Gi-protein-coupled 5-HT1B/D receptor agonist sumatriptan induces type i hyperalgesic priming

Pain

Volumn 157, Issue 8, 2016, Pages 1773-1782

  Araldi, Dioneia ^a   Ferrari, Luiz F ^a   Levine, Jon D ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

5 HT 1B receptor; 5 HT 1D receptor; Chronic pain; GPCRs; Hyperalgesia; Hyperalgesic priming; Triptans

Indexed keywords

3 [2 [2 (4 METHYL 1 PIPERIDINYL)ETHYL] 1 PYRROLIDINESULFONYL]PHENOL; 3 [4 (3 CHLOROPHENYL) 1 PIPERAZINYL] 1,1 DIPHENYL 2 PROPANOL; CORDYCEPIN; ISOLECTIN B4; NAS 181; PERTUSSIS TOXIN; PROSTAGLANDIN E2; PROTEIN KINASE C EPSILON; SAPORIN; SEROTONIN 1B RECEPTOR; SEROTONIN 1D RECEPTOR; SEROTONIN ANTAGONIST; SUMATRIPTAN SUCCINATE; UNCLASSIFIED DRUG; RIBOSOME INACTIVATING PROTEIN 1; SEROTONIN 1 AGONIST; SUMATRIPTAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; FEMALE; MALE; MECHANICAL HYPERALGESIA; NONHUMAN; PAIN RECEPTOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SEX DIFFERENCE; TYPE I HYPERALGESIA PRIMING; ANIMAL; CHEMICALLY INDUCED; CHRONIC PAIN; DRUG EFFECTS; HYPERALGESIA; PAIN THRESHOLD; PATHOPHYSIOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; CHRONIC PAIN; FEMALE; HYPERALGESIA; MALE; NOCICEPTORS; PAIN THRESHOLD; RATS; RATS, SPRAGUE-DAWLEY; RIBOSOME INACTIVATING PROTEINS, TYPE 1; SEROTONIN 5-HT1 RECEPTOR AGONISTS; SUMATRIPTAN;

EID: 84979696898     PISSN: 03043959     EISSN: 18726623     Source Type: Journal    
DOI: 10.1097/j.pain.0000000000000581     Document Type: Article

References (96)

