Endocannabinoid modulation of dopaminergic motor circuits

Frontiers in Pharmacology

Volumn 3 JUN, Issue , 2012, Pages

  Morera Herreras, Teresa ^a   Miguelez, Cristina ^a   Aristieta, Asier ^a   Ruiz Ortega, Jose Angel ^a   Ugedo, Luisa ^a  

^a UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

Author keywords

Basal ganglia; Dopamine; Electrophysiology; Endocannabinoids; Motor circuits

Indexed keywords

ANTIPARKINSON AGENT; CANNABINOID 1 RECEPTOR; CANNABINOID 1 RECEPTOR ANTAGONIST; CANNABINOID RECEPTOR; CANNABINOID RECEPTOR AGONIST; DOPAMINE; DOPAMINE RECEPTOR; ENDOCANNABINOID; G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR 55; LEVODOPA; N (4 HYDROXYPHENYL)ARACHIDONAMIDE; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 1;

ACTION POTENTIAL; ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; ARTICLE; BASAL GANGLION; BEHAVIOR CHANGE; BRAIN ELECTROPHYSIOLOGY; BRAIN FUNCTION; BRAIN NERVE CELL; CELL ACTIVATION; DENERVATION; DOPAMINE RELEASE; DOPAMINERGIC ACTIVITY; DOPAMINERGIC NERVE CELL; DOPAMINERGIC SYSTEM; DRUG MECHANISM; DYSKINESIA; FOREBRAIN; GABAERGIC TRANSMISSION; HUMAN; HYPOKINESIA; IN VIVO STUDY; INTRACELLULAR SIGNALING; LOCOMOTION; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MOTOR ACTIVITY; MOTOR DYSFUNCTION; MOTOR PERFORMANCE; NERVE CELL MEMBRANE POTENTIAL; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NEUROANATOMY; NEUROCHEMISTRY; NEUROMODULATION; NEUROPROTECTION; NONHUMAN; PARKINSON DISEASE; PARKINSONISM; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; RECEPTOR BINDING; REGULATORY MECHANISM; SUBSTITUTION THERAPY;

EID: 84866178388     PISSN: None     EISSN: 16639812     Source Type: Journal    
DOI: 10.3389/fphar.2012.00110     Document Type: Article

References (109)

1. Ahlskog, J. E., and Muenter, M. D. (2001). Frequency of levodopa-related dyskinesias and motor fluctuations as estimated from the cumulative literature. Mov. Disord. 16,448-458.
2. Anderson, L. A., Anderson, J. J., Chase, T. N., and Walters, J. R. (1995). The cannabinoid agonists WIN 55,212-2 and CP 55,940 attenuate rotational behavior induced by a dopamine D1 but not a D2 agonist in rats with unilateral lesions of the nigrostriatal pathway. Brain Res. 691,106-114.
3. Atwood, B. K., and Mackie, K. (2010). CB2: a cannabinoid receptor with an identity crisis. Br. J. Pharmacol. 160, 467-479.
4. Benarroch, E. (2007). Endocannabinoids in basal ganglia circuits implications for Parkinson disease. Neurology 69, 306-309.
5. Brotchie, J. M. (2003). CB1 cannabinoid receptor signalling in Parkinson's disease. Curr. Opin. Pharmacol. 3, 54-61.
6. Brown, T. M., Brotchie, J. M., and Fitzjohn, S. M. (2003). Cannabinoids decrease corticostriatal synaptic transmission via an effect on glutamate uptake. J. Neurosci. 23, 11073-11077.
7. Calabresi, P., Picconi, B., Tozzi, A., and Di Filippo, M. (2007). Dopamine-mediated regulation of corticostriatal synaptic plasticity. Trends Neurosci. 30,211-219.
8. Carroll, C. B., Bain, P. G., Teare, L., Liu, X., Joint, C., Wroath, C., Parkin, S. G., Fox, P., Wright, D., Hobart, J., and Zajicek, J. P. (2004). Cannabis for dyskinesia in Parkinson disease: a randomized double-blind crossover study. Neurology 63, 1245-1250.
