Physiology and Pathology of Voltage-Gated T-Type Calcium Channels

  • Adriano Senatore
  • J. David SpaffordEmail author


T-type channels are low voltage-activated members of the calcium channel family that also includes the high voltage-activated Cav1 and Cav2 channels. T-type channels open with only minimal depolarization or in response to hyperpolarization of the cell membrane and are associated with regulating excitability and pacemaking at subthreshold voltages. Interestingly, increasing evidence suggests that the subthreshold properties of T-type channels are exploited for other cellular processes including low-threshold synaptic vesicle release (excitation-secretion coupling), myocyte contraction and tone (excitation-contraction coupling), and cell cycle control. T-type channels are implicated in several pathologies including epilepsy, autism, sleep disturbances, pain, hypertension, and cancer. With the advent of novel blockers selective for T-type channels, their important contributions to normal cellular/organismal physiology, as well as to pathology, are becoming clearer.


Autism Spectrum Disorder Window Current Cav2 Channel Childhood Absence Epilepsy Myocyte Contraction 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Anderson MP, Mochizuki T, Xie J, Fischler W, Manger JP, Talley EM, Scammell TE, Tonegawa S (2005) Thalamic Cav3.1 T-type Ca2+ channel plays a crucial role in stabilizing sleep. Proc Natl Acad Sci USA 102:1743–1748PubMedCentralPubMedCrossRefGoogle Scholar
  2. Anderson D, Mehaffey WH, Iftinca M, Rehak R, Engbers JD, Hameed S, Zamponi GW, Turner RW (2010) Regulation of neuronal activity by Cav3-Kv4 channel signaling complexes. Nat Neurosci 13:333–337PubMedCrossRefGoogle Scholar
  3. Angstadt JD, Calabrese RL (1989) A hyperpolarization-activated inward current in heart interneurons on the medicinal leech. J Neurosci 9:2846–2857PubMedGoogle Scholar
  4. Arias-Olguín II, Vitko I, Fortuna M, Baumgart JP, Sokolova S, Shumilin IA, Van Deusen A, Soriano-García M, Gomora JC, Perez-Reyes E (2008) Characterization of the gating brake in the I-II loop of Cav3.2 T-type Ca2+ channels. J Biol Chem 283:8136–8144PubMedCentralPubMedCrossRefGoogle Scholar
  5. Boehme R, Uebele VN, Renger JJ, Pedroarena C (2011) Rebound excitation triggered by synaptic inhibition in cerebellar nuclear neurons is suppressed by selective T-type calcium channel block. J Neurophysiol 106:2653–2661PubMedCrossRefGoogle Scholar
  6. Bourinet E, Alloui A, Monteil A, Barrère C, Couette B, Poirot O, Pages A, McRory J, Snutch TP, Eschalier A, Nargeot J (2005) Silencing of the Cav3.2 T-type calcium channel gene in sensory neurons demonstrates its major role in nociception. EMBO J 24:315–324PubMedCentralPubMedCrossRefGoogle Scholar
  7. Broicher T, Kanyshkova T, Meuth P, Pape H-C, Budde T (2008) Correlation of T-channel coding gene expression, I-T, and the low threshold Ca2+ spike in the thalamus of a rat model of absence epilepsy. Mol Cell Neurosci 39:384–399PubMedCrossRefGoogle Scholar
  8. Carbone E, Giancippoli A, Marcantoni A, Guido D, Carabelli V (2006) A new role for T-type channels in fast “low-threshold” exocytosis. Cell Calcium 40:147–154PubMedCrossRefGoogle Scholar
