Targeting to 5-HT1F receptor subtype for migraine treatment: Lessons from the past, implications for the future

Central Nervous System Agents in Medicinal Chemistry

Volumn 12, Issue 4, 2012, Pages 241-249

  Mitsikostas, Dimos D ^a   Tfelt Hansen, Peer ^b  

^a ATHENS NAVAL HOSPITAL   (Greece)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Lasmiditan; Migraine; Serotonine; Serotonine 1F receptors

Indexed keywords

5 (4 FLUOROBENZAMIDO) 3 (1 METHYL 4 PIPERIDINYL) 1H INDOLE FUMARATE; LASMIDITAN; N (3 DIMETHYLAMINO 2, 3, 4, 9 TETRAHYDRO 1H CARBAZOL 6 YL) 4 FLUOROBENZAMIDE; N (3 DIMETHYLAMINO 2,3,4,9 TETRAHYDRO 1H CARBAZOL 6 YL) 4 FLUOROBENZAMIDE; PLACEBO; PROTEIN C FOS; SEROTONIN; SEROTONIN 1B RECEPTOR; SEROTONIN 1D RECEPTOR; SEROTONIN 1F RECEPTOR; SUMATRIPTAN; UNCLASSIFIED DRUG;

ASTHENIA; DIZZINESS; DRUG DOSE COMPARISON; DRUG EFFICACY; DRUG SAFETY; FATIGUE; HUMAN; MIGRAINE; NAUSEA; NEUROTRANSMISSION; NOCICEPTION; NONHUMAN; PARESTHESIA; PHASE 1 CLINICAL TRIAL (TOPIC); RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; SOMNOLENCE; TREATMENT OUTCOME; TREATMENT RESPONSE; TRIGEMINAL NUCLEUS; TRIGEMINUS GANGLION; VERTIGO;

EID: 84870201174     PISSN: 18715249     EISSN: 18756166     Source Type: Journal    
DOI: 10.2174/187152412803760627     Document Type: Review

References (69)

