Vesicular monoamine transporter-2 and aromatic l-amino acid decarboxylase gene therapy prevents development of motor complications in parkinsonian rats after chronic intermittent l-3,4-dihydroxyphenylalanine administration

Experimental Neurology

Volumn 197, Issue 1, 2006, Pages 215-224

  Lee, Won Yong ^a   Lee, Eun Ah ^a,b   Jeon, Mi Young ^a   Kang, Ho Young ^a   Park, Yong Gu ^c  

^a Sungkyunkwan University School of Medicine   (South Korea)

^b Seodaemoon Hospital   (South Korea)

^c Yonsei University   (South Korea)

Author keywords

AADC; Dopamine; Gene therapy; l DOPA; Motor fluctuations; Parkinson's disease; Short duration response; VMAT 2

Indexed keywords

AROMATIC LEVO AMINO ACID DECARBOXYLASE; LEVODOPA; VESICULAR MONOAMINE TRANSPORTER 2;

AKINESIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BEHAVIOR; CELL BASED GENE THERAPY; CONTROLLED STUDY; CORPUS STRIATUM; DNA MODIFICATION; DRUG EFFECT; EXPERIMENTAL MODEL; FEMALE; FIBROBLAST; FORELIMB; GENETIC TRANSDUCTION; LONG TERM CARE; MOTOR DYSFUNCTION; NONHUMAN; PARKINSONISM; PRIORITY JOURNAL; RAT; TREATMENT OUTCOME;

ANIMALS; ANTIPARKINSON AGENTS; AROMATIC-L-AMINO-ACID DECARBOXYLASES; CELLS, CULTURED; DATA INTERPRETATION, STATISTICAL; DOPAMINE; FEMALE; FIBROBLASTS; FORELIMB; GENE THERAPY; LEVODOPA; MEDIAL FOREBRAIN BUNDLE; MICROSCOPY, IMMUNOELECTRON; PARKINSON DISEASE; RATS; RATS, INBRED F344; SUBCELLULAR FRACTIONS; VESICULAR MONOAMINE TRANSPORT PROTEINS;

EID: 29144514762     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2005.09.012     Document Type: Article

References (77)