  9. Catterall WA (2010) Ion channel voltage sensors: structure, function, and pathophysiology. Neuron 67:915–928PubMedCentralPubMedCrossRefGoogle Scholar
  10. Cazade M, Bidaud I, Hansen PB, Lory P, Chemin J (2013) 5,6-EET potently inhibits T-type calcium channels: implication in the regulation of the vascular tone. Pflügers ArchGoogle Scholar
  11. Chen CC, Lamping KG, Nuno DW, Barresi R, Prouty SJ, Lavoie JL, Cribbs LL, England SK, Sigmund CD, Weiss RM, Williamson RA, Hill JA, Campbell KP (2003) Abnormal coronary function in mice deficient in α 1H T-type Ca2+ channels. Science 302:1416–1418PubMedCrossRefGoogle Scholar
  12. Cheng RC, Tikhonov DB, Zhorov BS (2010) Structural modeling of calcium binding in the selectivity filter of the L-type calcium channel. Eur Biophys J 39:839–853PubMedCrossRefGoogle Scholar
  13. Cheong E, Lee S, Choi BJ, Sun M, Lee CJ, Shin HS (2008) Tuning thalamic firing modes via simultaneous modulation of T- and L-Type Ca2+ channels controls pain sensory gating in the thalamus. J Neurosci 28:13331–13340PubMedCrossRefGoogle Scholar
  14. Chiang CS, Huang CH, Chieng H, Chang YT, Chang D, Chen JJ, Chen YC, Chen YH, Shin HS, Campbell KP, Chen CC (2009) The CaV3.2 T-type Ca2+ channel is required for pressure overload-induced cardiac hypertrophy in mice. Circ Res 104:522–530PubMedCrossRefGoogle Scholar
  15. Choi S, Na HS, Kim J, Lee J, Lee S, Kim D, Park J, Chen CC, Campbell KP, Shin HS (2007) Attenuated pain responses in mice lacking Ca(V)3.2 T-type channels. Genes Brain Behav 6:425–431PubMedCrossRefGoogle Scholar
  16. Clapham DE (2007) Calcium signaling. Cell 131:1047–1058PubMedCrossRefGoogle Scholar
  17. Cribbs LL (2006) T-type Ca2+ channels in vascular smooth muscle: multiple functions. Cell Calcium 40:221–230PubMedCrossRefGoogle Scholar
  18. Cribbs L (2010) T-type calcium channel expression and function in the diseased heart. Channels 4:447–452PubMedCrossRefGoogle Scholar
  19. Crunelli V, Cope DW, Hughes SW (2006) Thalamic T-type Ca2+ channels and NREM sleep. Cell Calcium 40:175–190PubMedCentralPubMedCrossRefGoogle Scholar
  20. Diaz-Lezama N, Hernández-Elvira M, Sandoval A, Monroy A, Felix R, Monjaraz E (2010) Ghrelin inhibits proliferation and increases T-type Ca2+ channel expression in PC-3 human prostate carcinoma cells. Biochem Biophys Res Commun 403:24–9PubMedCrossRefGoogle Scholar
  21. Doyle DA, Morais Cabral J, Pfuetzner RA, Kuo A, Gulbis JM, Cohen SL, Chait BT, MacKinnon R (1998) The structure of the potassium channel: molecular basis of K + conduction and selectivity. Science 280:69–77PubMedCrossRefGoogle Scholar
  22. Dreyfus FM, Tscherter A, Errington AC, Renger JJ, Shin HS, Uebele VN, Crunelli V, Lambert RC, Leresche N (2010) Selective T-type calcium channel block in thalamic neurons reveals channel redundancy and physiological impact of I(T)window. J Neurosci 30:99–109PubMedCentralPubMedCrossRefGoogle Scholar
  23. Ernst WL, Zhang Y, Yoo JW, Ernst SJ, Noebels JL (2009) Genetic enhancement of thalamocortical network activity by elevating α1g-mediated low-voltage-activated calcium current induces pure absence epilepsy. J Neurosci 29:1615–1625PubMedCentralPubMedCrossRefGoogle Scholar
