Age-related decline in striatal dopamine content and motor performance occurs in the absence of nigral cell loss in a genetic mouse model of Parkinson's disease

European Journal of Neuroscience

Volumn 24, Issue 9, 2006, Pages 2622-2630

  Colebrooke, Rebecca E ^a   Humby, Trevor ^a,b   Lynch, Patrick J ^a   McGowan, Daniel P ^a   Xia, Jing ^a   Emson, Piers C ^a  

^a BABRAHAM INSTITUTE   (United Kingdom)

^b CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

Dopamine; L DOPA; Locomotor activity; VMAT2

Indexed keywords

CATECHOL; DOPAMINE; MONOAMINE; TYROSINE 3 MONOOXYGENASE;

AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; BRAIN METABOLISM; CONTROLLED STUDY; CORPUS STRIATUM; CYTOSOL; DOPAMINERGIC NERVE CELL; IMMUNOCOMPETENT CELL; LOCOMOTION; MALE; MOTOR COORDINATION; MOTOR DYSFUNCTION; MOTOR PERFORMANCE; MOUSE; MOUSE STRAIN; NERVE CELL DEGENERATION; NEUROCHEMISTRY; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; QUANTITATIVE ANALYSIS; ROTAROD TEST; SENESCENCE; SUBSTANTIA NIGRA;

AGING; ANIMALS; ANTIPARKINSON AGENTS; BLOTTING, WESTERN; CORPUS STRIATUM; DISEASE MODELS, ANIMAL; DOPAMINE; IMMUNOHISTOCHEMISTRY; LEVODOPA; MALE; MICE; MICE, MUTANT STRAINS; MOTOR ACTIVITY; MOTOR SKILLS; NERVE DEGENERATION; PARKINSON DISEASE; PHOSPHORYLATION; SUBSTANTIA NIGRA; TYROSINE 3-MONOOXYGENASE; VESICULAR MONOAMINE TRANSPORT PROTEINS;

EID: 33750911761     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2006.05143.x     Document Type: Article

References (55)

