Calcitonin gene-related peptide (CGRP) receptor antagonists in the treatment of migraine

CNS Drugs

Volumn 24, Issue 7, 2010, Pages 539-548

  Durham, Paul L ^a   Vause, Carrie V ^a  

^a MISSOURI STATE UNIVERSITY   (United States)

Author keywords

Antimigraines, general; Calcitonin gene related peptide receptor antagonists, general; Migraine; MK 3207, general; Olcegepant, general; Telcagepant, general.

Indexed keywords

BI 44370; BIBN 4096 BS; CALCITONIN GENE RELATED PEPTIDE RECEPTOR ANTAGONIST; MK 09474; MK 3207; OLCEGEPANT; PLACEBO; TELCAGEPANT; UNCLASSIFIED DRUG;

ALLODYNIA; BLOOD PRESSURE; BRAIN; CELL TYPE; CHRONIC PAIN; CLINICAL TRIAL; DIZZINESS; DRUG EFFICACY; DRUG TARGETING; DRUG WITHDRAWAL; GLIA CELL; HEART RATE; HUMAN; LIVER FUNCTION TEST; LIVER TOXICITY; MIGRAINE; NAUSEA; NERVE CELL; NOCICEPTIVE RECEPTOR; PAIN; PRIORITY JOURNAL; REVIEW; SENSITIZATION; SIDE EFFECT; SOMNOLENCE; TRIGEMINAL NERVE; TRIGEMINAL NUCLEUS; TRIGEMINUS GANGLION;

AZEPINES; CALCITONIN GENE-RELATED PEPTIDE; CLINICAL TRIALS AS TOPIC; DIPEPTIDES; HUMANS; IMIDAZOLES; MIGRAINE DISORDERS; QUINAZOLINES; RECEPTORS, CALCITONIN GENE-RELATED PEPTIDE; TREATMENT OUTCOME;

EID: 77953273344     PISSN: 11727047     EISSN: 11791934     Source Type: Journal    
DOI: 10.2165/11534920-000000000-00000     Document Type: Review

References (104)