1. Ahn AH, BasbaumAI. Where do triptans act in the treatment of migraine? PAIN 2005;115:1-4
2. Aley KO, Levine JD. Role of protein kinase A in the maintenance of inflammatory pain. J Neurosci 1999;19:2181-6
3. Aley KO, Martin A, McMahon T, Mok J, Levine JD, Messing RO. Nociceptor sensitization by extracellular signal-regulated kinases. J Neurosci 2001;21:6933-9
4. AleyKO,MessingRO,Mochly-Rosen D, Levine JD.Chronic hypersensitivity for inflammatory nociceptor sensitization mediated by the epsilon isozyme of protein kinase C. J Neurosci 2000;20:4680-5
5. Amrutkar DV, Ploug KB, 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 generelated peptide in the rat trigeminovascular system. Pain 2012;153: 830-8
6. Angst MS, Clark JD. Opioid-induced hyperalgesia a qualitative systematic review. Anesthesiology 2006;104:570-87
7. Araldi D, Ferrari LF, Levine JD. Repeated mu-opioid exposure induces a novel form of the hyperalgesic priming model for transition to chronic pain. J Neurosci 2015;35:12502-17
8. Araldi D, Ferrari LF, Levine JD. Adenosine-A1 receptor agonist induced hyperalgesic priming type II. PAIN 2016;157:698-709
9. Becerra L, Bishop J, Barmettler G, Xie Y, Navratilova E, Porreca F, Borsook D. Triptans disrupt brain networks and promote stress-induced CSD-like responses in cortical and subcortical areas. J Neurophysiol 2016;115:208-17
10. Bigal ME, Lipton RB. Excessive acute migraine medication use and migraine progression. Neurology 2008;71:1821-8
11. Bigal ME, Lipton RB. Overuse of acute migraine medications and migraine chronification. Curr Pain Headache Rep 2009;13:301-7
12. BogenO, Alessandri-Haber N, ChuC,Gear RW, Levine JD. Generation of a pain memory in the primary afferent nociceptor triggered by PKCepsilon activation of CPEB. J Neurosci 2012;32:2018-26
13. Bonaventure P, Voorn P, Luyten WH, Leysen JE. 5HT1B and 5HT1D receptor mRNA differential co-localization with peptide mRNA in the guinea pig trigeminal ganglion. Neuroreport 1998;9:641-5
14. Borle AB, Snowdowne KW. Measurement of intracellular free calcium in monkey kidney cells with aequorin. Science 1982;217:252-4
15. Bruinvels AT, Landwehrmeyer B, Gustafson EL, Durkin MM, Mengod G, Branchek TA, Hoyer D, Palacios JM. Localization of 5-HT1B, 5-HT1D alpha, 5-HT1E and 5-HT1F receptor messenger RNA in rodent and primate brain. Neuropharmacology 1994;33:367-86
16. Burch RM, Axelrod J. Dissociation of bradykinin-induced prostaglandin formation from phosphatidylinositol turnover in Swiss 3T3 fibroblasts: evidence forGprotein regulation of phospholipase A2. Proc Natl Acad Sci U S A 1987;84:6374-8
17. Burstein R, Jakubowski M. Analgesic triptan action in an animal model of intracranial pain a race against the development of central sensitization. Ann Neurol 2004;55:27-36
18. Burstein R, Levy D, Jakubowski M. Effects of sensitization of trigeminovascular neurons to triptan therapy during migraine. Rev Neurol (Paris) 2005;161:658-60
19. Burstein R, Yarnitsky D, Goor-Aryeh I, Ransil BJ, Bajwa ZH. An association between migraine and cutaneous allodynia. Ann Neurol 2000;47:614-24
20. Carson L, Lewis D, Tsou M, McGuire E, Surran B, Miller C, Vu TA. Abdominal migraine an under-diagnosed cause of recurrent abdominal pain in children. Headache 2011;51:707-12
21. Chen L, Malarick C, Seefeld L, Wang S, Houghton M, Mao J. Altered quantitative sensory testing outcome in subjects with opioid therapy. PAIN 2009;143:65-70
22. Choi JI, Koehrn FJ, Sorkin LS. Carrageenan induced phosphorylation of Akt is dependent on neurokinin-1 expressing neurons in the superficial dorsal horn. Mol Pain 2012;8:4
23. Chu LF, Angst MS, Clark D. Opioid-induced hyperalgesia in humans: molecular mechanisms and clinical considerations. Clin J Pain 2008;24: 479-96
24. Classey JD, Bartsch T, Goadsby PJ. Distribution of 5-HT(1B), 5-HT(1D) and 5-HT(1F) receptor expression in rat trigeminal and dorsal root ganglia neurons: relevance to the selective anti-migraine effect of triptans. Brain Res 2010;1361:76-85
25. Dahlof CG, Dodick D, Dowson AJ, Pascual J. How does almotriptan compare with other triptans? A review of data from placebo-controlled clinical trials. Headache 2002;42:99-113
