Systemic cannabinoids produce CB1-mediated antinociception by activation of descending serotonergic pathways that act upon spinal 5-HT7 and 5-HT2A receptors

European Journal of Pharmacology

Volumn 649, Issue 1-3, 2010, Pages 183-194

  Seyrek, Melik ^a   Kahraman, Serdar ^a   Deveci, Mehmet Salih ^a   Yesilyurt, Ozgur ^a   Dogrul, Ahmet ^a  

^a GULHANE SCHOOL OF MEDICINE   (Turkey)

Author keywords

5 HT2A receptor; 5 HT7 receptor; Analgesia; Cannabinoid; Pain; Serotonin

Indexed keywords

1 (2,3 DICHLOROBENZOYL) 5 METHOXY 2 METHYL 3 (2 MORPHOLINOETHYL)INDOLE; 2,3 DIHYDRO 5 METHYL 3 (MORPHOLINOMETHYL) 6 (1 NAPHTHOYL)PYRROLO[1,2,3 DE][1,4]BENZOXAZINE; 3 [2 [2 (4 METHYL 1 PIPERIDINYL)ETHYL] 1 PYRROLIDINESULFONYL]PHENOL; 5,7 DIHYDROXYTRYPTAMINE; ARACHIDONYL 20 CHLOROETHYLAMIDE; CANNABINOID 1 RECEPTOR AGONIST; KETANSERIN; N [2 [4 (2 METHOXYPHENYL) 1 PIPERAZINYL]ETHYL] N (2 PYRIDYL)CYCLOHEXANECARBOXAMIDE; ONDANSETRON; RIMONABANT; RISPERIDONE; SEROTONIN 1A RECEPTOR; SEROTONIN 2A RECEPTOR; SEROTONIN 3A RECEPTOR; SEROTONIN 7 RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANTINOCICEPTION; ARTICLE; CONTROLLED STUDY; DOSE RESPONSE; DOSE TIME EFFECT RELATION; DRUG EFFECT; DRUG EFFICACY; DRUG MECHANISM; DRUG RECEPTOR BINDING; HOT PLATE TEST; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SEROTONINERGIC NERVE CELL; SEROTONINERGIC SYSTEM; TAIL FLICK TEST; VENTRAL ROOT;

ANALGESICS, NON-NARCOTIC; ANIMALS; CANNABINOIDS; DOSE-RESPONSE RELATIONSHIP, DRUG; HOT TEMPERATURE; MALE; MICE; MICE, INBRED BALB C; NERVE TISSUE PROTEINS; NEURONS; PAIN MEASUREMENT; PROTEIN ISOFORMS; RECEPTOR, CANNABINOID, CB1; RECEPTOR, CANNABINOID, CB2; RECEPTOR, SEROTONIN, 5-HT2A; RECEPTORS, SEROTONIN; SEROTONIN AGENTS; SEROTONIN ANTAGONISTS; SPINAL CORD; SYNAPTIC TRANSMISSION;

EID: 78049307519     PISSN: 00142999     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejphar.2010.09.039     Document Type: Article

References (62)

