94
Views
1
CrossRef citations to date
0
Altmetric
Review

The bright side of psychoactive substances: cannabinoid-based drugs in motor diseases

&
Pages 1351-1362 | Received 23 May 2016, Accepted 30 Jun 2016, Published online: 19 Jul 2016

References

  • Mechoulam R, Parker LA. The endocannabinoid system and the brain. Annu Rev Psychol. 2013;64:21–47.
  • Howlett AC. Cannabinoid receptor signaling. Handb Exp Pharmacol. 2005;168:53–79.
  • Fezza F, Bari M, Florio R, et al. Endocannabinoids, related compounds and their metabolic routes. Molecules. 2014;19:17078–17106.
  • Lu CH, Mackie K. An introduction to the endogenous cannabinoid system. Biol Psychiatry. 2016;79:516–525.
  • De Petrocellis L, Di Marzo V. Non-CB1, non-CB2 receptors for endocannabinoids, plant cannabinoids, and synthetic cannabimimetics: focus on G-protein-coupled receptors and transient receptor potential channels. J Neuroimmune Pharmacol. 2010;5:103–121.
  • Di Marzo V, De Petrocellis L. Fifty years of ‘cannabinoid research’ and the need for a new nomenclature. In: Di Marzo V, editor. Cannabinoids. Chichester (UK): John Wiley & Sons, Ltd; 2014.
  • Di Marzo V, Piscitelli F. The endocannabinoid system and its modulation by phytocannabinoids. Neurotherapeutics. 2015;12:692–698.
  • Wang Q, Liu Y, Zhou J. Neuroinflammation in Parkinson’s disease and its potential as therapeutic target. Transl Neurodegener. 2015;4:19.
  • Lotia M, Jankovic J. New and emerging medical therapies in Parkinson’s disease. Expert Opin Pharmacother. 2016;17:895–909.
  • Cazorla M, Kang UJ, Kellendonk C. Balancing the basal ganglia circuitry: a possible new role for dopamine D2 receptors in health and disease. Mov Disord. 2015;30:895–903.
  • DeLong MR, Wichmann T. Circuits and circuit disorders of the basal ganglia. Arch Neurol. 2007;64:20–24.
  • Martin AB, Fernandez-Espejo E, Ferrer B, et al. Expression and function of CB1 receptor in the rat striatum: localization and effects on D1 and D2 dopamine receptor-mediated motor behaviors. Neuropsychopharmacology. 2008;33:1667–1679.
  • Hu SS-J, Mackie K. Distribution of the endocannabinoid system in the central nervous system. Handb Exp Pharmacol. 2015;231:59–93.
  • Kreitzer AC, Malenka RC. Endocannabinoid-mediated rescue of striatal LTD and motor deficits in Parkinson’s disease models. Nature. 2007;445:643–647.
  • Surmeier DJ, Plotkin J, Shen W. Dopamine and synaptic plasticity in dorsal striatal circuits controlling action selection. Curr Opin Neurobiol. 2009;19:621–628.
  • Picconi B, Bagetta V, Ghiglieri V, et al. Inhibition of phosphodiesterases rescues striatal long-term depression and reduces levodopa-induced dyskinesia. Brain. 2011;134:375–387.
  • Lastres-Becker I, Cebeira M, De Ceballos ML, et al. 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;14:1827–1832.
  • Van Laere K, Casteels C, Lunskens S, et al. Regional changes in type 1 cannabinoid receptor availability in Parkinson’s disease in vivo. Neurobiol Aging. 2012;33:620.e1–620.e8.
  • Pisani A, Fezza F, Galati S, et al. High endogenous cannabinoid levels in the cerebrospinal fluid of untreated Parkinson’s disease patients. Ann Neurol. 2005;57:777–779.
  • Pisani V, Moschella V, Bari M, et al. Dynamic changes of anandamide in the cerebrospinal fluid of Parkinson’s disease patients. Mov Disord. 2010;25:920–924.
  • Pisani V, Madeo G, Tassone A, et al. Homeostatic changes of the endocannabinoid system in Parkinson’s disease. Mov Disord. 2011;26:216–222.
