T-type Calcium Channels in Health and Disease

Author(s): Dan Wang*, Lotten Ragnarsson, Richard J. Lewis

Journal Name: Current Medicinal Chemistry

Volume 27 , Issue 19 , 2020

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Abstract:

Low Voltage-Activated (LVA) T-type calcium channels are characterized by transient current and Low Threshold Spikes (LTS) that trigger neuronal firing and oscillatory behavior. Combined with their preferential localization in dendrites and their specific “window current”, T-type calcium channels are considered to be key players in signal amplification and synaptic integration. Assisted by the emerging pharmacological tools, the structural determinants of channel gating and kinetics, as well as novel physiological and pathological functions of T-type calcium channels, are being uncovered. In this review, we provide an overview of structural determinants in T-type calcium channels, their involvement in disorders and diseases, the development of novel channel modulators, as well as Structure-Activity Relationship (SAR) studies that lead to rational drug design.

Keywords: T-type calcium channels, structural determinants, channel function, pathophysiological roles, modulators, rational drug design.

[1]
Ertel, E.A.; Campbell, K.P.; Harpold, M.M.; Hofmann, F.; Mori, Y.; Perez-Reyes, E.; Schwartz, A.; Snutch, T.P.; Tanabe, T.; Birnbaumer, L.; Tsien, R.W.; Catterall, W.A. Nomenclature of voltage-gated calcium channels. Neuron, 2000, 25(3), 533-535.
[http://dx.doi.org/10.1016/S0896-6273(00)81057-0] [PMID: 10774722]
[2]
Carbone, E.; Lux, H.D. A low voltage-activated, fully inactivating Ca channel in vertebrate sensory neurones. Nature, 1984, 310(5977), 501-502.
[http://dx.doi.org/10.1038/310501a0] [PMID: 6087159]
[3]
Hess, P.; Lansman, J.B.; Tsien, R.W. Different modes of Ca channel gating behaviour favoured by dihydropyridine Ca agonists and antagonists. Nature, 1984, 311(5986), 538-544.
[http://dx.doi.org/10.1038/311538a0] [PMID: 6207437]
[4]
Dolphin, A.C. A short history of voltage-gated calcium channels. Br. J. Pharmacol., 2006, 147(Suppl. 1), S56-S62.
[http://dx.doi.org/10.1038/sj.bjp.0706442] [PMID: 16402121]
[5]
Savalli, N.; Pantazis, A.; Sigg, D.; Weiss, J.N.; Neely, A.; Olcese, R. The α2δ-1 subunit remodels CaV1.2 voltage sensors and allows Ca2+ influx at physiological membrane potentials. J. Gen. Physiol., 2016, 148(2), 147-159.
[http://dx.doi.org/10.1085/jgp.201611586] [PMID: 27481713]
[6]
Minor, D.L., Jr; Findeisen, F.; Daniel, L. Progress in the structural understanding of voltage-gated calcium channel (CaV) function and modulation. Channels (Austin), 2010, 4(6), 459-474.
[http://dx.doi.org/10.4161/chan.4.6.12867] [PMID: 21139419]
[7]
Catterall, W.A. Voltage-gated calcium channels. Cold Spring Harb. Perspect. Biol., 2011, 3(8) a003947
[http://dx.doi.org/10.1101/cshperspect.a003947] [PMID: 21746798]
[8]
Wu, J.; Yan, Z.; Li, Z.; Yan, C.; Lu, S.; Dong, M.; Yan, N. Structure of the voltage-gated calcium channel Cav1.1 complex. Science, 2015, 350(6267) aad2395
[http://dx.doi.org/10.1126/science.aad2395] [PMID: 26680202]
[9]
Catterall, W.A.; Perez-Reyes, E.; Snutch, T.P.; Striessnig, J. International Union of Pharmacology. XLVIII. Nomenclature and structure-function relationships of voltage-gated calcium channels. Pharmacol. Rev., 2005, 57(4), 411-425.
[http://dx.doi.org/10.1124/pr.57.4.5] [PMID: 16382099]
[10]
Saegusa, H.; Kurihara, T.; Zong, S.; Kazuno, A.; Matsuda, Y.; Nonaka, T.; Han, W.; Toriyama, H.; Tanabe, T. Suppression of inflammatory and neuropathic pain symptoms in mice lacking the N-type Ca2+ channel. EMBO J., 2001, 20(10), 2349-2356.
[http://dx.doi.org/10.1093/emboj/20.10.2349] [PMID: 11350923]
[11]
Doan, L. Voltage-gated calcium channels and pain. Tech. Reg. Anesth. Pain Manage., 2010, 14, 42-47.
[http://dx.doi.org/10.1053/j.trap.2010.03.003]
[12]
Miljanich, G.P. Ziconotide: neuronal calcium channel blocker for treating severe chronic pain. Curr. Med. Chem., 2004, 11(23), 3029-3040.
[http://dx.doi.org/10.2174/0929867043363884] [PMID: 15578997]
[13]
Deer, T.R.; Pope, J.E.; Hayek, S.M.; Bux, A.; Buchser, E.; Eldabe, S.; De Andrés, J.A.; Erdek, M.; Patin, D.; Grider, J.S.; Doleys, D.M.; Jacobs, M.S.; Yaksh, T.L.; Poree, L.; Wallace, M.S.; Prager, J.; Rauck, R.; DeLeon, O.; Diwan, S.; Falowski, S.M.; Gazelka, H.M.; Kim, P.; Leong, M.; Levy, R.M.; McDowell, G., II; McRoberts, P.; Naidu, R.; Narouze, S.; Perruchoud, C.; Rosen, S.M.; Rosenberg, W.S.; Saulino, M.; Staats, P.; Stearns, L.J.; Willis, D.; Krames, E.; Huntoon, M.; Mekhail, N. The polyanalgesic consensus conference (pacc): recommendations on intrathecal drug infusion systems best practices and guidelines. Neuromodulation, 2017, 20(2), 96-132.
[http://dx.doi.org/10.1111/ner.12538] [PMID: 28042904]
[14]
Deer, T.; Rauck, R.L.; Kim, P.; Saulino, M.F.; Wallace, M.; Grigsby, E.J.; Huang, I.Z.; Mori, F.; Vanhove, G.F.; McDowell, G.C., II Effectiveness and safety of intrathecal ziconotide: Interim analysis of the patient registry of intrathecal ziconotide management (PRIZM). Pain Pract., 2018, 18(2), 230-238.
[http://dx.doi.org/10.1111/papr.12599] [PMID: 28449352]
[15]
Staats, P.S.; Yearwood, T.; Charapata, S.G.; Presley, R.W.; Wallace, M.S.; Byas-Smith, M.; Fisher, R.; Bryce, D.A.; Mangieri, E.A.; Luther, R.R.; Mayo, M.; McGuire, D.; Ellis, D. Intrathecal ziconotide in the treatment of refractory pain in patients with cancer or AIDS: a randomized controlled trial. JAMA, 2004, 291(1), 63-70.
[http://dx.doi.org/10.1001/jama.291.1.63] [PMID: 14709577]
[16]
Grabner, M.; Friedrich, K.; Knaus, H-G.; Striessnig, J.; Scheffauer, F.; Staudinger, R.; Koch, W.J.; Schwartz, A.; Glossmann, H. Calcium channels from Cyprinus carpio skeletal muscle. Proc. Natl. Acad. Sci. USA, 1991, 88(3), 727-731.
[http://dx.doi.org/10.1073/pnas.88.3.727] [PMID: 1846962]
[17]
Ellis, S.B.; Williams, M.E.; Ways, N.R.; Brenner, R.; Sharp, A.H.; Leung, A.T.; Campbell, K.P.; McKenna, E.; Koch, W.J.; Hui, A. Sequence and expression of mRNAs encoding the alpha 1 and alpha 2 subunits of a DHP-sensitive calcium channel. Science, 1988, 241(4873), 1661-1664.
[http://dx.doi.org/10.1126/science.2458626] [PMID: 2458626]
[18]
Vajna, R.; Schramm, M.; Pereverzev, A.; Arnhold, S.; Grabsch, H.; Klöckner, U.; Perez-Reyes, E.; Hescheler, J.; Schneider, T. New isoform of the neuronal Ca2+ channel α1E subunit in islets of Langerhans and kidney. Eur. J. Biochem., 1998, 257, 274-285.
[http://dx.doi.org/10.1046/j.1432-1327.1998.2570274.x]
[19]
Biel, M.; Ruth, P.; Bosse, E.; Hullin, R.; Stühmer, W.; Flockerzi, V.; Hofmann, F. Primary structure and functional expression of a high voltage activated calcium channel from rabbit lung. FEBS Lett., 1990, 269(2), 409-412.
[http://dx.doi.org/10.1016/0014-5793(90)81205-3] [PMID: 2169433]
[20]
Mikami, A.; Imoto, K.; Tanabe, T.; Niidome, T.; Mori, Y.; Takeshima, H.; Narumiya, S.; Numa, S. Primary structure and functional expression of the cardiac dihydropyridine-sensitive calcium channel. Nature, 1989, 340(6230), 230-233.
[http://dx.doi.org/10.1038/340230a0] [PMID: 2474130]
[21]
Seino, S.; Chen, L.; Seino, M.; Blondel, O.; Takeda, J.; Johnson, J.H.; Bell, G.I. Cloning of the alpha 1 subunit of a voltage-dependent calcium channel expressed in pancreatic beta cells. Proc. Natl. Acad. Sci. USA, 1992, 89(2), 584-588.
[http://dx.doi.org/10.1073/pnas.89.2.584] [PMID: 1309948]
[22]
Yiru, S. Investigation and characterization of splice variations of LType Ca2+ channel, CaV1.3, in chick basilar papilla and rat cochlear hair cells: limplications in hearing, (Doctoral dissertation),. 2007.
[23]
McRory, J.E.; Hamid, J.; Doering, C.J.; Garcia, E.; Parker, R.; Hamming, K.; Chen, L.; Hildebrand, M.; Beedle, A.M.; Feldcamp, L.; Zamponi, G.W.; Snutch, T.P. The CACNA1F gene encodes an L-type calcium channel with unique biophysical properties and tissue distribution. J. Neurosci., 2004, 24(7), 1707-1718.
[http://dx.doi.org/10.1523/JNEUROSCI.4846-03.2004] [PMID: 14973233]
[24]
Dubel, S.J.; Starr, T.V.; Hell, J.; Ahlijanian, M.K.; Enyeart, J.J.; Catterall, W.A.; Snutch, T.P. Molecular cloning of the alpha-1 subunit of an omega-conotoxin-sensitive calcium channel. Proc. Natl. Acad. Sci. USA, 1992, 89(11), 5058-5062.
[http://dx.doi.org/10.1073/pnas.89.11.5058] [PMID: 1317580]
[25]
Xu, J.H.; Long, L.; Wang, J.; Tang, Y.C.; Hu, H.T.; Soong, T.W.; Tang, F.R. Nuclear localization of Ca(v)2.2 and its distribution in the mouse central nervous system, and changes in the hippocampus during and after pilocarpine-induced status epilepticus. Neuropathol. Appl. Neurobiol., 2010, 36(1), 71-85.
[http://dx.doi.org/10.1111/j.1365-2990.2009.01044.x] [PMID: 19811616]
[26]
Pereverzev, A.; Klöckner, U.; Henry, M.; Grabsch, H.; Vajna, R.; Olyschläger, S.; Viatchenko-Karpinski, S.; Schröder, R.; Hescheler, J.; Schneider, T. Structural diversity of the voltage-dependent Ca2+ channel alpha1E-subunit. Eur. J. Neurosci., 1998, 10(3), 916-925.
[http://dx.doi.org/10.1046/j.1460-9568.1998.00099.x] [PMID: 9753159]
[27]
Monteil, A.; Chemin, J.; Bourinet, E.; Mennessier, G.; Lory, P.; Nargeot, J. Molecular and functional properties of the human alpha(1G) subunit that forms T-type calcium channels. J. Biol. Chem., 2000, 275(9), 6090-6100.