1. Lipton R, Stewart W, Diamond S, et al. Prevalence and burden of migraine in the United States: data from the American Migraine Study II. Headache 2001; 41: 646-657
2. Stewart W, Lipton R, Celentano D, et al. Prevalence of migraine headache in the United States: relation to age, income, race, and other sociodemographic factors. JAMA 1991; 267: 64-69
3. Bigal ME, Lipton RB. The epidemiology, burden, and co-morbidities of migraine. Neurol Clin 2009; 27 (2): 321-334
4. Moskowitz MA. The visceral organ brain: implications for the pathophysiology of vascular head pain. Neurology 1991; 41 (2 Pt 1): 182-186
5. Goadsby PJ. Recent advances in understanding migraine mechanisms, molecules and therapeutics. Trends Mol Med 2007; 13 (1): 39-44
6. McCulloch J, Uddman R, Kingman T, et al. Calcitonin gene-related peptide: functional role in cerebrovascular regulation. Proc Natl Acad Sci USA 1986; 83: 5731-5735
7. O'Conner T, Van der Kooy D. Enrichment of a vasoactive neuropeptide (calcitonin gene related peptide) in the tri-geminal sensory projection to the intracranial arteries. J Neurosci 1988; 8: 2468-2476
8. Blau JN, Dexter SL. The site of pain origin during migraine attacks. Cephalalgia 1981; 1 (3): 143-147
9. Link AS, Kuris A, Edvinsson L. Treatment of migraine attacks based on the interaction with the trigemino-cere-brovascular system. J Headache Pain 2008; 9 (1): 5-12
10. Humphrey P, Feniuk W. Mode of action of the anti-migraine drug sumatriptan. Trends Pharmacol Sci 1991; 12 (12): 444-446
11. Bolay H, Reuter U, Dunn A, et al. Intrinsic brain activity triggers trigeminal meningeal afferents in a migraine model. Nat Med 2002; 8 (2): 136-142
12. Hargreaves R. New migraine and pain research. Headache 2007; 47 Suppl. 1: S26-43
13. Pietrobon D. Migraine: new molecular mechanisms. Neuro-scientist 2005; 11 (4): 373-386
14. Buzzi M, Bonamini M, Moskowitz M. Neurogenic model of migraine. Cephalalgia 1995; 15: 277-280
15. O'Conner T, Van der Kooy D. Pattern of intracranial and extracranial projections of trigeminal ganglion cells. J Neurosci 1986; 6: 2200-2207
16. Edvinsson L, Goadsby P. Neuropeptides in migraine and cluster headache. Cephalalgia 1994; 14: 320-327
17. Hargreaves R, Shepheard S. Pathophysiology of migraine: new insights. Can J Neurol Sci 1999; 26 Suppl. 3: S12-9
18. Pietrobon D, Striessnig J. Neurobiology of migraine. Nat Rev Neurosci 2003; 4 (5): 386-398
19. Amara S, Arriza J, Leff S, et al. Expression in brain of a messenger RNA encoding a novel neuropeptide homologous to calcitonin gene-related peptide. Science 1985; 229: 1094-1097
20. Juaneda C, Dumont Y, Quirion R. The molecular phar-macology of CGRP and related peptide receptor subtypes. Trends Pharmacol Sci 2000; 21 (11): 432-438
21. Steenbergh P, Hoppener J, Zandberg J, et al. A second human calcitonin/CGRP gene. FEBS Lett 1985; 183: 403-407
22. Van Rossum D, Hanisch U, Quirion R. Neuroanatomical localization, pharmacological characterization and functions of CGRP, related peptides and their receptors. Neurosci Biobehav Rev 1997; 21 (5): 649-678
23. Rosenfeld M, Mermod J-J, Amara S, et al. Production of a novel neuropeptide encoded by the calcitonin gene via tissue-specific RNA processing. Nature 1983; 304: 129-135
24. Sternini C. Enteric and visceral afferent CGRP neurons: targets of innervation and differential expression patterns. Ann N Y Acad Sci 1992; 657: 170-186
25. Goadsby P, Edvinsson L, Elkman R. Vasoactive peptide release in the extracerebral circulation of humans during migraine headache. Ann Neurol 1990; 28: 183-187
26. Bellamy J, Cady R, Durham P. Salivary levels of CGRP and VIP in rhinosinusitis and migraine patients. Headache 2006; 46: 24-33
27. Cady R, Vause C, Ho T, et al. Elevated saliva calcitonin gene-related peptide levels during acute migraine predict therapeutic response to rizatriptan. Headache 2009; 49: 1258-1266
