Endocannabinoid Receptors in the CNS: Potential Drug Targets for the Prevention and Treatment of Neurologic and Psychiatric Disorders

Author(s): José Antonio Estrada*, Irazú Contreras

Journal Name: Current Neuropharmacology

Volume 18 , Issue 8 , 2020

DOI : 10.2174/1570159X18666200217140255

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Abstract:

The endocannabinoid system participates in the regulation of CNS homeostasis and functions, including neurotransmission, cell signaling, inflammation and oxidative stress, as well as neuronal and glial cell proliferation, differentiation, migration and survival. Endocannabinoids are produced by multiple cell types within the CNS and their main receptors, CB1 and CB2, are expressed in both neurons and glia. Signaling through these receptors is implicated in the modulation of neuronal and glial alterations in neuroinflammatory, neurodegenerative and psychiatric conditions, including Alzheimer’s, Parkinson’s and Huntington’s disease, multiple sclerosis, amyotrophic lateral sclerosis, stroke, epilepsy, anxiety and depression. The therapeutic potential of endocannabinoid receptors in neurological disease has been hindered by unwelcome side effects of current drugs used to target them; however, due to their extensive expression within the CNS and their involvement in physiological and pathological process in nervous tissue, they are attractive targets for drug development. The present review highlights the potential applications of the endocannabinoid system for the prevention and treatment of neurologic and psychiatric disorders.

Keywords: Endocannabinoids, endocannabinoid receptors, neuroinflammation, neurodegeneration, psychiatric disease, drug targets.

[1]
Di Marzo, V.; Fontana, A.; Cadas, H.; Schinelli, S.; Cimino, G.; Schwartz, J.C.; Piomelli, D. Formation and inactivation of endogenous cannabinoid anandamide in central neurons. Nature, 1994, 372(6507), 686-691.
[http://dx.doi.org/10.1038/372686a0] [PMID: 7990962]
[2]
Stella, N.; Schweitzer, P.; Piomelli, D. A second endogenous cannabinoid that modulates long-term potentiation. Nature, 1997, 388(6644), 773-778.
[http://dx.doi.org/10.1038/42015] [PMID: 9285589]
[3]
Deutsch, D.G.; Chin, S.A. Enzymatic synthesis and degradation of anandamide, a cannabinoid receptor agonist. Biochem. Pharmacol., 1993, 46(5), 791-796.
[http://dx.doi.org/10.1016/0006-2952(93)90486-G] [PMID: 8373432]
[4]
Blankman, J.L.; Simon, G.M.; Cravatt, B.F. A comprehensive profile of brain enzymes that hydrolyze the endocannabinoid 2-arachidonoylglycerol. Chem. Biol., 2007, 14(12), 1347-1356.
[http://dx.doi.org/10.1016/j.chembiol.2007.11.006] [PMID: 18096503]
[5]
Ahn, K.; McKinney, M.K.; Cravatt, B.F. Enzymatic pathways that regulate endocannabinoid signaling in the nervous system. Chem. Rev., 2008, 108(5), 1687-1707.
[http://dx.doi.org/10.1021/cr0782067] [PMID: 18429637]
[6]
Herkenham, M.; Lynn, A.B.; Little, M.D.; Johnson, M.R.; Melvin, L.S.; de Costa, B.R.; Rice, K.C. Cannabinoid receptor localization in brain. Proc. Natl. Acad. Sci. USA, 1990, 87(5), 1932-1936.
[http://dx.doi.org/10.1073/pnas.87.5.1932] [PMID: 2308954]
[7]
Jansen, E.M.; Haycock, D.A.; Ward, S.J.; Seybold, V.S. Distribution of cannabinoid receptors in rat brain determined with aminoalkylindoles. Brain Res., 1992, 575(1), 93-102.
[http://dx.doi.org/10.1016/0006-8993(92)90428-C] [PMID: 1504787]
[8]
Glass, M.; Dragunow, M.; Faull, R.L. Cannabinoid receptors in the human brain: a detailed anatomical and quantitative autoradiographic study in the fetal, neonatal and adult human brain. Neuroscience, 1997, 77(2), 299-318.
[http://dx.doi.org/10.1016/S0306-4522(96)00428-9] [PMID: 9472392]
[9]
Mato, S.; Del Olmo, E.; Pazos, A. Ontogenetic development of cannabinoid receptor expression and signal transduction functionality in the human brain. Eur. J. Neurosci., 2003, 17(9), 1747-1754.
[http://dx.doi.org/10.1046/j.1460-9568.2003.02599.x] [PMID: 12752773]
[10]
Kendall, D.A.; Yudowski, G.A. Cannabinoid Receptors in the Central Nervous System: Their Signaling and Roles in Disease. Front. Cell. Neurosci., 2017, 10, 294.
[http://dx.doi.org/10.3389/fncel.2016.00294] [PMID: 28101004]
[11]
Chanda, D.; Neumann, D.; Glatz, J.F.C. The endocannabinoid system: Overview of an emerging multi-faceted therapeutic target. Prostaglandins Leukot. Essent. Fatty Acids, 2019, 140, 51-56.
[http://dx.doi.org/10.1016/j.plefa.2018.11.016] [PMID: 30553404]
[12]
Zou, S.; Kumar, U. Cannabinoid Receptors and the Endocannabinoid System: Signaling and Function in the Central Nervous System. Int. J. Mol. Sci., 2018, 19(3), e833
[http://dx.doi.org/10.3390/ijms19030833] [PMID: 29533978]
[13]
Kreitzer, A.C.; Regehr, W.G. Retrograde inhibition of presynaptic calcium influx by endogenous cannabinoids at excitatory synapses onto Purkinje cells. Neuron, 2001, 29(3), 717-727.
[http://dx.doi.org/10.1016/S0896-6273(01)00246-X] [PMID: 11301030]
[14]
Ohno-Shosaku, T.; Maejima, T.; Kano, M. Endogenous cannabinoids mediate retrograde signals from depolarized postsynaptic neurons to presynaptic terminals. Neuron, 2001, 29(3), 729-738.
[http://dx.doi.org/10.1016/S0896-6273(01)00247-1] [PMID: 11301031]
[15]
Wilson, R.I.; Nicoll, R.A. Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature, 2001, 410(6828), 588-592.
[http://dx.doi.org/10.1038/35069076] [PMID: 11279497]
[16]
Castillo, P.E.; Younts, T.J.; Chávez, A.E.; Hashimotodani, Y. Endocannabinoid signaling and synaptic function. Neuron, 2012, 76(1), 70-81.
[http://dx.doi.org/10.1016/j.neuron.2012.09.020] [PMID: 23040807]
[17]
Tsuboi, K.; Uyama, T.; Okamoto, Y.; Ueda, N. Endocannabinoids and related N-acylethanolamines: biological activities and metabolism. Inflamm. Regen., 2018, 38, 28.
[http://dx.doi.org/10.1186/s41232-018-0086-5] [PMID: 30288203]
[18]
Diana, M.A.; Marty, A. Endocannabinoid-mediated short-term synaptic plasticity: depolarization-induced suppression of inhibition (DSI) and depolarization-induced suppression of excitation (DSE). Br. J. Pharmacol., 2004, 142(1), 9-19.
[http://dx.doi.org/10.1038/sj.bjp.0705726] [PMID: 15100161]
[19]
Busquets-Garcia, A.; Bains, J.; Marsicano, G. CB1 Receptor Signaling in the Brain: Extracting Specificity from Ubiquity. Neuropsychopharmacology, 2018, 43(1), 4-20.
[http://dx.doi.org/10.1038/npp.2017.206] [PMID: 28862250]
[20]
Fišar, Z.; Singh, N.; Hroudová, J. Cannabinoid-induced changes in respiration of brain mitochondria. Toxicol. Lett., 2014, 231(1), 62-71.
[http://dx.doi.org/10.1016/j.toxlet.2014.09.002] [PMID: 25195527]
[21]
Lee, S.H.; Ledri, M.; Tóth, B.; Marchionni, I.; Henstridge, C.M.; Dudok, B.; Kenesei, K.; Barna, L.; Szabó, S.I.; Renkecz, T.; Oberoi, M.; Watanabe, M.; Limoli, C.L.; Horvai, G.; Soltesz, I.; Katona, I. Multiple forms of endocannabinoid and endovanilloid signaling regulate the tonic control of GABA release. J. Neurosci., 2015, 35(27), 10039-10057.
[http://dx.doi.org/10.1523/JNEUROSCI.4112-14.2015] [PMID: 26157003]
[22]
Kaczocha, M.; Glaser, S.T.; Deutsch, D.G.; Lennarz, W.J. Identification of intracellular carriers for the endocannabinoid anandamide. Proc. Natl. Acad. Sci. USA, 2009, 106(15), 6375-6380.
[http://dx.doi.org/10.1073/pnas.0901515106] [PMID: 19307565]
[23]
Compagnucci, C.; Di Siena, S.; Bustamante, M.B.; Di Giacomo, D.; Di Tommaso, M.; Maccarrone, M.; Grimaldi, P.; Sette, C. Type-1 (CB1) cannabinoid receptor promotes neuronal differentiation and maturation of neural stem cells. PLoS One, 2013, 8(1), e54271
[http://dx.doi.org/10.1371/journal.pone.0054271] [PMID: 23372698]
[24]
Araque, A.; Castillo, P.E.; Manzoni, O.J.; Tonini, R. Synaptic functions of endocannabinoid signaling in health and disease. Neuropharmacology, 2017, 124, 13-24.
[http://dx.doi.org/10.1016/j.neuropharm.2017.06.017] [PMID: 28625718]
[25]
Stempel, A.V.; Stumpf, A.; Zhang, H.Y.; Özdoğan, T.; Pannasch, U.; Theis, A.K.; Otte, D.M.; Wojtalla, A.; Rácz, I.; Ponomarenko, A.; Xi, Z.X.; Zimmer, A.; Schmitz, D. Cannabinoid Type 2 receptors mediate a cell type-specific plasticity in the hippocampus. Neuron, 2016, 90(4), 795-809.
[http://dx.doi.org/10.1016/j.neuron.2016.03.034] [PMID: 27133464]
[26]
Atwood, B.K.; Straiker, A.; Mackie, K. CB2 cannabinoid receptors inhibit synaptic transmission when expressed in cultured autaptic neurons. Neuropharmacology, 2012, 63(4), 514-523.
[http://dx.doi.org/10.1016/j.neuropharm.2012.04.024] [PMID: 22579668]
[27]
Navarro, G.; Morales, P.; Rodríguez-Cueto, C.; Fernández-Ruiz, J.; Jagerovic, N.; Franco, R. Targeting cannabinoid CB2 receptors in the central nervous system. medicinal chemistry approaches with focus on neurodegenerative disorders. Front. Neurosci., 2016, 10, 406.
