Involvement of gap junction channels in the pathophysiology of migraine with aura

Frontiers in Physiology

Volumn 5 FEB, Issue , 2014, Pages

  Sarrouilhe, Denis ^a   Dejean, Catherine ^b   Mesnil, Marc ^a  

^a UNIVERSITÉ DE POITIERS   (France)

^b Centre Hospitalier Henri Laborit (Poitiers)   (France)

Author keywords

Aura; Connexin; Cortical spreading depression; Gap junction; Pannexin; Tonabersat; Trigeminovascular

Indexed keywords

ACETYLSALICYLIC ACID; AMITRIPTYLINE; CANDESARTAN; CARBENOXOLONE; DICLOFENAC; ERGOT DERIVATIVE; FLUNARIZINE; GABAPENTIN; GAP JUNCTION PROTEIN; IBUPROFEN; KETOPROFEN; LAMOTRIGINE; LISINOPRIL; METHYSERGIDE; METOPROLOL; NAPROXEN; NONSTEROID ANTIINFLAMMATORY AGENT; OLCEGEPANT; OXETORONE; PIZOTIFEN; PLACEBO; PROBENECID; PROPRANOLOL; TELCAGEPANT; TELMISARTAN; TONABERSAT; TOPIRAMATE; TRIPTAN DERIVATIVE; UNINDEXED DRUG; VALPROIC ACID;

ANTIINFLAMMATORY ACTIVITY; BRAIN CORTEX; BRAIN STEM; CENTRAL NERVOUS SYSTEM; DOSE RESPONSE; DRUG WITHDRAWAL; GAP JUNCTION; HUMAN; HYPOTENSION; MIGRAINE WITH AURA; NEUROGENIC INFLAMMATION; NEUROTRANSMISSION; NONHUMAN; PATHOPHYSIOLOGY; PROPHYLAXIS; PROTEIN LOCALIZATION; REVIEW; SPREADING CORTICAL DEPRESSION; STRUCTURE ACTIVITY RELATION; THALAMUS; UNSPECIFIED SIDE EFFECT; VASOCONSTRICTION;

EID: 84895429192     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2014.00078     Document Type: Review

References (81)