[http://dx.doi.org/10.1074/jbc.275.9.6090] [PMID: 10692398]
[28]
Talley, E.M.; Cribbs, L.L.; Lee, J-H.; Daud, A.; Perez-Reyes, E.; Bayliss, D.A. Differential distribution of three members of a gene family encoding low voltage-activated (T-type) calcium channels. J. Neurosci., 1999, 19(6), 1895-1911.
[http://dx.doi.org/10.1523/JNEUROSCI.19-06-01895.1999] [PMID: 10066243]
[29]
Emerick, M.C.; Stein, R.; Kunze, R.; McNulty, M.M.; Regan, M.R.; Hanck, D.A.; Agnew, W.S. Profiling the array of Ca(v)3.1 variants from the human T-type calcium channel gene CACNA1G: alternative structures, developmental expression, and biophysical variations. Proteins, 2006, 64(2), 320-342.
[http://dx.doi.org/10.1002/prot.20877] [PMID: 16671074]
[30]
Jagannathan, S.; Punt, E.L.; Gu, Y.; Arnoult, C.; Sakkas, D.; Barratt, C.L.; Publicover, S.J. Identification and localization of T-type voltage-operated calcium channel subunits in human male germ cells. Expression of multiple isoforms. J. Biol. Chem., 2002, 277(10), 8449-8456.
[http://dx.doi.org/10.1074/jbc.M105345200] [PMID: 11751928]
[31]
Cribbs, L.L.; Lee, J.H.; Yang, J.; Satin, J.; Zhang, Y.; Daud, A.; Barclay, J.; Williamson, M.P.; Fox, M.; Rees, M.; Perez-Reyes, E. Cloning and characterization of alpha1H from human heart, a member of the T-type Ca2+ channel gene family. Circ. Res., 1998, 83(1), 103-109.
[http://dx.doi.org/10.1161/01.RES.83.1.103] [PMID: 9670923]
[32]
Williams, M.E.; Washburn, M.S.; Hans, M.; Urrutia, A.; Brust, P.F.; Prodanovich, P.; Harpold, M.M.; Stauderman, K.A. Structure and functional characterization of a novel human low-voltage activated calcium channel. J. Neurochem., 1999, 72(2), 791-799.
[http://dx.doi.org/10.1046/j.1471-4159.1999.0720791.x] [PMID: 9930755]
[33]
Bourinet, E.; Alloui, A.; Monteil, A.; Barrère, C.; Couette, B.; Poirot, O.; Pages, A.; McRory, J.; Snutch, T.P.; Eschalier, A.; Nargeot, J. Silencing of the Cav3.2 T-type calcium channel gene in sensory neurons demonstrates its major role in nociception. EMBO J., 2005, 24(2), 315-324.
[http://dx.doi.org/10.1038/sj.emboj.7600515] [PMID: 15616581]
[34]
Usoskin, D.; Furlan, A.; Islam, S.; Abdo, H.; Lönnerberg, P.; Lou, D.; Hjerling-Leffler, J.; Haeggström, J.; Kharchenko, O.; Kharchenko, P.V.; Linnarsson, S.; Ernfors, P. Unbiased classification of sensory neuron types by large-scale single-cell RNA sequencing. Nat. Neurosci., 2015, 18(1), 145-153.
[http://dx.doi.org/10.1038/nn.3881] [PMID: 25420068]
[35]
Carbone, E.; Lux, H.D. A low voltage-activated calcium conductance in embryonic chick sensory neurons. Biophys. J., 1984, 46(3), 413-418.
[http://dx.doi.org/10.1016/S0006-3495(84)84037-0] [PMID: 6487739]
[36]
Perez-Reyes, E. Molecular physiology of low-voltage-activated t-type calcium channels. Physiol. Rev., 2003, 83(1), 117-161.
[http://dx.doi.org/10.1152/physrev.00018.2002] [PMID: 12506128]
[37]
Lee, J.H.; Daud, A.N.; Cribbs, L.L.; Lacerda, A.E.; Pereverzev, A.; Klöckner, 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., 1999, 19(6), 1912-1921.
[http://dx.doi.org/10.1523/JNEUROSCI.19-06-01912.1999] [PMID: 10066244]
[38]
Perez-Reyes, E.; Cribbs, L.L.; Daud, A.; Lacerda, A.E.; Barclay, J.; Williamson, M.P.; Fox, M.; Rees, M.; Lee, J.H. Molecular characterization of a neuronal low-voltage-activated T-type calcium channel. Nature, 1998, 391(6670), 896-900.
[http://dx.doi.org/10.1038/36110] [PMID: 9495342]
[39]
Anderson, D.; Mehaffey, W.H.; Iftinca, M.; Rehak, R.; Engbers, J.D.; Hameed, S.; Zamponi, G.W.; Turner, R.W. Regulation of neuronal activity by Cav3-Kv4 channel signaling complexes. Nat. Neurosci., 2010, 13(3), 333-337.
[http://dx.doi.org/10.1038/nn.2493] [PMID: 20154682]
[40]
Anderson, D.; Rehak, R.; Hameed, S.; Mehaffey, W.H.; Zamponi, G.W.; Turner, R.W. Regulation of the KV4.2 complex by CaV3.1 calcium channels. Channels (Austin), 2010, 4(3), 163-167.
[http://dx.doi.org/10.4161/chan.4.3.11955] [PMID: 20458163]
[41]
Engbers, J.D.; Anderson, D.; Asmara, H.; Rehak, R.; Mehaffey, W.H.; Hameed, S.; McKay, B.E.; Kruskic, M.; Zamponi, G.W.; Turner, R.W. Intermediate conductance calcium-activated potassium channels modulate summation of parallel fiber input in cerebellar Purkinje cells. Proc. Natl. Acad. Sci. USA, 2012, 109(7), 2601-2606.
[http://dx.doi.org/10.1073/pnas.1115024109] [PMID: 22308379]
[42]
Wang, L.; Bhattacharjee, A.; Fu, J.; Li, M. Abnormally expressed low-voltage-activated calcium channels in beta-cells from NOD mice and a related clonal cell line. Diabetes, 1996, 45(12), 1678-1683.
[http://dx.doi.org/10.2337/diab.45.12.1678] [PMID: 8922351]
[43]
Barnett, D.W.; Pressel, D.M.; Misler, S. Voltage-dependent Na+ and Ca2+ currents in human pancreatic islet beta-cells: evidence for roles in the generation of action potentials and insulin secretion. Pflugers Arch., 1995, 431(2), 272-282.
[http://dx.doi.org/10.1007/BF00410201] [PMID: 9026789]
[44]
Davalli, A.M.; Biancardi, E.; Pollo, A.; Socci, C.; Pontiroli, A.E.; Pozza, G.; Clementi, F.; Sher, E.; Carbone, E. Dihydropyridine-sensitive and -insensitive voltage-operated calcium channels participate in the control of glucose-induced insulin release from human pancreatic beta cells. J. Endocrinol., 1996, 150(2), 195-203.
[http://dx.doi.org/10.1677/joe.0.1500195] [PMID: 8869586]
[45]
Braun, M.; Ramracheya, R.; Bengtsson, M.; Zhang, Q.; Karanauskaite, J.; Partridge, C.; Johnson, P.R.; Rorsman, P. Voltage-gated ion channels in human pancreatic beta-cells: electrophysiological characterization and role in insulin secretion. Diabetes, 2008, 57(6), 1618-1628.
[http://dx.doi.org/10.2337/db07-0991] [PMID: 18390794]
[46]
Clozel, J-P.; Ertel, E.A.; Ertel, S.I. Voltage-gated T-type Ca2+ channels and heart failure. Proc. Assoc. Am. Physicians, 1999, 111(5), 429-437.
[http://dx.doi.org/10.1111/paa.1999.111.5.429] [PMID: 10519164]
[47]
Maeda, Y.; Aoki, Y.; Sekiguchi, F.; Matsunami, M.; Takahashi, T.; Nishikawa, H.; Kawabata, A. Hyperalgesia induced by spinal and peripheral hydrogen sulfide: evidence for involvement of Cav3.2 T-type calcium channels. Pain, 2009, 142(1-2), 127-132.
[http://dx.doi.org/10.1016/j.pain.2008.12.021] [PMID: 19167819]
[48]
Okubo, K.; Takahashi, T.; Sekiguchi, F.; Kanaoka, D.; Matsunami, M.; Ohkubo, T.; Yamazaki, J.; Fukushima, N.; Yoshida, S.; Kawabata, A. Inhibition of T-type calcium channels and hydrogen sulfide-forming enzyme reverses paclitaxel-evoked neuropathic hyperalgesia in rats. Neuroscience, 2011, 188, 148-156.
[http://dx.doi.org/10.1016/j.neuroscience.2011.05.004] [PMID: 21596106]
[49]
Todorovic, S.M.; Meyenburg, A.; Jevtovic-Todorovic, V. Mechanical and thermal antinociception in rats following systemic administration of mibefradil, a T-type calcium channel blocker. Brain Res., 2002, 951(2), 336-340.
[http://dx.doi.org/10.1016/S0006-8993(02)03350-4] [PMID: 12270514]
[50]
Dogrul, A.; Gardell, L.R.; Ossipov, M.H.; Tulunay, F.C.; Lai, J.; Porreca, F. Reversal of experimental neuropathic pain by T-type calcium channel blockers. Pain, 2003, 105(1-2), 159-168.
[http://dx.doi.org/10.1016/S0304-3959(03)00177-5] [PMID: 14499432]
[51]
Marksteiner, R.; Schurr, P.; Berjukow, S.; Margreiter, E.; Perez-Reyes, E.; Hering, S. Inactivation determinants in segment IIIS6 of Ca(v)3.1. J. Physiol., 2001, 537(Pt 1), 27-34.
[http://dx.doi.org/10.1111/j.1469-7793.2001.0027k.x] [PMID: 11711558]
[52]
Staes, M.; Talavera, K.; Klugbauer, N.; Prenen, J.; Lacinová, L.; Droogmans, G.; Hofmann, F.; Nilius, B. The amino side of the C-terminus determines fast inactivation of the T-type calcium channel alpha1G. J. Physiol., 2001, 530(Pt 1), 35-45.
[http://dx.doi.org/10.1111/j.1469-7793.2001.0035m.x] [PMID: 11136856]
[53]
Chemin, J.; Monteil, A.; Dubel, S.; Nargeot, J.; Lory, P. The alpha1I T-type calcium channel exhibits faster gating properties when overexpressed in neuroblastoma/glioma NG 108-15 cells. Eur. J. Neurosci., 2001, 14(10), 1678-1686.
[http://dx.doi.org/10.1046/j.0953-816x.2001.01796.x] [PMID: 11860462]
[54]
Hamid, J.; Peloquin, J.B.; Monteil, A.; Zamponi, G.W. Determinants of the differential gating properties of Cav3.1 and Cav3.3 T-type channels: a role of domain IV? Neuroscience, 2006, 143(3), 717-728.
[http://dx.doi.org/10.1016/j.neuroscience.2006.08.023] [PMID: 16996222]
[55]
Arias, J.M.; Murbartián, J.; Vitko, I.; Lee, J.H.; Perez-Reyes, E. Transfer of β subunit regulation from high to low voltage-gated Ca2+ channels. FEBS Lett., 2005, 579(18), 3907-3912.
[http://dx.doi.org/10.1016/j.febslet.2005.06.008] [PMID: 15987636]
[56]
Perez-Reyes, E. Characterization of the gating brake in the I-II loop of CaV3 T-type calcium channels. Channels (Austin), 2010, 4(6), 453-458.
[http://dx.doi.org/10.4161/chan.4.6.12889] [PMID: 21099341]
[57]
Arias-Olguín, I.I.; Vitko, I.; Fortuna, M.; Baumgart, J.P.; Sokolova, S.; Shumilin, I.A.; Van Deusen, A.; Soriano-García, M.; Gomora, J.C.; Perez-Reyes, E. Characterization of the gating brake in the I-II loop of Ca(v)3.2 T-type Ca(2+) channels. J. Biol. Chem., 2008, 283(13), 8136-8144.