26. De Felice M, Ossipov MH, Wang R, Dussor G, Lai J, Meng ID, Chichorro J, Andrews JS, Rakhit S, Maddaford S, Dodick D, Porreca F. Triptaninduced enhancement of neuronal nitric oxide synthase in trigeminal ganglion dural afferents underlies increased responsiveness to potential migraine triggers. Brain 2010;133(pt 8):2475-88
27. De Felice M, Ossipov MH, Wang R, Lai J, Chichorro J, Meng I, Dodick DW, Vanderah TW, Dussor G, Porreca F. Triptan-induced latent sensitization a possible basis for medication overuse headache. Ann Neurol 2010;67:325-37
28. Diener HC, Limmroth V. Medication-overuse headache a worldwide problem. Lancet Neurol 2004;3:475-83
29. Dina OA, Khasar SG, Gear RW, Levine JD. Activation of Gi induces mechanical hyperalgesia poststress or inflammation. Neuroscience 2009;160:501-7
30. Ferrari LF, Bogen O, Chu C, Levine JD. Peripheral administration of translation inhibitors reverses increased hyperalgesia in a model of chronic pain in the rat. J Pain 2013;14:731-8
31. Ferrari LF, Bogen O, Levine JD. Second messengers mediating the expression of neuroplasticity in a model of chronic pain in the rat. J Pain 2014;15:312-20
32. Ferrari LF, Bogen O, Reichling DB, Levine JD. Accounting for the delay in the transition from acute to chronic pain axonal and nuclear mechanisms. J Neurosci 2015;35:495-507
33. Ferrari LF, Levine E, Levine JD. Role of a novel nociceptor autocrine mechanism in chronic pain. Eur J Neurosci 2013;37:1705-13
34. Ferrari LF, Levine JD. Plasma membrane mechanisms in a preclinical rat model of chronic pain. J Pain 2015;16:60-6
35. Ferrari MD, Goadsby PJ, Roon KI, Lipton RB. Triptans (serotonin, 5-HT1B/1D agonists) in migraine: detailed results and methods of a metaanalysis of 53 trials. Cephalalgia 2002;22:633-58
36. Ferrari MD, Roon KI, Lipton RB, Goadsby PJ. Oral triptans (serotonin 5-HT(1B/1D) agonists) in acute migraine treatment a meta-analysis of 53 trials. Lancet 2001;358:1668-75
37. Gerhardt CC, van Heerikhuizen H. Functional characteristics of heterologously expressed 5-HT receptors. Eur J Pharmacol 1997;334:1-23
38. Ghiotto N, Sances G, Galli F, Tassorelli C, Guaschino E, Sandrini G, Nappi G. Medication overuse headache and applicability of the ICHD-II diagnostic criteria: 1-year follow-up study (CARE I protocol). Cephalalgia 2009;29:233-43
39. Goadsby PJ. The pharmacology of headache. Prog Neurobiol 2000;62: 509-25
40. Goadsby PJ, Lipton RB, Ferrari MD. Migraine-current understanding and treatment. N Engl J Med 2002;346:257-70
41. Green AL, Gu P, De Felice M, Dodick D, Ossipov MH, Porreca F. Increased susceptibility to cortical spreading depression in an animal model of medication-overuse headache. Cephalalgia 2013;34:594-604
42. Hamblin MW, Metcalf MA. Primary structure and functional characterization of a human 5-HT1D-type serotonin receptor. Mol Pharmacol 1991;40:143-8
43. Hargreaves RJ, Shepheard SL. Pathophysiology of migraine-new insights. Can J Neurol Sci 1999;26(suppl 3):S12-19
44. Hay JL, White JM, Bochner F, Somogyi AA, Semple TJ, Rounsefell B. Hyperalgesia in opioid-managed chronic pain and opioid-dependent patients. J Pain 2009;10:316-22
45. Headache Classification Committee, Olesen J, Bousser MG, Diener HC, Dodick D, First M, Goadsby PJ, Gobel H, Lainez MJ, Lance JW, Lipton RB, Nappi G, Sakai F, Schoenen J, Silberstein SD, Steiner TJ. New appendix criteria open for a broader concept of chronic migraine. Cephalalgia 2006;26:742-6
46. 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;909:112-20
47. Humphrey PP. The discovery of a new drug class for the acute treatment of migraine. Headache 2007;47(suppl 1):S10-19
48. Johnson JA, Gray MO, Chen CH, Mochly-Rosen D. A protein kinase C translocation inhibitor as an isozyme-selective antagonist of cardiac function. J Biol Chem 1996;271:24962-6
49. Johnston MM, Rapoport AM. Triptans for the management of migraine. Drugs 2010;70:1505-18
50. Joseph EK, BogenO, Alessandri-Haber N, Levine JD. PLC-beta 3 signals upstream of PKC epsilon in acute and chronic inflammatory hyperalgesia. PAIN 2007;132:67-73
51. Joseph EK, Chen X, Bogen O, Levine JD. Oxaliplatin acts on IB4-positive nociceptors to induce an oxidative stress-dependent acute painful peripheral neuropathy. J Pain 2008;9:463-72
52. Joseph EK, Levine JD. Hyperalgesic priming is restricted to isolectin B4-positive nociceptors. Neuroscience 2010;169:431-5
