Pharmacological targeting of spreading depression in migraine

References

• Lipton RB, Stewart WF. The epidemiology of migraine. Eur. Neurol.34(Suppl. 2), 6–11 (1994).
   PubMed Web of Science ®Google Scholar
• Ayata C. Cortical spreading depression triggers migraine attack: pro. Headache50(4), 725–730 (2010).
   PubMed Web of Science ®Google Scholar
• Hadjikhani N, Sanchez Del Rio M, Wu O et al. Mechanisms of migraine aura revealed by functional MRI in human visual cortex. Proc. Natl Acad. Sci. USA98(8), 4687–4692 (2001).
   PubMed Web of Science ®Google Scholar
• Leo L, Gherardini L, Barone V et al. Increased susceptibility to cortical spreading depression in the mouse model of familial hemiplegic migraine type 2. PLoS Genet.7(6), e1002129 (2011).
   Google Scholar
• Eikermann-Haerter K, Dilekoz E, Kudo C et al. Genetic and hormonal factors modulate spreading depression and transient hemiparesis in mouse models of familial hemiplegic migraine type 1. J. Clin. Invest.119(1), 99–109 (2009).
   PubMed Web of Science ®Google Scholar
• Eikermann-Haerter K, Yuzawa I, Dilekoz E, Joutel A, Moskowitz MA, Ayata C. Cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy syndrome mutations increase susceptibility to spreading depression. Ann. Neurol.69(2), 413–418 (2011).
   PubMed Web of Science ®Google Scholar
• Zhang X, Levy D, Kainz V, Noseda R, Jakubowski M, Burstein R. Activation of central trigeminovascular neurons by cortical spreading depression. Ann. Neurol.69(5), 855–865 (2011).
   PubMed Web of Science ®Google Scholar
• Zhang X, Levy D, Noseda R, Kainz V, Jakubowski M, Burstein R. Activation of meningeal nociceptors by cortical spreading depression: implications for migraine with aura. J. Neurosci.30(26), 8807–8814 (2010).
   PubMed Web of Science ®Google Scholar
• 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.8(2), 136–142 (2002).
   PubMed Web of Science ®Google Scholar
• Ayata C, Jin H, Kudo C, Dalkara T, Moskowitz MA. Suppression of cortical spreading depression in migraine prophylaxis. Ann. Neurol.59(4), 652–661 (2006).
   PubMed Web of Science ®Google Scholar
• Leao AAP. Spreading depression of activity in cerebral cortex. J. Neurophysiol.7, 359–390 (1944).
   Google Scholar
• Strong AJ. Detecting and characterizing spreading depression in the injured human brain. J. Cereb. Blood Flow Metab.23(1), 748 (2003).
   PubMed Web of Science ®Google Scholar
• Strong AJ, Fabricius M, Boutelle MG et al. Spreading and synchronous depressions of cortical activity in acutely injured human brain. Stroke33(12), 2738–2743 (2002).
   PubMed Web of Science ®Google Scholar
• Fabricius M, Fuhr S, Bhatia R et al. Cortical spreading depression and peri-infarct depolarization in acutely injured human cerebral cortex. Brain129(Pt 3), 778–790 (2006).
   PubMed Web of Science ®Google Scholar
• Mayevsky A, Doron A, Manor T, Meilin S, Zarchin N, Ouaknine GE. Cortical spreading depression recorded from the human brain using a multiparametric monitoring system. Brain Res.740(1–2), 268–274 (1996).
   PubMed Web of Science ®Google Scholar
• Ayata C. Spreading depression: from serendipity to targeted therapy in migraine prophylaxis. Cephalalgia29(10), 1095–1114 (2009).
   PubMed Web of Science ®Google Scholar
• Kaube H, Goadsby PJ. Anti-migraine compounds fail to modulate the propagation of cortical spreading depression in the cat. Eur. Neurol.34(1), 30–35 (1994).