[http://dx.doi.org/10.1074/jbc.M708761200] [PMID: 18218623]
[58]
Baumgart, J.P.; Vitko, I.; Bidaud, I.; Kondratskyi, A.; Lory, P.; Perez-Reyes, E. I-II loop structural determinants in the gating and surface expression of low voltage-activated calcium channels. PLoS One, 2008, 3(8) e2976
[http://dx.doi.org/10.1371/journal.pone.0002976] [PMID: 18714336]
[59]
Blesneac, I.; Chemin, J.; Bidaud, I.; Huc-Brandt, S.; Vandermoere, F.; Lory, P. Phosphorylation of the Cav3.2 T-type calcium channel directly regulates its gating properties. Proc. Natl. Acad. Sci. USA, 2015, 112(44), 13705-13710.
[http://dx.doi.org/10.1073/pnas.1511740112] [PMID: 26483470]
[60]
Chemin, J.; Taiakina, V.; Monteil, A.; Piazza, M.; Guan, W.; Stephens, R.F.; Kitmitto, A.; Pang, Z.P.; Dolphin, A.C.; Perez-Reyes, E.; Dieckmann, T.; Guillemette, J.G.; Spafford, J.D. Calmodulin regulates Cav3 T-type channels at their gating brake. J. Biol. Chem., 2017, 292(49), 20010-20031.
[http://dx.doi.org/10.1074/jbc.M117.807925] [PMID: 28972185]
[61]
Lee, N.; Jeong, S.; Kim, K.C.; Kim, J.A.; Park, J.Y.; Kang, H.W.; Perez-Reyes, E.; Lee, J.H. Ca2+ regulation of CaV3.3 T-type Ca2+ channel is mediated by calmodulin. Mol. Pharmacol., 2017, 92(3), 347-357.
[http://dx.doi.org/10.1124/mol.117.108530] [PMID: 28696213]
[62]
Wolfe, J.T.; Wang, H.; Howard, J.; Garrison, J.C.; Barrett, P.Q. T-type calcium channel regulation by specific G-protein betagamma subunits. Nature, 2003, 424(6945), 209-213.
[http://dx.doi.org/10.1038/nature01772] [PMID: 12853961]
[63]
Welsby, P.J.; Wang, H.; Wolfe, J.T.; Colbran, R.J.; Johnson, M.L.; Barrett, P.Q. A mechanism for the direct regulation of T-type calcium channels by Ca2+/calmodulin-dependent kinase II. J. Neurosci., 2003, 23(31), 10116-10121.
[http://dx.doi.org/10.1523/JNEUROSCI.23-31-10116.2003] [PMID: 14602827]
[64]
Chemin, J.; Monteil, A.; Bourinet, E.; Nargeot, J.; Lory, P. Alternatively spliced alpha(1G) (Ca(V)3.1) intracellular loops promote specific T-type Ca(2+) channel gating properties. Biophys. J., 2001, 80(3), 1238-1250.
[http://dx.doi.org/10.1016/S0006-3495(01)76100-0] [PMID: 11222288]
[65]
Park, J-Y.; Kang, H-W.; Jeong, S-W.; Lee, J-H. Multiple structural elements contribute to the slow kinetics of the Cav3.3 T-type channel. J. Biol. Chem., 2004, 279(21), 21707-21713.
[http://dx.doi.org/10.1074/jbc.M400684200] [PMID: 15016809]
[66]
Gomora, J.C.; Murbartián, J.; Arias, J.M.; Lee, J-H.; Perez-Reyes, E. Cloning and expression of the human T-type channel Ca(v)3.3: insights into prepulse facilitation. Biophys. J., 2002, 83(1), 229-241.
[http://dx.doi.org/10.1016/S0006-3495(02)75164-3] [PMID: 12080115]
[67]
McRory, J.E.; Santi, C.M.; Hamming, K.S.; Mezeyova, J.; Sutton, K.G.; Baillie, D.L.; Stea, A.; Snutch, T.P. Molecular and functional characterization of a family of rat brain T-type calcium channels. J. Biol. Chem., 2001, 276(6), 3999-4011.
[http://dx.doi.org/10.1074/jbc.M008215200] [PMID: 11073957]
[68]
Kang, H.W.; Park, J.Y.; Lee, J.H. Distinct contributions of different structural regions to the current kinetics of the Cav3.3 T-type Ca2+ channel. Biochim. Biophys. Acta, 2008, 1778(12), 2740-2748.
[http://dx.doi.org/10.1016/j.bbamem.2008.08.002] [PMID: 18760992]
[69]
García-Caballero, A.; Gadotti, V.M.; Stemkowski, P.; Weiss, N.; Souza, I.A.; Hodgkinson, V.; Bladen, C.; Chen, L.; Hamid, J.; Pizzoccaro, A.; Deage, M.; François, A.; Bourinet, E.; Zamponi, G.W. The deubiquitinating enzyme USP5 modulates neuropathic and inflammatory pain by enhancing Cav3.2 channel activity. Neuron, 2014, 83(5), 1144-1158.
[http://dx.doi.org/10.1016/j.neuron.2014.07.036] [PMID: 25189210]
[70]
Jeong, S.W.; Park, B.G.; Park, J.Y.; Lee, J.W.; Lee, J.H. Divalent metals differentially block cloned T-type calcium channels. Neuroreport, 2003, 14(11), 1537-1540.
[http://dx.doi.org/10.1097/00001756-200308060-00028] [PMID: 12960781]
[71]
Kang, H.W.; Park, J.Y.; Jeong, S.W.; Kim, J.A.; Moon, H.J.; Perez-Reyes, E.; Lee, J.H. A molecular determinant of nickel inhibition in Cav3.2 T-type calcium channels. J. Biol. Chem., 2006, 281(8), 4823-4830.
[http://dx.doi.org/10.1074/jbc.M510197200] [PMID: 16377633]
[72]
Kang, H.W.; Vitko, I.; Lee, S.S.; Perez-Reyes, E.; Lee, J.H. Structural determinants of the high affinity extracellular zinc binding site on Cav3.2 T-type calcium channels. J. Biol. Chem., 2010, 285(5), 3271-3281.
[http://dx.doi.org/10.1074/jbc.M109.067660] [PMID: 19940152]
[73]
Nelson, M.T.; Joksovic, P.M.; Su, P.; Kang, H.W.; Van Deusen, A.; Baumgart, J.P.; David, L.S.; Snutch, T.P.; Barrett, P.Q.; Lee, J.H.; Zorumski, C.F.; Perez-Reyes, E.; Todorovic, S.M. Molecular mechanisms of subtype-specific inhibition of neuronal T-type calcium channels by ascorbate. J. Neurosci., 2007, 27(46), 12577-12583.
[http://dx.doi.org/10.1523/JNEUROSCI.2206-07.2007] [PMID: 18003836]
[74]
Nelson, M.T.; Woo, J.; Kang, H.W.; Vitko, I.; Barrett, P.Q.; Perez-Reyes, E.; Lee, J.H.; Shin, H.S.; Todorovic, S.M. Reducing agents sensitize C-type nociceptors by relieving high-affinity zinc inhibition of T-type calcium channels. J. Neurosci., 2007, 27(31), 8250-8260.
[http://dx.doi.org/10.1523/JNEUROSCI.1800-07.2007] [PMID: 17670971]
[75]
Snead, O.C., III Basic mechanisms of generalized absence seizures. Ann. Neurol., 1995, 37(2), 146-157.
[http://dx.doi.org/10.1002/ana.410370204] [PMID: 7847856]
[76]
Gloor, P.; Fariello, R.G. Generalized epilepsy: some of its cellular mechanisms differ from those of focal epilepsy. Trends Neurosci., 1988, 11(2), 63-68.
[http://dx.doi.org/10.1016/0166-2236(88)90166-X] [PMID: 2465601]
[77]
Steriade, M.; McCormick, D.A.; Sejnowski, T.J. Thalamocortical oscillations in the sleeping and aroused brain. Science, 1993, 262(5134), 679-685.
[http://dx.doi.org/10.1126/science.8235588] [PMID: 8235588]
[78]
Crunelli, V.; Lightowler, S.; Pollard, C.E. A T-type Ca2+ current underlies low-threshold Ca2+ potentials in cells of the cat and rat lateral geniculate nucleus. J. Physiol., 1989, 413, 543-561.
[http://dx.doi.org/10.1113/jphysiol.1989.sp017668] [PMID: 2557441]
[79]
Huguenard, J.R.; Prince, D.A. Intrathalamic rhythmicity studied in vitro: nominal T-current modulation causes robust antioscillatory effects. J. Neurosci., 1994, 14(9), 5485-5502.
[http://dx.doi.org/10.1523/JNEUROSCI.14-09-05485.1994] [PMID: 8083749]
[80]
Tringham, E.; Powell, K.L.; Cain, S.M.; Kuplast, K.; Mezeyova, J.; Weerapura, M.; Eduljee, C.; Jiang, X.; Smith, P.; Morrison, J.L.; Jones, N.C.; Braine, E.; Rind, G.; Fee-Maki, M.; Parker, D.; Pajouhesh, H.; Parmar, M.; O’Brien, T.J.; Snutch, T.P. T-type calcium channel blockers that attenuate thalamic burst firing and suppress absence seizures. Sci. Transl. Med., 2012, 4(121) 121ra19
[http://dx.doi.org/10.1126/scitranslmed.3003120] [PMID: 22344687]
[81]
Coulter, D.A.; Huguenard, J.R.; Prince, D.A. Characterization of ethosuximide reduction of low-threshold calcium current in thalamic neurons. Ann. Neurol., 1989, 25(6), 582-593.
[http://dx.doi.org/10.1002/ana.410250610] [PMID: 2545161]
[82]
Suzuki, S.; Kawakami, K.; Nishimura, S.; Watanabe, Y.; Yagi, K.; Seino, M.; Miyamoto, K. Zonisamide blocks T-type calcium channel in cultured neurons of rat cerebral cortex. Epilepsy Res., 1992, 12(1), 21-27.
[http://dx.doi.org/10.1016/0920-1211(92)90087-A] [PMID: 1326433]
[83]
Kito, M.; Maehara, M.; Watanabe, K. Mechanisms of T-type calcium channel blockade by zonisamide. Seizure, 1996, 5(2), 115-119.
[http://dx.doi.org/10.1016/S1059-1311(96)80104-X] [PMID: 8795126]
[84]
Gomora, J.C.; Daud, A.N.; Weiergräber, M.; Perez-Reyes, E. Block of cloned human T-type calcium channels by succinimide antiepileptic drugs. Mol. Pharmacol., 2001, 60(5), 1121-1132.
[http://dx.doi.org/10.1124/mol.60.5.1121] [PMID: 11641441]
[85]
Huguenard, J.R. Block of T -Type Ca(2+) Channels is an important action of succinimide antiabsence drugs. Epilepsy Curr., 2002, 2(2), 49-52.
[http://dx.doi.org/10.1046/j.1535-7597.2002.00019.x] [PMID: 15309165]
[86]
Matthews, E.A.; Dickenson, A.H. Effects of ethosuximide, a T-type Ca(2+) channel blocker, on dorsal horn neuronal responses in rats. Eur. J. Pharmacol., 2001, 415(2-3), 141-149.
[http://dx.doi.org/10.1016/S0014-2999(01)00812-3] [PMID: 11274992]
[87]
Leresche, N.; Parri, H.R.; Erdemli, G.; Guyon, A.; Turner, J.P.; Williams, S.R.; Asprodini, E.; Crunelli, V. On the action of the anti-absence drug ethosuximide in the rat and cat thalamus. J. Neurosci., 1998, 18(13), 4842-4853.
[http://dx.doi.org/10.1523/JNEUROSCI.18-13-04842.1998] [PMID: 9634550]
[88]
Crunelli, V.; Leresche, N. Block of thalamic T-type Ca2+ channels by ethosuximide is not the whole story. Epilepsy Curr., 2002, 2(2), 53-56.
[http://dx.doi.org/10.1046/j.1535-7597.2002.00024.x] [PMID: 15309166]
[89]
Tsakiridou, E.; Bertollini, L.; de Curtis, M.; Avanzini, G.; Pape, H.C. Selective increase in T-type calcium conductance of reticular thalamic neurons in a rat model of absence epilepsy. J. Neurosci., 1995, 15(4), 3110-3117.
