T-type calcium channels in burst-firing, network synchrony, and epilepsy

Biochimica et Biophysica Acta - Biomembranes

Volumn 1828, Issue 7, 2013, Pages 1572-1578

  Cain, Stuart M ^a   Snutch, Terrance P ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Burst firing; Epilepsy; Low threshold calcium potential; Low threshold spike; Neural network; T type calcium channel; Thalamocortical system

Indexed keywords

CALCIUM CHANNEL T TYPE;

ABSENCE; DISEASE ASSOCIATION; EPILEPSY; GENE MUTATION; GENE SILENCING; HUMAN; LIMBIC EPILEPSY; NERVE CELL MEMBRANE POTENTIAL; NERVE CELL NETWORK; NEUROMODULATION; NONHUMAN; PERCEPTIVE THRESHOLD; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; SPIKE WAVE; SYNAPTIC TRANSMISSION;

ACTION POTENTIALS; ANIMALS; CALCIUM; CALCIUM CHANNELS, T-TYPE; EPILEPSY, ABSENCE; HUMANS; NERVE NET;

EID: 84876940954     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2012.07.028     Document Type: Review

References (85)

1. W.A. Catterall, E. Perez-Reyes, T.P. Snutch, and J. Striessnig International Union of Pharmacology XLVIII Nomenclature and structure-function relationships of voltage-gated calcium channels Pharmacol. Rev. 57 2005 411 425
2. E. Perez-Reyes Molecular physiology of low-voltage-activated T-type calcium channels Physiol. Rev. 83 2003 117 161
3. S.M. Cain, and T.P. Snutch Contributions of T-type calcium channel isoforms to neuronal firing Channels 4 2010 44 51
4. J. Xu, and C.E. Clancy Ionic mechanisms of endogenous bursting in CA3 hippocampal pyramidal neurons: a model study PLoS One 3 2008 e2056
5. H. Jahnsen, and R. Llinas Voltage-dependent burst-to-tonic switching of thalamic cell activity: an in vitro study Arch. Ital. Biol. 122 1984 73 82
6. H.H. Yazdi, M. Janahmadi, and G. Behzadi The role of small-conductance Ca2 +-activated K + channels in the modulation of 4-aminopyridine-induced burst firing in rat cerebellar Purkinje cells Brain Res. 1156 2007 59 66
7. Y. Lee, J.-H. Han, C.-S. Lim, D.-J. Chang, Y.-S. Lee, H. Soh, C.-S. Park, and B.-K. Kaang Impairment of a parabolic bursting rhythm by the ectopic expression of a small conductance Ca2 +-activated K + channel in Aplysia neuron R15 Neurosci. Lett. 349 2003 53 57
8. D. Contreras The role of T-channels in the generation of thalamocortical rhythms CNS Neurol. Disord. Drug Targets 5 2006 571 585
9. M.C. Iftinca, and G.W. Zamponi Regulation of neuronal T-type calcium channels Trends Pharmacol. Sci. 30 2009 32 40
10. S.M. Cain, and T.P. Snutch Voltage-gated calcium channels and disease Biofactors 37 2011 197 205
11. P.J. Adams, and T.P. Snutch Calcium channelopathies: voltage-gated calcium channels Subcell. Biochem. 45 2007 215 251
12. J. Chemin, A. Monteil, E. Perez-Reyes, E. Bourinet, J. Nargeot, and P. Lory Specific contribution of human T-type calcium channel isotypes (alpha(1G), alpha(1H) and alpha(1I)) to neuronal excitability J. Physiol. 540 2002 3 14