1. Bambico F.R., Katz N., Debonnel G., Gobbi G. Cannabinoids elicit antidepressant-like behavior and activate serotonergic neurons through the medial prefrontal cortex. J. Neurosci. 2007, 27:11700-11711.
2. Basbaum A.I., Fields H.L. The origin of descending pathways in the dorsolateral funiculus of the spinal cord of the cat and rat: further studies on the anatomy of pain modulation. J. Comp. Neurol. 1979, 187:513-531.
3. Braz J.M., Basbaum A.I. Genetically expressed transneuronal tracer reveals direct and indirect serotonergic descending control circuits. J. Comp. Neurol. 2008, 507:1990-2003.
4. Brenchat A., Romero L., García M., Pujol M., Burgueño J., Torrens A., Hamon M., Baeyens J.M., Buschmann H., Zamanillo D., Vela J.M. 5-HT7 receptor activation inhibits mechanical hypersensitivity secondary to capsaicin sensitization in mice. Pain 2009, 141:239-247.
5. Chen Y.P., Chen S.R., Pan H.L. Systemic morphine inhibits dorsal horn projection neurons through spinal cholinergic system independent of descending pathways. J. Pharmacol. Exp. Ther. 2005, 314:611-617.
6. Chin C.L., Tovcimak A.E., Hradil V.P., Seifert T.R., Hollingsworth P.R., Chandran P., Zhu C.Z., Zhong C., Ryther K., Gallagher M.E., Chin C.L., Tovcimak A.E., Hradil V.P., Fox G.B., Dart M.J., Honore P., Meyer M.D. Differential effects of cannabinoid receptor agonists on regional brain activity using pharmacological MRI. Br. J. Pharmacol. 2008, 153:367-379.
7. Dableh L.J., Yashpal K., Henry J.L. Physiological evidence of a postsynaptic inhibition of the tail flick reflex by a cannabinoid receptor agonist. Eur J Pharmacol. 2009, 602:36-40.
8. Dogrul A., Gardell L.R., Ma S., Ossipov M.H., Porreca F., Lai J. Knock-down of spinal CB1 receptors produces abnormal pain and elevates spinal dynorphin content in mice. Pain 2000, 100:203-209.
9. Dogrul A., Gul H., Akar A., Yildiz O., Bilgin F., Guzeldemir E. Topical cannabinoid antinociception: synergy with spinal sites. Pain 2003, 105:11-16.
10. Dogrul A., Gul H., Yildiz O., Bilgin F., Guzeldemir M.E. Cannabinoids blocks tactile allodynia in diabetic mice without attenuation of its antinociceptive effect. Neurosci. Lett. 2004, 368:82-86.
11. Dogrul A., Ossipov M.H., Porreca F. Differential mediation of descending pain facilitation and inhibition by spinal 5HT-3 and 5HT-7 receptors. Brain Res. 2009, 1280:52-59.
12. Dogrul A., Seyrek M. Systemic morphine produce antinociception mediated by spinal 5-HT7, but not 5-HT1A and 5-HT2 receptors in the spinal cord. Br. J. Pharmacol. 2006, 149:498-505.
13. Doly S., Fischer J., Brisorgueil M.J., Verge D., Conrath M. Pre- and postsynaptic localization of the 5-HT7 receptor in rat dorsal spinal cord: immunocytochemical evidence. J. Comp. Neurol. 2005, 26:256-269.
14. Doly S., Madeira A., Fischer J., Brisorgueil M.J., Daval G., Bernard R., Vergé D., Conrath M. The 5-HT2A receptor is widely distributed in the rat spinal cord and mainly localized at the plasma membrane of postsynaptic neurons. J. Comp. Neurol. 2004, 472:496-511.
15. Egashira N., Matsuda T., Koushi E., Higashihara F., Mishima K., Chidori S., Hasebe N., Iwasaki K., Nishimura R., Oishi R., Fujiwara M. Delta(9)-tetrahydrocannabinol prolongs the immobility time in the mouse forced swim test: involvement of cannabinoid CB(1) receptor and serotonergic system. Eur. J. Pharmacol. 2008, 589:117-121.
