Functional characterization and analgesic effects of mixed cannabinoid receptor/T-type channel ligands

Molecular Pain

Volumn 7, Issue , 2011, Pages

  You, Haitao ^a   Gadotti, Vinicius M ^a   Petrov, Ravil R ^b   Zamponi, Gerald W ^a   Diaz, Philippe ^b  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF MONTANA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANALGESIC AGENT; CALCIUM CHANNEL T TYPE; CANNABINOID 1 RECEPTOR; CANNABINOID 1 RECEPTOR AGONIST; CANNABINOID 2 RECEPTOR; CANNABINOID 2 RECEPTOR AGONIST; FORMALDEHYDE; NMP 139; NMP 140; NMP 141; NMP 144; NMP 4; NMP 7; SEROTONIN 2A RECEPTOR; SEROTONIN 2C RECEPTOR; UNCLASSIFIED DRUG; CARBAZOLE DERIVATIVE; CARBOLINE DERIVATIVE; LIGAND; NMP144 COMPOUND; NMP4 COMPOUND; NMP7 COMPOUND;

ANALGESIC ACTIVITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BINDING COMPETITION; CALCIUM CURRENT; CELL STRAIN HEK293; CHO CELL; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOSE RESPONSE; DRUG POTENCY; DRUG RECEPTOR BINDING; DRUG SCREENING; DRUG SELECTIVITY; DRUG STRUCTURE; DRUG SYNTHESIS; HUMAN; HUMAN CELL; IC 50; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATORY PAIN; MALE; MOUSE; NEUROGENIC PAIN; NOCICEPTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PAIN; PRIORITY JOURNAL; RADIOASSAY; RAT; RESPONSE TIME; STEADY STATE; TRANSIENT EXPRESSION; VOLTAGE CLAMP; WHOLE CELL; ANIMAL; CRICETULUS; DRUG ANTAGONISM; HAMSTER; METABOLISM;

ANALGESICS; ANIMALS; CALCIUM CHANNELS, T-TYPE; CARBAZOLES; CARBOLINES; CHO CELLS; CRICETINAE; CRICETULUS; HEK293 CELLS; HUMANS; LIGANDS; RATS; RECEPTOR, CANNABINOID, CB1; RECEPTOR, CANNABINOID, CB2;

EID: 81155151486     PISSN: None     EISSN: 17448069     Source Type: Journal    
DOI: 10.1186/1744-8069-7-89     Document Type: Article

References (54)

