Role of α-synuclein in 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced Parkinsonism in mice

Neuroscience

Volumn 118, Issue 4, 2003, Pages 985-1002

  Schluter O M ^a,b,f   Fornai, F ^d   Alessandri M G ^e   Takamori, S ^c   Geppert, M ^b,g   Jahn, R ^c   Sudhof T C ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

^c MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^d UNIVERSITY OF PISA   (Italy)

^e IRCCS Stella Maris   (Italy)

^f STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^g PFIZER INC   (United States)

Author keywords

Dopamine; Methamphetamine; Neurotransmitter release; Synapse; Synaptic vesicle

Indexed keywords

1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; ALPHA SYNUCLEIN; DOPAMINE; METHAMPHETAMINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN STEM; CHEMICAL COMPOSITION; CONTROLLED STUDY; DOPAMINE METABOLISM; FEMALE; GENE DELETION; HOMOLOGOUS RECOMBINATION; KNOCKOUT MOUSE; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PARKINSONISM; PRIORITY JOURNAL;

EID: 0038404962     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(03)00036-8     Document Type: Article

References (95)

1. Abeliovich A., Schmitz Y., Farinas I., Choi-Lundberg D., Ho W.H., Castillo P.E., Shinsky N., Verdugo J.M., Armanini M., Ryan A., Hynes M., Phillips H., Sulzer D., Rosenthal A. Mice lacking alpha-synuclein display functional deficits in the nigrostriatal dopamine system. Neuron. 25:2000;239-252.
2. Akopian A.N., Wood J.N. Peripheral nervous system-specific genes identified by subtractive cDNA cloning. J Biol Chem. 270:1995;21264-21270.
3. Ali S.F., David S.N., Newport G.D. Age-related susceptibility to MPTP-induced neurotoxicity in mice. Neurotoxicology. 14:1993;29-34.
4. Andreassen O.A., Ferrante R.J., Dedeoglu A., Albers D.W., Klivenyi P., Carlson E.J., Epstein C.J., Beal M.F. Mice with a partial deficiency of manganese superoxide dismutase show increased vulnerability to the mitochondrial toxins malonate, 3-nitropropionic acid, and MPTP. Exp Neurol. 167:2001;189-195.
5. Buchman V.L., Hunter H.J., Pinon L.G., Thompson J., Privalova E.M., Ninkina N.N., Davies A.M. Persyn, a member of the synuclein family, has a distinct pattern of expression in the developing nervous system. J Neurosci. 18:1998;9335-9341.
6. Chan P., DeLanney L.E., Irwin I., Langston J.W., Di Monte D. Rapid ATP loss caused by 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine in mouse brain. J Neurochem. 57:1999;348-351.
7. Chou J.H., Jahn R. Binding of Rab3A to synaptic vesicles. J Biol Chem. 275:2000;9433-9440.
8. Clayton D.F., George J.M. The synucleins a family of proteins involved in synaptic function, plasticity, neurodegeneration and disease . Trends Neurosci. 21:1998;249-254.
9. Clayton D.F., George J.M. Synucleins in synaptic plasticity and neurodegenerative disorders. J Neurosci Res. 58:1999;120-129.
10. Conway K.A., Harper J.D., Lansbury P.T. Accelerated in vitro fibril formation by a mutant alpha-synuclein linked to early-onset Parkinson disease. Nat Med. 4:1998;1318-1320.
11. Conway K.A., Lee S.J., Rochet J.C., Ding T.T., Williamson R.E., Lansbury P.T. Jr. Acceleration of oligomerization, not fibrillization, is a shared property of both alpha-synuclein mutations linked to early-onset Parkinson's disease implications for pathogenesis and therapy . Proc. Natl. Acad. Sci. U.S.A. 97:2000;571-576.
