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Regulation of the CaV3.2 calcium channels in health and disease Regulácia CaV3.2 vápnikových kanálov v zdraví a chorobe Cover

Regulation of the CaV3.2 calcium channels in health and disease Regulácia CaV3.2 vápnikových kanálov v zdraví a chorobe

By: Ľ. Lacinová  
Open Access
|Nov 2017

References

  1. [1] Agler HL, Evans J, Tay LH, Anderson MJ, Colecraft HM, Yue DT. G protein-gated inhibitory module of N-type (Cav2.2) Ca2+ channels. Neuron. 2005; 46:891-904.10.1016/j.neuron.2005.05.01115953418
  2. [2] Aguado C, Garcia-Madrona S, Gil-Minguez M, Lujan R. Ontogenic Changes and Differential Localization of T-type Ca(2+) Channel Subunits Cav3.1 and Cav3.2 in Mouse Hippocampus and Cerebellum. Front Neuroanat. 2016; 10:83.
  3. [3] Ayoola C, Hwang SM, Hong SJ, Rose KE, Boyd C, Bozic N, Park JY, Osuru HP, DiGruccio MR, Covey DF, Jevtovic-Todorovic V, Todorovic SM. Inhibition of CaV3.2 T-type calcium channels in peripheral sensory neurons contributes to analgesic properties of epipregnanolone. Psychopharmacology (Berl). 2014; 231:3503-15.10.1007/s00213-014-3588-0413504424800894
  4. [4] 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; 29:13106-14.10.1523/JNEUROSCI.2919-09.2009666521119846698
  5. [5] Berthier C, Monteil A, Lory P, Strube C. Alpha(1H) mRNA in single skeletal muscle fibres accounts for T-type calcium current transient expression during fetal development in mice. J Physiol. 2002; 539:681-91.10.1113/jphysiol.2001.013246229018111897840
  6. [6] 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 U S A. 2015; 112:13705-10.10.1073/pnas.1511740112464075926483470
  7. [7] Bourinet E, Alloui A, Monteil A, Barrere C, Couette B, Poirot O, Pages A, McRory J, Snutch TP, 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; 24:315-24.10.1038/sj.emboj.760051554580715616581
  8. [8] Boycott HE, Dallas ML, Elies J, Pettinger L, Boyle JP, Scragg JL, Gamper N, Peers C. Carbon monoxide inhibition of Cav3.2 T-type Ca2+ channels reveals tonic modulation by thioredoxin. FASEB J. 2013; 27:3395-407.10.1096/fj.13-22724923671274
  9. [9] Braun M, Ramracheya R, Bengtsson M, Zhang Q, Karanauskaite J, Partridge C, Johnson PR, Rorsman P. Voltage-gated ion channels in human pancreatic beta-cells: electrophysiological characterization and role in insulin secretion. Diabetes. 2008; 57:1618-28.10.2337/db07-099118390794
  10. [10] Cohen DM. Regulation of TRP channels by N-linked glycosylation. Semin Cell Dev Biol. 2006; 17:630-7. 10.1016/j.semcdb.2006.11.00717215147
  11. [11] Cribbs LL, Lee JH, Yang J, Satin J, Zhang Y, Daud A, Barclay J, Williamson MP, Fox M, Rees M, Perez-Reyes E. Cloning and characterization of a1H from human heart, a member of the T-type Ca2+ channel gene family. Circ Res. 1998; 83:103-9.10.1161/01.RES.83.1.1039670923
  12. [12] Darszon A, Lopez-Martinez P, Acevedo JJ, Hernandez-Cruz A, Trevino CL. T-type Ca2+ channels in sperm function. Cell Calcium. 2006; 40:241-52.10.1016/j.ceca.2006.04.02816797697