1. Abrams, C. K., and Scherer, S. S. (2012). Gap junctions in inherited human disorders of the central nervous system. Biochim. Biophys. Acta 1818, 2030-2047. doi: 10.1016/j.bbamem.2011.08.015.
2. Alldredge, B. (2008). Clinical connexions. J. Clin. Pathol. 61, 885-890. doi: 10.1136/jcp.2008.055699.
3. Antilla, V., Stefansson, H., Kallela, M., Todt, U., Terwindt, G. M., Calafato, M. S., et al. (2010). Genome-wide association study of migraine implicates a common susceptibility variant on 8q22.1. Nat. Genet. 42, 869-873. doi: 10.1038/ng.652.
4. Aurora, S. K., Barrodale, P. M., McDonald, S. A., Jakubowski, M., and Burstein, R. (2009). Revisiting the efficacy of sumatriptan therapy during the aura phase of migraine. Headache 49, 1001-1004. doi: 10.1111/j.1526-4610.2009.01429.x.
5. Aurora, S. K., Kori, S. H., Barrodale, P., McDonald, S. A., and Haseley, D. (2006). Gastric stasis in migraine: more than just a paroxysmal abnormality during a migraine attack. Headache 46, 57-63. doi: 10.1111/j.1526-4610.2006.00311.x.
6. Bekkelund, S. I., and Alstadhaug, K. B. (2011). Migraine prophylactic drugs-something new under the sun? Expert Opin. Investig. Drugs 20, 1201-1210. doi: 10.1517/13543784.2011.601741.
7. Bialer, M., Johannessen, S. I., Levy, R. H., Perucca, E., Tomson, T., and White, H. S. (2013). Progress report on new antiepileptic drugs: a summary of the eleventh Eilat conference (EILAT XI). Epilepsy Res. 103, 2-30. doi: 10.1016/j.eplepsyres.2012.10.001.
8. Bolay, H., Reuter, U., Dunn, A. K., Huang, Z., Boas, D. A., and Moskowitz, M. A. (2002). Intrinsic brain activity triggers trigeminal meningeal afferents in a migraine model. Nat. Med. 8, 136-142. doi: 10.1038/nm0202-136.
9. Bradley, D. P., Smith, M. I., Netsiri, C., Smith, J. M., Bockhorst, K. H. J., Hall, L. D., et al. (2001). Diffusion-weighted MRI used to detect in vivo modulation of cortical spreading depression: comparison of sumatriptan and tonabersat. Exp. Neurol. 172, 342-353. doi: 10.1006/exnr.2001.7809.
10. Budunova, I. V., and Williams, G. M. (1994). Cell culture assays for chemicals with tumor-promoting or tumor-inhibiting activity based on the modulation of intercellular communication. Cell Biol. Toxicol. 10, 71-116. doi: 10.1007/BF00756491.
11. Chakravarty, A. (2010). How triggers trigger acute migraine attacks: a hypothesis. Med. Hypotheses 74, 750-753. doi: 10.1016/j.mehy.2009.10.027.
12. Chan, W. N., Evans, J. M., Hadley, M. S., Herdon, H. J., Jerman, J. C., Parsons, A. A., et al. (1999). Identification of (-)-cis-6-acetyl-4S-(3-chloro-4-fluoro-benzoylamino)-3,4-dihydro-2,2-dimethyl-2H-benzo[b] pyran-3S-ol as a potential antimigraine agent. Bioorg. Med. Chem. Lett. 9, 285-290. doi: 10.1016/S0960-894X(98)00728-8.
13. Charles, A. C., and Baca, S. M. (2013). Cortical spreading depression and migraine. Nat. Rev. Neurol. 9, 637-644. doi: 10.1038/nrneurol.2013.192.
14. Chasman, D. I., Schurks, M., Anttila, V., de Vries, B., Schminke, U., Launer, L. J., et al. (2011). Genome-wide association study reveals three susceptibility loci for common migraine in the general population. Nat. Genet. 43, 695-699. doi: 10.1038/ng.856.
15. Chiang, C. Y., Li, Z., Dostrovsky, J. O., and Sessle, B. J. (2010). Central sensitization in medullary dorsal horn involves gap junctions and hemichannels. Neuroreport 21, 233-237. doi: 10.1097/WNR.0b013e328336eecb.
16. Costa, C., Tozzi, A., Rainero, I., Cupini, L. M., Calabresi, P., Ayata, C., et al. (2013). Cortical spreading depression as a target for anti-migraine agents. J. Headache Pain 14, 62. doi: 10.1186/1129-2377-14-62.