[http://dx.doi.org/10.1523/JNEUROSCI.15-04-03110.1995] [PMID: 7722649]
[90]
Talley, E.M.; Solórzano, G.; Depaulis, A.; Perez-Reyes, E.; Bayliss, D.A. Low-voltage-activated calcium channel subunit expression in a genetic model of absence epilepsy in the rat. Brain Res. Mol. Brain Res., 2000, 75(1), 159-165.
[http://dx.doi.org/10.1016/S0169-328X(99)00307-1] [PMID: 10648900]
[91]
Graef, J.D.; Nordskog, B.K.; Wiggins, W.F.; Godwin, D.W. An acquired channelopathy involving thalamic T-type Ca2+ channels after status epilepticus. J. Neurosci., 2009, 29(14), 4430-4441.
[http://dx.doi.org/10.1523/JNEUROSCI.0198-09.2009] [PMID: 19357270]
[92]
Proft, J.; Rzhepetskyy, Y.; Lazniewska, J.; Zhang, F.X.; Cain, S.M.; Snutch, T.P.; Zamponi, G.W.; Weiss, N. The Cacna1h mutation in the GAERS model of absence epilepsy enhances T-type Ca2+ currents by altering calnexin-dependent trafficking of Cav3.2 channels. Sci. Rep., 2017, 7(1), 11513.
[http://dx.doi.org/10.1038/s41598-017-11591-5] [PMID: 28912545]
[93]
Kim, D.; Song, I.; Keum, S.; Lee, T.; Jeong, M.J.; Kim, S.S.; McEnery, M.W.; Shin, H.S. Lack of the burst firing of thalamocortical relay neurons and resistance to absence seizures in mice lacking alpha(1G) T-type Ca(2+) channels. Neuron, 2001, 31(1), 35-45.
[http://dx.doi.org/10.1016/S0896-6273(01)00343-9] [PMID: 11498049]
[94]
Ernst, W.L.; Zhang, Y.; Yoo, J.W.; Ernst, S.J.; Noebels, J.L. Genetic enhancement of thalamocortical network activity by elevating α 1g-mediated low-voltage-activated calcium current induces pure absence epilepsy. J. Neurosci., 2009, 29(6), 1615-1625.
[http://dx.doi.org/10.1523/JNEUROSCI.2081-08.2009] [PMID: 19211869]
[95]
Chen, Y.; Lu, J.; Pan, H.; Zhang, Y.; Wu, H.; Xu, K.; Liu, X.; Jiang, Y.; Bao, X.; Yao, Z.; Ding, K.; Lo, W.H.; Qiang, B.; Chan, P.; Shen, Y.; Wu, X. Association between genetic variation of CACNA1H and childhood absence epilepsy. Ann. Neurol., 2003, 54(2), 239-243.
[http://dx.doi.org/10.1002/ana.10607] [PMID: 12891677]
[96]
Vitko, I.; Chen, Y.; Arias, J.M.; Shen, Y.; Wu, X.R.; 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., 2005, 25(19), 4844-4855.
[http://dx.doi.org/10.1523/JNEUROSCI.0847-05.2005] [PMID: 15888660]
[97]
Liang, J.; Zhang, Y.; Chen, Y.; Wang, J.; Pan, H.; Wu, H.; Xu, K.; Liu, X.; Jiang, Y.; Shen, Y.; Wu, X. Common polymorphisms in the CACNA1H gene associated with childhood absence epilepsy in Chinese Han population. Ann. Hum. Genet., 2007, 71(Pt 3), 325-335.
[http://dx.doi.org/10.1111/j.1469-1809.2006.00332.x] [PMID: 17156077]
[98]
Heron, S.E.; Khosravani, H.; Varela, D.; Bladen, C.; Williams, T.C.; Newman, M.R.; Scheffer, I.E.; Berkovic, S.F.; Mulley, J.C.; Zamponi, G.W. Extended spectrum of idiopathic generalized epilepsies associated with CACNA1H functional variants. Ann. Neurol., 2007, 62(6), 560-568.
[http://dx.doi.org/10.1002/ana.21169] [PMID: 17696120]
[99]
Singh, B.; Monteil, A.; Bidaud, I.; Sugimoto, Y.; Suzuki, T.; Hamano, S.; Oguni, H.; Osawa, M.; Alonso, M.E. Delgado- Escueta, A.V.; Inoue, Y.; Yasui-Furukori, N.; Kaneko, S.; Lory, P.; Yamakawa, K. Mutational analysis of CACNA1G in idiopathic generalized epilepsy. Mutation in brief #962. Hum. Mutat., 2007, 28(5), 524-525.
[http://dx.doi.org/10.1002/humu.9491] [PMID: 17397049]
[100]
Chen, Y.; Lu, J.; Zhang, Y.; Pan, H.; Wu, H.; Xu, K.; Liu, X.; Jiang, Y.; Bao, X.; Zhou, J.; Liu, W.; Shi, G.; Shen, Y.; Wu, X. T-type calcium channel gene alpha (1G) is not associated with childhood absence epilepsy in the Chinese Han population. Neurosci. Lett., 2003, 341(1), 29-32.
[http://dx.doi.org/10.1016/S0304-3940(03)00124-1] [PMID: 12676336]
[101]
Cheong, E.; Shin, H.S. T-type Ca2+ channels in normal and abnormal brain functions. Physiol. Rev., 2013, 93(3), 961-992.
[http://dx.doi.org/10.1152/physrev.00010.2012] [PMID: 23899559]
[102]
Wang, H.; Naghavi, M.; Allen, C.; Barber, R.; Carter, A.; Casey, D.; Charlson, F.; Chen, A.; Coates, M.; Coggeshall, M. GBD 2015 Mortality and Causes of Death Collaborators. Global, regional, and national life expectancy, all-cause mortality, and cause-specific mortality for 249 causes of death, 1980-2015: a systematic analysis for the Global Burden of Disease Study 2015. Lancet, 2016, 388(10053), 1459-1544.
[http://dx.doi.org/10.1016/S0140-6736(16)31012-1] [PMID: 27733281]
[103]
Vos, T.; Allen, C.; Arora, M.; Barber, R.M.; Bhutta, Z.A.; Brown, A.; Carter, A.; Casey, D.C.; Charlson, F.J.; Chen, A.Z. GBD 2015 Disease and Injury Incidence and Prevalence Collaborators. Global, regional, and national incidence, prevalence, and years lived with disability for 310 diseases and injuries, 1990-2015: a systematic analysis for the Global Burden of Disease Study 2015. Lancet, 2016, 388(10053), 1545-1602.
[http://dx.doi.org/10.1016/S0140-6736(16)31678-6] [PMID: 27733282]
[104]
Hammond, C.; Bergman, H.; Brown, P. Pathological synchronization in Parkinson’s disease: networks, models and treatments. Trends Neurosci., 2007, 30(7), 357-364.
[http://dx.doi.org/10.1016/j.tins.2007.05.004] [PMID: 17532060]
[105]
Hutchison, W.D.; Allan, R.J.; Opitz, H.; Levy, R.; Dostrovsky, J.O.; Lang, A.E.; Lozano, A.M. Neurophysiological identification of the subthalamic nucleus in surgery for Parkinson’s disease. Ann. Neurol., 1998, 44(4), 622-628.
[http://dx.doi.org/10.1002/ana.410440407] [PMID: 9778260]
[106]
Murata, M.; Hasegawa, K.; Kanazawa, I. Japan Zonisamide on PD Study Group. Zonisamide improves motor function in Parkinson disease: a randomized, double-blind study. Neurology, 2007, 68(1), 45-50.
[http://dx.doi.org/10.1212/01.wnl.0000250236.75053.16] [PMID: 17200492]
[107]
Bermejo, P.E.; Anciones, B. A review of the use of zonisamide in Parkinson’s disease. Ther. Adv. Neurol. Disorder., 2009, 2(5), 313-317.
[http://dx.doi.org/10.1177/1756285609338501] [PMID: 21180621]
[108]
Yang, Z-Q.; Barrow, J.C.; Shipe, W.D.; Schlegel, K-A.S.; Shu, Y.; Yang, F.V.; Lindsley, C.W.; Rittle, K.E.; Bock, M.G.; Hartman, G.D.; Uebele, V.N.; Nuss, C.E.; Fox, S.V.; Kraus, R.L.; Doran, S.M.; Connolly, T.M.; Tang, C.; Ballard, J.E.; Kuo, Y.; Adarayan, E.D.; Prueksaritanont, T.; Zrada, M.M.; Marino, M.J.; Graufelds, V.K.; DiLella, A.G.; Reynolds, I.J.; Vargas, H.M.; Bunting, P.B.; Woltmann, R.F.; Magee, M.M.; Koblan, K.S.; Renger, J.J. Discovery of 1,4-substituted piperidines as potent and selective inhibitors of T-type calcium channels. J. Med. Chem., 2008, 51(20), 6471-6477.
[http://dx.doi.org/10.1021/jm800830n] [PMID: 18817368]
[109]
Xiang, Z.; Thompson, A.D.; Brogan, J.T.; Schulte, M.L.; Melancon, B.J.; Mi, D.; Lewis, L.M.; Zou, B.; Yang, L.; Morrison, R.; Santomango, T.; Byers, F.; Brewer, K.; Aldrich, J.S.; Yu, H.; Dawson, E.S.; Li, M.; McManus, O.; Jones, C.K.; Daniels, J.S.; Hopkins, C.R.; Xie, X.S.; Conn, P.J.; Weaver, C.D.; Lindsley, C.W. The discovery and characterization of ML218: a novel, centrally active T-type calcium channel inhibitor with robust effects in STN neurons and in a rodent model of Parkinson’s disease. ACS Chem. Neurosci., 2011, 2(12), 730-742.
[http://dx.doi.org/10.1021/cn200090z] [PMID: 22368764]
[110]
Devergnas, A.; Chen, E.; Ma, Y.; Hamada, I.; Pittard, D.; Kammermeier, S.; Mullin, A.P.; Faundez, V.; Lindsley, C.W.; Jones, C.; Smith, Y.; Wichmann, T. Anatomical localization of Cav3.1 calcium channels and electrophysiological effects of T-type calcium channel blockade in the motor thalamus of MPTP-treated monkeys. J. Neurophysiol., 2016, 115(1), 470-485.
[http://dx.doi.org/10.1152/jn.00858.2015] [PMID: 26538609]
[111]
Ono, K.; Iijima, T. Cardiac T-type Ca(2+) channels in the heart. J. Mol. Cell. Cardiol., 2010, 48(1), 65-70.
[http://dx.doi.org/10.1016/j.yjmcc.2009.08.021] [PMID: 19729018]
[112]
Horiba, M.; Muto, T.; Ueda, N.; Opthof, T.; Miwa, K.; Hojo, M.; Lee, J.K.; Kamiya, K.; Kodama, I.; Yasui, K. T-type Ca2+ channel blockers prevent cardiac cell hypertrophy through an inhibition of calcineurin-NFAT3 activation as well as L-type Ca2+ channel blockers. Life Sci., 2008, 82(11-12), 554-560.
[http://dx.doi.org/10.1016/j.lfs.2007.11.010] [PMID: 18275974]
[113]
Furukawa, T.; Nukada, T.; Namiki, Y.; Miyashita, Y.; Hatsuno, K.; Ueno, Y.; Yamakawa, T.; Isshiki, T. Five different profiles of dihydropyridines in blocking T-type Ca(2+) channel subtypes (Cav3.1 (α1G), Cav3.2 (α1H), and Cav3.3 (α1I)) expressed in Xenopus oocytes. Eur. J. Pharmacol., 2009, 613(1-3), 100-107.
[http://dx.doi.org/10.1016/j.ejphar.2009.04.036] [PMID: 19401195]
[114]
Uchino, T.; Lee, T.S.; Kaku, T.; Yamashita, N.; Noguchi, T.; Ono, K. Voltage-dependent and frequency-independent inhibition of recombinant Cav3.2 T-type Ca2+ channel by bepridil. Pharmacology, 2005, 74(4), 174-181.