  • Fernández-Ruiz J, Gonzáles S. Cannabinoid control of motor function at the basal ganglia. Handb Exp Pharmacol. 2005;168:479–507.
  • Di Marzo V, Bifulco M, De Petrocellis L. The endocannabinoid system and its therapeutic exploitation. Nat Rev Drug Discov. 2004;3:771–784.
  • Atwood BK, Straiker A, Mackie K. CB₂: therapeutic target-in-waiting. Prog Neuropsychopharmacol Biol Psychiatry. 2012;38:16–20.
  • Price DA, Martinez AA, Seillier A, et al. 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;29:2177–2186.
  • Meschler JP, Howlett AC, Madras BK. Cannabinoid receptor agonist and antagonist effects on motor function in normal and 1-methyl-4-phenyl-1,2,5,6-tetrahydropyridine (MPTP)-treated non-human primates. Psychopharmacology (Berl). 2001;156:79–85.
  • Chung YC, Bok E, Huh SH, et al. Cannabinoid receptor type 1 protects nigrostriatal dopaminergic neurons against MPTP neurotoxicity by inhibiting microglial activation. J Immunol. 2011;187:6508–6517.
  • Martinez A, Macheda T, Morgese MG, et al. The cannabinoid agonist WIN55212-2 decreases L-DOPA-induced PKA activation and dyskinetic behavior in 6-OHDA-treated rats. Neurosci Res. 2012;72:236–242.
  • González S, Scorticati C, García-Arencibia M, et al. Effects of rimonabant, a selective cannabinoid CB1 receptor antagonist, in a rat model of Parkinson’s disease. Brain Res. 2006;1073-1074:209–219.
  • van der Stelt M, Fox SH, Hill M, et al. 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;19:1140–1142.
  • García C, Palomo-Garo C, García-Arencibia M, et al. Symptom-relieving and neuroprotective effects of the phytocannabinoid Δ⁹-THCV in animal models of Parkinson’s disease. Br J Pharmacol. 2011;163:1495–1506.
  • Garcia-Arencibia M, Gonzalez S, De Lago E, et al. Evaluation of the neuroprotective effect of cannabinoids in a rat model of Parkinson’s disease: importance of antioxidant and cannabinoid receptor-independent properties. Brain Res. 2007;1134:162–170.
  • Blázquez C, Chiarlone A, Sagredo O, et al. Loss of striatal type 1 cannabinoid receptors is a key pathogenic factor in Huntington’s disease. Brain. 2011;134:119–136.
  • Lastres-Becker I, Bizat N, Boyer F, et al. Potential involvement of cannabinoid receptors in 3-nitropropionic acid toxicity in vivo. Neuroreport. 2004;15:2375–2379.
  • Lastres-Becker I, Bizat N, Boyer F, et al. Effects of cannabinoids in the rat model of Huntington’s disease generated by an intrastriatal injection of malonate. Neuroreport. 2003;14:813–816.
  • Pintor A, Tebano MT, Martire A, et al. The cannabinoid receptor agonist WIN 55,212-2 attenuates the effects induced by quinolinic acid in the rat striatum. Neuropharmacology. 2006;51:1004–1012.
  • Palazuelos J, Aguado T, Pazos MR, et al. Microglial CB2 cannabinoid receptors are neuroprotective in Huntington’s disease excitotoxicity. Brain. 2009;132:3152–3164.
  • Sagredo O, González S, Aroyo I, et al. Cannabinoid CB2 receptor agonists protect the striatum against malonate toxicity: relevance for Huntington’s disease. Glia. 2009;57:1154–1167.
  • Concannon RM, Okine BN, Finn DP, et al. Differential upregulation of the cannabinoid CB₂ receptor in neurotoxic and inflammation-driven rat models of Parkinson’s disease. Exp Neurol. 2015;269:133–141.
  • García MC, Cinquina V, Palomo-Garo C, et al. Identification of CB₂ receptors in human nigral neurons that degenerate in Parkinson’s disease. Neurosci Lett. 2015;587:1–4.
  • Gómez-Gálvez Y, Palomo-Garo C, Fernández-Ruiz J, et al. 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.
