Effect of JWH-250, JWH-073 and their interaction on “tetrad”, sensorimotor, neurological and neurochemical responses in mice

Andrea Ossato1, Isabella Canazza1, Claudio Trapella2, Fabrizio Vincenzi3, Maria Antonietta De Luca4, Claudia Rimondo5, Katia Varani3, Pier Andrea Borea3, Giovanni Serpelloni6, Matteo Marti1,7
1Department of Life Sciences and Biotechnology (SVeB), University of Ferrara, Italy
2Department of Chemistry and Pharmaceutical Sciences, University of Ferrara, Italy
3Department of Medical Sciences, University of Ferrara, Italy
4Department of Biomedical Sciences, University of Cagliari, Italy
5Department of Public Health and Community Medicine, University of Verona, Italy
6Department of Neuroscience, Psychology, Medicine and Child Health (NEUROFARBA), University of Florence, Italy
7Center for Neuroscience and Istituto Nazionale di Neuroscienze, Italy

Tài liệu tham khảo

Adriaan Bouwknecht, 2007, The stress-induced hyperthermia paradigm as a physiological animal model for anxiety: a review of pharmacological and genetic studies in the mouse, Neurosci. Biobehav. Rev., 31, 41, 10.1016/j.neubiorev.2006.02.002 Aung, 2000, Influence of the N-1 alkyl chain length of cannabimimetic indoles upon CB(1) and CB(2) receptor binding, Drug Alcohol Depend., 60, 133, 10.1016/S0376-8716(99)00152-0 Auwarter, 2009, ‘Spice’ and other herbal blends: harmless incense or cannabinoid designer drugs?, J. Mass Spectrom., 44, 832, 10.1002/jms.1558 Bereiter, 2002, Topical cannabinoid agonist, WIN55,212-2, reduces cornea-evoked trigeminal brainstem activity in the rat, Pain, 99, 547, 10.1016/S0304-3959(02)00271-3 Bortolato, 2005, The CB receptor agonist WIN 55,212-2 fails to elicit disruption of prepulse inhibition of the startle in Sprague–Dawley rats, Psychopharmacology, 177, 264, 10.1007/s00213-004-1941-4 Brents, 2012, 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, 952, 10.1016/j.bcp.2012.01.004 Brents, 2013, Differential drug–drug interactions of the synthetic Cannabinoids JWH-018 and JWH-073: implications for drug abuse liability and pain therapy, J. Pharmacol. Exp. Ther., 346, 350, 10.1124/jpet.113.206003 Carder, 1972, Marihuana and shock induced aggression in rats, Physiol. Behav., 8, 599, 10.1016/0031-9384(72)90081-9 Carlini, 1972, Aggressive behaviour induced by marihuana compounds and amphetamine in rats previously made dependent on morphine, Experientia, 28, 542, 10.1007/BF01931867 Carlini, 1976, Environmental and drug interference with effects of marihuana*, Ann. N. Y. Acad. Sci., 281, 229, 10.1111/j.1749-6632.1976.tb27934.x Cha, 2014, Dependence potential of the synthetic cannabinoids JWH-073, JWH-081, and JWH-210: in vivo and in vitro approaches, Biomol. Ther., 22, 363, 10.4062/biomolther.2014.039 Compton, 1992, Pharmacological profile of a series of bicyclic cannabinoid analogs: classification as cannabimimetic agents, J. Pharmacol. Exp. Ther., 260, 201 Cristino, 2006, Immunohistochemical localization of cannabinoid type 1 and vanilloid transient receptor potential vanilloid type 1 receptors in the mouse brain, Neuroscience, 139, 1405, 10.1016/j.neuroscience.2006.02.074 Dasilva, 2012, Endocannabinoid CB1 receptors modulate visual output from the thalamus, Psychopharmacology, 219, 835, 10.1007/s00213-011-2412-3 De Luca, 2015, Stimulation OF IN VIVO dopamine transmission and intravenous self-administration in rats and mice by JWH-018, a Spice cannabinoid, Neuropharmacology, 99, 705, 