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Effect of carbamazepine on tetrodotoxin-resistant Na+ channels in trigeminal ganglion neurons innervating to the dura

  • Han, Jin-Eon (Department of Pharmacology, School of Dentistry, Kyungpook National University) ;
  • Cho, Jin-Hwa (Department of Pharmacology, School of Dentistry, Kyungpook National University) ;
  • Nakamura, Michiko (Department of Pharmacology, School of Dentistry, Kyungpook National University) ;
  • Lee, Maan-Gee (Brain Science & Engineering Institute, Kyungpook National University) ;
  • Jang, Il-Sung (Department of Pharmacology, School of Dentistry, Kyungpook National University)
  • Received : 2018.03.27
  • Accepted : 2018.09.12
  • Published : 2018.11.01

Abstract

Migraine is a neurological disorder characterized by recurrent and disabling severe headaches. Although several anticonvulsant drugs that block voltagedependent $Na^+$ channels are widely used for migraine, far less is known about the therapeutic actions of carbamazepine on migraine. In the present study, therefore, we characterized the effects of carbamazepine on tetrodotoxin-resistant (TTX-R) $Na^+$ channels in acutely isolated rat dural afferent neurons, which were identified by the fluorescent dye DiI. The TTX-R $Na^+$ currents were measured in medium-sized DiIpositive neurons using the whole-cell patch clamp technique in the voltage-clamp mode. While carbamazepine had little effect on the peak amplitude of transient $Na^+$ currents, it strongly inhibited steady-state currents of transient as well as persistent $Na^+$ currents in a concentration-dependent manner. Carbamazepine had only minor effects on the voltage-activation relationship, the voltage-inactivation relationship, and the use-dependent inhibition of TTX-R $Na^+$ channels. However, carbamazepine changed the inactivation kinetics of TTX-R $Na^+$ channels, significantly accelerating the development of inactivation and delaying the recovery from inactivation. In the current-clamp mode, carbamazepine decreased the number of action potentials without changing the action potential threshold. Given that the sensitization of dural afferent neurons by inflammatory mediators triggers acute migraine headaches and that inflammatory mediators potentiate TTX-R $Na^+$ currents, the present results suggest that carbamazepine may be useful for the treatment of migraine headaches.

Keywords

References

  1. Goadsby PJ. Recent advances in understanding migraine mechanisms, molecules and therapeutics. Trends Mol Med. 2007;13:39-44. https://doi.org/10.1016/j.molmed.2006.11.005
  2. Diener HC, Dodick DW, Goadsby PJ, Lipton RB, Olesen J, Silberstein SD. Chronic migraine--classification, characteristics and treatment. Nat Rev Neurol. 2012;8:162-171. https://doi.org/10.1038/nrneurol.2012.13
  3. Ferrari MD. The economic burden of migraine to society. Pharmacoeconomics. 1998;13:667-676. https://doi.org/10.2165/00019053-199813060-00003
  4. Michel P, Dartigues JF, Lindoulsi A, Henry P. Loss of productivity and quality of life in migraine sufferers among French workers: results from the GAZEL cohort. Headache. 1997;37:71-78. https://doi.org/10.1046/j.1526-4610.1997.3702071.x
  5. Evers S, Afra J, Frese A, Goadsby PJ, Linde M, May A, Sandor PS. EFNS guideline on the drug treatment of migraine--revised report of an EFNS task force. Eur J Neurol. 2009;16:968-981. https://doi.org/10.1111/j.1468-1331.2009.02748.x
  6. Malik SN, Hopkins M, Young WB, Silberstein SD. Acute migraine treatment: patterns of use and satisfaction in a clinical population. Headache. 2006;46:773-780. https://doi.org/10.1111/j.1526-4610.2006.00437.x