9. Carroll, C. B., Zeissler, M. L., Hanemann, C.O., and Zajicek, J.P. (2012). Delta(9) -THC exerts a direct neuroprotective effect in a human cell culture model of Parkinson's disease. Neuropathol. Appl. Neurobiol. doi: 10.111/J.1365-2990.2011.01248.X
10. Cavanaugh, D. J., Chesler, A. T., Jackson, A. C., Sigal, Y. M., Yamanaka, H., Grant, R., O'Donnell, D., Nicoll, R. A., Shah, N. M., Julius, D., and Basbaum, A. I. (2011). Trpv1 reporter mice reveal highly restricted brain distribution and functional expression in arteriolar smooth muscle cells. J. Neurosci. 31, 5067-5077.
11. Centonze, D., Gubellini, P., Picconi, B., Calabresi, P., Giacomini, P., and Bernardi, G. (1999). Unilateral dopamine denervation blocks corticostriatal LTP. J. Neurophysiol. 82, 3575-3579.
12. Chung, Y. C., Bok, E., Huh, S. H., Park, J. Y., Yoon, S. H., Kim, S. R., Kim, Y S., Maeng, S., Park, S. H., and Jin, B. K. (2011). Cannabinoid receptor type 1 protects nigrostriatal dopaminergic neurons against MPTP neurotoxic-ity by inhibiting microglial activation. J. Immunol. 187, 6508-6517.
13. Compton, D. R., Aceto, M. D., Lowe, J., and Martin, B. R. (1996). In vivo characterization of a specific cannabinoid receptor antagonist (SR141716A): inhibition of delta 9-tetrahydrocannabinol-induced responses and apparent agonist activity. J. Pharmacol. Exp. Ther. 277, 586-594.
14. Compton, D. R., and Martin, B. R. (1997). The effect of the enzyme inhibitor phenylmethylsulfonyl fluoride on the pharmacological effect of anandamide in the mouse model of cannabimimetic activity. J. Pharmacol Exp. Ther. 283, 1138-1143.
15. Crawley, J. N., Corwin, R. L., Robinson, J. K., Felder, C. C., Devane, W. A., and Axelrod, J. (1993). Anandamide, an endogenous ligand of the cannabinoid receptor, induces hypomotility and hypothermia in vivo in rodents. Pharmacol. Biochem. Behav. 46,967-972.
16. Cristino, L., De Petrocellis, L., Pryce, G., Baker, D., Guglielmotti, V., and Di Marzo, V. (2006). Immunohistochemical localization of cannabinoid type 1 and vanilloid transient receptor potential vanilloid type 1 receptors in the mouse brain. Neuroscience 139, 1405-1415.
17. de Lago, E., De Miguel, R., Lastres-Becker, I., Ramos, J. A., and Fernandez-Ruiz, J. (2004). 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. 1007, 152-159.
18. Devane, W. A., Hanus, L., Breuer, A., Pertwee, R. G., Stevenson, L. A., Griffin, G., Gibson, D., Mandelbaum, A., Etinger, A., and Mechoulam, R. (1992). Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science 258, 1946-1949.
19. Di Marzo, V., Fontana, A., Cadas, H., Schinelli, S., Cimino, G., Schwartz, J. C., and Piomelli, D. (1994). Formation and inactivation of endogenous cannabinoid anandamide in central neurons. Nature 372, 686-691.
20. Di Marzo, V., Melck, D., Bisogno, T., and De Petrocellis, L. (1998). Endocannabinoids: endogenous cannabinoid receptor ligands with neuromodulatory action. Trends Neurosci. 21,521-528.
21. Fernandez-Espejo, E., Caraballo, I., De Fonseca, F. R., El Banoua, F., Ferrer, B., Flores, J. A., and Galan-Rodriguez, B. (2005). Cannabinoid CB1 antagonists possess antiparkinsonian efficacy only in rats with very severe nigral lesion in experimental parkinsonism. Neurobiol. Dis. 18, 591-601.
22. Fernandez-Ruiz, J. (2009). The endocannabinoid system as a target for the treatment of motor dysfunction. Br. I Pharmacol. 156, 1029-1040.
