Modulation of Cav3.2 T-type calcium channel permeability by asparagine-linked glycosylation

Channels

Volumn 10, Issue 3, 2016, Pages 175-184

  Ondacova, Katarina ^a   Karmazinova, Maria ^a   Lazniewska, Joanna ^b   Weiss, Norbert ^b   Lacinova, Lubica ^a  

^a INSTITUTE OF MOLECULAR PHYSIOLOGY AND GENETICS   (Slovakia)

^b INSTITUTE OF ORGANIC CHEMISTRY AND BIOCHEMISTRY   (Czech Republic)

Author keywords

Cav3.2; calcium channel; gating; glycosylation; T type channel

Indexed keywords

ASPARAGINE; CALCIUM CHANNEL T TYPE; COMPLEMENTARY DNA; VOLTAGE GATED CHLORIDE CHANNEL; CACNA1H PROTEIN, HUMAN;

ARTICLE; CALCIUM CONDUCTANCE; DEPOLARIZATION; DIABETIC NEUROPATHY; EPILEPSY; GLYCOSYLATION; HUMAN; HUMAN CELL; MATHEMATICAL ANALYSIS; MEMBRANE PERMEABILITY; MODULATION; NEUROPATHIC PAIN; OXIDATIVE PHOSPHORYLATION; PROTEIN EXPRESSION; UBIQUITINATION; CHANNEL GATING; CHEMISTRY; ELECTROPHYSIOLOGY; HEK293 CELL LINE; METABOLISM; PERMEABILITY;

ASPARAGINE; CALCIUM CHANNELS, T-TYPE; ELECTROPHYSIOLOGICAL PHENOMENA; GLYCOSYLATION; HEK293 CELLS; HUMANS; ION CHANNEL GATING; PERMEABILITY;

EID: 84978393937     PISSN: 19336950     EISSN: 19336969     Source Type: Journal    
DOI: 10.1080/19336950.2016.1138189     Document Type: Article

References (47)