13. A.S. Kozlov, F. McKenna, J.H. Lee, L.L. Cribbs, E. Perez-Reyes, A. Feltz, and R.C. Lambert Distinct kinetics of cloned T-type Ca2 + channels lead to differential Ca2 + entry and frequency-dependence during mock action potentials Eur. J. Neurosci. 11 1999 4149 4158
14. A.C. Errington, J.J. Renger, V.N. Uebele, and V. Crunelli State-dependent firing determines intrinsic dendritic Ca2 + signaling in thalamocortical neurons J. Neurosci. 30 2010 14843 14853
15. S.R. Williams, and G.J. Stuart Action potential backpropagation and somato-dendritic distribution of ion channels in thalamocortical neurons J. Neurosci. 20 2000 1307 1317
16. J.R. Huguenard Neuronal circuitry of thalamocortical epilepsy and mechanisms of antiabsence drug action Adv. Neurol. 79 1999 991 999
17. J.P. Manning, D.A. Richards, and N.G. Bowery Pharmacology of absence epilepsy Trends Pharmacol. Sci. 24 2003 542 549
18. H. Blumenfeld Cellular and network mechanisms of spike-wave seizures Epilepsia 46 2005 21 33
19. S. Kakei, J. Na, and Y. Shinoda Thalamic terminal morphology and distribution of single corticothalamic axons originating from layers 5 and 6 of the cat motor cortex J. Comp. Neurol. 437 2001 170 185
20. A. Destexhe, T. Bal, D.A. McCormick, and T.J. Sejnowski Ionic mechanisms underlying synchronized oscillations and propagating waves in a model of ferret thalamic slices J. Neurophysiol. 76 1996 2049 2070
21. P. Landry, and M. Deschênes Intracortical arborizations and receptive fields of identified ventrobasal thalamocortical afferents to the primary somatic sensory cortex in the cat J. Comp. Neurol. 199 1981 345 371
22. D. Pinault The thalamic reticular nucleus: structure, function and concept Brain Res. Brain Res. Rev. 46 2004 1 31
23. X.B. Liu, C.N. Honda, and E.G. Jones Distribution of four types of synapse on physiologically identified relay neurons in the ventral posterior thalamic nucleus of the cat J. Comp. Neurol. 352 1995 69 91
24. J.S. Isaacson, and B.W. Strowbridge Olfactory reciprocal synapses: dendritic signaling in the CNS Neuron 20 1998 749 761
25. J. Johnston, and K.R. Delaney Synaptic activation of T-type Ca2 + channels via mGluR activation in the primary dendrite of mitral cells J. Neurophysiol. 103 2010 2557 2569
26. S.W. Hughes, M. Lorincz, D.W. Cope, K.L. Blethyn, K.A. Kekesi, H.R. Parri, G. Juhasz, and V. Crunelli Synchronized oscillations at alpha and theta frequencies in the lateral geniculate nucleus Neuron 42 2004 253 268
27. B. Singh, A. Monteil, I. Bidaud, Y. Sugimoto, T. Suzuki, S. Hamano, H. Oguni, M. Osawa, M.E. Alonso, A.V. Delgado-Escueta, Y. Inoue, N. Yasui-Furukori, S. Kaneko, P. Lory, and K. Yamakawa Mutational analysis of CACNA1G in idiopathic generalized epilepsy Hum. Mutat. 28 2007 524 525
28. Y. Chen, J. Lu, H. Pan, Y. Zhang, H. Wu, K. Xu, X. Liu, Y. Jiang, X. Bao, Z. Yao, K. Ding, W.H. Lo, B. Qiang, P. Chan, Y. Shen, and X. Wu Association between genetic variation of CACNA1H and childhood absence epilepsy Ann. Neurol. 54 2003 239 243
29. S.E. Heron, H. Khosravani, D. Varela, C. Bladen, T.C. Williams, M.R. Newman, I.E. Scheffer, S.F. Berkovic, J.C. Mulley, and G.W. Zamponi Extended spectrum of idiopathic generalized epilepsies associated with CACNA1H functional variants Ann. Neurol. 62 2007 560 568
