Novel halogenated derivates of JWH-018: Behavioral and binding studies in mice

Neuropharmacology

Volumn 95, Issue , 2015, Pages 68-82

  Vigolo, A ^a   Ossato, A ^a   Trapella, C ^a,c   Vincenzi, F ^a   Rimondo, C ^c   Seri, C ^c   Varani, K ^a   Serpelloni, G ^c   Marti, M ^a,b,c  

^a UNIVERSITY OF FERRARA   (Italy)

^b Istituto Nazionale di Neuroscienze   (Italy)

^c Presidency of the Council of Ministers   (Italy)

Author keywords

CB1 receptor; JWH 018; JWH 018 Br; JWH 018 Cl; Synthetic cannabinoids; 9 THC

Indexed keywords

1 (2,4 DICHLOROPHENYL) 5 (4 IODOPHENYL) 4 METHYL N (1 PIPERIDYL) 1H PYRAZOLE 3 CARBOXAMIDE; 1 (5 BROMOPENTYL) 3 (1 NAPHTHOYL)INDOLE; 1 (5 CHLOROPENTYL) 3 (1 NAPHTHOYL)INDOLE; 3 (1 NAPHTHOYL) 1 PENTYLINDOLE; CANNABINOID 1 RECEPTOR; CANNABINOID RECEPTOR AGONIST; DRONABINOL; HALIDE; UNCLASSIFIED DRUG; 1-(5-BROMOPENTYL)-3-(1-NAPHTHOYL)INDOLE; 1-(5-CHLOROPENTYL)-3-(1-NAPHTHOYL)INDOLE; 1-PENTYL-3-(1-NAPHTHOYL)INDOLE; CANNABINOID; CANNABINOID 2 RECEPTOR; INDOLE DERIVATIVE; NAPHTHALENE DERIVATIVE; PIPERIDINE DERIVATIVE; PYRAZOLE DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BEHAVIOR; BINDING AFFINITY; CATALEPSY; COMPETITIVE BINDING ASSAY; CONTROLLED STUDY; CONVULSION; HALOGENATION; HYPERREFLEXIA; HYPOTHERMIA; IN VITRO STUDY; IN VIVO STUDY; MALE; MOTOR DYSFUNCTION; MOUSE; MYOCLONUS; NEUROTOXICITY; NONHUMAN; PAIN THRESHOLD; PRIORITY JOURNAL; RECEPTOR BINDING; SEIZURE; AGONISTS; ANIMAL; ANTAGONISTS AND INHIBITORS; BINDING COMPETITION; CHEMICALLY INDUCED; CHEMISTRY; CHO CELL LINE; CRICETULUS; DRUG EFFECTS; GENETICS; HUMAN; INSTITUTE FOR CANCER RESEARCH MOUSE; METABOLISM; MOTOR ACTIVITY; PATHOLOGICAL REFLEX;

ANIMALS; BINDING, COMPETITIVE; CANNABINOID RECEPTOR AGONISTS; CANNABINOIDS; CATALEPSY; CHO CELLS; CRICETULUS; HALOGENATION; HUMANS; HYPOTHERMIA; INDOLES; MALE; MICE, INBRED ICR; MOTOR ACTIVITY; NAPHTHALENES; PAIN THRESHOLD; PIPERIDINES; PYRAZOLES; RECEPTOR, CANNABINOID, CB1; RECEPTOR, CANNABINOID, CB2; REFLEX, ABNORMAL; SEIZURES;

EID: 84925367850     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2015.02.008     Document Type: Article

References (59)