  24. Escoffier J, Boisseau S, Serres C, Chen CC, Kim D, Stamboulian S, Shin HS, Campbell KP, De Waard M, Arnoult C (2007) Expression, localization and functions in acrosome reaction and sperm motility of Ca(V)3.1 and Ca(V)3.2 channels in sperm cells: an evaluation from Ca(V)3.1 and Ca(V)3.2 deficient mice. J Cell Physiol 212:753–763PubMedCrossRefGoogle Scholar
  25. Ferron L, Capuano V, Deroubaix E, Coulombe A, Renaud JF (2002) Functional and molecular characterization of a T-type Ca2+ channel during fetal and postnatal rat heart development. J Mol Cell Cardiol 34:533–546PubMedCrossRefGoogle Scholar
  26. Gackière F, Warnier M, Katsogiannou M, Derouiche S, Delcourt P, Dewailly E, Slomianny C, Humez S, Prevarskaya N, Roudbaraki M, Mariot P (2013) Functional coupling between large-conductance potassium channels and Cav3.2 voltage-dependent calcium channels participates in prostate cancer cell growth. Biol Open 2:941–951PubMedCentralPubMedCrossRefGoogle Scholar
  27. Harraz OF, Brett SE, Welsh DG (2013) Nitric oxide suppresses vascular voltage-gated T-type Ca2+ channels through cGMP/PKG signaling. Am J Physiol 306:H279–H285Google Scholar
  28. Hurtado R, Bub G, Herzlinger DA (2014) Molecular signature of tissues with pacemaker activity in the heart and upper urinary tract involves coexpressed hyperpolarization-activated cation and T-type Ca2+ channels. FASEB J 28:730–739PubMedCrossRefGoogle Scholar
  29. Iftinca MC (2011) Neuronal T-type calcium channels: what’s new? Iftinca: T-type channel regulation. J Med Life 4:126–138PubMedCentralPubMedGoogle Scholar
  30. Jagodic MM, Pathirathna S, Nelson MT, Mancuso S, Joksovic PM, Rosenberg ER, Bayliss DA, Jevtovic-Todorovic V, Todorovic SM (2007) Cell-specific alterations of T-type calcium current in painful diabetic neuropathy enhance excitability of sensory neurons. J Neurosci 27:3305–3316PubMedCrossRefGoogle Scholar
  31. Jagodic MM, Pathirathna S, Joksovic PM, Lee W, Nelson MT, Naik AK, Su P, Jevtovic-Todorovic V, Todorovic SM (2008) Upregulation of the T-type calcium current in small rat sensory neurons after chronic constrictive injury of the sciatic nerve. J Neurophysiol 99:3151–3156PubMedCentralPubMedCrossRefGoogle Scholar
  32. Jensen LJ, Holstein-Rathlou NH (2009) Is there a role for T-type Ca2+ channels in regulation of vasomotor tone in mesenteric arterioles? Can J Physiol Pharmacol 87:8–20PubMedCrossRefGoogle Scholar
  33. Jones EG (2010) Thalamocortical dysrhythmia and chronic pain. Pain 150:4–5PubMedCrossRefGoogle Scholar
  34. Kang HW, Park JY, Jeong SW, Kim JA, Moon HJ, Perez-Reyes E, Lee JH (2006) A molecular determinant of nickel inhibition in Cav3.2 T-type calcium channels. J Biol Chem 281:4823–4830PubMedCrossRefGoogle Scholar
  35. Kang HW, Moon HJ, Joo SH, Lee JH (2007) Histidine residues in the IS3-IS4 loop are critical for nickel-sensitive inhibition of the Ca(v)3.2 calcium channel. FEBS Lett 581:5774–5780PubMedCrossRefGoogle Scholar