  7. Silberstein SD, Marmura MJ. Acute migraine treatment. Headache. 2015;55:1-2.
  8. Silberstein SD, Goadsby PJ. Migraine: preventive treatment. Cephalalgia. 2002;22:491-512. https://doi.org/10.1046/j.1468-2982.2002.00386.x
  9. Silberstein SD. Preventive treatment of migraine. Trends Pharmacol Sci. 2006;27:410-415. https://doi.org/10.1016/j.tips.2006.06.003
  10. Sidhu HS, Sadhotra A. Current status of the new antiepileptic drugs in chronic pain. Front Pharmacol. 2016;7:276.
  11. Rogawski M. Common pathophysiologic mechanisms in migraine and epilepsy. Arch Neurol. 2008;65:709-714.
  12. Linde M, Mulleners WM, Chronicle EP, McCrory DC. Topiramate for the prophylaxis of episodic migraine in adults. Cochrane Database Syst Rev. 2013;6:CD010610.
  13. Linde M, Mulleners WM, Chronicle EP, McCrory DC. Valproate (valproic acid or sodium valproate or a combination of the two) for the prophylaxis of episodic migraine in adults. Cochrane Database Syst Rev. 2013;6:CD010611.
  14. Rompel H, Bauermeister PW. Aetiology of migraine and prevention with carbamazepine (Tegretol): results of a double-blind, cross-over study. S Afr Med J. 1970;44:75-80.
  15. Steiner TJ, Findley LJ, Yuen AW. Lamotrigine versus placebo in the prophylaxis of migraine with and without aura. Cephalalgia. 1997;17:109-112. https://doi.org/10.1046/j.1468-2982.1997.1702109.x
  16. Silberstein S, Saper J, Berenson F, Somogyi M, McCague K, D'Souza J. Oxcarbazepine in migraine headache: a double-blind, randomized, placebo-controlled study. Neurology. 2008;70:548-555. https://doi.org/10.1212/01.wnl.0000297551.27191.70
  17. Gupta P, Singh S, Goyal V, Shukla G, Behari M. Low-dose topiramate versus lamotrigine in migraine prophylaxis (the Lotolamp study). Headache. 2007;47:402-412.
  18. Tanelian DL, Brose WG. Neuropathic pain can be relieved by drugs that are use-dependent sodium channel blockers: lidocaine, carbamazepine, and mexiletine. Anesthesiology. 1991;74:949-951. https://doi.org/10.1097/00000542-199105000-00026
  19. Baker KA, Taylor JW, Lilly GE. Treatment of trigeminal neuralgia: use of baclofen in combination with carbamazepine. Clin Pharm. 1985;4:93-96.
  20. Sidebottom A, Maxwell S. The medical and surgical management of trigeminal neuralgia. J Clin Pharm Ther. 1995;20:31-35. https://doi.org/10.1111/j.1365-2710.1995.tb00622.x
  21. Backonja MM. Use of anticonvulsants for treatment of neuropathic pain. Neurology. 2002;59(5 Suppl 2):S14-17. https://doi.org/10.1212/WNL.59.5_suppl_2.S14
  22. Rush AM, Elliott JR. Phenytoin and carbamazepine: differential inhibition of sodium currents in small cells from adult rat dorsal root ganglia. Neurosci Lett. 1997;226:95-98. https://doi.org/10.1016/S0304-3940(97)00258-9
  23. Brau ME, Dreimann M, Olschewski A, Vogel W, Hempelmann G. Effect of drugs used for neuropathic pain management on tetrodotoxin-resistant Na+ currents in rat sensory neurons. Anesthesiology. 2001;94:137-144. https://doi.org/10.1097/00000542-200101000-00024
  24. Harriott AM, Gold MS. Electrophysiological properties of dural afferents in the absence and presence of inflammatory mediators. J Neurophysiol. 2009;101:3126-3134. https://doi.org/10.1152/jn.91339.2008
