Role of CB2 receptors and cGMP pathway on the cannabinoid-dependent antiepileptic effects in an in vivo model of partial epilepsy

Epilepsy Research - Tập 108 - Trang 1711-1718 - 2014
Valerio Rizzo1,2, Fabio Carletti1, Giuditta Gambino1, Girolamo Schiera1, Carla Cannizzaro3, Giuseppe Ferraro1, Pierangelo Sardo1
1Dipartimento di Biomedicina Sperimentale e Neuroscienze Cliniche (Bio.Ne.C.), Sezione di Fisiologia umana “G. Pagano”, Università degli Studi di Palermo, Corso Tukory, 129–90134 Palermo, Italy
2Department of Neuroscience, The Scripps Research Institute, Scripps Florida 130 Scripps Way, Jupiter, FL 33458
3Dipartimento di Scienze per la Promozione della salute, Università degli Studi di Palermo, Via del Vespro, 133, 90100 Palermo, Italy

Tài liệu tham khảo

Ahern, 2002, cGMP and S-nitrosylation: two routes for modulation of neuronal excitability by NO, Trends Neurosci., 25, 510, 10.1016/S0166-2236(02)02254-3 Arancio, 2001, Presynaptic role of cGMP-dependent protein kinase during long-lasting potentiation, J. Neurosci., 21, 143, 10.1523/JNEUROSCI.21-01-00143.2001 Azad, 2001, Differential role of the nitric oxide pathway on delta(9)-THC-induced central nervous system effects in the mouse, Eur. J. Neurosci., 13, 561, 10.1046/j.1460-9568.2001.01431.x Bahremand, 2009, Involvement of nitrergic system in the anticonvulsant effect of the cannabinoid CB(1) agonist ACEA in the pentylenetetrazole-induced seizure in mice, Epilepsy Res., 84, 110, 10.1016/j.eplepsyres.2009.01.003 Bolognini, 2012, AM630 behaves as a protean ligand at the human cannabinoid CB2 receptor, Br. J. Pharmacol., 165, 2561, 10.1111/j.1476-5381.2011.01503.x Braakman, 2009, Rimonabant induces partial seizures in a patient with a history of generalized epilepsy, Epilepsia, 50, 2171, 10.1111/j.1528-1167.2009.02203.x Burette, 2002, Synaptic localization of nitric oxide synthase and soluble guanylyl cyclase in the hippocampus, J. Neurosci., 22, 8961, 10.1523/JNEUROSCI.22-20-08961.2002 Cabral, 2008, CB2 receptors in the brain: role in central immune function, Br. J. Pharmacol., 153, 240, 10.1038/sj.bjp.0707584 Carletti, 2013, Antiepileptic effect of dimethyl sulfoxide in a rat model of temporal lobe epilepsy, Neurosci. Lett., 546, 31, 10.1016/j.neulet.2013.04.031 Castillo, 2012, Endocannabinoid signaling and synaptic function, Neuron, 76, 70, 10.1016/j.neuron.2012.09.020 Chevaleyre, 2006, Endocannabinoid-mediated synaptic plasticity in the CNS, Annu. Rev. Neurosci., 29, 37, 10.1146/annurev.neuro.29.051605.112834 Deadwyler, 1995, Cannabinoids modulate voltage sensitive potassium A-current in hippocampal neurons via a cAMP-dependent process, J. Pharmacol. Exp. Ther., 273, 734 den Boon, 2012, Excitability of prefrontal cortical pyramidal neurons is modulated by activation of intracellular type-2 cannabinoid receptors, Proc. Natl. Acad. Sci. U.S.A., 109, 3534, 10.1073/pnas.1118167109 Deshpande, 2007, Cannabinoid CB1 receptor antagonists cause status epilepticus-like activity in the hippocampal neuronal culture model of acquired epilepsy, Neurosci. Lett., 411, 11, 10.1016/j.neulet.2006.09.046 Devane, 1988, Determination and characterization of a cannabinoid receptor in rat brain, Mol. Pharmacol., 34, 605 Feil, 2008, NO/cGMP-dependent modulation of synaptic transmission, Handb. Exp. Pharmacol., 184, 529, 10.1007/978-3-540-74805-2_16 Fernández-Ruiz, 2007, Cannabinoid CB2 receptor: a new target for controlling neural cell survival?, Trends Pharmacol. Sci., 28, 39, 10.1016/j.tips.2006.11.001 García-Gutiérrez, 2012, Chronic blockade of cannabinoid CB2 receptors induces anxiolytic-like actions associated with alterations in GABA(A) receptors, Br. J. Pharmacol., 165, 951, 10.1111/j.1476-5381.2011.01625.x Ghasemi, 2007, Role of the nitric oxide pathway and the endocannabinoid system in neurogenic relaxation of corpus cavernosum from biliary cirrhotic rats, Br. J. Pharmacol., 151, 591, 10.1038/sj.bjp.0707279 Gong, 2006, Cannabinoid CB2 receptors: immunohistochemical localization in rat brain, Brain Res., 1071, 10, 10.1016/j.brainres.2005.11.035 Hill, 2013, Cannabidivarin-rich cannabis extracts are anticonvulsant in mouse and rat via a CB1 receptor-independent mechanism, Br. J. Pharmacol., 170, 679, 