   PubMed Web of Science ®Google Scholar
• Bogdanov VB, Multon S, Chauvel V et al. Migraine preventive drugs differentially affect cortical spreading depression in rat. Neurobiol. Dis.41(2), 430–435 (2011).
   PubMed Web of Science ®Google Scholar
• Hoffmann U, Dilekoz E, Kudo C, Ayata C. Oxcarbazepine does not suppress cortical spreading depression. Cephalalgia31(5), 537–542 (2011).
   PubMed Web of Science ®Google Scholar
• Hoffmann U, Dilekoz E, Kudo C, Ayata C. Gabapentin suppresses cortical spreading depression susceptibility. J. Cereb. Blood Flow Metab.30(9), 1588–1592 (2010).
   PubMed Web of Science ®Google Scholar
• Akerman S, Goadsby PJ. Topiramate inhibits cortical spreading depression in rat and cat: impact in migraine aura. Neuroreport16(12), 1383–1387 (2005).
   PubMed Web of Science ®Google Scholar
• Read SJ, Smith MI, Hunter AJ, Upton N, Parsons AA. SB-220453, a potential novel antimigraine agent, inhibits nitric oxide release following induction of cortical spreading depression in the anaesthetized cat. Cephalalgia20(2), 92–99 (2000).
   PubMedGoogle Scholar
• Smith MI, Read SJ, Chan WN et al. Repetitive cortical spreading depression in a gyrencephalic feline brain: inhibition by the novel benzoylamino-benzopyran SB-220453. Cephalalgia20(6), 546–553 (2000).
   PubMed Web of Science ®Google Scholar
• Bradley DP, Smith MI, Netsiri C et al. Diffusion-weighted MRI used to detect in vivo modulation of cortical spreading depression: comparison of sumatriptan and tonabersat. Exp. Neurol.172(2), 342–353 (2001).
   PubMed Web of Science ®Google Scholar
• Read SJ, Hirst WD, Upton N, Parsons AA. Cortical spreading depression produces increased cGMP levels in cortex and brain stem that is inhibited by tonabersat (SB-220453) but not sumatriptan. Brain Res.891(1–2), 69–77 (2001).
   PubMed Web of Science ®Google Scholar
• Marrannes R, Wauquier A, Reid K, De Prins E. Effects of drugs on cortical spreading depression. In: The Prelude to The Migraine Attack. Baillière Tindall, Oxford, UK, 158–173 (1986).
   Google Scholar
• Hansen A, Lauritzen M, Tfelt-Hansen P. Spreading cortical depression and antimigraine drugs. In: The Pharmacological Basis of Migraine Therapy. Amery WK, Van Nueten JM, Waquier A (Eds). Putman, London, UK, 161–170 (1984).
   Google Scholar
• Reid KH, Marrannes R, Wauquier A. Effects of flunarizine on rat cerebral cortex. Drug Development Research10, 107–116 (1987).
   Google Scholar
• Wauquier A, Ashton D, Marrannes R. The effects of flunarizine in experimental models related to the pathogenesis of migraine. Cephalalgia5(Suppl. 2), 119–123 (1985).
   PubMedGoogle Scholar
• Marrannes R, De Prins E, Fransen J, Clincke G. Neuropharmacology of spreading depression. In: Migraine: Basic Mechanisms and Treatment. Lehmenkuhler A, Grotemeyer KH, Tegtmeier F (Eds). Urban & Schwarzenberg, MD, USA 431–443 (1993).
   Google Scholar
• dos Santos AA, Pinheiro PC, de Lima DS et al. Fluoxetine inhibits cortical spreading depression in weaned and adult rats suckled under favorable and unfavorable lactation conditions. Exp. Neurol.200(2), 275–282 (2006).