  25. Murase K, Ryu PD, Randic M. Excitatory and inhibitory amino acids and peptide-induced responses in acutely isolated rat spinal dorsal horn neurons. Neurosci Lett. 1989;103:56-63. https://doi.org/10.1016/0304-3940(89)90485-0
  26. Galletti F, Cupini LM, Corbelli I, Calabresi P, Sarchielli P. Pathophysiological basis of migraine prophylaxis. Prog Neurobiol. 2009;89:176-192. https://doi.org/10.1016/j.pneurobio.2009.07.005
  27. Chiossi L, Negro A, Capi M, Lionetto L, Martelletti P. Sodium channel antagonists for the treatment of migraine. Expert Opin Pharmacother. 2014;15:1697-1706. https://doi.org/10.1517/14656566.2014.929665
  28. Lampl C, Katsarava Z, Diener HC, Limmroth V. Lamotrigine reduces migraine aura and migraine attacks in patients with migraine with aura. J Neurol Neurosurg Psychiatry. 2005;76:1730-1732. https://doi.org/10.1136/jnnp.2005.063750
  29. Drake ME Jr, Greathouse NI, Renner JB, Armentbright AD. Openlabel zonisamide for refractory migraine. Clin Neuropharmacol. 2004;27:278-280. https://doi.org/10.1097/01.wnf.0000150866.98887.77
  30. Mohammadianinejad SE, Abbasi V, Sajedi SA, Majdinasab N, Abdollahi F, Hajmanouchehri R, Faraji A. Zonisamide versus topiramate in migraine prophylaxis: a double-blind randomized clinical trial. Clin Neuropharmacol. 2011;34:174-177. https://doi.org/10.1097/WNF.0b013e318225140c
  31. Johannessen CU. Mechanisms of action of valproate: a commentatory. Neurochem Int. 2000;37:103-110. https://doi.org/10.1016/S0197-0186(00)00013-9
  32. Shank RP, Gardocki JF, Streeter AJ, Maryanoff BE. An overview of the preclinical aspects of topiramate: pharmacology, pharmacokinetics, and mechanism of action. Epilepsia. 2000;41 Suppl 1:S3-9.
  33. Schmidt D, Elger CE. What is the evidence that oxcarbazepine and carbamazepine are distinctly different antiepileptic drugs? Epilepsy Behav. 2004;5:627-635. https://doi.org/10.1016/j.yebeh.2004.07.004
  34. Dailey JW, Reith ME, Yan QS, Li MY, Jobe PC. Carbamazepine increases extracellular serotonin concentration: lack of antagonism by tetrodotoxin or zero $Ca^{2+}$. Eur J Pharmacol. 1997;328:153-162. https://doi.org/10.1016/S0014-2999(97)83041-5
  35. Dailey JW, Reith ME, Steidley KR, Milbrandt JC, Jobe PC. Carbamazepine- induced release of serotonin from rat hippocampus in vitro. Epilepsia. 1998;39:1054-1063. https://doi.org/10.1111/j.1528-1157.1998.tb01290.x
  36. Kawata Y, Okada M, Murakami T, Kamata A, Zhu G, Kaneko S. Pharmacological discrimination between effects of carbamazepine on hippocampal basal, $Ca^{2+}$- and $K^{+}$-evoked serotonin release. Br J Pharmacol. 2001;133:557-567. https://doi.org/10.1038/sj.bjp.0704104
  37. Tatsumi M, Groshan K, Blakely RD, Richelson E. Pharmacological profile of antidepressants and related compounds at human monoamine transporters. Eur J Pharmacol. 1997;340:249-258. https://doi.org/10.1016/S0014-2999(97)01393-9
  38. Xu XM, Yang C, Liu Y, Dong MX, Zou DZ, Wei YD. Efficacy and feasibility of antidepressants for the prevention of migraine in adults: a meta-analysis. Eur J Neurol. 2017;24:1022-1031. https://doi.org/10.1111/ene.13320
