Performance of movement in hemiparkinsonian rats influences the modifications induced by dopamine agonists in striatal efferent dynorphinergic neurons

Experimental Neurology

Volumn 247, Issue , 2013, Pages 663-672

  Frau, Lucia ^a   Morelli, Micaela ^a,b   Simola, Nicola ^a  

^a UNIVERSITY OF CAGLIARI   (Italy)

^b CNR   (Italy)

Author keywords

6 OHDA; In situ hybridization; Movement; MRNA; Parkinson's disease; Priming; Restrainer; Striatonigral; Striatopallidal; Zif 268

Indexed keywords

2,3,4,5 TETRAHYDRO 7,8 DIHYDROXY 1 PHENYL 1H 3 BENZAZEPINE; APOMORPHINE; DOPAMINE RECEPTOR STIMULATING AGENT; DYNORPHIN; ENKEPHALIN; GLUTAMATE DECARBOXYLASE 67; MESSENGER RNA; OXIDOPAMINE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DYNORPHIN GENE; EFFERENT NERVE; ENKEPHALIN GENE; EXPERIMENTAL RAT; GAD67 GENE; GENE; GENE ACTIVATION; GENE EXPRESSION REGULATION; MALE; MOVEMENT (PHYSIOLOGY); NEUROCHEMISTRY; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; PARKINSONISM; PRIORITY JOURNAL; RAT; SINGLE CELL ANALYSIS; ZIF 268 GENE;

1-PHENYL-2,3,4,5-TETRAHYDRO-(1H)-3-BENZAZEPINE-7,8-DIOL; 6-HYDROXYDOPAMINE; 6-OHDA; ANALYSIS OF VARIANCE; ANOVA; D(1) RECEPTOR; D(2) RECEPTOR; DOPAMINE TYPE 1 RECEPTOR; DOPAMINE TYPE 2 RECEPTOR; GAD67; GLUTAMIC ACID DECARBOXYLASE 67; IN SITU HYBRIDIZATION; MESSENGER RNA; MOVEMENT; MRNA; PARKINSON'S DISEASE; PD; PRIMING; RESTRAINER; RIBONUCLEASE; RNASE; SALINE-SODIUM CITRATE; SKF 38393; SSC; STRIATONIGRAL; STRIATOPALLIDAL; ZIF-268;

2,3,4,5-TETRAHYDRO-7,8-DIHYDROXY-1-PHENYL-1H-3-BENZAZEPINE; ADRENERGIC AGENTS; ANALYSIS OF VARIANCE; ANIMALS; APOMORPHINE; CORPUS STRIATUM; DISEASE MODELS, ANIMAL; DOPAMINE AGONISTS; DYNORPHINS; EARLY GROWTH RESPONSE PROTEIN 1; ENKEPHALINS; FUNCTIONAL LATERALITY; GENE EXPRESSION REGULATION; MALE; MOTOR NEURONS; MOVEMENT; OXIDOPAMINE; PARKINSON DISEASE; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER;

EID: 84881377159     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2013.03.002     Document Type: Article

References (57)