[http://dx.doi.org/10.1159/000085329] [PMID: 15855830]
[115]
Su, A.I.; Welsh, J.B.; Sapinoso, L.M.; Kern, S.G.; Dimitrov, P.; Lapp, H.; Schultz, P.G.; Powell, S.M.; Moskaluk, C.A.; Frierson, H.F., Jr; Hampton, G.M. Molecular classification of human carcinomas by use of gene expression signatures. Cancer Res., 2001, 61(20), 7388-7393.
[PMID: 11606367]
[116]
Mariot, P.; Vanoverberghe, K.; Lalevee, N.; Rossier, M.F.; Prevarskaya, N. Overexpression of an alpha 1H (Cav3.2) T-type calcium channel during neuroendocrine differentiation of human prostate cancer cells. J. Biol. Chem., 2002, 277(13), 10824-10833.
[http://dx.doi.org/10.1074/jbc.M108754200] [PMID: 11799114]
[117]
Das, A.; Pushparaj, C.; Herreros, J.; Nager, M.; Vilella, R.; Portero, M.; Pamplona, R.; Matias-Guiu, X.; Martí, R.M.; Cantí, C. T-type calcium channel blockers inhibit autophagy and promote apoptosis of malignant melanoma cells. Pigment Cell Melanoma Res., 2013, 26(6), 874-885.
[http://dx.doi.org/10.1111/pcmr.12155] [PMID: 23931340]
[118]
Dziegielewska, B.; Gray, L.S.; Dziegielewski, J. T-type calcium channels blockers as new tools in cancer therapies. Pflugers Arch., 2014, 466(4), 801-810.
[http://dx.doi.org/10.1007/s00424-014-1444-z] [PMID: 24449277]
[119]
Ohkubo, T.; Yamazaki, J. T-type voltage-activated calcium channel Cav3.1, but not Cav3.2, is involved in the inhibition of proliferation and apoptosis in MCF-7 human breast cancer cells. Int. J. Oncol., 2012, 41(1), 267-275.
[http://dx.doi.org/10.3892/ijo.2012.1422] [PMID: 22469755]
[120]
Ranzato, E.; Magnelli, V.; Martinotti, S.; Waheed, Z.; Cain, S.M.; Snutch, T.P.; Marchetti, C.; Burlando, B. Epigallocatechin-3-gallate elicits Ca2+ spike in MCF-7 breast cancer cells: essential role of Cav3.2 channels. Cell Calcium, 2014, 56(4), 285-295.
[http://dx.doi.org/10.1016/j.ceca.2014.09.002] [PMID: 25260713]
[121]
Woolf, C.J. Central sensitization: implications for the diagnosis and treatment of pain. Pain, 2011, 152(3)(Suppl.), S2-S15.
[http://dx.doi.org/10.1016/j.pain.2010.09.030] [PMID: 20961685]
[122]
Osteen, J.D.; Herzig, V.; Gilchrist, J.; Emrick, J.J.; Zhang, C.; Wang, X.; Castro, J.; Garcia-Caraballo, S.; Grundy, L.; Rychkov, G.Y.; Weyer, A.D.; Dekan, Z.; Undheim, E.A.; Alewood, P.; Stucky, C.L.; Brierley, S.M.; Basbaum, A.I.; Bosmans, F.; King, G.F.; Julius, D. Selective spider toxins reveal a role for the Nav1.1 channel in mechanical pain. Nature, 2016, 534(7608), 494-499.
[http://dx.doi.org/10.1038/nature17976] [PMID: 27281198]
[123]
King, G.F.; Vetter, I. No gain, no pain: NaV1.7 as an analgesic target. ACS Chem. Neurosci., 2014, 5(9), 749-751.
[http://dx.doi.org/10.1021/cn500171p] [PMID: 25111714]
[124]
Ashraf, S. Editorial: voltage-gated calcium 2.2 channels: therapeutic target for chronic arthritic pain? Arthritis Rheumatol., 2015, 67(6), 1416-1418.
[http://dx.doi.org/10.1002/art.39092] [PMID: 25733131]
[125]
Altier, C.; Zamponi, G.W. Targeting Ca2+ channels to treat pain: T-type versus N-type. Trends Pharmacol. Sci., 2004, 25(9), 465-470.
[http://dx.doi.org/10.1016/j.tips.2004.07.004] [PMID: 15559248]
[126]
Snutch, T.P.; Zamponi, G.W. Recent advances in the development of T-type calcium channel blockers for pain intervention. Br. J. Pharmacol., 2018, 175(12), 2375-2383.
[http://dx.doi.org/10.1111/bph.13906] [PMID: 28608534]
[127]
Yusaf, S.P.; Goodman, J.; Pinnock, R.D.; Dixon, A.K.; Lee, K. Expression of voltage-gated calcium channel subunits in rat dorsal root ganglion neurons. Neurosci. Lett., 2001, 311(2), 137-141.
[http://dx.doi.org/10.1016/S0304-3940(01)02038-9] [PMID: 11567797]
[128]
Jagodic, M.M.; Pathirathna, S.; Joksovic, P.M.; Lee, W.; Nelson, M.T.; Naik, A.K.; Su, P.; Jevtovic-Todorovic, V.; Todorovic, S.M. Upregulation of the T-type calcium current in small rat sensory neurons after chronic constrictive injury of the sciatic nerve. J. Neurophysiol., 2008, 99(6), 3151-3156.
[http://dx.doi.org/10.1152/jn.01031.2007] [PMID: 18417624]
[129]
Choi, S.; Na, H.S.; Kim, J.; Lee, J.; Lee, S.; Kim, D.; Park, J.; Chen, C.C.; Campbell, K.P.; Shin, H.S. Attenuated pain responses in mice lacking Ca(V)3.2 T-type channels. Genes Brain Behav., 2007, 6(5), 425-431.
[http://dx.doi.org/10.1111/j.1601-183X.2006.00268.x] [PMID: 16939637]
[130]
Shin, H.S.; Cheong, E.J.; Choi, S.; Lee, J.; Na, H.S. T-type Ca2+ channels as therapeutic targets in the nervous system. Curr. Opin. Pharmacol., 2008, 8(1), 33-41.
[http://dx.doi.org/10.1016/j.coph.2007.12.003] [PMID: 18203662]
[131]
Lee, M.J.; Shin, T.J.; Lee, J.E.; Choo, H.; Koh, H.Y.; Chung, H.J.; Pae, A.N.; Lee, S.C.; Kim, H.J. KST5468, a new T-type calcium channel antagonist, has an antinociceptive effect on inflammatory and neuropathic pain models. Pharmacol. Biochem. Behav., 2010, 97(2), 198-204.
[http://dx.doi.org/10.1016/j.pbb.2010.07.018] [PMID: 20678515]
[132]
Kim, D.; Park, D.; Choi, S.; Lee, S.; Sun, M.; Kim, C.; Shin, H.S. Thalamic control of visceral nociception mediated by T-type Ca2+ channels. Science, 2003, 302(5642), 117-119.
[http://dx.doi.org/10.1126/science.1088886] [PMID: 14526084]
[133]
Abe, K.; Kimura, H. The possible role of hydrogen sulfide as an endogenous neuromodulator. J. Neurosci., 1996, 16(3), 1066-1071.
[http://dx.doi.org/10.1523/JNEUROSCI.16-03-01066.1996] [PMID: 8558235]
[134]
Matsunami, M.; Tarui, T.; Mitani, K.; Nagasawa, K.; Fukushima, O.; Okubo, K.; Yoshida, S.; Takemura, M.; Kawabata, A. Luminal hydrogen sulfide plays a pronociceptive role in mouse colon. Gut, 2009, 58(6), 751-761.
[http://dx.doi.org/10.1136/gut.2007.144543] [PMID: 18852258]
[135]
Matsunami, M.; Kirishi, S.; Okui, T.; Kawabata, A. Chelating luminal zinc mimics hydrogen sulfide-evoked colonic pain in mice: possible involvement of T-type calcium channels. Neuroscience, 2011, 181, 257-264.
[http://dx.doi.org/10.1016/j.neuroscience.2011.02.044] [PMID: 21354272]
[136]
Tsubota-Matsunami, M.; Noguchi, Y.; Okawa, Y.; Sekiguchi, F.; Kawabata, A. Colonic hydrogen sulfide-induced visceral pain and referred hyperalgesia involve activation of both Ca(v)3.2 and TRPA1 channels in mice. J. Pharmacol. Sci., 2012, 119(3), 293-296.
[http://dx.doi.org/10.1254/jphs.12086SC] [PMID: 22785020]
[137]
Marger, F.; Gelot, A.; Alloui, A.; Matricon, J.; Ferrer, J.F.S.; Barrère, C.; Pizzoccaro, A.; Muller, E.; Nargeot, J.; Snutch, T.P.; Eschalier, A.; Bourinet, E.; Ardid, D. T-type calcium channels contribute to colonic hypersensitivity in a rat model of irritable bowel syndrome. Proc. Natl. Acad. Sci. USA, 2011, 108(27), 11268-11273.
[http://dx.doi.org/10.1073/pnas.1100869108] [PMID: 21690417]
[138]
Bourinet, E.; Francois, A.; Laffray, S. T-type calcium channels in neuropathic pain. Pain, 2016, 157(Suppl. 1), S15-S22.
[http://dx.doi.org/10.1097/j.pain.0000000000000469] [PMID: 26785151]
[139]
Bladen, C.; Gadotti, V.M.; Gündüz, M.G.; Berger, N.D.; Şimşek, R.; Şafak, C.; Zamponi, G.W. 1,4-Dihydropyridine derivatives with T-type calcium channel blocking activity attenuate inflammatory and neuropathic pain. Pflugers Arch., 2015, 467(6), 1237-1247.
[http://dx.doi.org/10.1007/s00424-014-1566-3] [PMID: 24990197]
[140]
Takahashi, T.; Aoki, Y.; Okubo, K.; Maeda, Y.; Sekiguchi, F.; Mitani, K.; Nishikawa, H.; Kawabata, A. Upregulation of Ca(v)3.2 T-type calcium channels targeted by endogenous hydrogen sulfide contributes to maintenance of neuropathic pain. Pain, 2010, 150(1), 183-191.
[http://dx.doi.org/10.1016/j.pain.2010.04.022] [PMID: 20546998]
[141]
Wen, X.J.; Li, Z.J.; Chen, Z.X.; Fang, Z.Y.; Yang, C.X.; Li, H.; Zeng, Y.M. Intrathecal administration of Cav3.2 and Cav3.3 antisense oligonucleotide reverses tactile allodynia and thermal hyperalgesia in rats following chronic compression of dorsal root of ganglion. Acta Pharmacol. Sin., 2006, 27(12), 1547-1552.
[http://dx.doi.org/10.1111/j.1745-7254.2006.00461.x] [PMID: 17112407]
[142]
Na, H.S.; Choi, S.; Kim, J.; Park, J.; Shin, H.S. Attenuated neuropathic pain in Cav3.1 null mice. Mol. Cells, 2008, 25(2), 242-246.
[PMID: 18414012]
[143]
Wen, X.J.; Xu, S.Y.; Chen, Z.X.; Yang, C.X.; Liang, H.; Li, H. The roles of T-type calcium channel in the development of neuropathic pain following chronic compression of rat dorsal root ganglia. Pharmacology, 2010, 85(5), 295-300.
[http://dx.doi.org/10.1159/000276981] [PMID: 20453553]
[144]
Khomula, E.V.; Viatchenko-Karpinski, V.Y.; Borisyuk, A.L.; Duzhyy, D.E.; Belan, P.V.; Voitenko, N.V. Specific functioning of Cav3.2 T-type calcium and TRPV1 channels under different types of STZ-diabetic neuropathy. Biochim. Biophys. Acta, 2013, 1832(5), 636-649.
[http://dx.doi.org/10.1016/j.bbadis.2013.01.017] [PMID: 23376589]
[145]
Todorovic, S.M.; Jevtovic-Todorovic, V. Targeting of CaV3.2 T-type calcium channels in peripheral sensory neurons for the treatment of painful diabetic neuropathy. Pflugers Arch., 2014, 466(4), 701-706.
