Impaired behavioural and molecular adaptations to dopamine denervation and repeated L-DOPA treatment in Nur77-knockout mice

European Journal of Neuroscience

Volumn 24, Issue 3, 2006, Pages 795-805

  St Hilaire, Michel ^a   Bourhis, Emmanuelle ^a   Lévesque, Daniel ^a,b   Rouillard, Claude ^a,b  

^a LAVAL UNIVERSITY   (Canada)

^b UNIVERSITÉ LAVAL   (Canada)

Author keywords

Dopamine D3 receptors; Dynorphin; Enkephalin; Neurotensin; Nuclear receptor; Parkinson's disease

Indexed keywords

BENSERAZIDE; DOPAMINE; DOPAMINE 3 RECEPTOR; DYNORPHIN; ENKEPHALIN; LEVODOPA; MESSENGER RNA; NEUROPEPTIDE; NEUROTENSIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENERVATION; GENE; GENE DELETION; GENE EXPRESSION; KNOCKOUT MOUSE; MOUSE; MOUSE STRAIN; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; NUR77 GENE; PARKINSONISM; PRIORITY JOURNAL;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; ANTIPARKINSON AGENTS; BENSERAZIDE; CORPUS STRIATUM; DENERVATION; DISEASE MODELS, ANIMAL; DNA-BINDING PROTEINS; DOPAMINE; DOPAMINE AGENTS; DRUG RESISTANCE; ENKEPHALINS; LEVODOPA; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MOTOR ACTIVITY; NEURAL PATHWAYS; NEUROTENSIN; PARKINSON DISEASE; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RECEPTORS, DOPAMINE D3; RECEPTORS, STEROID; TRANSCRIPTION FACTORS;

EID: 33747216804     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2006.04954.x     Document Type: Article

References (52)

