Neurochemical changes in the striatum of dyskinetic rats after administration of the cannabinoid agonist WIN55,212-2

Neurochemistry International

Volumn 54, Issue 1, 2009, Pages 56-64

  Morgese, M G ^a,b   Cassano, T ^a   Gaetani, S ^c   Macheda, T ^a   Laconca, L ^a,c   Dipasquale, P ^c   Ferraro, L ^d   Antonelli, T ^d   Cuomo, V ^c   Giuffrida, A ^b  

^a UNIVERSITY OF FOGGIA   (Italy)

^b Mays Cancer Center at UT Health San Antonio   (United States)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

^d UNIVERSITY OF FERRARA   (Italy)

Author keywords

6 Hydroxydopamine; Dopamine; Glutamate; Microdialysis; Parkinson's disease

Indexed keywords

2,3 DIHYDRO 5 METHYL 3 (MORPHOLINOMETHYL) 6 (1 NAPHTHOYL)PYRROLO[1,2,3 DE][1,4]BENZOXAZINE; CANNABINOID RECEPTOR AGONIST; DOPAMINE; GLUTAMIC ACID; LEVODOPA; OXIDOPAMINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; DYSKINESIA; HEMISPHERE; IN VIVO STUDY; MALE; MICRODIALYSIS; NEUROCHEMISTRY; NONHUMAN; PRIORITY JOURNAL; RAT; SHAM PROCEDURE; TURNOVER TIME;

AMPHETAMINE; ANIMALS; BENZOXAZINES; CALCIUM CHANNEL BLOCKERS; CANNABINOIDS; CORPUS STRIATUM; DOPAMINE; DYSKINESIAS; GLUTAMINE; HOMOVANILLIC ACID; LEVODOPA; MALE; MORPHOLINES; NAPHTHALENES; OXIDOPAMINE; RATS; RATS, WISTAR;

RATTUS;

EID: 59049100493     PISSN: 01970186     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuint.2008.10.007     Document Type: Article

References (81)

