Familial hemiplegic migraine type 1 mutations W1684R and V1696I alter G protein-mediated regulation of CaV2.1 voltage-gated calcium channels

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1822, Issue 8, 2012, Pages 1238-1246

  Garza López, Edgar ^a   Sandoval, Alejandro ^b   González Ramírez, Ricardo ^c   Gandini, María A ^a   Van den Maagdenberg, Arn ^d   De Waard, Michel ^e,f   Felix, Ricardo ^a  

^a DEPARTAMENTO DE FÍSICA   (Mexico)

^b UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^c HOSPITAL GENERAL DR MANUEL GEA GONZÁLEZ   (Mexico)

^d LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^e GRENOBLE INSTITUT DES NEUROSCIENCES   (France)

^f UNIV GRENOBLE ALPES   (France)

Author keywords

Calcium channel; Familial hemiplegic migraine; FHM 1; G protein regulation; Migraine

Indexed keywords

ENKEPHALIN[2 DEXTRO ALANINE 4 METHYLPHENYLALANINE 5 GLYCINE]; G PROTEIN COUPLED RECEPTOR; GUANINE NUCLEOTIDE BINDING PROTEIN; MU OPIATE RECEPTOR; VOLTAGE GATED CALCIUM CHANNEL;

ARTICLE; CELL CULTURE; CELL STRAIN HEK293; CEREBELLAR ATAXIA; CONTROLLED STUDY; EMBRYO; FAMILIAL HEMIPLEGIC MIGRAINE; FAMILIAL HEMIPLEGIC MIGRAINE TYPE 1; GENE CONTROL; GENE EXPRESSION; GENE MUTATION; HUMAN; HUMAN CELL; MISSENSE MUTATION; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL;

ANIMALS; CALCIUM CHANNELS, N-TYPE; CELL LINE; CEREBELLAR ATAXIA; GENOME-WIDE ASSOCIATION STUDY; GENOTYPE; GTP-BINDING PROTEINS; HEK293 CELLS; HUMANS; ION CHANNEL GATING; MICE; MIGRAINE DISORDERS; MUTATION; RATS; RECEPTORS, OPIOID, MU; TRANSFECTION;

EID: 84861215890     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2012.04.008     Document Type: Article

References (50)