1. A.N. Akopian, N.B. Ruparel, N.A. Jeske, A. Patwardhan, and K.M. Hargreaves Role of ionotropic cannabinoid receptors in peripheral antinociception and antihyperalgesia Trends Pharmacol. Sci. 30 2009 79 84
2. A. Athanasiou, A.B. Clarke, A.E. Turner, N.M. Kumaran, S. Vakilpour, P.A. Smith, D. Bagiokou, T.D. Bradshaw, A.D. Westwell, L. Fang, D.N. Lobo, C.S. Constantinescu, V. Calabrese, A. Loesch, S.P. Alexander, R.H. Clothier, D.A. Kendall, and T.E. Bates Cannabinoid receptor agonists are mitochondrial inhibitors: a unified hypothesis of how cannabinoids modulate mitochondrial function and induce cell death Biochem. Biophys. Res. Commun. 364 2007 131 137
3. V. Auwarter, S. Dresen, W. Weinmann, M. Muller, M. Putz, and N. Ferreiros 'Spice' and other herbal blends: harmless incense or cannabinoid designer drugs? J. Mass Spectrom. 44 2009 832 837
4. A.I. Basbaum, D.M. Bautista, G. Scherrer, and D. Julius Cellular and molecular mechanisms of pain Cell 139 2009 267 284
5. L.K. Brents, A. Gallus-Zawada, A. Radominska-Pandya, T. Vasiljevik, T.E. Prisinzano, W.E. Fantegrossi, J.H. Moran, and P.L. Prather Monohydroxylated metabolites of the K2 synthetic cannabinoid JWH-073 retain intermediate to high cannabinoid 1 receptor (CB1R) affinity and exhibit neutral antagonist to partial agonist activity Biochem. Pharmacol. 83 2012 952 961
6. L.K. Brents, E.E. Reichard, S.M. Zimmerman, J.H. Moran, W.E. Fantegrossi, and P.L. Prather Phase I hydroxylated metabolites of the K2 synthetic cannabinoid JWH-018 retain in vitro and in vivo cannabinoid 1 receptor affinity and activity PLoS One 6 2011 e21917
7. G. Calo, A. Rizzi, G. Marzola, R. Guerrini, S. Salvadori, L. Beani, D. Regoli, and C. Bianchi Pharmacological characterization of the nociceptin receptor mediating hyperalgesia in the mouse tail withdrawal assay Br. J. Pharmacol. 125 1998 373 378
8. D.R. Compton, M.R. Johnson, L.S. Melvin, and B.R. Martin Pharmacological profile of a series of bicyclic cannabinoid analogs: classification as cannabimimetic agents J. Pharmacol. Exp. Ther. 260 1992 201 209
9. T.E. D'Ambra, K.G. Estep, M.R. Bell, M.A. Eissenstat, K.A. Josef, S.J. Ward, D.A. Haycock, E.R. Baizman, F.M. Casiano, and N.C. Beglin et al. Conformationally restrained analogues of pravadoline: nanomolar potent, enantioselective, (aminoalkyl)indole agonists of the cannabinoid receptor J. Med. Chem. 35 1992 124 135
10. EMCDDA Understanding the 'Spice' Phenomenon Thematic papers 2009 European Monitoring Centre for Drugs and Drug Addiction http://www.emcdda.europa.eu/publications/thematic-papers/spice
11. EMCDDA-Europol Annual Report on the Implementation of Council Decision 2005/387/JHA (New Drugs in Europe, 2012) 2012 EMCDDA Lisbon May 2013 http://www.emcdda.europa.eu/publications/implementation-reports/2012
12. F. Fan, D.R. Compton, S. Ward, L. Melvin, and B.R. Martin Development of cross-tolerance between delta 9-tetrahydrocannabinol, CP 55,940 and WIN 55,212 J. Pharmacol. Exp. Ther. 271 1994 1383 1390
13. W.E. Fantegrossi, J.H. Moran, A. Radominska-Pandya, and P.L. Prather Distinct pharmacology and metabolism of K2 synthetic cannabinoids compared to delta(9)-THC: mechanism underlying greater toxicity? Life Sci. 97 2014 45 54
14. A.G. Fitton, and R.G. Pertwee Changes in body temperature and oxygen consumption rate of conscious mice produced by intrahypothalamic and intracerebroventricular injections of delta 9-tetrahydrocannabinol Br. J. Pharmacol. 75 1982 409 414