30. J. Liang, Y. Zhang, Y. Chen, J. Wang, H. Pan, H. Wu, K. Xu, X. Liu, Y. Jiang, Y. Shen, and X. Wu Common polymorphisms in the CACNA1H gene associated with childhood absence epilepsy in Chinese Han population Ann. Hum. Genet. 71 2007 325 335
31. G.W. Zamponi, P. Lory, and E. Perez-Reyes Role of voltage-gated calcium channels in epilepsy Pflugers Arch. 460 2009 395 403
32. I. Vitko, Y. Chen, J.M. Arias, Y. Shen, X.R. Wu, and E. Perez-Reyes Functional characterization and neuronal modeling of the effects of childhood absence epilepsy variants of CACNA1H, a T-type calcium channel J. Neurosci. 25 2005 4844 4855
33. I. Vitko, I. Bidaud, J.M. Arias, A. Mezghrani, P. Lory, and E. Perez-Reyes The I-II loop controls plasma membrane expression and gating of Cav32 T-type Ca2 + channels: a paradigm for childhood absence epilepsy mutations J. Neurosci. 27 2007 322 330
34. H. Khosravani, C. Altier, B. Simms, K.S. Hamming, T.P. Snutch, J. Mezeyova, J.E. McRory, and G.W. Zamponi Gating effects of mutations in the Cav32 T-type calcium channel associated with childhood absence epilepsy J. Biol. Chem. 279 2004 9681 9684
35. H. Khosravani, C. Bladen, D.B. Parker, T.P. Snutch, J.E. McRory, and G.W. Zamponi Effects of Cav32 channel mutations linked to idiopathic generalized epilepsy Ann. Neurol. 57 2005 745 749
36. J.B. Peloquin, H. Khosravani, W. Barr, C. Bladen, R. Evans, J. Mezeyova, D. Parker, T.P. Snutch, J.E. McRory, and G.W. Zamponi Functional analysis of Ca32 T-type calcium channel mutations linked to childhood absence epilepsy Epilepsia 47 2006 655 658
37. J.L. Wang, C.Y. Han, Y.H. Jing, Y.C. Chen, N. Feng, J.J. Lu, Y.H. Zhang, H. Pan, H.S. Wu, K.M. Xu, Y.W. Jiang, J.M. Liang, L. Wang, X.L. Wang, Y. Shen, and X.R. Wu The effect of CACNA1H gene G773D mutation on calcium channel function Chin. J. Med. Gen. 23 2006 369 373
38. K.L. Powell, S.M. Cain, C. Ng, S. Sirdesai, L.S. David, M. Kyi, E. Garcia, J.R. Tyson, C.A. Reid, M. Bahlo, S.J. Foote, T.P. Snutch, and T.J. O'Brien A Cav32 T-type calcium channel point mutation has splice-variant- specific effects on function and segregates with seizure expression in a polygenic rat model of absence epilepsy J. Neurosci. 29 2009 371 380
39. P.J. Adams, E. Garcia, L.S. David, K.J. Mulatz, S.D. Spacey, and T.P. Snutch Ca(V)21 P/Q-type calcium channel alternative splicing affects the functional impact of familial hemiplegic migraine mutations: implications for calcium channelopathies Channels 3 2009 110 121
40. P.J. Adams, R.L. Rungta, E. Garcia, A.M. van den Maagdenberg, B.A. Macvicar, and T.P. Snutch Contribution of calcium-dependent facilitation to synaptic plasticity revealed by migraine mutations in the P/Q-type calcium channel Proc. Natl. Acad. Sci. U. S. A. 107 2010 18694 18699
41. S.M. Cain, and T.P. Snutch Voltage-Gated Calcium Channels in Epilepsy - Jasper's Basic Mechanisms of the Epilepsies 4th ed. 2012 Oxford University Press Bethesda, U.S.A.