12. Crowther R.A., Jakes R., Spillantini M.G., Goedert M. Synthetic filaments assembled from C-terminally truncated alpha-synuclein. FEBS Lett. 436:1998;309-312.
13. Davidson W.S., Jonas A., Clayton D.F., George J.M. Stabilization of α-synuclein secondary structure upon binding to synthetic membranes. J Biol Chem. 273:1998;9443-9449.
14. Desai V.G., Feuers R.J., Hart R.W., Ali S.F. MPP(+)-induced neurotoxicity in mouse is age-dependent enhanced by the selective inhibition of complexes of electron transport . Brain Res. 715:1996;1-8.
15. Dickson D.W. Alpha-synuclein and the Lewy body disorders. Curr Opin Neurol. 14:2001;423-432.
16. Dougherty W.G., Carrington J.C., Cary S.M., Parks T.D. Biochemical and mutational analysis of a plant virus polyprotein cleavage site. EMBO J. 7:1988;1281-1287.
17. Ellis C.E., Schwartzberg P.L., Grider T.L., Fink D.W., Nussbaum R.L. alpha-synuclein is phosphorylated by members of the Src family of protein-tyrosine kinases. J Biol Chem. 276:2001;3879-3884.
18. Edelmann L., Hanson P.I., Chapman E., Jahn R. Synaptobrevin binding to synaptophysin a potential mechanism for controlling the exocytotic fusion machine . EMBO J. 14:1995;224-231.
19. Feany M.B., Bender W.W. A Drosophila model of Parkinson's disease. Nature. 404:2000;394-398.
20. Fornai F., Alessandrì M.G., Torracca M.T., Bassi L., Corsini G.U. Effects of noradrenergic lesions on MPTP/MPP+ kinetics and MPTP-induced nigrostriatal dopamine depletions. J Pharmacol Exp Ther. 283:1997;100-107.
21. Fornai F., Giorgi F.S., Alessandrì M.G., Giusiani M., Corsini G.U. Effects of pretreatment with DSP-4 on methamphetamine-induced striatal dopamine losses and pharmacokinetics. J Neurochem. 72:1999;777-784.
22. Fornai F., Chen K., Giorgi F.S., Gesi M., Alessandrì M.G., Shih J.C. Striatal dopamine metabolism in monoamine oxidase B deficient mice a brain dialysis study . J Neurochem. 73:1999;2434-2440.
23. Forno L.S. Neuropathology of Parkinson's disease. J Neuropathol Exp Neurol. 55:1996;259-272.
24. Gai W.P., Power J.H., Blumbergs P.C., Blessing W.W. Multiple-system atrophy a new alpha-synuclein disease? Lancet. 352:1998;547-548.
25. George J.M., Jin H., Woods W.S., Clayton D.F. Characterization of a novel protein regulated during the critical period for song learning in the zebra finch. Neuron. 15:1995;361-372.
26. Giovanni A., Sieber B.-A., Heikkila R.E., Sonsalla P.K. Studies on species-sensitivity to the dopaminergic neurotoxin 1-methy-4-phenyl-1,2,3,6-tetrahydropyridine. I Systemic administration . J Pharmacol Exp Ther. 270:1994;1000-1007.
27. Giovanni A., Sonsalla P.K., Heikkila R.E. Studies on species-sensitivity to the dopaminergic neurotoxin 1-methy-4-phenyl-1,2,3,6-tetrahydropyridine. II Central administration of 1-methyl-4-phenylpyridinium . J Pharmacol Exp Ther. 270:1994;1008-1014.
28. Goedert M. Alpha-synuclein and neurodegenerative diseases. Nat Rev Neurosci. 2:2001;492-501.
29. Guan K.L., Dixon J.E. Eukaryotic proteins expressed in Escherichia coli an improved thrombin cleavage and purification procedure of fusion proteins with glutathione S-transferase . Anal Biochem. 192:1991;262-267.
30. Hashimoto M., Hsu L.J., Sisk A., Xia Y., Takeda A., Sundsmo M., Masliah E. Human recombinant NACP/alpha-synuclein is aggregated and fibrillated in vitro relevance for Lewy body disease . Brain Res. 799:1998;301-306.