23. Fernandez-Ruiz, J., Moreno-Martet, M., Rodriguez-Cueto, C., Palomo-Garo, C., Gomez-Canas, M., Valdeolivas, S., Guaza, C., Romero, J., Guzman, M., Mechoulam, R., and Ramos, J. A. (2011). Prospects for cannabinoid therapies in basal ganglia disorders. Br. I Pharmacol. 163,1365-1378.
24. Fernandez-Ruiz, J., Romero, J., Velasco, G., Tolon, R. M., Ramos, J. A., and Guzman, M. (2007). Cannabinoid CB2 receptor: a new target for controlling neural cell survival? Trends Pharmacol. Sci. 28, 39-45.
25. Ferrer, B., Asbrock, N., Kathuria, S., Piomelli, D., and Giuffrida, A. (2003). Effects of levodopa onendo-cannabinoid levels in rat basal ganglia: implications for the treatment of levodopa-induced dyskine-sias. Eur. J. Neurosci. 18,1607-1614.
26. Fox, S. H., Henry, B., Hill, M., Crossman, A., and Brotchie, J. (2002). Stimulation of cannabinoid receptors reduces levodopa-induced dyskinesia in the MPTP-lesioned nonhuman primate model of Parkinson's disease. Mov. Disord. 17,1180-1187.
27. French, E. D., Dillon, K., and Wu, X. (1997). Cannabinoids excite dopamine neurons in the ventral tegmentum and substantia nigra. Neuroreport 8, 649-652.
28. Garcia-Arencibia, M., Gonzalez, S., De Lago, E., Ramos, J. A., Mechoulam, R., and Fernandez-Ruiz, J. (2007). 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. 1134, 162-170.
29. Gerdeman, G., and Lovinger, D. M. (2001). CB1 cannabinoid receptor inhibits synaptic release of glutamate in rat dorsolateral striatum. J. Neurophysiol. 85, 468-471.
30. Giuffrida, A., Parsons, L. H., Kerr, T. M., Rodriguez de Fonseca, F., Navarro,M., and Piomelli, D. (1999). Dopamine activation of endogenous cannabinoid signaling in dorsal striatum. Nat. Neurosci. 2, 358-363.
31. Glass, M., and Felder, C. C. (1997). Concurrent stimulation of cannabinoid CB1 and dopamine D2 receptors augments cAMP accumulation in striatal neurons: evidence for a Gs linkage to the CB1 receptor. J. Neurosci. 17,5327-5333.
32. Gong, J. P., Onaivi, E. S., Ishiguro, H., Liu, Q. R., Tagliaferro, P. A., Brusco, A., and Uhl, G. R. (2006). Cannabinoid CB2 receptors: immunohistochemical localization in rat brain. Brain Res. 1071, 10-23.
33. Gonzalez, S., Mena, M. A., Lastres-Becker, I., Serrano, A., De Yebenes, J. G., Ramos, J. A., and Fernandez-Ruiz, J. (2005). Cannabinoid CB(1) receptors in the basal ganglia and motor response to activation or blockade of these receptors in parkin-null mice. Brain Res. 1046, 195-206.
34. Gonzalez, S., Romero, J., De Miguel, R., Lastres-Becker, I., Villanua, M. A., Makriyannis, A., Ramos, J. A., and Fernandez-Ruiz, J. J. (1999). Extrapyramidal and neuroendocrine effects of AM404, an inhibitor of the carriermediated transport of anandamide. Life Sci. 65, 327-336.
35. Gonzalez, S., Scorticati, C., Garcia-Arencibia, M., De Miguel, R., Ramos, J. A., and Fernandez-Ruiz, J. (2006). Effects of rimonabant, a selective cannabinoid CB1 receptor antagonist, in a rat model of Parkinson's disease. Brain Res. 1073-1074, 209-219.
36. Gubellini, P., Picconi, B., Bari, M., Battista, N., Calabresi, P., Centonze, D., Bernardi, G., Finazzi-Agro, A., and Maccarrone, M. (2002). Experimental parkinsonism alters endocannabinoid degradation: implications for striatal glutamatergic transmission. J. Neurosci. 22, 6900-6907.
37. Herkenham, M., Lynn, A. B., de Costa, B. R., and Richfield, E. K. (1991). Neuronal localization of cannabinoid receptors in the basal ganglia of the rat. Brain Res. 547, 267-274.