1. W.A.Catterall, E.Perez-Reyes, T.P.Snutch, J.Striessnig. International Union of Pharmacology. XLVIII. Nomenclature and structure-function relationships of voltage-gated calcium channels. Pharmacol Rev 2005; 57:411-25; PMID:16382099; http://dx.doi.org/10.1124/pr.57.4.5
2. E.Perez-Reyes Molecular physiology of low-voltage-activated T-type calcium channels. Physiol Rev 2003; 83:117-61; PMID:12506128; http://dx.doi.org/10.1152/physrev.00018.2002
3. 2+ channels and NREM sleep. Cell Calcium 2006; 40:175-90; PMID:16777223; http://dx.doi.org/10.1016/j.ceca.2006.04.022
4. T.Bal, D.A.McCormick. Synchronized oscillations in the inferior olive are controlled by the hyperpolarization-activated cation current I(h). J Neurophysiol 1997; 77:3145-56; PMID:9212264
5. C.Beurrier, P.Congar, B.Bioulac, C.Hammond. Subthalamic nucleus neurons switch from single-spike activity to burst-firing mode. J Neurosci 1999; 19:599-609; PMID:9880580
6. F.Sotty, M.Danik, F.Manseau, F.Laplante, R.Quirion, S.Williams. Distinct electrophysiological properties of glutamatergic, cholinergic and GABAergic rat septohippocampal neurons: novel implications for hippocampal rhythmicity. J Physiol 2003; 551:927-43; PMID:12865506; http://dx.doi.org/10.1113/jphysiol.2003.046847
7. N.Weiss, S.Hameed, J.M.Fernández-Fernández, K.Fablet, M.Karmazinova, C.Poillot, J.Proft, L.Chen, I.Bidaud, A.Monteil, et al. A Ca(v)3.2/syntaxin-1A signaling complex controls T-type channel activity and low-threshold exocytosis. J Biol Chem 2012; 287:2810-8; PMID:22130660; http://dx.doi.org/10.1074/jbc.M111.290882
8. N.Weiss, G.W.Zamponi. Control of low-threshold exocytosis by T-type calcium channels. Biochim Biophys Acta 2013; 1828:1579-86; PMID:22885170; http://dx.doi.org/10.1016/j.bbamem.2012.07.031
9. 2+ channels. Biochim Biophys Acta 2013; 1828:1550-9; PMID:22975282; http://dx.doi.org/10.1016/j.bbamem.2012.08.032
10. 2+ channels. Channels (Austin) 2015; 9:68-9; PMID:25715174; http://dx.doi.org/10.1080/19336950.2015.1017995
11. G.W.Zamponi, J.Striessnig, A.Koschak, A.C.Dolphin. The physiology, pathology, and pharmacology of voltage-gated calcium channels and their future therapeutic potential. Pharmacol Rev 2015; 67:821-70; PMID:26362469; http://dx.doi.org/10.1124/pr.114.009654
12. S.M'Dahoma, V.M.Gadotti, F.X.Zhang, B.Park, J.H.Nam, V.Onnis, G.Balboni, J.Y.Lee, G.W.Zamponi. Effect of the T-type channel blocker KYS-05090S in mouse models of acute and neuropathic pain. Pflugers Arch 2016; 468:193-9; http://dx.doi.org/10.1007/s00424-015-1733-1.
13. H.Yu, J.B.Seo, S.R.Jung, D.S.Koh, B.Hille. Noradrenaline upregulates T-type calcium channels in rat pinealocytes. J Physiol 2015; 593:887-904; PMID:25504572; http://dx.doi.org/10.1113/jphysiol.2014.284208
14. H.Sellak, C.Zhou, B.Liu, H.Chen, T.M.Lincoln, S.Wu. Transcriptional regulation of α1H T-type calcium channel under hypoxia. Am J Physiol Cell Physiol 2014; 307:C648-56; PMID:25099734; http://dx.doi.org/10.1152/ajpcell.00210.2014
15. V3.2: bi-directionality by early growth response 1 (Egr1) and repressor element 1 (RE-1) protein-silencing transcription factor (REST). J Biol Chem 2012; 287:15489-501; PMID:22431737; http://dx.doi.org/10.1074/jbc.M111.310763
16. J.Murbartián, J.M.Arias, E.Perez-Reyes. Functional impact of alternative splicing of human T-type Cav3.3 calcium channels. J Neurophysiol 2004; 92:3399-407; PMID:15254077; http://dx.doi.org/10.1152/jn.00498.2004
