Clinical and preclinical rationale for CGRP-receptor antagonists in the treatment of migraine

Headache

Volumn 48, Issue 8, 2008, Pages 1259-1268

  Tepper, Stewart J ^a,b   Stillman, Mark J ^a  

^a NEUROLOGICAL INSTITUTE   (United States)

^b LERNER RESEARCH INSTITUTE   (United States)

Author keywords

BIBN4096; Calcitonin gene related peptide; Migraine; MK 0974; Olcegepant; RAMP1; Telcagepant

Indexed keywords

AVITRIPTAN; BIBN 4096 BS; CALCITONIN GENE RELATED PEPTIDE; CALCITONIN GENE RELATED PEPTIDE RECEPTOR; CALCITONIN GENE RELATED PEPTIDE RECEPTOR ANTAGONIST; CYCLIC AMP DEPENDENT PROTEIN KINASE; DIHYDROERGOTAMINE; GLYCERYL TRINITRATE; MK 0974; OLCEGEPANT; PLACEBO; PROTEIN KINASE C; RECEPTOR ACTIVITY MODIFYING PROTEIN 1; RIZATRIPTAN; SUBSTANCE P; SUMATRIPTAN; TELCAGEPANT; UNCLASSIFIED DRUG; ZOLMITRIPTAN;

BLOOD BRAIN BARRIER; BLOOD LEVEL; CAT; DIZZINESS; DRUG EFFICACY; DRUG SAFETY; EXTRAVASATION; FATIGUE; HEADACHE; HUMAN; MIGRAINE; NAUSEA; NONHUMAN; PARESTHESIA; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN SECRETION; REVIEW; SOMNOLENCE; TRANSGENIC MOUSE; TRIGEMINUS GANGLION; XEROSTOMIA;

ANIMALS; AZEPINES; CLINICAL TRIALS AS TOPIC; DIPEPTIDES; DRUG EVALUATION, PRECLINICAL; HUMANS; IMIDAZOLES; MIGRAINE DISORDERS; QUINAZOLINES; RECEPTORS, CALCITONIN GENE-RELATED PEPTIDE;

EID: 51549089370     PISSN: 00178748     EISSN: 15264610     Source Type: Journal    
DOI: 10.1111/j.1526-4610.2008.01214.x     Document Type: Review

References (77)