   PubMed Web of Science ®Google Scholar
• Guedes RC, Amancio-Dos-Santos A, Manhaes-De-Castro R, Costa-Cruz RR. Citalopram has an antagonistic action on cortical spreading depression in well-nourished and early-malnourished adult rats. Nutr. Neurosci.5(2), 115–123 (2002).
   PubMed Web of Science ®Google Scholar
• Read SJ, Parsons AA. Sumatriptan modifies cortical free radical release during cortical spreading depression. A novel antimigraine action for sumatriptan? Brain Res.870(1–2), 44–53 (2000).
   PubMed Web of Science ®Google Scholar
• Moskowitz MA, Nozaki K, Kraig RP. Neocortical spreading depression provokes the expression of c-fos protein-like immunoreactivity within trigeminal nucleus caudalis via trigeminovascular mechanisms. J. Neurosci.13(3), 1167–1177 (1993).
   PubMed Web of Science ®Google Scholar
• Mulleners WM, Chronicle EP. Anticonvulsants in migraine prophylaxis: a Cochrane review. Cephalalgia28(6), 585–597 (2008).
   PubMed Web of Science ®Google Scholar
• Silberstein SD, Neto W, Schmitt J, Jacobs D. Topiramate in migraine prevention: results of a large controlled trial. Arch. Neurol.61(4), 490–495 (2004).
   PubMed Web of Science ®Google Scholar
• Silberstein SD, Collins SD. Safety of divalproex sodium in migraine prophylaxis: an open-label, long-term study. Long-term Safety of Depakote in Headache Prophylaxis Study Group. Headache39(9), 633–643 (1999).
   PubMedGoogle Scholar
• Taylor CP. Mechanisms of analgesia by gabapentin and pregabalin – calcium channel alpha2-delta [Cavalpha2-delta] ligands. Pain142(1–2), 13–16 (2009).
   PubMed Web of Science ®Google Scholar
• Eikermann-Haerter K, Yuzawa I, Qin T et al. Enhanced subcortical spreading depression in familial hemiplegic migraine type 1 mutant mice. J. Neurosci.31(15), 5755–5763 (2011).
   PubMed Web of Science ®Google Scholar
• Silberstein SD, Schoenen J, Gobel H et al. Tonabersat, a gap-junction modulator: efficacy and safety in two randomized, placebo-controlled, dose-ranging studies of acute migraine. Cephalalgia29(Suppl. 2), 17–27 (2009).
   PubMedGoogle Scholar
• Dahlof CG, Hauge AW, Olesen J. Efficacy and safety of tonabersat, a gap-junction modulator, in the acute treatment of migraine: a double-blind, parallel-group, randomized study. Cephalalgia29(Suppl. 2), 7–16 (2009).
   PubMed Web of Science ®Google Scholar
• Goadsby PJ, Ferrari MD, Csanyi A, Olesen J, Mills JG. Randomized, double-blind, placebo-controlled, proof-of-concept study of the cortical spreading depression inhibiting agent tonabersat in migraine prophylaxis. Cephalalgia29(7), 742–750 (2009).
   PubMedGoogle Scholar
• Hauge AW, Asghar MS, Schytz HW, Christensen K, Olesen J. Effects of tonabersat on migraine with aura: a randomised, double-blind, placebo-controlled crossover study. Lancet Neurol.8(8), 718–723 (2009).
   PubMed Web of Science ®Google Scholar
• D’Andrea G, Granella F, Cadaldini M, Manzoni GC. Effectiveness of lamotrigine in the prophylaxis of migraine with aura: an open pilot study. Cephalalgia19(1), 64–66 (1999).
   PubMed Web of Science ®Google Scholar
• Lampl C, Katsarava Z, Diener HC, Limmroth V. Lamotrigine reduces migraine aura and migraine attacks in patients with migraine with aura. J. Neurol. Neurosurg. Psychiatry76(12), 1730–1732 (2005).
