Res 83: 103-109, 1998.
13. Cuajungco MP, Lees GJ. Prevention of zinc neurotoxicity in vivo by N,N,N′, N′-tetrakis (2-pyridylmethyl) ethylene-diamine (TPEN). Neuroreport 7: 1301-1304, 1996.
14. D'Arcangelo G, D'Antuono M, Biagini G, Warren R, Tancredi V, Avoli M. Thalamocortical oscillations in a genetic model of absence seizures. Eur J Neurosci 16: 2383-2393, 2002.
15. Destexhe A, Contreras D, Steriade M, Sejnowski TJ, Huguenard JR. In vivo, in vitro, and computational analysis of dendritic calcium currents in thalamic reticular neurons. J Neurosci 16: 169-185, 1996.
16. Destexhe A, Sejnowski TJ. Interactions between membrane conductances underlying thalamocortical slow-wave oscillations. Physiol Rev 83: 1401-1453, 2003.
17. Elinder F, Madeja M, Arhem P. Surface charges of K channels. Effects of strontium on five cloned channels expressed in Xenopus oocytes. J Gen Physiol 108: 325-332, 1996.
18. Fox AP, Nowycky MC, Tsien RW. Single-channel recordings of three types of calcium channels in chick sensory neurones. J Physiol 394: 173-200, 1987.
19. Frederickson CJ, Giblin LJ 3rd, Rengarajan B, Masalha R, Frederickson CJ, Zeng Y, Lopez EV, Koh JY, Chorin U, Besser L, Hershfinkel M, Li Y, Thompson RB, Krezel A. Synaptic release of zinc from brain slices: factors governing release, imaging, and accurate calculation of concentration. J Neurosci Methods 154: 19-29, 2006a.
20. Frederickson CJ, Giblin LJ, Krezel A, McAdoo DJ, Muelle RN, Zeng Y, Balaji RV, Masalha R, Thompson RB, Fierke CA, Sarvey JM, de Valdenebro M, Prough DS, Zornow MH. Concentrations of extracellular free zinc (pZn)(e) in the central nervous system during simple anesthetization, ischemia and reperfusion. Exp Neurol 198: 285-293, 2006b.
21. Frederickson CJ, Koh JY, Bush AI. The neurobiology of zinc in health and disease. Nat Rev Neurosci 6: 449-462, 2005.
22. Frederickson CJ, Suh SW, Silva D, Frederickson CJ, Thompson RB. Importance of zinc in the central nervous system: the zinc-containing neuron. J Nutr 130: 1471S-1483S, 2000.
23. Fuentealba P, Timofeev I, Bazhenov M, Sejnowski TJ, Steriade M. Membrane bistability in thalamic reticular neurons during spindle oscillations. J Neurophysiol 93: 294-304, 2005.
24. Gibbs JW 3rd, Zhang YF, Shumate MD, Coulter DA. Regionally selective blockade of GABAergic inhibition by zinc in the thalamocortical system: functional significance. J Neurophysiol 83: 1510-1521, 2000.
25. Harris RJ, Symon L, Branston NM, Bayhan M. Changes in extracellular calcium activity in cerebral ischemia. J Cereb Blood Flow Metab. 1: 203-9, 1981.
26. 2+: an endogenous modulator of ligand- and voltage-gated ion channels. Neuropharmacology 33: 935-952, 1994.
27. o during repetitive electrical stimulation and during pentetrazol induced seizure activity in the sensorimotor cortex of cats. Pfluegers 398: 310-317, 1983.
28. Heinemann U, Lux HD, Gutnick MJ. Extracellular free calcium and potassium during paroxsmal activity in the cerebral cortex of the cat. Exp Brain Res 27: 237-243, 1977.
29. Hille B. Ionic Channels of Excitable Membranes. Sunderland, MA: Sinauer, 1992.
30. Hines ML, Carnevale NT. The NEURON simulation environment. Neural Comput 9: 1179-1209, 1997.
31. Hodgkin AL, Huxley AF. A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol 117: 500-544, 1952.
32. Horning MS, Trombley PQ. Zinc and copper influence excitability of rat olfactory bulb neurons by multiple mechanisms. J Neurophysiol 86: 1652-1660, 2001.
33. Howell GA, Welch MG, Frederickson CJ. Stimulation-induced uptake and release of zinc in hippocampal slices. Nature 308: 736-738, 1984.
34. 2+-dependent burst firing in GABAergic neurons of rat thalamic reticular nucleus. J Neurosci 12: 3804-3817, 1992.
35. Jeong SW, Park BG, Park JY, Lee JW, Lee JH. Divalent metals differentially block cloned T-type calcium channels. Neuroreport 14: 1537-1540, 2003.
36. 2+ currents of rat reticular thalamic neurons and their modulation by enflurane. J Physiol 566: 125-142, 2005a.
37. 2+ channels of reticular thalamic neurons and recombinant Ca(v) 3.3 channels. Br J Pharmacol 144: 59-70, 2005b.
38. Kay AR. Evidence for chelatable zinc in the extracellular space of the hippocampus but little evidence for synaptic release of Zn. J Neurosci 23: 6847-6855, 2003.