31. Heikkila R.E., Hess A., Duvoisin R.C. Dopaminergic neurotoxicity of 1-methyl-4-phenyl-1,2,5,6-tetrahydropyridine in mice. Science. 224:1984;1451-1453.
32. Heikkila R.E., Manzino L., Cabbat F.S., Duvoisin R.C. Protection against the dopaminergic toxicity of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine by monoamine oxidase inhibitors. Nature. 311:1984;467-469.
33. Heintz N., Zoghbi H.Y. Insights from mouse models into the molecular basis of neurodegeneration. Annu Rev Physiol. 62:2000;779-802.
34. Hell J.W., Maycox P.R., Stadler H., Jahn R. Uptake of GABA by rat brain synaptic vesicles isolated by a new procedure. EMBO J. 7:1988;3023-3029.
35. Hogan K.A., Staal R.G.W., Sonsalla P.K. Analysis of VMAT2 binding after methamphetamine or MPTP treatment disparity between homogenates and vesicle preparations . J Neurochem. 74:2000;2217-2220.
36. Hooper M., Hardy K., Handyside A., Hunter S., Monk M. HPRT-deficient (Lesch-Nyhan) mouse embryos derived from germline colonization by cultured cells. Nature. 326:1987;292-295.
37. Huttner W.B., Schiebler W., Greengard P., De Camilli P. Synapsin I (protein I), a nerve terminal-specific phosphoprotein III . Its association with synaptic vesicles studied in a highly purified synaptic vesicle preparation. J Cell Biol. 96:1983;1374-1388.
38. Irizarry M.C., Growdon W., Gomez-Isla T., Newell K., George J.M., Clayton D.F., Hyman B.T. Nigral and cortical Lewy bodies and dystrophic nigral neurites in Parkinson's disease and cortical Lewy body disease contain alpha-synuclein immunoreactivity. J Neuropathol Exp Neurol. 57:1998;334-337.
39. Jahn R., Schiebler W., Ouimet C., Greengard P.A. 38,000-dalton membrane protein (p38) present in synaptic vesicles. Proc Natl Acad Sci USA. 82:1985;4137-4141.
40. Javitch J.A., D'Amato R.J., Strittmatter S.M., Snyder S.H. Parkinsonism-inducing neurotoxin N-methyl-4-phenyl-1,2,3,6-tetrahydropyridine uptake of the metabolite N-methyl-4-phenylpyridinium by dopamine neurons explains selective toxicity . Proc Natl Acad Sci USA. 82:1985;2173-2177.
41. Jensen P.H., Nielsen M.S., Jakes R., Dotti C.G., Goedert M. Binding of alpha-synuclein to brain vesicles is abolished by familial Parkinson's disease mutation. J Biol Chem. 273:1998;26292-26294.
42. Ji H., Liu Y.E., Jia T., Wang M., Liu J., Xiao G., Joseph B.K., Rosen C., Shi Y.E. Identification of a breast cancer-specific gene, BCSG1, by direct differential cDNA sequencing. Cancer Res. 57:1997;759-764.
43. Kahle P.J., Neumann M., Ozmen L., Haass C. Physiology and pathophysiology of alpha-synuclein cell culture and transgenic animal models based on a Parkinson's disease-associated protein . Ann NY Acad Sci. 920:2000;33-41.
44. Kahle P.J., Neumann M., Ozmen L., Muller V., Jacobsen H., Schindzielorz A., Okochi M., Leimer U., van Der Putten H., Probst A., Kremmer E., Kretzschmar H.A., Haass C. Subcellular localization of wild-type and Parkinson's disease-associated mutant alpha-synuclein in human and transgenic mouse brain. J Neurosci. 20:2000;6365-6373.
45. Kitada T., Asakawa S., Hattori N., Matsumine H., Yamamura Y., Minoshima S., Yokochi M., Mizuno Y., Shimizu N. Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature. 392:1998;605-608.