1. Adermark L., and Lovinger D.M. Retrograde endocannabinoid signaling at striatal synapses requires a regulated postsynaptic release step. Proc. Natl. Acad. Sci. U.S.A. 104 (2007) 20564-20569
2. Amalric M., Ouagazzal A., Baunez C., and Nieoullon A. Functional interactions between glutamate and dopamine in the rat striatum. Neurochem. Int. 25 (1994) 123-131
3. Arabadzisz D., Antal K., Parpan F., Emri Z., and Fritschy J.M. Epileptogenesis and chronic seizures in a mouse model of temporal lobe epilepsy are associated with distinct EEG patterns and selective neurochemical alterations in the contralateral hippocampus. Exp. Neurol. 194 (2005) 76-90
4. 3H]serotonin release from the rat hippocampus. Neurochem. Int. 52 (2008) 95-102
5. Bambico F.R., Katz N., Debonnel G., and Gobbi G. Cannabinoids elicit antidepressant-like behavior and activate serotonergic neurons through the medial prefrontal cortex. J. Neurosci. 27 (2007) 11700-11711
6. Bamford N.S., Zhang H., Schmitz Y., Wu N.P., Cepeda C., Levine M.S., Schmauss C., Zakharenko S.S., Zablow L., and Sulzer D. Heterosynaptic dopamine neurotransmission selects sets of corticostriatal terminals. Neuron 42 (2004) 653-663
7. Beltramo M., de Fonseca F.R., Navarro M., Calignano A., Gorriti M.A., Grammatikopoulos G., Sadile A.G., Giuffrida A., and Piomelli D. Reversal of dopamine D(2) receptor responses by an anandamide transport inhibitor. J. Neurosci. 20 (2000) 3401-3407
8. Blanchet P.J., Calon F., Morissette M., Hadj Tahar A., Belanger N., Samadi P., Grondin R., Gregoire L., Meltzer L., Di Paolo T., and Bedard P.J. Relevance of the MPTP primate model in the study of dyskinesia priming mechanisms. Parkinsonism Relat. Disord. 10 (2004) 297-304
9. Brotchie J.M. CB1 cannabinoid receptor signalling in Parkinson's disease. Curr. Opin. Pharmacol. 3 (2003) 54-61
10. Buck K., and Ferger B. Intrastriatal inhibition of aromatic amino acid decarboxylase prevents l-DOPA-induced dyskinesia: a bilateral reverse in vivo microdialysis study in 6-hydroxydopamine lesioned rats. Neurobiol. Dis. 29 (2008) 210-220
11. Cadogan A.K., Alexander S.P., Boyd E.A., and Kendall D.A. Influence of cannabinoids on electrically evoked dopamine release and cyclic AMP generation in the rat striatum. J. Neurochem. 69 (1997) 1131-1137
12. Cai G., Zhen X., Uryu K., and Friedman E. Activation of extracellular signal-regulated protein kinases is associated with a sensitized locomotor response to D(2) dopamine receptor stimulation in unilateral 6-hydroxydopamine-lesioned rats. J. Neurosci. 20 (2000) 1849-1857
13. Carey R.J. Chronic l-dopa treatment in the unilateral 6-OHDA rat: evidence for behavioral sensitization and biochemical tolerance. Brain Res. 568 (1991) 205-214
14. Carlsson M., and Carlsson A. Interactions between glutamatergic and monoaminergic systems within the basal ganglia-implications for schizophrenia and Parkinson's disease. Trends Neurosci. 13 (1990) 272-276
15. Carta M., Lindgren H.S., Lundblad M., Stancampiano R., Fadda F., and Cenci M.A. Role of striatal l-DOPA in the production of dyskinesia in 6-hydroxydopamine lesioned rats. J. Neurochem. 96 (2006) 1718-1727
16. Cenci M., and Lindgren H. Advances in understanding l-DOPA-induced dyskinesia. Curr. Opin. Neurobiol. 17 (2007) 665-671
17. Cenci M.A. Dopamine dysregulation of movement control in l-DOPA-induced dyskinesia. Trends Neurosci. 30 (2007) 236-243
18. Cenci M.A., and Lundblad M. Utility of 6-hydroxydopamine lesioned rats in the preclinical screening of novel treatment for Parkinson disease. In: LeDoux M. (Ed). Animal Models of Movements Disorders (2005), Elsevier Academic Press, Burlington pp. 193-208
19. Cenci M.A., and Lundblad M. Ratings of l-DOPA-induced dyskinesia in the unilateral 6-OHDA lesion model of Parkinson's disease in rats and mice. Curr. Protoc. Neurosci. (2007) Chapter 9, Unit 9, p. 25
20. Cenci M.A., Lee C.S., and Bjorklund A. l-DOPA-induced dyskinesia in the rat is associated with striatal overexpression of prodynorphin- and glutamic acid decarboxylase mRNA. Eur. J. Neurosci. 10 (1998) 2694-2706
21. Childers S.R., and Deadwyler S.A. Role of cyclic AMP in the actions of cannabinoid receptors. Biochem. Pharmacol. 52 (1996) 819-827