17. Dahl, G., and Keane, R. W. (2012). Pannexin: from discovery to bedside in 11 ± 4 years? Brain Res. 1487, 150-159. doi: 10.1016/j.brainres.2012.04.058.
18. Dahlöf, C. G. H., Hauge, A. W., and Olesen, J. (2009). Efficacy and safety of tonabersat, a gap-junction modulator, in the acute treatment of migraine: a double-blind, parallel-group, randomized study. Cephalalgia 29, 7-16. doi: 10.1111/j.1468-2982.2009.01975.x.
19. Damodaram, S., Thalakoti, S., Freeman, S. E., Garrett, F. G., and Durham, P. L. (2008). Tonabersat inhibits trigeminal ganglion neuronal-satellite glial cell signaling. Headache 49, 5-20. doi: 10.1111/j.1526-4610.2008.01262.x.
20. D'Andrea, G., Collavito, D., Dalle Carbonare, M., and Leon, A. (2011). Migraine with aura: conventional and non-conventional treatments. Neurol. Sci. 32, S121-S129. doi: 10.1007/s10072-011-0529-0.
21. Durham, P. L., and Garrett, F. G. (2009). Neurological mechanisms of migraine: potential of the gap-junction modulator tonabersat in prevention of migraine. Cephalalgia 29, 1-6. doi: 10.1111/j.1468-2982.2009.01976.x.
22. Edvinsson, L., Villalón, C. M., and MaassenVanDenBrink, A. (2012). Basic mechanisms of migraine and its acute treatment. Pharmacol. Ther. 136, 319-333. doi: 10.1016/j.pharmthera.2012.08.011.
23. Eriksen, M. K., Thomsen, L. L., Andersen, I., Nazim, F., and Olesen, J. (2004). Clinical characteristics of 362 patients with familial migraine with aura. Cephalalgia 24, 564-575. doi: 10.1111/j.1468-2982.2003.00718.x.
24. Evers, S., Afra, J., Frese, A., Goadsby, P. J., Linde, M., May, A., et al. (2009). EFNS guideline on the drug treatment of migraine-revised report of an EFNS task force. Eur. J. Neurol. 16, 968-981. doi: 10.1111/j.1468-1331.2009.02748.x.
25. Garrett, F. G., and Durham, P. L. (2008). Differential expression of connexins in trigeminal ganglion neurons and satellite glial cells in response to chronic or acute joint inflammation. Neuron. Glia Biol. 4, 295-306. doi: 10.1017/S1740925X09990093.
26. Goadsby, P. J., Charbit, A. R., Andreou, A. P., Akerman, S., and Holland, P. R. (2009a). Neurobiology of migraine. Nat. Rev. Neurosci. 161, 327-341. doi: 10.1016/j.neuroscience.2009.03.019.
27. Goadsby, P. J., Ferrari, M. D., Csanyi, A., Olesen, J., and Mills, J. G. (2009b). Randomized, double-blind, placebo-controlled, proof-of-concept study of the cortical spreading depression inhibiting agent tonabersat in migraine prophylaxis. Cephalalgia 29, 742-750. doi: 10.1111/j.1468-2982.2008.01804.x.
28. Hauge, A. W., Asghar, M. S., Schytz, H. W., Christensen, K., and Olesen, J. (2009). Effects of tonabersat on migraine with aura: a randomized, double-blind, placebo-controlled crossover study. Lancet Neurol. 8, 718-723. doi: 10.1016/S1474-4422(09)70135-8.
29. Haut, S. R., Bigal, M. E., and Lipton, R. B. (2006). Chronic disorders with episodic manifestations: focus on epilepsy and migraine. Lancet Neurol. 5, 148-157. doi: 10.1016/S1474-4422(06)70348-9.
30. Headache classification subcommittee of the International Headache Society. (2004). The international classification of headache disorders: 2nd edition. Cephalalgia 24, 9-160.
31. Hervé, J. C., Bourmeyster, N., and Sarrouilhe, D. (2004). Diversity in protein-protein interactions of connexins: emerging roles. Biochim. Biophys. Acta 1662, 22-41. doi: 10.1016/j.bbamem.2003.10.022.
32. Hervé, J. C., and Sarrouilhe, D. (2005). Connexin-made channels as pharmacological targets. Curr. Pharm. Des. 11, 1941-1958. doi: 10.2174/1381612054021060.