  36. Kraus RL, Li Y, Gregan Y, Gotter AL, Uebele VN, Fox SV, Doran SM, Barrow JC, Yang ZQ, Reger TS, Koblan KS, Renger JJ (2010) In vitro characterization of T-type calcium channel antagonist TTA-A2 and in vivo effects on arousal in mice. J Pharmacol Exp Ther 335:409–417PubMedCrossRefGoogle Scholar
  37. Lee J, Kim D, Shin H-S (2004) Lack of delta waves and sleep disturbances during non-rapid eye movement sleep in mice lacking α1G -subunit of T-type calcium channels. Proc Natl Acad Sci USA 101:18195–18199PubMedCentralPubMedCrossRefGoogle Scholar
  38. Lee SE, Ahn DS, Lee YH (2009) Role of T-type Ca channels in the spontaneous phasic contraction of pregnant rat uterine smooth muscle. Korean J Physiol Pharmacol 13:241–249PubMedCentralPubMedCrossRefGoogle Scholar
  39. Li W, Zhang SL, Wang N, Zhang BB, Li M (2011) Blockade of T-type Ca2+ channels inhibits human ovarian cancer cell proliferation. Cancer Investig 29:339–346CrossRefGoogle Scholar
  40. Liang J, Zhang Y, Wang J, Pan H, Wu H, Xu K, Liu X, Jiang Y, Shen Y, Wu X (2006) New variants in the CACNA1H gene identified in childhood absence epilepsy. Neurosci Lett 406:27–32PubMedCrossRefGoogle Scholar
  41. Liang J, Zhang Y, Chen Y, Wang J, Pan H, Wu H, Xu K, Liu X, Jiang Y, Shen Y, Wu X (2007) Common polymorphisms in the CACNA1H gene associated with childhood absence epilepsy in Chinese Han population. Ann Hum Genet 71:325–335PubMedCrossRefGoogle Scholar
  42. Long SB, Tao X, Campbell EB, MacKinnon R (2007) Atomic structure of a voltage-dependent K+ channel in a lipid membrane-like environment. Nature 450:376–382PubMedCrossRefGoogle Scholar
  43. Lory P, Bidaud I, Chemin J (2006) T-type calcium channels in differentiation and proliferation. Cell Calcium 40:135–146PubMedCrossRefGoogle Scholar
  44. Lu AT, Dai X, Martinez-Agosto JA, Cantor RM (2012) Support for calcium channel gene defects in autism spectrum disorders. Mol Autism 3:18PubMedCentralPubMedCrossRefGoogle Scholar
  45. Manni R, Terzaghi M (2010) Comorbidity between epilepsy and sleep disorders. Epilepsy Res 90:171–177PubMedCrossRefGoogle Scholar
  46. Marger F, Gelot A, Alloui A, Matricon J, Ferrer JF, Barrère C, Pizzoccaro A, Muller E, Nargeot J, Snutch TP, Eschalier A, Bourinet E, Ardid D (2011) T-type calcium channels contribute to colonic hypersensitivity in a rat model of irritable bowel syndrome. Proc Natl Acad Sci USA 108:11268–11273PubMedCentralPubMedCrossRefGoogle Scholar
  47. Matsunami M, Kirishi S, Okui T, Kawabata A (2011) Chelating luminal zinc mimics hydrogen sulfide-evoked colonic pain in mice: possible involvement of T-type calcium channels. Neuroscience 181:257–264PubMedCrossRefGoogle Scholar
  48. McRory JE, Santi CM, Hamming KS, Mezeyova J, Sutton KG, Baillie DL, Stea A, Snutch TP (2001) Molecular and functional characterization of a family of rat brain T-type calcium channels. J Biol Chem 276:3999–4011PubMedCrossRefGoogle Scholar
  49. Nakayama H, Bodi I, Correll RN, Chen X, Lorenz J, Houser SR, Robbins J, Schwartz A, Molkentin JD (2009) Alpha1G-dependent T-type Ca2+ current antagonizes cardiac hypertrophy through a NOS3-dependent mechanism in mice. J Clin Invest 119:3787–3796PubMedCentralPubMedCrossRefGoogle Scholar