28. Goadsby P, Edvinsson L. The trigeminovascular system and migraine: studies characterizing cerebrovascular and neuropeptide changes seen in humans and cats. Ann Neurol 1993; 33: 48-56
29. Lassen L, Haderslev P, Jacobsen V, et al. CGRP may play a causative role in migraine. Cephalalgia 2002; 22 (1): 54-61
30. Olesen J, Diener H, Husstedt I, et al. Calcitonin gene-related peptide receptor antagonist BIBN 4096 BS for the acute treatment of migraine. N Engl J Med 2004; 350: 1104-1110
31. Ottosson A, Edvinsson L. Release of histamine from dural mast cells by substance P and calcitonin gene-related peptide. Cephalalgia 1997; 17 (3): 166-174
32. Messlinger K, Hanesch U, Kurosawa M, et al. Calcitonin gene related peptide released from dural nerve fibers mediates increase of meningeal blood flow in the rat. Can J Physiol Pharmacol 1995; 73 (7): 1020-1024
33. Strassman A, Raymond S, Burnstein R. Sensitization of meningeal sensory neurons and the origin of headaches. Nature 1996; 384: 560-564
34. Durham P, Russo A. New insights into the molecular ac-tions of serotonergic antimigraine drugs. Pharmacol Ther 2002; 94: 77-92
35. Thalakoti S, Patil V, Damodaram S, et al. Neuron-glia signaling in trigeminal ganglion: implications for migraine pathology. Headache 2007; 47 (7): 1008-1023
36. Zhang XC, Strassman AM, Burstein R, et al. Sensitization and activation of intracranial meningeal nociceptors by mast cell mediators. J Pharmacol Exp Ther 2007; 322 (2): 806-812
37. Schaible HG. On the role of tachykinins and calcitonin gene-related peptide inthe spinal mechanismsof nociception and in the induction and maintenance of inflammation-evoked hyperexcitability in spinal cord neurons (with special reference to nociception in joints). Prog Brain Res 1996; 113: 423-441
38. Ruda MA, Ling QD, Hohmann AG, et al. Altered noci-ceptive neuronal circuits after neonatal peripheral inflammation. Science 2000; 289 (5479): 628-631
39. Neugebauer V, Rumenapp P, Schaible HG. Calcitonin gene-related peptide is involved in the spinal processing of mechanosensory input from the rat's knee joint and in the generation and maintenance of hyperexcitability of dorsal horn-neurons during development of acute inflammation. Neuroscience 1996; 71 (4): 1095-1109
40. Cridland RA, Henry JL. Effects of intrathecal administra-tion of neuropeptides on a spinal nociceptive reflex in the rat: VIP, galanin, CGRP, TRH, somatostatin and angio-tensin II. Neuropeptides 1988; 11 (1): 23-32
41. Sun R, Lawand N, Willis W. The role of calcitonin gene-related peptide (CGRP) in the generation and maintenance of mechanical allodynia and hyperalgesia in rats after intradermal injection of capsaicin. Pain 2003; 104: 201-208
42. Sun R, Tu Y, Lawand N, et al. Calcitonin gene-related peptide receptor activation produces PKA-and PKC-dependent mechanical hyperalgesia and central sensitiza-tion. J Neurophysiol 2004; 92: 2859-2866
43. Galeazza MT, Garry MG, Yost HJ, et al. Plasticity in the synthesis and storage of substance P and calcitonin gene-related peptide in primary afferent neurons during peripheral inflammation. Neuroscience 1995; 66 (2): 443-458
44. Oku R, Satoh M, Fujii N, et al. Calcitonin gene-related peptide promotes mechanical nociception by potentiating release of substance P from the spinal dorsal horn in rats. Brain Res 1987; 403 (2): 350-354
45. Biella G, Panara C, Pecile A, et al. Facilitatory role of calcitonin gene-related peptide (CGRP) on excitation induced by substance P (SP) and noxious stimuli in rat spinal dorsal horn neurons: an iontophoretic study in vivo. Brain Res 1991; 559 (2): 352-356
46. Bennett AD, Chastain KM, Hulsebosch CE. Alleviation of mechanical and thermal allodynia by CGRP(8-37) in a rodent model of chronic central pain. Pain 2000; 86 (1-2): 163-175
47. Hay DL, Poyner DR, Quirion R. International Union of Pharmacology: LXIX. Status of the calcitonin gene-related peptide subtype 2 receptor. Pharmacol Rev 2008; 60 (2): 143-145