38. Herkenham, M., Lynn, A. B., Little, M. D., Johnson, M. R., Melvin, L. S., de Costa, B. R., and Rice, K. C. (1990). Cannabinoid receptor localization in brain. Proc. Natl. Acad. Sci. U.S.A. 87, 1932-1936.
39. Jeon, P., Yang, S., Jeong, H., and Kim, H. (2011). Cannabinoid receptor agonist protects cultured dopaminergic neurons from the death by the proteasomal dysfunction. Anat. Cell Biol. 44, 135-142.
40. Julian, M. D., Martin, A. B., Cuellar, B., Rodriguez de Fonseca, F., Navarro, M., Moratalla, R., and Garcia-Segura, L. M. (2003). Neuroanatomical relationship between type 1 cannabinoid receptors and dopaminergic systems in the rat basal ganglia. Neuroscience 119, 309-318.
41. Kearn, C. S., Blake-Palmer, K., Daniel, E., Mackie, K., and Glass, M. (2005). Concurrent stimulation of cannabinoid CB1 and dopamine D2 receptors enhances heterodimer formation: a mechanism for receptor crosstalk. Mol Pharmacol. 67, 1697-1704.
42. Kelsey, J. E., Harris, O., and Cassin, J. (2009). The CB(1) antagonist rimonabant is adjunctively therapeutic as well as monotherapeutic in an animal model of Parkinson's disease. Behav. Brain Res. 203, 304-307.
43. Kofalvi, A., Rodrigues, R. J., Ledent, C., Mackie, K., Vizi, E. S., Cunha, R. A., and Sperlagh, B. (2005). Involvement of cannabinoid receptors in the regulation of neurotransmitter release in the rodent striatum: a combined immunochemical and pharmacological analysis. J. Neurosci. 25, 2874-2884.
44. Kreitzer, A. C., and Malenka, R. C. (2007). Endocannabinoid-mediated rescue of striatal LTD and motor deficits in Parkinson's disease models. Nature 445, 643-647.
45. Lastres-Becker, I., Cebeira, M., de Ceballos, M. L., Zeng, B. Y., Jenner, P., Ramos, J. A., and Fernandez-Ruiz, J. J. (2001). 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. 14,1827-1832.
46. Lastres-Becker, I., Molina-Holgado, F., Ramos, J. A., Mechoulam, R., and Fernandez-Ruiz, J. (2005). Cannabinoids provide neuroprotection against 6-hydroxydopamine toxicity in vivo and in vitro: relevance to Parkinson's disease. Neurobiol. Dis. 19, 96-107
47. Lauckner, J.E., Jensen, J.B., Chen, H.Y., Lu, H.C., Hille, B., and Mackie, K. (2008).GPR55 is a cannabinoid receptor that increases intracellular calcium and inhibits Mcurrent. Proc. Natl. Acad. Sci. U.S.A. 105, 2699-2704.
48. Ledent, C., Valverde, O., Cossu, G., Petitet, F., Aubert, J. F., Beslot, E, Bohme, G. A., Imperato, A., Pedrazzini, T., Roques, B. P., Vassart, G., Fratta, W., and Parmentier, M. (1999). Unresponsiveness to cannabinoids and reduced addictive effects of opiates in CB1 receptor knockout mice. Science 283, 401-404.
49. Lovinger, D. M. (2010). Neurotransmitter roles in synaptic modulation, plasticity and learning in the dorsal striatum. Neuropharmacology 58, 951-961.
50. Maccarrone, M., Gubellini, P., Bari, M., Picconi, B., Battista, N., Centonze, D., Bernardi, G., Finazzi-Agro, A., and Calabresi, P. (2003). Levodopa treatment reverses endocannabinoid system abnormalities in experimental parkinsonism. J. Neurochem. 85, 1018-1025.
51. Mackie, K. (2005). Distribution of cannabinoid receptors in the central and peripheral nervous system. Handb. Exp. Pharmacol. 168, 299-325.