  50. Nelson MT, Woo J, Kang HW, Vitko I, Barrett PQ, Perez-Reyes E, Lee JH, Shin HS, Todorovic SM (2007) Reducing agents sensitize C-type nociceptors by relieving high-affinity zinc inhibition of T-type calcium channels. J Neurosci 27:8250–8260PubMedCrossRefGoogle Scholar
  51. Oguri A, Tanaka T, Iida H, Meguro K, Takano H, Oonuma H, Nishimura S, Morita T, Yamasoba T, Nagai R, Nakajima T (2010) Involvement of CaV3.1 T-type calcium channels in cell proliferation in mouse preadipocytes. Am J Physiol 298:C1414–C1423CrossRefGoogle Scholar
  52. Ono K, Iijima T (2010) Cardiac T-type Ca2+ channels in the heart. J Mol Cell Cardiol 48:65–70PubMedCrossRefGoogle Scholar
  53. Parrino L, De Paolis F, Milioli G, Gioi G, Grassi A, Riccardi S, Colizzi E, Terzano MG (2012) Distinctive polysomnographic traits in nocturnal frontal lobe epilepsy. Epilepsia 53:1178–1184PubMedCrossRefGoogle Scholar
  54. Payandeh J, Scheuer T, Zheng N, Catterall WA (2011) The crystal structure of a voltage-gated sodium channel. Nature 475:353–358PubMedCentralPubMedCrossRefGoogle Scholar
  55. Perez-Reyes E (2003) Molecular physiology of low-voltage-activated T-type calcium channels. Physiol Rev 83:117–161PubMedGoogle Scholar
  56. Perez-Reyes E (2010) Characterization of the gating brake in the I-II loop of CaV3 T-type calcium channels. Channels 4:453–458PubMedCentralPubMedCrossRefGoogle Scholar
  57. Roderick HL, Cook SJ (2008) Ca2+ signalling checkpoints in cancer: remodelling Ca2+ for cancer cell proliferation and survival. Nat Rev Cancer 8:361–375PubMedCrossRefGoogle Scholar
  58. Schmunk G, Gargus JJ (2013) Channelopathy pathogenesis in autism spectrum disorders. Front Genet 4:222PubMedCentralPubMedCrossRefGoogle Scholar
  59. Senatore A, Spafford JD (2012) Gene transcription and splicing of T-type channels are evolutionarily-conserved strategies for regulating channel expression and gating. PLoS One 7:e37409PubMedCentralPubMedCrossRefGoogle Scholar
  60. Senatore A, Zhorov BS, Spafford JD (2012) CaV3 T-type calcium channels. WIREs Membr Transp Signall 1:467–491. doi: 10.1002/wmts.41 CrossRefGoogle Scholar
  61. Senatore A, Guan W, Boone AN, Spafford JD (2014) CaV3 T-type calcium channels become sodium channels using alternate extracellular turret residues outside the selectivity filter. J Biol Chem 289(17):11952–11969PubMedCrossRefGoogle Scholar
  62. Shcheglovitov A, Kostyuk P, Shuba Y (2007) Selectivity signatures of three isoforms of recombinant T-type Ca2+ channels. Biochim Biophys Acta 1768:1406–1419PubMedCrossRefGoogle Scholar
  63. Shen L, Ahuja N, Shen Y, Habib NA, Toyota M, Rashid A, Issa JP (2002) DNA methylation and environmental exposures in human hepatocellular carcinoma. J Natl Cancer Inst 94:755–761PubMedCrossRefGoogle Scholar
  64. Shtonda B, Avery L (2005) CCA-1, EGL-19 and EXP-2 currents shape action potentials in the Caenorhabditis elegans pharynx. J Exp Biol 208:2177–2190PubMedCentralPubMedCrossRefGoogle Scholar
  65. Singh B, Monteil A, Bidaud I, Sugimoto Y, Suzuki T, Hamano S, Oguni H, Osawa M, Alonso ME, Delgado-Escueta AV, Inoue Y, Yasui-Furukori N, Kaneko S, Lory P, Yamakawa K (2007) Mutational analysis of CACNA1G in idiopathic generalized epilepsy. Hum Mutat 28:524–525PubMedCrossRefGoogle Scholar