39. Khosravani H, Altier C, Simms B, Hamming KS, Snutch TP, Mezeyova J, McRory JE, Zamponi GW. Gating effects of mutations in the Cav3.2 T-type calcium channel associated with childhood absence epilepsy. J Biol Chem 279: 9681-9684, 2004.
40. Kostyuk PG, Shuba Ya M, Savchenko AN. Three types of calcium channels in the membrane of mouse sensory neurons. Pfluegers 411: 661-669, 1988.
41. 2+ entry and frequency dependence during mock action potentials. Eur J Neurosci 11: 4149-4158, 1999.
42. Lee JH, Daud AN, Cribbs LL, Lacerda AE, Pereverzev A, Klockner U, Schneider T, Perez-Reyes E. Cloning and expression of a novel member of the low voltage-activated T-type calcium channel family. J Neurosci 19: 1912-1921, 1999.
43. Mathie A, Sutton GL, Clarke CE, Veale EL. Zinc and copper: pharmacological probes and endogenous modulators of neuronal excitability. Pharmacol Ther 111: 567-583, 2006.
44. Matias CM, Matos NC, Arif M, Dionisio JC, Quinta-Ferreira ME. Effect of the zinc chelator N,N,N′,N′-tetrakis (2-pyridylmethyl)ethylenediamine (TPEN) on hippocampal mossy fiber calcium signals and on synaptic transmission. Biol. Res. 39: 521-530, 2006.
45. McCormick DA, Huguenard JR. A model of the electrophysiological properties of thalamocortical relay neurons. J Neurophysiol 68: 1384-1400, 1992.
46. Mengual E, Casanovas-Aguilar C, Perez-Clausell J, Gimenez-Amaya JM. Thalamic distribution of zinc-rich terminal fields and neurons of origin in the rat. Neuroscience 102: 863-884, 2001.
47. Murbartian J, Arias JM, Perez-Reyes E. Functional impact of alternative splicing of human T-type Cav3.3 calcium channels. J Neurophysiol 92: 3399-3407, 2004.
48. 2+ currents of rat thalamic relay neurons. Neurosci Res 47: 261-5, 2003.
49. Perez-Reyes E. Molecular physiology of low-voltage-activated t-type calcium channels. Physiol Rev 83: 117-161, 2003.
50. Perez-Reyes E, Cribbs LL, Daud A, Lacerda AE, Barclay J, Williamson MP, Fox M, Rees M, Lee JH. Molecular characterization of a neuronal low-voltage-activated T-type calcium channel. Nature 391: 896-900, 1998.
51. Qian J, Noebels JL. Visualization of transmitter release with zinc fluorescence detection at the mouse hippocampal mossy fiber synapse. J Physiol 566: 747-758, 2005.
52. Raymond V, Lapied B. Hyperpolarization-activated inward potassium and calcium-sensitive chloride currents in beating pacemaker insect neurosecretory cells (dorsal unpaired median neurons). Neuroscience 93: 1207-1218, 1999.
53. Shuba YM, Teslenko VI, Savchenko AN, Pogorelaya NH. The effect of permeant ions on single calcium channel activation in mouse neuroblastoma cells: ion-channel interaction. J Physiol 443: 25-44, 1991.
54. Steriade M. Sleep, epilepsy and thalamic reticular inhibitory neurons. Trends Neurosci 28: 317-24, 2005.
55. Steriade M, McCormick DA, Sejnowski TJ. Thalamocortical oscillations in the sleeping and aroused brain. Science 262: 679-85, 1993.
56. 2+ channel alpha1G. J Gen Physiol 121: 529-540, 2003.
57. Talley EM, Cribbs LL, Lee JH, Daud A, Perez-Reyes E, Bayliss DA. Differential distribution of three members of a gene family encoding low voltage-activated (T-type) calcium channels. J Neurosci 19: 1895-1911, 1999.
58. Thompson RB, Whetsell WO, Jr, Maliwal BP, Fierke CA, Frederickson CJ. Fluorescence microscopy of stimulated Zn(II) release from organotypic cultures of mammalian hippo-campus using a carbonic anhydrase-based biosensor system. J Neurosci Methods 96: 35-45, 2000.
59. Traboulsie A, Chemin J, Chevalier M, Quignard JF, Nargeot J, Lory P. Subunit-specific modulation of T-type calcium channels by zinc. J Physiol 578: 159-171, 2007.
60. Tsien RW, Lipscombe D, Madison DV, Bley KR, Fox AP. Multiple types of neuronal calcium channels and their selective modulation. Trends Neurosci 11: 431-438, 1988.
61. 2+ spillover modulates heterosynaptic N-methyl-D-aspartate receptor activity in hippocampal CA3 circuits. J Cell Biol 158: 215-220, 2002.
62. Vitko I, Chen Y, Arias JM, Shen Y, Wu XR, Perez-Reyes E. Functional characterization and neuronal modeling of the effects of childhood absence epilepsy variants of CACNA1H, a T-type calcium channel. J Neurosci 25: 4844-4855, 2005.
63. A receptors in an acquired absence epilepsy model. Brain Res 1013: 230-240, 2004.
64. Yue BW, Huguenard JR. The role of H-current in regulating strength and frequency of thalamic network oscillations. Thalamus Related Syst 1: 95-103, 2001.