15. H.D. Gilchrist, B.L. Allard, and D.A. Simone Enhanced withdrawal responses to heat and mechanical stimuli following intraplantar injection of capsaicin in rats Pain 67 1996 179 188
16. S.J. Govaerts, E. Hermans, and D.M. Lambert Comparison of cannabinoid ligands affinities and efficacies in murine tissues and in transfected cells expressing human recombinant cannabinoid receptors Eur. J. Pharm. Sci. 23 2004 233 243
17. H. Gugelmann, R. Gerona, C. Li, B. Tsutaoka, K.R. Olson, and D. Lung 'Crazy Monkey' poisons man and dog: human and canine seizures due to PB-22, a novel synthetic cannabinoid Clin. Toxicol. (Phila) 52 2014 635 638
18. J. Guindon, and A.G. Hohmann Cannabinoid CB2 receptors: a therapeutic target for the treatment of inflammatory and neuropathic pain Br. J. Pharmacol. 153 2008 319 334
19. M. Hermanns-Clausen, S. Kneisel, B. Szabo, and V. Auwarter Acute toxicity due to the confirmed consumption of synthetic cannabinoids: clinical and laboratory findings Addiction 108 2013 534 544
20. A.G. Hohmann, K. Tsou, and J.M. Walker Cannabinoid suppression of noxious heat-evoked activity in wide dynamic range neurons in the lumbar dorsal horn of the rat J. Neurophysiol. 81 1999 575 583
21. M. Honda, M. Suzuki, K. Nakayama, and T. Ishikawa Role of alpha2C-adrenoceptors in the reduction of skin blood flow induced by local cooling in mice Br. J. Pharmacol. 152 2007 91 100
22. J.W. Huffman, D. Dai, B.R. Martin, and D.R. Compton Design, synthesis and pharmacology of cannabimimetic indoles Bioorg. Med. Chem. Lett. 4 1994 563 566
23. S. Irwin Comprehensive observational assessment: Ia. A systematic, quantitative procedure for assessing the behavioral and physiologic state of the mouse Psychopharmacologia 13 1968 222 257
24. J. Lapoint, L.P. James, C.L. Moran, L.S. Nelson, R.S. Hoffman, and J.H. Moran Severe toxicity following synthetic cannabinoid ingestion Clin. Toxicol. (Phila) 49 2011 760 764
25. S. Macri, C. Ceci, L. Altabella, R. Canese, and G. Laviola The directive 2010/63/EU on animal experimentation may skew the conclusions of pharmacological and behavioural studies Sci. Rep. 3 2013 2380
26. T. Maeda, W. Hamabe, Y. Gao, Y. Fukazawa, K. Kumamoto, M. Ozaki, and S. Kishioka Morphine has an antinociceptive effect through activation of the okadaic-acid-sensitive Ser/Thr protein phosphatases PP 2 A and PP5 estimated by tail-pinch test in mice Brain Res. 1056 2005 191 199
27. R. Marshell, T. Kearney-Ramos, L.K. Brents, W.S. Hyatt, S. Tai, P.L. Prather, and W.E. Fantegrossi In vivo effects of synthetic cannabinoids JWH-018 and JWH-073 and phytocannabinoid Delta-THC in mice: inhalation versus intraperitoneal injection Pharmacol. Biochem. Behav. 124C 2014 40 47
28. M. Marti, F. Mela, M. Fantin, S. Zucchini, J.M. Brown, J. Witta, M. Di Benedetto, B. Buzas, R.K. Reinscheid, S. Salvadori, R. Guerrini, P. Romualdi, S. Candeletti, M. Simonato, B.M. Cox, and M. Morari Blockade of nociceptin/orphanin FQ transmission attenuates symptoms and neurodegeneration associated with Parkinson's disease J. Neurosci. 25 2005 9591 9601
29. M. Marti, F. Mela, C. Veronesi, R. Guerrini, S. Salvadori, M. Federici, N.B. Mercuri, A. Rizzi, G. Franchi, L. Beani, C. Bianchi, and M. Morari Blockade of nociceptin/orphanin FQ receptor signaling in rat substantia nigra pars reticulata stimulates nigrostriatal dopaminergic transmission and motor behavior J. Neurosci. 24 2004 6659 6666