1. Dodick DW. Brainstem dysfunction in chronic migraine as evidenced by neurophysiological and positron emission tomography (PET) studies - an editorial comment. Headache. 2007 47 : 1004 1007.
2. Pietrobon D, Striessnig J. Neurobiology of migraine. Nat Rev Neurosci. 2003 4 : 386 398.
3. Durham PL. CGRP receptor antagonists - a fresh approach to migraine therapy? N Engl J Med. 2004 350 : 1073 1074.
4. Durham PL. Emerging neural theories of migraine pathogenesis: Calcitonin gene-related peptide (CGRP) and migraine. Headache. 2006 46 (Suppl. 1 S3 S8.
5. Michelangeli VP, Findlay DM, Fletcher A, Martin TJ. Calcitonin gene-related peptide (CGRP) acts independently of calcitonin on cyclic AMP formation in clonal osteogenic sarcoma cells (UMR 106-01). Calcif Tissue Int. 1986 39 : 44 48.
6. Fiscus RR, Zhou HL, Wang X, et al. Calcitonin gene-related peptide (CGRP)-induced cyclic AMP, cyclic GMP and vasorelaxant responses in rat thoracic aorta are antagonized by blockers of endothelium-derived relaxant factor (EDRF). Neuropeptides. 1991 20 : 133 143.
7. Wang X, Han C, Fiscus RR. Calcitonin gene-related peptide (CGRP) causes endothelium-dependent cyclic AMP, cyclic GMP and vasorelaxant responses in rat abdominal aorta. Neuropeptides. 1991 20 : 115 124.
8. Raymond LA, Tingley WG, Blackstone CD, Roche KW, Huganir RL. Glutamate receptor modulation by protein phosphorylation. J Physiol Paris. 1994 88 : 181 192.
9. Hatt H. Modification of glutamate receptor channels: Molecular mechanisms and functional consequences. Naturwissenschaften. 1999 86 : 177 186.
10. Swope SL, Moss SJ, Raymond LA, Huganir RL. Regulation of ligand-gated ion channels by protein phosphorylation. Adv Second Messenger Phosphoprotein Res. 1999 33 : 49 78.
11. Sexton PM, McKenzie JS, Mason RT, Moseley JM, Martin TJ, Mendelsohn FA. Localization of binding sites for calcitonin gene-related peptide in rat brain by in vitro autoradiography. Neuroscience. 1986 19 : 1235 1245.
12. Kawai Y, Takami K, Shiosaka S, et al. Topographic localization of calcitonin gene-related peptide in the rat brain: An immunohistochemical analysis. Neuroscience. 1985 15 : 747 763.
13. Oliver KR, Wainwright A, Kinsey AM, Heavens RP, Sirinathsinghji DJ, Hill RG. Regional and cellular localization of calcitonin gene-related peptide-receptor component protein mRNA in the guinea-pig central nervous system. Brain Res Mol Brain Res. 1999 66 : 205 210.
14. Ma W, Chabot JG, Powell KJ, Jhamandas K, Dickerson IM, Quirion R. Localization and modulation of calcitonin gene-related peptide-receptor component protein-immunoreactive cells in the rat central and peripheral nervous systems. Neuroscience. 2003 120 : 677 694.
15. Ramadan NM, Buchanan TM. New and future migraine therapy. Pharmacol Ther. 2006 112 : 199 212.
16. Buldyrev I, Tanner NM, Hsieh H, Dodd EG, Nguyen LT, Balkowiec A. Calcitonin gene-related peptide enhances release of native brain-derived neurotrophic factor from trigeminal ganglion neurons. J Neurochem. 2006 99 : 1338 1350.
17. Han JS, Li W, Neugebauer V. Critical role of calcitonin gene-related peptide 1 receptors in the amygdala in synaptic plasticity and pain behavior. J Neurosci. 2005 25 : 10717 10728.
18. Raskin NH, Hosobuchi Y, Lamb S. Headache may arise from perturbation of brain. Headache 1987 27 : 416 420.
19. Weiller C, May A, Limmroth V, et al. Brain stem activation in spontaneous human migraine attacks. Nat Med. 1995 1 : 658 660.
20. Amara SG, Jonaas V, Jonas V, Rosenfeld MG, Ong ES, Evans RM. Alternative RNA processing in calcitonin gene expression generates mRNAs encoding different polypeptide products. Nature. 1982 298 : 240 244.
21. Brain SD. Calcitonin gene-related peptide (CGRP) antagonists: Blockers of neuronal transmission in migraine. Br J Pharmacol. 2004 142 : 1053 1054.
22. Kane SA, Salvatore CA, Hershey JC, et al. Profile of MK-0974, the first orally bioavailable CGRP receptor antagonist. Headache. 2007 47 : 812 (abstract).
23. Goadsby PJ, Edvinsson L, Ekman R. Release of vasoactive peptides in the extracerebral circulation of humans and the cat during activation of the trigeminovascular system. Ann Neurol. 1988 23 : 193 196.
24. Tvedskov JF, Lipka K, Ashina M, Iversen HK, Schifter S, Olesen J. No increase of calcitonin gene-related peptide in jugular blood during migraine. Ann Neurol. 2005 58 : 561 568.
25. Zagami AS, Goadsby PJ, Edvinsson L. Stimulation of the superior sagittal sinus in the cat causes release of vasoactive peptides. Neuropeptides. 1990 16 : 69 75.
