Effects of familial hemiplegic migraine type 1 mutation T666M on voltage-gated calcium channel activities in trigeminal ganglion neurons

Journal of Neurophysiology

Volumn 107, Issue 6, 2012, Pages 1666-1680

  Tao, Jin ^a   Liu, Ping ^a   Xiao, Zheman ^a   Zhao, Hucheng ^a   Gerber, Benjamin R ^a   Cao, Yu Qing ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Low voltage activated T type current; Neuronal excitability

Indexed keywords

ISOLECTIN B4; VOLTAGE GATED CALCIUM CHANNEL;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL DENSITY; CELL SIZE; CELL SUBPOPULATION; ELECTRIC POTENTIAL; ELECTROPHYSIOLOGY; FAMILIAL HEMIPLEGIC MIGRAINE; GENE MUTATION; HEMIPARESIS; HUMAN; KNOCKOUT MOUSE; MOUSE; NERVE CELL; NERVE CELL EXCITABILITY; NERVE CELL MEMBRANE STEADY POTENTIAL; NOCICEPTION; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; REPOLARIZATION; TRIGEMINUS GANGLION; WHOLE CELL;

ANIMALS; CALCIUM CHANNELS, N-TYPE; CALCIUM SIGNALING; CELLS, CULTURED; HUMANS; ION CHANNEL GATING; MICE; MICE, KNOCKOUT; MUTATION; NEURONS; PATCH-CLAMP TECHNIQUES; TRIGEMINAL GANGLION;

EID: 84863260618     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00551.2011     Document Type: Article

References (67)