[http://dx.doi.org/10.1007/s00424-014-1452-z] [PMID: 24482063]
[146]
Weiss, N.; Black, S.A.; Bladen, C.; Chen, L.; Zamponi, G.W. Surface expression and function of Cav3.2 T-type calcium channels are controlled by asparagine-linked glycosylation. Pflugers Arch., 2013, 465(8), 1159-1170.
[http://dx.doi.org/10.1007/s00424-013-1259-3] [PMID: 23503728]
[147]
Orestes, P.; Osuru, H.P.; McIntire, W.E.; Jacus, M.O.; Salajegheh, R.; Jagodic, M.M.; Choe, W.; Lee, J.; Lee, S.S.; Rose, K.E.; Poiro, N.; Digruccio, M.R.; Krishnan, K.; Covey, D.F.; Lee, J.H.; Barrett, P.Q.; Jevtovic-Todorovic, V.; Todorovic, S.M. Reversal of neuropathic pain in diabetes by targeting glycosylation of Ca(V)3.2 T-type calcium channels. Diabetes, 2013, 62(11), 3828-3838.
[http://dx.doi.org/10.2337/db13-0813] [PMID: 23835327]
[148]
Garcia-Caballero, A.; Gadotti, V.; Weiss, N.; Zamponi, G.W. Treatment of pain by inhibition of USP5 deubiquitinase., U.S. Patent No. WO2014045126A3. 2018.
[149]
Xiao, W.; Naso, L.; Bennett, G.J. Experimental studies of potential analgesics for the treatment of chemotherapy-evoked painful peripheral neuropathies. Pain Med., 2008, 9(5), 505-517.
[http://dx.doi.org/10.1111/j.1526-4637.2007.00301.x] [PMID: 18777607]
[150]
Okubo, K.; Nakanishi, H.; Matsunami, M.; Shibayama, H.; Kawabata, A. Topical application of disodium isostearyl 2-O-L-ascorbyl phosphate, an amphiphilic ascorbic acid derivative, reduces neuropathic hyperalgesia in rats. Br. J. Pharmacol., 2012, 166(3), 1058-1068.
[http://dx.doi.org/10.1111/j.1476-5381.2012.01835.x] [PMID: 22229645]
[151]
Zamponi, G.W.; Bourinet, E.; Snutch, T.P. Nickel block of a family of neuronal calcium channels: subtype- and subunit-dependent action at multiple sites. J. Membr. Biol., 1996, 151(1), 77-90.
[http://dx.doi.org/10.1007/s002329900059] [PMID: 8661496]
[152]
Sun, H.S.; Hui, K.; Lee, D.W.; Feng, Z.P. Zn2+ sensitivity of high- and low-voltage activated calcium channels. Biophys. J., 2007, 93(4), 1175-1183.
[http://dx.doi.org/10.1529/biophysj.106.103333] [PMID: 17526568]
[153]
Traboulsie, A.; Chemin, J.; Chevalier, M.; Quignard, J.F.; Nargeot, J.; Lory, P. Subunit-specific modulation of T-type calcium channels by zinc. J. Physiol., 2007, 578(Pt 1), 159-171.
[http://dx.doi.org/10.1113/jphysiol.2006.114496] [PMID: 17082234]
[154]
Noh, J.; Kim, M.K.; Chung, J.M. A novel mechanism of zinc block on alpha1G-like low-threshold T-type Ca2+ channels in a rat thalamic relay neuron. Neurosci. Res., 2010, 66(4), 353-358.
[http://dx.doi.org/10.1016/j.neures.2009.12.005] [PMID: 20025910]
[155]
Lacinová, L.; Klugbauer, N.; Hofmann, F. Regulation of the calcium channel alpha(1G) subunit by divalent cations and organic blockers. Neuropharmacology, 2000, 39(7), 1254-1266.
[http://dx.doi.org/10.1016/S0028-3908(99)00202-6] [PMID: 10760367]
[156]
Shafer, T.J. Effects of Cd2+, Pb2+ and CH3Hg+ on high voltage-activated calcium currents in pheochromocytoma (PC12) cells: potency, reversibility, interactions with extracellular Ca2+ and mechanisms of block. Toxicol. Lett., 1998, 99(3), 207-221.
[http://dx.doi.org/10.1016/S0378-4274(98)00225-2] [PMID: 9862287]
[157]
Obejero-Paz, C.A.; Gray, I.P.; Jones, S.W. Y3+ block demonstrates an intracellular activation gate for the alpha1G T-type Ca2+ channel. J. Gen. Physiol., 2004, 124(6), 631-640.
[http://dx.doi.org/10.1085/jgp.200409167] [PMID: 15572343]
[158]
Mlinar, B.; Enyeart, J.J. Block of current through T-type calcium channels by trivalent metal cations and nickel in neural rat and human cells. J. Physiol., 1993, 469, 639-652.
[http://dx.doi.org/10.1113/jphysiol.1993.sp019835] [PMID: 8271221]
[159]
Beedle, A.M.; Hamid, J.; Zamponi, G.W. Inhibition of transiently expressed low- and high-voltage-activated calcium channels by trivalent metal cations. J. Membr. Biol., 2002, 187(3), 225-238.
[http://dx.doi.org/10.1007/s00232-001-0166-2] [PMID: 12163980]
[160]
Monteil, A.; Chemin, J.; Leuranguer, V.; Altier, C.; Mennessier, G.; Bourinet, E.; Lory, P.; Nargeot, J. Specific properties of T-type calcium channels generated by the human alpha 1I subunit. J. Biol. Chem., 2000, 275(22), 16530-16535.
[http://dx.doi.org/10.1074/jbc.C000090200] [PMID: 10749850]
[161]
Lee, J.H.; Gomora, J.C.; Cribbs, L.L.; Perez-Reyes, E. Nickel block of three cloned T-type calcium channels: low concentrations selectively block alpha1H. Biophys. J., 1999, 77(6), 3034-3042.
[http://dx.doi.org/10.1016/S0006-3495(99)77134-1] [PMID: 10585925]
[162]
Perchenet, L.; Bénardeau, A.; Ertel, E.A. Pharmacological properties of Ca(V)3.2, a low voltage-activated Ca2+ channel cloned from human heart. Naunyn Schmiedebergs Arch. Pharmacol., 2000, 361(6), 590-599.
[http://dx.doi.org/10.1007/s002100000238] [PMID: 10882033]
[163]
Thévenod, F.; Jones, S.W. Cadmium block of calcium current in frog sympathetic neurons. Biophys. J., 1992, 63(1), 162-168.
[http://dx.doi.org/10.1016/S0006-3495(92)81575-8] [PMID: 1330026]
[164]
Díaz, D.; Bartolo, R.; Delgadillo, D.M.; Higueldo, F.; Gomora, J.C. Contrasting effects of Cd2+ and Co2+ on the blocking/unblocking of human Cav3 channels. J. Membr. Biol., 2005, 207(2), 91-105.
[http://dx.doi.org/10.1007/s00232-005-0804-1] [PMID: 16477530]
[165]
Wakamori, M.; Strobeck, M.; Niidome, T.; Teramoto, T.; Imoto, K.; Mori, Y. Functional characterization of ion permeation pathway in the N-type Ca2+ channel. J. Neurophysiol., 1998, 79(2), 622-634.
[http://dx.doi.org/10.1152/jn.1998.79.2.622] [PMID: 9463426]
[166]
McDonough, S.I.; Bean, B.P. Mibefradil inhibition of T-type calcium channels in cerebellar purkinje neurons. Mol. Pharmacol., 1998, 54(6), 1080-1087.
[http://dx.doi.org/10.1124/mol.54.6.1080] [PMID: 9855637]
[167]
Francois, A.; Kerckhove, N.; Meleine, M.; Alloui, A.; Barrere, C.; Gelot, A.; Uebele, V.N.; Renger, J.J.; Eschalier, A.; Ardid, D.; Bourinet, E. State-dependent properties of a new T-type calcium channel blocker enhance Ca(V)3.2 selectivity and support analgesic effects. Pain, 2013, 154(2), 283-293.
[http://dx.doi.org/10.1016/j.pain.2012.10.023] [PMID: 23257507]
[168]
Martin, R.L.; Lee, J.H.; Cribbs, L.L.; Perez-Reyes, E.; Hanck, D.A. Mibefradil block of cloned T-type calcium channels. J. Pharmacol. Exp. Ther., 2000, 295(1), 302-308.
[PMID: 10991994]
[169]
Mehrke, G.; Zong, X.G.; Flockerzi, V.; Hofmann, F. The Ca(++)-channel blocker Ro 40-5967 blocks differently T-type and L-type Ca++ channels. J. Pharmacol. Exp. Ther., 1994, 271(3), 1483-1488.
[PMID: 7996461]
[170]
Uebele, V.N.; Nuss, C.E.; Fox, S.V.; Garson, S.L.; Cristescu, R.; Doran, S.M.; Kraus, R.L.; Santarelli, V.P.; Li, Y.; Barrow, J.C.; Yang, Z.Q.; Schlegel, K.A.; Rittle, K.E.; Reger, T.S.; Bednar, R.A.; Lemaire, W.; Mullen, F.A.; Ballard, J.E.; Tang, C.; Dai, G.; McManus, O.B.; Koblan, K.S.; Renger, J.J. Positive allosteric interaction of structurally diverse T-type calcium channel antagonists. Cell Biochem. Biophys., 2009, 55(2), 81-93.
[http://dx.doi.org/10.1007/s12013-009-9057-4] [PMID: 19582593]
[171]
Kopecky, B.J.; Liang, R.; Bao, J. T-type calcium channel blockers as neuroprotective agents. Pflugers Arch., 2014, 466(4), 757-765.
[http://dx.doi.org/10.1007/s00424-014-1454-x] [PMID: 24563219]
[172]
Inayoshi, A.; Sugimoto, Y.; Funahashi, J.; Takahashi, S.; Matsubara, M.; Kusaka, H. Mechanism underlying the block of human Cav3.2 T-type Ca2+ channels by benidipine, a dihydropyridine Ca2+ channel blocker. Life Sci., 2011, 88(19-20), 898-907.
[http://dx.doi.org/10.1016/j.lfs.2011.03.019] [PMID: 21466810]
[173]
Furukawa, T.; Miura, R.; Honda, M.; Kamiya, N.; Mori, Y.; Takeshita, S.; Isshiki, T.; Nukada, T. Identification of R(-)-isomer of efonidipine as a selective blocker of T-type Ca2+ channels. Br. J. Pharmacol., 2004, 143(8), 1050-1057.
[http://dx.doi.org/10.1038/sj.bjp.0705944] [PMID: 15545287]
[174]
Perez-Reyes, E.; Van Deusen, A.L.; Vitko, I. Molecular pharmacology of human Cav3.2 T-type Ca2+ channels: block by antihypertensives, antiarrhythmics, and their analogs. J. Pharmacol. Exp. Ther., 2009, 328(2), 621-627.
[http://dx.doi.org/10.1124/jpet.108.145672] [PMID: 18974361]
[175]
Santi, C.M.; Cayabyab, F.S.; Sutton, K.G.; McRory, J.E.; Mezeyova, J.; Hamming, K.S.; Parker, D.; Stea, A.; Snutch, T.P. Differential inhibition of T-type calcium channels by neuroleptics. J. Neurosci., 2002, 22(2), 396-403.
[http://dx.doi.org/10.1523/JNEUROSCI.22-02-00396.2002] [PMID: 11784784]
[176]
Belardetti, F.; Tringham, E.; Eduljee, C.; Jiang, X.; Dong, H.; Hendricson, A.; Shimizu, Y.; Janke, D.L.; Parker, D.; Mezeyova, J.; Khawaja, A.; Pajouhesh, H.; Fraser, R.A.; Arneric, S.P.; Snutch, T.P. A fluorescence-based high-throughput screening assay for the identification of T-type calcium channel blockers. Assay Drug Dev. Technol., 2009, 7(3), 266-280.