  • Di Marzo V, Hill MP, Bisogno T, et al. Enhanced levels of endogenous cannabinoids in the globus pallidus are associated with a reduction in movement in an animal model of Parkinson’s disease. Faseb J. 2000;14:1432–1438.
  • Romero J, Berrendero F, Pérez-Rosado A, et al. Unilateral 6-hydroxydopamine lesions of nigrostriatal dopaminergic neurons increased CB1 receptor mRNA levels in the caudate-putamen. Life Sci. 2000;66:485–494.
  • Gubellini P, Picconi B, Bari M, et al. Experimental parkinsonism alters endocannabinoid degradation: implications for striatal glutamatergic transmission. J Neurosci. 2002;22:6900–6907.
  • Walsh S, Gorman AM, Finn DP, et al. The effects of cannabinoid drugs on abnormal involuntary movements in dyskinetic and non-dyskinetic 6-hydroxydopamine lesioned rats. Brain Res. 2010;1363:40–48.
  • Obeso JA, Rodríguez-Oroz MC, Benitez-Temino B, et al. Functional organization of the basal ganglia: therapeutic implications for Parkinson’s disease. Mov Disord. 2008;23:S548–S559.
  • Morgese MG, Cassano T, Cuomo V, et al. Anti-dyskinetic effects of cannabinoids in a rat model of Parkinson’s disease: role of CB(1) and TRPV1 receptors. Exp Neurol. 2007;208:110–119.
  • De Lago E, De Miguel R, Lastres-Becker I, et al. 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;1007:152–159.
  • Fernandez-Espejo E, Caraballo I, De Fonseca FR, et al. Cannabinoid CB1 antagonists possess antiparkinsonian efficacy only in rats with very severe nigral lesion in experimental parkinsonism. Neurobiol Dis. 2005;18:591–601.
  • García-Arencibia M, Ferraro L, Tanganelli S, et al. Enhanced striatal glutamate release after the administration of rimonabant to 6-hydroxydopamine-lesioned rats. Neurosci Lett. 2008;438:10–13.
  • Kelsey JE, Harris O, Cassin J. The CB(1) antagonist rimonabant is adjunctively therapeutic as well as monotherapeutic in an animal model of Parkinson’s disease. Behav Brain Res. 2009;203:304–307.
  • Cao X, Liang L, Hadcock JR, et al. Blockade of cannabinoid type 1 receptors augments the antiparkinsonian action of levodopa without affecting dyskinesias in 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-treated rhesus monkeys. J Pharmacol Exp Ther. 2007;323:318–326.
  • Gutiérrez-Valdez AL, García-Ruiz R, Anaya-Martínez V, et al. The combination of L-DOPA/rimonabant for effective dyskinesia treatment and cytological preservation in a rat model of Parkinson’s disease and L-DOPA-induced dyskinesia. Behav Pharmacol. 2013;24:640–652.
  • Kluger B, Triolo P, Jones W, et al. The therapeutic potential of cannabinoids for movement disorders. Mov Disord. 2015;30:313–327.
  • Roze E, Cahill E, Martin E, et al. Huntington’s disease and striatal signaling. Front Neuroanat. 2011;5:55–86.
  • Denovan-Wright EM, Robertson HA. Cannabinoid receptor messenger RNA levels decrease in a subset of neurons of the lateral striatum, cortex and hippocampus of transgenic Huntington’s disease mice. Neuroscience. 2000;98:705–713.
  • Glass M, Dragunow M, Faull RL. The pattern of neurodegeneration in Huntington’s disease: a comparative study of cannabinoid, dopamine, adenosine and GABA(A) receptor alterations in the human basal ganglia in Huntington’s disease. Neuroscience. 2000;97:505–519.
  • Van Laere K, Casteels C, Dhollander I, et al. Widespread decrease of type 1 cannabinoid receptor availability in Huntington disease in vivo. J Nucl Med. 2010;51:1413–1417.
  • Dowie MJ, Bradshaw HB, Howard ML, et al. Altered CB1 receptor and endocannabinoid levels precede motor symptom onset in a transgenic mouse model of Huntington’s disease. Neuroscience. 2009;163:456–465.