46. Klivenyi P., St Clair D., Wermer M., Yen H.C., Oberley T., Yang L., Flint Beal M. Manganese superoxide dismutase overexpression attenuates MPTP toxicity. Neurobiol Dis. 5:1998;253-258.
47. Krüger R., Kuhn W., Muller T., Woitalla D., Graeber M., Kosel S., Przuntek H., Epplen J.T., Schols L., Riess O. Ala30Pro mutation in the gene encoding alpha-synuclein in Parkinson's disease. Nat Genet. 18:1998;106-108.
48. Lang A.E., Lozano A.M. Parkinson's disease. N Engl J Med. 339:1998;1130-1143.
49. Langston J.W., Ballard P., Tetrud J.W., Irwin I. Chronic parkinsonism in humans due to a product of meperidine-analog synthesis. Science. 219:1983;979-980.
50. Leng Y., Chase T.N., Bennett M.C. Muscarinic receptor stimulation induces translocation of an alpha-synuclein oligomer from plasma membrane to a light vesicle fraction in cytoplasm. J Biol Chem. 276:2001;28212-28218.
51. Leroy E., Boyer R., Auburger G., Leube B., Ulm G., Mezey E., Harta G., Brownstein M.J., Jonnalagada S., Chernova T., Dehejia A., Lavedan C., Gasser T., Steinbach P.J., Wilkinson K.D., Polymeropoulos M.H. The ubiquitin pathway in Parkinson's disease. Nature. 395:1998;451-452.
52. Lotharius J., O'Malley K.L. The parkinsonism-inducing drug 1-methyl-4-phenylpyridinium triggers intracellular dopamine oxidation a novel mechanism of toxicity . J Biol Chem. 275:2000;38581-38588.
53. Lotharius J., Dugan L.L., O'Malley K.L. Distinct mechanisms underlie neurotoxin-mediated cell death in cultured dopaminergic neurons. J Neurosci. 19:1999;1284-1293.
54. Lowe J., Lennox G., Leigh P.N. Disorders of movement and system degenerations. Graham D.I., Lantos P. Greenfield's neuropathology, Vol, 2. 1997;281-366 Arnold, London.
55. Lowry O.H., Rosebrough N.J., Farr A.L., Randall R.J. Protein measurement with the Folin phenol reagent. J Biol Chem. 193:1951;265-275.
56. Maroteaux L., Campanelli J.T., Scheller R.H. Synuclein a neuron-specific protein localized to the nucleus and presynaptic nerve terminal . J Neurosci. 8:1988;2804-2815.
57. Masliah E., Rockenstein E., Veinbergs I., Mallory M., Hashimoto M., Takeda A., Sagara Y., Sisk A., Mucke L. Dopaminergic loss and inclusion body formation in alpha-synuclein mice implications for neurodegenerative disorders . Science. 287:2000;1265-1269.
58. Miller G.W., Gainetdinov R.R., Levey A.I., Caron M.G. Dopamine transporters and neuronal injury. Trends Pharmacol Sci. 20:1999;424-429.
59. Murphy D.D., Rueter S.M., Trojanowski J.Q., Lee V.M. Synucleins are developmentally expressed, and alpha-synuclein regulates the size of the presynaptic vesicular pool in primary hippocampal neurons. J Neurosci. 20:2000;3214-3220.
60. Nicklas W.J., Vyas I., Heikkila R.E. Inhibition of NADH-linked oxidation in brain mitochondria by 1-methyl-4-phenyl-pyridine, a metabolite of the neurotoxin, 1-methyl-4-phenyl-1,2,5,6-tetrahydropyridine. Life Sci. 36:1985;2503-2508.
61. O'Dell S.J., Weihmuller F.B., Marshall J.F. Methamphethamine-induced dopamine overflow and injury to striatal dopamine terminals attenuation by dopamine D1and D2 antagonists . J Neurochem. 60:1993;1792-1799.
62. Polymeropoulos M.H., Lavedan C., Leroy E., Ide S.E., Dehejia A., Dutra A., Pike B., Root H., Rubenstein J., Boyer R., Stenroos E.S., Chandrasekharappa S., Athanassiadou A., Papapetropoulos T., Johnson W.G., Lazzarini A.M., Duvoisin R.C., Di Iorio G., Golbe L.I., Nussbaum R.L. Mutation in the alphasynuclein gene identified in families with Parkinson's disease. Science. 276:1997;2045-2047.