1. Anden, N.E.H., Fuxe, K., Hamberger, B. & Hokfelt, T. (1966) A quantitative study on the nigro-neostriatal dopamine neuron system in the rat. Acta Physiol. Scand., 67, 306-312.
2. Bernheimer, H., Birkmayer, W., Hornykiewicz, O., Jellinger, K. & Seitelberger, F. (1973) Brain dopamine and the syndromes of Parkinson and Huntington. Clinical, morphological and neurochemical correlations. J. Neurol. Sci., 20, 415-455.
3. Cappai, R., Leck, S.L., Tew, D.J., Williamson, N.A., Smith, D.P., Galatis, D., Sharples, R.A., Curtain, C.C., Ali, F.E., Cherny, R.A., Culvenor, J.G., Bottomley, S.P., Masters, C.L., Barnham, K.J. & Hill, A.F. (2005) Dopamine promotes alpha-synuclein aggregation into SDS-resistant soluble oligomers via a distinct folding pathway. Faseb J., 19, 1377-1379.
4. Carter, R.J., Lione, L.A., Humby, T., Mangiarini, L., Mahal, A., Bates, G.P., Dunnett, S.B. & Morton, A.J. (1999) Characterization of progressive motor deficits in mice transgenic for the human Huntington's disease mutation. J. Neurosci., 19, 3248-3257.
5. Chen, L., Cagniard, B., Mathews, T., Jones, S., Koh, H.C., Ding, Y., Carvey, P.M., Ling, Z., Kang, U.J. & Zhuang, X. (2005) Age-dependent motor deficits and dopaminergic dysfunction in DJ-1 null mice. J. Biol. Chem., 280, 21418-21426.
6. Cohen, G. (1984) Oxy-radical toxicity in catecholamine neurons. Neurotoxicology, 5, 77-82.
7. Conway, K.A., Rochet, J.C., Bieganski, R.M. & Lansbury, P.T. Jr (2001) Kinetic stabilization of the alpha-synuclein protofibril by a dopamine-alpha-synuclein adduct. Science, 294, 1346-1349.
8. Couzin, J. (2001) Parkinson's disease. Dopamine may sustain toxic protein. Science, 294, 1257-1258.
9. Dauer, W. & Przedborski, S. (2003) Parkinson's disease: mechanisms and models. Neuron, 39, 889-909.
10. Dawson, T., Mandir, A. & Lee, M. (2002) Animal models of PD: pieces of the same puzzle? Neuron, 35, 219-222.
11. Dunkley, P.R., Bobrovskaya, L., Graham, M.E., von Nagy-Felsobuki, E.I. & Dickson, P.W. (2004) Tyrosine hydroxylase phosphorylation: regulation and consequences. J. Neurochem., 91, 1025-1043.
12. Ehringer, H. & Hornykiewicz, O. (1960) [Distribution of noradrenaline and dopamine (3-hydroxytyramine) in the human brain and their behavior in diseases of the extrapyramidal system.] . Klin. Wochenschr., 38, 1236-1239.
13. Fahn, S. (2003) Description of Parkinson's disease as a clinical syndrome. Ann. NY Acad. Sci., 991, 1-14.
14. Filloux, F. & Townsend, J.J. (1993) Pre- and postsynaptic neurotoxic effects of dopamine demonstrated by intrastriatal injection. Exp. Neurol., 119, 79-88.
15. Fleming, S.M., Fernagut, P.O. & Chesselet, M.F. (2005) Genetic mouse models of parkinsonism: strengths and limitations. J. Amer. Soc. Exp. NeuroTherapeutics, 2, 495-503.
16. Fon, E.A., Pothos, E.N., Sun, B.C., Killeen, N., Sulzer, D. & Edwards, R.H. (1997) Vesicular transport regulates monoamine storage and release but is not essential for amphetamine action. Neuron, 19, 1271-1283.
17. Gerfen, C.R. (2003) D1 dopamine receptor supersensitivity in the dopamine-depleted striatum animal model of Parkinson's disease. Neuroscientist, 9, 455-462.
18. Gozlan, H., Daval, G., Verge, D., Spampinato, U., Fattaccini, C.M., Gallissot, M.C., el Mestikawy, S. & Hamon, M. (1990) Aging associated changes in serotoninergic and dopaminergic pre- and postsynaptic neurochemical markers in the rat brain. Neurobiol. Aging, 11, 437-449.
19. Guevara-Guzman, R., Emson, P.C. & Kendrick, K.M. (1994) Modulation of in vivo striatal transmitter release by nitric oxide and cyclic GMP. J. Neurochem., 62, 807-810.
20. Hastings, T.G., Lewis, D.A. & Zigmond, M.J. (1996) Role of oxidation in the neurotoxic effects of intrastriatal dopamine injections. Proc. Natl Acad. Sci. USA, 93, 1956-1961.