53. Joseph EK, Parada CA, Levine JD. Hyperalgesic priming in the rat demonstrates marked sexual dimorphism. PAIN 2003;105:143-50
54. Kakisaka Y, Wakusawa K, Haginoya K, Uematsu M, Tsuchiya S. Abdominal migraine associated with ecchymosis of the legs and buttocks: does the symptom imply an unknown mechanism of migraine? Tohoku J Exp Med 2010;221:49-51
55. Kayser V, Aubel B, Hamon M, Bourgoin S. The antimigraine 5-HT 1B/1D receptor agonists, sumatriptan, zolmitriptan and dihydroergotamine, attenuate pain-related behaviour in a rat model of trigeminal neuropathic pain. Br J Pharmacol 2002;137:1287-97
56. Khasabov SG, Rogers SD, Ghilardi JR, Peters CM, Mantyh PW, Simone DA. Spinal neurons that possess the substance P receptor are required for the development of central sensitization. J Neurosci 2002;22:9086-98
57. Khasar SG, Burkham J, Dina OA, Brown AS, Bogen O, Alessandri-Haber N, Green PG, Reichling DB, Levine JD. Stress induces a switch of intracellular signaling in sensory neurons in a model of generalized pain. J Neurosci 2008;28:5721-30
58. Khasar SG, Lin YH, Martin A, Dadgar J, McMahon T, Wang D, Hundle B, Aley KO, Isenberg W, McCarter G, Green PG, Hodge CW, Levine JD, Messing RO. A novel nociceptor signaling pathway revealed in protein kinase C epsilon mutant mice. Neuron 1999;24:253-60
59. Kras JV, Weisshaar CL, Pall PS, Winkelstein BA. Pain from intra-articular NGF or joint injury in the rat requires contributions from peptidergic joint afferents. Neurosci Lett 2015;604:193-8
60. Lee M, Silverman SM, Hansen H, Patel VB, Manchikanti L. A comprehensive review of opioid-induced hyperalgesia. Pain Physician 2011;14:145-61
61. Ma QP, Hill R, Sirinathsinghji D. Colocalization of CGRP with 5-HT1B/1D receptors and substance P in trigeminal ganglion neurons in rats. Eur J Neurosci 2001;13:2099-104
62. Mantyh PW, Rogers SD, Honore P, Allen BJ, Ghilardi JR, Li J, Daughters RS, Lappi DA, Wiley RG, Simone DA. Inhibition of hyperalgesia by ablation of lamina I spinal neurons expressing the substance P receptor. Science 1997;278:275-9
63. Mao J. Opioid-induced abnormal pain sensitivity: implications in clinical opioid therapy. PAIN 2002;100:213-17
64. Maroteaux L, Saudou F, Amlaiky N, Boschert U, Plassat JL, Hen R. Mouse 5HT1B serotonin receptor: cloning, functional expression, and localization in motor control centers. Proc Natl Acad Sci U S A 1992;89: 3020-4
65. Mercadante S, Arcuri E. Hyperalgesia and opioid switching. Am J Hosp Palliat Care 2005;22:291-4
66. Nishiguchi J, Sasaki K, Seki S, Chancellor MB, Erickson KA, de Groat WC, Kumon H, Yoshimura N. Effects of isolectin B4-conjugated saporin, a targeting cytotoxin, on bladder overactivity induced by bladder irritation. Eur J Neurosci 2004;20:474-82
67. Oladosu FA, Maixner W, Nackley AG. Alternative splicing of G proteincoupled receptors: relevance to pain management. Mayo Clin Proc 2015; 90:1135-51
68. Olesen J, Burstein R, Ashina M, Tfelt-Hansen P. Origin of pain in migraine: evidence for peripheral sensitisation. Lancet Neurol 2009;8:679-90
69. Parada CA, Reichling DB, Levine JD. Chronic hyperalgesic priming in the rat involves a novel interaction between cAMP and PKCepsilon second messenger pathways. PAIN 2005;113:185-90
70. Parada CA, Yeh JJ, Joseph EK, Levine JD. Tumor necrosis factor receptor type-1 in sensory neurons contributes to induction of chronic enhancement of inflammatory hyperalgesia in rat. Eur J Neurosci 2003; 17:1847-52
71. Pierce PA, Xie GX, Levine JD, Peroutka SJ. 5-Hydroxytryptamine receptor subtype messenger RNAs in rat peripheral sensory and sympathetic ganglia a polymerase chain reaction study. Neuroscience 1996;70:553-9
72. Potrebic S, Ahn AH, Skinner K, Fields HL, Basbaum AI. Peptidergic nociceptors of both trigeminal and dorsal root ganglia express serotonin 1D receptors: implications for the selective antimigraine action of triptans. J Neurosci 2003;23:10988-97
73. Reichling DB, Levine JD. Critical role of nociceptor plasticity in chronic pain. Trends Neurosci 2009;32:611-18
74. Rios C, Gomes I, Devi LA. mu opioid and CB1 cannabinoid receptor interactions: reciprocal inhibition of receptor signaling and neuritogenesis. Br J Pharmacol 2006;148:387-95
