Differential effect of NR2A and NR2B subunit selective NMDA receptor antagonists on striato-pallidal neurons: Relationship to motor response in the 6-hydroxydopamine model of parkinsonism

Journal of Neurochemistry

Volumn 106, Issue 2, 2008, Pages 957-968

  Fantin, Martina ^a   Auberson, Yves P ^b   Morari, Michele ^a  

^a UNIVERSITY OF FERRARA   (Italy)

^b NOVARTIS PHARMA AG   (Switzerland)

Author keywords

6 hydroxydopamine; GABA; Microdialysis; NMDA receptor subunits; NVP AAM077; Ro 25 6981

Indexed keywords

4 AMINOBUTYRIC ACID; 4 BENZYL ALPHA (4 HYDROXYPHENYL) BETA METHYL 1 PIPERIDINEPROPANOL; GLUTAMIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2A; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; NVP AAM 077; OXIDOPAMINE; UNCLASSIFIED DRUG; 5 (ALPHA METHYL 4 BROMOBENZYLAMINO)PHOSPHONOMETHYL 1,4 DIHYDROQUINOXALINE 2,3 DIONE; 5-(ALPHA-METHYL-4-BROMOBENZYLAMINO)PHOSPHONOMETHYL-1,4-DIHYDROQUINOXALINE-2,3-DIONE; ADRENERGIC RECEPTOR STIMULATING AGENT; AMINO ACID RECEPTOR BLOCKING AGENT; PHENOL DERIVATIVE; PIPERIDINE DERIVATIVE; QUINOXALINE DERIVATIVE;

AKINESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRADYKINESIA; CONTROLLED STUDY; CORPUS STRIATUM; EXPERIMENTAL MODEL; FUNCTIONAL ASSESSMENT; GLOBUS PALLIDUS; MALE; MICRODIALYSIS; MOTOR ACTIVITY; NONHUMAN; PARKINSONISM; PRIORITY JOURNAL; RAT; SUBSTANTIA NIGRA; ANIMAL; ANIMAL BEHAVIOR; DISEASE MODEL; DRUG EFFECT; METHODOLOGY; NERVE CELL; PARKINSON DISEASE; PATHOLOGY; SPRAGUE DAWLEY RAT;

PARKINSONIA; RATTUS;

ADRENERGIC AGENTS; ANIMALS; BEHAVIOR, ANIMAL; CORPUS STRIATUM; DISEASE MODELS, ANIMAL; EXCITATORY AMINO ACID ANTAGONISTS; GLOBUS PALLIDUS; MALE; MICRODIALYSIS; MOTOR ACTIVITY; NEURONS; OXIDOPAMINE; PARKINSON DISEASE; PHENOLS; PIPERIDINES; QUINOXALINES; RATS; RATS, SPRAGUE-DAWLEY;

EID: 51649094917     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2008.05439.x     Document Type: Article

References (57)