  13. [13] Eckle VS, Shcheglovitov A, Vitko I, Dey D, Yap CC, Winckler B, Perez-Reyes E. Mechanisms by which a CACNA1H mutation in epilepsy patients increases seizure susceptibility. J Physiol. 2014; 592:795-809.10.1113/jphysiol.2013.264176393471524277868
  14. [14] Elies J, Scragg JL, Boyle JP, Gamper N, Peers C. Regulation of the T-type Ca(2+) channel Cav3.2 by hydrogen sulfide: emerging controversies concerning the role of H2 S in nociception. J Physiol. 2016; 594:4119-29.10.1113/JP270963496774126804000
  15. [15] Elies J, Scragg JL, Dallas ML, Huang D, Huang S, Boyle JP, Gamper N, Peers C. Inhibition of T-type Ca2+ Channels by Hydrogen Sulfide. Adv Exp Med Biol. 2015; 860:353-60.10.1007/978-3-319-18440-1_4026303500
  16. [16] Elies J, Scragg JL, Huang S, Dallas ML, Huang D, MacDougall D, Boyle JP, Gamper N, Peers C. Hydrogen sulfide inhibits Cav3.2 T-type Ca2+ channels. FASEB J. 2014; 28:5376-87. 10.1096/fj.14-25711325183670
  17. [17] Ernst WL, Zhang Y, Yoo JW, Ernst SJ, Noebels JL. Genetic enhancement of thalamocortical network activity by elevating alpha 1g-mediated low-voltage-activated calcium current induces pure absence epilepsy. J Neurosci. 2009; 29:1615-25.10.1523/JNEUROSCI.2081-08.2009266067319211869
  18. [18] Ferdous Z, Qureshi MA, Jayaprakash P, Parekh K, John A, Oz M, Raza H, Dobrzynski H, Adrian TE, Howarth FC. Different Profile of mRNA Expression in Sinoatrial Node from Streptozotocin- Induced Diabetic Rat. PLoS One. 2016; 11:e0153934.10.1371/journal.pone.0153934483825827096430
  19. [19] Gadotti VM, Caballero AG, Berger ND, Gladding CM, Chen L, Pfeifer TA, Zamponi GW. Small organic molecule disruptors of Cav3.2 - USP5 interactions reverse inflammatory and neuropathic pain. Mol Pain. 2015; 11:12.10.1186/s12990-015-0011-8436409925889575
  20. [20] Garcia-Caballero A, Gadotti VM, Chen L, Zamponi GW. A cellpermeant peptide corresponding to the cUBP domain of USP5 reverses inflammatory and neuropathic pain. Mol Pain. 2016; 12.10.1177/1744806916642444495596627130589
  21. [21] Garcia-Caballero A, Gadotti VM, Stemkowski P, Weiss N, Souza IA, Hodgkinson V, Bladen C, Chen L, Hamid J, Pizzoccaro A, Deage M, Francois A, Bourinet E, Zamponi GW. The deubiquitinating enzyme USP5 modulates neuropathic and inflammatory pain by enhancing Cav3.2 channel activity. Neuron. 2014; 83:1144-58.
  22. [22] Gilmore AJ, Heblinski M, Reynolds A, Kassiou M, Connor M. Inhibition of human recombinant T-type calcium channels by N-arachidonoyl 5-HT. Br J Pharmacol. 2012; 167:1076-88.10.1111/j.1476-5381.2012.02047.x349298822624680
  23. [23] Hayashi K, Wakino S, Sugano N, Ozawa Y, Homma K, Saruta T.Ca2+ channel subtypes and pharmacology in the kidney. Circ Res. 2007; 100:342-53.10.1161/01.RES.0000256155.31133.49
  24. [24] Heron SE, Khosravani H, Varela D, Bladen C, Williams TC, Newman MR, Scheffer IE, Berkovic SF, Mulley JC, Zamponi GW. Extended spectrum of idiopathic generalized epilepsies associated with CACNA1H functional variants. Ann Neurol. 2007; 62:560-8.10.1002/ana.21169