26. Goadsby PJ, Edvinsson L, Ekman R. Vasoactive peptide release in the extracerebral circulation of humans during migraine headache. Ann Neurol. 1990 28 : 183 187.
27. Goadsby PJ, Edvinsson L. The trigeminovascular system and migraine: Studies characterizing cerebrovascular and neuropeptide changes seen in humans and cats. Ann Neurol. 1993 33 : 48 56.
28. Goadsby PJ, Edvinsson L. Joint 1994 Wolff Award Presentation. Peripheral and central trigeminovascular activation in cat is blocked by the serotonin (5HT)-1D receptor agonist 311C90. Headache. 1994 34 : 394 399.
29. Knight YE, Edvinsson L, Goadsby PJ. Blockade of calcitonin gene-related peptide release after superior sagittal sinus stimulation in cat: A comparison of avitriptan and CP122,288. Neuropeptides. 1999 33 : 41 46.
30. Durham PL, Russo AF. Regulation of calcitonin gene-related peptide secretion by a serotonergic antimigraine drug. J Neurosci. 1999 19 : 3423 3429.
31. Gallai V, Sarchielli P, Floridi A, et al. Vasoactive peptide levels in the plasma of young migraine patients with and without aura assessed both interictally and ictally. Cephalalgia. 1995 15 : 384 390.
32. Lassen LH, Haderslev PA, Jacobsen VB, Iversen HK, Sperling B, Olesen J. CGRP may play a causative role in migraine. Cephalalgia. 2002 22 : 54 61.
33. Petersen KA, Birk S, Lassen LH, et al. The CGRP-antagonist, BIBN4096BS does not affect cerebral or systemic haemodynamics in healthy volunteers. Cephalalgia. 2005 25 : 139 147.
34. Juhasz G, Zsombok T, Modos EA, et al. O-induced migraine attack: Strong increase in plasma calcitonin gene-related peptide (CGRP) concentration and negative correlation with platelet serotonin release. Pain. 2003 106 : 461 470.
35. Durham PL, Dong PX, Belasco KT, et al. Neuronal expression and regulation of CGRP promoter activity following viral gene transfer into cultured trigeminal ganglia neurons. Brain Res. 2004 997 : 103 110.
36. Silberstein SD, Mauskop A, Dodick DW, et al. Program to assess headache treatment strategies: An observational study of botulinum toxin type A in the preventive treatment of headache. Headache. 2006 46 : 846 847 (abstract).
37. Silberstein SD, Mauskop A, Dodick DW, et al. Predictors of outcomes with botulinum toxin type A in the preventive treatment of headache. Cephalalgia. 2006 26 : 1371 (abstract).
38. Durham PL, Cady R, Cady R. Regulation of calcitonin gene-related peptide secretion from trigeminal nerve cells by botulinum toxin type A: Implications for migraine therapy. Headache. 2004 44 : 35 43.
39. Zhang Z, Winborn CS, Marquez de Prado B, Russo AF. Sensitization of calcitonin gene-related peptide receptors by receptor activity-modifying protein-1 in the trigeminal ganglion. J Neuroscience. 2007 27 : 2693 2703.
40. Storer RJ, Goadsby PJ. Microiontophoretic application of serotonin (5HT)1B/1D agonists inhibits trigeminal cell firing in the cat. Brain. 1997 120 : 2171 2177.
41. Storer RJ, Akerman S, Goadsby PJ. Calcitonin gene-related peptide (CGRP) modulates nociceptive trigeminovascular transmission in the cat. Br J Pharmacol. 2004 142 : 1171 1181.
42. Yu LC, Weng XH, Wang JW, Lundeberg T. Involvement of calcitonin gene-related peptide and its receptor in anti-nociception in the periaqueductal grey of rats. Neurosci Lett. 2003 349 : 1 4.
43. Durham PL, Russo AF. Stimulation of the calcitonin gene-related peptide enhancer by mitogen-activated protein kinases and repression by an antimigraine drug in trigeminal ganglia neurons. J Neurosci. 2003 23 : 807 815.
44. Russo AF. Ramping it up: RAMP1 and the implications for migraine. Pharmacogenomics. 2007 8 : 687 690.
45. 8-37 at the CGRP2 receptor of the rat prostatic vas deferens. Br J Pharmacol. 1999 126 : 1163 1170.
46. 8-37. Br J Pharmacol. 1999 128 : 283 292.
47. Escott KJ, Beattie DT, Connor HE, Brain SD. Trigeminal ganglion stimulation increases facial skin blood flow in the rat: A major role for calcitonin gene-related peptide. Brain Res. 1995 69 : 93 99.
48. Longmore J, Hogg JE, Hutson PE, Hill RG. Effects of two truncated forms of human calcitonin-gene related peptide: Implications for receptor classification. Eur J Pharmacol. 1994 265 : 53 59.
49. 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 : 5921 5931.
50. Doods H, Hallermayer G, Wu D, et al. Pharmacological profile of BIBN4096BS, the first selective small molecule CGRP antagonist. Br J Pharmacol. 2000 129 : 420 423.
51. Edvinsson L. Clinical data on the CGRP antagonist BIBN4096BS for treatment of migraine attacks. CNS Drug Rev. 2005 11 : 69 76.