1. Stovner, L., Hagen, K., Jensen, R., Katsarava, Z., Lipton, R., Scher, A., Steiner, T., Zwart, J.A. The global burden of headache: a documentation of headache prevalence and disability worldwide. Cephalalgia, 2007, 27, 193-210.
2. Rasmussen, B.K., Olesen, J. Migraine with aura and migraine without aura: an epidemiological study. Cephalalgia, 1992,12, 221-228.
3. Bigal, M.E., Serrano, D., Reed, M., Lipton, R.B. Chronic migraine in the population: burden, diagnosis, and satisfaction with treatment. Neurology, 2008,71,559-566.
4. WHO. The world health report 2001-mental health: new understanding, new hope (revised edition). Geneva: World Health Organization, 2002, 19-45.
5. Andlin-Sobocki, P., Jonsson, B., Wittchen, H.U., Olesen, J. Cost of disorders of the brain in Europe. Eur. J. Neurol., 2005, 12 (suppl 1) CNSAMC 12-4 Board Page Required 1-27.
6. Stewart, W.F., Ricci, J.A., Chee, E., Morganstein, D., Lipton, R. Lost productive time and cost due to common pain conditions in the US workforce. JAMA, 2003, 290, 2443-2454.
7. Moskowitz, M.A., Reinhard, J.F. Jr, Romero, J., Melamed, E., Pettibone, D.J. Neurotransmitters and the fifth cranial nerve: is there a relation to the headache phase of migraine? Lancet, 1979, 2, 883-885.
8. Mayberg, M., Langer, R.S., Zervas, N.T., Moskowitz, M.A. Perivascular meningeal projections from cat trigeminal ganglia: possible pathway for vascular headaches in man. Science, 1981, 213, 228-230.
9. Olesen, J., Goadsby, P.J. Synthesis of migraine mechanisms. In: Olesen, J., Goadsby, P.J., Ramadan, N.M., Tfelt-Hansen, P., Welch, K.M.A, eds. The Headaches. 3rd Ed. Philadelphia: Lippincott Williams & Wilkins 2006, 393-398.
10. Burstein, R., Strassman, A., Moskowitz, M. Can cortical spreading depression activate central trigeminovascular neurons without peripheral input? Pitfalls of a new concept. Cephalalgia, 2012, 32(6), 509-511.
11. Goadsby, P.J., Akerman, S. The trigeminovascular system does not require a peripheral sensory input to be activated--migraine is a central disorder. Focus on 'Effect of cortical spreading depression on basal and evoked traffic in the trigeminovascular sensory system'. Cephalalgia, 2012, 32, 3-5.
12. Olesen, J., Burstein, R., Ashina, M., Tfelt-Hansen, P. Origin of pain (nociception) in migraine. Lancet Neurol., 2009, 8, 679-690.
13. Saxena, P.R., Tfelt-Hansen, P. Triptans, 5HT1B/1D agonists in the acute treatment of migraine. In: Olesen J, Goadsby PJ, Ramadan NM, Tfelt-Hansen P, Welch KMA, eds. The Headaches. 3rd Ed. Philadelphia: Lippincott Williams & Wilkins 2006, 469-503.
14. Tfelt-Hansen, P., De Vries, P., Saxena, P.R. Triptans in migraine. A comparative review of pharmacology, pharmacokinetics and efficacy. Drugs, 2000, 60, 1259-1287.
15. Tfelt-Hansen, P., Olesen, J. Taking the negative view of current migraine treatments: the unmet needs. CNS Drugs, 2012, 26,375-382.
16. Tfelt-Hansen, P. Clinical pharmacology of current and future drugs for the acute treatment of migraine: a review and an update. Curr. Clin. Pharmacol., 2012, 7, 66-72.
17. Ferrari, A., Tiraferri, I., Neri, L., Sternieri, E. Why pharmacokinetic differences among oral triptans have little clinical importance: a comment. J. Headache Pain, 2011, 12, 5-12.
18. Tfelt-Hansen, P., Koehler, P.J. One Hundred years of migraine research: major clinical and scientific observations from 1910 to 2010. Headache, 2011, 51, 752-778.
19. Sicuteri, F., Michelacci, S., Franchi, G. Antagonism between an antiserotonin-the butanolamide of 1-methyl-lysergic acid--and the effects of a histamine-liberating substance 48/80 B. W. in man. Int. Arch. Allergy Appl. Immunol.,1959, 15, 291-299.
20. Lance, J.W. 5-Hydroxytryptamine and its role in migraine. Eur. Neurol., 1991, 31, 279-281.