22. Cinar R., Freund T.F., Katona I., Mackie K., and Szucs M. Reciprocal inhibition of G-protein signaling is induced by CB(1) cannabinoid and GABA(B) receptor interactions in rat hippocampal membranes. Neurochem. Int. 52 (2008) 1402-1409
23. Di Monte D.A., McCormack A., Petzinger G., Janson A.M., Quik M., and Langston W.J. Relationship among nigrostriatal denervation, parkinsonism, and dyskinesias in the MPTP primate model. Mov. Disord. 15 (2000) 459-466
24. Domenici M.R., Azad S.C., Marsicano G., Schierloh A., Wotjak C.T., Dodt H.U., Zieglgansberger W., Lutz B., and Rammes G. Cannabinoid receptor type 1 located on presynaptic terminals of principal neurons in the forebrain controls glutamatergic synaptic transmission. J. Neurosci. 26 (2006) 5794-5799
25. Ferraro L., Tomasini M.C., Gessa G.L., Bebe B.W., Tanganelli S., and Antonelli T. The cannabinoid receptor agonist WIN 55,212-2 regulates glutamate transmission in rat cerebral cortex: an in vivo and in vitro study. Cereb. Cortex 11 (2001) 728-733
26. Ferrer B., Asbrock N., Kathuria S., Piomelli D., and Giuffrida A. Effects of levodopa on endocannabinoid levels in rat basal ganglia: implications for the treatment of levodopa-induced dyskinesias. Eur. J. Neurosci. 18 (2003) 1607-1614
27. Freiman I., and Szabo B. Cannabinoids depress excitatory neurotransmission between the subthalamic nucleus and the globus pallidus. Neuroscience 133 (2005) 305-313
28. French E.D., Dillon K., and Wu X. Cannabinoids excite dopamine neurons in the ventral tegmentum and substantia nigra. Neuroreport 8 (1997) 649-652
29. Gerdeman G., and Lovinger D.M. CB1 cannabinoid receptor inhibits synaptic release of glutamate in rat dorsolateral striatum. J. Neurophysiol. 85 (2001) 468-471
30. Gerdeman G.L., Ronesi J., and Lovinger D.M. Postsynaptic endocannabinoid release is critical to long-term depression in the striatum. Nat. Neurosci. 5 (2002) 446-451
31. Gibaldi M., and Perrier D. Pharmacokinetics. 1st edition vol. 1 (1975), Marcel Dekker, New York pp. 37-40
32. Giuffrida A., Parsons L.H., Kerr T.M., Rodriguez de Fonseca F., Navarro M., and Piomelli D. Dopamine activation of endogenous cannabinoid signaling in dorsal striatum. Nat. Neurosci. 2 (1999) 358-363
33. Glass M., and Felder C.C. 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 (1997) 5327-5333
34. Graybiel A.M., Aosaki T., Flaherty A.W., and Kimura M. The basal ganglia and adaptive motor control. Science 265 (1994) 1826-1831
35. Gubellini P., Picconi B., Bari M., Battista N., Calabresi P., Centonze D., Bernardi G., Finazzi-Agro A., and Maccarrone M. Experimental parkinsonism alters endocannabinoid degradation: implications for striatal glutamatergic transmission. J. Neurosci. 22 (2002) 6900-6907
36. Herkenham M., Lynn A.B., de Costa B.R., and Richfield E.K. Neuronal localization of cannabinoid receptors in the basal ganglia of the rat. Brain Res. 547 (1991) 267-274
37. Hossain M.A., and Weiner N. Dopaminergic functional supersensitivity: effects of chronic l-dopa and carbidopa treatment in an animal model of Parkinson's disease. J. Pharmacol. Exp. Ther. 267 (1993) 1105-1111
38. Howlett A.C., and Fleming R.M. Cannabinoid inhibition of adenylate cyclase. Pharmacology of the response in neuroblastoma cell membranes. Mol. Pharmacol. 26 (1984) 532-538
39. Huang C.C., Lo S.W., and Hsu K.S. Presynaptic mechanisms underlying cannabinoid inhibition of excitatory synaptic transmission in rat striatal neurons. J. Physiol. 532 (2001) 731-748
40. 18F]fluoro-l-3,4-dihydroxyphenylalanine uptake in the brain of 6-hydroxydopamine-lesioned rats. Neurodegener. Dis. 1 (2004) 109-112
41. Kearn C.S., Blake-Palmer K., Daniel E., Mackie K., and Glass M. Concurrent stimulation of cannabinoid CB1 and dopamine D2 receptors enhances heterodimer formation: a mechanism for receptor cross-talk?. Mol. Pharmacol. 67 (2005) 1697-1704
42. Kofalvi A., Rodrigues R.J., Ledent C., Mackie K., Vizi E.S., Cunha R.A., and Sperlagh B. Involvement of cannabinoid receptors in the regulation of neurotransmitter release in the rodent striatum: a combined immunochemical and pharmacological analysis. J. Neurosci. 25 (2005) 2874-2884