42. E.A. Cavalheiro The pilocarpine model of epilepsy Ital. J. Neurol. Sci. 16 1995 33 37
43. E.A. Cavalheiro, N.F. Santos, and M.R. Priel The pilocarpine model of epilepsy in mice Epilepsia 37 1996 1015 1019
44. H. Su, D. Sochivko, A. Becker, J. Chen, Y. Jiang, Y. Yaari, and H. Beck Upregulation of a T-type Ca2 + channel causes a long-lasting modification of neuronal firing mode after status epilepticus J. Neurosci. 22 2002 3645 3655
45. Y. Yaari, C. Yue, and H. Su Recruitment of apical dendritic T-type Ca2 + channels by backpropagating spikes underlies de novo intrinsic bursting in hippocampal epileptogenesis J. Physiol. 580 2007 435 450
46. E.R. Sanabria, H. Su, and Y. Yaari Initiation of network bursts by Ca2 + - dependent intrinsic bursting in the rat pilocarpine model of temporal lobe epilepsy J. Physiol. 532 2001 205 216
47. A.J. Becker, J. Pitsch, D. Sochivko, T. Opitz, M. Staniek, C.C. Chen, K.P. Campbell, S. Schoch, Y. Yaari, and H. Beck Transcriptional upregulation of Cav32 mediates epileptogenesis in the pilocarpine model of epilepsy J. Neurosci. 28 2008 13341 13353
48. J. Wellmer, H. Su, H. Beck, and Y. Yaari Long-lasting modification of intrinsic discharge properties in subicular neurons following status epilepticus Eur. J. Neurosci. 16 2002 259 266
49. J.D. Graef, B.K. Nordskog, W.F. Wiggins, and D.W. Godwin An acquired channelopathy involving thalamic T-type Ca2 + channels after status epilepticus J. Neurosci. 29 2009 4430 4441
50. S.M. Cain, and T.P. Snutch Voltage-gated calcium channels in epilepsy Epilepsia 51 2010 11-11
51. Y. Zhang, M. Mori, D.L. Burgess, and J.L. Noebels Mutations in high-voltage-activated calcium channel genes stimulate low-voltage-activated currents in mouse thalamic relay neurons J. Neurosci. 22 2002 6362 6371
52. W.L. Ernst, Y. Zhang, J.W. Yoo, S.J. Ernst, and J.L. Noebels Genetic enhancement of thalamocortical network activity by elevating alpha 1g-mediated low-voltage-activated calcium current induces pure absence epilepsy J. Neurosci. 29 2009 1615 1625
53. E. Cheong, Y. Zheng, K. Lee, J. Lee, S. Kim, M. Sanati, S. Lee, Y.S. Kim, and H.S. Shin Deletion of phospholipase C beta4 in thalamocortical relay nucleus leads to absence seizures Proc. Natl. Acad. Sci. U. S. A. 106 2009 21912 21917
54. E. Cheong, S. Lee, B.J. Choi, M. Sun, C.J. Lee, and H.-S. Shin Tuning thalamic firing modes via simultaneous modulation of T- and L-type Ca2 + channels controls pain sensory gating in the thalamus J. Neurosci. 28 2008 13331 13340
55. D. Kim, I. Song, S. Keum, T. Lee, M.J. Jeong, S.S. Kim, M.W. McEnery, and H.S. Shin Lack of the burst firing of thalamocortical relay neurons and resistance to absence seizures in mice lacking alpha(1G) T-type Ca2 + channels Neuron 31 2001 35 45
56. N.A. Hawkins, and J.A. Kearney Confirmation of an epilepsy modifier locus on mouse chromosome 11 and candidate gene analysis by RNA-Seq Genes Brain Behav. 11 2012 452 460
57. A.M. Coenen, and E.L. Van Luijtelaar Genetic animal models for absence epilepsy: a review of the WAG/Rij strain of rats Behav. Genet. 33 2003 635 655
58. O. Akman, T. Demiralp, N. Ates, and F.Y. Onat Electroencephalographic differences between WAG/Rij and GAERS rat models of absence epilepsy Epilepsy Res. 2010