[http://dx.doi.org/10.1089/adt.2009.191] [PMID: 19530894]
[177]
Enyeart, J.J.; Biagi, B.A.; Day, R.N.; Sheu, S.S.; Maurer, R.A. Blockade of low and high threshold Ca2+ channels by diphenylbutylpiperidine antipsychotics linked to inhibition of prolactin gene expression. J. Biol. Chem., 1990, 265(27), 16373-16379.
[PMID: 1697857]
[178]
Ijjaali, I.; Barrere, C.; Nargeot, J.; Petitet, F.; Bourinet, E. Ligand-based virtual screening to identify new T-type calcium channel blockers. Channels (Austin), 2007, 1(4), 300-304.
[http://dx.doi.org/10.4161/chan.4999] [PMID: 18708747]
[179]
Bertolesi, G.E.; Shi, C.; Elbaum, L.; Jollimore, C.; Rozenberg, G.; Barnes, S.; Kelly, M.E. The Ca(2+) channel antagonists mibefradil and pimozide inhibit cell growth via different cytotoxic mechanisms. Mol. Pharmacol., 2002, 62(2), 210-219.
[http://dx.doi.org/10.1124/mol.62.2.210] [PMID: 12130671]
[180]
Todorovic, S.M.; Perez-Reyes, E.; Lingle, C.J. Anticonvulsants but not general anesthetics have differential blocking effects on different T-type current variants. Mol. Pharmacol., 2000, 58(1), 98-108.
[http://dx.doi.org/10.1124/mol.58.1.98] [PMID: 10860931]
[181]
Peduto, V.A.; Concas, A.; Santoro, G.; Biggio, G.; Gessa, G.L. Biochemical and electrophysiologic evidence that propofol enhances GABAergic transmission in the rat brain. Anesthesiology, 1991, 75(6), 1000-1009.
[http://dx.doi.org/10.1097/00000542-199112000-00012] [PMID: 1660227]
[182]
Jarvis, M.F.; Scott, V.E.; McGaraughty, S.; Chu, K.L.; Xu, J.; Niforatos, W.; Milicic, I.; Joshi, S.; Zhang, Q.; Xia, Z. A peripherally acting, selective T-type calcium channel blocker, ABT-639, effectively reduces nociceptive and neuropathic pain in rats. Biochem. Pharmacol., 2014, 89(4), 536-544.
[http://dx.doi.org/10.1016/j.bcp.2014.03.015] [PMID: 24726441]
[183]
Serra, J.; Duan, W.R.; Locke, C.; Solà, R.; Liu, W.; Nothaft, W. Effects of a T-type calcium channel blocker, ABT-639, on spontaneous activity in C-nociceptors in patients with painful diabetic neuropathy: a randomized controlled trial. Pain, 2015, 156(11), 2175-2183.
[http://dx.doi.org/10.1097/j.pain.0000000000000249] [PMID: 26035253]
[184]
Ziegler, D.; Duan, W.R.; An, G.; Thomas, J.W.; Nothaft, W. A randomized double-blind, placebo-, and active-controlled study of T-type calcium channel blocker ABT-639 in patients with diabetic peripheral neuropathic pain. Pain, 2015, 156(10), 2013-2020.
[http://dx.doi.org/10.1097/j.pain.0000000000000263] [PMID: 26067585]
[185]
Wallace, M.; Duan, R.; Liu, W.; Locke, C.; Nothaft, W. A randomized, double-blind, placebo-controlled, crossover study of the T-type calcium channel blocker ABT-639 in an intradermal capsaicin experimental pain model in healthy adults. Pain Med., 2016, 17(3), 551-560.
[http://dx.doi.org/10.1093/pm/pnv068] [PMID: 26814294]
[186]
Egan, M.F.; Zhao, X.; Smith, A.; Troyer, M.D.; Uebele, V.N.; Pidkorytov, V.; Cox, K.; Murphy, M.; Snavely, D.; Lines, C.; Michelson, D. Randomized controlled study of the T-type calcium channel antagonist MK-8998 for the treatment of acute psychosis in patients with schizophrenia. Hum. Psychopharmacol., 2013, 28(2), 124-133.
[http://dx.doi.org/10.1002/hup.2289] [PMID: 23532746]
[187]
Lee, M. Z944: a first in class T-type calcium channel modulator for the treatment of pain. J. Peripher. Nerv. Syst., 2014, 19(Suppl. 2), S11-S12.
[http://dx.doi.org/10.1111/jns.12080_2] [PMID: 25269728]
[188]
Bezençon, O.; Heidmann, B.; Siegrist, R.; Stamm, S.; Richard, S.; Pozzi, D.; Corminboeuf, O.; Roch, C.; Kessler, M.; Ertel, E.A.; Reymond, I.; Pfeifer, T.; de Kanter, R.; Toeroek-Schafroth, M.; Moccia, L.G.; Mawet, J.; Moon, R.; Rey, M.; Capeleto, B.; Fournier, E. Toeroek- Schafroth, M.; Moccia, L.G.; Mawet, J.; Moon, R.; Rey, M.; Capeleto, B.; Fournier, E. Discovery of a potent, selective T-type calcium channel blocker as a drug candidate for the treatment of generalized epilepsies. J. Med. Chem., 2017, 60(23), 9769-9789.
[http://dx.doi.org/10.1021/acs.jmedchem.7b01236] [PMID: 29116786]
[189]
Uslaner, J.M.; Smith, S.M.; Huszar, S.L.; Pachmerhiwala, R.; Hinchliffe, R.M.; Vardigan, J.D.; Nguyen, S.J.; Surles, N.O.; Yao, L.; Barrow, J.C.; Uebele, V.N.; Renger, J.J.; Clark, J.; Hutson, P.H. T-type calcium channel antagonism produces antipsychotic-like effects and reduces stimulant-induced glutamate release in the nucleus accumbens of rats. Neuropharmacology, 2012, 62(3), 1413-1421.
[http://dx.doi.org/10.1016/j.neuropharm.2010.11.015] [PMID: 21110986]
[190]
Kraus, R.L.; Li, Y.; Gregan, Y.; Gotter, A.L.; Uebele, V.N.; Fox, S.V.; Doran, S.M.; Barrow, J.C.; Yang, Z-Q.; Reger, T.S.; Koblan, K.S.; Renger, J.J. In vitro characterization of T-type calcium channel antagonist TTA-A2 and in vivo effects on arousal in mice. J. Pharmacol. Exp. Ther., 2010, 335(2), 409-417.
[http://dx.doi.org/10.1124/jpet.110.171058] [PMID: 20682849]
[191]
Heo, J.H.; Seo, H.N.; Choe, Y.J.; Kim, S.; Oh, C.R.; Kim, Y.D.; Rhim, H.; Choo, D.J.; Kim, J.; Lee, J.Y. T-type Ca2+ channel blockers suppress the growth of human cancer cells. Bioorg. Med. Chem. Lett., 2008, 18(14), 3899-3901.
[http://dx.doi.org/10.1016/j.bmcl.2008.06.034] [PMID: 18585035]
[192]
Kang, H.B.; Rim, H.K.; Park, J.Y.; Choi, H.W.; Choi, D.L.; Seo, J.H.; Chung, K.S.; Huh, G.; Kim, J.; Choo, D.J.; Lee, K.T.; Lee, J.Y. In vivo evaluation of oral anti-tumoral effect of 3,4-dihydroquinazoline derivative on solid tumor. Bioorg. Med. Chem. Lett., 2012, 22(2), 1198-1201.
[http://dx.doi.org/10.1016/j.bmcl.2011.11.083] [PMID: 22177784]
[193]
M’Dahoma, S.; Gadotti, V.M.; Zhang, F.X.; Park, B.; Nam, J.H.; Onnis, V.; Balboni, G.; Lee, J.Y.; Zamponi, G.W. Effect of the T-type channel blocker KYS-05090S in mouse models of acute and neuropathic pain. Pflugers Arch., 2016, 468(2), 193-199.
[http://dx.doi.org/10.1007/s00424-015-1733-1] [PMID: 26354962]
[194]
You, H.; Gadotti, V.M.; Petrov, R.R.; Zamponi, G.W.; Diaz, P. Functional characterization and analgesic effects of mixed cannabinoid receptor/T-type channel ligands. Mol. Pain, 2011, 7, 89.
[http://dx.doi.org/10.1186/1744-8069-7-89] [PMID: 22093952]
[195]
Berger, N.D.; Gadotti, V.M.; Petrov, R.R.; Chapman, K.; Diaz, P.; Zamponi, G.W. NMP-7 inhibits chronic inflammatory and neuropathic pain via block of Cav3.2 T-type calcium channels and activation of CB2 receptors. Mol. Pain, 2014, 10, 77.
[http://dx.doi.org/10.1186/1744-8069-10-77] [PMID: 25481027]
[196]
Stolberg, S.G. Heart drug withdrawn as evidence shows it could be lethal. New York Times, 1998.
[197]
Huang, W.; Lu, C.; Wu, Y.; Ouyang, S.; Chen, Y. T-type calcium channel antagonists, mibefradil and NNC-55-0396 inhibit cell proliferation and induce cell apoptosis in leukemia cell lines. J. Exp. Clin. Cancer Res., 2015, 34, 54.
[http://dx.doi.org/10.1186/s13046-015-0171-4] [PMID: 25989794]
[198]
Ma, G.; Allen, T.J.; Cooper, M.E.; Cao, Z. Calcium channel blockers, either amlodipine or mibefradil, ameliorate renal injury in experimental diabetes. Kidney Int., 2004, 66(3), 1090-1098.
[http://dx.doi.org/10.1111/j.1523-1755.2004.00859.x] [PMID: 15327403]
[199]
Ozawa, Y.; Hayashi, K.; Nagahama, T.; Fujiwara, K.; Saruta, T. Effect of T-type selective calcium antagonist on renal microcirculation: studies in the isolated perfused hydronephrotic kidney. Hypertension, 2001, 38(3), 343-347.
[http://dx.doi.org/10.1161/01.HYP.38.3.343] [PMID: 11566902]
[200]
Hayashi, K.; Wakino, S.; Homma, K.; Sugano, N.; Saruta, T. Pathophysiological significance of T-type Ca2+ channels: role of T-type Ca2+ channels in renal microcirculation. J. Pharmacol. Sci., 2005, 99(3), 221-227.
[http://dx.doi.org/10.1254/jphs.FMJ05002X6] [PMID: 16293936]
[201]
Ohishi, M.; Takagi, T.; Ito, N.; Terai, M.; Tatara, Y.; Hayashi, N.; Shiota, A.; Katsuya, T.; Rakugi, H.; Ogihara, T. Renal-protective effect of T-and L-type calcium channel blockers in hypertensive patients: an amlodipine-to-benidipine crhangeover (ABC) study. Hypertens. Res., 2007, 30(9), 797-806.
[http://dx.doi.org/10.1291/hypres.30.797] [PMID: 18037772]
[202]
Sasaki, H.; Saiki, A.; Endo, K.; Ban, N.; Yamaguchi, T.; Kawana, H.; Nagayama, D.; Ohhira, M.; Oyama, T.; Miyashita, Y.; Shirai, K. Protective effects of efonidipine, a T- and L-type calcium channel blocker, on renal function and arterial stiffness in type 2 diabetic patients with hypertension and nephropathy. J. Atheroscler. Thromb., 2009, 16(5), 568-575.
[http://dx.doi.org/10.5551/jat.1628] [PMID: 19749494]
[203]
Chemin, J.; Monteil, A.; Perez-Reyes, E.; Nargeot, J.; Lory, P. Direct inhibition of T-type calcium channels by the endogenous cannabinoid anandamide. EMBO J., 2001, 20(24), 7033-7040.
[http://dx.doi.org/10.1093/emboj/20.24.7033] [PMID: 11742980]
[204]
Barbara, G.; Alloui, A.; Nargeot, J.; Lory, P.; Eschalier, A.; Bourinet, E.; Chemin, J. T-type calcium channel inhibition underlies the analgesic effects of the endogenous lipoamino acids. J. Neurosci., 2009, 29(42), 13106-13114.