43. Kreitzer A.C., and Malenka R.C. Dopamine modulation of state-dependent endocannabinoid release and long-term depression in the striatum. J. Neurosci. 25 (2005) 10537-10545
44. Kreitzer A.C., and Malenka R.C. Endocannabinoid-mediated rescue of striatal LTD and motor deficits in Parkinson's disease models. Nature 445 (2007) 643-647
45. Lindgren H.S., Rylander D., Ohlin K.E., Lundblad M., and Cenci M.A. The "motor complication syndrome" in rats with 6-OHDA lesions treated chronically with l-DOPA: relation to dose and route of administration. Behav. Brain Res. 177 (2007) 150-159
46. Lisovoski F., Haby C., Borrelli E., Schleef C., Revel M.O., Hindelang C., and Zwiller J. Induction of D2 dopamine receptor mRNA synthesis in a 6-hydroxydopamine parkinsonian rat model. Brain Res. Bull. 28 (1992) 697-701
47. Lundblad M. A model of l-DOPA-induced dyskinesia in 6-hydroxydopamine lesioned mice: relation to motor and cellular parameters of nigrostriatal function. Neurobiol. Dis. 16 (2004) 110-123
48. Lundblad M., Picconi B., Lindgren H., and Cenci M.A. A model of l-DOPA-induced dyskinesia in 6-hydroxydopamine lesioned mice: relation to motor and cellular parameters of nigrostriatal function. Neurobiol. Dis. 16 (2004) 110-123
49. Lundblad M., Andersson M., Winkler C., Kirik D., Wierup N., and Cenci M.A. Pharmacological validation of behavioural measures of akinesia and dyskinesia in a rat model of Parkinson's disease. Eur. J. Neurosci. 15 (2002) 120-132
50. Mackie K. Distribution of cannabinoid receptors in the central and peripheral nervous system. Handb. Exp. Pharmacol. 168 (2005) 299-325
51. Malone D.T., and Taylor D.A. Modulation by fluoxetine of striatal dopamine release following Delta9-tetrahydrocannabinol: a microdialysis study in conscious rats. Br. J. Pharmacol. 128 (1999) 21-26
52. Marsden C.D., and Parkes J.D. "On-off" effects in patients with Parkinson's disease on chronic levodopa therapy. Lancet 1 (1976) 292-296
53. Martin A.B., Fernandez-Espejo E., Ferrer B., Gorriti M.A., Bilbao A., Navarro M., Rodriguez de Fonseca F., and Moratalla R. Expression and function of CB(1) receptor in the rat striatum: localization and effects on D(1) and D(2) dopamine receptor-mediated motor behaviors. Neuropsychopharmacology 33 (2008) 1667-1679
54. Meissner W., Ravenscroft P., Reese R., Harnack D., Morgenstern R., Kupsch A., Klitgaard H., Bioulac B., Gross C.E., Bezard E., and Boraud T. Increased slow oscillatory activity in substantia nigra pars reticulata triggers abnormal involuntary movements in the 6-OHDA-lesioned rat in the presence of excessive extracellular striatal dopamine. Neurobiol. Dis. 22 (2006) 586-598
55. Mela F., Marti M., Dekundy A., Danysz W., Morari M., and Cenci M.A. Antagonism of metabotropic glutamate receptor type 5 attenuates l-DOPA-induced dyskinesia and its molecular and neurochemical correlates in a rat model of Parkinson's disease. J. Neurochem. 101 (2007) 483-497
56. Meschler J.P., and Howlett A.C. Signal transduction interactions between CB1 cannabinoid and dopamine receptors in the rat and monkey striatum. Neuropharmacology 40 (2001) 918-926
57. Miklyaeva E.I., Whishaw I.Q., and Kolb B. A golgi analysis of cortical pyramidal cells in the unilateral parkinson rat: absence of change in the affected hemisphere vs hypertrophy in the intact hemisphere. Restor. Neurol. Neurosci. 25 (2007) 91-99
58. Monory K., Blaudzun H., Massa F., Kaiser N., Lemberger T., Schutz G., Wotjak C.T., Lutz B., and Marsicano G. Genetic dissection of behavioural and autonomic effects of Delta(9)-tetrahydrocannabinol in mice. PLoS Biol. 5 (2007) e269
59. Morari M., Marti M., Sbrenna S., Fuxe K., Bianchi C., and Beani L. Reciprocal dopamine-glutamate modulation of release in the basal ganglia. Neurochem. Int. 33 (1998) 383-397
60. Morgese M.G., Cassano T., Cuomo V., and Giuffrida A. Anti-dyskinetic effects of cannabinoids in a rat model of Parkinson's disease: role of CB(1) and TRPV1 receptors. Exp. Neurol. 208 (2007) 110-119
61. Narushima M., Uchigashima M., Fukaya M., Matsui M., Manabe T., Hashimoto K., Watanabe M., and Kano M. Tonic enhancement of endocannabinoid-mediated retrograde suppression of inhibition by cholinergic interneuron activity in the striatum. J. Neurosci. 27 (2007) 496-506