  25. [25] Heron SE, Phillips HA, Mulley JC, Mazarib A, Neufeld MY, Berkovic SF, Scheffer IE. Genetic variation of CACNA1H in idiopathic generalized epilepsy. Ann Neurol. 2004; 55:595-6.10.1002/ana.20028
  26. [26] Hu C, Depuy SD, Yao J, McIntire WE, Barrett PQ. Protein kinase A activity controls the regulation of T-type CaV3.2 channels by Gbetagamma dimers. J Biol Chem. 2009; 284:7465-73.10.1074/jbc.M808049200
  27. [27] Huang D, Huang S, Gao H, Liu Y, Qi J, Chen P, Wang C, Scragg JL, Vakurov A, Peers C, Du X, Zhang H, Gamper N. Redox-Dependent Modulation of T-Type Ca(2+) Channels in Sensory Neurons Contributes to Acute Anti-Nociceptive Effect of Substance P. Antioxid Redox Signal. 2016; 25:233-51.10.1089/ars.2015.6560
  28. [28] Huguenard JR. Low-voltage-activated (T-type) calcium-channel genes identified. Trends Neurosci. 1998; 21:451-2.10.1016/S0166-2236(98)01331-9
  29. [29] Husse B, Franz WM. Generation of cardiac pacemaker cells by programming and differentiation. Biochim Biophys Acta. 2016; 1863:1948-52.10.1016/j.bbamcr.2015.12.00426681531
  30. [30] Chemin J, Mezghrani A, Bidaud I, Dupasquier S, Marger F, Barrere C, Nargeot J, Lory P. Temperature-dependent modulation of CaV3 T-type calcium channels by protein kinases C and A in mammalian cells. J Biol Chem. 2007; 282:32710-8.10.1074/jbc.M70274620017855364
  31. [31] Chemin J, Monteil A, Perez-Reyes E, Bourinet E, Nargeot J, Lory P. Specific contribution of human T-type calcium channel isotypes (alpha(1G), alpha(1H) and alpha(1I)) to neuronal excitability. J Physiol. 2002; 540:3-14.10.1113/jphysiol.2001.013269229020911927664
  32. [32] 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; 20:7033-40.10.1093/emboj/20.24.703312577911742980
  33. [33] Chen Y, Lu J, Pan H, Zhang Y, Wu H, Xu K, Liu X, Jiang Y, Bao X, Yao Z, Ding K, Lo WH, Qiang B, Chan P, Shen Y, Wu X. Association between genetic variation of CACNA1H and childhood absence epilepsy. Ann Neurol. 2003; 54:239-43.10.1002/ana.10607
  34. [34] Kang HW, Park JY, Jeong SW, Kim JA, Moon HJ, Perez-Reyes E, Lee JH. A molecular determinant of nickel inhibition in Cav3.2 T-type calcium channels. J Biol Chem. 2006; 281:4823-30.10.1074/jbc.M510197200
  35. [35] Kawabata A, Ishiki T, Nagasawa K, Yoshida S, Maeda Y, Takahashi T, Sekiguchi F, Wada T, Ichida S, Nishikawa H. Hydrogen sulfide as a novel nociceptive messenger. Pain. 2007; 132:74-81.10.1016/j.pain.2007.01.026
  36. [36] Kim D, Song I, Keum S, Lee T, Jeong MJ, Kim SS, McEnery MW, Shin HS. Lack of the burst firing of thalamocortical relay neurons and resistance to absence seizures in mice lacking a1G T-type Ca2+ channels. Neuron. 2001; 31:35-45.10.1016/S0896-6273(01)00343-9
  37. [37] Lacinova L. Pharmacology of recombinant low-voltage activated calcium channels. Curr Drug Targets CNS Neurol Disord. 2004; 3:105-11.10.2174/156800704348254315078185
  38. [38] Lacinova L. Voltage-dependent calcium channels. Gen Physiol Biophys. 2005; 24 Suppl 1:1-78.
  39. [39] Lacinova L, Klugbauer N, Hofmann F. Low voltage activated calcium channels: from genes to function. Gen Physiol Biophys. 2000; 19:121-36.