17. I.Latour, D.F.Louw, A.M.Beedle, J.Hamid, G.R.Sutherland, G.W.Zamponi. Expression of T-type calcium channel splice variants in human glioma. Glia 2004; 48:112-9; PMID:15378657; http://dx.doi.org/10.1002/glia.20063
18. K.L.Powell, S.M.Cain, C.Ng, S.Sirdesai, L.S.David, M.Kyi, E.Garcia, J.R.Tyson, C.A.Reid, M.Bahlo, et al. A Cav3.2 T-type calcium channel point mutation has splice-variant-specific effects on function and segregates with seizure expression in a polygenic rat model of absence epilepsy. J Neurosci 2009; 29:371-80; PMID:19144837; http://dx.doi.org/10.1523/JNEUROSCI.5295-08.2009
19. V3.2 T-type calcium channel mediate voltage-dependent facilitation and associate with cardiac hypertrophy and development. Channels (Austin) 2010; 4:375-89; PMID:20699644; http://dx.doi.org/10.4161/chan.4.5.12874
20. J.T.Wolfe, H.Wang, J.Howard, J.C.Garrison, P.Q.Barrett. T-type calcium channel regulation by specific G-protein betagamma subunits. Nature 2003; 424:209-13; PMID:12853961; http://dx.doi.org/10.1038/nature01772
21. K.A.Aromolaran, K.A.Benzow, L.L.Cribbs, M.D.Koob, E.S.Piedras-Rentería. T-type current modulation by the actin-binding protein Kelch-like 1. Am J Physiol Cell Physiol 2010; 298:C1353-62; PMID:20147652; http://dx.doi.org/10.1152/ajpcell.00235.2009
22. A.García-Caballero, V.M.Gadotti, P.Stemkowski, N.Weiss, I.A.Souza, V.Hodgkinson, C.Bladen, L.Chen, J.Hamid, A.Pizzoccaro, et al. The deubiquitinating enzyme USP5 modulates neuropathic and inflammatory pain by enhancing Cav3.2 channel activity. Neuron 2014; 83:1144-58; PMID:25189210; http://dx.doi.org/10.1016/j.neuron.2014.07.036
23. I.Blesneac, J.Chemin, I.Bidaud, S.Huc-Brandt, F.Vandermoere, P.Lory. 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; PMID:26483470
24. N.Weiss, S.A.Black, C.Bladen, L.Chen, G.W.Zamponi. Surface expression and function of Cav3.2 T-type calcium channels are controlled by asparagine-linked glycosylation. Pflugers Arch 2013; 465:1159-70; PMID:23503728; http://dx.doi.org/10.1007/s00424-013-1259-3
25. V3.2 T-type calcium channels. Diabetes 2013; 62:3828-38; PMID:23835327; http://dx.doi.org/10.2337/db13-0813
26. B.Fermini, R.D.Nathan. Removal of sialic acid alters both T- and L-type calcium currents in cardiac myocytes. Am J Physiol 1991; 260:H735-43; PMID:2000969
27. H.F.Yee, J.N.Weiss, G.A.Langer. Neuraminidase selectively enhances transient Ca2+ current in cardiac myocytes. Am J Physiol 1989; 256:C1267-72; PMID:2544097
28. J.Lazniewska, N.Weiss. The “sweet” side of ion channels. Rev Physiol Biochem Pharmacol 2014; 167:67-114; PMID:25239698
29. A.R.Ednie, E.S.Bennett. Modulation of voltage-gated ion channels by sialylation. Compr Physiol 2012; 2:1269-301; PMID:23798301
30. S.Penuela, A.W.Lohman, W.Lai, L.Gyenis, D.W.Litchfield, B.E.Isakson, D.W.Laird. Diverse post-translational modifications of the pannexin family of channel-forming proteins. Channels (Austin) 2014; 8:124-30; PMID:24418849; http://dx.doi.org/10.4161/chan.27422
31. E.Bennett, M.S.Urcan, S.S.Tinkle, A.G.Koszowski, S.R.Levinson. Contribution of sialic acid to the voltage dependence of sodium channel gating. A possible electrostatic mechanism. J Gen Physiol 1997; 109:327-43; PMID:9089440; http://dx.doi.org/10.1085/jgp.109.3.327
32. Y.Zhang, H.A.Hartmann, J.Satin. Glycosylation influences voltage-dependent gating of cardiac and skeletal muscle sodium channels. J Membr Biol 1999; 171:195-207; PMID:10501828; http://dx.doi.org/10.1007/s002329900571