33. Holland, P. R., Akerman, S., and Goadsby, P. J. (2010). Cortical spreading depression-associated cerebral blood flow changes induced by mechanical stimulation are modulated by AMPA and GABA receptors. Cephalalgia 30, 519-527. doi: 10.1111/j.1468-2982.2009.02021.x.
34. Kar, R., Batra, N., Riquelme, M. A., and Jiang, J. X. (2012). Biological role of connexin intercellular channels and hemichannels. Arch. Biochem. Biophys. 524, 2-15. doi: 10.1016/j.abb.2012.03.008.
35. Karatas, H., Erdener, S. E., Gursoy-Ozdemir, Y., Lule, S., Eren-Koçak, E., Sen, Z. D., et al. (2013). Spreading depression triggers headache by activating neuronal panx1 channels. Science 339, 1092-1095. doi: 10.1126/science.1231897.
36. Kruit, M. C., van Buchem, M. A., Launer, L. J., Terwindt, G. M., and Ferrari, M. D. (2010). Migraine is associated with an increased risk of deep white matter lesions, subclinical posterior circulation infarcts and brain iron accumulation: the population-based MRI camera-study. Cephalalgia 30, 129-136. doi: 10.1111/j.1468-2982.2009.01904.x.
37. Kumar, N. M., and Gilula, N. B. (1996). The gap junction communication channel. Cell 84, 381-388. doi: 10.1016/S0092-8674(00)81282-9.
38. Kurth, T., Chabriat, H., and Bousser, M. G. (2012). Migraine and stroke: a complex association with clinical implications. Lancet Neurol. 11, 92-100. doi: 10.1016/S1474-4422(11)70266-6.
39. Lafrenière, R. G., Cader, M. Z., Poulin, J. F., Andres-Enguix, I., Simoneau, M., and Gupta, N. (2010). A dominant-negative mutation in the TRESK potassium channel is linked to familial migraine with aura. Nat. Med. 16, 1157-1161. doi: 10.1038/nm.2216.
40. Lampl, C., Katsarava, Z., Diener, H. C., and Limmroth, V. (2005). Lamotrigine reduces migraine aura and migraine attacks in patients with migraine with aura. J. Neurol. Neurosurg. Psychiatry 76, 1730-1732. doi: 10.1136/jnnp.2005.063750.
41. Lipton, R. B., Bigal, M. E., Steiner, T. J., Silberstein, S. B., and Olesen, J. (2004). Classification of primary headaches. Neurology 63, 427-435. doi: 10.1212/01.WNL.0000133301.66364.9B.
42. Lipton, R. B., Stewart, W. F., Diamond, S., Diamond, M. L., and Reed, M. (2001). Prevalence and burden of migraine in the United States: data from the American migraine study II. Headache 41, 646-657. doi: 10.1046/j.1526-4610.2001.041007646.x.
43. MaassenVanDenBrink, A., van den Broek, R. W. M., de Vries, R., Upton, N., Parsons, A. A., and Saxena, P. R. (2000). The potential anti-migraine compound SB-220453 does not contract human isolated blood vessels or myocardium; a comparison with sumatriptan. Cephalalgia 20, 538-545. doi: 10.1046/j.1468-2982.2000.00078.x.
44. MacVicar, B. A., and Thompson, R. J. (2009). Non-junction functions of pannexin-1 channels. Trends Neurosci. 33, 93-102. doi: 10.1016/j.tins.2009.11.007.
45. Margineanu, D. G., and Klitgaard, H. (2006). The connexin 36 blockers quinine, quinidine and mefloquine inhibit cortical spreading depression in a rat neocortical slice model in vitro. Brain Res. Bull. 71, 23-28. doi: 10.1016/j.brainresbull.2006.07.011.
46. Marmura, M. J., and Silberstein, S. D. (2011). Current understanding and treatment of headache disorders: five new things. Neurology 76, S31-S35. doi: 10.1212/WNL.0b013e31820c95cc.
47. Martins-Ferreira, H., Nedergaard, M., and Nicholson, C. (2000). Perspectives on spreading depression. Brain Res. Rev. 32, 215-234. doi: 10.1016/S0165-0173(99)00083-1.
48. Nakase, T., and Naus, C. C. (2004). Gap junctions and neurological disorders of the central nervous system. Biochim. Biophys. Acta 1662, 149-158. doi: 10.1016/j.bbamem.2004.01.009.