63. Przedborski S., Kostic V., Jackson-Lewis V., Naini A.B., Simonetti S., Fahn S., Carlson E., Epstein C.J., Cadet J.L. Transgenic mice with increased Cu/Zn-superoxide dismutase activity are resistant to N-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced neurotoxicity. J Neurosci. 12:1992;1658-1667.
64. Przedborski S., Jackson-Lewis V. Mechanisms of MPTP toxicity. Mov Disord. 13:(suppl 1):1998;35-38.
65. Ramsay R.R., Singer T.P. Energy-dependent uptake of N-methyl-4-phenylpyridinium, the neurotoxic metabolite of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine, by mitochondria. J Biol Chem. 261:1986;7585-7587.
66. Ramsay R.R., Krueger M.J., Youngster S.K., Gluck M.R., Casida J.E., Singer T.P. Interaction of 1-methyl-4-phenylpyridinium ion (MPP+) and its analogs with the rotenone/piericidin binding site of NADH dehydrogenase. J Neurochem. 56:1991;1184-1190.
67. Rathke-Hartlieb S., Kahle P.J., Neumann M., Ozmen L., Haid S., Okochi M., Haass C., Schulz J.B. Sensitivity to MPTP is not increased in Parkinson's disease-associated mutant alpha-synuclein transgenic mice. J Neurochem. 77:2001;1181-1184.
68. Richfield E.K., Thiruchelvam M.J., Cory-Slechta D.A., Wuertzer C., Gainetdinov R.R., Caron M.G., Di Monte D.A., Federoff H.J. Behavioral and neurochemical effects of wild-type and mutated human alpha-synuclein in transgenic mice. Exp Neurol. 175:2002;35-48.
69. Rosahl T.W., Spillane D., Missler M., Herz J., Selig D.K., Wolff J.R., Hammer R.E., Malenka R.C., Südhof T.C. Essential functions of synapsins I and II in synaptic vesicle regulation. Nature. 375:1995;488-493.
70. Sambrook J., Fritsch E.F., Maniatis T. Molecular cloning: a laboratory manual. 1989;Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
71. Schlüter O.M., Schnell E., Verhage M., Tzonopoulos T., Nicoll R.A., Janz R., Malenka R.C., Geppert M., Südhof T.C. Rabphilin knock-out mice reveal that rabphilin is not required for rab3 function in regulating neurotransmitter release. J Neurosci. 19:1999;5834-5846.
72. Seiden L.S., Ricaurte G.A. Neurotoxicity of methamphetamine and related drugs. Melzer H.Y. Psychopharmacology the third generation of progress . 1987;359-366 Raven Press, New York.
73. Sirinathsinghji D.J., Heavens R.P., McBride C.S. Dopamine-releasing action of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) and 1-methyl-4-phenylpyridine (MPP+) in the neostriatum of the rat as demonstrated in vivo by the push-pull perfusion technique dependence on sodium but not calcium ions . Brain Res. 443:1988;101-116.
74. Song J.-Y., Ichtchenko K., Südhof T.C., Brose N. Neuroligin 1 is a postsynaptic cell-adhesion molecule of excitaory synapses. Proc Natl Acad Sci USA. 96:1999;1100-1125.
75. Sonsalla P.K., Nicklas W.J., Heikkila R.E. Role for excitatory amino acids in methamphetamine-induced nigrostriatal dopaminergic toxicity. Science. 243:1989;398-400.
76. Sonsalla P.K., Giovanni A., Sieber B.A., Delle Donne K., Manzino L. Characteristics of dopaminergic neurotoxicity produced by MPTP and methamphetamine. Ann NY Acad Sci. 648:1992;229-238.
77. Soriano P., Montgomery C., Geske R., Bradley A. Targeted disruption of the c-src proto-oncogene leads to osteopetrosis in mice. Cell. 64:1991;693-702.