1. Pertwee RG, Howlett AC, Abood ME, Alexander SP, Di Marzo V, Elphick MR, Greasley PJ, Hansen HS, Kunos G, Mackie K, et al. International Union of Basic and Clinical Pharmacology. LXXIX. Cannabinoid receptors and their ligands: beyond CB and CB. Pharmacol Rev 2010, 62:588-631. 10.1124/pr.110.003004, 21079038.
2. Matsuda LA, Lolait SJ, Brownstein MJ, Young AC, Bonner TI. Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature 1990, 346:561-564. 10.1038/346561a0, 2165569.
3. Munro S, Thomas KL, Abu-Shaar M. Molecular characterization of a peripheral receptor for cannabinoids. Nature 1993, 365:61-65. 10.1038/365061a0, 7689702.
4. Henry DJ, Chavkin C. Activation of inwardly rectifying potassium channels (GIRK1) by co-expressed rat brain cannabinoid receptors in Xenopus oocytes. Neurosci Lett 1995, 186:91-94. 10.1016/0304-3940(95)11289-9, 7777206.
5. Mackie K, Lai Y, Westenbroek R, Mitchell R. Cannabinoids activate an inwardly rectifying potassium conductance and inhibit Q-type calcium currents in AtT20 cells transfected with rat brain cannabinoid receptor. J Neurosci 1995, 15:6552-6561.
6. McAllister SD, Griffin G, Satin LS, Abood ME. Cannabinoid receptors can activate and inhibit G protein-coupled inwardly rectifying potassium channels in a xenopus oocyte expression system. J Pharmacol Exp Ther 1999, 291:618-626.
7. Mackie K, Hille B. Cannabinoids inhibit N-type calcium channels in neuroblastoma-glioma cells. Proc Natl Acad Sci USA 1992, 89:3825-3829. 10.1073/pnas.89.9.3825, 525583, 1315042.
8. Felder CC, Joyce KE, Briley EM, Mansouri J, Mackie K, Blond O, Lai Y, Ma AL, Mitchell RL. Comparison of the pharmacology and signal transduction of the human cannabinoid CB1 and CB2 receptors. Mol Pharmacol 1995, 48:443-450.
9. Lichtman AH, Martin BR. Delta 9-tetrahydrocannabinol impairs spatial memory through a cannabinoid receptor mechanism. Psychopharmacology (Berl) 1996, 126:125-131.
10. Martin BR, Lichtman AH. Cannabinoid transmission and pain perception. Neurobiol Dis 1998, 5:447-461. 10.1006/nbdi.1998.0218, 9974177.
11. Howlett AC, Barth F, Bonner TI, Cabral G, Casellas P, Devane WA, Felder CC, Herkenham M, Mackie K, Martin BR, et al. International Union of Pharmacology. XXVII. Classification of cannabinoid receptors. Pharmacol Rev 2002, 54:161-202. 10.1124/pr.54.2.161, 12037135.
12. Pertwee RG. Pharmacological actions of cannabinoids. Handb Exp Pharmacol 2005, 1-51.
13. Benito C, Kim WK, Chavarria I, Hillard CJ, Mackie K, Tolon RM, Williams K, Romero J. A glial endogenous cannabinoid system is upregulated in the brains of macaques with simian immunodeficiency virus-induced encephalitis. J Neurosci 2005, 25:2530-2536. 10.1523/JNEUROSCI.3923-04.2005, 15758162.
14. Maresz K, Carrier EJ, Ponomarev ED, Hillard CJ, Dittel BN. Modulation of the cannabinoid CB2 receptor in microglial cells in response to inflammatory stimuli. J Neurochem 2005, 95:437-445. 10.1111/j.1471-4159.2005.03380.x, 16086683.
15. Zhang J, Hoffert C, Vu HK, Groblewski T, Ahmad S, O'Donnell D. Induction of CB2 receptor expression in the rat spinal cord of neuropathic but not inflammatory chronic pain models. Eur J Neurosci 2003, 17:2750-2754. 10.1046/j.1460-9568.2003.02704.x, 12823482.
16. Wotherspoon G, Fox A, McIntyre P, Colley S, Bevan S, Winter J. Peripheral nerve injury induces cannabinoid receptor 2 protein expression in rat sensory neurons. Neuroscience 2005, 135:235-245. 10.1016/j.neuroscience.2005.06.009, 16084654.
17. Romero-Sandoval A, Eisenach JC. Spinal cannabinoid receptor type 2 activation reduces hypersensitivity and spinal cord glial activation after paw incision. Anesthesiology 2007, 106:787-794. 10.1097/01.anes.0000264765.33673.6c, 17413917.
18. Ibrahim MM, Porreca F, Lai J, Albrecht PJ, Rice FL, Khodorova A, Davar G, Makriyannis A, Vanderah TW, Mata HP, Malan TP. CB2 cannabinoid receptor activation produces antinociception by stimulating peripheral release of endogenous opioids. Proc Natl Acad Sci USA 2005, 102:3093-3098. 10.1073/pnas.0409888102, 549497, 15705714.