52. Mackie, K. (2008). Cannabinoid receptors: where they are and what they do. J. Neuroendocrinol. 20(Suppl. 1), 10-14.
53. Mailleux, P., and Vanderhaeghen, J. J. (1992). Localization of cannabinoid receptor in the human developing and adult basal ganglia. Higher levels in the striatonigral neurons. Neurosci. Lett. 148, 173-176.
54. Mallet, N., Ballion, B., Le Moine, C., and Gonon, E. (2006). Cortical inputs and GABA interneurons imbalance projection neurons in the striatum of parkinsonian rats. J. Neurosci. 26, 3875-3884.
55. Marcellino, D., Carriba, P., Filip, M., Borgkvist, A., Frankowska, M., Bel-lido, I., Tanganelli, S., Muller, C. E., Fisone, G., Lluis, C., Agnati, L. F., Franco, R., and Fuxe, K. (2008). Antagonistic cannabinoid CB1/dopamine D2 receptor interactions in striatal CB1/D2 heteromers. A combined neurochemical and behavioral analysis. Neuropharmacology 54, 815-823.
56. Marinelli, S., di Marzo, V., Berretta, N., Matias, I., Maccarrone, M., Bernardi, G., and Mercuri, N. B. (2003). Presynaptic facilitation of glutamatergic synapses to dopaminergic neurons of the rat substantia nigra by endogenous stimulation of vanilloid receptors. J. Neurosci. 23, 3136-3144.
57. Marinelli, S., Di Marzo, V., Florenzano, F., Fezza, F., Viscomi, M. T., Van Der Stelt, M., Bernardi, G., Molinari, M., MacCarrone, M., and Mercuri, N. B. (2007). N-arachidonoyldopamine tunes synaptic transmission onto dopaminergic neurons by activating both cannabinoid and vanilloid receptors. Neuropsychopharmacology 32, 298-308.
58. Martin, A. B.,Fernandez-Espejo,E., Ferrer, B., Gorriti, M. A., Bilbao, A., Navarro, M., Rodriguez de Fonseca, E, and Moratalla, R. (2008). Expression and function of CB1 receptor in the rat striatum: localization and effects on D1 and D2 dopamine receptormediated motor behaviors. Neuropsychopharmacology 33, 1667-1679.
59. Martinez, A., Macheda, T., Morgese, M. G., Trabace, L., and Giuffrida, A. (2012). The cannabinoid agonist WIN55212-2 decreases L-DOPA-induced PKA activation and dyskinetic behavior in 6-OHDA-treated rats. Neurosci. Res. 72, 236-242.
60. Mathur, B. N., Capik, N. A., Alvarez, V. A., and Lovinger, D. M. (2011). Serotonin induces long-term depression at corticostriatal synapses. J. Neurosci. 31, 7402-7411.
61. Matsuda, L. A., Lolait, S. J., Brownstein, M. J., Young, A. C., and Bonner, T. I. (1990). Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature 346, 561-564.
62. Matyas, F., Yanovsky, Y., Mackie, K., Kelsch, W., Misgeld, U., and Freund, T. E (2006). Subcellular localization of type 1 cannabinoid receptors in the rat basal ganglia. Neuroscience 137,337-361.
63. Mechoulam, R., Ben-Shabat, S., Hanus, L., Ligumsky, M., Kaminski, N. E., Schatz, A. R., Gopher, A., Almog, S., Martin, B. R., Compton, D. R., Pertwee, R. G., Griffin, G., Bayewitch, M., Barg, J., and Vogel, Z. (1995). Identification of an endogenous 2-monoglyceride, present in canine gut, that binds to cannabinoid receptors. Biochem. Pharmacol. 50, 83-90.
64. Melis, M., Gessa, G. L., and Diana, M. (2000). Different mechanisms for dopaminergic excitation induced by opiates and cannabinoids in the rat midbrain. Prog. Neuropsychopharmacol Biol. Psychiatry 24, 993-1006.
65. Meschler, J. P., and Howlett, A. C. (2001). Signal transduction interactions between CB1 cannabinoid and dopamine receptors in the rat and monkey striatum. Neuropharmacology 40, 918-926.
66. Mesnage, V., Houeto, J. L., Bonnet, A. M., Clavier, I., Arnulf, I., Cattelin, E, Le Fur, G., Damier, P., Welter, M. L., and Agid, Y. (2004). Neurokinin B, neurotensin, and cannabinoid receptor antagonists and Parkinson disease. Clin. Neuropharmacol. 27, 108-110.