16. Finn D.P., Jhaveri M.D., Beckett S.R., Roe C.H., Kendall D.A., Marsden C.A., Chapman V. Effects of direct periaqueductal grey administration of a cannabinoid receptor agonist on nociceptive and aversive responses in rats. Neuropharmacology 2003, 45:594-604.
17. Forbes I.T., Douglas S., Gribble A.D., Ife R.J., Lightfoot A.P., Garner A.E., Riley G.J., Jeffrey P., Stevens A.J., Stean T.O., Thomas D.R. SB-656104-A: a novel 5-HT7 receptor antagonist with improved in vivo properties. Bioorg. Med. Chem. Lett. 2002, 12:3341-3344.
18. Forster E.A., Cliffe I.A., Bill D.J., Dover G.M., Jones D., Reilly Y., Fletcher A. A pharmacological profile of the selective silent 5-HT1A receptor antagonist, WAY-100635. Eur. J. Pharmacol. 1995, 281:81-88.
19. Freeman A.J., Cunningham K.T., Tyers M.B. Selectivity of 5-HT3 receptor antagonists and anti-emetic mechanisms of action. Anticancer Drugs 1992, 3:79-85.
20. Gardell L.R., Burgess S.E., Dogrul A., Ossipov M.H., Malan T.P., Lai J., Porreca F. Pronociceptive effects of spinal dynorphin promote cannabinoid-induced pain and antinociceptive tolerance. Pain 2002, 98:79-88.
21. Garzón J., de la Torre-Madrid E., Rodríguez-Muñoz M., Vicente-Sánchez A., Sánchez-Blázquez P. Gz mediates the long-lasting desensitization of brain CB1 receptors and is essential for cross-tolerance with morphine. Mol. Pain 2009, 5:11.
22. Hagan J.J., Price G.W., Jeffrey P., Deeks N.J., Stean T., Piper D., Smith M.I., Upton N., Medhurst A.D., Middlemiss D.N., Riley G.J., Lovell P.J., Bromidge S.M., Thomas D.R. Characterization of SB-269970-A, a selective 5-HT7 receptor antagonist. Br. J. Pharmacol. 2000, 130:539-548.
23. Häring M., Marsicano G., Lutz B., Monory K. Identification of the cannabinoid receptor type 1 in serotonergic cells of raphe nuclei in mice. Neuroscience 2007, 146:1212-1219.
24. Heinricher M.M., Tavares I., Leithe J.L., Lumb B.M. Descending control of nociception: specificity, recruitment and plasticity. Brain Res. Rev. 2009, 60:214-225.
25. Hillard C.J., Manna S., Greenberg M.J., Dicamelli R., Ross R.A., Stevenson L.A., Murphy V., Pertwee R.G., Campbell W.B. Synthesis and characterization of potent and selective agonists of the neuronal cannabinoid receptor (CB1). J. Pharmacol. Exp. Ther. 1999, 289:1427-1433.
26. Hohmann A.G., Suplita R.L. Endocannabinoid mechanisms of pain modulation. AAPS J. 2006, 8:693-708.
27. Hung K.C., Wu H.E., Mizoguchi H., Leiterman R., Tseng L.F. Intrathecal treatment with 6-hydroxydopmine block the antinociception induced by endomorphin-1 and endomorphin-2 given intracerebroventricularly in the mouse. J. Pharmacol. Sci. 2003, 93:299-306.
28. Hylden J.L., Wilcox G.L. Intrathecal morphine in mice: a new technique. Eur. J. Pharmacol. 1980, 17:313-316.
29. Ibrahim M.M., Rude M.L., Stagg N.J., Mata H.P., Lai J., Vanderah T.W., Porreca F., Buckley N.E., Makriyannis A., Malan T.P. CB2 cannabinoid receptor mediation of antinociception. Pain 2006, 122:36-42.
30. Knight J.A., Smith C., Toohey N., Klein M.T., Teitler M. Pharmacological analysis of the novel, rapid, and potent inactivation of the human 5-Hydroxytryptamine7 receptor by risperidone, 9-OH-Risperidone, and other inactivating antagonists. Mol. Pharmacol. 2009, 75:374-380.