19. Malan TP, Ibrahim MM, Deng H, Liu Q, Mata HP, Vanderah T, Porreca F, Makriyannis A. CB2 cannabinoid receptor-mediated peripheral antinociception. Pain 2001, 93:239-245. 10.1016/S0304-3959(01)00321-9, 11514083.
20. Yao BB, Hsieh GC, Frost JM, Fan Y, Garrison TR, Daza AV, Grayson GK, Zhu CZ, Pai M, Chandran P, et al. In vitro and in vivo characterization of A-796260: a selective cannabinoid CB2 receptor agonist exhibiting analgesic activity in rodent pain models. Br J Pharmacol 2008, 153:390-401. 10.1038/sj.bjp.0707568, 2219533, 17994110.
21. Altier C, Zamponi GW. Targeting Ca2+ channels to treat pain: T-type versus N-type. Trends Pharmacol Sci 2004, 25:465-470. 10.1016/j.tips.2004.07.004, 15559248.
22. Marger F, Gelot A, Alloui A, Matricon J, Ferrer JF, Barrere C, Pizzoccaro A, Muller E, Nargeot J, Snutch TP, et al. T-type calcium channels contribute to colonic hypersensitivity in a rat model of irritable bowel syndrome. Proc Natl Acad Sci USA 2011, 108:11268-11273. 10.1073/pnas.1100869108, 21690417.
23. Orestes P, Todorovic SM. Are neuronal voltage-gated calcium channels valid cellular targets for general anesthetics?. Channels (Austin) 2010, 4:518-522.
24. Park J, Luo ZD. Calcium channel functions in pain processing. Channels (Austin) 2010, 4:510-517.
25. Zamponi GW, Lewis RJ, Todorovic SM, Arneric SP, Snutch TP. Role of voltage-gated calcium channels in ascending pain pathways. Brain Res Rev 2009, 60:84-89. 10.1016/j.brainresrev.2008.12.021, 2692704, 19162069.
26. Matthews EA, Dickenson AH. Effects of ethosuximide, a T-type Ca(2+) channel blocker, on dorsal horn neuronal responses in rats. Eur J Pharmacol 2001, 415:141-149. 10.1016/S0014-2999(01)00812-3, 11274992.
27. Bourinet E, Alloui A, Monteil A, Barrere C, Couette B, Poirot O, Pages A, McRory J, Snutch TP, Eschalier A, Nargeot J. Silencing of the Cav3.2 T-type calcium channel gene in sensory neurons demonstrates its major role in nociception. Embo J 2005, 24:315-324. 10.1038/sj.emboj.7600515, 545807, 15616581.
28. Ross HR, Gilmore AJ, Connor M. Inhibition of human recombinant T-type calcium channels by the endocannabinoid N-arachidonoyl dopamine. Br J Pharmacol 2009, 156:740-750. 10.1111/j.1476-5381.2008.00072.x, 2697747, 19226289.
29. Chemin J, Monteil A, Perez-Reyes E, Nargeot J, Lory P. Direct inhibition of T-type calcium channels by the endogenous cannabinoid anandamide. Embo J 2001, 20:7033-7040. 10.1093/emboj/20.24.7033, 125779, 11742980.
30. Barbara G, Alloui A, Nargeot J, Lory P, Eschalier A, Bourinet E, Chemin J. T-type calcium channel inhibition underlies the analgesic effects of the endogenous lipoamino acids. J Neurosci 2009, 29:13106-13114. 10.1523/JNEUROSCI.2919-09.2009, 19846698.
31. Ross HR, Napier I, Connor M. Inhibition of recombinant human T-type calcium channels by Delta9-tetrahydrocannabinol and cannabidiol. J Biol Chem 2008, 283:16124-16134. 10.1074/jbc.M707104200, 18390906.
32. Diaz P, Phatak SS, Xu J, Astruc-Diaz F, Cavasotto CN, Naguib M. 6-Methoxy-N-alkyl isatin acylhydrazone derivatives as a novel series of potent selective cannabinoid receptor 2 inverse agonists: design, synthesis, and binding mode prediction. J Med Chem 2009, 52:433-444. 10.1021/jm801353p, 19115816.
33. Elmes SJ, Jhaveri MD, Smart D, Kendall DA, Chapman V. Cannabinoid CB2 receptor activation inhibits mechanically evoked responses of wide dynamic range dorsal horn neurons in naive rats and in rat models of inflammatory and neuropathic pain. Eur J Neurosci 2004, 20:2311-2320. 10.1111/j.1460-9568.2004.03690.x, 15525273.
34. Curto-Reyes V, Llames S, Hidalgo A, Menendez L, Baamonde A. Spinal and peripheral analgesic effects of the CB2 cannabinoid receptor agonist AM1241 in two models of bone cancer-induced pain. Br J Pharmacol 2010, 160:561-573. 10.1111/j.1476-5381.2009.00629.x, 2931557, 20233215.
35. Yu XH, Cao CQ, Martino G, Puma C, Morinville A, St-Onge S, Lessard E, Perkins MN, Laird JM. A peripherally restricted cannabinoid receptor agonist produces robust anti-nociceptive effects in rodent models of inflammatory and neuropathic pain. Pain 151:337-344.