[http://dx.doi.org/10.3389/fnins.2016.00406] [PMID: 27679556]
[28]
Gong, J.P.; Onaivi, E.S.; Ishiguro, H.; Liu, Q.R.; Tagliaferro, P.A.; Brusco, A.; Uhl, G.R. Cannabinoid CB2 receptors: immunohistochemical localization in rat brain. Brain Res., 2006, 1071(1), 10-23.
[http://dx.doi.org/10.1016/j.brainres.2005.11.035] [PMID: 16472786]
[29]
Caterina, M.J.; Schumacher, M.A.; Tominaga, M.; Rosen, T.A.; Levine, J.D.; Julius, D. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature, 1997, 389(6653), 816-824.
[http://dx.doi.org/10.1038/39807] [PMID: 9349813]
[30]
Chávez, A.E.; Chiu, C.Q.; Castillo, P.E. TRPV1 activation by endogenous anandamide triggers postsynaptic long-term depression in dentate gyrus. Nat. Neurosci., 2010, 13(12), 1511-1518.
[http://dx.doi.org/10.1038/nn.2684] [PMID: 21076423]
[31]
Younts, T.J.; Castillo, P.E. Endogenous cannabinoid signaling at inhibitory interneurons. Curr. Opin. Neurobiol., 2014, 26, 42-50.
[http://dx.doi.org/10.1016/j.conb.2013.12.006] [PMID: 24650503]
[32]
Manduca, A.; Lassalle, O.; Sepers, M.; Campolongo, P.; Cuomo, V.; Marsicano, G.; Kieffer, B.; Vanderschuren, L.J.; Trezza, V.; Manzoni, O.J. interacting cannabinoid and opioid receptors in the nucleus accumbens core control adolescent social play. Front. Behav. Neurosci., 2016, 10, 211.
[http://dx.doi.org/10.3389/fnbeh.2016.00211] [PMID: 27899885]
[33]
Walter, L.; Franklin, A.; Witting, A.; Moller, T.; Stella, N. Astrocytes in culture produce anandamide and other acylethanolamides. J. Biol. Chem., 2002, 277(23), 20869-20876.
[http://dx.doi.org/10.1074/jbc.M110813200] [PMID: 11916961]
[34]
Walter, L.; Stella, N. Endothelin-1 increases 2-arachidonoyl glycerol (2-AG) production in astrocytes. Glia, 2003, 44(1), 85-90.
[http://dx.doi.org/10.1002/glia.10270] [PMID: 12951660]
[35]
Gabrielli, M.; Battista, N.; Riganti, L.; Prada, I.; Antonucci, F.; Cantone, L.; Matteoli, M.; Maccarrone, M.; Verderio, C. Active endocannabinoids are secreted on extracellular membrane vesicles. EMBO Rep., 2015, 16(2), 213-220.
[http://dx.doi.org/10.15252/embr.201439668] [PMID: 25568329]
[36]
Witting, A.; Walter, L.; Wacker, J.; Möller, T.; Stella, N. P2X7 receptors control 2-arachidonoylglycerol production by microglial cells. Proc. Natl. Acad. Sci. USA, 2004, 101(9), 3214-3219.
[http://dx.doi.org/10.1073/pnas.0306707101] [PMID: 14976257]
[37]
Bernal-Chico, A.; Canedo, M.; Manterola, A.; Victoria Sánchez-Gómez, M.; Pérez-Samartín, A.; Rodríguez-Puertas, R.; Matute, C.; Mato, S. Blockade of monoacylglycerol lipase inhibits oligodendrocyte excitotoxicity and prevents demyelination in vivo. Glia, 2015, 63(1), 163-176.
[http://dx.doi.org/10.1002/glia.22742] [PMID: 25130621]
[38]
Navarrete, M.; Araque, A. Endocannabinoids mediate neuron-astrocyte communication. Neuron, 2008, 57(6), 883-893.
[http://dx.doi.org/10.1016/j.neuron.2008.01.029] [PMID: 18367089]
[39]
Navarrete, M.; Araque, A. Endocannabinoids potentiate synaptic transmission through stimulation of astrocytes. Neuron, 2010, 68(1), 113-126.
[http://dx.doi.org/10.1016/j.neuron.2010.08.043] [PMID: 20920795]
[40]
Andrade-Talavera, Y.; Duque-Feria, P.; Paulsen, O.; Rodríguez-Moreno, A. Presynaptic spike timing-dependent long-term depression in the mouse hippocampus. Cereb. Cortex, 2016, 26(8), 3637-3654.
[http://dx.doi.org/10.1093/cercor/bhw172] [PMID: 27282393]
[41]
Han, J.; Kesner, P.; Metna-Laurent, M.; Duan, T.; Xu, L.; Georges, F.; Koehl, M.; Abrous, D.N.; Mendizabal-Zubiaga, J.; Grandes, P.; Liu, Q.; Bai, G.; Wang, W.; Xiong, L.; Ren, W.; Marsicano, G.; Zhang, X. Acute cannabinoids impair working memory through astroglial CB1 receptor modulation of hippocampal LTD. Cell, 2012, 148(5), 1039-1050.
[http://dx.doi.org/10.1016/j.cell.2012.01.037] [PMID: 22385967]
[42]
Gorzkiewicz, A.; Szemraj, J. Brain endocannabinoid signaling exhibits remarkable complexity. Brain Res. Bull., 2018, 142, 33-46.
[http://dx.doi.org/10.1016/j.brainresbull.2018.06.012] [PMID: 29953913]
[43]
Panikashvili, D.; Shein, N.A.; Mechoulam, R.; Trembovler, V.; Kohen, R.; Alexandrovich, A.; Shohami, E. The endocannabinoid 2-AG protects the blood-brain barrier after closed head injury and inhibits mRNA expression of proinflammatory cytokines. Neurobiol. Dis., 2006, 22(2), 257-264.
[http://dx.doi.org/10.1016/j.nbd.2005.11.004] [PMID: 16364651]
[44]
Wettschureck, N.; van der Stelt, M.; Tsubokawa, H.; Krestel, H.; Moers, A.; Petrosino, S.; Schütz, G.; Di Marzo, V.; Offermanns, S. Forebrain-specific inactivation of Gq/G11 family G proteins results in age-dependent epilepsy and impaired endocannabinoid formation. Mol. Cell. Biol., 2006, 26(15), 5888-5894.
[http://dx.doi.org/10.1128/MCB.00397-06] [PMID: 16847339]
[45]
Van Laere, K.; Casteels, C.; Dhollander, I.; Goffin, K.; Grachev, I.; Bormans, G.; Vandenberghe, W. Widespread decrease of type 1 cannabinoid receptor availability in Huntington disease in vivo. J. Nucl. Med., 2010, 51(9), 1413-1417.
[http://dx.doi.org/10.2967/jnumed.110.077156] [PMID: 20720046]
[46]
Westlake, T.M.; Howlett, A.C.; Bonner, T.I.; Matsuda, L.A.; Herkenham, M. Cannabinoid receptor binding and messenger RNA expression in human brain: an in vitro receptor autoradiography and in situ hybridization histochemistry study of normal aged and Alzheimer’s brains. Neuroscience, 1994, 63(3), 637-652.
[http://dx.doi.org/10.1016/0306-4522(94)90511-8] [PMID: 7898667]
[47]
Ramirez, S.H.; Haskó, J.; Skuba, A.; Fan, S.; Dykstra, H.; McCormick, R.; Reichenbach, N.; Krizbai, I.; Mahadevan, A.; Zhang, M.; Tuma, R.; Son, Y.J.; Persidsky, Y. Activation of cannabinoid receptor 2 attenuates leukocyte-endothelial cell interactions and blood-brain barrier dysfunction under inflammatory conditions. J. Neurosci., 2012, 32(12), 4004-4016.
[http://dx.doi.org/10.1523/JNEUROSCI.4628-11.2012] [PMID: 22442067]
[48]
Cassano, T.; Calcagnini, S.; Pace, L.; De Marco, F.; Romano, A.; Gaetani, S. Cannabinoid receptor 2 signaling in neurodegenerative disorders: from pathogenesis to a promising therapeutic target. Front. Neurosci., 2017, 11, 30.
[http://dx.doi.org/10.3389/fnins.2017.00030] [PMID: 28210207]
[49]
Giuffrida, A.; Leweke, F.M.; Gerth, C.W.; Schreiber, D.; Koethe, D.; Faulhaber, J.; Klosterkötter, J.; Piomelli, D. Cerebrospinal anandamide levels are elevated in acute schizophrenia and are inversely correlated with psychotic symptoms. Neuropsychopharmacology, 2004, 29(11), 2108-2114.
[http://dx.doi.org/10.1038/sj.npp.1300558] [PMID: 15354183]
[50]
Haller, J.; Bakos, N.; Szirmay, M.; Ledent, C.; Freund, T.F. The effects of genetic and pharmacological blockade of the CB1 cannabinoid receptor on anxiety. Eur. J. Neurosci., 2002, 16(7), 1395-1398.
[http://dx.doi.org/10.1046/j.1460-9568.2002.02192.x] [PMID: 12405999]
[51]
Beyer, C.E.; Dwyer, J.M.; Piesla, M.J.; Platt, B.J.; Shen, R.; Rahman, Z.; Chan, K.; Manners, M.T.; Samad, T.A.; Kennedy, J.D.; Bingham, B.; Whiteside, G.T. Depression-like phenotype following chronic CB1 receptor antagonism. Neurobiol. Dis., 2010, 39(2), 148-155.
[http://dx.doi.org/10.1016/j.nbd.2010.03.020] [PMID: 20381618]
[52]
Cota, D.; Steiner, M.A.; Marsicano, G.; Cervino, C.; Herman, J.P.; Grübler, Y.; Stalla, J.; Pasquali, R.; Lutz, B.; Stalla, G.K.; Pagotto, U. Requirement of cannabinoid receptor type 1 for the basal modulation of hypothalamic-pituitary-adrenal axis function. Endocrinology, 2007, 148(4), 1574-1581.
[http://dx.doi.org/10.1210/en.2005-1649] [PMID: 17194743]
[53]
Navarrete, M.; Díez, A.; Araque, A. Astrocytes in endocannabinoid signalling. Philos. Trans. R. Soc. Lond. B Biol. Sci., 2014, 369(1654), 20130599
[http://dx.doi.org/10.1098/rstb.2013.0599] [PMID: 25225093]
[54]
Hill, M.N.; McLaughlin, R.J.; Bingham, B.; Shrestha, L.; Lee, T.T.; Gray, J.M.; Hillard, C.J.; Gorzalka, B.B.; Viau, V. Endogenous cannabinoid signaling is essential for stress adaptation. Proc. Natl. Acad. Sci. USA, 2010, 107(20), 9406-9411.