21. Saxena, P.R., Ferrari, M.D. From serotonin receptor classification to the antimigraine drug sumatriptan. Cephalalgia, 1992, 12, 187-196.
22. Ferrari, M.D., Odink, J., Frölich, M., Tapparelli, C., Portielje, J.E. Release of platelet Met-enkephalin, but not serotonin, in migraine. A platelet response unique to migraine patients? J. Neurol. Sci., 1989, 93, 51-60.
23. Saxena, P.R., Verdouw, P.D. Effects of methysergide and 5-hydroxytryptamine on carotid blood flow distribution in pigs: further evidence for the presence of atypical 5-HT receptors. Br. J. Pharmacol., 1984, 82, 817-826.
24. Humphrey, P.P.A., Apperley, E., Feniuk, W., Perren, M.J. A rational approach to identifying a fundamentally new drug for the treatment of migraine. In: Saxena P.R., Wallis, D.I., Wouters, W., Bevan, P, eds. Cardiovascular pharmacology of 5hydroxytryptamine: prospective therapeutic applications. Dordrecht: Kluwer Academic, 1990, 416-431.
25. Humphrey, P.P.A., Feniuk, W. Mode of action of the antimigraine drug sumatriptan. Trends Pharmacol. Sci., 1991, 12, 444-446.
26. Phebus, L.A., Johnson, K.W., Zgombick, J.M., Gilbert, P.J., Van Belle, K., Mancuso, V., Nelson, D.L., Calligaro, D.O., Kiefer, A.D. Jr., Branchek, T.A., Flaugh, M.E. Characterization of LY344864 as a pharmacological tool to study 5-HT1F receptors: binding affinities, brain penetration and activity in the neurogenic dural inflammation model of migraine. Life Sci., 1997, 61, 2117-2126.
27. Ramadan, N.M., Skljarevski, V., Phebus, L.A., Johnson, K.W. 5- HT1F receptor agonists in acute migraine treatment: a hypothesis. Cephalalgia, 2003, 23, 776-785.
28. Hoyer, D., Clarke, D.E., Fozard, J.R., Hartig, P.R., Martin, G.R., Mylecharane, E.J. P.R., Saxena, P.R., Humphrey, P.P. International Union of Pharmacology classification of receptors for 5-hydroxytryptamine (Serotonin). Pharmacol. Rev., 1994, 46,157-203.
29. Mitsikostas, D.D., Sanchez del Rio, M. Receptor systems mediating c-fos expression within trigeminal nucleus caudalis in animal models of migraine. Brain Res. Brain Res. Rev., 2001, 35, 20-35.
30. Bruinvels, A.T., Landwehrmeyer, B., Moskowitz, M.A., Hoyer, D. Evidence for the presence of 5-HT1B receptor messenger RNA in neurons of the rat trigeminal ganglia. Eur. J. Pharmacol., 1992, 227, 357-359.
31. Durham, P.L., Russo, A.F. Serotonergic repression of mitogenactivated protein kinase control of the calcitonin gene-related peptide enhancer. Mol. Endocrinol., 1998, 12, 1002-1009.
32. Durham, P.L., Sharma, R.V., Russo, A.F. Repression of the calcitonin gene-related peptide promoter by 5-HT1 receptor activation. J. Neurosci., 1997, 17, 9545-9553.
33. Razzaque, Z., Pickard, J.D., Ma, Q.P., Shaw, D., Morrison, K., Wang, T., Longmore, J. 5-HT1B-receptors and vascular reactivity in human isolated blood vessels: assessment of the potential craniovascular selectivity of sumatriptan. Br. J. Clin. Pharmacol., 2002, 53, 266-274.
34. Hou, M., Kanje, M., Longmore, J., Tajti, J., Uddman, R., Edvinsson, L. 5-HT(1B) and 5-HT(1D) receptors in the human trigeminal ganglion: co-localization with calcitonin gene-related peptide, substance P and nitric oxide synthase. Brain Res., 2001, 909, 112-120.
35. Gomez-Mancilla, B., Cutler, N.R., Leibowitz, M.T., Spierings, E.L., Klapper, J.A., Diamond, S., Goldstein, J., Smith, T., Couch, J.R., Fleishaker, J., Azie, N., Blunt, D.E. Safety and efficacy of PNU-142633, a selective 5-HT1D agonist, in patients with acute migraine. Cephalalgia, 2001, 21, 727-732.
36. Ma, Q.P. Co-localization of 5-HT(1B/1D/1F) receptors and glutamate in trigeminal ganglia in rats. Neuroreport, 2001, 12, 1589-1591.