36. You H, Altier C, Zamponi GW. CCR2 receptor ligands inhibit Cav3.2 T-type calcium channels. Mol Pharmacol 2010, 77:211-217. 10.1124/mol.109.059022, 19864434.
37. Hsieh GC, Pai M, Chandran P, Hooker BA, Zhu CZ, Salyers AK, Wensink EJ, Zhan C, Carroll WA, Dart MJ, et al. Central and peripheral sites of action for CB receptor mediated analgesic activity in chronic inflammatory and neuropathic pain models in rats. Br J Pharmacol 2011, 162:428-440. 10.1111/j.1476-5381.2010.01046.x, 20880025.
38. Khasabova IA, Chandiramani A, Harding-Rose C, Simone DA, Seybold VS. Increasing 2-arachidonoyl glycerol signaling in the periphery attenuates mechanical hyperalgesia in a model of bone cancer pain. Pharmacol Res 64:60-67.
39. Nackley AG, Zvonok AM, Makriyannis A, Hohmann AG. Activation of cannabinoid CB2 receptors suppresses C-fiber responses and windup in spinal wide dynamic range neurons in the absence and presence of inflammation. J Neurophysiol 2004, 92:3562-3574. 10.1152/jn.00886.2003, 15317842.
40. Bondaletov VGBV, Lopatinskii VP. Formylcarbazoles. Synthesis and use. Izvestiya Vysshikh Uchebnykh Zavedenii, Khimiya i Khimicheskaya Tekhnologiya 1987, 30:3-9.
41. Pajda MBD. Fast preparation method of aromatic aldehydes from carbazole and hydroxyaromatic derivatives under microwave irradiation. Modern polymeric materials for environmental applications, International Seminar, 2nd,; Krakow, Poland 2006, 129-132.
42. Block MH, Boyer S, Brailsford W, Brittain DR, Carroll D, Chapman S, Clarke DS, Donald CS, Foote KM, Godfrey L, et al. Discovery and optimization of a series of carbazole ureas as NPY5 antagonists for the treatment of obesity. J Med Chem 2002, 45:3509-3523. 10.1021/jm011125x, 12139462.
43. Chino NMY, Sakakibara S. Modification of Trp-residues during the acidolysis of Boc-groups: effect of scavengers. Peptide Chemistry 1978, 15.
44. Bonjoch J, Diaba F, Pages L, Perez D, Soca L, Miralpeix M, Vilella D, Anton P, Puig C. Synthesis and structure-activity relationships of gamma-carboline derivatives as potent and selective cysLT(1) antagonists. Bioorg Med Chem Lett 2009, 19:4299-4302. 10.1016/j.bmcl.2009.05.094, 19505824.
45. Khorana N, Purohit A, Herrick-Davis K, Teitler M, Glennon RA. gamma-Carbolines: binding at 5-HT5A serotonin receptors. Bioorg Med Chem 2003, 11:717-722. 10.1016/S0968-0896(02)00527-8, 12538001.
46. Beedle AM, Hamid J, Zamponi GW. Inhibition of transiently expressed low- and high-voltage-activated calcium channels by trivalent metal cations. J Membr Biol 2002, 187:225-238. 10.1007/s00232-001-0166-2, 12163980.
47. Gerard CM, Mollereau C, Vassart G, Parmentier M. Molecular cloning of a human cannabinoid receptor which is also expressed in testis. Biochem J 1991, 279(Pt 1):129-134. 1151556, 1718258.
48. Armbruster BN, Roth BL. Mining the receptorome. J Biol Chem 2005, 280:5129-5132.
49. Jensen NH, Roth BL. Massively parallel screening of the receptorome. Comb Chem High Throughput Screen 2008, 11:420-426. 10.2174/138620708784911483, 18673270.
50. Strachan RT, Ferrara G, Roth BL. Screening the receptorome: an efficient approach for drug discovery and target validation. Drug Discov Today 2006, 11:708-716. 10.1016/j.drudis.2006.06.012, 16846798.
51. Naguib M, Diaz P, Xu JJ, Astruc-Diaz F, Craig S, Vivas-Mejia P, Brown DL. MDA7: a novel selective agonist for CB2 receptors that prevents allodynia in rat neuropathic pain models. Br J Pharmacol 2008, 155:1104-1116. 2597252, 18846037.
52. Hunskaar S, Hole K. The formalin test in mice: dissociation between inflammatory and non-inflammatory pain. Pain 1987, 30:103-114. 10.1016/0304-3959(87)90088-1, 3614974.
53. Tjolsen A, Berge OG, Hunskaar S, Rosland JH, Hole K. The formalin test: an evaluation of the method. Pain 1992, 51:5-17. 10.1016/0304-3959(92)90003-T, 1454405.
54. Hylden JL, Wilcox GL. Intrathecal morphine in mice: a new technique. Eur J Pharmacol 1980, 67:313-316. 10.1016/0014-2999(80)90515-4, 6893963.