67. Mezey, E., Toth, Z. E., Cortright, D. N., Arzubi, M. K., Krause, J. E., Elde, R., Guo, A., Blumberg, P. M., and Szallasi, A. (2000). Distribution of mRNA for vanilloid receptor subtype 1 (VR1), and VR1-like immunoreactivity, in the central nervous system of the rat and human. Proc. Natl Acad. Sci. U.S.A. 97,3655-3660.
68. Micale, V., Cristino, L., Tamburella, A., Petrosino, S., Leggio, G. M., Drago, E, and di Marzo, V. (2009). Anxiolytic effects in mice of a dual blocker of fatty acid amide hydrolase and transient receptor potential vanilloid type-1 channels. Neuropsychopharmacology 34, 593-606.
69. Miller, A. S., Sanudo-Pena, M. C., and Walker, J.M. (1998). Ipsilateral turning behavior induced by unilateral microinjections of a cannabinoid into the rat subthalamic nucleus. Brain Res. 793,7-11.
70. Morera-Herreras, T., Ruiz-Ortega, J. A., Gomez-Urquijo, S., and Ugedo, L. 2008). Involvement of subthalamic nucleus in the stimulatory effect of Delta(9)-tetrahydrocannabinol on dopaminergic neurons. Neuroscience 151,817-823.
71. Morgese, M. G., Cassano, T., Cuomo, V., and Giuffrida, A. (2007). Antidyskinetic effects of cannabinoids in a rat model of Parkinson's disease: role of CB(1) and TRPV1 receptors. Exp.Neurol. 208,110-119.
72. Munro, S., Thomas, K. L., and Abu-Shaar, M. (1993). Molecular characterization of a peripheral receptor for cannabinoids. Nature 365, 61-65.
73. Navarro, M., Fernandez-Ruiz, J. J., De Miguel, R., Hernandez, M. L., Cebeira, M., and Ramos, J. A. (1993). Motor disturbances induced by an acute dose of delta 9-tetrahydrocannabinol: possible involvement of nigrostriatal dopaminergic alterations. Pharmacol. Biochem. Behav. 45, 291-298.
74. Nicola, S. M., Surmeier, J., and Malenka, R. C. (2000). Dopaminergic modulation of neuronal excitability in the striatum and nucleus accumbens. Annu. Rev. Neurosci. 23, 185-215.
75. O'Connor, W T. (1998). Functional neuroanatomy of the basal ganglia as studied by dualprobe microdialysis. Nucl. Med. Biol. 25, 743-746.
76. Oka, S., Nakajima, K., Yamashita, A., Kishimoto, S., and Sugiura, T. (2007). Identification of GPR55 as a lysophosphatidylinositol receptor. Biochem. Biophys. Res. Commun. 362, 928-934.
77. Onn, S. P., West, A. R., and Grace, A. A. (2000). Dopaminemediated regulation of striatal neuronal and network interactions. Trends Neurosci. 23, S48-S56.
78. Paul, M. L., Graybiel, A. M., David, J. C., and Robertson, H. A. (1992). D1-like and D2-like dopamine receptors synergistically activate rotation and c-fos expression in the dopaminedepleted striatum in a rat model of Parkinson's disease. J. Neurosci. 12, 3729-3742.
79. Perez-Rial, S., Garcia-Gutierrez, M. S., Molina, J. A., Perez-Nievas, B. G., Ledent, C., Leiva, C., Leza, J. C., and Manzanares, J. (2011). Increased vulnerability to 6-hydroxydopamine lesion and reduced development of dyskinesias in mice lacking CB1 cannabinoid receptors. Neurobiol. Aging 32, 631-645.
80. Picconi, B., Pisani, A., Barone, I., Bonsi, P., Centonze, D., Bernardi, G., and Calabresi, P. (2005). Pathological synaptic plasticity in the striatum: implications for Parkinson's disease. Neurotoxicology 26, 779-783.