10.1016/j.neuropharm.2015.08.041 Dhawan, 2006, Evaluation of the in vivo receptor occupancy for the behavioral effects of cannabinoids using a radiolabeled cannabinoid receptor agonist, R-[125/131I]AM2233, Synapse, 60, 93, 10.1002/syn.20277 Di Chiara, 2004, Dopamine and drug addiction: the nucleus accumbens shell connection, Neuropharmacology, 47, 227, 10.1016/j.neuropharm.2004.06.032 Dresen, 2010, Monitoring of herbal mixtures potentially containing synthetic cannabinoids as psychoactive compounds, J. Mass Spectrom., 45, 1186, 10.1002/jms.1811 EMCDDA, 2009, Understanding the ‘Spice’ phenomenon Fantegrossi, 2014, Distinct pharmacology and metabolism of K2 synthetic cannabinoids compared to Delta(9)-THC: mechanism underlying greater toxicity?, Life Sci., 97, 45, 10.1016/j.lfs.2013.09.017 Fattore, 2011, Beyond THC: the new generation of cannabinoid designer drugs, Front. Behav. Neurosci., 5, 60, 10.3389/fnbeh.2011.00060 Garkun, 2014, Cannabinoid-dependent potentiation of inhibition at eye opening in mouse V1, Front. Cell. Neurosci., 8, 46, 10.3389/fncel.2014.00046 Ginsburg, 2012, JWH-018 and JWH-073: delta(9)-tetrahydrocannabinol-like discriminative stimulus effects in monkeys, J. Pharmacol. Exp. Ther., 340, 37, 10.1124/jpet.111.187757 Gomez-Nieto, 2014, Origin and function of short-latency inputs to the neural substrates underlying the acoustic startle reflex, Front. Neurosci., 8, 216 Gottardo, 2012, Direct screening of herbal blends for new synthetic cannabinoids by MALDI-TOF MS, J. Mass Spectrom., 47, 141, 10.1002/jms.2036 Govaerts, 2004, Comparison of cannabinoid ligands affinities and efficacies in murine tissues and in transfected cells expressing human recombinant cannabinoid receptors, Eur. J. Pharm. Sci., 23, 233, 10.1016/j.ejps.2004.07.013 Grigoryev, 2011, Gas and liquid chromatography-mass spectrometry studies on the metabolism of the synthetic phenylacetylindole cannabimimetic JWH-250, the psychoactive component of smoking mixtures, J. Chromatogr. B Anal. Technol. Biomed. Life Sci., 879, 2519, 10.1016/j.jchromb.2011.07.004 Grotenhermen, 2003, Pharmacokinetics and pharmacodynamics of cannabinoids, Clin. Pharmacokinet., 42, 327, 10.2165/00003088-200342040-00003 Guindon, 2008, Cannabinoid CB2 receptors: a therapeutic target for the treatment of inflammatory and neuropathic pain, Br. J. Pharmacol., 153, 319, 10.1038/sj.bjp.0707531 Gurney, 2014, Pharmacology, toxicology, and adverse effects of synthetic cannabinoid drugs, Forensic Sci. Rev., 26 Ham, 1975, Absence of interaction between delta9-tetrahydrocannabinol (delta-THC) and cannabidiol (CBD) in aggression, muscle control and body temperature experiments in mice, Psychopharmacologia, 41, 169, 10.1007/BF00421075 Hamdam, 2013, Safety pharmacology — current and emerging concepts, Toxicol. Appl. Pharmacol., 273, 229, 10.1016/j.taap.2013.04.039 Hemelt, 2008, Superior colliculus control of vibrissa movements, J. Neurophysiol., 100, 1245, 10.1152/jn.90478.2008 Herkenham, 1991, Characterization and localization of cannabinoid receptors in rat brain: a quantitative in vitro autoradiographic study, J. Neurosci., 11, 563, 10.1523/JNEUROSCI.11-02-00563.1991 Hermanns-Clausen, 2013, Acute toxicity due to the confirmed consumption of synthetic cannabinoids: clinical and laboratory findings, Addiction, 108, 534, 10.1111/j.1360-0443.2012.04078.x Ho, 2010, Endocannabinoid modulation of hyperaemia evoked by physiologically relevant stimuli in the rat