31. Lau T., Schloss P. The cannabinoid CB1 receptor is expressed on serotonergic and dopaminergic neurons. Eur. J. Pharmacol. 2008, 578:137-141.
32. Lichtman A.H., Martin B.R. Spinal and supraspinal components of cannabinoid-induced antinociception. J. Pharmacol. Exp. Ther. 1991, 258:517-523.
33. Liu F.Y., Xing G.G., Qu X.X., Xu I.S., Han J.S., Wan Y. Roles of 5-hydroxytryptamine (5-HT) receptor subtypes in the inhibitory effects of 5-HT on C-fiber responses of spinal wide dynamic range neurons in rats. J. Pharmacol. Exp. Ther. 2007, 321:1046-1053.
34. Liu R.J., Zhang R.X., Qiao J.T., Dafny N. Interrelations of opioids with monoamines in descending inhibition of nociceptive transmission at the spinal level: an immunocytochemical study. Brain Res. 1999, 830:183-190.
35. Lovell P.J., Bromidge S.M., Dabbs S., Duckworth D.M., Forbes I.T., Jennings A.J., King F.D., Middlemiss D.N., Rahman S.K., Saunders D.V., Collin L.L., Hagan J.J., Riley G.J., Thomas D.R. A novel, potent, and selective 5-HT(7) antagonist: (R)-3-(2-(2-(4-methylpiperidin-1-yl)ethyl)pyrrolidine-1-sulfonyl) phenol (SB-269970). J. Med. Chem. 2000, 43:342-345.
36. Mallet C., Daulhac L., Bonnefont J., Ledent C., Etienne M., Chapuy E., Libert F., Eschalier A. Endocannabinoid and serotonergic systems are needed for acetaminophen-induced analgesia. Pain 2008, 139:190-200.
37. Martin W.J., Lai N.K., Patrick S.L., Tsou K., Walker J.M. Antinociceptive actions of cannabinoids following intraventricular administration in rats. Brain Res. 1993, 629:300-304.
38. Martin W.J., Patrick S.L., Coffin P.O., Tsou K., Walker J.M. An examination of the central sites of action of cannabinoid-induced antinociception in the rat. Life Sci. 1995, 56:2103-2109.
39. Martin W.J., Tsou K., Walker J.M. Cannabinoid receptor-mediated inhibition of the rat tail-flick reflex after microinjection into the rostral ventromedial medulla. Neurosci. Lett. 1998, 242:33-36.
40. Meng I.D., Manning B.H., Martin W.J., Fields H.L. An analgesia circuit activated by cannabinoids. Nature 1998, 395:381-383.
41. Meuser T., Pietruck C., Gabriel A., Xie G.X., Lim K.J., Palmer P. 5-HT7 receptors are involved in mediating 5-HT induced activation of rat primary afferent neurons. Life Sci. 2002, 7:2279-2289.
42. Millan M.J. Descending control of pain. Prog. Neurobiol. 2002, 66:355-474.
43. Nasrallah H.A. Atypical antipsychotic-induced metabolic side effects: insights from receptor-binding profiles. Mol. Psychiatry 2008, 13:27-35.
44. Noga B.R., Johnson D.M., Riesgo M.I., Pinzon A. Locomotor-activated neurons of the cat.I. Serotonergic innervation and co-localization of 5-HT7, 5-HT2A, and 5-HT1A receptors in the thoraco-lumbar spinal cord. J. Neurophysiol. 2009, 102:1560-1576.
45. Oatway M.A., Chen Y., Weaver L.C. The 5-HT3 receptor facilitates at-level mechanical allodynia following spinal cord injury. Pain 2004, 110:259-268.
46. Oyama T., Ueda M., Kuraishi Y., Akaike A., Satoh M. Dual effect of serotonin on formalin-induced nociception in the rat spinal cord. Neurosci. Res. 1996, 25:129-135.
47. Palazzo E., De Novellis V., Petrosino S., Marabese I., Vita D., Giordano C., Di Marzo V., Mangoni G.S., Rossi F., Maione S. Neuropathic pain and the endocannabinoid system in the dorsal raphe: pharmacological treatment and interactions with the serotonergic system. Eur. J. Neurosci. 2006, 24:2011-2020.