30. M. Marti, C. Trapella, M. Barbieri, C. Rimondo, and G. Serpelloni Synthetic cannabinoid JWH-018 impairs object recognition memory in mice: behavioral and electrophysiological evidence Curr. Drug Abuse Rev. 6 2013 293 http://mededlive.co.uk/nps-social/2013/09/synthetic-cannabinoid-jwh-018-impairs-object-recognition-memory-in-mice-behavioral-and-electrophysiological-evidence/
31. M. Marti, A. Ossato, C. Trapella, C. Seri, C. Rimondo, and G. Serpelloni JWH-018 and its N-pentyl-halogenated derivates impair sensory motor functions in mice Proceeding of the First Monothematic Congress of the Italian Society of Pharmacology: "Old and New Drugs of Abuse, Issues and Research Approaches". November 28 to 29, Verona, Italy 2013 17
32. M. Marti Pharmaco-toxicological and physio-pathological effects of new synthetic psychoactive molecules Proceeding of the First International Conference "New Drugs 2014" May 14 to 15, Rome, Italy 2014 25 http://newdrugs2014.blogspot.it/2014/07/brochure-finalef.html
33. W.J. Martin, A.G. Hohmann, and J.M. Walker Suppression of noxious stimulus-evoked activity in the ventral posterolateral nucleus of the thalamus by a cannabinoid agonist: correlation between electrophysiological and antinociceptive effects J. Neurosci. 16 1996 6601 6611
34. F. McGlone, and D. Reilly The cutaneous sensory system Neurosci. Biobehav Rev. 34 2010 148 159
35. P.J. McLaughlin, G.A. Thakur, V.K. Vemuri, E.D. McClure, C.M. Brown, K.M. Winston, J.T. Wood, A. Makriyannis, and J.D. Salamone Behavioral effects of the novel potent cannabinoid CB1 agonist AM 4054 Pharmacol. Biochem. Behav. 109 2013 16 22
36. L.R. McMahon, and W. Koek Differences in the relative potency of SR 141716A and AM 251 as antagonists of various in vivo effects of cannabinoid agonists in C57BL/6J mice Eur. J. Pharmacol. 569 2007 70 76
37. D. McQuade, S. Hudson, P.I. Dargan, and D.M. Wood First European case of convulsions related to analytically confirmed use of the synthetic cannabinoid receptor agonist AM-2201 Eur. J. Clin. Pharmacol. 69 2013 373 376
38. F. Musshoff, B. Madea, G. Kernbach-Wighton, W. Bicker, S. Kneisel, M. Hutter, and V. Auwarter Driving under the influence of synthetic cannabinoids ("Spice"): a case series Int. J. Leg. Med. 128 2014 59 64
39. S.P. Nikas, J. Grzybowska, D.P. Papahatjis, A. Charalambous, A.R. Banijamali, R. Chari, P. Fan, T. Kourouli, S. Lin, A.J. Nitowski, G. Marciniak, Y. Guo, X. Li, C.L. Wang, and A. Makriyannis The role of halogen substitution in classical cannabinoids: a CB1 pharmacophore model AAPS J. 6 2004 e30
40. S.E. O'Sullivan, M.D. Randall, and S.M. Gardiner The in vitro and in vivo cardiovascular effects of Delta9-tetrahydrocannabinol in rats made hypertensive by chronic inhibition of nitric-oxide synthase J. Pharmacol. Exp. Ther. 321 2007 663 672
41. C.A. Paronis, S.P. Nikas, V.G. Shukla, and A. Makriyannis Delta(9)-tetrahydrocannabinol acts as a partial agonist/antagonist in mice Behav. Pharmacol. 23 2012 802 805
42. J.L. Poklis, D. Amira, L.E. Wise, J.M. Wiebelhaus, B.J. Haggerty, A.H. Lichtman, and A. Poklis Determination of naphthalen-1-yl-(1-pentylindol-3-yl)methanone (JWH-018) in mouse blood and tissue after inhalation exposure to 'buzz' smoke by HPLC/MS/MS Biomed. Chromatogr. 26 2012 1393 1398