1. Albin R. L., Young A. B. and Penney J. B. (1989) The functional anatomy of basal ganglia disorders. Trends Neurosci. 12, 366-375.
2. Alexander G. E. and Crutcher M. D. (1990) Functional architecture of basal ganglia circuits: neural substrates of parallel processing. Trends Neurosci. 13, 266-271.
3. Auberson Y. P., Allgeier H., Bischoff S., Lingenhoehl K., Moretti R. and Schmutz M. (2002) 5-Phosphonomethylquinoxalinediones as competitive NMDA receptor antagonists with a preference for the human 1A/2A, rather than 1A/2B receptor composition. Bioorg. Med. Chem. Lett. 12, 1099-1102.
4. Blanchet P. J., Papa S. M., Merman L. V., Mouradian M. M. and Chase T. N. (1997) Modulation of levodopa-induced motor response complications by NMDA antagonists in Parkinson's disease. Neurosci. Biobehav. Rev. 21, 447-453.
5. Blanchet P. J., Konitsiotis S., Whittemore E. R., Zhou Z. L., Woodward R. M. and Chase T. N. (1999) Differing effects of N-methyl-D- aspartate receptor subtype selective antagonists on dyskinesias in levodopa-treated l-methyl-4-phenyl-tetrahydropyridine monkeys. J. Pharmacol. Exp. Ther. 290, 1034-1040.
6. Chapman M. A. and See R. E. (1996) Differential effects of unique profile antipsychotic drugs on extracellular amino acids in the ventral pallidum and globus pallidus of rats. J. Pharmacol. Exp. Ther. 277, 1586-1594.
7. Chase T. N. and Oh J. D.(2000) Striatal mechanisms and pathogenesis of parkinsonian signs and motor complications. Ann. Neurol. 47, S122-S129; discussion S129-S130.
8. Dingledine R., Borges K., Bowie D. and Traynelis S. F. (1999) The glutamate receptor ion channels. Pharmacol. Rev. 51, 7-61.
9. Dunah A. W., Wang Y., Yasuda R. P., Kameyama K., Huganir R. L., Wolfe B. B. and Standaert D. G. (2000) Alterations in subunit expression, composition, and phosphorylation of striatal N-methyl- D-aspartate glutamate receptors in a rat 6-hydroxydopamine model of Parkinson's disease. Mol. Pharmacol. 57, 342-352.
10. Engber T. M., Papa S. M., Boldry R. C. and Chase T. N. (1994) NMDA receptor blockade reverses motor response alterations induced by levodopa. Neuroreport 5, 2586-2588.
11. Fantin M., Marti M., Auberson Y. P. and Morari M. (2007) NR2A and NR2B subunit containing NMDA receptors differentially regulate striatal output pathways. J. Neurochem. 103, 2200-2211.
12. Feng B., Tse H. W., Skifter D. A., Morley R., Jane D. E. and Monaghan D. T. (2004) Structure-activity analysis of a novel NR2C/NR2D- preferring NMDA receptor antagonist: l-(phenanthrene-2-car- bonyl) piperazine-2,3-dicarboxylic acid. Br. J. Pharmacol. 141, 508-516.
13. Fiorentini C., Rizzetti M. C, Busi C, Bontempi S., Collo G., Spano P. and Missale C. (2006) Loss of synaptic Dl dopamine/N-methyl-D- aspartate glutamate receptor complexes in L-DOPA-induced dyskinesia in the rat. Mol. Pharmacol. 69, 805-812.
14. Fischer G., Mutel V, Trube G., Malherbe P., Kew J. N, Mohacsi E., Heitz M. P. and Kemp J. A. (1997) Ro 25-6981, a highly potent and selective blocker of N-methyl-D-aspartate receptors containing the NR2B subunit. Characterization in vitro. J. Pharmacol. Exp. Ther. 283, 1285-1292.
15. Ganguly A. and Keefe K. A. (2001) Unilateral dopamine depletion increases expression of the 2A subunit of the N-methyl-D-aspartate receptor in enkephalin-positive and enkephalin-negative neurons. Neuroscience 103, 405-412.
16. Gardoni F., Picconi B., Ghiglieri V., Polli F., Bagetta V., Bernardi G., Cattabeni F., Di Luca M. and Calabresi P. (2006) A critical interaction between NR2B and MAGUK in L-DOPA induced dyskinesia. J. Neurosci. 26, 2914-2922.
17. Hallett P. J. and Standaert D. G. (2004) Rationale for and use of NMDA receptor antagonists in Parkinson's disease. Pharmacol. Ther. 102, 155-174.
18. Hallett P. J., Dunah A. W., Ravenscroft P., Zhou S., Bezard E., Crossman A. R., Brotchie J. M. and Standaert D. G. (2005) Alterations of striatal NMDA receptor subunits associated with the development of dyskinesia in the MPTP-lesioned primate model of Parkinson's disease. Neuropharmacology 48, 503-516.