81. Pisani, A., Fezza, F., Galati, S., Battista, N., Napolitano, S., Finazzi-Agro, A., Bernardi, G., Brusa, L., Pierantozzi, M., Stanzione, P., and Maccarrone, M. (2005). High endogenous cannabinoid levels in the cerebrospinal fluid of untreated Parkinson's disease patients. Ann. Neurol. 57, 777-779.
82. Pisani, V., Moschella, V., Bari, M., Fezza, F., Galati, S., Bernardi, G., Stanzione, P., Pisani, A., and Maccarrone, M. (2010). Dynamic changes of anandamide in the cerebrospinal fluid of Parkinson's disease patients. Mov. Disord. 25, 920-924.
83. Prescott, W R., Gold, L. H., and Martin, B. R. (1992). Evidence for separate neuronal mechanisms for the discriminative stimulus and catalepsy induced by delta 9-THC in the rat. Psychopharmacology (Berl.) 107, 117-124.
84. Price, D. A., Martinez, A. A., Seillier, A., Koek, W., Acosta, Y., Fernandez, E., Strong, R., Lutz, B., Marsicano, G., Roberts, J. L., and Giuffrida, A. (2009). 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. 29,2177-2186.
85. Romero, J., Berrendero, F., Perez-Rosado, A., Manzanares, J., Rojo, A., Fernandez-Ruiz, J. J., de Yebenes, J. G., and Ramos, J. A. (2000). Unilateral 6-hydroxydopamine lesions of nigrostriatal dopaminergic neurons increased CB1 receptor mRNA levels in the caudateputamen. Life Sci. 66, 485-494.
86. Romero, J., Garcia, L., Cebeira, M., Zadrozny, D., Fernandez-Ruiz, J. J., and Ramos, J. A. (1995). The endogenous cannabinoid receptor ligand, anandamide, inhibits the motor behavior: role of nigrostriatal dopaminergic neurons. Life Sci. 56, 2033-2040.
87. Ryberg, E., Larsson, N., Sjogren, S., Hjorth, S., Hermansson, N. O., Leonova, J., Elebring, T., Nilsson, K., Drmota, T., and Greasley, P. J. (2007). The orphan receptor GPR55 is a novel cannabinoid receptor. Br. J. Pharmacol. 152, 1092-1101.
88. Sanudo-Pena, M. C., Force, M., Tsou, K., Miller, A. S., and Walker, J. M. (1998). Effects of intrastriatal cannabinoids on rotational behavior in rats: interactions with the dopaminergic system. Synapse 30, 221-226.
89. Sanudo-Pena, M. C., Patrick, S. L., Patrick, R. L., and Walker, J. M. (1996). Effects of intranigral cannabinoids on rotational behavior in rats: interactions with the dopaminergic system. Neurosci. Lett. 206, 21-24.
90. Sanudo-Pena, M. C., and Walker, J. M. (1997). Role of the subthalamic nucleus in cannabinoid actions in the substantia nigra of the rat. J. Neurophysiol. 77, 1635-1638.
91. Sawzdargo, M., Nguyen, T., Lee, D. K., Lynch, K. R., Cheng, R., Heng, H. H., George, S. R., and O'Dowd, B. E (1999). Identification and cloning of three novel human G protein-coupled receptor genes GPR52, PsiGPR53 and GPR55: GPR55 is extensively expressed in human brain. Brain Res. Mol. Brain Res. 64, 193-198.
92. Sharir, H., and Abood, M. E. (2010). Pharmacological characterization of GPR55, a putative cannabinoid receptor. Pharmacol Ther. 126, 301-313.
93. Shen, W., Flajolet, M., Greengard, P., and Surmeier, D. J. (2008). Dichotomous dopaminergic control of striatal synaptic plasticity. Science 321, 848-851.
94. Silverdale, M. A., Mcguire, S., Mcinnes, A., Crossman, A. R., and Brotchie, J. M. (2001). Striatal cannabinoid CB1 receptor mRNA expression is decreased in the reserpine-treated rat model of Parkinson's disease. Exp. Neurol. 169, 400-406.
95. Solinas, M., Justinova, Z., Goldberg, S. R., and Tanda, G. (2006). Anandamide administration alone and after inhibition of fatty acid amide hydrolase (FAAH) increases dopamine levels in the nucleus accumbens shell in rats. J. Neurochem. 98,408-419.
