Reversal of dyskinesias in an animal model of Parkinson's disease by continuous L-DOPA delivery using rAAV vectors

Brain

Volumn 128, Issue 3, 2005, Pages 559-569

  Carlsson, Thomas ^a   Winkler, Christian ^a,b   Burger, Corinna ^c   Muzyczka, Nicholas ^c   Mandel, Ronald J ^c,d   Cenci, Angela ^a   Björklund, Anders ^a   Kirik, Deniz ^a  

^a LUND UNIVERSITY   (Sweden)

^b HANNOVER MEDICAL SCHOOL   (Germany)

^c UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^d UNIVERSITY OF FLORIDA   (United States)

Author keywords

Dyskinesia; Gene therapy; GTP cyclohydrolase 1; Parkinson's disease; Tyrosine hydroxylase

Indexed keywords

DOPAMINE; GUANOSINE TRIPHOSPHATE CYCLOHYDROLASE I; LEVODOPA; MESSENGER RNA; PARVOVIRUS VECTOR; PREPROENKEPHALIN; PRODYNORPHIN; TRANSCRIPTION FACTOR FOSB; TYROSINE 3 MONOOXYGENASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINERGIC NERVE CELL; DYSKINESIA; FEMALE; GENE TRANSFER; IN VIVO STUDY; INVOLUNTARY MOVEMENT; MOTOR DYSFUNCTION; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; TREATMENT OUTCOME; VIRAL GENE DELIVERY SYSTEM; VIRUS RECOMBINANT; ADENO ASSOCIATED VIRUS; ANIMAL; BIOSYNTHESIS; DISEASE MODEL; DRUG ADMINISTRATION; GENE THERAPY; GENE VECTOR; GENETICS; METABOLISM; METHODOLOGY; PATHOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; CORPUS STRIATUM; DEPENDOVIRUS; DISEASE MODELS, ANIMAL; DRUG ADMINISTRATION SCHEDULE; DYSKINESIA, DRUG-INDUCED; FEMALE; GENE THERAPY; GENE TRANSFER TECHNIQUES; GENETIC VECTORS; LEVODOPA; PARKINSON DISEASE; RATS; RATS, SPRAGUE-DAWLEY;

EID: 15044365742     PISSN: 00068950     EISSN: None     Source Type: Journal    
DOI: 10.1093/brain/awh374     Document Type: Article

References (51)