1. + channel currents of rat dorsal root ganglion neurons. J Neurophysiol 85: 644-658, 2001a.
2. Abdulla FA, Smith PA. Axotomy-and autotomy-induced changes in the excitability of rat dorsal root ganglion neurons. J Neurophysiol 85: 630-643, 2001b.
3. Adams PJ, Garcia E, David LS, Mulatz KJ, Spacey SD, Snutch TP. Ca(V)2.1 P/Q-type calcium channel alternative splicing affects the functional impact of familial hemiplegic migraine mutations: implications for calcium channelopathies. Channels 3: 110-121, 2009.
4. 2+ channels governing generation of miniature and evoked excitatory synaptic currents in spinal laminae I and II. J Neurosci 18: 8740-8750, 1998.
5. Barrett CF, Cao YQ, Tsien RW. Gating deficiency in a familial hemiplegic migraine type 1 mutant P/Q-type calcium channel. J Biol Chem 280: 24064-24071, 2005.
6. Borgland SL, Connor M, Christie MJ. Nociceptin inhibits calcium channel currents in a subpopulation of small nociceptive trigeminal ganglion neurons in mouse. J Physiol 536: 35-47, 2001.
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 24: 315-324, 2005.
8. Burstein R. Deconstructing migraine headache into peripheral and central sensitization. Pain 89: 107-110, 2001.
9. Cao YQ. Voltage-gated calcium channels and pain. Pain 126: 5-9, 2006.
10. 2+ channelopathy. Neuron 43: 387-400, 2004.
11. 2+ channel activity and inhibitory synaptic transmission. Proc Natl Acad Sci USA 102: 2590-2595, 2005.
12. + currents generates distinct firing patterns in different subtypes of adult mouse trigeminal ganglion neurones. J Physiol 586: 5101-5118, 2008.
13. Ceruti S, Villa G, Fumagalli M, Colombo L, Magni G, Zanardelli M, Fabbretti E, Verderio C, van den Maagdenberg AM, Nistri A, Abbracchio MP. Calcitonin gene-related peptide-mediated enhancement of purinergic neuron/glia communication by the algogenic factor bradykinin in mouse trigeminal ganglia from wild-type and R192Q Cav2.1 knock-in mice: implications for basic mechanisms of migraine pain. J Neurosci 31: 3638-3649, 2011.
14. 2+ channels. Science 302: 1416-1418, 2003.
15. Choi S, Na HS, Kim J, Lee J, Lee S, Kim D, Park J, Chen CC, Campbell KP, Shin HS. Attenuated pain responses in mice lacking Ca(V)3.2 T-type channels. Genes Brain Behav 6: 425-431, 2007.
16. de Vries B, Frants RR, Ferrari MD, van den Maagdenberg AM. Molecular genetics of migraine. Hum Genet 126: 115-132, 2009.
17. Durham PL, Russo AF. Regulation of calcitonin gene-related peptide secretion by a serotonergic antimigraine drug. J Neurosci 19: 3423-3429, 1999.
18. Ebersberger A, Portz S, Meissner W, Schaible HG, Richter F. Effects of N-, P/Q-and L-type calcium channel blockers on nociceptive neurones of the trigeminal nucleus with input from the dura. Cephalalgia 24: 250-261, 2004.
19. Eikermann-Haerter K, Dilekoz E, Kudo C, Savitz SI, Waeber C, Baum MJ, Ferrari MD, van den Maagdenberg AM, Moskowitz MA, Ayata C. Genetic and hormonal factors modulate spreading depression and transient hemiparesis in mouse models of familial hemiplegic migraine type 1. J Clin Invest 119: 99-109, 2009.
20. Fang Z, Park CK, Li HY, Kim HY, Park SH, Jung SJ, Kim JS, Monteil A, Oh SB, Miller RJ. Molecular basis of Ca(v)2.3 calcium channels in rat nociceptive neurons. J Biol Chem 282: 4757-4764, 2007.
21. Fioretti B, Catacuzzeno L, Sforna L, Gerke-Duncan MB, van den Maagdenberg AM, Franciolini F, Connor M, Pietrobon D. Trigeminal ganglion neuron subtype-specific alterations of CaV2.1 calcium current and excitability in a Cacna1a mouse model of migraine. J Physiol 589: 5879-5895, 2011.
22. Hans M, Luvisetto S, Williams ME, Spagnolo M, Urrutia A, Tottene A, Brust PF, Johnson EC, Harpold MM, Stauderman KA, Pietrobon D. Functional consequences of mutations in the human alpha1A calcium channel subunit linked to familial hemiplegic migraine. J Neurosci 19: 1610-1619, 1999.
23. Headache Classification Subcommittee of the International Headache Society. The International Classification of Headache Disorders: 2nd edition. Cephalalgia 24, Suppl 1: 9-160, 2004.