   PubMed Web of Science ®Google Scholar
• Steiner TJ, Findley LJ, Yuen AW. Lamotrigine versus placebo in the prophylaxis of migraine with and without aura. Cephalalgia17(2), 109–112 (1997).
   PubMed Web of Science ®Google Scholar
• Gupta P, Singh S, Goyal V, Shukla G, Behari M. Low-dose topiramate versus lamotrigine in migraine prophylaxis (the Lotolamp study). Headache47(3), 402–412 (2007).
   PubMed Web of Science ®Google Scholar
• Kelley NE, Tepper DE. Rescue Therapy for acute migraine, part 1: triptans, dihydroergotamine, and magnesium. Headache52(1), 114–128 (2012).
   PubMedGoogle Scholar
• Mauskop A, Altura BM. Role of magnesium in the pathogenesis and treatment of migraines. Clin. Neurosci.5(1), 24–27 (1998).
   PubMedGoogle Scholar
• Ramadan NM, Halvorson H, Vande-Linde A, Levine SR, Helpern JA, Welch KM. Low brain magnesium in migraine. Headache29(9), 590–593 (1989).
   PubMed Web of Science ®Google Scholar
• van der Hel WS, van den Bergh WM, Nicolay K, Tulleken KA, Dijkhuizen RM. Suppression of cortical spreading depressions after magnesium treatment in the rat. Neuroreport9(10), 2179–2182 (1998).
   PubMed Web of Science ®Google Scholar
• Silberstein S, Saper J, Berenson F, Somogyi M, McCague K, D’Souza J. Oxcarbazepine in migraine headache: a double-blind, randomized, placebo-controlled study. Neurology70(7), 548–555 (2008).
   PubMed Web of Science ®Google Scholar
• Taylor FR. Nutraceuticals and headache: the biological basis. Headache51(3), 484–501 (2011).
   PubMed Web of Science ®Google Scholar
• Bruijn J, Duivenvoorden H, Passchier J, Locher H, Dijkstra N, Arts WF. Medium-dose riboflavin as a prophylactic agent in children with migraine: a preliminary placebo-controlled, randomised, double-blind, cross-over trial. Cephalalgia30(12), 1426–1434 (2010).
   PubMed Web of Science ®Google Scholar
• Schoenen J, Jacquy J, Lenaerts M. Effectiveness of high-dose riboflavin in migraine prophylaxis. A randomized controlled trial. Neurology50(2), 466–470 (1998).
   PubMed Web of Science ®Google Scholar
• Boehnke C, Reuter U, Flach U, Schuh-Hofer S, Einhaupl KM, Arnold G. High-dose riboflavin treatment is efficacious in migraine prophylaxis: an open study in a tertiary care centre. Eur. J. Neurol.11(7), 475–477 (2004).
   PubMed Web of Science ®Google Scholar
• Kaube H, Herzog J, Kaufer T, Dichgans M, Diener HC. Aura in some patients with familial hemiplegic migraine can be stopped by intranasal ketamine. Neurology55(1), 139–141 (2000).
   PubMed Web of Science ®Google Scholar
• Goldstein M, Chen TC. The epidemiology of disabling headache. Adv. Neurol.33, 377–390 (1982).
   PubMedGoogle Scholar
• Waters WE, O’Connor PJ. Epidemiology of headache and migraine in women. J. Neurol. Neurosurg. Psychiatry34(2), 148–153 (1971).
   PubMed Web of Science ®Google Scholar
• Eriksen MK, Thomsen LL, Olesen J. Implications of clinical subtypes of migraine with aura. Headache46(2), 286–297 (2006).
   PubMed Web of Science ®Google Scholar
• Smith SS. Estrogen administration increases neuronal responses to excitatory amino acids as a long-term effect. Brain Res.503(2), 354–357 (1989).
   PubMed Web of Science ®Google Scholar
• Sato K, Matsuki N, Ohno Y, Nakazawa K. Estrogens inhibit L-glutamate uptake activity of astrocytes via membrane estrogen receptor alpha. J. Neurochem.86(6), 1498–1505 (2003).