96. Svenningsson, P., Fredholm, B. B., Bloch, B., and Le Moine, C. (2000). Co-stimulation of D(1)/D(5) and D(2) dopamine receptors leads to an increase in c-fos messenger RNA in cholinergic interneu-rons and a redistribution of c-fos messenger RNA in striatal projection neurons. Neuroscience 98, 749-757.
97. Szabo, B., Wallmichrath, I., Mathonia, P., and Pfreundtner, C. (2000). Cannabinoids inhibit excitatory neurotransmission in the substantia nigra pars reticulata. Neuroscience 97, 89-97.
98. Tanda, G., Pontieri, E E., and Di Chiara, G. (1997). Cannabinoid and heroin activation of mesolimbic dopamine transmission by a common mu1 opioid receptor mechanism. Science 276, 2048-2050.
99. Tang, K., Low, M. J., Grandy, D. K., and Lovinger, D. M. (2001). Dopamine-dependent synaptic plasticity in striatum during in vivo development. Proc. Natl. Acad. Sci. U.S.A. 98, 1255-1260.
100. Tseng, K. Y., Kasanetz, F., Kargieman, L., Riquelme, L. A., and Murer, M. G. (2001). Cortical slow oscillatory activity is reflected in the membrane potential and spike trains of striatal neurons in rats with chronic nigrostriatal lesions. J. Neurosci. 21, 6430-6439.
101. Tsou, K., Brown, S., Sanudo-Pena, M. C., Mackie, K., and Walker, J. M. (1998). Immunohistochemical distribution of cannabinoid CB1 receptors in the rat central nervous system. Neuroscience 83, 393-411.
102. van der Stelt, M., and Di Marzo, V. (2003). The endocannabinoid system in the basal ganglia and in the mesolimbic reward system: implications for neurological and psychiatric disorders. Eur. J. Pharmacol. 480, 133-150.
103. van der Stelt, M., Fox, S. H., Hill, M., Crossman, A. R., Petrosino, S., di Marzo, V., and Brotchie, J. M. (2005). A role for endocannabinoids in the generation of parkinsonism and levodopa-induced dyskinesia in MPTP-lesioned non-human primate models of Parkinson's disease. FASEBJ. 19, 1140-1142.
104. Van Laere, K., Casteels, C., Lunskens, S., Goffin, K., Grachev, I. D., Bormans, G., and Vandenberghe, W. (2012). Regional changes in type 1 cannabinoid receptor availability in Parkinson's disease in vivo. Neurobiol Aging 33, 620.e621-620.e628.
105. Van Sickle, M. D., Duncan, M., Kingsley, P. J., Mouihate, A., Urbani, P., Mackie, K., Stella, N., Makriyannis, A., Piomelli, D., Davison, J. S., Marnett, L. J., di Marzo, V., Pittman, Q. J., Patel, K. D., and Sharkey, K. A. (2005). Identification and functional characterization of brainstem cannabinoid CB2 receptors. Science 310,329-332.
106. Wallmichrath, I., and Szabo, B. (2002). Cannabinoids inhibit striatonigral GABAergic neurotransmission in the mouse. Neuroscience 113, 671-682.
107. Walsh, S., Gorman, A. M., Finn, D. P., and Dowd, E. (2010a). The effects of cannabinoid drugs on abnormal involuntary movements in dyskinetic and non-dyskinetic 6-hydroxydopamine lesioned rats. Brain Res. 1363, 40-48.
108. Walsh, S., Mnich, K., Mackie, K., Gorman, A. M., Finn, D. P., and Dowd, E. (2010b). Loss of cannabinoid CB1 receptor expression in the 6-hydroxydopamine-induced nigrostriatal terminal lesion model of Parkinson's disease in the rat. Brain Res. Bull. 81, 543-548.
109. Zimmer, A., Zimmer, A. M., Hohmann, A. G., Herkenham, M., and Bonner, T. I. (1999). Increased mortality, hypoactivity, and hypoalgesia in cannabinoid CB1 receptor knockout mice. Proc. Natl. Acad. Sci. U.S.A. 96, 5780-5785.