1. J.E. Ahlskog, and M.D. Muenter Frequency of levodopa-related dyskinesias and motor fluctuations as estimated from the cumulative literature Mov. Disord. 16 2001 448 458
2. S. Amara Monoamine transporters: basic biology and clinical implications Neuroscience 1 1995 259 268
3. K.S. Bankiewicz, J.L. Eberling, M. Kohutnicka, W. Jagust, P. Pivirotto, J. Bringas, J. Cunningham, T.F. Budinger, and J. Harvey-White Convection-enhanced delivery of AAV vector in parkinsonian monkeys; in vivo detection of gene expression and restoration of dopaminergic function using pro-drug approach Exp. Neurol. 164 2000 2 14
4. C. Bencsics, S.R. Wachtel, S. Milstien, K. Hatakeyama, J.B. Becker, and U.J. Kang Double transduction with GTP cyclohydrolase I and tyrosine hydroxylase is necessary for spontaneous synthesis of l-DOPA by primary fibroblasts J. Neurosci. 16 1996 4449 4456
5. H. Bernheimer, W. Birkmayer, and O. Hornykiewicz Brain dopamine and the syndromes of Parkinson and Huntington: clinical, morphological, and neurochemical correlations J. Neurol. Sci. 20 1973 415 455
6. W. Birkmayer, and O. Hornykiewicz Der l-3, 4-Dioxyphenylalanin (=DOPA) effekt bei der Parkinson-Akinese Wien. Klin. Wochenschr. 73 1961 787 788
7. R.D. Broadwell, and A.M. Cataldo The neuronal endoplasmic reticulum: its cytochemistry and contribution to the endomembrane system: I. Cell bodies and dendrites J. Histochem. Cytochem. 31 1983 1077 1088
8. T. Carlsson, C. Winkler, C. Burger, N. Muzyczka, R.J. Mandel, A. Cenci, and A. Kirik Reversal of dyskinesias in an animal model of Parkinson's disease by continuous l-DOPA delivery using rAAV vectors Brain 128 2005 559 569
9. J.M. Cedarbaum, M. Silvestri, and H. Kutt Sustained enteral administration of levodopa increases and interrupted infusion decreases levodopa dose requirements Neurology 40 1990 995 997
10. J.W. Chang, S.R. Wachtel, D. Young, and U.J. Kang Biochemical and anatomical characterization of forepaw adjusting steps in rat models of Parkinson's disease: studies on medial forebrain bundle and striatal lesions Neuroscience 88 1999 617 628
11. T.N. Chase Levodopa therapy: consequences of the nonphysiologic replacement of dopamine Neurology 50 1998 S17 S25
12. T.N. Chase, T.M. Engber, and M.M. Mouradian Palliative and prophylactic benefits of continuously administered dopaminomimetics in Parkinson's disease Neurology 44 1994 S15 S18
13. M. Contin, R. Riva, P. Martinelli, G. Procaccianti, P. Cortelli, P. Avoni, and A. Baruzzi Response to a standard oral levodopa test in parkinsonian patients with and without motor fluctuations Clin. Neuropharmacol. 13 1990 19 28
14. J.R. Cooper, F.E. Bloom, and R.H. Roth The Biochemical Basis of Neuropharmacology 1996 Oxford Univ. Press New York
15. C.G. Cotzias, M.H. Van Woert, and L.M. Schiffer Aromatic amino acids and modification of parkinsonism N. Engl. J. Med. 276 1967 374 379
16. M. Del Zompo, M.P. Piccardi, S. Ruiu, M. Quartu, G.L. Gessa, and A. Vaccari Selective MPP+ uptake into synaptic dopamine vesicles: possible involvement in MPTP neurotoxicity Br. J. Pharmacol. 109 1993 411 414
17. T.M. Engber, R.C. Boldry, S. Kuo, and T.N. Chase Dopaminergic modulation of striatal neuropeptides: differential effects of D1 and D2 receptor stimulation on somatostatin, neuropeptide Y, neurotensin, dynorphin and enkephalin Brain Res. 581 1992 261 268
18. J.D. Erickson, and L.E. Eiden Functional identification and molecular cloning of a human brain vesicular monoamine transporter J. Neurochem. 61 1993 2314 2317
19. J.D. Erickson, L.E. Eiden, and B.J. Hoffman Expression cloning of a reserpine-sensitive vesicular monoamine transporter Proc. Natl. Acad. Sci. U. S. A. 89 1992 10993 10997