33. I.Watanabe, H.G.Wang, J.J.Sutachan, J.Zhu, E.Recio-Pinto, W.B.Thornhill. Glycosylation affects rat Kv1.1 potassium channel gating by a combined surface potential and cooperative subunit interaction mechanism. J Physiol 2003; 550:51-66; PMID:12879861; http://dx.doi.org/10.1113/jphysiol.2003.040337
34. I.Watanabe, J.Zhu, J.J.Sutachan, A.Gottschalk, E.Recio-Pinto, W.B.Thornhill. The glycosylation state of Kv1.2 potassium channels affects trafficking, gating, and simulated action potentials. Brain Res 2007; 1144:1-18; PMID:17324383; http://dx.doi.org/10.1016/j.brainres.2007.01.092
35. T.A.Schwetz, S.A.Norring, E.S.Bennett. N-glycans modulate K(v)1.5 gating but have no effect on K(v)1.4 gating. Biochim Biophys Acta 2010; 1798:367-75; PMID:19961828; http://dx.doi.org/10.1016/j.bbamem.2009.11.018
36. 2+. Gen Physiol Biophys 2007; 26:234-9
37. R.A.Schwalbe, Z.Wang, B.A.Wible, A.M.Brown. Potassium channel structure and function as reported by a single glycosylation sequon. J Biol Chem 1995; 270:15336-40; PMID:7797521; http://dx.doi.org/10.1074/jbc.270.25.15336
38. D.Baycin-Hizal, A.Gottschalk, E.Jacobson, S.Mai, D.Wolozny, H.Zhang, S.S.Krag, M.J.Betenbaugh. Physiologic and pathophysiologic consequences of altered sialylation and glycosylation on ion channel function. Biochem Biophys Res Commun 2014; 453:243-53; PMID:24971539; http://dx.doi.org/10.1016/j.bbrc.2014.06.067
39. A.François, S.Laffray, A.Pizzoccaro, A.Eschalier, E.Bourinet. T-type calcium channels in chronic pain: mouse models and specific blockers. Pflugers Arch 2014; 466:707-17; PMID:24590509; http://dx.doi.org/10.1007/s00424-014-1484-4
40. E.Bourinet, C.Altier, M.E.Hildebrand, T.Trang, M.W.Salter, G.W.Zamponi. Calcium-permeable ion channels in pain signaling. Physiol Rev 2014; 94:81-140; PMID:24382884; http://dx.doi.org/10.1152/physrev.00023.2013
41. X.H.Cao, H.S.Byun, S.R.Chen, H.L.Pan. Diabetic neuropathy enhances voltage-activated Ca2+ channel activity and its control by M4 muscarinic receptors in primary sensory neurons. J Neurochem 2011; 119:594-603; PMID:21883220; http://dx.doi.org/10.1111/j.1471-4159.2011.07456.x
42. E.Tsakiridou, L.Bertollini, M.de Curtis, G.Avanzini, H.C.Pape. Selective increase in T-type calcium conductance of reticular thalamic neurons in a rat model of absence epilepsy. J Neurosci 1995; 15:3110-7; PMID:7722649
43. Y.Zhang, M.Mori, D.L.Burgess, J.L.Noebels. Mutations in high-voltage-activated calcium channel genes stimulate low-voltage-activated currents in mouse thalamic relay neurons. J Neurosci 2002; 22:6362-71; PMID:12151514
44. Y.Zhang, A.P.Vilaythong, D.Yoshor, J.L.Noebels. Elevated thalamic low-voltage-activated currents precede the onset of absence epilepsy in the SNAP25-deficient mouse mutant coloboma. J Neurosci 2004; 24:5239-48; PMID:15175394; http://dx.doi.org/10.1523/JNEUROSCI.0992-04.2004
45. S.M.Cain, T.P.Snutch. T-type calcium channels in burst-firing, network synchrony, and epilepsy. Biochim Biophys Acta 2013; 1828:1572-8; PMID:22885138; http://dx.doi.org/10.1016/j.bbamem.2012.07.028
46. Y.Chen, J.Lu, H.Pan, Y.Zhang, H.Wu, K.Xu, X.Liu, Y.Jiang, X.Bao, Z.Yao, et al. Association between genetic variation of CACNA1H and childhood absence epilepsy. Ann Neurol 2003; 54:239-43; PMID:12891677; http://dx.doi.org/10.1002/ana.10607
47. H.Khosravani, C.Altier, B.Simms, K.S.Hamming, T.P.Snutch, J.Mezeyova, J.E.McRory, G.W.Zamponi. Gating effects of mutations in the Cav3.2 T-type calcium channel associated with childhood absence epilepsy. J Biol Chem 2004; 279:9681-4; PMID:14729682; http://dx.doi.org/10.1074/jbc.C400006200