[http://dx.doi.org/10.1073/pnas.0914661107] [PMID: 20439721]
[55]
Viveros, M.P.; Marco, E.M.; Llorente, R.; López-Gallardo, M. Endocannabinoid system and synaptic plasticity: implications for emotional responses. Neural Plast., 2007, 2007, 52908.
[http://dx.doi.org/10.1155/2007/52908] [PMID: 17641734]
[56]
Barna, I.; Zelena, D.; Arszovszki, A.C.; Ledent, C. The role of endogenous cannabinoids in the hypothalamo-pituitary-adrenal axis regulation: in vivo and in vitro studies in CB1 receptor knockout mice. Life Sci., 2004, 75(24), 2959-2970.
[http://dx.doi.org/10.1016/j.lfs.2004.06.006] [PMID: 15454346]
[57]
Abbott, N.J. Inflammatory mediators and modulation of blood-brain barrier permeability. Cell. Mol. Neurobiol., 2000, 20(2), 131-147.
[http://dx.doi.org/10.1023/A:1007074420772] [PMID: 10696506]
[58]
Huber, J.D.; Witt, K.A.; Hom, S.; Egleton, R.D.; Mark, K.S.; Davis, T.P. Inflammatory pain alters blood-brain barrier permeability and tight junctional protein expression. Am. J. Physiol. Heart Circ. Physiol., 2001, 280(3), H1241-H1248.
[http://dx.doi.org/10.1152/ajpheart.2001.280.3.H1241] [PMID: 11179069]
[59]
Hickey, W.F. Migration of hematogenous cells through the blood-brain barrier and the initiation of CNS inflammation. Brain Pathol., 1991, 1(2), 97-105.
[http://dx.doi.org/10.1111/j.1750-3639.1991.tb00646.x] [PMID: 1669702]
[60]
Ek, M.; Engblom, D.; Saha, S.; Blomqvist, A.; Jakobsson, P.J.; Ericsson-Dahlstrand, A. Inflammatory response: pathway across the blood-brain barrier. Nature, 2001, 410(6827), 430-431.
[http://dx.doi.org/10.1038/35068632] [PMID: 11260702]
[61]
Mestre, L.; Iñigo, P.M.; Mecha, M.; Correa, F.G.; Hernangómez-Herrero, M.; Loría, F.; Docagne, F.; Borrell, J.; Guaza, C. Anandamide inhibits Theiler’s virus induced VCAM-1 in brain endothelial cells and reduces leukocyte transmigration in a model of blood brain barrier by activation of CB(1) receptors. J. Neuroinflammation, 2011, 8, 102.
[http://dx.doi.org/10.1186/1742-2094-8-102] [PMID: 21851608]
[62]
Droogan, A.G.; McMillan, S.A.; Douglas, J.P.; Hawkins, S.A. Serum and cerebrospinal fluid levels of soluble adhesion molecules in multiple sclerosis: predominant intrathecal release of vascular cell adhesion molecule-1. J. Neuroimmunol., 1996, 64(2), 185-191.
[http://dx.doi.org/10.1016/0165-5728(95)00174-3] [PMID: 8632061]
[63]
Matsuda, M.; Tsukada, N.; Miyagi, K.; Yanagisawa, N. Increased levels of soluble vascular cell adhesion molecule-1 (VCAM-1) in the cerebrospinal fluid and sera of patients with multiple sclerosis and human T lymphotropic virus type-1-associated myelopathy. J. Neuroimmunol., 1995, 59(1-2), 35-40.
[http://dx.doi.org/10.1016/0165-5728(95)00023-U] [PMID: 7541057]
[64]
Rothoerl, R.D.; Schebesch, K.M.; Kubitza, M.; Woertgen, C.; Brawanski, A.; Pina, A.L. ICAM-1 and VCAM-1 expression following aneurysmal subarachnoid hemorrhage and their possible role in the pathophysiology of subsequent ischemic deficits. Cerebrovasc. Dis., 2006, 22(2-3), 143-149.
[http://dx.doi.org/10.1159/000093243] [PMID: 16691023]
[65]
Rossi, B.; Zenaro, E.; Angiari, S.; Ottoboni, L.; Bach, S.; Piccio, L.; Pietronigro, E.C.; Scarpini, E.; Fusco, M.; Leon, A.; Constantin, G. Inverse agonism of cannabinoid CB1 receptor blocks the adhesion of encephalitogenic T cells in inflamed brain venules by a protein kinase A-dependent mechanism. J. Neuroimmunol., 2011, 233(1-2), 97-105.
[http://dx.doi.org/10.1016/j.jneuroim.2010.12.005] [PMID: 21216016]
[66]
Rom, S.; Zuluaga-Ramirez, V.; Dykstra, H.; Reichenbach, N.L.; Pacher, P.; Persidsky, Y. Selective activation of cannabinoid receptor 2 in leukocytes suppresses their engagement of the brain endothelium and protects the blood-brain barrier. Am. J. Pathol., 2013, 183(5), 1548-1558.
[http://dx.doi.org/10.1016/j.ajpath.2013.07.033] [PMID: 24055259]
[67]
Maccarrone, M.; Fiori, A.; Bari, M.; Granata, F.; Gasperi, V.; De Stefano, M.E.; Finazzi-Agrò, A.; Strom, R. Regulation by cannabinoid receptors of anandamide transport across the blood-brain barrier and through other endothelial cells. Thromb. Haemost., 2006, 95(1), 117-127.
[http://dx.doi.org/10.1160/TH05-06-0413] [PMID: 16543970]
[68]
Hind, W.H.; Tufarelli, C.; Neophytou, M.; Anderson, S.I.; England, T.J.; O’Sullivan, S.E. Endocannabinoids modulate human blood-brain barrier permeability in vitro. Br. J. Pharmacol., 2015, 172(12), 3015-3027.
[http://dx.doi.org/10.1111/bph.13106] [PMID: 25651941]
[69]
Correa, F.; Docagne, F.; Mestre, L.; Loría, F.; Hernangómez, M.; Borrell, J.; Guaza, C. Cannabinoid system and neuroinflammation: implications for multiple sclerosis. Neuroimmunomodulation, 2007, 14(3-4), 182-187.
[http://dx.doi.org/10.1159/000110644] [PMID: 18073512]
[70]
Tang, Y.; Le, W. Differential roles of m1 and m2 microglia in neurodegenerative diseases. Mol. Neurobiol., 2016, 53(2), 1181-1194.
[http://dx.doi.org/10.1007/s12035-014-9070-5] [PMID: 25598354]
[71]
Malek, N.; Popiolek-Barczyk, K.; Mika, J.; Przewlocka, B.; Starowicz, K. Anandamide, Acting via CB2 Receptors, Alleviates LPS-Induced Neuroinflammation in Rat Primary Microglial Cultures. Neural Plast., 2015, 2015, 130639
[http://dx.doi.org/10.1155/2015/130639] [PMID: 26090232]
[72]
Ativie, F.; Komorowska, J.A.; Beins, E.; Albayram, Ö.; Zimmer, T.; Zimmer, A.; Tejera, D.; Heneka, M.; Bilkei-Gorzo, A. Cannabinoid 1 receptor signaling on hippocampal gabaergic neurons influences microglial activity. Front. Mol. Neurosci., 2018, 11, 295.
[http://dx.doi.org/10.3389/fnmol.2018.00295] [PMID: 30210289]
[73]
Romero-Sandoval, E.A.; Horvath, R.; Landry, R.P.; DeLeo, J.A. Cannabinoid receptor type 2 activation induces a microglial anti-inflammatory phenotype and reduces migration via MKP induction and ERK dephosphorylation. Mol. Pain, 2009, 5, 25.
[http://dx.doi.org/10.1186/1744-8069-5-25] [PMID: 19476641]
[74]
Boorman, E.; Zajkowska, Z.; Ahmed, R.; Pariante, C.M.; Zunszain, P.A. Crosstalk between endocannabinoid and immune systems: a potential dysregulation in depression? Psychopharmacology (Berl.), 2016, 233(9), 1591-1604.
[http://dx.doi.org/10.1007/s00213-015-4105-9] [PMID: 26483037]
[75]
Hernangómez, M.; Mestre, L.; Correa, F.G.; Loría, F.; Mecha, M.; Iñigo, P.M.; Docagne, F.; Williams, R.O.; Borrell, J.; Guaza, C. CD200-CD200R1 interaction contributes to neuroprotective effects of anandamide on experimentally induced inflammation. Glia, 2012, 60(9), 1437-1450.
[http://dx.doi.org/10.1002/glia.22366] [PMID: 22653796]
[76]
Grabner, G.F.; Eichmann, T.O.; Wagner, B.; Gao, Y.; Farzi, A.; Taschler, U.; Radner, F.P.; Schweiger, M.; Lass, A.; Holzer, P.; Zinser, E.; Tschöp, M.H.; Yi, C.X.; Zimmermann, R. Deletion of monoglyceride lipase in astrocytes attenuates lipopolysaccharide-induced neuroinflammation. J. Biol. Chem., 2016, 291(2), 913-923.
[http://dx.doi.org/10.1074/jbc.M115.683615] [PMID: 26565024]
[77]
Bisicchia, E.; Chiurchiù, V.; Viscomi, M.T.; Latini, L.; Fezza, F.; Battistini, L.; Maccarrone, M.; Molinari, M. Activation of type-2 cannabinoid receptor inhibits neuroprotective and antiinflammatory actions of glucocorticoid receptor α: when one is better than two. Cell. Mol. Life Sci., 2013, 70(12), 2191-2204.
[http://dx.doi.org/10.1007/s00018-012-1253-5] [PMID: 23296125]
[78]
Berrendero, F.; Romero, J.; García-Gil, L.; Suarez, I.; De la Cruz, P.; Ramos, J.A.; Fernández-Ruiz, J.J. Changes in cannabinoid receptor binding and mRNA levels in several brain regions of aged rats. Biochim. Biophys. Acta, 1998, 1407(3), 205-214.
[http://dx.doi.org/10.1016/S0925-4439(98)00042-8] [PMID: 9748581]
[79]
Long, L.E.; Lind, J.; Webster, M.; Weickert, C.S. Developmental trajectory of the endocannabinoid system in human dorsolateral prefrontal cortex. BMC Neurosci., 2012, 13, 87.
[http://dx.doi.org/10.1186/1471-2202-13-87] [PMID: 22827915]
[80]
Wenger, T.; Gerendai, I.; Fezza, F.; González, S.; Bisogno, T.; Fernandez-Ruiz, J.; Di Marzo, V. The hypothalamic levels of the endocannabinoid, anandamide, peak immediately before the onset of puberty in female rats. Life Sci., 2002, 70(12), 1407-1414.
[http://dx.doi.org/10.1016/S0024-3205(01)01516-8] [PMID: 11883716]
[81]
Di Marzo, V.; Stella, N.; Zimmer, A. Endocannabinoid signalling and the deteriorating brain. Nat. Rev. Neurosci., 2015, 16(1), 30-42.