   PubMedGoogle Scholar
• Woolley CS, Weiland NG, McEwen BS, Schwartzkroin PA. Estradiol increases the sensitivity of hippocampal CA1 pyramidal cells to NMDA receptor-mediated synaptic input: correlation with dendritic spine density. J. Neurosci.17(5), 1848–1859 (1997).
   PubMed Web of Science ®Google Scholar
• Nagel-Leiby S, Welch KM, Grunfeld S, D’Andrea G. Ovarian steroid levels in migraine with and without aura. Cephalalgia10(3), 147–152 (1990).
   PubMedGoogle Scholar
• MacGregor EA. Oestrogen and attacks of migraine with and without aura. Lancet Neurol.3(6), 354–361 (2004).
   PubMed Web of Science ®Google Scholar
• Ertresvag JM, Zwart JA, Helde G, Johnsen HJ, Bovim G. Headache and transient focal neurological symptoms during pregnancy, a prospective cohort. Acta Neurol. Scand.111(4), 233–237 (2005).
   PubMedGoogle Scholar
• Granella F, Sances G, Zanferrari C, Costa A, Martignoni E, Manzoni GC. Migraine without aura and reproductive life events: a clinical epidemiological study in 1300 women. Headache33(7), 385–389 (1993).
   PubMed Web of Science ®Google Scholar
• Smith MJ, Adams LF, Schmidt PJ, Rubinow DR, Wassermann EM. Effects of ovarian hormones on human cortical excitability. Ann. Neurol.51(5), 599–603 (2002).
   PubMed Web of Science ®Google Scholar
• Fettes I. Migraine in the menopause. Neurology53(4 Suppl. 1), S29–S33 (1999).
   Google Scholar
• Thomsen LL, Eriksen MK, Roemer SF, Andersen I, Olesen J, Russell MB. A population-based study of familial hemiplegic migraine suggests revised diagnostic criteria. Brain125(Pt 6), 1379–1391 (2002).
   PubMed Web of Science ®Google Scholar
• Lichten EML, Whitty J, Peiper AD. The use of leuprolide acetate in the diagnosis and treatment of menstrual migraine: the role of artificially induced menopause. Headache6, 313–317 (1995).
   Google Scholar
• Murray SC, Muse KN. Effective treatment of severe menstrual migraine headaches with gonadotropin-releasing hormone agonist and ‘add-back’ therapy. Fertil. Steril.67(2), 390–393 (1997).
   PubMed Web of Science ®Google Scholar
• Sood SV. Hemiplegic migraine associated with menstruation. J. Obstet. Gynaecol. Br. Commonw.78(8), 762–763 (1971).
   PubMedGoogle Scholar
• Martin VT, Behbehani M. Ovarian hormones and migraine headache: understanding mechanisms and pathogenesis – part 2. Headache46(3), 365–386 (2006).
   PubMed Web of Science ®Google Scholar
• Twyman RE, Macdonald RL. Neurosteroid regulation of GABAA receptor single-channel kinetic properties of mouse spinal cord neurons in culture. J. Physiol.456, 215–245 (1992).
   PubMed Web of Science ®Google Scholar
• Stewart WF, Lipton RB, Chee E, Sawyer J, Silberstein SD. Menstrual cycle and headache in a population sample of migraineurs. Neurology55(10), 1517–1523 (2000).
   PubMed Web of Science ®Google Scholar
• Eikermann-Haerter K, Baum MJ, Ferrari MD, van den Maagdenberg AM, Moskowitz MA, Ayata C. Androgenic suppression of spreading depression in familial hemiplegic migraine type 1 mutant mice. Ann. Neurol.66(4), 564–568 (2009).