48. Pertwee R.G. The pharmacology of cannabinoid receptors and their ligands: an overview. Int. J. Obes. (Lond) 2006, 30:13-18.
49. Sain N.M., Liang A., Kane S.A., Urban M.O. Antinociceptive effects of the non-selective cannabinoid receptor agonist CP 55, 940 are absent in CB1(-/-) and not CB2(-/-) mice in models of acute and persistent pain. Neuropharmacology 2009, 57:235-241.
50. Secher A., Husum H., Holst B., Egerod K.L., Mellerup E. Risperidone treatment increases CB(1) receptor binding in rat brain. Neuroendocrinology 2010, 91:155-168.
51. Smith C., Rahman T., Toohey N., Mazurkiewicz J., Herrick-Davis K., Teitler M. Risperidone irreversibly binds to and inactivates the 5-HT7 serotonin receptor. Mol. Pharmacol. 2006, 70:1264-1270.
52. Song B., Chen W., Marvizón J.C. Inhibition of opioid release in the rat spinal cord by serotonin 5-HT(1A) receptors. Brain Res. 2007, 1158:57-62.
53. Steenwinckel J.V., Noghero A., Thibault K., Brisorgueil M.J., Fische J., Conrath M. The 5-HT2A receptor is mainly expressed in nociceptive sensory neurons in rat lumbar dorsal root ganglia. Neuroscience 2009, 161:838-846.
54. Svízenská I., Dubovỳ P., Sulcová A. Cannabinoid receptors 1 and 2 (CB1 and CB2), their distribution, ligands and functional involvement in nervous system structure-a short review. Pharmacol. Biochem. Behav. 2008, 90:501-511.
55. Toohey N., Klein M.T., Knight J., Smith C., Teitler M. Human 5-HT7 receptor-induced inactivation of forskolin-stimulated adenylate cyclase by risperidone, 9-OH-risperidone and other "inactivating antagonists". Mol. Pharmacol. 2009, 76:552-559.
56. Valenzano K.J., Tafesse L., Lee G., Harrison J.E., Boulet J.M., Gottshall S.L., Mark L., Pearson M.S., Miller W., Shan S., Rabadi L., Rotshteyn Y., Chaffer S.M., Turchin P.I., Elsemore D.A., Toth M., Koetzner L., Whiteside G.T. Pharmacological and pharmacokinetic characterization of the cannabinoid receptor 2 agonist, GW405833, utilizing rodent models of acute and chronic pain, anxiety, ataxia and catalepsy. Neuropharmacology 2005, 48:658-672.
57. Walker J.M., Huang S.M. Cannabinoid analgesia. Pharmacol. Ther. 2002, 95:127-135.
58. Wang Y.Y., Wei Y.Y., Huang J., Wang W., Tamamaki N., Li Y.Q., Wu S.X. Expression patterns of 5-HT receptor subtypes 1A and 2A on GABAergic neurons within the spinal dorsal horn of GAD67-GFP knock-in mice. J. Chem. Neuroanat. 2009, 38:75-81.
59. Whiteside G.T., Lee G.P., Valenzano K.J. The role of the cannabinoid CB2 receptor in pain transmission and therapeutic potential of small molecule CB2 receptor agonists. Curr. Med. Chem. 2007, 14:917-936.
60. Xie H., Dong Z.Q., Ma F., Bauer W.R., Wang X., Wu G.C. Involvement of serotonin 2A receptors in the analgesic effect of tramadol in mono-arthritic rats. Brain Res. 2008, 1210:76-83.
61. Yanarates O., Dogrul A., Yildirim V., Sahin A., Sizlan A., Seyrek M., Akgul O., Kozak O., Kurt E., Aypar U. Spinal 5-HT7 receptors play an important role in the antinociceptive and antihyperalgesic effects of tramadol and its metabolite, o-desmethyltramadol, via activation of descending serotonergic pathways. Anesthesiology 2010, 112:696-710.
62. Zimmermann M. Ethical guidelines for investigations of experimental pain in conscious animals. Pain 1983, 16:109-110.