[http://dx.doi.org/10.1038/nrn3876] [PMID: 25524120]
[82]
Albayram, O.; Alferink, J.; Pitsch, J.; Piyanova, A.; Neitzert, K.; Poppensieker, K.; Mauer, D.; Michel, K.; Legler, A.; Becker, A.; Monory, K.; Lutz, B.; Zimmer, A.; Bilkei-Gorzo, A. Role of CB1 cannabinoid receptors on GABAergic neurons in brain aging. Proc. Natl. Acad. Sci. USA, 2011, 108(27), 11256-11261.
[http://dx.doi.org/10.1073/pnas.1016442108] [PMID: 21690345]
[83]
Bilkei-Gorzo, A.; Albayram, O.; Ativie, F.; Chasan, S.; Zimmer, T.; Bach, K.; Zimmer, A. Cannabinoid 1 receptor signaling on GABAergic neurons influences astrocytes in the ageing brain. PLoS One, 2018, 13(8), e0202566
[http://dx.doi.org/10.1371/journal.pone.0202566] [PMID: 30114280]
[84]
Stella, N. Cannabinoid and cannabinoid-like receptors in microglia, astrocytes, and astrocytomas. Glia, 2010, 58(9), 1017-1030.
[http://dx.doi.org/10.1002/glia.20983] [PMID: 20468046]
[85]
Ribeiro, R.; Yu, F.; Wen, J.; Vana, A.; Zhang, Y. Therapeutic potential of a novel cannabinoid agent CB52 in the mouse model of experimental autoimmune encephalomyelitis. Neuroscience, 2013, 254, 427-442.
[http://dx.doi.org/10.1016/j.neuroscience.2013.09.005] [PMID: 24036373]
[86]
Palazuelos, J.; Aguado, T.; Pazos, M.R.; Julien, B.; Carrasco, C.; Resel, E.; Sagredo, O.; Benito, C.; Romero, J.; Azcoitia, I.; Fernández-Ruiz, J.; Guzmán, M.; Galve-Roperh, I. Microglial CB2 cannabinoid receptors are neuroprotective in Huntington’s disease excitotoxicity. Brain, 2009, 132(Pt 11), 3152-3164.
[http://dx.doi.org/10.1093/brain/awp239] [PMID: 19805493]
[87]
Hardy, J. The amyloid hypothesis for Alzheimer’s disease: a critical reappraisal. J. Neurochem., 2009, 110(4), 1129-1134.
[http://dx.doi.org/10.1111/j.1471-4159.2009.06181.x] [PMID: 19457065]
[88]
Sastre, M.; Klockgether, T.; Heneka, M.T. Contribution of inflammatory processes to Alzheimer’s disease: molecular mechanisms. Int. J. Dev. Neurosci., 2006, 24(2-3), 167-176.
[http://dx.doi.org/10.1016/j.ijdevneu.2005.11.014] [PMID: 16472958]
[89]
White, J.A.; Manelli, A.M.; Holmberg, K.H.; Van Eldik, L.J.; Ladu, M.J. Differential effects of oligomeric and fibrillar amyloid-beta 1-42 on astrocyte-mediated inflammation. Neurobiol. Dis., 2005, 18(3), 459-465.
[http://dx.doi.org/10.1016/j.nbd.2004.12.013] [PMID: 15755672]
[90]
Marsicano, G.; Goodenough, S.; Monory, K.; Hermann, H.; Eder, M.; Cannich, A.; Azad, S.C.; Cascio, M.G.; Gutiérrez, S.O.; van der Stelt, M.; López-Rodriguez, M.L.; Casanova, E.; Schütz, G.; Zieglgänsberger, W.; Di Marzo, V.; Behl, C.; Lutz, B. CB1 cannabinoid receptors and on-demand defense against excitotoxicity. Science, 2003, 302(5642), 84-88.
[http://dx.doi.org/10.1126/science.1088208] [PMID: 14526074]
[91]
Mulder, J.; Zilberter, M.; Pasquaré, S.J.; Alpár, A.; Schulte, G.; Ferreira, S.G.; Köfalvi, A.; Martín-Moreno, A.M.; Keimpema, E.; Tanila, H.; Watanabe, M.; Mackie, K.; Hortobágyi, T.; de Ceballos, M.L.; Harkany, T. Molecular reorganization of endocannabinoid signalling in Alzheimer’s disease. Brain, 2011, 134(Pt 4), 1041-1060.
[http://dx.doi.org/10.1093/brain/awr046] [PMID: 21459826]
[92]
Jung, K.M.; Astarita, G.; Yasar, S.; Vasilevko, V.; Cribbs, D.H.; Head, E.; Cotman, C.W.; Piomelli, D. An amyloid β42-dependent deficit in anandamide mobilization is associated with cognitive dysfunction in Alzheimer’s disease. Neurobiol. Aging, 2012, 33(8), 1522-1532.
[http://dx.doi.org/10.1016/j.neurobiolaging.2011.03.012] [PMID: 21546126]
[93]
Benito, C.; Núñez, E.; Tolón, R.M.; Carrier, E.J.; Rábano, A.; Hillard, C.J.; Romero, J. Cannabinoid CB2 receptors and fatty acid amide hydrolase are selectively overexpressed in neuritic plaque-associated glia in Alzheimer’s disease brains. J. Neurosci., 2003, 23(35), 11136-11141.
[http://dx.doi.org/10.1523/JNEUROSCI.23-35-11136.2003] [PMID: 14657172]
[94]
Ramírez, B.G.; Blázquez, C.; Gómez del Pulgar, T.; Guzmán, M.; de Ceballos, M.L. Prevention of Alzheimer’s disease pathology by cannabinoids: neuroprotection mediated by blockade of microglial activation. J. Neurosci., 2005, 25(8), 1904-1913.
[http://dx.doi.org/10.1523/JNEUROSCI.4540-04.2005] [PMID: 15728830]
[95]
Ahmad, R.; Goffin, K.; Van den Stock, J.; De Winter, F.L.; Cleeren, E.; Bormans, G.; Tournoy, J.; Persoons, P.; Van Laere, K.; Vandenbulcke, M. In vivo type 1 cannabinoid receptor availability in Alzheimer’s disease. Eur. Neuropsychopharmacol., 2014, 24(2), 242-250.
[http://dx.doi.org/10.1016/j.euroneuro.2013.10.002] [PMID: 24189376]
[96]
Solas, M.; Francis, P.T.; Franco, R.; Ramírez, M.J. CB2 receptor and amyloid pathology in frontal cortex of Alzheimer’s disease patients. Neurobiol. Aging, 2013, 34(3), 805-808.
[http://dx.doi.org/10.1016/j.neurobiolaging.2012.06.005] [PMID: 22763024]
[97]
Currais, A.; Quehenberger, O.M.; Armando, A.; Daugherty, D.; Maher, P.; Schubert, D. Amyloid proteotoxicity initiates an inflammatory response blocked by cannabinoids. NPJ Aging Mech. Dis., 2016, 2, 16012.
[http://dx.doi.org/10.1038/npjamd.2016.12] [PMID: 28721267]
[98]
Ehrhart, J.; Obregon, D.; Mori, T.; Hou, H.; Sun, N.; Bai, Y.; Klein, T.; Fernandez, F.; Tan, J.; Shytle, R.D. Stimulation of cannabinoid receptor 2 (CB2) suppresses microglial activation. J. Neuroinflammation, 2005, 2, 29.
[http://dx.doi.org/10.1186/1742-2094-2-29] [PMID: 16343349]
[99]
Janefjord, E.; Mååg, J.L.; Harvey, B.S.; Smid, S.D. Cannabinoid effects on β amyloid fibril and aggregate formation, neuronal and microglial-activated neurotoxicity in vitro. Cell. Mol. Neurobiol., 2014, 34(1), 31-42.
[http://dx.doi.org/10.1007/s10571-013-9984-x] [PMID: 24030360]
[100]
Harvey, B.S.; Ohlsson, K.S.; Mååg, J.L.; Musgrave, I.F.; Smid, S.D. Contrasting protective effects of cannabinoids against oxidative stress and amyloid-β evoked neurotoxicity in vitro. Neurotoxicology, 2012, 33(1), 138-146.
[http://dx.doi.org/10.1016/j.neuro.2011.12.015] [PMID: 22233683]
[101]
van der Stelt, M.; Mazzola, C.; Esposito, G.; Matias, I.; Petrosino, S.; De Filippis, D.; Micale, V.; Steardo, L.; Drago, F.; Iuvone, T.; Di Marzo, V. Endocannabinoids and beta-amyloid-induced neurotoxicity in vivo: effect of pharmacological elevation of endocannabinoid levels. Cell. Mol. Life Sci., 2006, 63(12), 1410-1424.
[http://dx.doi.org/10.1007/s00018-006-6037-3] [PMID: 16732431]
[102]
Tanveer, R.; Gowran, A.; Noonan, J.; Keating, S.E.; Bowie, A.G.; Campbell, V.A. The endocannabinoid, anandamide, augments Notch-1 signaling in cultured cortical neurons exposed to amyloid-β and in the cortex of aged rats. J. Biol. Chem., 2012, 287(41), 34709-34721.
[http://dx.doi.org/10.1074/jbc.M112.350678] [PMID: 22891244]
[103]
Esposito, G.; Scuderi, C.; Valenza, M.; Togna, G.I.; Latina, V.; De Filippis, D.; Cipriano, M.; Carratù, M.R.; Iuvone, T.; Steardo, L. Cannabidiol reduces Aβ-induced neuroinflammation and promotes hippocampal neurogenesis through PPARγ involvement. PLoS One, 2011, 6(12), e28668
[http://dx.doi.org/10.1371/journal.pone.0028668] [PMID: 22163051]
[104]
Martín-Moreno, A.M.; Brera, B.; Spuch, C.; Carro, E.; García-García, L.; Delgado, M.; Pozo, M.A.; Innamorato, N.G.; Cuadrado, A.; de Ceballos, M.L. Prolonged oral cannabinoid administration prevents neuroinflammation, lowers β-amyloid levels and improves cognitive performance in Tg APP 2576 mice. J. Neuroinflammation, 2012, 9, 8.
[http://dx.doi.org/10.1186/1742-2094-9-8] [PMID: 22248049]
[105]
Bachmeier, C.; Beaulieu-Abdelahad, D.; Mullan, M.; Paris, D. Role of the cannabinoid system in the transit of beta-amyloid across the blood-brain barrier. Mol. Cell. Neurosci., 2013, 56, 255-262.
[http://dx.doi.org/10.1016/j.mcn.2013.06.004] [PMID: 23831388]
[106]
Aso, E.; Juvés, S.; Maldonado, R.; Ferrer, I. CB2 cannabinoid receptor agonist ameliorates Alzheimer-like phenotype in AβPP/PS1 mice. J. Alzheimers Dis., 2013, 35(4), 847-858.