1. Andersson, M., Hilbertson, A. & Cenci, M.A. (1999) Striatal fosB expression is causally linked with 1-DOPA-induced abnormal involuntary movements and the associated upregulation of striatal prodynorphin mRNA in a rat model of Parkinson's disease. Neurobiol. Dis., 6, 461-474.
2. Backman, C., Perlmann, T., Wallen, A., Hoffer, B.J. & Morales, M. (1999) A selective group of dopaminergic neurons express Nurr1 in the adult mouse brain. Brain Res., 851, 125-132.
3. Beaudry, G., Langlois, M.-C., Weppe, I., Rouillard, C. & Lévesque, D. (2000) Contrasting patterns and cellular specificity of transcriptional regulation of the nuclear receptor Nerve Growth Factor-inducible B by haloperidol and clozapine in the rat forebrain. J. Neurochem., 75, 1694-1702.
4. Berendse, H.W., Galis-de Graaf, Y. & Groenewegen, H.J. (1992) Topographical organisation and relationship with ventral striatal compartments of prefrontal corticostriatal projections in the rat. J. Comp. Neurol., 316, 314-347.
5. Bezard, E., Gross, C.E. & Brotchie, J.M. (2003) Presymptomatic compensation in Parkinson's disease is not dopamine-mediated. Trends Neurosci., 26, 215-221.
6. 3 receptor expression as a mechanism of behavioral sensitization to levodopa. Proc. Natl Acad. Sci. USA, 94, 3363-3367.
7. Bordet, R., Ridray, S., Schwartz, J.C. & Sokoloff, P. (2000) Involvement of the direct striatonigral pathway in levodopa-induced sensitization in 6-hydroxydopamine-lesioned rats. Eur. J. Neurosci., 12, 2117-2123.
8. 125I](R)-trans-7-hydroxy-2-[N-propyl-N-(3′;-iodo-2′;- propenyl)amino]tetralin binding to dopamine D3 receptors in rat olfactory tubercle. J. Pharmacol. Exp. Ther., 268, 935-942.
9. Calon, F., Birdi, S., Rajput, A.H., Hornykiewicz, O., Bédard, P.J. & Di Paolo, T. (2002) Increase of preproenkephalin mRNA levels in the putamen of Parkinson disease patient with levodopa-induced dyskinesia. J. Neuropathol. Exp. Neurol., 61, 186-196.
10. Calon, F., Grondin, R., Morissette, M., Goulet, M., Blanchet, P.J., Di Paolo, T. & Bédard, P.J. (2000) Molecular basis of levodopa-induced dyskinesias. Ann. Neurol., 47, S70-S78.
11. Castel, M.-N., Morino, P., Nylander, I., Terenius, L. & Hökfelt, T. (1994) Differential dopaminergic regulation of the neurotensin striatonigral and striatopallidal pathways in the rat. Eur. J. Pharmacol., 262, 1-10.
12. Cenci, M.A., Lee, C.S. & Bjorklund, A. (1998) L-DOPA-induced dyskinesia in the rat is associated with striatal overexpression of prodynorphin- and glutamic acid decarboxylase mRNA. Eur. J. Neurosci., 10, 2694-2706.
13. Chan, R.M., Stewart, M.J. & Crabb, D.W. (1997) A direct repeat (DR-1) element in the first exon modulates transcription of the preproenkephalin A gene. Brain Res. Mol. Brain Res., 45, 50-58.
14. Chase, T.N., Mouradian, M.M. & Engber, T.M. (1993) Motor response complications and the function of striatal efferent systems. Neurology, 43, S23-S27.
15. Cossette, M., Parent, A. & Lévesque, D. (2004) Tyrosine hydroxylase-positive neurons intrinsic to the human striatum express the transcription factor Nurr1. Eur. J. Neurosci., 20, 2089-2095.
16. Crawford, P.A., Sadovsky, Y., Woodson, K., Lee, S.L. & Milbrandt, J. (1995) Adrenocortical function and regulation of the steroid 21-hydroxylase gene in NGFI-B-deficient mice. Mol. Cell Biol., 15, 4331-4316.
17. Doucet, J.P., Nakabeppu, Y., Bedard, P.J., Hope, B.T., Nestler, E.J., Jasmin, B.J., Chen, J.S., Iadarola, M.J., St Jean, M., Wigle, N., Blanchet, P., Grondin, R. & Robertson, G.S. (1996) Chronic alterations in dopaminergic neurotransmission produce a persistent elevation of deltaFosB-like protein(s) in both the rodent and primate striatum. Eur. J. Neurosci., 8, 365-381.
18. Éthier, I., Beaudry, G., St-Hilaire, M., Milbrandt, J., Rouillard, C. & Lévesque, D. (2004a) The transcription factor NGFI-B (Nur77) and retinoids play a critical role in acute neuroleptic-induced extrapyramidal effect and neuropeptide gene expression. Neuropsychopharmacology, 29, 335-346.