59. T. Broicher, T. Kanyshkova, P. Meuth, H.C. Pape, and T. Budde Correlation of T-channel coding gene expression, IT, and the low threshold Ca2 + spike in the thalamus of a rat model of absence epilepsy Mol. Cell. Neurosci. 39 2008 384 399
60. M. Inoue, J. Duysens, J.M. Vossen, and A.M. Coenen Thalamic multiple-unit activity underlying spike-wave discharges in anesthetized rats Brain Res. 612 1993 35 40
61. A. Gorji, C. Mittag, P. Shahabi, T. Seidenbecher, and H.-C. Pape Seizure-related activity of intralaminar thalamic neurons in a genetic model of absence epilepsy Neurobiol. Dis. 43 2011 266 274
62. T. Seidenbecher, and H.C. Pape Contribution of intralaminar thalamic nuclei to spike-and-wave-discharges during spontaneous seizures in a genetic rat model of absence epilepsy Eur. J. Neurosci. 13 2001 1537 1546
63. C. Marescaux, M. Vergnes, and A. Depaulis Genetic absence epilepsy in rats from Strasbourg - a review J. Neural Transm. Suppl. 35 1992 37 69
64. S.J. Slaght, N. Leresche, J.M. Deniau, V. Crunelli, and S. Charpier Activity of thalamic reticular neurons during spontaneous genetically determined spike and wave discharges J. Neurosci. 22 2002 2323 2334
65. D. Pinault, N. Leresche, S. Charpier, J.M. Deniau, C. Marescaux, M. Vergnes, and V. Crunelli Intracellular recordings in thalamic neurones during spontaneous spike and wave discharges in rats with absence epilepsy J. Physiol. 509 Pt. 2 1998 449 456
66. E. Tsakiridou, L. Bertollini, M. de Curtis, G. Avanzini, and H.C. Pape Selective increase in T-type calcium conductance of reticular thalamic neurons in a rat model of absence epilepsy J. Neurosci. 15 1995 3110 3117
67. E.M. Talley, L.L. Cribbs, J.H. Lee, A. Daud, E. Perez-Reyes, and D.A. Bayliss Differential distribution of three members of a gene family encoding low voltage-activated (T-type) calcium channels J. Neurosci. 19 1999 1895 1911
68. E.M. Talley, G. Solorzano, A. Depaulis, E. Perez-Reyes, and D.A. Bayliss Low-voltage-activated calcium channel subunit expression in a genetic model of absence epilepsy in the rat Brain Res. Mol. Brain Res. 75 2000 159 165
69. D. Pinault Cellular interactions in the rat somatosensory thalamocortical system during normal and epileptic 5-9 Hz oscillations J. Physiol. 552 2003 881 905
70. S. Charpier, N. Leresche, J.M. Deniau, S. Mahon, S.W. Hughes, and V. Crunelli On the putative contribution of GABA(B) receptors to the electrical events occurring during spontaneous spike and wave discharges Neuropharmacology 38 1999 1699 1706
71. J.T. Paz, M. Chavez, S. Saillet, J.M. Deniau, and S. Charpier Activity of ventral medial thalamic neurons during absence seizures and modulation of cortical paroxysms by the nigrothalamic pathway J. Neurosci. 27 2007 929 941
72. M. Chipaux, S. Charpier, and P.-O. Polack Chloride-mediated inhibition of the ictogenic neurones initiating genetically-determined absence seizures Neuroscience 192 2011 642 651
73. H. Blumenfeld Consciousness and epilepsy: why are patients with absence seizures absent? Prog. Brain Res. 150 2005 271 286
74. C.E. Landisman, and B.W. Connors VPM and PoM nuclei of the rat somatosensory thalamus: intrinsic neuronal properties and corticothalamic feedback Cereb. Cortex 17 2007 2853 2865