10.1111/bph.12321 Hofmann, 2013, Marijuana, endocannabinoids, and epilepsy: potential and challenges for improved therapeutic intervention, Exp. Neurol., 244, 43, 10.1016/j.expneurol.2011.11.047 Howlett, 2004, Cannabinoid physiology and pharmacology: 30 years of progress, Neuropharmacology, 47, 345, 10.1016/j.neuropharm.2004.07.030 Jones, 2008, Cannabinoid receptor-mediated translocation of NO-sensitive guanylyl cyclase and production of cyclic GMP in neuronal cells, Neuropharmacology, 54, 23, 10.1016/j.neuropharm.2007.06.027 Jones, 2012, Cannabidiol exerts anti-convulsant effects in animal models of temporal lobe and partial seizures, Seizure, 21, 344, 10.1016/j.seizure.2012.03.001 Kreitzer, 2001, Retrograde inhibition of presynaptic calcium influx by endogenous cannabinoids at excitatory synapses onto Purkinje cells, Neuron, 29, 717, 10.1016/S0896-6273(01)00246-X Llano, 1991, Calcium entry increases the sensitivity of cerebellar Purkinje cells to applied GABA and decreases inhibitory synaptic currents, Neuron, 6, 565, 10.1016/0896-6273(91)90059-9 Maggi, 1986, Suitability of urethane anesthesia for physiopharmacological investigations in various systems. Part 1: General considerations, Experientia, 42, 109, 10.1007/BF01952426 Makara, 2007, Involvement of nitric oxide in depolarization-induced suppression of inhibition in hippocampal pyramidal cells during activation of cholinergic receptors, J. Neurosci., 27, 10211, 10.1523/JNEUROSCI.2104-07.2007 Matsuda, 1990, Structure of a cannabinoid receptor and functional expression of the cloned cDNA, Nature, 346, 561, 10.1038/346561a0 Mergia, 2009, Genetic mouse models of the NO receptor ‘soluble’ guanylyl cyclases, Handb. Exp. Pharmacol., 191, 33, 10.1007/978-3-540-68964-5_3 Monory, 2006, The endocannabinoid system controls key epileptogenic circuits in the hippocampus, Neuron, 51, 455, 10.1016/j.neuron.2006.07.006 Morgan, 2009, Functional CB2 type cannabinoid receptors at CNS synapses, Neuropharmacology, 57, 356, 10.1016/j.neuropharm.2009.07.017 Mukherjee, 2004, Species comparison and pharmacological characterization of rat and human CB2 cannabinoid receptors, Eur. J. Pharmacol., 505, 1, 10.1016/j.ejphar.2004.09.058 Neitz, 2011, Presynaptic nitric oxide/cGMP facilitates glutamate release via hyperpolarization-activated cyclic nucleotide-gated channels in the hippocampus, Eur. J. Neurosci., 33, 1611, 10.1111/j.1460-9568.2011.07654.x Pan, 1996, Rat brain cannabinoid receptor modulates N-type Ca2+ channels in a neuronal expression system, Mol. Pharmacol., 49, 707 Paxinos, 1986 Rizzo, 2009, Evidences of cannabinoids-induced modulation of paroxysmal events in an experimental model of partial epilepsy in the rat, Neurosc. Lett., 462, 135, 10.1016/j.neulet.2009.07.014 Robello, 1996, Nitric oxide and GABAA receptor function in the rat cerebral cortex and cerebellar granule cells, Neuroscience, 74, 99, 10.1016/0306-4522(96)00110-8 Sardo, 2006, Involvement of nitric oxide-soluble guanylyl cyclase pathway in the control of maximal dentate gyrus activation in the rat, J. Neural Transm., 113, 1855, 10.1007/s00702-006-0491-9 Sardo, 2008, Lamotrigine differently modulates 7-nitroindazole and l-arginine influence on rat maximal dentate gyrus activation, J. Neural Transm., 115, 27, 10.1007/s00702-007-0824-3 Stefano, 1998, Anandamide amidase inhibition enhances anandamide-stimulated nitric oxide release in invertebrate neural tissues, Brain Res., 793, 341, 10.1016/S0006-8993(98)00273-X Stringer, 1995, In the hippocampus in vivo, nitric oxide does not appear to function as an endogenous antiepileptic agent, Exp. Brain Res., 105, 391 Stringer, 1989, Maximal dentate gyrus activation: characteristics and alterations after repeated seizures, J. Neurophysiol., 62, 136, 10.1152/jn.1989.62.1.136 Van Sickle, 2005, Identification and functional characterization of brainstem cannabinoid CB2 receptors, Science, 310, 329, 10.1126/science.1115740 Wallace, 2003, The endogenous cannabinoid system regulates seizure frequency and duration in a model of temporal lobe epilepsy, J. Pharmacol. Exp. Ther., 307, 129, 10.1124/jpet.103.051920 Wilson, 2001, Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses, Nature, 410, 588, 10.1038/35069076