1. Albin R.L., Young A.B., Penney J.B. The functional anatomy of basal ganglia disorders. Trends Neurosci. 1989, 12:366-375.
2. Aubert I., Guigoni C., Håkansson K., Li Q., Dovero S., Barthe N., Bioulac B.H., Gross C.E., Fisone G., Bloch B., Bezard E. Increased D1 dopamine receptor signaling in levodopa-induced dyskinesia. Ann. Neurol. 2005, 57:17-26.
3. Barone P., Morelli M., Popoli M., Cicarelli G., Campanella G., Di Chiara G. Behavioural sensitization in 6-hydroxydopamine lesioned rats involves the dopamine signal transduction: changes in DARPP-32 phosphorylation. Neuroscience 1994, 61:867-873.
4. Blanchet P.J., Fang J., Gillespie M., Sabounjian L., Locke K.W., Gammans R., Mouradian M.M., Chase T.N. Effects of the full dopamine D1 receptor agonist dihydrexidine in Parkinson's disease. Clin. Neuropharmacol. 1998, 21:339-343.
5. Boraud T., Bezard E., Bioulac B., Gross C.E. From single extracellular unit recording in experimental and human Parkinsonism to the development of a functional concept of the role played by the basal ganglia in motor control. Prog. Neurobiol. 2002, 66:265-283.
6. Calon F., Grondin R., Morissette M., Goulet M., Blanchet P.J., Di Paolo T., Bédard P.J. Molecular basis of levodopa-induced dyskinesias. Ann. Neurol. 2000, 47:S70-S78.
7. Carta A., Fenu S., Morelli M. Alterations in GAD67, dynorphin and enkephalin mRNA in striatal output neurons following priming in the 6-OHDA model of Parkinson's disease. Neurol. Sci. 2001, 22:59-60.
8. Carta A.R., Fenu S., Pala P., Tronci E., Morelli M. Selective modifications in GAD67 mRNA levels in striatonigral and striatopallidal pathways correlate to dopamine agonist priming in 6-hydroxydopamine-lesioned rats. Eur. J. Neurosci. 2003, 18:2563-2572.
9. Carta A.R., Tronci E., Pinna A., Morelli M. Different responsiveness of striatonigral and striatopallidal neurons to L-DOPA after a subchronic intermittent L-DOPA treatment. Eur. J. Neurosci. 2005, 21:1196-1204.
10. Carta A.R., Frau L., Pinna A., Pontis S., Simola N., Schintu N., Morelli M. Behavioral and biochemical correlates of the dyskinetic potential of dopaminergic agonists in the 6-OHDA lesioned rat. Synapse 2008, 62:524-533.
11. Carta A.R., Frau L., Pinna A., Morelli M. Dyskinetic potential of dopamine agonists is associated with different striatonigral/striatopallidal zif-268 expression. Exp. Neurol. 2010, 224:395-402.
12. Cenci M.A., Lee C.S., Bjorklund A. L-DOPA-induced dyskinesia in the rat is associated with striatal overexpression of prodynorphin and glutamic acid decarboxylase mRNA. Eur. J. Neurosci. 1998, 10:2694-2706.
13. Cenci M.A., Ohlin K.E., Rylander D. Plastic effects of L-DOPA treatment in the basal ganglia and their relevance to the development of dyskinesia. Parkinsonism Relat. Disord. 2009, 15:S59-S63.
14. Cohen A.D., Tillerson J.L., Smith A.D., Schallert T., Zigmond M.J. Neuroprotective effects of prior limb use in 6-hydroxydopamine-treated rats: possible role of GDNF. J. Neurochem. 2003, 85:299-305.
15. Crocker S.J., Morelli M., Wigle N., Nakabeppu Y., Robertson G.S. D1-receptor-related priming is attenuated by antisense-mediated 'Knockdown' of FosB expression. Mol. Brain Res. 1998, 53:69-77.
16. Döbrössy M., Busse M., Piroth T., Rosser A., Dunnett S., Nikkhah G. Neurorehabilitation with neural transplantation. Neurorehabil. Neural Repair 2010, 24:692-701.
17. Dutra M.F., Jaeger M., Ilha J., Kalil-Gaspar P.I., Marcuzzo S., Achaval M. Exercise improves motor deficits and alters striatal GFAP expression in a 6-OHDA-induced rat model of Parkinson's disease. Neurol. Sci. 2012, 33:1137-1144.
18. Frazzitta G., Bertotti G., Uccellini D., Maestri R. Parkinson's disease rehabilitation: a pilot study with 1year follow up. Mov. Disord. 2010, 25:1762-1763.
19. Frazzitta G., Bertotti G., Morelli M., Riboldazzi G., Pelosin E., Balbi P., Boveri N., Comi C., Turla M., Leva S., Felicetti G., Maestri R. Rehabilitation improves dyskinesias in Parkinsonian patients: a pilot study comparing two different rehabilitative treatments. NeuroRehabilitation 2012, 30:295-301.