20. J.D. Erickson, M.K. Schafer, T.L. Bonner, L.E. Eiden, and E. Weihe Distinct pharmacological properties and distribution in neurons and endocrine cells of two isoforms of the human vesicular monoamine transporter Proc. Natl. Acad. Sci. U.S.A. 93 1996 5166 5171
21. G. Fabbrini, J. Juncos, M.M. Mouradian, C. Serrati, and T.N. Chase Levodopa pharmacokinetic mechanisms and motor fluctuations in Parkinson's disease Ann. Neurol. 21 1987 370 376
22. F. Fumagalli, R.R. Gainetdinov, Y.M. Wang, K.J. Valenzano, G.W. Miller, and M.G. Caron Increased methamphetamine neurotoxicity in heterozygous vesicular monoamine transporter 2 knock-out mice J. Neurosci. 19 1999 2424 2431
23. R.R. Gainetdinov, F. Fumagalli, Y.M. Wang, S.R. Jones, A.I. Levey, G.W. Miller, and M.G. Caron Increased MPTP neurotoxicity in vesicular monoamine transporter 2 heterozygote knockout mice J. Neurochem. 70 1998 1973 1978
24. S.T. Gancher, J.G. Nutt, and W.R. Woodward Time course of tolerance to apomorphine in parkinsonism Clin. Pharmacol. Ther. 52 1992 504 510
25. B. Gasnier, E. Krejci, D. Bottom, J. Massoulie, and J.-P. Henry Expression of a bovine vesicular monoamine transporter in COS cells FEBS Lett. 342 1994 225 229
26. C.R. Gerfen, T.M. Engber, L.C. Mahan, Z. Susel, T.N. Chase, F.J. Monsma Jr., and D.R. Sibley D1 and D2 dopamine receptor-regulated gene expression of striatonigral and striatopallidal neurons Science 250 1990 1429 1432
27. D.C. German, C.L. Liang, K.F. Manaye, K. Lane, and P.K. Sonsalla Pharmacological inactivation of the vesicular monoamine transporter can enhance 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced neurodegeneration of midbrain dopaminergic neurons, but not locus coeruleus noradrenergic neurons Neuroscience 101 2000 1063 1069
28. 3H]flunitrazepam Neuroscience 57 1993 673 681
29. T. Hattori, P.L. McGeer, and E.G. McGeer Dendro axonic neurotransmission. II. Morphological sites for the synthesis, binding and release of neurotransmitters in dopaminergic dendrites in the substantia nigra and cholinergic dendrites in the neostriatum Brain Res. 170 1979 71 83
30. O. Hornykiewicz, and S.J. Kish Biochemical pathophysiology of Parkinson's disease Adv. Neurol. 45 1986 19 34
31. J.L. Juncos, T.M. Engber, R. Raisman, Z. Susel, F. Thibaut, A. Ploska, Y. Agid, and T.N. Chase Continuous and intermittent levodopa differentially affect basal ganglia function Ann. Neurol. 25 1989 473 478
32. U.J. Kang Genetic modification of cells with retrovirus vectors for grafting into the central nervous system M.G. Kaplitt A.D. Loewy Viral Vectors: Gene Therapy and Neuroscience Applications 1995 Academic San Diego 211 237
33. U.J. Kang, L.J. Fisher, T.H. Joh, K.L. O'Malley, and F.H. Gage Regulation of dopamine production by genetically modified primary fibroblasts J. Neurosci. 13 1993 5203 5211
34. D. Kirik, C. Rosenblad, and A. Bjorklund Characterization of behavioral and neurodegenerative changes following partial lesions of the nigrostriatal dopamine system induced by intrastriatal 6-hydroxydopamine in the rat Exp. Neurol. 152 1998 259 277
35. W.Y. Lee, J.W. Chang, N.L. Nemeth, and U.J. Kang Vesicular monoamine transporter-2 and aromatic l-amino acid decarboxylase enhance dopamine delivery after l-3, 4-dihydroxyphenylalanine administration in Parkinsonian rats J. Neurosci. 19 1999 3266 3274
36. E.A. Lee, W.Y. Lee, Y.S. Kim, and U.J. Kang The effects of chronic l-DOPA therapy on pharmacodynamic parameters in a rat model of motor response fluctuations Exp. Neurol. 184 2003 304 312
37. S.E. Leff, K.G. Rendahl, S.K. Spratt, U.J. Kang, and R.J. Mandel In vivo l-DOPA production by genetically modified primary rat fibroblast or 9L gliosarcoma cell grafts via coexpression of GTP cyclohydrolase I with tyrosine hydroxylase Exp. Neurol. 151 1998 249 264