  40. [40] Lalevee N, Rebsamen MC, Barrere-Lemaire S, Perrier E, Nargeot J, Benitah JP, Rossier MF. Aldosterone increases T-type calcium channel expression and in vitro beating frequency in neonatal rat cardiomyocytes. Cardiovasc Res. 2005; 67:216-24.10.1016/j.cardiores.2005.05.00915919070
  41. [41] Lazniewska J, Rzhepetskyy Y, Zhang FX, Zamponi GW, Weiss N. Cooperative roles of glucose and asparagine-linked glycosylation in T-type calcium channel expression. Pflugers Arch. 2016.10.1007/s00424-016-1881-y27659162
  42. [42] Li L, Rose P, Moore PK. Hydrogen sulfide and cell signaling. Annu Rev Pharmacol Toxicol. 2011; 51:169-87.10.1146/annurev-pharmtox-010510-10050521210746
  43. [43] M’Dahoma S, Gadotti VM, Zhang FX, Park B, Nam JH, Onnis V, Balboni G, Lee JY, Zamponi GW. Effect of the T-type channel blocker KYS-05090S in mouse models of acute and neuropathic pain. Pflugers Arch. 2016; 468:193-9.10.1007/s00424-015-1733-126354962
  44. [44] Maturana A, Lenglet S, Python M, Kuroda S, Rossier MF. Role of the T-type calcium channel CaV3.2 in the chronotropic action of corticosteroids in isolated rat ventricular myocytes. Endocrinology. 2009; 150:3726-34.10.1210/en.2008-172719443576
  45. [45] 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 a1I subunit. J Biol Chem. 2000; 275:16530-5.10.1074/jbc.C00009020010749850
  46. [46] Moremen KW, Tiemeyer M, Nairn AV. Vertebrate protein glycosylation: diversity, synthesis and function. Nat Rev Mol Cell Biol. 2012; 13:448-62.10.1038/nrm3383393401122722607
  47. [47] Nelson MT, Woo J, Kang HW, Vitko I, Barrett PQ, Perez-Reyes E, Lee JH, Shin HS, Todorovic SM. Reducing agents sensitize C-type nociceptors by relieving high-affinity zinc inhibition of T-type calcium channels. Journal of Neuroscience. 2007; 27:8250-8260.10.1523/JNEUROSCI.1800-07.2007667306817670971
  48. [48] Ohkubo T, Inoue Y, Kawarabayashi T, Kitamura K. Identification and electrophysiological characteristics of isoforms of T-type calcium channel Ca(v)3.2 expressed in pregnant human uterus. Cell Physiol Biochem. 2005; 16:245-54.10.1159/00008985016301824
  49. [49] Ondacova K, Karmazinova M, Lazniewska J, Weiss N, Lacinova L. Modulation of Cav3.2 T-type calcium channel permeability by asparagine-linked glycosylation. Channels (Austin). 2016; 10:175-84.10.1080/19336950.2016.1138189495458426745591
  50. [50] Orestes P, Osuru HP, McIntire WE, Jacus MO, Salajegheh R, Jagodic MM, Choe W, Lee J, Lee SS, Rose KE, Poiro N, Digruccio MR, Krishnan K, Covey DF, Lee JH, Barrett PQ, Jevtovic-Todorovic V, Todorovic SM. Reversal of neuropathic pain in diabetes by targeting glycosylation of Ca(V)3.2 T-type calcium channels. Diabetes. 2013; 62:3828-38.10.2337/db13-0813380661223835327
  51. [51] Perez-Reyes E. Molecular physiology of low-voltage-activated T-type calcium channels. Physiol Rev. 2003; 83:117-61.10.1152/physrev.00018.200212506128
  52. [52] Ross HR, Gilmore AJ, Connor M. Inhibition of human recombinant T-type calcium channels by the endocannabinoid N-arachidonoyl dopamine. Br J Pharmacol. 2009; 156:740-50.10.1111/j.1476-5381.2008.00072.x269774719226289
  53. [53] Rzhepetskyy Y, Lazniewska J, Blesneac I, Pamphlett R, Weiss N. CACNA1H missense mutations associated with amyotrophic lateral sclerosis alter Cav3.2 T-type calcium channel activity and reticular thalamic neuron firing. Channels (Austin). 2016; 10:466-77.10.1080/19336950.2016.1204497503477627331657
  54. [54] Scholl UI, Stolting G, Nelson-Williams C, Vichot AA, Choi M, Loring E, Prasad ML, Goh G, Carling T, Juhlin CC, Quack I, Rump LC, Thiel A, Lande M, Frazier BG, Rasoulpour M, Bowlin DL, Sethna CB, Trachtman H, Fahlke C, Lifton RP. Recurrent gain of function mutation in calcium channel CACNA1H causes early-onset hypertension with primary aldosteronism. Elife. 2015; 4:e06315.10.7554/eLife.06315440844725907736