21. Herkenham, M., Little, M.D., Bankiewicz, K., Yang, S.C., Markey, S.P. & Johannessen, J.N. (1991) Selective retention of MPP+ within the monoaminergic systems of the primate brain following MPTP administration: an in vivo autoradiographic study. Neuroscience, 40, 133-158.
22. Hornykiewicz, O. (1998) Biochemical aspects of Parkinson's disease. Neurology, 51, S2-S9.
23. Humby, T., Laird, F.M., Davies, W. & Wilkinson, L.S. (1999) Visuospatial attentional functioning in mice: interactions between cholinergic manipulations and genotype. Eur. J. Neurosci., 11, 2813-2823.
24. Iancu, R., Mohapel, P., Brundin, P. & Paul, G. (2005) Behavioral characterization of a unilateral 6-OHDA-lesion model of Parkinson's disease in mice. Behav. Brain Res., 162, 1-10.
25. Irwin, I., DeLanney, L.E., McNeill, T., Chan, P., Forno, L.S., Murphy, G.M. Jr, Di Monte, D.A., Sandy, M.S. & Langston, J.W. (1994) Aging and the nigrostriatal dopamine system: a non-human primate study. Neurodegeneration, 3, 251-265.
26. Jenner, P. & Olanow, C.W. (1996) Oxidative stress and the pathogenesis of Parkinson's disease. Neurology, 47, S161-S170.
27. Kahle, P.J., Neumann, M., Ozmen, L. & Haass, C. (2000) Physiology and pathophysiology of alpha-synuclein. Cell culture and transgenic animal models based on a Parkinson's disease-associated protein. Ann. NY Acad. Sci., 920, 33-41.
28. Kim, D.S., Palmiter, R.D., Cummins, A. & Gerfen, C.R. (2006) Reversal of supersensitive striatal dopamine D (1) receptor signaling and extracellular signal-regulated kinase activity in dopamine-deficient mice. Neuroscience, 137, 1381-1388.
29. Lotharius, J., Barg, S., Wiekop, P., Lundberg, C., Raymon, H.K. & Brundin, P. (2002) Effect of mutant alpha-synuclein on dopamine homeostasis in a new human mesencephalic cell line. J. Biol. Chem., 277, 38884-38894.
30. Lotharius, J. & Brundin, P. (2002) Impaired dopamine storage resulting from alpha-synuclein mutations may contribute to the pathogenesis of Parkinson's disease. Hum. Mol. Genet., 11, 2395-2407.
31. Luesse, H.G., Schiefer, J., Spruenken, A., Puls, C., Block, F. & Kosinski, C.M. (2001) Evaluation of R6/2 HD transgenic mice for therapeutic studies in Huntington's disease: behavioral testing and impact of diabetes mellitus. Behav. Brain Res., 126, 185-195.
32. Marek, K., Jennings, D. & Seibyl, J. (2002) Do dopamine agonists or levodopa modify Parkinson's disease progression? Eur. J. Neurol., 9 (Suppl. 3), 15-22.
33. Meissner, W., Prunier, C., Guilloteau, D., Chalon, S., Gross, C.E. & Bezard, E. (2003) Time-course of nigrostriatal degeneration in a progressive MPTP-lesioned macaque model of Parkinson's disease. Mol. Neurobiol., 28, 209-218.
34. Michel, P.P. & Hefti, F. (1990) Toxicity of 6-hydroxydopamine and dopamine for dopaminergic neurons in culture. J. Neurosci. Res., 26, 428-435.
35. Miguez, J.M., Aldegunde, M., Paz-Valinas, L., Recio, J. & Sanchez-Barcelo, E. (1999) Selective changes in the contents of noradrenaline, dopamine and serotonin in rat brain areas during aging. J. Neural Transm., 106, 1089-1098.
36. Mooslehner, K.A., Chan, P.M., Xu, W., Liu, L., Smadja, C., Humby, T., Allen, N.D., Wilkinson, L.S. & Emson, P.C. (2001) Mice with very low expression of the vesicular monoamine transporter 2 gene survive into adulthood: potential mouse model for parkinsonism. Mol. Cell Biol., 21, 5321-5331.
37. Moretti, A., Carfagna, N. & Trunzo, F. (1987) Effect of aging on monoamines and their metabolites in the rat brain. Neurochem. Res., 12, 1035-1039.
38. Narabayashi, H. (1995) The neural mechanisms and progressive nature of symptoms of Parkinson's disease - based on clinical, neurophysiological and morphological studies. J. Neural Transm. Park. Dis. Dement. Sect., 10, 63-75.