1. Goadsby P.J., Lipton R.B., Ferrari M.D. Migraine - current understanding and treatment. N. Engl. J. Med. 2002, 346:257-270.
2. Anttila V., Stefansson H., Kallela M., Todt U., Terwindt G.M., Calafato M.S., Nyholt D.R., Dimas A.S., Freilinger T., Müller-Myhsok B., Artto V., Inouye M., Alakurtti K., Kaunisto M.A., Hämäläinen E., De Vries B., Stam A.H., Weller C.M., Heinze A., Heinze-Kuhn K., Goebel I., Borck G., Göbel H., Steinberg S., Wolf C., Björnsson A., Gudmundsson G., Kirchmann M., Hauge A., Werge T., Schoenen T., Eriksson J.G., Hagen K., Stovner L., Wichmann H.E., Meitinger T., Alexander M., Moebus S., Schreiber S., Aulchenko Y.S., Breteler M.M., Uitterlinden A.G., Hofman A., Van Duijn C.M., Tikka-Kleemola P., Vepsäläinen S., Lucae S., Tozzi F., Muglia P., Barrett J., Kaprio J., Färkkilä M., Peltonen L., Stefansson K., Zwart J.A., Ferrari M.D., Olesen J., Daly M., Wessman M., Van den Maagdenberg A.M., Dichgans M., Kubisch C., Dermitzakis E.T., Frants R.R., Palotie A. Genome-wide association study of migraine implicates a common susceptibility variant on 8q22.1. Nat. Genet. 2010, 42:869-873. on behalf of the International Headache Genetics Consortium.
3. Chasman D.I., Schürks M., Anttila V., De Vries B., Schminke U., Launer L.J., Terwindt G.M., Van den Maagdenberg A.M., Fendrich K., Völzke H., Ernst F., Griffiths L.R., Buring J.E., Kallela M., Freilinger T., Kubisch C., Ridker P.M., Palotie A., Ferrari M.D., Hoffmann W., Zee R.Y., Kurth T. Genome-wide association study reveals three susceptibility loci for common migraine in the general population. Nat. Genet. 2011, 43:695-698.
4. Ferrari M.D., Van den Maagdenberg A.M., Frants R.R., Goadsby P.J. Migraine as a cerebral ionopathy with impaired central sensory processing. Molecular Neurology 2007, 439-461. Elsevier, Amsterdam. S.G. Waxman (Ed.).
5. Rajakulendran S., Kaski D., Hanna M.G. Neuronal P/Q-type calcium channel dysfunction in inherited disorders of the CNS. Nat. Rev. Neurol. 2012, 8:86-96.
6. Ducros A., Dernier C., Joutel A., Cecillon M., Lescoat C., Vahedi K., Darcel F., Vicaut E., Bousser M.G., Tournier-Lasserve E. The clinical spectrum of familial hemiplegic migraine associated with mutations in a neuronal calcium channel. N. Engl. J. Med. 2001, 354:17-24.
7. De Vries B., Frants R.R., Ferrari M.D., Van den Maagdenberg A.M. Molecular genetics of migraine. Hum. Genet. 2009, 126:115-132.
8. Felix R. Calcium channelopathies. Neuromolecular Med. 2006, 8:307-318.
9. Pietrobon D. Familial hemiplegic migraine. Neurotherapeutics 2007, 4:274-284.
10. O.D. Uchitel, C.G. Inchauspe, F.J. Urbano, M.N. Di Guilmi, CaV2.1 voltage activated calcium channels and synaptic transmission in familial hemiplegic migraine pathogenesis. J. Physiol. Paris (in press).
11. V2.1 calcium channel function from mouse models of familial hemiplegic migraine. J. Physiol. 2010, 588:1871-1878.
12. 1A calcium channel subunit linked to familial hemiplegic migraine. J. Neurosci. 1999, 19:1610-1619.
13. V2.1 current density in neurons. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:13284-13289.
14. Barrett C.F., Cao Y.Q., Tsien R.W. Gating deficiency in a familial hemiplegic migraine type 1 mutant P/Q-type calcium channel. J. Biol. Chem. 2005, 280:24064-24071.
15. Van den Maagdenberg A.M., Pietrobon D., Pizzorusso T., Kaja S., Broos L.A., Cesetti T., Van de Ven R.C., Tottene A., Van der Kaa J., Plomp J.J., Frants R.R., Ferrari M.D. A Cacna1a knockin migraine mouse model with increased susceptibility to cortical spreading depression. Neuron 2004, 41:701-710.
16. V2.1 S218L mice. Ann. Neurol. 2010, 67:85-98.
17. V2.1 knockin migraine mice. Neuron 2009, 61:762-773.
18. V2.1) calcium channels expressed in human embryonic kidney cells. J. Physiol. 2003, 546:337-347.
19. V2.1 calcium channels during direct G-protein regulation. Pflugers Arch. 2008, 457:315-326.
20. Serra S.A., Fernandez-Castillo N., Macaya A., Cormand B., Valverde M.A., Fernandez-Fernandez J.M. The hemiplegic migraine-associated Y1245C mutation in CACNA1A results in a gain of channel function due to its effect on the voltage sensor and G-protein-mediated inhibition. Pflugers Arch. 2009, 458:489-502.