75. Ruat M, Traiffort E, Leurs R, Tardivel-Lacombe J, Diaz J, Arrang JM, Schwartz JC. Molecular cloning, characterization, and localization of a high-affinity serotonin receptor (5-HT7) activating cAMP formation. Proc Natl Acad Sci U S A 1993;90:8547-51
76. Silberstein SD. Practice parameter: evidence-based guidelines for migraine headache (an evidence-based review): report of the Quality Standards Subcommittee of the American Academy of Neurology. Neurology 2000;55:754-62
77. Silberstein SD, Olesen J, Bousser MG, Diener HC, Dodick D, First M, Goadsby PJ, Gobel H, Lainez MJ, Lance JW, Lipton RB, Nappi G, Sakai F, Schoenen J, Steiner TJ; International Headache Society. The International Classification of Headache Disorders, 2nd Edition (ICHDII)-revision of criteria for 8.2 Medication-overuse headache. Cephalalgia 2005;25:460-5
78. Taiwo YO, Bjerknes LK, Goetzl EJ, Levine JD. Mediation of primary afferent peripheral hyperalgesia by the cAMP second messenger system. Neuroscience 1989;32:577-80
79. Taiwo YO, Heller PH, Levine JD. Mediation of serotonin hyperalgesia by the cAMP second messenger system. Neuroscience 1992;48:479-83
80. Taiwo YO, Levine JD. Prostaglandin effects after elimination of indirect hyperalgesic mechanisms in the skin of the rat. Brain Res 1989;492: 397-9
81. Taiwo YO, Levine JD. Serotonin is a directly-acting hyperalgesic agent in the rat. Neuroscience 1992;48:485-90
82. Tepper SJ, Rapoport AM, Sheftell FD. Mechanisms of action of the 5-HT1B/1D receptor agonists. Arch Neurol 2002;59:1084-8
83. Tfelt-Hansen P. Efficacy and adverse events of subcutaneous, oral, and intranasal sumatriptan used for migraine treatment a systematic review based on number needed to treat. Cephalalgia 1998;18:532-8
84. Tfelt-Hansen P, De Vries P, Saxena PR. Triptans in migraine a comparative review of pharmacology, pharmacokinetics and efficacy. Drugs 2000;60:1259-87
85. Tipton AF, Tarash I,McGuire B,Charles A, Pradhan AA. The effects of acute and preventive migraine therapies in a mouse model of chronic migraine. Cephalalgia 2015, pii: 0333102415623070. [Epub ahead of print]
86. Van Sande J, Allgeier A, Massart C, Czernilofsky A, Vassart G, Dumont JE, Maenhaut C. The human and dog 5-HT1D receptors can both activate and inhibit adenylate cyclase in transfected cells. Eur J Pharmacol 1993;247:177-84
87. Vierck CJ Jr, Kline RH, Wiley RG. Intrathecal substance p-saporin attenuates operant escape from nociceptive thermal stimuli. Neuroscience 2003;119:223-32
88. Villalon CM, Heiligers JP, Centurion D, De Vries P, Saxena PR. Characterization of putative 5-HT7 receptors mediating tachycardia in the cat. Br J Pharmacol 1997;121:1187-95
89. Vulchanova L, Olson TH, Stone LS, Riedl MS, Elde R, Honda CN. Cytotoxic targeting of isolectin IB4-binding sensory neurons. Neuroscience 2001;108:143-55
90. Wang X, Fang Y, Liang J, Yan M, Hu R, Pan X. 5-HT7 receptors are involved in neurogenic dural vasodilatation in an experimental model of migraine. J Mol Neurosci 2014;54:164-70
91. Wang X, Fang Y, Liang J, Yin Z, Miao J, Luo N. Selective inhibition of 5-HT7 receptor reduces CGRP release in an experimental model for migraine. Headache 2010;50:579-87
92. Weisshaar CL, Winkelstein BA. Ablating spinal NK1-bearing neurons eliminates the development of pain and reduces spinal neuronal hyperexcitability and inflammation from mechanical joint injury in the rat. J Pain 2014;15:378-86
93. Wiley RG, Kline RHT, Vierck CJ Jr. Anti-nociceptive effects of selectively destroying substance P receptor-expressing dorsal horn neurons using [Sar9,Met(O2)11]-substance P-saporin: behavioral and anatomical analyses. Neuroscience 2007;146:1333-45
94. Wotherspoon G, Priestley JV. Expression of the 5-HT1B receptor by subtypes of rat trigeminal ganglion cells. Neuroscience 2000;95: 465-71
95. Zgombick JM, Borden LA, Cochran TL, Kucharewicz SA, Weinshank RL, Branchek TA. Dual coupling of cloned human 5-hydroxytryptamine1D alpha and 5-hydroxytryptamine1D beta receptors stably expressed in murine fibroblasts: inhibition of adenylate cyclase and elevation of intracellular calcium concentrations via pertussis toxin-sensitive G protein(s). Mol Pharmacol 1993;44:575-82
96. Zgombick JM, Weinshank RL, Macchi M, Schechter LE, Branchek TA, Hartig PR. Expression and pharmacological characterization of a canine 5-hydroxytryptamine1D receptor subtype. Mol Pharmacol 1991;40: 1036-42