primary somatosensory cortex, Br. J. Pharmacol., 160, 736, 10.1111/j.1476-5381.2010.00772.x Hohmann, 1999, Cannabinoid suppression of noxious heat-evoked activity in wide dynamic range neurons in the lumbar dorsal horn of the rat, J. Neurophysiol., 81, 575, 10.1152/jn.1999.81.2.575 Huffman, 1994, Design, synthesis and pharmacology of cannabimimetic indoles, Bioorg. Med. Chem. Lett., 4, 563, 10.1016/S0960-894X(01)80155-4 Huffman, 2005, 1-Pentyl-3-phenylacetylindoles, a new class of cannabimimetic indoles, Bioorg. Med. Chem. Lett., 15, 4110, 10.1016/j.bmcl.2005.06.008 ICH S7A, 2001. US Food and Drug Administration Guidance for industry: safety pharmacology studies for human pharmaceuticals (S7A). http://www.fda.gov/downloads/drugs/guidancecomplianceregulatoryinformation/guidances/ucm074959.pdf Irwin, 1968, Comprehensive observational assessment: Ia. A systematic, quantitative procedure for assessing the behavioral and physiologic state of the mouse, Psychopharmacologia, 13, 222, 10.1007/BF00401402 Jenkins, 2004, Differential modulation of withdrawal reflexes by a cannabinoid in the rabbit, Brain Res., 1012, 146, 10.1016/j.brainres.2004.03.045 Koch, 1999, The neurobiology of startle, Prog. Neurobiol., 59, 107, 10.1016/S0301-0082(98)00098-7 Kozlov, 2015, Nociceptive reactions in rats during repeated stress exposure, Bull. Exp. Biol. Med., 159, 708, 10.1007/s10517-015-3054-y Lecca, 2006, Monitoring extracellular dopamine in the rat nucleus accumbens shell and core during acquisition and maintenance of intravenous WIN 55,212-2 self-administration, Psychopharmacology, 188, 63, 10.1007/s00213-006-0475-3 Liu, 2008, Cannabinoid receptor blockade reveals parallel plasticity mechanisms in different layers of mouse visual cortex, Neuron, 58, 340, 10.1016/j.neuron.2008.02.020 Macri, 2013, Behavioral responses to acute and sub-chronic administration of the synthetic cannabinoid JWH-018 in adult mice prenatally exposed to corticosterone, Neurotox. Res., 24, 15, 10.1007/s12640-012-9371-2 Malone, 2006, The effect of Delta9-tetrahydrocannabinol on sensorimotor gating in socially isolated rats, Behav. Brain Res., 166, 101, 10.1016/j.bbr.2005.07.009 Mansbach, 1996, Effects of the cannabinoid CB1 receptor antagonist SR141716A on the behavior of pigeons and rats, Psychopharmacology, 124, 315, 10.1007/BF02247436 Marshell, 2014, 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, 40, 10.1016/j.pbb.2014.05.010 Marsicano, 1999, Expression of the cannabinoid receptor CB1 in distinct neuronal subpopulations in the adult mouse forebrain, Eur. J. Neurosci., 11, 4213, 10.1046/j.1460-9568.1999.00847.x Marti, 2004, Blockade of nociceptin/orphanin FQ receptor signaling in rat substantia nigra pars reticulata stimulates nigrostriatal dopaminergic transmission and motor behavior, J. Neurosci., 24, 6659, 10.1523/JNEUROSCI.0987-04.2004 Marti, 2005, Blockade of nociceptin/orphanin FQ transmission attenuates symptoms and neurodegeneration associated with Parkinson's Disease, Eur. J. Neurosci., 25, 9591, 10.1523/JNEUROSCI.2546-05.2005 Marti, 2013, JWH-018 and its N-pentyl-halogenated derivates impair sensory motor functions in mice Martin, 1996, 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, 6601, 10.1523/JNEUROSCI.16-20-06601.1996 Martin, 2003, Effects of cannabinoid receptor ligands on psychosis-relevant behavior models in the rat, Psychopharmacology, 165, 128, 10.1007/s00213-002-1240-x Mattsson, 1996, A performance