52. Iovino M, Feifel U, Yong CL, Wolters JM, Wallenstein G. 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 : 645 656.
53. Olesen J, Diener H-C, Husstedt IW, for the BIBN 4096 BS Clinical Proof of Concept Study Group, 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.
54. Salvatore CA, Hershey JC, Corcoran HA, et al. Pharmacological characterization of MK-0974 [N-[(3R,6S)-6-(2,3-difluorophenyl)-2-oxo-1-(2,2,2- trifluoroethyl)azepan-3-yl]-4-(2-oxo-2,3-dihydro-1 H-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.
55. Fan X (F), Assaid CA, Ho T. An adaptive two-stage design in a Phase 2 dose-finding trial to treat acute migraine. Neurology. 2007 68 (Suppl. 1 A195 (abstract).
56. Sinclair SR, Kane SA, Xiao A, et al. MK-0974 oral CGRP antagonist inhibits capsaicin-induced increase in dermal microvascular blood flow. Neurology. 2007 68 (Suppl. 1 A307 (abstract), also in Headache 2007;47:811 (abstract).
57. Sinclair SR, Boyle JE, de Lepeleire I, et al. MK-0974, a novel oral CGRP antagonist, exhibits similar pharmacokinetics during and between migraine attacks. Headache. 2007 47 : 811 812 (abstract).
58. Ho TW, Mannix LK, Fan X, et al., on behalf of the MK- 0974 Protocol 004 study group. Randomized controlled trial of an oral CGRP receptor antagonist, MK-0974, in acute treatment of migraine. Neurology. 2008 70 : 1304 1312.
59. Ho TW. Platform presentation. American Headache Society meeting, Chicago, 2007.
60. Ho TW, Ferrari MD, Dodick DW, et al. Antimigraine efficacy and tolerability of the novel oral CGRP receptor antagonist MK-0974: A Phase III clinical trial versus placebo and zolmitriptan. Headache. 2008 48 : S7 8 (abstract).
61. Dodick DW, Galet V, Kost J, Assaid C, Ho TW. Sustained pain freedom and no adverse events" as an endpoint in clinical trials of acute migraine treatments: Application to patient-level data from a trial of the CGRP receptor antagonist, MK-0974, and zolmitriptan. Headache. 2008 48 : S41 42 (abstract).
62. TW H. Platform presentation, American Headache Society meeting. Boston. 2008.
63. Behm MO, Blanchard RL, Murphy MG, et al. Assessment of the effect of MK-0974, and oral CGRP receptor antagonist, on spontaneous ischemia in patients with stable cardiovascular disease. Headache. 2008 48 : S39.
64. Van dr Schueren BJ, Blanchard R, Murphy MG, et al. Effect of MK-0974, an oral CGRP antagonist, on the hemodynamic response to sublingual nitroglycerin. Headache. 2008 48 : S63 64.
65. Levy D, Burstein R, Strassman AM. Calcitonin gene-related peptide does not excite or sensitize meningeal nociceptors: Implications for the pathophysiology of migraine. Ann Neurol. 2005 58 : 698 705.
66. Fischer MJ, Koulchitsky S, Messlinger K. The nonpeptide calcitonin gene-related peptide receptor antagonist BIBN4096BS lowers the activity of neurons with meningeal input in the rat spinal trigeminal nucleus. J Neurosci. 2005 25 : 5877 5883.
67. Goodsby PJ, Edvinsson L. Human in vivo evidence for trigeminovascular activation in cluster headache. Neuropeptide changes and effects of acute attack therapies. Brain. 1994 117 (Pt. 3 427 434.
68. Fanciullacci M, Alessandri M, Figini M, Geppetti P, Michelacci S. Increase in plasma calcitonin gene-related peptide from the extracerebral circulation during nitroglycerin-induced cluster headache attack. Pain. 1995 60 : 119 123.
69. Goadsby PJ, Edvinsson L. Neuropeptide changes in a case of chronic paroxysmal hemicrania - evidence for trigemino-parasympathetic activation. Cephalalgia. 1996 16 : 448 450.
70. Edvinsson L. A pathophysiological view of primary headaches. Funct Neurol. 2000 15 (Suppl. 3 50 60.
71. Goto K, Miyauchi T, Homma S, Ohshima N. Calcitonin gene-related peptide in the regulation of cardiac function. Ann N Y Acad Sci. 1992 657 : 194 203.
72. Joyce CD, Fiscus RR, Wang X, Dries DJ, Morris RC, Prinz RA. Calcitonin gene-related peptide levels are elevated in patients with sepsis. Surgery. 1990 108 : 1097 1101.
73. Kopp S. Neuroendocrine, immune, and local responses related to temporomandibular disorders. J Orofac Pain. 2001 15 : 9 28.
74. Sessle BJ. New insights into peripheral chemical mediators of temporomandibular pain and inflammation. J Orofac Pain. 2001 15 : 5.
75. Byers MR. Dynamic plasticity of dental sensory nerve structure and cytochemistry. Arch Oral Biol. 1994 39 (Suppl 13S 21S.
76. Belmonte C, Acosta MC, Gallar J. Neural basis of sensation in intact and injured corneas. Exp Eye Res. 2004 78 : 513 525.
77. Hay DL, Poyner DR, Sexton PM. GPCR modulations by RAMPs. Pharmacol Ther. 2006 109 : 173 197.