19. Éthier, I., Kagechika, H., Shudo, K., Rouillard, C. & Lévesque, D. (2004b) Docosahexaenoic acid reduces haloperidol-induced dyskinesias in mice: Involvement of Nur77 and retionoid receptors. Biol. Psych., 56, 522-526.
20. Franklin, K.B.J. & Paxinos, G. (2002) The Mouse Brain in Stereotaxic Coordinates. Academic Press, San Diego.
21. Gerfen, C.R. (2000) Molecular effects of dopamine on striatal-projection pathways. Trends Neurosci., 23, S64-S70.
22. Gerfen, C.R., Miyachi, S., Paletzki, R. & Brown, P. (2002) D1 dopamine receptor supersensitivity in the dopamine-depleted striatum results from a switch in the regulation of ERK1/2/MAP kinase. J. Neurosci., 22, 5042-5054.
23. Hazel, T.G., Nathans, D. & Lau, L.F. (1988) A gene inducible by serum growth factors encodes a member of the steroid and thyroid hormone receptor superfamily. Proc. Natl Acad. Sci. USA, 85, 8444-8448.
24. Henry, B., Crossman, A. & Brotchie, J. (1999) Effect of repeated L-DOPA, bromocriptine, or lisuride administration on preproenkephalin-A and preproenkephalin-B mRNA levels in the striatum of the 6-hydroxydopamine-lesioned rat. Exp. Neurol., 155, 204-220.
25. Lapointe, N., St-Hilaire, M., Martinoli, M.-G., Blanchet, J., Gould, P., Rouillard, C. & Cicchetti, F. (2004) Rotenone induced non-specific central nervous system and systemic toxicity. FASEB J., 18, 717-719.
26. Le Moine, C. & Bloch, B. (1995) D1 and D2 dopamine receptor gene expression in the rat striatum: Sensitive cRNA probes demonstrate prominent segregation of D1 and D2 mRNAs in distinct neuronal populations of the dorsal and ventral striatum. J. Comp. Neurol., 355, 418-426.
27. Lee, S.L., Wesselschmidt, R.L., Linette, G.P., Kanagawa, O., Russell, J.H. & Milbrandt, J. (1995) Unimpaired thymic and peripheral T cell death in mice lacking the nuclear receptor NGFI-B (Nur77). Science, 269, 532-535.
28. Lévesque, D., Diaz, J., Pilon, C., Martres, M.P., Giros, B., Souil, E., Schott, D., Morgat, J.L., Schwartz, J.C. & Sokoloff, P. (1992) Identification, characterization, and localization of the dopamine D3 receptor in rat brain using 7-[3H]hydroxy-N,N-di-n-propyl-2-aminotetralin. Proc. Natl Acad. Sci. USA, 89, 8155-8159.
29. Lévesque, D., Martres, M.-P., Diaz, J., Griffon, N., Lammers, C.H., Sokoloff, P. & Schwartz, J.-C. (1995) A paradoxical regulation of the dopamine D3 receptor expression suggests the involvement of an anterograde factor from dopamine neurons. Proc. Natl Acad. Sci. USA, 92, 1719-1723.
30. Lundblad, M., Picconi, B., Lindgren, H. & Cenci, M.A. (2004) A model of L-DOPA-induced dyskinesia in 6-hydroxydopamine lesioned mice: relation to motor and cellular parameters of nigrostriatal function. Neurobiol. Dis., 16, 110-123.
31. McGeorge, A.J. & Faull, R.L.M.K. (1989) The organisation of the projection from the cerebral cortex to the striatum in the rat. Neuroscience, 29, 503-537.
32. Milbrandt, J. (1988) Nerve growth factor induces a gene homologous to the glucocorticoid receptor gene. Neuron, 1, 183-188.
33. Perlmann, T. & Jansson, L. (1995) A novel pathway for vitamin A signaling mediated by RXR heterodimerization with NGFI-B and NURR1. Genes Dev., 9, 769-782.
34. Rouillard, C., Bédard, P.J., Falardeau, P. & Di Paolo, T. (1987) Behavioral and biochemical evidence for different effect of repeated administration of L-Dopa and bromocriptine on denervated versus non-denervated striatal dopamine receptors. Neuropharmacology, 26, 1601-1606.
35. Rouillard, C., St-Hilaire, M., Hodler, C., Paquet, B., Gilbert, F., Drolet, G. & Lévesque, D. (2004) Enkephalin KO mice have an increased sensitivity to denervation and repeated L-DOPA but do not show behavioural sensitization after repeated treatment with amphetamine. Soc. Neurosci. Abstr., 30, 562.2.