1. Ahlskog JE, Muenter MD. Frequency of levodopa-related dyskinesias and motor fluctuations as estimated from the cumulative literature. Mov Disord 2001; 16: 448-58.
2. Andersson M, Hilbertson A, Cenci MA. 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 1999; 6: 461-74.
3. Andersson M, Konradi C, Cenci MA. cAMP response element-binding protein is required for dopamine-dependent gene expression in the intact but not the dopamine-denervated striatum. J Neurosci 2001; 21: 9930-43.
4. Bencsics C, Wachtel SR, Milstien S, Hatakeyama K, Becker JB, Kang UJ. Double transduction with GTP cyclohydrolase I and tyrosine hydroxylase is necessary for spontaneous synthesis of L-DOPA by primary fibroblasts. J Neurosci 1996; 16: 4449-56.
5. Calon F, Grondin R, Morissette M, Goulet M, Blanchet PJ, Di Paolo T, et al. Molecular basis of levodopa-induced dyskinesias. Ann Neurol 2000; 47: S70-8.
6. Cenci MA, Lee CS, 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: 2694-706.
7. Cenci MA, Whishaw IQ, Schallert T. Animal models of neurological deficits: how relevant is the rat? Nat Rev Neurosci 2002; 3: 574-9.
8. Chang JW, Wachtel SR, Young D, Kang UJ. Biochemical and anatomical characterization of forepaw adjusting steps in rat models of Parkinson's disease: studies on medial forebrain bundle and striatal lesions. Neuroscience 1999; 88: 617-28.
9. Chase TN. Levodopa therapy: consequences of the nonphysiologic replacement of dopamine. Neurology 1998; 50: S17-25.
10. Civelli O, Douglass J, Goldstein A, Herbert E. Sequence and expression of the rat prodynorphin gene. Proc Natl Acad Sci USA 1985; 82: 4291-5.
11. Corti O, Sanchez-Capelo A, Colin P, Hanoun N, Hamon M, Mallet J. Long-term doxycycline-controlled expression of human tyrosine hydroxylase after direct adenovirus-mediated gene transfer to a rat model of Parkinson's disease. Proc Natl Acad Sci USA 1999; 96: 12120-5.
12. Doucet JP, Nakabeppu Y, Bedard PJ, Hope BT, Nestler EJ, Jasmin BJ, et al. Chronic alterations in dopaminergic neurotransmission produce a persistent elevation of deltaFosB-like protein(s) in both the rodent and primate striatum. Eur J Neurosci 1996; 8: 365-81.
13. Henry B, Crossman AR, Brotchie JM. Characterization of enhanced behavioral responses to L-DOPA following repeated administration in the 6-hydroxydopamine-lesioned rat model of Parkinson's disease. Exp Neurol 1998; 151: 334-42.
14. Henry B, Crossman AR, Brotchie JM. 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 1999; 155: 204-20.
15. Henry B, Fox SH, Crossman AR, Brotchie JM. Mu- and delta-opioid receptor antagonists reduce levodopa-induced dyskinesia in the MPTP-lesioned primate model of Parkinson's disease. Exp Neurol 2001; 171: 139-46.
16. Henry B, Duty S, Fox SH, Crossman AR, Brotchie JM. Increased striatal pre-proenkephalin B expression is associated with dyskinesia in Parkinson's disease. Exp Neurol 2003; 183: 458-68.
17. Horellou P, Vigne E, Castel MN, Bameoud P, Colin P, Perricaudet M, et al. Direct intracerebral gene transfer of an adenoviral vector expressing tyrosine hydroxylase in a rat model of Parkinson's disease. Neuroreport 1994; 6: 49-53.
18. Howells RD, Kilpatrick DL, Bhatt R, Monahan JJ, Poonian M, Udenfriend S. Molecular cloning and sequence determination of rat preproenkephalin cDNA: sensitive probe for studying transcriptional changes in rat tissues. Proc Natl Acad Sci USA 1984; 81: 7651-5.
19. Johansson PA, Andersson M, Andersson KE, Cenci MA. Alterations in cortical and basal ganglia levels of opioid receptor binding in a rat model of 1-DOPA-induced dyskinesia. Neurobiol Dis 2001; 8: 220-39.
20. Kaplitt MG, Leone P, Samulski RJ, Xiao X, Pfaff DW, O'Malley KL, et al. Long-term gene expression and phenotypic correction using adeno-associated virus vectors in the mammalian brain. Nat Genet 1994; 8: 148-54.
21. Kirik D, Rosenblad C, Bjorklund A. Characterization of behavioral and neurodegenerative changes following partial lesions of the nigrostriatal dopamine system induced by intrastriatal 6-hydroxydopamine in the rat. Exp Neurol 1998; 152: 259-77.
22. Kirik D, Rosenblad C, Bjorklund A, Mandel RJ. Long-term rAAV-mediated gene transfer of GDNF in the rat Parkinson's model: intrastriatal but not intranigral transduction promotes functional regeneration in the lesioned nigrostriatal system. J Neurosci 2000; 20: 4686-700.
23. Kirik D, Georgievska B, Burger C, Winkler C, Muzyczka N, Mandel RJ, et al. Reversal of motor impairments in parkinsonian rats by continuous intrastriatal delivery of L-dopa using rAAV-mediated gene transfer. Proc Natl Acad Sci USA 2002; 99: 4708-13.
24. Lee CS, Cenci MA, Schulzer M, Bjorklund A. Embryonic ventral mesencephalic grafts improve levodopa-induced dyskinesia in a rat model of Parkinson's disease. Brain 2000; 123: 1365-79.
25. Lundblad M, Andersson M, Winkler C, Kirik D, Wierup N, Cenci MA. Pharmacological validation of behavioural measures of akinesia and dyskinesia in a rat model of Parkinson's disease. Eur J Neurosci 2002; 15: 120-32.