[http://dx.doi.org/10.3233/JAD-130137] [PMID: 23515018]
[107]
Esposito, G.; De Filippis, D.; Steardo, L.; Scuderi, C.; Savani, C.; Cuomo, V.; Iuvone, T. CB1 receptor selective activation inhibits beta-amyloid-induced iNOS protein expression in C6 cells and subsequently blunts tau protein hyperphosphorylation in co-cultured neurons. Neurosci. Lett., 2006, 404(3), 342-346.
[http://dx.doi.org/10.1016/j.neulet.2006.06.012] [PMID: 16837132]
[108]
Aso, E.; Palomer, E.; Juvés, S.; Maldonado, R.; Muñoz, F.J.; Ferrer, I. CB1 agonist ACEA protects neurons and reduces the cognitive impairment of AβPP/PS1 mice. J. Alzheimers Dis., 2012, 30(2), 439-459.
[http://dx.doi.org/10.3233/JAD-2012-111862] [PMID: 22451318]
[109]
Walther, S.; Schüpbach, B.; Seifritz, E.; Homan, P.; Strik, W. Randomized, controlled crossover trial of dronabinol, 2.5 mg, for agitation in 2 patients with dementia. J. Clin. Psychopharmacol., 2011, 31(2), 256-258.
[http://dx.doi.org/10.1097/JCP.0b013e31820e861c] [PMID: 21364345]
[110]
Krishnan, S.; Cairns, R.; Howard, R. Cannabinoids for the treatment of dementia. Cochrane Database Syst. Rev., 2009, 2(2), CD007204
[PMID: 19370677]
[111]
Carroll, C.B.; Bain, P.G.; Teare, L.; Liu, X.; Joint, C.; Wroath, C.; Parkin, S.G.; Fox, P.; Wright, D.; Hobart, J.; Zajicek, J.P. Cannabis for dyskinesia in Parkinson disease: a randomized double-blind crossover study. Neurology, 2004, 63(7), 1245-1250.
[http://dx.doi.org/10.1212/01.WNL.0000140288.48796.8E] [PMID: 15477546]
[112]
Xu, J.Y.; Chen, C. Endocannabinoids in synaptic plasticity and neuroprotection. Neuroscientist, 2015, 21(2), 152-168.
[http://dx.doi.org/10.1177/1073858414524632] [PMID: 24571856]
[113]
Pisani, V.; Moschella, V.; Bari, M.; Fezza, F.; Galati, S.; Bernardi, G.; Stanzione, P.; Pisani, A.; Maccarrone, M. Dynamic changes of anandamide in the cerebrospinal fluid of Parkinson’s disease patients. Mov. Disord., 2010, 25(7), 920-924.
[http://dx.doi.org/10.1002/mds.23014] [PMID: 20461809]
[114]
de Lago, E.; de Miguel, R.; Lastres-Becker, I.; Ramos, J.A.; Fernández-Ruiz, J. Involvement of vanilloid-like receptors in the effects of anandamide on motor behavior and nigrostriatal dopaminergic activity: in vivo and in vitro evidence. Brain Res., 2004, 1007(1-2), 152-159.
[http://dx.doi.org/10.1016/j.brainres.2004.02.016] [PMID: 15064146]
[115]
Crawley, J.N.; Corwin, R.L.; Robinson, J.K.; Felder, C.C.; Devane, W.A.; Axelrod, J. Anandamide, an endogenous ligand of the cannabinoid receptor, induces hypomotility and hypothermia in vivo in rodents. Pharmacol. Biochem. Behav., 1993, 46(4), 967-972.
[http://dx.doi.org/10.1016/0091-3057(93)90230-Q] [PMID: 7906042]
[116]
Benarroch, E. Endocannabinoids in basal ganglia circuits: implications for Parkinson disease. Neurology, 2007, 69(3), 306-309.
[http://dx.doi.org/10.1212/01.wnl.0000267407.79757.75] [PMID: 17636069]
[117]
Adermark, L.; Talani, G.; Lovinger, D.M. Endocannabinoid-dependent plasticity at GABAergic and glutamatergic synapses in the striatum is regulated by synaptic activity. Eur. J. Neurosci., 2009, 29(1), 32-41.
[http://dx.doi.org/10.1111/j.1460-9568.2008.06551.x] [PMID: 19120438]
[118]
Lastres-Becker, I.; Cebeira, M.; de Ceballos, M.L.; Zeng, B.Y.; Jenner, P.; Ramos, J.A.; Fernández-Ruiz, J.J. Increased cannabinoid CB1 receptor binding and activation of GTP-binding proteins in the basal ganglia of patients with Parkinson’s syndrome and of MPTP-treated marmosets. Eur. J. Neurosci., 2001, 14(11), 1827-1832.
[http://dx.doi.org/10.1046/j.0953-816x.2001.01812.x] [PMID: 11860478]
[119]
van der Stelt, M.; Fox, S.H.; Hill, M.; Crossman, A.R.; Petrosino, S.; Di Marzo, V.; Brotchie, J.M. A role for endocannabinoids in the generation of parkinsonism and levodopa-induced dyskinesia in MPTP-lesioned non-human primate models of Parkinson’s disease. FASEB J., 2005, 19(9), 1140-1142.
[http://dx.doi.org/10.1096/fj.04-3010fje] [PMID: 15894565]
[120]
Van Laere, K.; Casteels, C.; Lunskens, S.; Goffin, K.; Grachev, I.D.; Bormans, G.; Vandenberghe, W. Regional changes in type 1 cannabinoid receptor availability in Parkinson’s disease in vivo. Neurobiol. Aging, 2012, 33(3), 620.e1-620.e8.
[http://dx.doi.org/10.1016/j.neurobiolaging.2011.02.009] [PMID: 21459482]
[121]
Lane, D.A.; Chan, J.; Lupica, C.R.; Pickel, V.M. Cannabinoid-1 receptor gene deletion has a compartment-specific affect on the dendritic and axonal availability of μ-opioid receptors and on dopamine axons in the mouse nucleus accumbens. Synapse, 2010, 64(12), 886-897.
[http://dx.doi.org/10.1002/syn.20807] [PMID: 20939059]
[122]
Pérez-Rial, S.; García-Gutiérrez, M.S.; Molina, J.A.; Pérez-Nievas, B.G.; Ledent, C.; Leiva, C.; Leza, J.C.; Manzanares, J. Increased vulnerability to 6-hydroxydopamine lesion and reduced development of dyskinesias in mice lacking CB1 cannabinoid receptors. Neurobiol. Aging, 2011, 32(4), 631-645.
[http://dx.doi.org/10.1016/j.neurobiolaging.2009.03.017] [PMID: 19419794]
[123]
Gómez-Gálvez, Y.; Palomo-Garo, C.; Fernández-Ruiz, J.; García, C. Potential of the cannabinoid CB(2) receptor as a pharmacological target against inflammation in Parkinson’s disease. Prog. Neuropsychopharmacol. Biol. Psychiatry, 2016, 64, 200-208.
[http://dx.doi.org/10.1016/j.pnpbp.2015.03.017] [PMID: 25863279]
[124]
Price, D.A.; Martinez, A.A.; Seillier, A.; Koek, W.; Acosta, Y.; Fernandez, E.; Strong, R.; Lutz, B.; Marsicano, G.; Roberts, J.L.; Giuffrida, A. WIN55,212-2, a cannabinoid receptor agonist, protects against nigrostriatal cell loss in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine mouse model of Parkinson’s disease. Eur. J. Neurosci., 2009, 29(11), 2177-2186.
[http://dx.doi.org/10.1111/j.1460-9568.2009.06764.x] [PMID: 19490092]
[125]
García, C.; Palomo-Garo, C.; García-Arencibia, M.; Ramos, J.; Pertwee, R.; Fernández-Ruiz, J. Symptom-relieving and neuroprotective effects of the phytocannabinoid Δ9-THCV in animal models of Parkinson’s disease. Br. J. Pharmacol., 2011, 163(7), 1495-1506.
[http://dx.doi.org/10.1111/j.1476-5381.2011.01278.x] [PMID: 21323909]
[126]
Ternianov, A.; Pérez-Ortiz, J.M.; Solesio, M.E.; García-Gutiérrez, M.S.; Ortega-Álvaro, A.; Navarrete, F.; Leiva, C.; Galindo, M.F.; Manzanares, J. Overexpression of CB2 cannabinoid receptors results in neuroprotection against behavioral and neurochemical alterations induced by intracaudate administration of 6-hydroxydopamine. Neurobiol. Aging, 2012, 33(2), 421.e1-421.e16.
[http://dx.doi.org/10.1016/j.neurobiolaging.2010.09.012] [PMID: 20980074]
[127]
Lastres-Becker, I.; Molina-Holgado, F.; Ramos, J.A.; Mechoulam, R.; Fernández-Ruiz, J. Cannabinoids provide neuroprotection against 6-hydroxydopamine toxicity in vivo and in vitro: relevance to Parkinson’s disease. Neurobiol. Dis., 2005, 19(1-2), 96-107.
[http://dx.doi.org/10.1016/j.nbd.2004.11.009] [PMID: 15837565]
[128]
Venderová, K.; Růzicka, E.; Vorísek, V.; Visnovský, P. Survey on cannabis use in Parkinson’s disease: subjective improvement of motor symptoms. Mov. Disord., 2004, 19(9), 1102-1106.
[http://dx.doi.org/10.1002/mds.20111] [PMID: 15372606]
[129]
Kindred, J.H.; Li, K.; Ketelhut, N.B.; Proessl, F.; Fling, B.W.; Honce, J.M.; Shaffer, W.R.; Rudroff, T. Cannabis use in people with Parkinson’s disease and Multiple Sclerosis: A web-based investigation. Complement. Ther. Med., 2017, 33, 99-104.
[http://dx.doi.org/10.1016/j.ctim.2017.07.002] [PMID: 28735833]
[130]
Sieradzan, K.A.; Fox, S.H.; Hill, M.; Dick, J.P.; Crossman, A.R.; Brotchie, J.M. Cannabinoids reduce levodopa-induced dyskinesia in Parkinson’s disease: a pilot study. Neurology, 2001, 57(11), 2108-2111.
[http://dx.doi.org/10.1212/WNL.57.11.2108] [PMID: 11739835]
[131]
Mesnage, V.; Houeto, J.L.; Bonnet, A.M.; Clavier, I.; Arnulf, I.; Cattelin, F.; Le Fur, G.; Damier, P.; Welter, M.L.; Agid, Y. Neurokinin B, neurotensin, and cannabinoid receptor antagonists and Parkinson disease. Clin. Neuropharmacol., 2004, 27(3), 108-110.