78. Specht C.G., Schoepfer R. Deletion of the alpha-synuclein locus in a subpopulation of C57BL/6J inbred mice. BMC Neurosci. 2:2001;11.
79. Spillantini M.G., Crowther R.A., Jakes R., Hasegawa M., Goedert M. α-Synuclein in filamentous inclusions of Lewy bodies from Parkinson's disease and dementia with Lewy bodies. Proc Natl Acad Sci USA. 95:1998;6469-6473.
80. Spillantini M.G., Schmidt M.L., Lee V.M., Trojanowski J.Q., Jakes R., Goedert M. α-synuclein in Lewy bodies. Nature. 388:1997;839-840.
81. Südhof T.C. The structure of the human synapsin I gene and protein. J Biol Chem. 265:1990;7849-7852.
82. Sulzer D., Rayport S. Amphetamine and other psychostimulants reduce pH gradients in midbrain dopaminergic neurons and chromaffin granules a mechanism of action . Neuron. 5:1990;797-808.
83. Surguchov A., Surgucheva I., Solessio E., Baehr W. Synoretin-A new protein belonging to the synuclein family. Mol Cell Neurosci. 13:1999;95-103.
84. Teng L., Crooks P.A., Sonsalla P.K., Dwoskin L.P. Lobeline and nicotine evoke [3H] overflow from rat striatal slices preloaded with [3H]dopamine differential inhibition of synaptosomal and vesicular [3H]dopamine uptake . J Pharmacol Exp Ther. 280:1997;1432-1444.
85. Thomas K.R., Capecchi M.R. Site-directed mutagenesis by gene targeting in mouse embryo-derived stem cells. Cell. 51:1987;503-512.
86. Tobaben S., Thakur P., Fernandez-Chacon R., Sudhof T.C., Rettig J., Stahl B. A trimeric protein complex functions as a synaptic chaperone machine. Neuron. 31:2001;987-999.
87. Tobe T., Nakajo S., Tanaka A., Mitoya A., Omata K., Nakaya K., Tomita M., Nakamura Y. Cloning and characterization of the cDNA encoding a novel brain-specific 14-kDa protein. J Neurochem. 59:1992;1624-1629.
88. Ueda K., Fukushima H., Masliah E., Xia Y., Iwai A., Yoshimoto M., Otero D.A., Kondo J., Ihara Y., Saitoh T. Molecular cloning of cDNA encoding an unrecognized component of amyloid in Alzheimer disease. Proc Natl Acad Sci USA. 90:1993;11282-11286.
89. Vila M., Vukosavic S., Jackson-Lewis V., Neystat M., Jakowec M., Przedborski S. α-synuclein up-regulation in substantia nigra dopaminergic neurons following administration of the parkinsonian toxin MPTP. J Neurochem. 74:2000;721-729.
90. Weinreb P.H., Zhen W., Poon A.W., Conway K.A., Lansbury P.T. Jr. NACP, a protein implicated in Alzheimer's disease and learning, is natively unfolded. Biochemistry. 35:1996;13709-13715.
91. Withers G.S., George J.M., Banker G.A., Clayton D.F. Delayed localization of synelfin (synuclein, NACP) to presynaptic terminals in cultured rat hippocampal neurons. Brain Res Dev Brain Res. 99:1997;87-94.
92. Yamamoto A., Lucas J.J., Hen R. Reversal of neuropathology and motor dysfunction in a conditional model of Huntington's disease. Cell. 101:2000;57-66.
93. Zhang Y., Dawson V.L., Dawson T.M. Oxidative stress and genetics in the pathogenesis of Parkinson's disease. Neurobiol Dis. 7:2000;240-250.
94. Zhang J., Graham D.G., Montine T.J., Ho Y.S. Enhanced N-methyl-4-phenyl,2,3,6-tetrahydropyridine toxicity in mice deficient in CuZn-superoxide dismutase or glutathione peroxidase. J Neuropathol Exp Neurol. 59:2000;53-61.
95. Zigmond M.J., Stricker E.M. Animal models of parkinsonism using selective neurotoxins clinical and basic implications . Int Rev Neurobiol. 31:1989;1-79.