26. Mandel RJ, Rendahl KG, Spratt SK, Snyder RO, Cohen LK, Leff SE. Characterization of intrastriatal recombinant adeno-associated virus-mediated gene transfer of human tyrosine hydroxylase and human GTP-cyclohydrolase I in a rat model of Parkinson's disease. J Neurosci 1998; 18: 4271-84.
27. Maneuf YP, Mitchell IJ, Crossman AR, Brotchie JM. On the role of enkephalin cotransmission in the GABAergic striatal efferents to the globus pallidus. Exp Neurol 1994; 125: 65-71.
28. McLaughlin SK, Collis P, Hermonat PL, Muzyczka N. Adeno-associated virus general transduction vectors: analysis of proviral structures. J Virol 1988; 62: 1963-73.
29. Metz GA, Farr T, Ballermann M, Whishaw IQ. Chronic levodopa therapy does not improve skilled reach accuracy or reach range on a pasta matrix reaching task in 6-OHDA dopamine-depleted (hemi-Parkinson analogue) rats. Eur J Neurosci 2001; 14: 27-37.
30. Mouradian MM, Juncos JL, Fabbrini G, Schlegel J, Bartko JJ, Chase TN. Motor fluctuations in Parkinson's disease: central pathophysiological mechanisms, Part II. Ann Neurol 1988; 24: 372-8.
31. Mouradian MM, Heuser IJ, Baronti F, Chase TN. Modification of central dopaminergic mechanisms by continuous levodopa therapy for advanced Parkinson's disease. Ann Neurol 1990; 27: 18-23.
32. Nutt JG, Obeso JA, Stocchi F. Continuous dopamine-receptor stimulation in advanced Parkinson's disease. Trends Neurosci 2000; 23: S109-15.
33. Nyholm D, Askmark H, Gomes-Trolin C, Knutson T, Lennernas H, Nystrom C, et al. Optimizing levodopa pharmacokinetics: intestinal infusion versus oral sustained-release tablets. Clin Neuropharmacol 2003; 26: 156-63.
34. Obeso JA, Olanow CW, Nutt JG. Levodopa motor complications in Parkinson's disease. Trends Neurosci 2000; 23: S2-7.
35. Paxinos G, Watson C. The rat brain in stereotaxic coordinates. San Diego: Academic Press; 1998.
36. Piccini P, Weeks RA, Brooks DJ. Alterations in opioid receptor binding in Parkinson's disease patients with levodopa-induced dyskinesias. Ann Neurol 1997; 42: 720-6.
37. Pietz K, Hagell P, Odin P. Subcutaneous apomorphine in late stage Parkinson's disease: a long term follow up. J Neurol Neurosurg Psychiatry 1998; 65: 709-16.
38. Poewe W, Wenning GK. Apomorphine: an underutilized therapy for Parkinson's disease. Mov Disord 2000; 15: 789-94.
39. Schauert T, Tillerson J. Intervention strategies for degeneration of dopamine neurons in parkinsonism: Optimising behavioral assessment of outcome. In: Central Nervous System Diseases: Innovative models of CNS disease: from molecule to therapy. Emerich DF, Dean III RL and Sandburg PR, (Eds), Totowa, NJ: Humana Press; 1999. p. 131-51.
40. Schneider JS, Decamp E, Wade T. Striatal preproenkephalin gene expression is upregulated in acute but not chronic parkinsonian monkeys: implications for the contribution of the indirect striatopallidal circuit to parkinsonian symptomatology. J Neurosci 1999; 19: 6643-9.
41. Steece-Collier K, Collier TJ, Danielson PD, Kurlan R, Yurek DM, Sladek JRJr. Embryonic mesencephalic grafts increase levodopa-induced forelimb hyperkinesia in parkinsonian rats. Mov Disord 2003; 18: 1442-54.
42. Stocchi F, Ruggieri S, Vacca L, Olanow CW. Prospective randomized trial of lisuride infusion versus oral levodopa in patients with Parkinson's disease. Brain 2002; 125: 2058-66.
43. Syed N, Murphy J, Zimmerman T Jr, Mark MH, Sage JI. Ten years' experience with enteral levodopa infusions for motor fluctuations in Parkinson's disease. Mov Disord 1998; 13: 336-8.
44. Szczypka MS, Mandel RJ, Donahue BA, Snyder RO, Leff SE, Palmiter RD. Viral gene delivery selectively restores feeding and prevents lethality of dopamine-deficient mice. Neuron 1999; 22: 167-78.
45. Tel BC, Zeng BY, Cannizzaro C, Pearce RK, Rose S, Jenner P. Alterations in striatal neuropeptide mRNA produced by repeated administration of L-DOPA, ropinirole or bromocriptine correlate with dyskinesia induction in MPTP-treated common marmosets. Neuroscience 2002; 115: 1047-58.
46. Ungerstedt U, Arbuthnott GW. Quantitative recording of rotational behavior in rats after 6-hydroxy-dopamine lesions of the nigrostriatal dopamine system. Brain Res 1970; 24: 485-93.
47. Wade TV, Schneider JS. Expression of striatal preprotachykinin mRNA in symptomatic and asymptomatic 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine- exposed monkeys is related to parkinsonian motor signs. J Neurosci 2001; 21: 4901-7.
48. West MJ. Stereological methods for estimating the total number of neurons and synapses: issues of precision and bias. Trends Neurosci 1999; 22: 51-61.
49. Winkler C, Kirik D, Bjorklund A, Cenci MA. 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 2002; 10: 165-86.
50. Xu L, Daly T, Gao C, Flotte TR, Song S, Byrne BJ, et al. CMV-beta-actin promoter directs higher expression from an adeno-associated viral vector in the liver than the cytomegalovirus or elongation factor 1 alpha promoter and results in therapeutic levels of human factor X in mice. Hum Gene Ther 2001; 12: 563-73.
51. Zolotukhin S, Byrne BJ, Mason E, Zolotukhin I, Potter M, Chesnut K, et al. Recombinant adeno-associated virus purification using novel methods improves infectious titer and yield. Gene Ther 1999; 6: 973-85.