21. 1A-containing high-voltage-activated calcium channels. Biophys. J. 1999, 76:1384-1400.
22. Castellano A., Wei X., Birnbaumer L., Perez-Reyes E. Cloning and expression of a neuronal calcium channel β subunit. J. Biol. Chem. 1993, 268:12359-12366.
23. 2 subunit. Proc. Natl. Acad. Sci. U. S. A. 1992, 89:3251-3255.
24. 2+ channel gating: evidence for β-subunit isoform-specific effects. J. Biol. Chem. 2004, 279:51844-51850.
25. V2.2 channels. Pflugers Arch. 2011, 461:447-459.
26. 2δ subunit. J. Neurosci. 1997, 17:6884-6891.
27. 2+ channels in insulin release. J. Biol. Chem. 2011, 286:15757-15765.
28. Hamill O.P., Marty A., Neher E., Sakmann B., Sigworth F.J. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 1981, 391:85-100.
29. + channel activity in HEK-293 cells. Cell. Mol. Neurobiol. 2004, 24:317-330.
30. Chen X., Wang Q., Ni F., Ma J. Structure of the full-length Shaker potassium channel Kv1.2 by normal-mode-based X-ray crystallographic refinement. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:11352-11357.
31. Liang J., Subramaniam S. Computation of molecular electrostatics with boundary element methods. Biophys. J. 1997, 73:1830-1841.
32. Bailey C.P., Connor M. Opioids: cellular mechanisms of tolerance and physical dependence. Curr. Opin. Pharmacol. 2005, 5:60-68.
33. Currie K.P., Fox A.P. Comparison of N- and P/Q- type voltage-gated calcium channel current inhibition. J. Neurosci. 1997, 17:4570-4579.
34. Arnot M.I., Stotz S.C., Jarvis S.E., Zamponi G.W. Differential modulation of N-type 1B and P/Q-type 1A calcium channels by different G protein subunit isoforms. J. Physiol. 2000, 527:203-212.
35. Cantí C., Bogdanov Y., Dolphin A.C. Interaction between G proteins and accessory β subunits in the regulation of α1B calcium channels in Xenopus oocytes. J. Physiol. 2000, 527:419-432.
36. Meza U., Adams B. G-protein-dependent facilitation of neuronal α1A, α1B, and α1E Ca channels. J. Neurosci. 1998, 18:5240-5252.
37. Zakharov S.D., Heymann J.B., Zhang Y.L., Cramer W.A. Membrane binding of the colicin E1 channel: activity requires an electrostatic interaction of intermediate magnitude. Biophys. J. 1996, 70:2774-2783.
38. Schleifer K.J., Höltje H.D. Molecular modelling investigation of wild-type and the R528H mutated segment IIS4 of human L-type voltage-gated calcium channels. Protein Eng. 1998, 11:1033-1040.
39. Hildebrandt A., Blossey R., Rjasanow S., Kohlbacher O., Lenhof H.P. Electrostatic potentials of proteins in water: a structured continuum approach. Bioinformatics 2007, 23:e99-e103.
40. 2+ channels - integration centers for neuronal signaling pathways. Trends Neurosci. 2006, 29:617-624.
41. Mori Y., Friedrich T., Kim M.S., Mikami A., Nakai J., Ruth P., Bosse E., Hofmann F., Flockerzi V., Furuichi T., Mikoshiba K., Imoto K., Tanabe T., Numa S. Primary structure and functional expression from complementary DNA of a brain calcium channel. Nature 1991, 350:398-402.
42. Starr T.V., Prystay W., Snutch T.P. Primary structure of a calcium channel that is highly expressed in the rat cerebellum. Proc. Natl. Acad. Sci. U. S. A. 1991, 88:5621-5625.
43. 2+ channel gene CACNL1A4. Cell 1996, 87:543-552.
44. Zhuchenko O., Bailey J., Bonnen P., Ashizawa T., Stockton D.W., Amos C., Dobyns W.B., Subramony S.H., Zoghbi H.Y., Lee C.C. Autosomal dominant cerebellar ataxia (SCA6) associated with small polyglutamine expansions in the α1A-voltage-dependent calcium channel. Nat. Genet. 1997, 15:62-69.
45. De Waard M., Liu H., Walker D., Scott V.E., Gurnett C.A., Campbell K.P. Direct binding of G-protein βγ complex to voltage-dependent calcium channels. Nature 1997, 385:446-450.
46. Zamponi G.W., Bourinet E., Nelson D., Nargeot J., Snutch T.P. Crosstalk between G proteins and protein kinase C mediated by the calcium channel alpha1 subunit. Nature 1997, 385:442-446.
47. V2 voltage-gated calcium channels. Channels (Austin) 2010, 4:497-509.
48. V2 calcium channels. Pharmacol. Rev. 2006, 58:837-862.
49. Van den Maagdenberg A.M., Haan J., Terwindt G.M., Ferrari M.D. Migraine: gene mutations and functional consequences. Curr. Opin. Neurol. 2007, 20:299-305.
50. Weiss N., Tournier-Lasserve E., De Waard M. Role of P/Q calcium channel in familial hemiplegic migraine. Med Sci (Paris) 2007, 23:53-63.