  55. [55] Splawski I, Timothy KW, Decher N, Kumar P, Sachse FB, Beggs AH, Sanguinetti MC, Keating MT. Severe arrhythmia disorder caused by cardiac L-type calcium channel mutations. Proc Natl Acad Sci U S A. 2005; 102:8089-96; discussion 8086-8.10.1073/pnas.0502506102114942815863612
  56. [56] Splawski I, Timothy KW, Sharpe LM, Decher N, Kumar P, Bloise R, Napolitano C, Schwartz PJ, Joseph RM, Condouris K, Tager- Flusberg H, Priori SG, Sanguinetti MC, Keating MT. Ca(V)1.2 calcium channel dysfunction causes a multisystem disorder including arrhythmia and autism. Cell. 2004; 119:19-31.10.1016/j.cell.2004.09.01115454078
  57. [57] Splawski I, Yoo DS, Stotz SC, Cherry A, Clapham DE, Keating MT. CACNA1H mutations in autism spectrum disorders. J Biol Chem. 2006; 281:22085-91.10.1074/jbc.M60331620016754686
  58. [58] Steinberg KM, Yu B, Koboldt DC, Mardis ER, Pamphlett R. Exome sequencing of case-unaffected-parents trios reveals recessive and de novo genetic variants in sporadic ALS. Sci Rep. 2015; 5:9124.10.1038/srep09124436064125773295
  59. [59] Todorovic SM, Jevtovic-Todorovic V. Neuropathic pain: role for presynaptic T-type channels in nociceptive signaling. Pflugers Arch. 2013; 465:921-7.10.1007/s00424-012-1211-y23322114
  60. [60] Ufret-Vincenty CA, Baro DJ, Lederer WJ, Rockman HA, Quinones LE, Santana LF. Role of sodium channel deglycosylation in the genesis of cardiac arrhythmias in heart failure. J Biol Chem. 2001; 276:28197-203. 10.1074/jbc.M10254820011369778
  61. [61] Wang G, Bochorishvili G, Chen Y, Salvati KA, Zhang P, Dubel SJ, Perez-Reyes E, Snutch TP, Stornetta RL, Deisseroth K, Erisir A, Todorovic SM, Luo JH, Kapur J, Beenhakker MP, Zhu JJ. CaV3.2 calcium channels control NMDA receptor-mediated transmission: a new mechanism for absence epilepsy. Genes Dev. 2015; 29:1535-51.10.1101/gad.260869.115452673726220996
  62. [62] Watanabe I, Wang HG, Sutachan JJ, Zhu J, Recio-Pinto E, Thornhill WB. Glycosylation affects rat Kv1.1 potassium channel gating by a combined surface potential and cooperative subunit interaction mechanism. J Physiol. 2003; 550:51-66.10.1113/jphysiol.2003.040337234301312879861
  63. [63] Weiss N, Black SA, Bladen C, Chen L, Zamponi GW. Surface expression and function of Cav3.2 T-type calcium channels are controlled by asparagine-linked glycosylation. Pflugers Arch. 2013; 465:1159-70.10.1007/s00424-013-1259-323503728
  64. [64] Welsby PJ, Wang H, Wolfe JT, Colbran RJ, Johnson ML, Barrett PQ. A mechanism for the direct regulation of T-type calcium channels by Ca2+/calmodulin-dependent kinase II. J Neurosci. 2003; 23:10116-21.10.1523/JNEUROSCI.23-31-10116.2003
  65. [65] Yao J, Davies LA, Howard JD, Adney SK, Welsby PJ, Howell N, Carey RM, Colbran RJ, Barrett PQ. Molecular basis for the modulation of native T-type Ca2+ channels in vivo by Ca2+/calmodulindependent protein kinase II. J Clin Invest. 2006; 116:2403-12.
  66. [66] Zamponi GW, Striessnig J, Koschak A, Dolphin AC. The Physiology, Pathology, and Pharmacology of Voltage-Gated Calcium Channels and Their Future Therapeutic Potential. Pharmacol Rev. 2015; 67:821-70.10.1124/pr.114.009654463056426362469
  67. [67] Zhang Y, Cribbs LL, Satin J. Arachidonic acid modulation of alpha1H, a cloned human T-type calcium channel. Am J Physiol Heart Circ Physiol. 2000; 278:H184-93.10.1152/ajpheart.2000.278.1.H18410644598
  68. [68] Zoghbi HY. Postnatal neurodevelopmental disorders: meeting at the synapse? Science. 2003; 302:826-30.10.1126/science.108907114593168
Language: English
Page range: 15 - 21
Submitted on: Oct 24, 2016
Accepted on: Mar 16, 2017
Published on: Nov 30, 2017
Published by: Comenius University in Bratislava, Faculty of Pharmacy
In partnership with: Paradigm Publishing Services
Publication frequency: 2 issues per year
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© 2017 Ľ. Lacinová, published by Comenius University in Bratislava, Faculty of Pharmacy
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