  • Pouladi MA, Stanek LM, Xie Y, et al. Marked differences in neurochemistry and aggregates despite similar behavioural and neuropathological features of Huntington disease in the full-length BACHD and YAC128 mice. Hum Mol Genet. 2012;21:2219–2232.
  • Woodman B, Butler R, Landles C, et al. The Hdh(Q150/Q150) knock-in mouse model of HD and the R6/2 exon 1 model develop comparable and widespread molecular phenotypes. Brain Res Bull. 2007;72:83–97.
  • Kloster E, Saft C, Epplen JT, et al. CNR1 variation is associated with the age at onset in Huntington disease. Eur J Med Genet. 2013;56:416–419.
  • Zuccato C, Tartari M, Crotti A, et al. Huntingtin interacts with REST/NRSF to modulate the transcription of NRSE-controlled neuronal genes. Nat Genet. 2003;35:76–83.
  • Cattaneo E, Zuccato C, Tartari M. Normal huntingtin function: an alternative approach to Huntington’s disease. Nat Rev Neurosci. 2005;6:919–930.
  • Chiarlone A, Bellocchio L, Blázquez C, et al. A restricted population of CB1 cannabinoid receptors with neuroprotective activity. Proc Natl Acad Sci U S A. 2014;111:8257–8262.
  • Laprairie RB, Kelly MEM, Denovan-Wright EM. Cannabinoids increase type 1 cannabinoid receptor expression in a cell culture model of striatal neurons: implications for Huntington’s disease. Neuropharmacology. 2013;72:47–57.
  • Laprairie RB, Bagher AM, Kelly MEM, et al. Type 1 cannabinoid receptor ligands display functional selectivity in a cell culture model of striatal medium spiny projection neurons. J Biol Chem. 2014;289:24845–24862.
  • Laprairie RB, Bagher AM, Kelly MEM, et al. Biased type 1 cannabinoid receptor signaling influences neuronal viability in a cell culture model of Huntington disease. Mol Pharmacol. 2016;89:364–375.
  • Battista N, Bari M, Tarditi A, et al. Severe deficiency of the fatty acid amide hydrolase (FAAH) activity segregates with the Huntington’s disease mutation in peripheral lymphocytes. Neurobiol Dis. 2007;27:108–116.
  • Bari M, Battista N, Valenza M. In vitro and in vivo models of Huntington’s disease show alterations in the endocannabinoid system. FEBS J. 2013;280:3376–3388.
  • Lastres-Becker I, Fezza F, Cebeira M, et al. Changes in endocannabinoid transmission in the basal ganglia in a rat model of Huntington’s disease. Neuroreport. 2001;12:2125–2129.
  • Bisogno T, Martire A, Petrosino S, et al. Symptom-related changes of endocannabinoid and palmitoylethanolamide levels in brain areas of R6/2 mice, a transgenic model of Huntington’s disease. Neurochem Int. 2008;52:307–313.
  • Dowie MJ, Howard ML, Nicholson LF, et al. Behavioural and molecular consequences of chronic cannabinoid treatment in Huntington’s disease transgenic mice. Neuroscience. 2010;170:324–336.
  • De Lago E, Fernández-Ruiz J, Ortega-Gutiérrez S, et al. UCM707, an inhibitor of the anandamide uptake, behaves as a symptom control agent in models of Huntington’s disease and multiple sclerosis, but fails to delay/arrest the progression of different motor-related disorders. Eur Neuropsychopharmacol. 2006;16:7–18.
  • Lastres-Becker I, Gómez M, De Miguel R, et al. Loss of cannabinoid CB(1) receptors in the basal ganglia in the late akinetic phase of rats with experimental Huntington’s disease. Neurotox Res. 2002;4:601–608.
  • Valdeolivas S, Pazos MR, Bisogno T, et al. The inhibition of 2-arachidonoyl-glycerol (2-AG) biosynthesis, rather than enhancing striatal damage, protects striatal neurons from malonate-induced death: a potential role of cyclooxygenase-2-dependent metabolism of 2-AG. Cell Death Dis. 2013;4:e862.