75. P.O. Polack, S. Mahon, M. Chavez, and S. Charpier Inactivation of the somatosensory cortex prevents paroxysmal oscillations in cortical and related thalamic neurons in a genetic model of absence epilepsy Cereb. Cortex 19 2009 2078 2091
76. L. Danober, C. Deransart, A. Depaulis, M. Vergnes, and C. Marescaux Pathophysiological mechanisms of genetic absence epilepsy in the rat Prog. Neurobiol. 55 1998 27 57
77. V. Crunelli, and N. Leresche Block of thalamic T-type Ca(2 +) channels by ethosuximide is not the whole story Epilepsy Curr. 2 2002 53 56
78. T.R. Browne, F.E. Dreifuss, P.R. Dyken, D.J. Goode, J.K. Penry, R.J. Porter, B.G. White, and P.T. White Ethosuximide in the treatment of absence (peptit mal) seizures Neurology 25 1975 515 524
79. R. Gulhan Aker, K. Tezcan, N. Carcak, E. Sakalli, D. Akin, and F.Y. Onat Localized cortical injections of ethosuximide suppress spike-and-wave activity and reduce the resistance to kindling in genetic absence epilepsy rats (GAERS) Epilepsy Res. 89 2009 7 16
80. J.P. Manning, D.A. Richards, N. Leresche, V. Crunelli, and N.G. Bowery Cortical-area specific block of genetically determined absence seizures by ethosuximide Neuroscience 123 2004 5 9
81. Z.Q. Yang, J.C. Barrow, W.D. Shipe, K.A. Schlegel, Y. Shu, F.V. Yang, C.W. Lindsley, K.E. Rittle, M.G. Bock, G.D. Hartman, V.N. Uebele, C.E. Nuss, S.V. Fox, R.L. Kraus, S.M. Doran, T.M. Connolly, C. Tang, J.E. Ballard, Y. Kuo, E.D. Adarayan, T. Prueksaritanont, M.M. Zrada, M.J. Marino, V.K. Graufelds, A.G. DiLella, I.J. Reynolds, H.M. Vargas, P.B. Bunting, R.F. Woltmann, M.M. Magee, K.S. Koblan, and J.J. Renger Discovery of 1,4-substituted piperidines as potent and selective inhibitors of T-type calcium channels J. Med. Chem. 51 2008 6471 6477
82. W.D. Shipe, J.C. Barrow, Z.Q. Yang, C.W. Lindsley, F.V. Yang, K.A. Schlegel, Y. Shu, K.E. Rittle, M.G. Bock, G.D. Hartman, C. Tang, J.E. Ballard, Y. Kuo, E.D. Adarayan, T. Prueksaritanont, M.M. Zrada, V.N. Uebele, C.E. Nuss, T.M. Connolly, S.M. Doran, S.V. Fox, R.L. Kraus, M.J. Marino, V.K. Graufelds, H.M. Vargas, P.B. Bunting, M. Hasbun-Manning, R.M. Evans, K.S. Koblan, and J.J. Renger Design, synthesis, and evaluation of a novel 4-aminomethyl-4- fluoropiperidine as a T-type Ca2 + channel antagonist J. Med. Chem. 51 2008 3692 3695
83. V.N. Uebele, C.E. Nuss, S.V. Fox, S.L. Garson, R. Cristescu, S.M. Doran, R.L. Kraus, V.P. Santarelli, Y. Li, J.C. Barrow, Z.Q. Yang, K.A. Schlegel, K.E. Rittle, T.S. Reger, R.A. Bednar, W. Lemaire, F.A. Mullen, J.E. Ballard, C. Tang, G. Dai, O.B. McManus, K.S. Koblan, and J.J. Renger Positive allosteric interaction of structurally diverse T-type calcium channel antagonists Cell Biochem. Biophys. 55 2009 81 93
84. R.L. Kraus, Y. Li, Y. Gregan, A.L. Gotter, V.N. Uebele, S.V. Fox, S.M. Doran, J.C. Barrow, Z.Q. Yang, T.S. Reger, K.S. Koblan, and J.J. Renger In vitro characterization of T-type calcium channel antagonist TTA-A2 and in vivo effects on arousal in mice J. Pharmacol. Exp. Ther. 335 2010 409 417
85. E. Tringham, K.L. Powell, S.M. Cain, K. Kuplast, J. Mezeyova, M. Weerapura, C. Eduljee, X. Jiang, P. Smith, J.-L. Morrison, N.C. Jones, E. Braine, G. Rind, M. Fee-Maki, D. Parker, H. Pajouhesh, M. Parmar, T.J. O'Brien, and T.P. Snutch T-type calcium channel blockers that attenuate thalamic burst firing and suppress absence seizures Sci. Transl. Med. 4 2012 121ra19