37. Nilsson, T., Longmore, J., Shaw, D., Pantev, E., Bard, J.A., Branchek, T., Edvinsson, L. Characterisation of 5-HT receptors in human coronary arteries by molecular and pharmacological techniques. Eur. J. Pharmacol., 1999, 372, 49-56.
38. Amlaiky, N., Ramboz, S., Boschert, U., Plassat, J.L., Hen, R. Isolation of a mouse 5HT1E-like serotonin receptor expressed predominantly in hippocampus. J. Biol. Chem., 1992, 267, 19761-1794.
39. Adham, N., Kao, H.T., Schecter, L.E., Bard, J., Olsen, M., Urquhart, D., Durkin, M., Hartig, P.R., Weinshank, R.L., Branchek, T.A. Cloning of another human serotonin receptor (5-HT1F): a fifth 5-HT1 receptor subtype coupled to the inhibition of adenylate cyclase. Proc. Natl. Acad. Sci. U.S.A., 1993, 90, 408-412.
40. Waeber, C., Moskowitz, M.A. Autoradiographic visualisation of [3H]5-carboxamidotryptamine binding sites in the guinea pig and rat brain. Eur. J. Pharmacol., 1995, 283, 31-46.
41. Waeber, C., Moskowitz, M.A. [3H]sumatriptan labels both 5-HT1D and 5-HT1F receptor binding sites in the guinea pig brain: an autoradiographic study. Naunyn Schmiedebergs Arch. Pharmacol., 1995, 352, 263-275.
42. Bhalla, P., Sharma, H.S., Wurch, T., Pauwels, P.J., Saxena, P.R. Molecular cloning and expression of the porcine trigeminal ganglion cDNA encoding a 5-HT(1F) receptor. Eur. J. Pharmacol., 2002, 436, 23-33.
43. Lucaites, V.L., Krushinski, J.H., Schaus, J.M., Audia, J.E., Nelson, D.L. [3H]LY334370, a novel radioligand for the 5-HT1F receptor. II. Autoradiographic localization in rat, guinea pig, monkey and human brain. Naunyn Schmiedebergs Arch. Pharmacol., 2005, 371, 178-184.
44. Bergerot, A., Holland, P.R., Akerman, S., Bartsch, T., Ahn, A.H., MaassenVanDenBrink, A., Reuter, U., Tassorelli, C., Schoenen, J., Mitsikostas, D.D., van den Maagdenberg, A.M., Goadsby, P.J. Animal models of migraine: looking at the component parts of a complex disorder. Eur. J. Neurosci., 2006, 24, 1517-1534.
45. Johnson, K.W., Schaus, J.M., Durkin, M.M., Audia, J.E., Kaldor, S.W., Flaugh, M.E., Adham, N., Zgombick, J.M., Cohen, M.L., Branchek, T.A., Phebus, L.A. 5-HT1F receptor agonists inhibit neurogenic dural inflammation in guinea pigs. Neuroreport, 1997, 8, 2237-2240.
46. Cohen, M.L., Schenck, K. 5-Hydroxytryptamine (1F) receptors do not participate in vasoconstriction: lack of vasoconstriction to LY344864, a selective serotonin(1F) receptor agonist in rabbit saphenous vein. J. Pharmacol. Exp. Ther., 1999, 290, 935-939.
47. Elhusseiny, A., Hamel, E. Sumatriptan elicits both constriction and dilation in human and bovine brain intracortical arterioles. Br. J. Pharmacol., 2001, 132, 55-62.
48. Mitsikostas, D.D., Sanchez del Rio M, Moskowitz, M.A., Waeber, C. Both 5-HT1B and 5-HT1F receptors modulate c-fos expression within rat trigeminal nucleus caudalis. Eur. J. Pharmacol., 1999, 369, 271-277.
49. Mitsikostas, D.D., del Rio, M., Waeber, C. 5-Hydroxytryptamine(1B/1D) and 5-hydroxytryptamine1F receptors inhibit capsaicin-induced c-fos immunoreactivity within mouse trigeminal nucleus caudalis. Cephalalgia, 2002, 22, 384-394.
50. Amrutkar, D.V., Ploug, K.B., Hay-Schmidt, A., Porreca, F., Olesen, J., Jansen-Olesen, I. mRNA expression of 5-hydroxytryptamine 1B, 1D, and 1F receptors and their role in controlling the release of calcitonin gene-related peptide in the rat trigeminovascular system. Pain, 2012, 153,830-838.
51. Katofiasc, M.A., Johnson, K.W., Phebus, L.A. L Y334370, a selective 5HTlF agonist, inhibits the central and peripheral projections of rat trigeminal sensory neurones. Society for Neuroscience [abstracts] 1998, 24,639.
52. Shepheard, S., Edvinsson, L., Cumberbatch, M., Williamson, D., Mason, G., Webb, J., Boyce, S., Hill, R., Hargreaves, R. Possible antimigraine mechanisms of action of the 5HT1F receptor agonist LY334370. Cephalalgia, 1999,19, 851-858.