20. Gerfen C.R., Engber T.M., Mahan L.C., Susel Z., Chase T.N., Monsma F.J., Sibley D.R. D1 and D2 dopamine receptor-regulated gene expression of striatonigral and striatopallidal neurons. Science 1990, 250:1429-1432.
21. Gerfen C.R., Miyachi S., Paletzki R., Brown P. D1 dopamine receptor supersensitivity in the dopamine-depleted striatum results from a switch in the regulation of ERK1/2/MAP kinase. J. Neurosci. 2002, 22:5042-5054.
22. Goodwin V.A., Richards S.H., Taylor R.S., Taylor A.H., Campbell J.L. The effectiveness of exercise interventions for people with Parkinson's disease: a systematic review and meta-analysis. Mov. Disord. 2008, 23:631-640.
23. Goulet M., Grondin R., Blanchet P.J., Bédard P.J., Di Paolo T. Dyskinesias and tolerance induced by chronic treatment with a D1 agonist administered in pulsatile or continuous mode do not correlate with changes of putaminal D1 receptors in drug-naive MPTP monkeys. Brain Res. 1996, 719:129-137.
24. Graybiel A.M. The basal ganglia: learning new tricks and loving it. Curr. Opin. Neurobiol. 2005, 15:638-644.
25. Hadj Tahar A., Grégoire L., Darré A., Bélanger N., Meltzer L., Bédard P.J. Effect of a selective glutamate antagonist on L-dopa-induced dyskinesias in drug-naive parkinsonian monkeys. Neurobiol. Dis. 2004, 15:171-176.
26. Konitsiotis S., Tsironis C. Levodopa-induced dyskinesia and rotational behavior in hemiparkinsonian rats: independent features or components of the same phenomenon?. Behav. Brain Res. 2006, 170:337-341.
27. Kreitzer A.C., Malenka R.C. Striatal plasticity and basal ganglia circuit function. Neuron 2008, 60:543-554.
28. Morelli M., Fenu S., Garau L., Di Chiara G. Time and dose dependence of the 'priming' of the expression of dopamine receptor supersensitivity. Eur. J. Pharmacol. 1989, 162:329-335.
29. Morelli M., Fenu S., Pinna A., Cozzolino A., Carta A., Di Chiara G. "Priming" to dopamine agonist-induced contralateral turning as a model of non-associative sensitization to the expression of the post-synaptic dopamine message. Behav. Pharmacol. 1993, 4:389-397.
30. Morelli M., Fenu S., Carta A., Di Chiara G. Effect of MK 801 on priming of D1-dependent contralateral turning and its relationship to c-fos expression in the rat caudate-putamen. Behav. Brain Res. 1996, 79:93-100.
31. Morin N., Grégoire L., Morissette M., Desrayaud S., Gomez-Mancilla B., Gasparini F., Di Paolo T. MPEP, an mGlu5 receptor antagonist, reduces the development of l-DOPA-induced motor complications in de novo parkinsonian monkeys: biochemical correlates. Neuropharmacology 2013, 66:355-364.
32. Nadjar A., Gerfen C.R., Bezard E. Priming for l-dopa-induced dyskinesia in Parkinson's disease: a feature inherent to the treatment or the disease?. Prog. Neurobiol. 2009, 87:1-9.
33. Packard M.G., Knowlton B.J. Learning and memory functions of the Basal Ganglia. Annu. Rev. Neurosci. 2002, 25:563-593.
34. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 1998, Academic Press, London. 4th ed.
35. Pellegrino L.J., Pellegrino A.S., Cushman A.J. A Stereotaxic Atlas of the Rat Brain 1979, Plenum Press, New York.
36. Picconi B., Centonze D., Håkansson K., Bernardi G., Greengard P., Fisone G., Cenci M.A., Calabresi P. Loss of bidirectional striatal synaptic plasticity in L-DOPA-induced dyskinesia. Nat. Neurosci. 2003, 6:501-506.
37. Picconi B., Pisani A., Barone I., Bonsi P., Centonze D., Bernardi G., Calabresi P. Pathological synaptic plasticity in the striatum: implications for Parkinson's disease. Neurotoxicology 2005, 26:779-783.
38. Pinna A., Morelli M., Drukarch B., Stoof J.C. Priming of 6-hydroxydopamine-lesioned rats with L-DOPA or quinpirole results in an increase in dopamine D1 receptor-dependent cyclic AMP production in striatal tissue. Eur. J. Pharmacol. 1997, 331:23-26.
39. Pinna A., Pontis S., Morelli M. Expression of dyskinetic movements and turning behaviour in subchronic L-DOPA 6-hydroxydopamine-treated rats is influenced by the testing environment. Behav. Brain Res. 2006, 171:175-178.