24. 2+ channels to nociceptive transmission in rat spinal lamina I neurons. Eur J Neurosci 19: 103-111, 2004.
25. Ho TW, Edvinsson L, Goadsby PJ. CGRP and its receptors provide new insights into migraine pathophysiology. Nat Rev Neurol 6: 573-582, 2010.
26. Hogan QH. Role of decreased sensory neuron membrane calcium currents in the genesis of neuropathic pain. Croat Med J 48: 9-21, 2007.
27. Hong KW, Kim CD, Rhim BY, Lee WS. Effect of omega-conotoxin GVIA and omega-agatoxin IVA on the capsaicin-sensitive calcitonin gene-related peptide release and autoregulatory vasodilation in rat pial arteries. J Cereb Blood Flow Metab 19: 53-60, 1999.
28. Iftinca M, Hamid J, Chen L, Varela D, Tadayonnejad R, Altier C, Turner RW, Zamponi GW. Regulation of T-type calcium channels by Rhoassociated kinase. Nat Neurosci 10: 854-860, 2007.
29. 2+ channels in trigeminal ganglion neurons from neonatal rats. Life Sci 73: 1175-1187, 2003.
30. Jagodic MM, Pathirathna S, Joksovic PM, Lee W, Nelson MT, Naik AK, Su P, Jevtovic-Todorovic V, Todorovic SM. Upregulation of the T-type calcium current in small rat sensory neurons after chronic constrictive injury of the sciatic nerve. J Neurophysiol 99: 3151-3156, 2008.
31. Jagodic MM, Pathirathna S, Nelson MT, Mancuso S, Joksovic PM, Rosenberg ER, Bayliss DA, Jevtovic-Todorovic V, Todorovic SM. Cellspecific alterations of T-type calcium current in painful diabetic neuropathy enhance excitability of sensory neurons. J Neurosci 27: 3305-3316, 2007.
32. Jen J, Kim GW, Baloh RW. Clinical spectrum of episodic ataxia type 2. Neurology 62: 17-22, 2004.
33. Jen JC, Graves TD, Hess EJ, Hanna MG, Griggs RC, Baloh RW. Primary episodic ataxias: diagnosis, pathogenesis and treatment. Brain 130: 2484-2493, 2007.
34. Julius D, Basbaum AI. Molecular mechanisms of nociception. Nature 413: 203-210, 2001.
35. Jun K, Piedras-Renteria ES, Smith SM, Wheeler DB, Lee SB, Lee TG, Chin H, Adams ME, Scheller RH, Tsien RW, Shin HS. Ablation of P/Q-type Ca(2+) channel currents, altered synaptic transmission, and progressive ataxia in mice lacking the alpha(1A)-subunit. Proc Natl Acad Sci USA 96: 15245-15250, 1999.
36. Knight YE, Bartsch T, Kaube H, Goadsby PJ. P/Q-type calcium-channel blockade in the periaqueductal gray facilitates trigeminal nociception: a functional genetic link for migraine? J Neurosci 22: RC213, 2002.
37. 2+ channel kinetics. J Biol Chem 273: 5586-5590, 1998.
38. Labrum RW, Rajakulendran S, Graves TD, Eunson LH, Bevan R, Sweeney MG, Hammans SR, Tubridy N, Britton T, Carr LJ, Ostergaard JR, Kennedy CR, Al-Memar A, Kullmann DM, Schorge S, Temple K, Davis MB, Hanna MG. Large scale calcium channel gene rearrangements in episodic ataxia and hemiplegic migraine: implications for diagnostic testing. J Med Genet 46: 786-791, 2009.
39. Lipton RB, Stewart WF, Diamond S, Diamond ML, Reed M. Prevalence and burden of migraine in the United States: data from the American Migraine Study II. Headache 41: 646-657, 2001.
40. McCallum JB, Kwok WM, Sapunar D, Fuchs A, Hogan QH. Painful peripheral nerve injury decreases calcium current in axotomized sensory neurons. Anesthesiology 105: 160-168, 2006.
41. Mintz IM, Venema VJ, Swiderek KM, Lee TD, Bean BP, Adams ME. P-type calcium channels blocked by the spider toxin omega-Aga-IVA. Nature 355: 827-829, 1992.
42. Morikawa T, Matsuzawa Y, Makita K, Katayama Y. Antimigraine drug, zolmitriptan, inhibits high-voltage activated calcium currents in a population of acutely dissociated rat trigeminal sensory neurons. Mol Pain 2: 10, 2006.
43. 2+ channel gating: evidence for beta-subunit isoform-specific effects. J Biol Chem 279: 51844-51850, 2004.
44. Nahm SS, Jung KY, Enger MK, Griffith WH, Abbott LC. Differential expression of T-type calcium channels in P/Q-type calcium channel mutant mice with ataxia and absence epilepsy. J Neurobiol 62: 352-360, 2005.
45. Nair A, Simonetti M, Birsa N, Ferrari MD, van den Maagdenberg AM, Giniatullin R, Nistri A, Fabbretti E. Familial hemiplegic migraine Ca(v)2.1 channel mutation R192Q enhances ATP-gated P2X3 receptor activity of mouse sensory ganglion neurons mediating trigeminal pain. Mol Pain 6: 48, 2010.