53. Nelson, D.L., Phebus, L.A., Johnson, K.W., Wainscott, D.B., Cohen, M.L., Calligaro, D.O., Xu, Y.C. Preclinical pharmacological profile of the selective 5-HT1F receptor agonist lasmiditan. Cephalalgia, 2010, 30,1159-1169.
54. Ramadan, N.M. Acute treatments: some blind alleys. Curr. Med. Res. Opin., 2001, 17 Suppl 1, s71-80.
55. Granier, L.A., Vandenhende, F., Gossen, D., Ramadan, N.M. Safety and efficacy of LY334370 IV during an acute migraine (abstract). Neurology, 2000, 54 (Suppl 3),A15.
56. Gossen, D., Granier, La., Vendenhende, F. Oral LY334370 in migraine. Results of Phase I studies (abstract). Cephalalgia, 2000, 20, 349.
57. Goldstein, D.J., Roon, K.I., Offen, W.W., Ramadan, N.M., Phebus, L.A., Johnson, K.W., Schaus, J.M., Ferrari, M.D. Selective seratonin 1F (5-HT(1F)) receptor agonist LY334370 for acute migraine: a randomised controlled trial. Lancet, 2001, 358, 1230-1234.
58. International Headache Society Clinical Trial Subcommittee. Guidelines for controlled trials of drugs in migraine. Second edition. Cephalalgia, 2000, 20, 765-786.
59. Ferrari, M.D., Färkkilä, M., Reuter, U., Pilgrim, A., Davis, C., Krauass, M., Diner, H-C. For the European COL-144 Investigators. Acute treatment of migraine with the selective 5-HT1F receptor agonist lasmiditan- A randomised proof-of-concept trial. Cephalalgia, 2010, 30, 1170-1178.
60. Färkkilä, M., Diener, H.C., Géraud, G., Láinez, M., Schoenen, J., Harner, N., Pilgrim, A., Reuter, U. For the COL MIG-202 study group. Efficacy and tolerability of lasmiditan, an oral 5-HT(1F) receptor agonist, for the acute treatment of migraine: a phase 2 randomised, placebo-controlled, parallel-group, dose-ranging study. Lancet Neurol., 2012, 11, 405-413.
61. Färkkilä, M., Diener, H-C., Géraud, G., Lániz, J.M., Schoenen, J., Pilgrim, A.J. Lasmiditan (COL-144), a selective 5HT1F agonist, is a rapid and effective oral treatment for acute migraine. J. Headache Pain, 2010, 11 (Suppl1), S43.
62. Ferrari, M.D., Roon, K.I., Lipton, R.B., Goadsby, P.J. Oral triptans (serotonin, 5-HT(1B/1D) agonists) an acute migraine treatment: a meta-analysis of 53 trials. Lancet, 2001, 358, 1668-1675.
63. Levy, D., Jakubowski, M., Burstein, R. Disruption of communication between peripheral and central trigeminovascular neurons mediates the antimigraine action of 5HT 1B/1D receptor agonists. Proc. Natl. Acad. Sci. U.S.A., 2004, 101, 4274-4279.
64. Goadsby, P.J., Charbit, A.R., Andreou, A.P., Akerman, S., Holland, P.R. Neurobiology of migraine. Neuroscience, 2009, 161, 327-341.
65. Dodick, D.W. Examining the essence of migraine-is it the blood vessel or the brain? A debate. Headache, 2008, 48, 661-667.
66. Chan, K.Y., Vermeersch, S., de Hoon, J., Villalón, C.M., Maassenvandenbrink, A. Potential mechanisms of prospective antimigraine drugs: a focus on vascular (side) effects. Pharmacol. Ther., 2011, 129, 332-351.
67. Lipton, R.B., Hamelsky, S.W., Dayno, J.M. What do patients with migraine want from acute migraine treatment? Headache, 2002, 42 Suppl 1,3-9.
68. Tfelt-Hansen, P., Pascual, J., Ramadan, N., Dahlöf, C., D'Amico, D., Diener, H.C., Hansen, J.M., Lanteri-Minet, M., Loder, E., McCrory, D., Plancade, S., Schwedt, T. International Headache Society Clinical Trials Subcommittee. Guidelines for controlled trials of drugs in migraine: third edition. A guide for investigators. Cephalalgia, 2012, 32, 6-38.
69. Tfelt-Hansen, P., Bjarnason, N.H., Dahlöf, C.G.H., Derry, S., Loder, E., Massiou, H. For the Task Force on Adverse Events in Migraine Trials of the Subcommittee on Clinical Trials of the International Headache Society. Evaluation and registration of adverse events in clinical drug trials in migraine. Cephalalgia, 2008, 28, 683-688.