48. Poyner D, Sexton P, Marshall I, et al. International Union of Pharmacology: XXXII. The mammalian calcitonin gene-related peptides, adrenomedullin, amylin, and calci-tonin receptors. Pharmacol Rev 2002; 54 (2): 233-246
49. Mallee J, Salvatore C, LeBourdelles B, et al. Receptor activity-modifying protein 1 determines the species selectivity of non-peptide CGRP receptor antagonists. J Biol Chem 2002; 277 (16): 14294-14298
50. Banerjee S, Evanson J, Harris E, et al. Identification of specific calcitonin-like receptor residues important for calcitonin gene-related peptide high affinity binding. BMC Pharmacol 2006; 15: 6-9
51. Maggi C, Rovero P, Giuliani S, et al. Biological activity of N-terminal fragments of calcitonin gene-related peptide. Eur J Pharmacol 1990; 179: 217-219
52. Zaidi M, Brain S, Tippins J, et al. Structure-activity re-lationship of human calcitonin-gene-related peptide. Biochem J 1990; 269: 775-780
53. Chiba T, Yamaguchi A, Yamatani T, et al. Calcitonin gene-related peptide receptor antagonist human CGRP-(8-37). Am J Physiol 1989; 256 (2 Pt 1): E331-5
54. Mentlein R, Roos T. Proteases involved in the metabolism of angiotensin II, bradykinin, calcitonin gene-related peptide (CGRP), and neuropeptide Y by vascular smooth muscle cells. Peptides 1996; 17: 709-720
55. Hughes SR, Brain SD. A calcitonin gene-related peptide (CGRP) antagonist (CGRP8-37) inhibits microvascular responses induced by CGRP and capsaicin in skin. Br J Pharmacol 1991 Nov; 104 (3): 738-742
56. 8-37, a CGRP antibody and an RNA-Spiegelmer on CGRP induced vasodilatation in the perfused and non-perfused rat middle cerebral artery. Br J Pharmacol 2007; 150: 633-640
57. Rist B, Lacroix J, Entzeroth M, et al. CGRP 27-37 ana-logues with high affinity to the CGRP1 receptor show antagonistic propertiesin arat blood flow assay. Regul Pept 1999; 79 (2-3): 153-158
58. Morara S, Wang LP, Filippov V, et al. Calcitonin gene-related peptide (CGRP) triggers Ca2+ responses in cultured astrocytes and in Bergmann glial cells from cerebellar slices. Eur J Neurosci 2008; 28 (11): 2213-2220
59. Levy D, Jakubowski M, Burstein R. Disruption of com-munication between peripheral and central trigemino-vascular neurons mediates the antimigraine action of 5HT1B/1D receptor agonists. Proc Natl Acad Sci USA 2004; 101 (12): 4274-4279
60. Lennerz JK, Ruhle V, Ceppa EP, et al. Calcitonin receptor-like receptor (CLR), receptor activity-modifying protein 1 (RAMP1), and calcitonin gene-related peptide (CGRP) immunoreactivity in the rat trigeminovascular system: differences between peripheral and central CGRP receptor distribution. J Comp Neurol 2008; 507 (3): 1277-1299
61. Moreno M, Cohen Z, Stanimirovic D, et al. Functional calcitonin gene-related peptide type 1 and adrenomedullin receptors in human trigeminal ganglia, brain vessels, and cerebromicrovascular or astroglial cells in culture. J Cereb Blood Flow Metab 1999; 19 (11): 1270-1278
62. Oliver K, Wainwright A, Edvinsson L, et al. Im-munohistochemical localization of calcitonin receptorlike receptor and receptor activity-modifying proteins in the human cerebral vasculature. J Cereb Blood Flow Metab 2002; 22 (5): 620-629
63. Edvinsson L, Alm R, Shaw D, et al. Effect of the CGRP receptor antagonist BIBN4096BS in human cerebral, coronary and omental arteries and in SK-N-MC cells. Eur J Pharmacol 2002; 434 (1-2): 49-53
64. Petersen KA, Nilsson E, Olesen J, et al. Presence and function of the calcitonin gene-related peptide receptor on rat pial arteries investigated in vitro and in vivo. Cepha-lalgia 2005; 25 (6): 424-432
65. Strassman AM, Weissner W, Williams M, et al. Axon diam-eters and intradural trajectories of the dural innervation in the rat. J Comp Neurol 2004; 473 (3): 364-376