36. Samadi, P., Grégoire, L. & Bédard, P.J. (2003) Opioid antagonists increase the dyskinetic response to dopaminergic agents in parkinsonian monkeys: interaction between dopamine and opioid systems. Neuropharmacology, 45, 954-963.
37. Samadi, P., Grégoire, L. & Bédard, P.J. (2004) The opioid agonist morphine decreases the dyskinetic response to dopaminergic agents in parkinsonian monkeys. Neurobiol. Dis., 16, 246-253.
38. Samadi, P., Grégoire, L., Hadj Tahar, A., Di Paolo, T., Rouillard, C. & Bédard, P.J. (2005a) Naltrexone in the short-term decreases antiparkinsonian response to 1-Dopa and in the long-term increases dyskinesias in drug-naive parkinsonian monkeys. Neuropharmacology, 49, 165-173.
39. Samadi, P., Grégoire, L., Rouillard, C. & Bédard, P.J. (2005b) Dyskinesias occur in response to saline and naltrexone alone after priming with combination of dopaminergic agents and naltrexone in the MPTP parkinsonian monkeys. Neurobiol. Dis., 19, 266-272.
40. Saucedo-Cardenas, O., Quintana-Hau, J.D., Le, W.D., Smidt, M.P., Cox, J.J., De Mayo, F., Burbach, J.P. & Conneely, O.M. (1998) Nurr1 is essential for the induction of the dopaminergic phenotype and the survival of ventral mesencephalic late dopaminergic precursor neurons. Proc. Natl Acad. Sci. USA, 95, 4013-4018.
41. Smith, Y., Raju, D.V., Pare, J.F. & Sidibe, M. (2004) The thalamostriatal system: a highly specific network of the basal ganglia circuitry. Trends Neurosci., 27, 520-527.
42. St-Hilaire, M., Landry, É., Lévesque, D. & Rouillard, C. (2003) Denervation and repeated L-DOPA induce a coordinate expression of the transcription factor NGFI-B in striatal projection pathways in hemi-parkinsonian rats. Neurobiol. Dis., 14, 98-109.
43. St-Hilaire, M., Landry, É., Lévesque, D. & Rouillard, C. (2005) Denervation and repeated 1-DOPA induce complex regulatory changes in neurochemical phenotypes of striatal neurons: Implication of a dopamine D1-dependent mechanism. Neurobiol. Dis., 20, 450-460.
44. Surmeier, D.J., Song,W.J.&Yan, Z. (1996) Coordinated expression of dopamine receptors in neostriatal medium spiny neurons. J. Neurosci., 16, 6579-6591.
45. Tel, B.C., Zeng, B.-Y., Cannizzaro, C., Pearce, R.K.B., Rose, S. & Jenner, P. (2002) Alteration in striatal neuropeptide mRNA produced by repeated administration of L-DOPA, ropinirole or bromocriptine correlate with dyskinesia induction in MPTP-treated common marmosets. Neuroscience, 115, 1047-1058.
46. Tremblay, M.-È ., Saint-Pierre, M., Bourhis, E., Lévesque, D., Rouillard, C. & Cicchetti, F. (2005) Neuroprotective effects of cystamine in aged parkinsonian mice. Neurobiol. Aging, 27, 862-870.
47. Ungerstedt, U. & Arbuthnott, G.W. (1970) Quantitative recording of rotational behavior in rats after 6-hydroxy-dopamine lesions of the nigrostriatal dopamine system. Brain Res., 24, 485-493.
48. Westin, J.E., Andersson, M., Lundblad, M. & Cenci, M.A. (2001) Persistent changes in striatal gene expression induced by long term L-DOPA treatment in a rat model of Parkinson's disease. Eur. J. Neurosci., 14, 1171-1176.
49. Wilson, T.E., Fahrner, T.J., Johnston, M. & Milbrandt, J. (1991) Identification of the DNA binding site for NGFI-B by genetic selection in yeast. Science, 252, 1296-1300.
50. Willuhn, I., Sun, W. & Steiner, H. (2003) Topography of cocaine-induced gene regulation in the rat striatum: relationship to cortical inputs and role of behavioural context. Eur. J. Neurosci., 17, 1053-1066.
51. Yoshikawa, K., Williams, C. & Sabol, S.L. (1984) Rat brain preproenkephalin mRNA. cDNA cloning, primary structure, and distribution in the central nervous system. J. Biol. Chem., 259, 14301-14308.
52. Zetterström, R.H., Williams, R., Perlmann, T. & Olson, L. (1996) Cellular expression of the immediate early transcription factors Nurr1 and NGFI-B suggests a gene regulatory role in several brain regions including the nigrostriatal dopamine system. Mol. Brain Res., 41, 111-120.