standard for clinical and functional observational battery examinations of rats, Int. J. Toxicol., 15, 239, 10.3109/10915819609008716 Miczek, 1978, Delta9-tetrahydrocannabinol: antiaggressive effects in mice, rats, and squirrel monkeys, Science, 199, 1459, 10.1126/science.415367 Miczek, 2007, Neurobiology of escalated aggression and violence, J. Neurosci., 27, 11803, 10.1523/JNEUROSCI.3500-07.2007 Morales, 2012, Getting to the core of addiction: Hooking CB2 receptor into drug abuse?, Nat. Med., 18, 504, 10.1038/nm.2722 Nagai, 2006, Antipsychotics improve Delta9-tetrahydrocannabinol-induced impairment of the prepulse inhibition of the startle reflex in mice, Pharmacol. Biochem. Behav., 84, 330, 10.1016/j.pbb.2006.05.018 Ossato, 2015, JWH-018 impairs sensorimotor functions in mice, Neuroscience, 300, 174, 10.1016/j.neuroscience.2015.05.021 Papanastassiou, 2004, Local application of the cannabinoid receptor agonist, WIN 55,212-2, to spinal trigeminal nucleus caudalis differentially affects nociceptive and non-nociceptive neurons, Pain, 107, 267, 10.1016/j.pain.2003.11.009 Papanti, 2013, “Spiceophrenia”: a systematic overview of “Spice”-related psychopathological issues and a case report, Hum. Psychopharmacol. Clin. Exp., 28, 379, 10.1002/hup.2312 Paronis, 2012, Delta(9)-Tetrahydrocannabinol acts as a partial agonist/antagonist in mice, Behav. Pharmacol., 23, 802, 10.1097/FBP.0b013e32835a7c4d Patel, 2002, The CB1 receptor antagonist SR141716 enhances stimulus-induced activation of the primary somatosensory cortex of the rat, Neurosci. Lett., 335, 95, 10.1016/S0304-3940(02)01170-9 Penn, 2011, Detection of synthetic cannabinoids in herbal incense products, Clin. Biochem., 44, 1163, 10.1016/j.clinbiochem.2011.06.078 Pietr, 2010, Cannabinoids reveal separate controls for whisking amplitude and timing in rats, J. Neurophysiol., 104, 2532, 10.1152/jn.01039.2009 Porsolt, 2002, New perspectives in CNS safety pharmacology, Fundam. Clin. Pharmacol., 16, 197, 10.1046/j.1472-8206.2002.00061.x Price, 2003, The neuronal distribution of cannabinoid receptor type 1 in the trigeminal ganglion of the rat, Neuroscience, 120, 155, 10.1016/S0306-4522(03)00333-6 Rajasekaran, 2013, Human metabolites of synthetic cannabinoids JWH-018 and JWH-073 bind with high affinity and act as potent agonists at cannabinoid type-2 receptors, Toxicol. Appl. Pharmacol., 269, 100, 10.1016/j.taap.2013.03.012 Redfern, 2005, Spectrum of effects detected in the rat functional observational battery following oral administration of non-CNS targeted compounds, J. Pharmacol. Toxicol. Methods, 52, 77, 10.1016/j.vascn.2005.04.005 Reig, 2014, Multisensory integration in the mouse striatum, Neuron, 83, 1200, 10.1016/j.neuron.2014.07.033 Schifano, 2009, Psychoactive drug or mystical incense? Overview of the online available information on Spice products, Int. J. Cult. Ment. Health, 2, 137, 10.1080/17542860903350888 Schneider, 2002, The cannabinoid agonist WIN 55,212-2 reduces sensorimotor gating and recognition memory in rats, Behav. Pharmacol., 13, 29, 10.1097/00008877-200202000-00003 Sedlacek, 2011, Sustained firing of cartwheel cells in the dorsal cochlear nucleus evokes endocannabinoid release and retrograde suppression of parallel fiber synapses, J. Neurosci., 31, 15807, 10.1523/JNEUROSCI.4088-11.2011 Seely, 2012, Spice drugs are more than harmless herbal blends: a review of the pharmacology and toxicology of synthetic