66. Doods H, Hallermayer G, Wu D, et al. Pharmacological profile of BIBN4096BS, the first selective small molecule CGRP antagonist. Br J Pharmacol 2000; 129 (3): 420-423
67. Rudolf K, Eberlein W, Engel W, et al. Development of human calcitonin gene-related peptide (CGRP) receptor antagonists: 1. Potent and selective small molecule CGRP antagonists. 1-[N2-[3,5-dibromo-N-[[4-(3,4-dihydro-2(1H)- oxoquinazolin-3-yl)-1-piperidinyl]carbonyl]-D-tyrosyl]-l-lysyl]-4-(4-pyridinyl) piperazine: the first CGRP antagonist for clinical trials in acute migraine. J Med Chem 2005; 48 (19): 5921-5931
68. Edvinsson L, Petersen K. CGRP-receptor antagonism in migraine treatment. CNS Neurol Disord Drug Targets 2007; 6: 240-246
69. Recober A, Russo A. Olcegepant, a non-peptide CGRP1 antagonist for migraine treatment. IDrugs 2007; 10: 566-574
70. Kapoor K, Arulmani U, Heiligers J, et al. Effects of BIBN4096BS on cardiac output distribution and on CGRP-induced carotid haemodynamic responses in the pig. Eur J Pharmacol 2003; 475 (1-3): 69-77
71. Salmon A, Damaj M, Marubio L, et al. Altered neuro-adaptation in opiate dependence and neurogenic inflammatory nociception in alpha CGRP-deficient mice. Nat Neurosci 2001; 4 (4): 357-358
72. Verheggen R, Bumann K, Kaumann A. BIBN4096BS is a potent competitive antagonist of the relaxant effects of alpha-CGRP on human temporal artery: comparison with CGRP(8-37). Br J Pharmacol 2002; 136: 120-126
73. Iovino M, Feifel U, Yong CL, et al. Safety, tolerability and pharmacokinetics of BIBN 4096 BS, the first selective small molecule calcitonin gene-related peptide receptor antagonist, following single intravenous administration in healthy volunteers. Cephalalgia 2004; 24 (8): 645-656
74. Zhang Z, Winborn C, Marquez de Prado B, et al. Sensiti-zation of calcitonin gene-related peptide receptors by receptor activity-modifying protein-1 in the trigeminal ganglion. J Neurosci 2007; 27 (10): 2693-2703
75. Ferrari M, Roon K, Lipton R, et al. Oral triptans (sero-tonin 5-HT(1B/1D) agonists) in acute migraine treatment: a meta-analysis of 53 trials. Lancet 2001; 358 (9294): 1668-1675
76. Petersen K, Lassen L, Birk S, et al. BIBN4096BS antag-onizes human alpha-calcitonin gene related peptide-induced headache and extracerebral artery dilatation. Clin Pharmacol Ther 2005; 77: 202-213
77. Williams TM, Stump CA, Nguyen DN, et al. Non-peptide calcitonin gene-related peptide receptor antagonists from a benzodiazepinone lead. Bioorg Med Chem Lett 2006; 16 (10): 2595-2598
78. Burgey CS, Paone DV, Shaw AW, et al. Synthesis of the (3R,6S)-3-amino-6-(2,3-difluorophenyl)azepan-2-one of telcagepant (MK-0974), a calcitonin gene-related peptide receptor antagonist for the treatment of migraine headache. Org Lett 2008; 10 (15): 3235-3238
79. Moore EL, Burgey CS, Paone DV, et al. Examining the binding properties of MK-0974: a CGRP receptor antagonist for the acute treatment of migraine. Eur J Pharmacol 2009; 602 (2-3): 250-254
80. Salvatore C, Hershey J, Corcoran H, et al. Pharmacological characterization of MK-0974 [N-[(3R,6S)-6-(2,3-di-fluorophenyl)-2-oxo-1-(2,2,2- trifluoroethyl)azepan-3-yl]-4-(2-oxo-2,3-dihydro-1H-imidazo[4,5-b]pyridin-1-yl) piperidine-1-carboxamide], a potent and orally active calcitonin gene-related peptide receptor antagonist for the treatment of migraine. J Pharmacol Exp Ther 2008; 324: 416-421
81. Salvatore CA, Hershey JC, Corcoran HA, et al. Pharmaco-logical characterization of MK-0974 [N-[(3R,6S)-6-(2, 3-difluorophenyl)-2-oxo-1-(2,2,2- trifluoroethyl)azepan-3-y l]-4-(2-oxo-2,3-dihydro-1H-imidazo[4,5-b]pyridin-1-yl) -piperidine-1-carbox amide], a potent and orally active calcitonin gene-related peptide receptor antagonist for the treatment of migraine. J Pharmacol Exp Ther 2008; 324 (2): 416-421
82. Ho TW, Mannix LK, Fan X, et al. Randomized controlled trial of an oral CGRP receptor antagonist, MK-0974, in acute treatment of migraine. Neurology 2008; 70 (16): 1304-1312