39. Nelson, E.L., Liang, C.L., Sinton, C.M. & German, D.C. (1996) Midbrain dopaminergic neurons in the mouse: computer-assisted mapping. J. Comp. Neurol., 369, 361-371.
40. Orth, M. & Tabrizi, S.J. (2003) Models of Parkinson's disease. Mov. Disord., 18, 729-737.
41. Reeves, S., Bench, C. & Howard, R. (2002) Ageing and the nigrostriatal dopaminergic system. Int. J. Geriatr. Psychiatry, 17, 359-370.
42. Sedelis, M., Hofele, K., Auburger, G.W., Morgan, S., Huston, J.P. & Schwarting, R.K. (2000) MPTP susceptibility in the mouse: behavioral, neurochemical, and histological analysis of gender and strain differences. Behav. Genet., 30, 171-182.
43. Slow, E.J., van Raamsdonk, J., Rogers, D., Coleman, S.H., Graham, R.K., Deng, Y., Oh, R., Bissada, N., Hossain, S.M., Yang, Y.Z., Li, X.J., Simpson, E.M., Gutekunst, C.A., Leavitt, B.R. & Hayden, M.R. (2003) Selective striatal neuronal loss in a YAC128 mouse model of Huntington disease. Hum. Mol. Genet., 12, 1555-1567.
44. Sofic, E., Riederer, P., Heinsen, H., Beckmann, H., Reynolds, G.P., Hebenstreit, G. & Youdim, M.B. (1988) Increased iron (III) and total iron content in post mortem substantia nigra of parkinsonian brain. J. Neural Transm., 74, 199-205.
45. Specht, C.G. & Schoepfer, R. (2001) Deletion of the alpha-synuclein locus in a subpopulation of C57BL/6J inbred mice. BMC Neurosci., 2, 11.
46. Spina, M.B. & Cohen, G. (1989) Dopamine turnover and glutathione oxidation: implications for Parkinson disease. Proc. Natl Acad. Sci. USA, 86, 1398-1400.
47. Stefanis, L., Larsen, K.E., Rideout, H.J., Sulzer, D. & Greene, L.A. (2001) Expression of A53T mutant but not wild-type alpha-synuclein in PC12 cells induces alterations of the ubiquitin-dependent degradation system, loss of dopamine release, and autophagic cell death. J. Neurosci., 21, 9549-9560.
48. Szczypka, M.S., Kwok, K., Brot, M.D., Marck, B.T., Matsumoto, A.M., Donahue, B.A. & Palmiter, R.D. (2001) Dopamine production in the caudate putamen restores feeding in dopamine-deficient mice. Neuron, 30, 819-828.
49. Takahashi, N., Miner, L.L., Sora, I., Ujike, H., Revay, R.S., Kostic, V., Jackson-Lewis, V., Przedborski, S. & Uhl, G.R. (1997) VMAT2 knockout mice: heterozygotes display reduced amphetamine-conditioned reward, enhanced amphetamine locomotion, and enhanced MPTP toxicity. Proc. Natl Acad. Sci. USA, 94, 9938-9943.
50. Ungerstedt, U. (1968) 6-Hydroxy-dopamine induced degeneration of central monoamine neurons. Eur. J. Pharmacol., 5, 107-110.
51. Ungerstedt, U. (1971) Postsynaptic supersensitivity after 6-hydroxy-dopamine induced degeneration of the nigro-striatal dopamine system. Acta Physiol. Scand. Suppl., 367, 69-93.
52. Wang, Y.M., Gainetdinov, R.R., Fumagalli, F., Xu, F., Jones, S.R., Bock, C.B., Miller, G.W., Wightman, R.M. & Caron, M.G. (1997) Knockout of the vesicular monoamine transporter 2 gene results in neonatal death and supersensitivity to cocaine and amphetamine. Neuron, 19, 1285-1296.
53. Wu, D.C., Teismann, P., Tieu, K., Vila, M., Jackson-Lewis, V., Ischiropoulos, H. & Przedborski, S. (2003) NADPH oxidase mediates oxidative stress in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine model of Parkinson's disease. Proc. Natl Acad. Sci. USA, 100, 6145-6150.
54. Xu, J., Kao, S.Y., Lee, F.J., Song, W., Jin, L.W. & Yankner, B.A. (2002) Dopamine-dependent neurotoxicity of alpha-synuclein: a mechanism for selective neurodegeneration in Parkinson disease. Nat. Med., 8, 600-606.
55. Ye, F.Q., Allen, P.S. & Martin, W.R. (1996) Basal ganglia iron content in Parkinson's disease measured with magnetic resonance. Mov. Disord., 11, 243-249.