cannabinoids, Prog. Neuro-Psychopharmacol. Biol. Psychiatry, 39, 234, 10.1016/j.pnpbp.2012.04.017 Showalter, 1996, Evaluation of binding in a transfected cell line expressing a peripheral cannabinoid receptor (CB2): identification of cannabinoid receptor subtype selective ligands, J. Pharmacol. Exp. Ther., 278, 989 Takahashi, 2014, Neurogenetics of aggressive behavior: studies in rodents, Curr. Top. Behav. Neurosci., 17, 3, 10.1007/7854_2013_263 Tanda, 1997, Contribution of blockade of the noradrenaline carrier to the increase of extracellular dopamine in the rat prefrontal cortex by amphetamine and cocaine, Eur. J. Neurosci., 9, 2077, 10.1111/j.1460-9568.1997.tb01375.x Tsou, 1998, Immunohistochemical distribution of cannabinoid CB1 receptors in the rat central nervous system, Neuroscience, 83, 393, 10.1016/S0306-4522(97)00436-3 Tzounopoulos, 2007, Coactivation of pre- and postsynaptic signaling mechanisms determines cell-specific spike-timing-dependent plasticity, Neuron, 54, 291, 10.1016/j.neuron.2007.03.026 Uchiyama, 2011, Identification and quantitation of two cannabimimetic phenylacetylindoles JWH-251 and JWH-250, and four cannabimimetic naphthoylindoles JWH-081, JWH-015, JWH-200, and JWH-073 as designer drugs in illegal products, Forensic Toxicol., 29, 25, 10.1007/s11419-010-0100-3 van Ree, 1984, Delta 1-Tetrahydrocannabinol but not cannabidiol reduces contact and aggressive behavior of rats tested in dyadic encounters, Psychopharmacology, 84, 561, 10.1007/BF00431467 Vigolo, 2015, Novel halogenated derivates of JWH-018: behavioral and binding studies in mice, Neuropharmacology, 95, 68, 10.1016/j.neuropharm.2015.02.008 Vincenzi, 2013, Antinociceptive effects of the selective CB2 agonist MT178 in inflammatory and chronic rodent pain models, Pain, 154, 864, 10.1016/j.pain.2013.02.007 Wegener, 2008, Effects of acute systemic and intra-cerebral stimulation of cannabinoid receptors on sensorimotor gating, locomotion and spatial memory in rats, Psychopharmacology, 198, 375, 10.1007/s00213-008-1148-1 Wiebelhaus, 2012, Inhalation exposure to smoke from synthetic “marijuana” produces potent cannabimimetic effects in mice, Drug Alcohol Depend., 126, 316, 10.1016/j.drugalcdep.2012.05.034 Wiley, 1998, Structure–activity relationships of indole- and pyrrole-derived cannabinoids, J. Pharmacol. Exp. Ther., 285, 995 Wiley, 2014, Moving around the molecule: relationship between chemical structure and in vivo activity of synthetic cannabinoids, Life Sci., 97, 55, 10.1016/j.lfs.2013.09.011 Wintermeyer, 2010, In vitro phase I metabolism of the synthetic cannabimimetic JWH-018, Anal. Bioanal. Chem., 398, 2141, 10.1007/s00216-010-4171-0 Winton-Brown, 2011, Modulation of auditory and visual processing by delta-9-tetrahydrocannabinol and cannabidiol: an FMRI study, Neuropsychopharmacology, 36, 1340, 10.1038/npp.2011.17 Xi, 2011, Brain cannabinoid CB(2) receptors modulate cocaine's actions in mice, Nat. Neurosci., 14, 1160, 10.1038/nn.2874 Yoneda, 2013, Developmental and visual input-dependent regulation of the CB1 cannabinoid receptor in the mouse visual cortex, PLoS One, 8, 10.1371/journal.pone.0053082 Zawilska, 2014, Spice/K2 drugs–more than innocent substitutes for marijuana, Int. J. Neuropsychopharmacol., 17, 509, 10.1017/S1461145713001247 Zhao, 2011, Mechanisms underlying input-specific expression of endocannabinoid-mediated synaptic plasticity in the dorsal cochlear nucleus, Hear. Res., 279, 67, 10.1016/j.heares.2011.03.007