62. O'Dell S.J., and Marshall J.F. Chronic l-dopa alters striatal NMDA receptors in rats with dopaminergic injury. Neuroreport 7 (1996) 2457-2461
63. Paxinos, G., Watson, C., 1998. The Rat Brain in Stereotaxic, Coordinates. 4th edition. California, USA: Academic Press, San Diego.
64. Picconi B., Centonze D., Hakansson K., Bernardi G., Greengard P., Fisone G., Cenci M.A., and Calabresi P. Loss of bidirectional striatal synaptic plasticity in l-DOPA-induced dyskinesia. Nat. Neurosci. 6 (2003) 501-506
65. Pierot L., Desnos C., Blin J., Raisman R., Scherman D., Javoy-Agid F., Ruberg M., and Agid Y. D1 and D2-type dopamine receptors in patients with Parkinson's disease and progressive supranuclear palsy. J. Neurol. Sci. 86 (1988) 291-306
66. Price D.A., Owens W.A., Gould G.G., Frazer A., Roberts J.L., Daws L.C., and Giuffrida A. CB1-independent inhibition of dopamine transporter activity by cannabinoids in mouse dorsal striatum. J. Neurochem. 101 (2007) 389-396
67. Riederer P., Lange K.W., Kornhuber J., and Danielczyk W. Glutamatergic-dopaminergic balance in the brain. Its importance in motor disorders and schizophrenia. Arzneimittelforschung 42 (1992) 265-268
68. Robelet S., Melon C., Guillet B., Salin P., and Kerkerian-Le Goff L. Chronic l-DOPA treatment increases extracellular glutamate levels and GLT1 expression in the basal ganglia in a rat model of Parkinson's disease. Eur. J. Neurosci. 20 (2004) 1255-1266
69. Rodriguez M., Morales I., Gonzalez-Mora J.L., Gomez I., Sabate M., Dopico J.G., Rodriguez-Oroz M.C., and Obeso J.A. Different levodopa actions on the extracellular dopamine pools in the rat striatum. Synapse 61 (2007) 61-71
70. Sergeeva O.A., Doreulee N., Chepkova A.N., Kazmierczak T., and Haas H.L. Long-term depression of cortico-striatal synaptic transmission by DHPG depends on endocannabinoid release and nitric oxide synthesis. Eur. J. Neurosci. 26 (2007) 1889-1894
71. 2, and KATP channels. Neurochem. Int. 52 (2008) 80-88
72. Sieradzan K.A., Fox S.H., Hill M., Dick J.P., Crossman A.R., and Brotchie J.M. Cannabinoids reduce levodopa-induced dyskinesia in Parkinson's disease: a pilot study. Neurology 57 (2001) 2108-2111
73. 3H]GABA release in the dopamine-denervated globus pallidus of the rat: the effect is dopamine independent and mediated by D2-like receptors. J. Neural Transm. 113 (2006) 1847-1853
74. Sossi V., de la Fuente-Fernandez R., Schulzer M., Troiano A.R., Ruth T.J., and Stoessl A.J. Dopamine transporter relation to dopamine turnover in Parkinson's disease: a positron emission tomography study. Ann. Neurol. 62 (2007) 468-474
75. Surmeier D.J., Ding J., Day M., Wang Z., and Shen W. D1 and D2 dopamine-receptor modulation of striatal glutamatergic signaling in striatal medium spiny neurons. Trends Neurosci. 30 (2007) 228-235
76. Takahashi K.A., and Castillo P.E. The CB1 cannabinoid receptor mediates glutamatergic synaptic suppression in the hippocampus. Neuroscience 139 (2006) 795-802
77. Tsou K., Brown S., Sanudo-Pena M.C., Mackie K., and Walker J.M. Immunohistochemical distribution of cannabinoid CB1 receptors in the rat central nervous system. Neuroscience 83 (1998) 393-411
78. Uchigashima M., Narushima M., Fukaya M., Katona I., Kano M., and Watanabe M. Subcellular arrangement of molecules for 2-arachidonoyl-glycerol-mediated retrograde signaling and its physiological contribution to synaptic modulation in the striatum. J. Neurosci. 27 (2007) 3663-3676
79. Wallmichrath I., and Szabo B. Cannabinoids inhibit striatonigral GABAergic neurotransmission in the mouse. Neuroscience 113 (2002) 671-682
80. Winkler C., Kirik D., Bjorklund A., and Cenci M.A. l-DOPA-induced dyskinesia in the intrastriatal 6-hydroxydopamine model of parkinson's disease: relation to motor and cellular parameters of nigrostriatal function. Neurobiol. Dis. 10 (2002) 165-186
81. Zeng B.Y., Dass B., Owen A., Rose S., Cannizzaro C., Tel B.C., and Jenner P. Chronic l-DOPA treatment increases striatal cannabinoid CB1 receptor mRNA expression in 6-hydroxydopamine-lesioned rats. Neurosci. Lett. 276 (1999) 71-74