  39. Silberstein SD. Migraine pathophysiology and its clinical implications. Cephalalgia. 2004;24 Suppl 2:2-7.
  40. Benemei S, Nicoletti P, Capone JG, Geppetti P. CGRP receptors in the control of pain and inflammation. Curr Opin Pharmacol. 2009;9:9-14. https://doi.org/10.1016/j.coph.2008.12.007
  41. Bolay H, Reuter U, Dunn AK, Huang Z, Boas DA, Moskowitz MA. Intrinsic brain activity triggers trigeminal meningeal afferents in a migraine model. Nat Med. 2002;8:136-142. https://doi.org/10.1038/nm0202-136
  42. Gold MS, Reichling DB, Shuster MJ, Levine JD. Hyperalgesic agents increase a tetrodotoxin-resistant Na+ current in nociceptors. Proc Natl Acad Sci USA. 1996;93:1108-1112. https://doi.org/10.1073/pnas.93.3.1108
  43. Gold MS, Levine JD, Correa AM. Modulation of TTX-R INa by PKC and PKA and their role in PGE2-induced sensitization of rat sensory neurons in vitro. J Neurosci. 1998;18:10345-10355. https://doi.org/10.1523/JNEUROSCI.18-24-10345.1998
  44. Nakamura M, Jang IS. Characterization of dural afferent neurons innervating cranial blood vessels within the dura in rats. Brain Res. 2018;1696:91-102. https://doi.org/10.1016/j.brainres.2018.06.007
  45. Schneider H, Stenzel E. [Carbamazepine--daily course in the serum during long term medication]. Bibl Psychiatr. 1975;(151):32-42.
  46. Bertilsson L. Clinical pharmacokinetics of carbamazepine. Clin Pharmacokinet. 1978;3:128-143. https://doi.org/10.2165/00003088-197803020-00003
  47. Taverna S, Mantegazza M, Franceschetti S, Avanzini G. Valproate selectively reduces the persistent fraction of Na+ current in neocortical neurons. Epilepsy Res. 1998;32:304-308. https://doi.org/10.1016/S0920-1211(98)00060-6
  48. Taverna S, Sancini G, Mantegazza M, Franceschetti S, Avanzini G. Inhibition of transient and persistent Na+ current fractions by the new anticonvulsant topiramate. J Pharmacol Exp Ther. 1999;288:960-968.
  49. Stafstrom CE. Persistent sodium current and its role in epilepsy. Epilepsy Curr. 2007;7:15-22. https://doi.org/10.1111/j.1535-7511.2007.00156.x
  50. Hains BC, Waxman SG. Sodium channel expression and the molecular pathophysiology of pain after SCI. Prog Brain Res. 2007;161:195-203.
  51. Hur YK, Choi IS, Cho JH, Park EJ, Choi JK, Choi BJ, Jang IS. Effects of carbamazepine and amitriptyline on tetrodotoxinresistant Na+ channels in immature rat trigeminal ganglion neurons. Arch Pharm Res. 2008;31:178-182. https://doi.org/10.1007/s12272-001-1138-x
  52. Willow M, Gonoi T, Catteral W. Voltage clamp analysis of the inhibitory actions of diphenyihydantoin and carbamazepine on voltagesensitive sodium channels in neuroblastoma cells. J Mol Pharmacol. 1985;27:549-558.
  53. Singh JN, Jain G, Ramarao P, Sharma SS. Inhibition of sodium current by carbamazepine in dorsal root ganglion neurons in vitro. Indian J Physiol Pharmacol. 2009;53:147-154.
  54. Crill WE. Persistent sodium current in mammalian central neurons. Annu Rev Physiol. 1996;58:349-362. https://doi.org/10.1146/annurev.ph.58.030196.002025
  55. Bennett BD, Callaway JC, Wilson CJ. Intrinsic membrane properties underlying spontaneous tonic firing in neostriatal cholinergic interneurons. J Neurosci. 2000;20:8493-8503. https://doi.org/10.1523/JNEUROSCI.20-22-08493.2000
  56. Taddese A, Bean BP. Subthreshold sodium current from rapidly inactivating sodium channels drives spontaneous firing of tuberomammillary neurons. Neuron. 2002;33:587-600. https://doi.org/10.1016/S0896-6273(02)00574-3
  57. Jackson AC, Yao GL, Bean BP. Mechanism of spontaneous firing in dorsomedial suprachiasmatic nucleus neurons. J Neurosci. 2004;24:7985-7998. https://doi.org/10.1523/JNEUROSCI.2146-04.2004
  58. Pape HC. Queer current and pacemaker: the hyperpolarizationactivated cation current in neurons. Annu Rev Physiol. 1996;58:299-327. https://doi.org/10.1146/annurev.ph.58.030196.001503