[http://dx.doi.org/10.1097/00002826-200405000-00003] [PMID: 15190231]
[132]
de Lago, E.; Moreno-Martet, M.; Cabranes, A.; Ramos, J.A.; Fernández-Ruiz, J. Cannabinoids ameliorate disease progression in a model of multiple sclerosis in mice, acting preferentially through CB1 receptor-mediated anti-inflammatory effects. Neuropharmacology, 2012, 62(7), 2299-2308.
[http://dx.doi.org/10.1016/j.neuropharm.2012.01.030] [PMID: 22342378]
[133]
Kozela, E.; Juknat, A.; Kaushansky, N.; Rimmerman, N.; Ben-Nun, A.; Vogel, Z. Cannabinoids decrease the th17 inflammatory autoimmune phenotype. J. Neuroimmune Pharmacol., 2013, 8(5), 1265-1276.
[http://dx.doi.org/10.1007/s11481-013-9493-1] [PMID: 23892791]
[134]
Sido, J.M.; Nagarkatti, P.S.; Nagarkatti, M. Role of Endocannabinoid Activation of Peripheral CB1 Receptors in the Regulation of Autoimmune Disease. Int. Rev. Immunol., 2015, 34(5), 403-414.
[http://dx.doi.org/10.3109/08830185.2014.921165] [PMID: 24911431]
[135]
Loría, F.; Petrosino, S.; Hernangómez, M.; Mestre, L.; Spagnolo, A.; Correa, F.; Di Marzo, V.; Docagne, F.; Guaza, C. An endocannabinoid tone limits excitotoxicity in vitro and in a model of multiple sclerosis. Neurobiol. Dis., 2010, 37(1), 166-176.
[http://dx.doi.org/10.1016/j.nbd.2009.09.020] [PMID: 19815071]
[136]
Lourbopoulos, A.; Grigoriadis, N.; Lagoudaki, R.; Touloumi, O.; Polyzoidou, E.; Mavromatis, I.; Tascos, N.; Breuer, A.; Ovadia, H.; Karussis, D.; Shohami, E.; Mechoulam, R.; Simeonidou, C. Administration of 2-arachidonoylglycerol ameliorates both acute and chronic experimental autoimmune encephalomyelitis. Brain Res., 2011, 1390, 126-141.
[http://dx.doi.org/10.1016/j.brainres.2011.03.020] [PMID: 21406188]
[137]
Arellano, G.; Acuña, E.; Reyes, L.I.; Ottum, P.A.; De Sarno, P.; Villarroel, L.; Ciampi, E.; Uribe-San Martín, R.; Cárcamo, C.; Naves, R. Th1 and Th17 Cells and Associated Cytokines Discriminate among Clinically Isolated Syndrome and Multiple Sclerosis Phenotypes. Front. Immunol., 2017, 8, 753.
[http://dx.doi.org/10.3389/fimmu.2017.00753] [PMID: 28713377]
[138]
Kozela, E.; Lev, N.; Kaushansky, N.; Eilam, R.; Rimmerman, N.; Levy, R.; Ben-Nun, A.; Juknat, A.; Vogel, Z. Cannabidiol inhibits pathogenic T cells, decreases spinal microglial activation and ameliorates multiple sclerosis-like disease in C57BL/6 mice. Br. J. Pharmacol., 2011, 163(7), 1507-1519.
[http://dx.doi.org/10.1111/j.1476-5381.2011.01379.x] [PMID: 21449980]
[139]
Mecha, M.; Yanguas-Casás, N.; Feliú, A.; Mestre, L.; Carrillo-Salinas, F.; Azcoitia, I.; Yong, V.W.; Guaza, C. The endocannabinoid 2-AG enhances spontaneous remyelination by targeting microglia. Brain Behav. Immun., 2019, 77, 110-126.
[http://dx.doi.org/10.1016/j.bbi.2018.12.013] [PMID: 30582962]
[140]
Maresz, K.; Pryce, G.; Ponomarev, E.D.; Marsicano, G.; Croxford, J.L.; Shriver, L.P.; Ledent, C.; Cheng, X.; Carrier, E.J.; Mann, M.K.; Giovannoni, G.; Pertwee, R.G.; Yamamura, T.; Buckley, N.E.; Hillard, C.J.; Lutz, B.; Baker, D.; Dittel, B.N. Direct suppression of CNS autoimmune inflammation via the cannabinoid receptor CB1 on neurons and CB2 on autoreactive T cells. Nat. Med., 2007, 13(4), 492-497.
[http://dx.doi.org/10.1038/nm1561] [PMID: 17401376]
[141]
Kong, W.; Li, H.; Tuma, R.F.; Ganea, D. Selective CB2 receptor activation ameliorates EAE by reducing Th17 differentiation and immune cell accumulation in the CNS. Cell. Immunol., 2014, 287(1), 1-17.
[http://dx.doi.org/10.1016/j.cellimm.2013.11.002] [PMID: 24342422]
[142]
Zajicek, J.; Fox, P.; Sanders, H.; Wright, D.; Vickery, J.; Nunn, A.; Thompson, A. Cannabinoids for treatment of spasticity and other symptoms related to multiple sclerosis (CAMS study): multicentre randomised placebo-controlled trial. Lancet, 2003, 362(9395), 1517-1526.
[http://dx.doi.org/10.1016/S0140-6736(03)14738-1] [PMID: 14615106]
[143]
Lutz, B.; Marsicano, G.; Maldonado, R.; Hillard, C.J. The endocannabinoid system in guarding against fear, anxiety and stress. Nat. Rev. Neurosci., 2015, 16(12), 705-718.
[http://dx.doi.org/10.1038/nrn4036] [PMID: 26585799]
[144]
Rubino, T.; Guidali, C.; Vigano, D.; Realini, N.; Valenti, M.; Massi, P.; Parolaro, D. CB1 receptor stimulation in specific brain areas differently modulate anxiety-related behaviour. Neuropharmacology, 2008, 54(1), 151-160.
[http://dx.doi.org/10.1016/j.neuropharm.2007.06.024] [PMID: 17692344]
[145]
Shonesy, B.C.; Bluett, R.J.; Ramikie, T.S.; Báldi, R.; Hermanson, D.J.; Kingsley, P.J.; Marnett, L.J.; Winder, D.G.; Colbran, R.J.; Patel, S. Genetic disruption of 2-arachidonoylglycerol synthesis reveals a key role for endocannabinoid signaling in anxiety modulation. Cell Rep., 2014, 9(5), 1644-1653.
[http://dx.doi.org/10.1016/j.celrep.2014.11.001] [PMID: 25466252]
[146]
Wyrofsky, R.; McGonigle, P.; Van Bockstaele, E.J. Drug discovery strategies that focus on the endocannabinoid signaling system in psychiatric disease. Expert Opin. Drug Discov., 2015, 10(1), 17-36.
[http://dx.doi.org/10.1517/17460441.2014.966680] [PMID: 25488672]
[147]
Tao, R.; Ma, Z. Neural circuit in the dorsal raphe nucleus responsible for cannabinoid-mediated increases in 5-HT efflux in the nucleus accumbens of the rat brain. ISRN Pharmacol., 2012, 2012, 276902
[http://dx.doi.org/10.5402/2012/276902] [PMID: 22830043]
[148]
Large, M.; Sharma, S.; Compton, M.T.; Slade, T.; Nielssen, O. Cannabis use and earlier onset of psychosis: a systematic meta-analysis. Arch. Gen. Psychiatry, 2011, 68(6), 555-561.
[http://dx.doi.org/10.1001/archgenpsychiatry.2011.5] [PMID: 21300939]
[149]
Fusar-Poli, P.; Crippa, J.A.; Bhattacharyya, S.; Borgwardt, S.J.; Allen, P.; Martin-Santos, R.; Seal, M.; Surguladze, S.A.; O’Carrol, C.; Atakan, Z.; Zuardi, A.W.; McGuire, P.K. Distinct effects of delta9-tetrahydrocannabinol and cannabidiol on neural activation during emotional processing. Arch. Gen. Psychiatry, 2009, 66(1), 95-105.
[http://dx.doi.org/10.1001/archgenpsychiatry.2008.519] [PMID: 19124693]
[150]
Hill, M.N.; McLaughlin, R.J.; Morrish, A.C.; Viau, V.; Floresco, S.B.; Hillard, C.J.; Gorzalka, B.B. Suppression of amygdalar endocannabinoid signaling by stress contributes to activation of the hypothalamic-pituitary-adrenal axis. Neuropsychopharmacology, 2009, 34(13), 2733-2745.
[http://dx.doi.org/10.1038/npp.2009.114] [PMID: 19710634]
[151]
Di, S.; Malcher-Lopes, R.; Marcheselli, V.L.; Bazan, N.G.; Tasker, J.G. Rapid glucocorticoid-mediated endocannabinoid release and opposing regulation of glutamate and γ-aminobutyric acid inputs to hypothalamic magnocellular neurons. Endocrinology, 2005, 146(10), 4292-4301.
[http://dx.doi.org/10.1210/en.2005-0610] [PMID: 15994343]
[152]
Hill, M.N.; Kumar, S.A.; Filipski, S.B.; Iverson, M.; Stuhr, K.L.; Keith, J.M.; Cravatt, B.F.; Hillard, C.J.; Chattarji, S.; McEwen, B.S. Disruption of fatty acid amide hydrolase activity prevents the effects of chronic stress on anxiety and amygdalar microstructure. Mol. Psychiatry, 2013, 18(10), 1125-1135.
[http://dx.doi.org/10.1038/mp.2012.90] [PMID: 22776900]
[153]
Busquets-Garcia, A.; Gomis-González, M.; Srivastava, R.K.; Cutando, L.; Ortega-Alvaro, A.; Ruehle, S.; Remmers, F.; Bindila, L.; Bellocchio, L.; Marsicano, G.; Lutz, B.; Maldonado, R.; Ozaita, A. Peripheral and central CB1 cannabinoid receptors control stress-induced impairment of memory consolidation. Proc. Natl. Acad. Sci. USA, 2016, 113(35), 9904-9909.
[http://dx.doi.org/10.1073/pnas.1525066113] [PMID: 27528659]
[154]
Ishiguro, H.; Horiuchi, Y.; Tabata, K.; Liu, Q.R.; Arinami, T.; Onaivi, E.S. Cannabinoid CB2 Receptor Gene and Environmental Interaction in the Development of Psychiatric Disorders. Molecules, 2018, 23(8), e1836
[http://dx.doi.org/10.3390/molecules23081836] [PMID: 30042304]
[155]
Howren, M.B.; Lamkin, D.M.; Suls, J. Associations of depression with C-reactive protein, IL-1, and IL-6: a meta-analysis. Psychosom. Med., 2009, 71(2), 171-186.
[http://dx.doi.org/10.1097/PSY.0b013e3181907c1b] [PMID: 19188531]
[156]
Dowlati, Y.; Herrmann, N.; Swardfager, W.; Liu, H.; Sham, L.; Reim, E.K.; Lanctôt, K.L. A meta-analysis of cytokines in major depression. Biol. Psychiatry, 2010, 67(5), 446-457.