49. Olesen, J., and Ashina, M. (2011). Emerging migraine treatments and drug targets. Trends Pharmacol. Sci. 32, 352-359. doi: 10.1016/j.tips.2011.02.016.
50. Olesen, J., Burstein, R., Ashina, M., and Tfelt-Hansen, P. (2009). Origin of pain in migraine: evidence for peripheral sensitisation. Lancet Neurol. 8, 679-690. doi: 10.1016/S1474-4422(09)70090-0.
51. Orthmann-Murphy, J. L., Abrams, C. K., and Scherer, S. S. (2007). Gap junctions couple astrocytes and oligodendrocytes. J. Mol. Neurosci. 35, 101-116. doi: 10.1007/s12031-007-9027-5.
52. Parsons, A. A., Bingham, S., Raval, P., Read, S., Thompson, M., and Upton, N. (2001). Tonabersat (SB-220453) a novel benzopyran with anticonvulsivant properties attenuates trigeminal nerve-induced neurovascular reflexes. Br. J. Pharmacol. 132, 1549-1557. doi: 10.1038/sj.bjp.0703932.
53. Peeters, M., Gunthorpe, M. J., Strijbos, P. J. L. M., Goldsmith, P., Upton, N., and James, M. F. (2007). Effects of pan-and subtype-selective N-Methyl-D-aspartate receptor antagonists on cortical spreading depression in the rat: therapeutic potential for migraine. J. Pharmacol. Exp. Ther. 321, 564-572. doi: 10.1124/jpet.106.117101.
54. Peroutka, S. J. (2009). 2008: the year in review. Headache 49, 796-802. doi: 10.1111/j.1526-4610.2009.01422.x.
55. Peters, O., Schipke, C. G., Hashimoto, Y., and Kettenmann, H. (2003). Different mechanisms promote astrocyte Ca2+ waves and spreading depression in mouse neocortex. J. Neurosci. 23, 9888-9896.
56. Rackauskas, M., Neverauskas, V., and Skeberdis, V. A. (2010). Diversity and properties of connexin gap junction channels. Medicina 63, 1-12.
57. Read, S. J., Smith, M. I., Hunter, A. J., Upton, N., and Parsons, A. A. (2000). SB-220453, a potential novel antimigraine agent, inhibits nitric oxide release following induction of cortical spreading depression in the anaesthetized cat. Cephalalgia 20, 92-99. doi: 10.1046/j.1468-2982.2000.00022.x.
58. Rouach, N., Avignone, E., Même, W., Koulakoff, A., Venance, L., Blomstrand, F., et al. (2002). Gap junctions and connexin expression in the normal and pathological central nervous system. Biol. Cell 94, 457-475. doi: 10.1016/S0248-4900(02)00016-3.
59. Sanchez del Rio, M., and Alvarez Linera, J. (2004). Functional neuroimaging of headaches. Lancet Neurol. 3, 645-651. doi: 10.1016/S1474-4422(04)00904-4.
60. Sandilos, J. J., and Bayliss, D. A. (2012). Physiological mechanisms for the modulation of pannexin1 channel activity. J. Physiol. 590, 6257-6266. doi: 10.1113/jphysiol.2012.240911.
61. Sarrouilhe, D., and Dejean, C. (2012). Gap junctional intercellular communication: a new mechanism in pathophysiology of migraine with aura. Therapeutic applications. Pathol. Biol. 60, 392-398. doi: 10.1016/j.patbio.2012.04.002.
62. Scemes, E. (2012). Nature of plasmalemmal functional "hemichannels". Biochim. Biophys. Acta 1818, 1880-1883. doi: 10.1016/j.bbamem.2011.06.005.
63. Scemes, E., and Giaume, C. (2006). Astrocyte calcium waves. Glia 54, 716-725. doi: 10.1002/glia.20374.
64. Silberstein, S. D. (2009). Tonabersat, a novel gap-junction modulator for the prevention of migraine. Cephalalgia 29, 28-35. doi: 10.1111/j.1468-2982.2009.01973.x.
65. Silberstein, S. D., Schoenen, J., Göbel, H., Diener, H. C., Elkind, A. H., Klapper, J. A., et al. (2009). Tonabersat, a gap-junction modulator: efficacy and safety in two randomized, placebo-controled, dose-ranging studies of acute migraine. Cephalalgia 29, 17-27. doi: 10.1111/j.1468-2982.2009.01974.x.