   PubMed Web of Science ®Google Scholar
• Moehlig RC. Methyl testosterone for migraine of women; report of sixty cases. J. Mich. State Med. Soc.54(5), 577–579 (1955).
   PubMedGoogle Scholar
• Calton GJ, Burnett JW. Danazol and migraine. N. Engl. J. Med.310(11), 721–722 (1984).
   PubMedGoogle Scholar
• Jonsson B, Von Reis G, Sahlgren E. [Testosterone therapy of headache]. Acta Psychiatr. Neurol. Scand.74, 102–105 (1951).
   Google Scholar
• Lichten EM, Bennett RS, Whitty AJ, Daoud Y. Efficacy of danazol in the control of hormonal migraine. J. Reprod. Med.36(6), 419–424 (1991).
   PubMed Web of Science ®Google Scholar
• Vincent FM. Migraine responsive to danazol. Neurology35(4), 618 (1985).
   PubMedGoogle Scholar
• Arango O, Bielsa O, Pascual-Calvet J, Herrero M, Gelabert-Mas A. [Disappearance of migraine crises in two patients with male infertility treated with human chorionic gonadotropin/human menopausal gonadotrophin]. Rev. Neurol.24(132), 977–979 (1996).
   PubMedGoogle Scholar
• Pringsheim T, Gooren L. Migraine prevalence in male to female transsexuals on hormone therapy. Neurology63(3), 593–594 (2004).
   PubMed Web of Science ®Google Scholar
• Nudler SI, Pagani MR, Urbano FJ, McEnery MW, Uchitel OD. Testosterone modulates Ca(v2.2) calcium channels’ functional expression at rat levator ani neuromuscular junction. Neuroscience134(3), 817–826 (2005).
   PubMedGoogle Scholar
• Kitahara Y, Taga K, Abe H, Shimoji K. The effects of anesthetics on cortical spreading depression elicitation and c-fos expression in rats. J. Neurosurg. Anesthesiol.13(1), 26–32 (2001).
   PubMedGoogle Scholar
• Kudo C, Nozari A, Moskowitz MA, Ayata C. The impact of anesthetics and hyperoxia on cortical spreading depression. Exp. Neurol.212(1), 201–206 (2008).
   PubMed Web of Science ®Google Scholar
• Triner WR, Bartfield JM, Birdwell M, Raccio-Robak N. Nitrous oxide for the treatment of acute migraine headache. Am. J. Emerg. Med.17(3), 252–254 (1999).
   PubMed Web of Science ®Google Scholar
• Loder E. Design considerations in migraine with aura trials: learning from experience. Cephalalgia30(9), 1027–1028 (2011).
   Google Scholar
• Welch KM, D’Andrea G, Tepley N, Barkley G, Ramadan NM. The concept of migraine as a state of central neuronal hyperexcitability. Neurol. Clin.8(4), 817–828 (1990).
   PubMed Web of Science ®Google Scholar
• Coppola G, Schoenen J. Cortical Excitability in Chronic Migraine. Curr. Pain Headache Rep.16(1), 93–100 (2012).
   PubMed Web of Science ®Google Scholar
• Lauritzen M, Dreier JP, Fabricius M, Hartings JA, Graf R, Strong AJ. Clinical relevance of cortical spreading depression in neurological disorders: migraine, malignant stroke, subarachnoid and intracranial hemorrhage, and traumatic brain injury. J. Cereb. Blood Flow Metab.31(1), 17–35 (2010).
   PubMedGoogle Scholar
• Strong AJ, Hartings JA, Dreier JP. Cortical spreading depression: an adverse but treatable factor in intensive care? Curr. Opin. Crit. Care.13(2), 126–133 (2007).
   PubMed Web of Science ®Google Scholar
• Eikermann-Haerter K, Hyun Lee J, Yuzawa I et al. Migraine mutations increase stroke vulnerability by facilitating ischemic depolarizations. Circulation125(2), 335–345 (2012).
   PubMedGoogle Scholar