38. M. Levivier, S. Przedborski, C. Bencsics, and U.J. Kang Intrastriatal implantation of fibroblasts genetically engineered to produce brain-derived neurotrophic factor prevents degeneration of dopaminergic neurons in a rat model of Parkinson's disease J. Neurosci. 15 1995 7810 7820
39. Y. Liu, D. Peter, A. Roghani, S. Schuldiner, G.G. Prive, D. Eisenberg, N. Brecha, and R.H. Edwards A cDNA that suppresses MPP+ toxicity encodes a vesicular amine transporter Cell 70 1992 539 551
40. L. Liu, W. Xu, K.A. Harrington, and P.C. Empson The molecular cloning and expression of human synaptic vesicle amine transporter that suppresses MPP+ toxicity Brain Res. Mol. Brain Res. 25 1994 90 96
41. R. Llinás The role of calcium in neuronal function F.O. Schmitt F.G. Worden The Neurosciences: Fourth Study Program 1979 MIT Cambridge, MA 555
42. S.K. Mahata, M. Mahata, R. Fisher-Colbrie, and H. Winkler Vesicle monoamine transporters 1 and 2: differential distribution and regulation of their mRNAs in chromaffin and ganglionic cells of rat adrenal medulla Neurosci. Lett. 156 1993 70 72
43. R.J. Mandel, S.K. Rendahl, S.K. Spratt, L.K. Snyder, L.K. Cohen, and S.E. Leff Characterization of intrastriatal recombinant adeno-associated virus-mediated gene transfer of human tyrosine hydroxylase and human GTP-cyclohydrolase 1 in a rat model of Parkinson's disease J. Neurosci. 18 1998 4271 4284
44. C.D. Marsden Parkinson's disease J. Neurol., Neurosurg. Psychiatry 57 1994 672 681
45. C.D. Marsden, and J.D. Parkes Success and problems of long-term levodopa therapy in Parkinson's disease Lancet 1 1977 345 349
46. G.W. Miller, R.R. Gainetdinov, A.I. Levey, and M.G. Caron Dopamine transporters and neuronal injury Trends Pharmacol. Sci. 20 1999 424 429
47. M.M. Mouradian, I.J. Heuser, F. Baronti, and T.N. Chase Modification of central dopaminergic mechanisms by continuous levodopa therapy for advanced Parkinson's disease Ann. Neurol. 27 1990 18 23
48. M.J. Nirenberg, J. Chan, Y. Liu, R.H. Edwards, and V.M. Pickel Ultrastructural localization of the vesicular monoamine transporter-2 in midbrain dopaminergic neurons: potential sites for somatodendritic storage and release of dopamine J. Neurosci. 16 1996 4135 4145
49. J.G. Nutt Long-term l-DOPA therapy: challenges to our understanding and for the care of people with Parkinson's disease Exp. Neurol. 184 2003 9 13
50. J.G. Nutt, and N.H.G. Holford The response to levodopa in Parkinson's disease: imposing pharmacological law and order Ann. Neurol. 39 1996 561 573
51. J.G. Nutt, W.R. Woodward, J.H. Carter, and S.T. Gancher Effect of long-term therapy on the pharmacodynamics of levodopa Arch. Neurol. 49 1992 1123 1130
52. J.G. Nutt, J.H. Carter, L. Van Houten, and W.R. Woodward Short- and long-duration responses to levodopa during the first year of levodopa therapy Ann. Neurol. 42 1997 349 355
53. J.G. Nutt, J.A. Obeso, and F. Stocchi Continuous dopamine-receptor stimulation in advanced Parkinson's disease Trends Neurosci. 23 2000 S109 S116
54. J.G. Nutt, J.H. Carter, E.S. Lea, and G.J. Sexton Evolution of the response to levodopa during the first 4 years of therapy Ann. Neurol. 51 2002 686 693
55. C.W. Olanow, and J.A. Obeso Preventing levodopa-induced dyskinesias Ann. Neurol. 47 2000 S167 S176
56. S.M. Papa, T.M. Engber, A.M. Kask, and T.N. Chase Motor fluctuations in levodopa treated parkinsonian rats: relation to lesion extent and treatment duration Brain Res. 662 1994 69 74
57. A. Peppe, J.M. Dambrosia, and T.N. Chase Risk factors for motor response complications in l-DOPA-treated parkinsonian patients Adv. Neurol. 60 1993 698 702
58. D. Peter, Y. Liu, C. Sternini, R. de Giorgio, N. Brecha, and R.H. Edwards Differential expression of two vesicular monoamine transporters J. Neurosci. 15 1995 6179 6188