66. Silverman, W. R., de Rivero Vaccari, J. P., Locovei, S., Qiu, F., Carlsson, S. K., Scemes, E., et al. (2009). The pannexin 1 channel activates the inflammasome in neurons and astrocytes. J. Biol. Chem. 284, 18143-18151. doi: 10.1074/jbc.M109.004804.
67. Silverman, W. R., Locovei, S., and Dahl, G. (2008). Probenecid, a gout remedy, inhibits pannexin 1 channels. Am. J. Physiol. Cell Physiol. 295, C761-C767. doi: 10.1152/ajpcell.00227.2008.
68. Smith, M. I., Read, S. J., Chan, W. N., Thompson, M., Hunter, A. J., Upton, N., et al. (2000). Repetitive cortical spreading depression in a gyrencephalic feline brain: inhibition by the novel benzoylamino-benzopyran SB-220453. Cephalalgia 20, 546-553. doi: 10.1046/j.1468-2982.2000.00092.x.
69. Söhl, G., Odermatt, B., Maxeiner, S., Degen, J., and Willecke, K. (2004). New insights into the expression and function of neural connexins with transgenic mouse mutants. Brain Res. Brain Res. Rev. 47, 245-259. doi: 10.1016/j.brainresrev.2004.05.006.
70. Sosinsky, G. E., and Nicholson, B. J. (2005). Structural organization of gap junction channels. Biochim. Biophys. Acta 1711, 99-125. doi: 10.1016/j.bbamem.2005.04.001.
71. Srinivas, M., Hopperstad, M. G., and Spray, D. C. (2001). Quinine blocks specific gap junction channel subtypes. Proc. Natl. Acad. Sci. U.S.A. 98, 10942-10947. doi: 10.1073/pnas.191206198.
72. Stovner, L. J., Zwart, J. A., Hagen, K., Terwindt, G. M., and Pascual, J. (2006). Epidemiology of headache in Europe. Eur. J. Neurol. 12, 333-345. doi: 10.1111/j.1468-1331.2006.01184.x.
73. Thalakoti, S., Patil, V. V., Damodaram, S., Vause, C. V., Langford, L. E., Freeman, S. E., et al. (2007). Neuron-glia signaling in trigeminal ganglion: implications for migraine pathology. Headache 47, 1008-1025. doi: 10.1111/j.1526-4610.2007.00854.x.
74. Tvedskov, J. F., Iversen, H. K., and Olesen, J. A. (2004). Double-blind study of SB-220453 (tonabersat) in the glyceryltrinitrate (GTN) model of migraine. Cephalalgia 24, 875-882. doi: 10.1111/j.1468-2982.2004.00762.x.
75. Vamos, E., Pardutz, A., Fejes, A., Tajti, J., Toldi, J., and Vecsei, L. (2009). Modulatory effects of probenecid on the nitroglycerin-induced changes in the rat caudal trigeminal nucleus. Eur. J. Pharmacol.621, 33-37. doi: 10.1016/j.ejphar.2009.08.034.
76. Wang, H., Cao, Y., Chiang, C.-Y., Dostrovsky, J. O., and Sessle, B. J. (2014). The gap junction blocker carbenoxolone attenuates nociceptive behavior and medullary dorsal horn central sensitization induced by partial infraorbital nerve transection in rats. Pain 155, 429-435. doi: 10.1016/j.pain.2013.11.004.
77. Woods, R. P., Iacoboni, M., and Mazziotta, J. C. (1994). Brief report: bilateral spreading cerebral hypoperfusion during spontaneous migraine headache. N. Engl. J. Med. 331, 1689-1692. doi: 10.1056/NEJM199412223312505.
78. Wu, W., Ye, Q., Wang, W., Yan, L. Y., Wang, Q., Xiao, H., et al. (2012). Amitriptyline calcium currents and intracellular calcium concentration in mouse trigeminal ganglion neurons. Neurosci. Lett. 506, 307-311. doi: 10.1016/j.neulet.2011.11.031.
79. Ye, Z.-C., Wyeth, M. S., Baltan-Tekkok, S., and Ransom, B. R. (2003). Functional hemichannels in astrocytes: a novel mechanism of glutamate release. J. Neurosci. 23, 3588-3596.
80. Yen, M. R., and Saier, M. H. Jr. (2007). Gap junctional proteins of animals: the innexin/pannexin superfamily. Prog. Biophys. Mol. Biol. 94, 5-14. doi: 10.1016/j.pbiomolbio.2007.03.006.
81. Zoidl, G., and Dermietzel, R. (2010). Gap junctions in inherited human disease. Pflugers Arch. 460, 451-466. doi: 10.1007/s00424-010-0789-1.