19. Hauber W. and Lutz S. (1999) Dopamine Dl or D2 receptor blockade in the globus pallidus produces akinesia in the rat. Behav. Brain Res. 106, 143-150.
20. Hernandez A., Sierra A., Valdiosera R., Florán B., Erlij D. and Aceves J. (2007) Presynaptic Dl dopamine receptors facilitate glutamatergic neurotransmission in the rat globus pallidus. Neurosci. Lett. 425, 188-191.
21. Konitsiotis S., Blanchet P. J., Verhagen L., Lamers E. and Chase T. N. (2000) AMPA receptor blockade improves levodopa-induced dyskinesia in MPTP monkeys. Neurology 54, 1589-1595.
22. Landwehrmeyer G. B., Standaert D. G., Testa C. M., Penney J. B. Jr and Young A. B. (1995) NMDA receptor subunit mRNA expression by projection neurons and interneurons in rat striatum. J. Neurosci. 15, 5297-5307.
23. Laurie D. J. and Seeburg P. H. (1994) Ligand affinities at recombinant N-methyl-D-aspartate receptors depend on subunit composition. Eur. J. Pharmacol. 268, 335-345.
24. Löschmann P. A., De Groote C., Smith L., Wullner U., Fischer G, Kemp J. A., Jenner P. and Klockgether T. (2004) Antiparkinsonian activity of Ro 25-6981, a NR2B subunit specific NMDA receptor antagonist, in animal models of Parkinson's disease. Exp. Neurol. 187, 86-93.
25. Maneuf Y. P., Mitchell I. J., Crossman A. R. and Brotchie J. M. (1994) On the role of enkephalin cotransmission in the GABAergic striatal efferents to the globus pallidus. Exp. Neurol. 125, 65-71.
26. Marin C., Papa S., Engber T. M., Bonastre M., Tolosa E. and Chase T. N. (1996) MK-801 prevents levodopa-induced motor response alterations in parkinsonian rats. Brain Res. 736, 202-205.
27. Marti M., Sbrenna S., Fuxe K, Bianchi C., Beani L. and Morari M. (1999) In vitro evidence for increased facilitation of striatal acetylcholine release via pre- and postsynaptic NMDA receptors in hemiparkinsonian rats. J. Neurochem. 72, 875-878.
28. Marti M., Mela F., Bianchi C, Beani L. and Morari M.(2002) Striatal dopamine-NMDA receptor interactions in the modulation of glutamate release in the substantia nigra pars reticulata in vivo: opposite role for Dl and D2 receptors. J. Neurochem. 83, 635-644.
29. Marti M., Mela F., Fantin M. et al. (2005) Blockade of nociceptin/or-phanin FQ transmission attenuates symptoms and neurodegenera- tion associated with Parkinson's disease. J. Neurosci. 25, 9591-9601.
30. Marti M., Trapella C, Viaro R. and Morari M. (2007) The nociceptin/orphanin FQ receptor antagonist J-l13397 and L-DOPA additively attenuate experimental parkinsonism through overinhibition of the nigrothalamic pathway. J. Neurosci. 27, 1297-1307.
31. Meguro H., Mori H., Araki K, Kushiya E., Kutsuwada T, Yamazaki M., Kumanishi T., Arakawa M., Sakimura K. and Mishina M. (1992)
32. Functional characterization of a heteromeric NMDA receptor channel expressed from cloned cDNAs. Nature 357, 70-74.
33. Mitchell I. J. and Carroll C. B. (1997) Reversal of parkinsonian symptoms in primates by antagonism of excitatory amino acids transmission: potential mechanisms of action. Neurosci. Biobehav. Rev. 21, 469-475.
34. Monaghan D. T. and Larsen H. (1997) NR1 and NR2 subunit contributions to N-methyl-D-aspartate receptor channel blocker pharmacology. J. Pharmacol. Exp. Ther. 280, 614-620.
35. Monyer H., Sprengel R., Schoepfer R., Herb A., Higuchi M., Lomeli H., Burnashev N., Sakmann B. and Seeburg R H. (1992) Heteromeric NMDA receptors: molecular and functional distinction of subtypes. Science 256, 1217-1221.
36. Morari M., Marti M., Sbrenna S., Fuxe K., Bianchi C. and Beani L. (1998) Reciprocal dopamine-glutamate modulation of release in the basal ganglia. Neurochem. Int. 33, 383-397.
37. Morissette M., Dridi M., Calon F., Tahar A. H., Meltzer L. T., Bedard R J. and Di Paolo T. (2006) Prevention of levodopa-induced dyskinesias by a selective NR1A/2B N-methyl-D-aspartate receptor antagonist in parkinsonian monkeys: implication of preproen- kephalin. Mov. Disord. 21, 9-17.
38. Mutel V., Buchy D., Klingelschmidt A., Messer J., BleuelZ., Kemp J. A. and Richards J. G. (1998) In vitro binding properties in rat brain of [3H]Ro 25-6981, a potent and selective antagonist of NMDA receptors containing NR2B subunits. J. Neurochem. 70, 2147-2155.