59. A. Peters, S.L. Palay, and H.D. Webster The Fine Structure of the Nervous System 1991 Oxford Up New York
60. R.M. Post Intermittent versus continuous stimulation: effect of time interval on the development of sensitization or tolerance Life Sci. 26 1980 1275 1282
61. B. Rosner Fundamentals of Biostatistics 4th ed. 1995 Duxbury Press Belmont 314 315
62. R. Sanchez-Pernaute, J. Harvey-White, J. Cunningham, and K.S. Bankiewicz Functional effect of adeno-associated virus mediated gene transfer of aromatic l-amino acid decarboxylase into the striatum of 6-OHDA-lesioned rats Mol. Ther. 4 2001 324 330
63. S. Schuldiner A molecular glimpse of vesicular monoamine transporters J. Neurochem. 62 1994 2067 2078
64. I. Shoulson, G.A. Glaubiger, and T.N. Chase On-off response: clinical and biochemical correlations during oral and intravenous levodopa administration in parkinsonian patients Neurology 25 1975 1144 1148
65. Y.H. Sohn, L.V. Metman, D. Bravi, I. Linfante, A. Aotsuka, M.M. Mouradian, and T.N. Chase Levodopa peak response time reflects severity of dopamine neuron loss in Parkinson's disease Neurology 44 1994 755 757
66. S.G. Speciale, C.L. Liang, P.K. Sonsalla, R.H. Edwards, and D.C. German The neurotoxin 1-methyl-4-phenylpyridinium is sequestered within neurons that contain the vesicular monoamine transporter Neuroscience 84 1998 1177 1185
67. R.G. Staal, and P.K. Sonsalla Inhibition of brain vesicular monoamine transporter (VMAT2) enhances 1-methyl-4-phenylpyridinium neurotoxicity in vivo in rat striata J. Pharmacol. Exp. Ther. 293 2000 336 342
68. D. Sulzer, C. St Remy, and S. Rayport Reserpine inhibits amphetamine action in ventral midbrain culture Mol. Pharmacol. 49 1996 338 342
69. M. Sun, L. Kong, X. Wang, C. Holmes, Q. Gao, G.R. Zhang, J. Pfeilschifter, D.S. Goldstein, and A.I. Geller Coexpression of tyrosine hydroxylase, GTP cyclohydrolase, I. Aromatic amino acid decarboxylase, and vesicular monoamine transporter 2 from a helper virus-free herpes simplex virus type 1 vector supports high-level, long-term biochemical and behavioral correction of a rat model of Parkinson's disease Hum. Gene Ther. 15 2004 1177 1196
70. N. Takahashi, L.L. Miner, I. Sora, H. Ujike, R.S. Revay, V. Kostic, V. Jackson-Lewis, S. Przedborski, and G.R. Uhl VMAT2 knockout mice: heterozygotes display reduced amphetamine-conditioned reward, enhanced amphetamine locomotion, and enhanced MPTP toxicity Proc. Natl. Acad. Sci. U. S. A. 94 1997 9938 9943
71. J.M. Trugman, C.A. Hubbard, and J.P. Bennett Dose-related effects of continuous levodopa infusion in rats with unilateral lesions of the substantia nigra Brain Res. 725 1996 177 183
72. G.R. Ulh Hypothesis: the role of dopaminergic transporters in selective vulnerability of cells in Parkinson's disease Ann. Neurol. 43 1998 555 560
73. J. Vaamonde, M.R. Luquin, and J.A. Obeso Levodopa consumption reduces dopaminergic receptor responsiveness in Parkinson's disease Clin. Neuropharmacol. 12 1989 271 284
74. H. von Grafenstein, R. Borges, and D.E. Knight The effect of botulinum toxin type D on the triggered and constitutive exocytosis/endocytosis cycles in cultures of bovine adrenal medullary cells FEBS Lett. 298 1992 118 122
75. S.R. Wachtel, C. Bencsics, and U.J. Kang The role of aromatic l-amino acid decarboxylase for dopamine replacement by genetically modified fibroblasts in a rat model of Parkinson's disease J. Neurochem. 69 1997 2055 2063
76. P. Weingarten, and Q.Y. Zhou Protection of intracellular dopamine cytotoxicity by dopamine disposition and metabolism factor J. Neurochem. 77 2001 776 785
77. M. Zappia, D. Bosco, M. Plastino, G. Nicoletti, D. Branca, R.L. Oliveri, U. Aguglia, A. Gambardella, and A. Quattrone Pharmacodynamics of the long-duration response to levodopa in PD Neurology 53 1999 557 560