  66. Splawski I, Yoo DS, Stotz SC, Cherry A, Clapham DE, Keating MT (2006) CACNA1H mutations in autism spectrum disorders. J Biol Chem 281:22085–91PubMedCrossRefGoogle Scholar
  67. Strom SP, Stone JL, Ten Bosch JR, Merriman B, Cantor RM, Geschwind DH, Nelson SF (2010) High-density SNP association study of the 17q21 chromosomal region linked to autism identifies CACNA1G as a novel candidate gene. Mol Psychiatry 15:996–1005PubMedCentralPubMedCrossRefGoogle Scholar
  68. Sui G, Fry CH, Malone-Lee J, Wu C (2009) Aberrant Ca2+ oscillations in smooth muscle cells from overactive human bladders. Cell Calcium 45:456–464PubMedCrossRefGoogle Scholar
  69. Talavera K, Nilius B (2006) Biophysics and structure-function relationship of T-type Ca2+ channels. Cell Calcium 40:97–114PubMedCrossRefGoogle Scholar
  70. Talley EM, Cribbs LL, Lee JH, Daud A, Perez-Reyes E, Bayliss DA (1999) Differential distribution of three members of a gene family encoding low voltage-activated (T-type) calcium channels. J Neurosci 19:1895–1911PubMedGoogle Scholar
  71. Talley EM, Solorzano G, Depaulis A, Perez-Reyes E, Bayliss DA (2000) Low-voltage-activated calcium channel subunit expression in a genetic model of absence epilepsy in the rat. Mol Brain Res 75:159–165PubMedCrossRefGoogle Scholar
  72. Taylor JT, Huang L, Pottle JE, Liu K, Yang Y, Zeng X, Keyser BM, Agrawal KC, Hansen JB, Li M (2008a) Selective blockage of T-type Ca2+ channels suppresses human breast cancer cell proliferation. Cancer Lett 267:116–124PubMedCrossRefGoogle Scholar
  73. Taylor JT, Zeng XB, Pottle JE, Lee K, Wang AR, Yi SG, Scruggs JAS, Sikka SS, Li M (2008b) Calcium signaling and T-type calcium channels in cancer cell cycling. World J Gastroenterol 14:4984–4991PubMedCentralPubMedCrossRefGoogle Scholar
  74. Toyota M, Ho C, Ohe-Toyota M, Baylin SB, Issa JP (1999) Inactivation of CACNA1G, a T-type calcium channel gene, by aberrant methylation of its 5' CpG island in human tumors. Cancer Res 59:4535–4541PubMedGoogle Scholar
  75. Tringham E, Powell KL, Cain SM, Kuplast K, Mezeyova J, Weerapura M, Eduljee C, Jiang X, Smith P, Morrison JL, Jones NC, Braine E, Rind G, Fee-Maki M, Parker D, Pajouhesh H, Parmar M, O’Brien TJ, Snutch TP (2012) T-type calcium channel blockers that attenuate thalamic burst firing and suppress absence seizures. Sci Transl Med 4:121ra119CrossRefGoogle Scholar
  76. Uebele VN, Gotter AL, Nuss CE, Kraus RL, Doran SM, Garson SL, Reiss DR, Li Y, Barrow JC, Reger TS, Yang ZQ, Ballard JE, Tang C, Metzger JM, Wang SP, Koblan KS, Renger JJ (2009) Antagonism of T-type calcium channels inhibits high-fat diet-induced weight gain in mice. J Clin Invest 119:1659–1667PubMedCentralPubMedCrossRefGoogle Scholar
  77. Ueki T, Toyota M, Sohn T, Yeo CJ, Issa JP, Hruban RH, Goggins M (2000) Hypermethylation of multiple genes in pancreatic adenocarcinoma. Cancer Res 60:1835–1839PubMedGoogle Scholar
  78. Vassort G, Talavera K, Alvarez JL (2006) Role of T-type Ca2+ channels in the heart. Cell Calcium 40:205–220PubMedCrossRefGoogle Scholar