40. Pisani A., Centonze D., Bernardi G., Calabresi P. Striatal synaptic plasticity: implications for motor learning and Parkinson's disease. Mov. Disord. 2005, 20:395-402.
41. Pollack A.E., Thomas L.I. D1 priming enhances both D1- and D2-mediated rotational behavior and striatal Fos expression in 6-hydroxydopamine lesioned rats. Pharmacol. Biochem. Behav. 2010, 94:346-351.
42. Pollack A.E., Turgeon S.M., Fink J.S. Apomorphine priming alters the response of striatal outflow pathways to D2 agonist stimulation in 6-hydroxydopamine-lesioned rats. Neuroscience 1997, 79:79-93.
43. Rascol O., Nutt J.G., Blin O., Goetz C.G., Trugman J.M., Soubrouillard C., Carter J.H., Currie L.J., Fabre N., Thalamas C., Giardina W.W., Wright S. Induction by dopamine D1 receptor agonist ABT-431 of dyskinesia similar to levodopa in patients with Parkinson disease. Arch. Neurol. 2001, 58:249-254.
44. Ravenscroft P., Chalon S., Brotchie J.M., Crossman A.R. Ropinirole versus L-DOPA effects on striatal opioid peptide precursors in a rodent model of Parkinson's disease: implications for dyskinesia. Exp. Neurol. 2004, 185:36-46.
45. Santini E., Valjent E., Usiello A., Carta M., Borgkvist A., Girault J.A., Hervé D., Greengard P., Fisone G. Critical involvement of cAMP/DARPP-32 and extracellular signal-regulated protein kinase signaling in L-DOPA-induced dyskinesia. J. Neurosci. 2007, 27:6995-7005.
46. Schallert T., Fleming S.M., Leasure J.L., Tillerson J.L., Bland S.T. CNS plasticity and assessment of forelimb sensorimotor outcome in unilateral rat models of stroke, cortical ablation, parkinsonism and spinal cord injury. Neuropharmacology 2000, 39:777-787.
47. Scholz B., Svensson M., Alm H., Sköld K., Fälth M., Kultima K., Guigoni C., Doudnikoff E., Li Q., Crossman A.R., Bezard E., Andrén P.E. Striatal proteomic analysis suggests that first L-dopa dose equates to chronic exposure. PLoS One 2008, 3:e1589.
48. Schouenborg J. Learning in sensorimotor circuits. Curr. Opin. Neurobiol. 2004, 14:693-697.
49. Simola N., Morelli M., Carta A.R. The 6-hydroxydopamine model of Parkinson's disease. Neurotox. Res. 2007, 11:151-167.
50. Simola N., Di Chiara G., Daniels W.M., Schallert T., Morelli M. Priming of rotational behavior by a dopamine receptor agonist in Hemiparkinsonian rats: movement-dependent induction. Neuroscience 2009, 158:1625-1631.
51. Smith A.D., Zigmond M.J. Can the brain be protected through exercise? Lessons from an animal model of parkinsonism. Exp. Neurol. 2003, 184:31-39.
52. Soghomonian J.J., Gonzales C., Chesselet M.F. Messenger RNAs encoding glutamate-decarboxylase are differentially affected by nigrostriatal lesions in subpopulations of striatal neurons. Brain Res. 1992, 576:68-79.
53. Tajiri N., Yasuhara T., Shingo T., Kondo A., Yuan W., Kadota T., Wang F., Baba T., Tayra J.T., Morimoto T., Jing M., Kikuchi Y., Kuramoto S., Agari T., Miyoshi Y., Fujino H., Obata F., Takeda I., Furuta T., Date I. Exercise exerts neuroprotective effects on Parkinson's disease model of rats. Brain Res. 2010, 1310:200-207.
54. Tillerson J.L., Cohen A.D., Philhower J., Miller G.W., Zigmond M.J., Schallert T. Forced limb-use effects on the behavioral and neurochemical effects of 6-hydroxydopamine. J. Neurosci. 2001, 21:4427-4435.
55. Van de Witte S.V., Drukarch B., Stoof J.C., Voorn P. Priming with L-DOPA differently affects dynorphin and substance P mRNA levels in the striatum of 6-hydroxydopamine-lesioned rats after challenge with dopamine D1-receptor agonist. Mol. Brain Res. 1998, 61:219-223.
56. Van De Witte S.V., Groenewegen H.J., Voorn P. MK-801 alters the effects of priming with L-DOPA on dopamine D1 receptor-induced changes in neuropeptide mRNA levels in the rat striatal output neurons. Synapse 2002, 43:1-11.
57. Vernier P., Julien J.F., Rataboul P., Fourrier O., Feuerstein C., Mallet J. Similar time course changes in striatal levels of glutamic acid decarboxylase and proenkephalin mRNA following dopaminergic deafferentation in the rat. J. Neurochem. 1988, 51:1375-1380.