[http://dx.doi.org/10.1523/JNEUROSCI.2919-09.2009] [PMID: 19846698]
[205]
Singh, A.; Hildebrand, M.E.; Garcia, E.; Snutch, T.P. The transient receptor potential channel antagonist SKF96365 is a potent blocker of low-voltage-activated T-type calcium channels. Br. J. Pharmacol., 2010, 160(6), 1464-1475.
[http://dx.doi.org/10.1111/j.1476-5381.2010.00786.x] [PMID: 20590636]
[206]
Casillas-Espinosa, P.M.; Hicks, A.; Jeffreys, A.; Snutch, T.P.; O’Brien, T.J.; Powell, K.L. Z944, a novel selective ttype calcium channel antagonist delays the progression of seizures in the amygdala kindling model. PLoS One, 2015, 10(8) e0130012
[http://dx.doi.org/10.1371/journal.pone.0130012] [PMID: 26274319]
[207]
Lee, J.; Kim, D.; Shin, H.S. Lack of delta waves and sleep disturbances during non-rapid eye movement sleep in mice lacking alpha1G-subunit of T-type calcium channels. Proc. Natl. Acad. Sci. USA, 2004, 101(52), 18195-18199.
[http://dx.doi.org/10.1073/pnas.0408089101] [PMID: 15601764]
[208]
Anderson, M.P.; Mochizuki, T.; Xie, J.; Fischler, W.; Manger, J.P.; Talley, E.M.; Scammell, T.E.; Tonegawa, S. Thalamic Cav3.1 T-type Ca2+ channel plays a crucial role in stabilizing sleep. Proc. Natl. Acad. Sci. USA, 2005, 102(5), 1743-1748.
[http://dx.doi.org/10.1073/pnas.0409644102] [PMID: 15677322]
[209]
Nordskog, B.K.; Hammarback, J.A.; Godwin, D.W. Diurnal gene expression patterns of T-type calcium channels and their modulation by ethanol. Neuroscience, 2006, 141(3), 1365-1373.
[http://dx.doi.org/10.1016/j.neuroscience.2006.04.031] [PMID: 16750304]
[210]
Deleuze, C.; David, F.; Béhuret, S.; Sadoc, G.; Shin, H-S.; Uebele, V.N.; Renger, J.J.; Lambert, R.C.; Leresche, N.; Bal, T. T-type calcium channels consolidate tonic action potential output of thalamic neurons to neocortex. J. Neurosci., 2012, 32(35), 12228-12236.
[http://dx.doi.org/10.1523/JNEUROSCI.1362-12.2012] [PMID: 22933804]
[211]
Lambert, R.C.; Bessaïh, T.; Crunelli, V.; Leresche, N. The many faces of T-type calcium channels. Pflugers Arch., 2014, 466(3), 415-423.
[http://dx.doi.org/10.1007/s00424-013-1353-6] [PMID: 24043572]
[212]
Flatters, S.J.; Bennett, G.J. Ethosuximide reverses paclitaxel- and vincristine-induced painful peripheral neuropathy. Pain, 2004, 109(1-2), 150-161.
[http://dx.doi.org/10.1016/j.pain.2004.01.029] [PMID: 15082137]
[213]
Hamidi, G.A.; Ramezani, M.H.; Arani, M.N.; Talaei, S.A.; Mesdaghinia, A.; Banafshe, H.R. Ethosuximide reduces allodynia and hyperalgesia and potentiates morphine effects in the chronic constriction injury model of neuropathic pain. Eur. J. Pharmacol., 2012, 674(2-3), 260-264.
[http://dx.doi.org/10.1016/j.ejphar.2011.11.026] [PMID: 22134003]
[214]
Kerckhove, N.; Mallet, C.; Pereira, B.; Chenaf, C.; Duale, C.; Dubray, C.; Eschalier, A. Assessment of the effectiveness and safety of Ethosuximide in the Treatment of non-Diabetic Peripheral Neuropathic Pain: EDONOT-protocol of a randomised, parallel, controlled, double-blinded and multicentre clinical trial. BMJ Open, 2016, 6(12) e013530
[http://dx.doi.org/10.1136/bmjopen-2016-013530] [PMID: 27986742]
[215]
Chuang, R.S.; Jaffe, H.; Cribbs, L.; Perez-Reyes, E.; Swartz, K.J. Inhibition of T-type voltage-gated calcium channels by a new scorpion toxin. Nat. Neurosci., 1998, 1(8), 668-674.
[http://dx.doi.org/10.1038/3669] [PMID: 10196582]
[216]
Sidach, S.S.; Mintz, I.M. Kurtoxin, a gating modifier of neuronal high- and low-threshold ca channels. J. Neurosci., 2002, 22(6), 2023-2034.
[http://dx.doi.org/10.1523/JNEUROSCI.22-06-02023.2002] [PMID: 11896142]
[217]
Zhu, H.L.; Wassall, R.D.; Cunnane, T.C.; Teramoto, N. Actions of kurtoxin on tetrodotoxin-sensitive voltage-gated Na+ currents, NaV1.6, in murine vas deferens myocytes. Naunyn Schmiedebergs Arch. Pharmacol., 2009, 379(5), 453-460.
[http://dx.doi.org/10.1007/s00210-008-0385-5] [PMID: 19127357]
[218]
Olamendi-Portugal, T.; García, B.I.; López-González, I.; Van Der Walt, J.; Dyason, K.; Ulens, C.; Tytgat, J.; Felix, R.; Darszon, A.; Possani, L.D. Two new scorpion toxins that target voltage-gated Ca2+ and Na+ channels. Biochem. Biophys. Res. Commun., 2002, 299(4), 562-568.
[http://dx.doi.org/10.1016/S0006-291X(02)02706-7] [PMID: 12459175]
[219]
López-González, I.; Olamendi-Portugal, T.; De la Vega-Beltrán, J.L.; Van der Walt, J.; Dyason, K.; Possani, L.D.; Felix, R.; Darszon, A. Scorpion toxins that block T-type Ca2+ channels in spermatogenic cells inhibit the sperm acrosome reaction. Biochem. Biophys. Res. Commun., 2003, 300(2), 408-414.
[http://dx.doi.org/10.1016/S0006-291X(02)02859-0] [PMID: 12504099]
[220]
Kraus, R.; Warren, V.; Smith, M.; Middleton, R.; Blumenthal, K.; Cohen, C. A spider toxin that inhibits activation of voltage-gated sodium channels. Biophys. J., 2002, 85A-85A.
[221]
Priest, B.T.; Blumenthal, K.M.; Smith, J.J.; Warren, V.A.; Smith, M.M. ProTx-I and ProTx-II: gating modifiers of voltage-gated sodium channels. Toxicon, 2007, 49(2), 194-201.
[http://dx.doi.org/10.1016/j.toxicon.2006.09.014] [PMID: 17087985]
[222]
Schmalhofer, W.A.; Calhoun, J.; Burrows, R.; Bailey, T.; Kohler, M.G.; Weinglass, A.B.; Kaczorowski, G.J.; Garcia, M.L.; Koltzenburg, M.; Priest, B.T. ProTx-II, a selective inhibitor of NaV1.7 sodium channels, blocks action potential propagation in nociceptors. Mol. Pharmacol., 2008, 74(5), 1476-1484.
[http://dx.doi.org/10.1124/mol.108.047670] [PMID: 18728100]
[223]
Kraus, R.; Warren, V.; Smith, M.; Middleton, R.; Cohen, C. Modulation of a1G and a1C by the spider toxin ProTx-II. In Soc. Neurosci. Abstr., 2000, 26, 623.
[224]
Bladen, C.; Hamid, J.; Souza, I.A.; Zamponi, G.W. Block of T-type calcium channels by protoxins I and II. Mol. Brain, 2014, 7, 36.
[http://dx.doi.org/10.1186/1756-6606-7-36] [PMID: 24886690]
[225]
Ohkubo, T.; Yamazaki, J.; Kitamura, K. Tarantula toxin ProTx-I differentiates between human T-type voltage-gated Ca2+ Channels Cav3.1 and Cav3.2. J. Pharmacol. Sci., 2010, 112(4), 452-458.
[http://dx.doi.org/10.1254/jphs.09356FP] [PMID: 20351484]
[226]
Cardoso, F.C.; Dekan, Z.; Smith, J.J.; Deuis, J.R.; Vetter, I.; Herzig, V.; Alewood, P.F.; King, G.F.; Lewis, R.J. Modulatory features of the novel spider toxin μ-TRTX-Df1a isolated from the venom of the spider Davus fasciatus. Br. J. Pharmacol., 2017, 174(15), 2528-2544.
[http://dx.doi.org/10.1111/bph.13865] [PMID: 28542706]
[227]
Bourinet, E.; Escoubas, P.; Marger, F.; Nargeot, J.; Lazdunski, M. Identification of novel antagonist toxins of T-type calcium channel for analgesic purposes., U.S. Patent No. EP2387581B1. 2014.
[228]
Bourinet, E.; Zamponi, G.W. Block of voltage-gated calcium channels by peptide toxins. Neuropharmacology, 2017, 127, 109-115.
[http://dx.doi.org/10.1016/j.neuropharm.2016.10.016] [PMID: 27756538]
[229]
Mary, R.; Giribaldi, J.; Lesport, P.; Bourinet, E.; Dutertre, S. Discovery, synthesis and characterization of PmuTx1-a new spider toxin that blocks T-type calcium channels CaV3.2. Toxicon, 2018, 149, 101.
[http://dx.doi.org/10.1016/j.toxicon.2018.02.019]
[230]
Gray, L.S.; Macdonald, T.L. The pharmacology and regulation of T type calcium channels: new opportunities for unique therapeutics for cancer. Cell Calcium, 2006, 40(2), 115-120.
[http://dx.doi.org/10.1016/j.ceca.2006.04.014] [PMID: 16806465]
[231]
Rossier, M.F. T-type calcium channel: a privileged gate for calcium entry and control of adrenal steroidogenesis. Front. Endocrinol. (Lausanne), 2016, 7, 43.
[http://dx.doi.org/10.3389/fendo.2016.00043] [PMID: 27242667]
[232]
Barrow, J.C.; Rittle, K.E.; Reger, T.S.; Yang, Z.Q.; Bondiskey, P.; McGaughey, G.B.; Bock, M.G.; Hartman, G.D.; Tang, C.; Ballard, J.; Kuo, Y.; Prueksaritanont, T.; Nuss, C.E.; Doran, S.M.; Fox, S.V.; Garson, S.L.; Kraus, R.L.; Li, Y.; Marino, M.J.; Kuzmick Graufelds, V.; Uebele, V.N.; Renger, J.J. Discovery of 4, 4-disubstituted quinazolin- 2-ones as T-type calcium channel antagonists. ACS Med. Chem. Lett., 2010, 1(2), 75-79.
[http://dx.doi.org/10.1021/ml100004r] [PMID: 24900180]
[233]
Xie, X.; Van Deusen, A.L.; Vitko, I.; Babu, D.A.; Davies, L.A.; Huynh, N.; Cheng, H.; Yang, N.; Barrett, P.Q.; Perez-Reyes, E. Validation of high throughput screening assays against three subtypes of Ca(v)3 T-type channels using molecular and pharmacologic approaches. Assay Drug Dev. Technol., 2007, 5(2), 191-203.
[http://dx.doi.org/10.1089/adt.2006.054] [PMID: 17477828]
[234]
Chavez-Colorado, E.; Herrera-Carrillo, Z.; Gomora, J.C. Blocking of T-Type calcium channels by TTA-A2 reveals a conservative binding site for state-dependent antagonists. Biophys. J., 2016, 110, 439a-440a.
[http://dx.doi.org/10.1016/j.bpj.2015.11.2369]
[235]
Schaller, D.; Gündüz, M.G.; Zhang, F.X.; Zamponi, G.W.; Wolber, G. Binding mechanism investigations guiding the synthesis of novel condensed 1,4-dihydropyridine derivatives with L-/T-type calcium channel blocking activity. Eur. J. Med. Chem., 2018, 155, 1-12.
[http://dx.doi.org/10.1016/j.ejmech.2018.05.032] [PMID: 29843108]


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VOLUME: 27
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Year: 2020
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