[http://dx.doi.org/10.1016/j.biopsych.2009.09.033] [PMID: 20015486]
[157]
Asnis, G.M.; De La Garza, R. II Interferon-induced depression in chronic hepatitis C: a review of its prevalence, risk factors, biology, and treatment approaches. J. Clin. Gastroenterol., 2006, 40(4), 322-335.
[http://dx.doi.org/10.1097/01.mcg.0000210099.36500.fe] [PMID: 16633105]
[158]
Tyring, S.; Gottlieb, A.; Papp, K.; Gordon, K.; Leonardi, C.; Wang, A.; Lalla, D.; Woolley, M.; Jahreis, A.; Zitnik, R.; Cella, D.; Krishnan, R. Etanercept and clinical outcomes, fatigue, and depression in psoriasis: double-blind placebo-controlled randomised phase III trial. Lancet, 2006, 367(9504), 29-35.
[http://dx.doi.org/10.1016/S0140-6736(05)67763-X] [PMID: 16399150]
[159]
Hinwood, M.; Morandini, J.; Day, T.A.; Walker, F.R. Evidence that microglia mediate the neurobiological effects of chronic psychological stress on the medial prefrontal cortex. Cereb. Cortex, 2012, 22(6), 1442-1454.
[http://dx.doi.org/10.1093/cercor/bhr229] [PMID: 21878486]
[160]
Su, F.; Yi, H.; Xu, L.; Zhang, Z. Fluoxetine and S-citalopram inhibit M1 activation and promote M2 activation of microglia in vitro. Neuroscience, 2015, 294, 60-68.
[http://dx.doi.org/10.1016/j.neuroscience.2015.02.028] [PMID: 25711936]
[161]
Moreira, F.A.; Grieb, M.; Lutz, B. Central side-effects of therapies based on CB1 cannabinoid receptor agonists and antagonists: focus on anxiety and depression. Best Pract. Res. Clin. Endocrinol. Metab., 2009, 23(1), 133-144.
[http://dx.doi.org/10.1016/j.beem.2008.09.003] [PMID: 19285266]
[162]
Habib, A.M.; Okorokov, A.L.; Hill, M.N.; Bras, J.T.; Lee, M.C.; Li, S.; Gossage, S.J.; van Drimmelen, M.; Morena, M.; Houlden, H.; Ramirez, J.D.; Bennett, D.L.H.; Srivastava, D.; Cox, J.J. Microdeletion in a FAAH pseudogene identified in a patient with high anandamide concentrations and pain insensitivity. Br. J. Anaesth., 2019, 123(2), e249-e253.
[http://dx.doi.org/10.1016/j.bja.2019.02.019] [PMID: 30929760]
[163]
Cravatt, B.F.; Demarest, K.; Patricelli, M.P.; Bracey, M.H.; Giang, D.K.; Martin, B.R.; Lichtman, A.H. Supersensitivity to anandamide and enhanced endogenous cannabinoid signaling in mice lacking fatty acid amide hydrolase. Proc. Natl. Acad. Sci. USA, 2001, 98(16), 9371-9376.
[http://dx.doi.org/10.1073/pnas.161191698] [PMID: 11470906]
[164]
Lichtman, A.H.; Shelton, C.C.; Advani, T.; Cravatt, B.F. Mice lacking fatty acid amide hydrolase exhibit a cannabinoid receptor-mediated phenotypic hypoalgesia. Pain, 2004, 109(3), 319-327.
[http://dx.doi.org/10.1016/j.pain.2004.01.022] [PMID: 15157693]
[165]
Huggins, J.P.; Smart, T.S.; Langman, S.; Taylor, L.; Young, T. An efficient randomised, placebo-controlled clinical trial with the irreversible fatty acid amide hydrolase-1 inhibitor PF-04457845, which modulates endocannabinoids but fails to induce effective analgesia in patients with pain due to osteoarthritis of the knee. Pain, 2012, 153(9), 1837-1846.
[http://dx.doi.org/10.1016/j.pain.2012.04.020] [PMID: 22727500]
[166]
Kerbrat, A.; Ferré, J.C.; Fillatre, P.; Ronzière, T.; Vannier, S.; Carsin-Nicol, B.; Lavoué, S.; Vérin, M.; Gauvrit, J.Y.; Le Tulzo, Y.; Edan, G. Acute neurologic disorder from an inhibitor of fatty acid amide hydrolase. N. Engl. J. Med., 2016, 375(18), 1717-1725.
[http://dx.doi.org/10.1056/NEJMoa1604221] [PMID: 27806235]
[167]
Calignano, A.; La Rana, G.; Giuffrida, A.; Piomelli, D. Control of pain initiation by endogenous cannabinoids. Nature, 1998, 394(6690), 277-281.
[http://dx.doi.org/10.1038/28393] [PMID: 9685157]
[168]
Guindon, J.; Desroches, J.; Beaulieu, P. The antinociceptive effects of intraplantar injections of 2-arachidonoyl glycerol are mediated by cannabinoid CB2 receptors. Br. J. Pharmacol., 2007, 150(6), 693-701.
[http://dx.doi.org/10.1038/sj.bjp.0706990] [PMID: 17179944]
[169]
Dziadulewicz, E.K.; Bevan, S.J.; Brain, C.T.; Coote, P.R.; Culshaw, A.J.; Davis, A.J.; Edwards, L.J.; Fisher, A.J.; Fox, A.J.; Gentry, C.; Groarke, A.; Hart, T.W.; Huber, W.; James, I.F.; Kesingland, A.; La Vecchia, L.; Loong, Y.; Lyothier, I.; McNair, K.; O’Farrell, C.; Peacock, M.; Portmann, R.; Schopfer, U.; Yaqoob, M.; Zadrobilek, J. Naphthalen-1-yl-(4-pentyloxynaphthalen-1-yl)methanone: a potent, orally bioavailable human CB1/CB2 dual agonist with antihyperalgesic properties and restricted central nervous system penetration. J. Med. Chem., 2007, 50(16), 3851-3856.
[http://dx.doi.org/10.1021/jm070317a] [PMID: 17630726]
[170]
Agarwal, N.; Pacher, P.; Tegeder, I.; Amaya, F.; Constantin, C.E.; Brenner, G.J.; Rubino, T.; Michalski, C.W.; Marsicano, G.; Monory, K.; Mackie, K.; Marian, C.; Batkai, S.; Parolaro, D.; Fischer, M.J.; Reeh, P.; Kunos, G.; Kress, M.; Lutz, B.; Woolf, C.J.; Kuner, R. Cannabinoids mediate analgesia largely via peripheral type 1 cannabinoid receptors in nociceptors. Nat. Neurosci., 2007, 10(7), 870-879.
[http://dx.doi.org/10.1038/nn1916] [PMID: 17558404]
[171]
Walker, J.M.; Hohmann, A.G.; Martin, W.J.; Strangman, N.M.; Huang, S.M.; Tsou, K. The neurobiology of cannabinoid analgesia. Life Sci., 1999, 65(6-7), 665-673.
[http://dx.doi.org/10.1016/S0024-3205(99)00289-1] [PMID: 10462067]
[172]
Racz, I.; Nadal, X.; Alferink, J.; Baños, J.E.; Rehnelt, J.; Martín, M.; Pintado, B.; Gutierrez-Adan, A.; Sanguino, E.; Manzanares, J.; Zimmer, A.; Maldonado, R. Crucial role of CB(2) cannabinoid receptor in the regulation of central immune responses during neuropathic pain. J. Neurosci., 2008, 28(46), 12125-12135.
[http://dx.doi.org/10.1523/JNEUROSCI.3400-08.2008] [PMID: 19005077]
[173]
Clark, A.K.; Yip, P.K.; Grist, J.; Gentry, C.; Staniland, A.A.; Marchand, F.; Dehvari, M.; Wotherspoon, G.; Winter, J.; Ullah, J.; Bevan, S.; Malcangio, M. Inhibition of spinal microglial cathepsin S for the reversal of neuropathic pain. Proc. Natl. Acad. Sci. USA, 2007, 104(25), 10655-10660.
[http://dx.doi.org/10.1073/pnas.0610811104] [PMID: 17551020]
[174]
Nent, E.; Nozaki, C.; Schmöle, A.C.; Otte, D.; Zimmer, A. CB2 receptor deletion on myeloid cells enhanced mechanical allodynia in a mouse model of neuropathic pain. Sci. Rep., 2019, 9(1), 7468.
[http://dx.doi.org/10.1038/s41598-019-43858-4] [PMID: 31097758]
[175]
Sokal, D.M.; Elmes, S.J.R.; Kendall, D.A.; Chapman, V. Intraplantar injection of anandamide inhibits mechanically-evoked responses of spinal neurones via activation of CB2 receptors in anaesthetised rats. Neuropharmacology, 2003, 45(3), 404-411.
[http://dx.doi.org/10.1016/S0028-3908(03)00195-3] [PMID: 12871657]
[176]
Nackley, A.G.; Zvonok, A.M.; Makriyannis, A.; Hohmann, A.G. 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(6), 3562-3574.
[http://dx.doi.org/10.1152/jn.00886.2003] [PMID: 15317842]
[177]
LaBuda, C.J.; Koblish, M.; Little, P.J. Cannabinoid CB2 receptor agonist activity in the hindpaw incision model of postoperative pain. Eur. J. Pharmacol., 2005, 527(1-3), 172-174.
[http://dx.doi.org/10.1016/j.ejphar.2005.10.020] [PMID: 16316653]
[178]
Hohmann, A.G.; Farthing, J.N.; Zvonok, A.M.; Makriyannis, A. Selective activation of cannabinoid CB2 receptors suppresses hyperalgesia evoked by intradermal capsaicin. J. Pharmacol. Exp. Ther., 2004, 308(2), 446-453.
[http://dx.doi.org/10.1124/jpet.103.060079] [PMID: 14610224]
[179]
Beltramo, M.; Bernardini, N.; Bertorelli, R.; Campanella, M.; Nicolussi, E.; Fredduzzi, S.; Reggiani, A. CB2 receptor-mediated antihyperalgesia: possible direct involvement of neural mechanisms. Eur. J. Neurosci., 2006, 23(6), 1530-1538.
[http://dx.doi.org/10.1111/j.1460-9568.2006.04684.x] [PMID: 16553616]
[180]
Pertwee, R.G.; Howlett, A.C.; Abood, M.E.; Alexander, S.P.; Di Marzo, V.; Elphick, M.R.; Greasley, P.J.; Hansen, H.S.; Kunos, G.; Mackie, K.; Mechoulam, R.; Ross, R.A. International Union of Basic and Clinical Pharmacology. LXXIX. Cannabinoid receptors and their ligands: beyond CB1 and CB2. Pharmacol. Rev., 2010, 62(4), 588-631.