  • Horswill JG, Bali U, Shaaban S, et al. PSNCBAM-1, a novel allosteric antagonist at cannabinoid CB1 receptors with hypophagic effects in rats. Br J Pharmacol. 2007;152:805–814.
  • Khajehali E, Malone DT, Glass M, et al. Biased agonism and biased allosteric modulation at the CB1 cannabinoid receptor. Mol Pharmacol. 2015;88:368–379.
  • Fernández-Ruiz J, Sagredo O, Pazos MR, et al. Cannabidiol for neurodegenerative disorders: important new clinical applications for this phytocannabinoid? Br J Clin Pharmacol. 2013;75:323–333.
  • Fernández-Ruiz J, Romer J, Ramos JA. Endocannabinoids and neurodegenerative disorders: Parkinson’s disease, Huntington’s chorea, Alzheimer’s disease and others. In: Pertwee RG, editor. Handbook of experimental pharmacology: endocannabinoids. Vol. 231. Dortmund (Germany): Springer; 2015. p. 233–259.
  • Valdeolivas S, Navarrete C, Cantarero I, et al. Neuroprotective properties of cannabigerol in Huntington’s disease: studies in R6/2 mice and 3-nitropropionate-lesioned mice. Neurotherapeutics. 2015;12:185–199.
  • Curtis A, Mitchell I, Patel S, et al. A pilot study using nabilone for symptomatic treatment in Huntington’s disease. Mov Disord. 2009;24:2254–2259.
  • López-Sendón Moreno JL, García Caldentey J, Trigo Cubillo P, et al. A double-blind, randomized, cross-over, placebo-controlled, pilot trial with Sativex in Huntington’s disease. J Neurol. 2016;263:1390–1400.
  • Whyte DA, Al-Hammadi S, Balhaj G, et al. Cannabinoids inhibit cellular respiration of human oral cancer cells. Pharmacology. 2010;85:328–335.
  • Bénard G, Massa F, Puente N, et al. Mitochondrial CB₁ receptors regulate neuronal energy metabolism. Nat Neurosci. 2012;15:558–564.
  • Velez-Pardo C, Jimenez-Del-Rio M, Lores-Arnaiz S, et al. Protective effects of the synthetic cannabinoids CP55,940 and JWH-015 on rat brain mitochondria upon paraquat exposure. Neurochem Res. 2010;35:1323–1332.
  • Nambu A, Tokuno H, Takada M. Functional significance of the cortico-subthalamo-pallidal ‘hyperdirect’ pathway. Neurosci Res. 2002;43:111–117.
  • Mink JW. The Basal Ganglia and involuntary movements: impaired inhibition of competing motor patterns. Arch Neurol. 2003;60:1365–1368.
  • Carriba P, Ortiz O, Patkar K, et al. Striatal adenosine A2A and cannabinoid CB1 receptors form functional heteromeric complexes that mediate the motor effects of cannabinoids. Neuropsychopharmacology. 2007;32:2249–2259.
  • Ferré S, Lluís C, Justinova Z, et al. Adenosine-cannabinoid receptor interactions. Implications for striatal function. Br J Pharmacol. 2010;160:443–453.
  • Ferreira SG, Gonçalves FQ, Marques JM, et al. Presynaptic adenosine A2A receptors dampen cannabinoid CB1 receptor-mediated inhibition of corticostriatal glutamatergic transmission. Br J Pharmacol. 2015;172:1074–1086.
  • Bonaventura J, Rico AJ, Moreno E, et al. L-DOPA-treatment in primates disrupts the expression of A(2A) adenosine-CB(1) cannabinoid-D(2) dopamine receptor heteromers in the caudate nucleus. Neuropharmacology. 2014;79:90–100.
  • Pinna A, Bonaventura J, Farré D, et al. L-DOPA disrupts adenosine A(2A)-cannabinoid CB(1)-dopamine D(2) receptor heteromer cross-talk in the striatum of hemiparkinsonian rats: biochemical and behavioral studies. Exp Neurol. 2014;253:180–191.
  • Fišar Z, Singh N, Hroudová J. Cannabinoid-induced changes in respiration of brain mitochondria. Toxicol Lett. 2014;231:62–71.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.