43. S.M. Rawls, J. Cabassa, E.B. Geller, and M.W. Adler CB1 receptors in the preoptic anterior hypothalamus regulate WIN 55212-2 [(4,5-dihydro-2-methyl-4(4-morpholinylmethyl)-1-(1-naphthalenyl-carbonyl)-6H-pyrr olo[3,2,1ij]quinolin-6-one]-induced hypothermia J. Pharmacol. Exp. Ther. 301 2002 963 968
44. C. Ruzza, A. Pulga, A. Rizzi, G. Marzola, R. Guerrini, and G. Calo Behavioural phenotypic characterization of CD-1 mice lacking the neuropeptide S receptor Neuropharmacology 62 2012 1999 2009
45. W.T. Schmeling, and M.J. Hosko Hypothermic effects of intraventricular and intravenous administration of cannabinoids in intact and brainstem transected cats Neuropharmacology 19 1980 567 573
46. A.B. Schneir, and T. Baumbacher Convulsions associated with the use of a synthetic cannabinoid product J. Med. Toxicol. 8 2012 62 64
47. K.A. Seely, J. Lapoint, J.H. Moran, and L. Fattore Spice drugs are more than harmless herbal blends: a review of the pharmacology and toxicology of synthetic cannabinoids Prog. Neuropsychopharmacol. Biol. Psychiatry 39 2012 234 243
48. J.R. Simmons, C.G. Skinner, J. Williams, C.S. Kang, M.D. Schwartz, and B.K. Wills Intoxication from smoking "spice" Ann. Emerg. Med. 57 2011 187 188
49. A. Teliban, F. Bartsch, M. Struck, R. Baron, and W. Janig Axonal thermosensitivity and mechanosensitivity of cutaneous afferent neurons Eur. J. Neurosci. 33 2011 110 118
50. S.S. Tuv, H. Krabseth, R. Karinen, K.M. Olsen, E.L. Oiestad, and V. Vindenes Prevalence of synthetic cannabinoids in blood samples from Norwegian drivers suspected of impaired driving during a seven weeks period Accid. Anal. Prev. 62 2014 26 31
51. N. Uchiyama, R. Kikura-Hanajiri, J. Ogata, and Y. Goda Chemical analysis of synthetic cannabinoids as designer drugs in herbal products Forensic Sci. Int. 198 2010 31 38
52. L.R. Vilela, D.C. Medeiros, G.H. Rezende, A.C. de Oliveira, M.F. Moraes, and F.A. Moreira Effects of cannabinoids and endocannabinoid hydrolysis inhibition on pentylenetetrazole-induced seizure and electroencephalographic activity in rats Epilepsy Res. 104 2013 195 202
53. F. Vincenzi, M. Targa, C. Corciulo, M.A. Tabrizi, S. Merighi, S. Gessi, G. Saponaro, P.G. Baraldi, P.A. Borea, and K. Varani Antinociceptive effects of the selective CB2 agonist MT178 in inflammatory and chronic rodent pain models Pain 154 2013 864 873
54. J.M. Walker, and S.M. Huang Cannabinoid analgesia Pharmacol. Ther. 95 2002 127 135
55. J.M. Wiebelhaus, J.L. Poklis, A. Poklis, R.E. Vann, A.H. Lichtman, and L.E. Wise Inhalation exposure to smoke from synthetic "marijuana" produces potent cannabimimetic effects in mice Drug Alcohol Depend. 126 2012 316 323
56. J.L. Wiley, D.R. Compton, D. Dai, J.A. Lainton, M. Phillips, J.W. Huffman, and B.R. Martin Structure-activity relationships of indole- and pyrrole-derived cannabinoids J. Pharmacol. Exp. Ther. 285 1998 995 1004
57. J.L. Wiley, J.A. Marusich, and J.W. Huffman Moving around the molecule: relationship between chemical structure and in vivo activity of synthetic cannabinoids Life Sci. 97 2014 55 63
58. J.L. Wiley, J.A. Marusich, B.R. Martin, and J.W. Huffman 1-Pentyl-3-phenylacetylindoles and JWH-018 share in vivo cannabinoid profiles in mice Drug Alcohol Depend. 123 2012 148 153
59. A. Wohlfarth, A.S. Gandhi, S. Pang, M. Zhu, K.B. Scheidweiler, and M.A. Huestis Metabolism of synthetic cannabinoids PB-22 and its 5-fluoro analog, 5F-PB-22, by human hepatocyte incubation and high-resolution mass spectrometry Anal. Bioanal. Chem. 406 2014 1763 1780