39. Nash J. E., Hill M. P. and Brotchie J. M. (1999) Antiparkinsonian actions of blockade of NR2B-containing NMDA receptors in the reser- pine-treated rat. Exp. Neurol. 155, 42-48.
40. Nash J. E., Fox S. H., Henry B., Hill M. P., Peggs D., McGuire S., Maneuf Y., Hille C., Brotchie J. M. and Crossman A. R. (2000) Antipar kinsonian actions of ifenprodil in the MPTP-lesioned marmoset model of Parkinson's disease. Exp. Neurol. 165, 136-142.
41. Nash J. E., Ravenscroft P., McGuire S., Crossman A. R., Menniti F. S. and Brotchie J. M. (2004) The NR2B-selective NMDA receptor antagonist CP-101,606 exacerbates L-DOPA-induced dyskinesia and provides mild potentiation of anti-parkinsonian effects of L- DOPA in the MPTP-lesioned marmoset model of Parkinson's disease. Exp. Neurol. 188, 471-479.
42. Ochi M., Koga K, Kurokawa M., Kase H., Nakamura J. and Kuwana Y. (2000) Systemic administration of adenosine A(2A) receptor antagonist reverses increased GABA release in the globus pallidus of unilateral 6-hydroxydopamine- lesioned rats: a microdialysis study. Neuroscience 100, 53-62.
43. Papa S. M. and Chase T. N. (1996) Levodopa-induced dyskinesias improved by a glutamate antagonist in Parkinsonian monkeys. Ann. Neurol. 39, 574-578.
44. Papa S. M., Boldry R. C., Engber T. M., Kask A. M. and Chase T. N. (1995) Reversal of levodopa-induced motor fluctuations in experimental parkinsonism by NMDA receptor blockade. Brain Res. 701, 13-18.
45. Paxinos G. and Watson C. (1982) The Rat Brain in Stereotaxic Coordinates. Academic Press, Sydney, NSW
46. Pycock C., Horton R. W. and Marsden C. D. (1976) The behavioural effects of manipulating GABA function in the globus pallidus. Brain Res. 116, 353-359.
47. Rajput A. H., Rajput A., Lang A. E., Kumar R., Uitti R. J. and Galvez- Jimenez N. (1998) New use for an old drug: amantadine benefits levodopa-induced dyskinesia. Mov. Disord. 13, 851.
48. Robertson R. G, Graham W. C., Sambrook M. A. and Crossman A. R. (1991) Further investigations into the pathophysiology of MPTP-induced parkinsonism in the primate: an intracerbral microdyalisis study of the globus pallidus. Brain Res. 563, 278-280.
49. Rozas G., Guerra M. J. and Labandeira-Garcia J. L. (1997) An automated rotarod method for quantitative drug-free evaluation of overall motor deficits in rat models of parkinsonism. Brain Res. 2, 75-84.
50. Sanberg P. R., Bunsey M. D., Giordano M. and Norman A. B. (1988) The catalepsy test: its ups and downs. Behav. Neurosci. 102, 748-759.
51. Standaert D. G., Friberg I. K., Landwehrmeyer G. B., Young A. B. and Penney J. B. Jr (1999) Expression of NMDA glutamate receptor subunit mRNAs in neurochemically identified projection and in-terneurons in the striatum of the rat. Brain Res. Mol. Brain Res. 64, 11-23.
52. Steece-Collier K., Chambers L. K., Jaw-Tsai S. S., Menniti F. S. and Greenamyre J. T. (2000) Antiparkinsonian actions of CP-101,606, an antagonist of NR2B subunit-containing N-methyl-D-aspartate receptors. Exp. Neurol. 163, 239-243.
53. Ulas J. and Cotman C. W. (1996) Dopaminergic denervation of striatum results in elevated expression of NR2A subunit. Neuroreport 7, 1789-1793.
54. Ungerstedt U. and Arbuthnott G. W. (1970) Quantitative recording of rotational behaviour in rats after 6-hydroxydopamine lesions of the nigrostriatal dopamine system. Brain Res. 24, 485-493.
55. Verhagen Merman L., Del Dotto P., Blanchet P. J., van den Munckhof P. and Chase T. N. (1998) Blockade of glutamatergic transmission as treatment for dyskinesias and motor fluctuations in Parkinson's disease. Amino Acids 14, 75-82.
56. Vrijmoed-de Vries M. C., Tonissen H. and Cools A. R. (1987) The relationship between hindlimb disturbances, forelimb disturbances and catalepsy after increasing doses of muscimol injected into the striatal-pallidal complex. Psychopharmacology 92, 73-77.
57. Wessell R. H., Ahmed S. M., Menniti F. S., Dunbar G. L., Chase T. N. and Oh J. D. (2004) NR2B selective NMDA receptor antagonist CP-101,606 prevents levodopa-induced motor response alterations in hemi-parkinsonian rats. Neuropharmacology 47, 184-194.