  79. Viscidi EW, Triche EW, Pescosolido MF, McLean RL, Joseph RM, Spence SJ, Morrow EM (2013) Clinical characteristics of children with autism spectrum disorder and co-occurring epilepsy. PLoS One 8:e67797PubMedCentralPubMedCrossRefGoogle Scholar
  80. Vitko I, Chen Y, Arias JM, Shen Y, Wu XR, Perez-Reyes E (2005) Functional characterization and neuronal modeling of the effects of childhood absence epilepsy variants of CACNA1H, a T-type calcium channel. J Neurosci 25:4844–4855PubMedCrossRefGoogle Scholar
  81. Vitko I, Bidaud I, Arias JM, Mezghrani A, Lory P, Perez-Reyes E (2007) The I-II loop controls plasma membrane expression and gating of Ca(v)3.2 T-type Ca2+ channels: a paradigm for childhood absence epilepsy mutations. J Neurosci 27:322–330PubMedCrossRefGoogle Scholar
  82. Weiss N, Zamponi GW (2013) Control of low-threshold exocytosis by T-type calcium channels. Biochim Biophys Acta 1828:1579–1586PubMedCrossRefGoogle Scholar
  83. Weiss N, Hameed S, Fernández-Fernández JM, Fablet K, Karmazinova M, Poillot C, Proft J, Chen L, Bidaud I, Monteil A, Huc-Brandt S, Lacinova L, Lory P, Zamponi GW, De Waard M (2012) A Cav3.2/syntaxin-1A signaling complex controls T-type channel activity and low-threshold exocytosis. J Biol Chem 287:2810–2818PubMedCentralPubMedCrossRefGoogle Scholar
  84. Weiss N, Black SA, Bladen C, Chen L, Zamponi GW (2013) Surface expression and function of Cav3.2 T-type calcium channels are controlled by asparagine-linked glycosylation. Pflugers Arch 465:1159–1170PubMedCrossRefGoogle Scholar
  85. Wen XJ, Xu SY, Chen ZX, Yang CX, Liang H, Li H (2010) The roles of T-type calcium channel in the development of neuropathic pain following chronic compression of rat dorsal root ganglia. Pharmacology 85:295–300PubMedCrossRefGoogle Scholar
  86. Wolfart J, Roeper J (2002) Selective coupling of T-type calcium channels to SK potassium channels prevents intrinsic bursting in dopaminergic midbrain neurons. J Neurosci 22:3404–3413PubMedGoogle Scholar
  87. Yang J, Ellinor PT, Sather WA, Zhang JF, Tsien RW (1993) Molecular determinants of Ca2+ selectivity and ion permeation in L-type Ca2+ channels. Nature 366:158–161PubMedCrossRefGoogle Scholar
  88. Yeoman MS, Brezden BL, Benjamin PR (1999) LVA and HVA Ca 2+ currents in ventricular muscle cells of the lymnaea heart. J Neurophysiol 82:2428–2440PubMedGoogle Scholar
  89. Young RC, Smith LH, McLaren MD (1993) T-type and L-type calcium currents in freshly dispersed human uterine smooth muscle cells. Am J Obstetr Gynecol 169:785–792CrossRefGoogle Scholar
  90. Zamponi GW, Lewis RJ, Todorovic SM, Arneric SP, Snutch TP (2009) Role of voltage-gated calcium channels in ascending pain pathways. Brain Res Rev 60:84–89PubMedCentralPubMedCrossRefGoogle Scholar
  91. Zhang Y, Mori M, Burgess DL, Noebels JL (2002) Mutations in high-voltage-activated calcium channel genes stimulate low-voltage-activated currents in mouse thalamic relay neurons. J Neurosci 22:6362–6371PubMedGoogle Scholar

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© Springer-Verlag Wien 2015

Authors and Affiliations

  1. 1.Neuroscience InstituteGeorgia State UniversityAtlantaUSA
  2. 2.Department of BiologyUniversity of WaterlooWaterlooCanada

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