83. Paone D, Shaw A, Nguyen D, et al. Potent, orally bioavail-able calcitonin gene-related peptide receptor antagonists for the treatment of migraine: discovery of N-[(3R,6S)-6-(2,3-difluorophenyl)-2-oxo-1-(2,2,2-trifluoroethyl) azepan-3-yl]-4-(2-oxo-2,3-dihydro-1H-imidazo[4,5-b]pyridin-1-yl) piperidine-1-carboxamide (MK-0974). J Med Chem 2007; 50: 5564-5567
84. Connor KM, Shapiro RE, Diener HC, et al. Randomized, controlled trial of telcagepant for the acute treatment of migraine. Neurology 2009; 73 (12): 970-977
85. Tepper SJ, Cleves C. Telcagepant, a calcitonin gene-related peptide antagonist for the treatment of migraine. Curr Opin Investig Drugs 2009; 10 (7): 711-720
86. Burgey CS, Potteiger CM, Deng JZ, et al. Optimization of azepanone calcitonin gene-related peptide (CGRP) receptor antagonists: development of novel spiropiperidines. Bioorg Med Chem Lett 2009; 19 (22): 6368-6372
87. Capuano A, De Corato A, Lisi L, et al. Proinflammatory-activated trigeminal satellite cells promote neuronal sen-sitization: relevance for migraine pathology. Mol Pain 2009; 5: 43-56
88. Williamson D, Hill R, Shepheard S, et al. The anti-migraine 5-HT(1B/1D) agonist rizatriptan inhibits neuro-genic dural vasodilation in anaesthetized guinea-pigs. Br J Pharmacol 2001; 133: 1029-1034
89. Reddington M, Priller J, Treichel J, et al. Astrocytes and microglia as potential targets for calcitonin gene related peptide in the central nervous system. Can J Physiol Pharmacol 1995; 73: 1047-1049
90. Han J, Li W, Neugebauer V. Critical role of calcitonin gene-related peptide 1 receptors in the amygdala in sy-naptic plasticity and pain behaviour. J Neurosci 2005; 25 (46): 10717-10728
91. Yu LC, Hou JF, Fu FH, et al. Roles of calcitonin gene-related peptide and its receptors in pain-related behavioral responses in the central nervous system. Neurosci Bio-behav Rev 2009; 33 (8): 1185-1191
92. Olesen J, Burstein R, Ashina M, et al. Origin of pain in migraine: evidence for peripheral sensitisation. Lancet Neurol 2009; 8 (7): 679-690
93. Levy D, Burstein R, Strassman A. Mast cell involvement in the pathophysiology of migraine headache: a hypothesis. Headache 2006; 46 Suppl. 1: S13-8
94. Li J, Vause C, Durham P. Calcitonin gene-related peptide stimulation of nitric oxide synthesis and release from tri-geminal ganglion glial cells. Brain Res 2008; 1196: 22-32
95. Vause CV, Durham PL. CGRP stimulation of iNOS and NO release from trigeminal ganglion glial cells involves mitogen-activated protein kinase pathways. J Neurochem 2009; 110 (3): 811-821
96. Cheng JK, Ji RR. Intracellular signaling in primary sensory neurons and persistent pain. Neurochem Res 2008; 33 (10): 1970-1978
97. Adwanikar H, Ji G, Li W, et al. Spinal CGRP1 receptors contribute to supraspinally organized pain behavior and pain-related sensitization of amygdala neurons. Pain 2007; 132 (1-2): 53-66
98. Bernard JF, Bandler R. Parallel circuits for emotional coping behaviour: new pieces in the puzzle. J Comp Neurol 1998; 401 (4): 429-436
99. Suter MR, Wen YR, Decosterd I, et al. Do glial cells con-trol pain? Neuron Glia Biol 2007; 3 (3): 255-268
100. Watkins L, Maier S. Beyond neurons: evidence that im-mune and glial cells contribute to pathological pain states. Physiol Rev 2002; 82: 981-1011
101. Watkins L, Milligan E, Maier S. Glial proinflammatory cytokines mediate exaggerated pain states: implications for clinical pain. Adv Exp Med Biol 2003; 521: 1-21
102. Wei F, Guo W, Zou S, et al. Supraspinal glial-neuronal interactions contribute to descending pain facilitation. J Neurosci 2008; 28 (42): 10482-10495
103. Ren K, Dubner R. Neuron-glia crosstalk gets serious: role in pain hypersensitivity. Curr Opin Anaesthesiol 2008; 21 (5): 570-579
104. Guo W, Wang H, Watanabe M, et al. Glial-cytokine-neu-ronal interactions underlying the mechanisms of persistent pain. J Neurosci 2007; 27 (22): 6006-6018