46. Nelson MT, Todorovic SM, Perez-Reyes E. The role of T-type calcium channels in epilepsy and pain. Curr Pharm Des 12: 2189-2197, 2006.
47. 2+ channel gene CACNL1A4. Cell 87: 543-552, 1996.
48. Perez-Reyes E. Molecular physiology of low-voltage-activated t-type calcium channels. Physiol Rev 83: 117-161, 2003.
49. Pietrobon D. Function and dysfunction of synaptic calcium channels: insights from mouse models. Curr Opin Neurobiol 15: 257-265, 2005.
50. Pietrobon D. Insights into migraine mechanisms and CaV2.1 calcium channel function from mouse models of familial hemiplegic migraine. J Physiol 588: 1871-1878, 2010.
51. Pietrobon D, Striessnig J. Neurobiology of migraine. Nat Rev 4: 386-398, 2003.
52. Price TJ, Flores CM. Critical evaluation of the colocalization between calcitonin gene-related peptide, substance P, transient receptor potential vanilloid subfamily type 1 immunoreactivities, and isolectin B4 binding in primary afferent neurons of the rat and mouse. J Pain 8: 263-272, 2007.
53. 2+ currents elicited by action potential waveforms in acutely isolated adult rat dorsal root ganglion neurons. J Neurosci 12: 1789-1801, 1992.
54. Snider WD, McMahon SB. Tackling pain at the source: new ideas about nociceptors. Neuron 20: 629-632, 1998.
55. 2+-dependent inactivation. J Neurosci 22: 10142-10152, 2002.
56. Strassman AM, Raymond SA, Burstein R. Sensitization of meningeal sensory neurons and the origin of headaches. Nature 384: 560-564, 1996.
57. Stucky CL, Lewin GR. Isolectin B(4)-positive and-negative nociceptors are functionally distinct. J Neurosci 19: 6497-6505, 1999.
58. Talley EM, Cribbs LL, Lee JH, Daud A, Perez-Reyes E, Bayliss DA. Differential distribution of three members of a gene family encoding low voltage-activated (T-type) calcium channels. J Neurosci 19: 1895-1911, 1999.
59. Tottene A, Fellin T, Pagnutti S, Luvisetto S, Striessnig J, Fletcher C, Pietrobon D. Familial hemiplegic migraine mutations increase Ca(2+) influx through single human CaV2.1 channels and decrease maximal CaV21 current density in neurons. Proc Natl Acad Sci USA 99: 13284-13289, 2002.
60. Tottene A, Pivotto F, Fellin T, Cesetti T, van den Maagdenberg AM, Pietrobon D. Specific kinetic alterations of human CaV2.1 calcium channels produced by mutation S218L causing familial hemiplegic migraine and delayed cerebral edema and coma after minor head trauma. J Biol Chem 280: 17678-17686, 2005.
61. Tottene A, Volsen S, Pietrobon D. Alpha(1E) subunits form the pore of three cerebellar R-type calcium channels with different pharmacological and permeation properties. J Neurosci 20: 171-178, 2000.
62. Tsien RW, Wheeler DB. Voltage-gated calcium channels. In: Calcium as a Cellular Regulator, edited by Carafoli E, Klee CB. New York: Oxford University Press 171-199, 1999.
63. van Den Maagdenberg AM, Pietrobon D, Pizzorusso T, Kaja S, Broos LA, Cesetti T, Van De Ven RC, Tottene A, Van Der Kaa J, Plomp JJ, Frants RR, Ferrari MD. A cacna1a knockin migraine mouse model with increased susceptibility to cortical spreading depression. Neuron 41: 701-710, 2004.
64. van den Maagdenberg AM, Pizzorusso T, Kaja S, Terpolilli N, Shapovalova M, Hoebeek FE, Barrett CF, Gherardini L, van de Ven RC, Todorov B, Broos LA, Tottene A, Gao Z, Fodor M, De Zeeuw CI, Frants RR, Plesnila N, Plomp JJ, Pietrobon D, Ferrari MD. High cortical spreading depression susceptibility and migraine-associated symptoms in Ca(v)2.1 S218L mice. Ann Neurol 67: 85-98, 2010.
65. Xie G, Clapcote SJ, Nieman BJ, Tallerico T, Huang Y, Vukobradovic I, Cordes SP, Osborne LR, Rossant J, Sled JG, Henderson JT, Roder JC. Forward genetic screen of mouse reveals dominant missense mutation in the P/Q-type voltage-dependent calcium channel, CACNA1A. Genes Brain Behav 6: 717-727, 2007.
66. Zhang Y, Mori M, Burgess DL, Noebels JL. Mutations in high-voltageactivated calcium channel genes stimulate low-voltage-activated currents in mouse thalamic relay neurons. J Neurosci 22: 6362-6371, 2002.
67. 2+ channelmutant mouse, tottering. J Physiol 547: 497-507, 2003.