[http://dx.doi.org/10.1124/pr.110.003004] [PMID: 21079038]
[181]
Ryberg, E.; Larsson, N.; Sjögren, S.; Hjorth, S.; Hermansson, N.O.; Leonova, J.; Elebring, T.; Nilsson, K.; Drmota, T.; Greasley, P.J. The orphan receptor GPR55 is a novel cannabinoid receptor. Br. J. Pharmacol., 2007, 152(7), 1092-1101.
[http://dx.doi.org/10.1038/sj.bjp.0707460] [PMID: 17876302]
[182]
Waldeck-Weiermair, M.; Zoratti, C.; Osibow, K.; Balenga, N.; Goessnitzer, E.; Waldhoer, M.; Malli, R.; Graier, W.F. Integrin clustering enables anandamide-induced Ca2+ signaling in endothelial cells via GPR55 by protection against CB1-receptor-triggered repression. J. Cell Sci., 2008, 121(Pt 10), 1704-1717.
[http://dx.doi.org/10.1242/jcs.020958] [PMID: 18445684]
[183]
Oka, S.; Nakajima, K.; Yamashita, A.; Kishimoto, S.; Sugiura, T. Identification of GPR55 as a lysophosphatidylinositol receptor. Biochem. Biophys. Res. Commun., 2007, 362(4), 928-934.
[http://dx.doi.org/10.1016/j.bbrc.2007.08.078] [PMID: 17765871]
[184]
Kapur, A.; Zhao, P.; Sharir, H.; Bai, Y.; Caron, M.G.; Barak, L.S.; Abood, M.E. Atypical responsiveness of the orphan receptor GPR55 to cannabinoid ligands. J. Biol. Chem., 2009, 284(43), 29817-29827.
[http://dx.doi.org/10.1074/jbc.M109.050187] [PMID: 19723626]
[185]
Shi, Q.X.; Yang, L.K.; Shi, W.L.; Wang, L.; Zhou, S.M.; Guan, S.Y.; Zhao, M.G.; Yang, Q. The novel cannabinoid receptor GPR55 mediates anxiolytic-like effects in the medial orbital cortex of mice with acute stress. Mol. Brain, 2017, 10(1), 38.
[http://dx.doi.org/10.1186/s13041-017-0318-7] [PMID: 28800762]
[186]
Lagalwar, S.; Bordayo, E.Z.; Hoffmann, K.L.; Fawcett, J.R.; Frey, W.H., II Anandamides inhibit binding to the muscarinic acetylcholine receptor. J. Mol. Neurosci., 1999, 13(1-2), 55-61.
[http://dx.doi.org/10.1385/JMN:13:1-2:55] [PMID: 10691292]
[187]
Savinainen, J.R.; Saario, S.M.; Niemi, R.; Järvinen, T.; Laitinen, J.T. An optimized approach to study endocannabinoid signaling: evidence against constitutive activity of rat brain adenosine A1 and cannabinoid CB1 receptors. Br. J. Pharmacol., 2003, 140(8), 1451-1459.
[http://dx.doi.org/10.1038/sj.bjp.0705577] [PMID: 14623770]
[188]
Kimura, T.; Ohta, T.; Watanabe, K.; Yoshimura, H.; Yamamoto, I. Anandamide, an endogenous cannabinoid receptor ligand, also interacts with 5-hydroxytryptamine (5-HT) receptor. Biol. Pharm. Bull., 1998, 21(3), 224-226.
[http://dx.doi.org/10.1248/bpb.21.224] [PMID: 9556149]
[189]
Hillard, C.J.; Bloom, A.S. delta 9-Tetrahydrocannabinol-induced changes in beta-adrenergic receptor binding in mouse cerebral cortex. Brain Res., 1982, 235(2), 370-377.
[http://dx.doi.org/10.1016/0006-8993(82)91016-2] [PMID: 6329417]
[190]
Croxford, J.L. Therapeutic potential of cannabinoids in CNS disease. CNS Drugs, 2003, 17(3), 179-202.
[http://dx.doi.org/10.2165/00023210-200317030-00004] [PMID: 12617697]
[191]
Venkatachalam, K.; Montell, C. TRP channels. Annu. Rev. Biochem., 2007, 76, 387-417.
[http://dx.doi.org/10.1146/annurev.biochem.75.103004.142819] [PMID: 17579562]
[192]
Starowicz, K.; Nigam, S.; Di Marzo, V. Biochemistry and pharmacology of endovanilloids. Pharmacol. Ther., 2007, 114(1), 13-33.
[http://dx.doi.org/10.1016/j.pharmthera.2007.01.005] [PMID: 17349697]
[193]
Di Marzo, V.; De Petrocellis, L.; Fezza, F.; Ligresti, A.; Bisogno, T. Anandamide receptors. Prostaglandins Leukot. Essent. Fatty Acids, 2002, 66(2-3), 377-391.
[http://dx.doi.org/10.1054/plef.2001.0349] [PMID: 12052051]
[194]
Akopian, A.N.; Ruparel, N.B.; Jeske, N.A.; Patwardhan, A.; Hargreaves, K.M. Role of ionotropic cannabinoid receptors in peripheral antinociception and antihyperalgesia. Trends Pharmacol. Sci., 2009, 30(2), 79-84.
[http://dx.doi.org/10.1016/j.tips.2008.10.008] [PMID: 19070372]
[195]
Ryskamp, D.A.; Redmon, S.; Jo, A.O.; Križaj, D. TRPV1 and endocannabinoids: emerging molecular signals that modulate mammalian vision. Cells, 2014, 3(3), 914-938.
[http://dx.doi.org/10.3390/cells3030914] [PMID: 25222270]
[196]
Lowin, T.; Straub, R.H. Cannabinoid-based drugs targeting CB1 and TRPV1, the sympathetic nervous system, and arthritis. Arthritis Res. Ther., 2015, 17, 226.
[http://dx.doi.org/10.1186/s13075-015-0743-x] [PMID: 26343051]
[197]
Oz, M.; Tchugunova, Y.B.; Dunn, S.M. Endogenous cannabinoid anandamide directly inhibits voltage-dependent Ca(2+) fluxes in rabbit T-tubule membranes. Eur. J. Pharmacol., 2000, 404(1-2), 13-20.
[http://dx.doi.org/10.1016/S0014-2999(00)00396-4] [PMID: 10980258]
[198]
Oz, M.; Yang, K.H.; Dinc, M.; Shippenberg, T.S. The endogenous cannabinoid anandamide inhibits cromakalim-activated K+ currents in follicle-enclosed Xenopus oocytes. J. Pharmacol. Exp. Ther., 2007, 323(2), 547-554.
[http://dx.doi.org/10.1124/jpet.107.125336] [PMID: 17682128]
[199]
Nicholson, R.A.; Liao, C.; Zheng, J.; David, L.S.; Coyne, L.; Errington, A.C.; Singh, G.; Lees, G. Sodium channel inhibition by anandamide and synthetic cannabimimetics in brain. Brain Res., 2003, 978(1-2), 194-204.
[http://dx.doi.org/10.1016/S0006-8993(03)02808-7] [PMID: 12834914]
[200]
Michalik, L.; Auwerx, J.; Berger, J.P.; Chatterjee, V.K.; Glass, C.K.; Gonzalez, F.J.; Grimaldi, P.A.; Kadowaki, T.; Lazar, M.A.; O’Rahilly, S.; Palmer, C.N.; Plutzky, J.; Reddy, J.K.; Spiegelman, B.M.; Staels, B.; Wahli, W. International Union of Pharmacology. LXI. Peroxisome proliferator-activated receptors. Pharmacol. Rev., 2006, 58(4), 726-741.
[http://dx.doi.org/10.1124/pr.58.4.5] [PMID: 17132851]
[201]
Bouaboula, M.; Hilairet, S.; Marchand, J.; Fajas, L.; Le Fur, G.; Casellas, P. Anandamide induced PPARgamma transcriptional activation and 3T3-L1 preadipocyte differentiation. Eur. J. Pharmacol., 2005, 517(3), 174-181.
[http://dx.doi.org/10.1016/j.ejphar.2005.05.032] [PMID: 15987634]
[202]
Ghosh, M.; Wang, H.; Ai, Y.; Romeo, E.; Luyendyk, J.P.; Peters, J.M.; Mackman, N.; Dey, S.K.; Hla, T. COX-2 suppresses tissue factor expression via endocannabinoid-directed PPARdelta activation. J. Exp. Med., 2007, 204(9), 2053-2061.
[http://dx.doi.org/10.1084/jem.20070828] [PMID: 17724132]
[203]
D’Agostino, G.; La Rana, G.; Russo, R.; Sasso, O.; Iacono, A.; Esposito, E. Acute intracerebroventricular administration of palmitoylethanolamide, an endogenous PPAR-agonist, modulates carrageenan-Induced paw edema in mice. J. Pharmacol. Exp. Ther., 2007, 322, 1137-1143.
[http://dx.doi.org/10.1124/jpet.107.123265] [PMID: 17565008]
[204]
LoVerme, J.; Russo, R.; La Rana, G.; Fu, J.; Farthing, J.; Mattace-Raso, G.; Meli, R.; Hohmann, A.; Calignano, A.; Piomelli, D. Rapid broad-spectrum analgesia through activation of peroxisome proliferator-activated receptor-alpha. J. Pharmacol. Exp. Ther., 2006, 319(3), 1051-1061.
[http://dx.doi.org/10.1124/jpet.106.111385] [PMID: 16997973]
[205]
Landreth, G.; Jiang, Q.; Mandrekar, S.; Heneka, M. PPARgamma agonists as therapeutics for the treatment of Alzheimer’s disease. Neurotherapeutics, 2008, 5(3), 481-489.
[http://dx.doi.org/10.1016/j.nurt.2008.05.003] [PMID: 18625459]
[206]
Altamura, C.; Ventriglia, M.; Martini, M.G.; Montesano, D.; Errante, Y.; Piscitelli, F.; Scrascia, F.; Quattrocchi, C.; Palazzo, P.; Seccia, S.; Vernieri, F.; Di Marzo, V. Elevation of Plasma 2-Arachidonoylglycerol Levels in Alzheimer’s Disease patients as a potential protective mechanism against neurodegenerative decline. J. Alzheimers Dis., 2015, 46(2), 497-506.
[http://dx.doi.org/10.3233/JAD-142349] [PMID: 25818503]
[207]
Pertwee, R.G. Emerging strategies for exploiting cannabinoid receptor agonists as medicines. Br. J. Pharmacol., 2009, 156(3), 397-411.
[http://dx.doi.org/10.1111/j.1476-5381.2008.00048.x] [PMID: 19226257]


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Article Details

VOLUME: 18
ISSUE: 8
Year: 2020
Published on: 09 September, 2020
Page: [769 - 787]
Pages: 19
DOI: 10.2174/1570159X18666200217140255
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