A critical review of the development and importance of proteinaceous aggregates in animal models of Parkinson's disease: New insights into Lewy body formation

Parkinsonism and Related Disorders

Volumn 10, Issue 4, 2004, Pages 191-202

  Meredith, Gloria E ^a   Halliday, Glenda M ^b   Totterdell, Susan ^c  

^a ROSALIND FRANKLIN UNIVERSITY OF MEDICINE AND SCIENCE   (United States)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Synuclein; 1 Methyl 4 phenyl 1,2,3,6 tetrahydropyridine; Inclusion bodies; Lewy bodies; Lipofuscins; Paraquat; PARK1; PARK2; Rotenone; Ubiquitin; Viral vectors

Indexed keywords

1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; ALPHA SYNUCLEIN; FUNGICIDE; HERBICIDE; MANEB; PARAQUAT; PROBENECID; ROTENONE; XENOBIOTIC AGENT;

CELL INCLUSION; GENE EXPRESSION; HUMAN; IMMUNOPATHOLOGY; LEWY BODY; METABOLISM; NONHUMAN; OXIDATIVE STRESS; PARKINSON DISEASE; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN AGGREGATION; REVIEW; TRANSGENIC ANIMAL;

ANIMALS; DISEASE MODELS, ANIMAL; HUMANS; INCLUSION BODIES; LEWY BODIES; PARKINSON DISEASE; PROTEINS;

EID: 2042476718     PISSN: 13538020     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.parkreldis.2004.01.001     Document Type: Review

References (86)

1. Ancolio K., Alves da Costa C., Ueda K., Checler F. α-synuclein and the Parkinson's disease-related mutant Ala53Thr-α-synuclein do not undergo proteasomal degradation in HEK293 and neuronal cells. Neurosci Lett. 285:2000;79-82
2. Arima K., Ueda K., Sunohara N., Hirai S., Izumiyama S., Tonozuka-Uehara H., Kawai M. Immunoelectron microscopic demonstration of NACP/alpha-synuclein epitopes on the filamentous component of Lewy bodies in Parkinson's disease and in dementia with Lewy bodies. Brain Res. 808:1998;93-100
3. Beal M.F. Experimental models of Parkinson's disease. Nat Rev Neurosci. 2:2001;325-332
4. Bence N.F., Sampat R.M., Kopito R.R. Impairment of the ubiquitin proteasome system by protein aggregation. Science. 292:2001;1552-1555
5. Bennett M.C., Bishop J.F., Leng Y., Chock P.B., Chase T.N., Mouradian M.M. Degradation of α-synuclein by proteasome. J Biol Chem. 274:1999;33855-33858
6. Betarbet R., Sherer T.B., MacKenzie G., Garcia-Osuna M., Panov A.V., Greenamyre J.T. Chronic systemic pesticide exposure reproduces features of Parkinson's disease. Nat Neurosci. 3:2000;1301-1306
7. Braak E., Braak H. Pathoanatomy of Parkinson's disease. J Neurol. 247:(Suppl 2):2000;II/3-II/10
8. Braak E., Sandmann-Keil D., Rub U., Gai W.P., de Vos R.A., Steur E.N., Arai K., Braak H. α-synuclein immunopositive Parkinson's disease-related inclusion bodies in lower brain stem nuclei. Acta Neuropathol. 101:2001;120-129
9. Brooks A.I., Chadwick C.A., Gelbard H.A., Cory-Slechta D.A., Federoff H.J. Paraquat elicited neurobehavioral syndrome caused by dopaminergic neuron loss. Brain Res. 823:1999;1-10
10. Cataldo A.M., Hamilton D.J., Barnett J.L., Paskevich P.A., Nixon R.A. Properties of the endosomal-lysosomal system in the human central nervous system: disturbances mark most neurons in populations at risk to degenerate in Alzheimer's disease. J Neurosci. 16:1996;186-199
11. Ciechanover A. The ubiquitin-mediated proteolytic pathway. Brain Pathol. 3:1993;67-75
12. Clayton D.F., George J.M. Synucleins in synaptic plasticity and neurodegenerative disorders. J Neurosci Res. 58:1999;120-129
13. Conway K.A., Harper J.D., Lansbury P.T. Accelerated in vitro fibril formation by a mutant α-synuclein linked to early-onset Parkinson's disease. Nat Med. 4:2000;1318-1320
14. Del Tredici K., Rub U., De Vos R.A., Bohl J.R., Braak H. Where does Parkinson's begin? J Neuropathol Exp Neurol. 61:2002;413-426
15. Duffy P.E., Tennyson V.M. Phase and electron microscopic observations of Lewy bodies and melanin granules in substantia nigra and locus ceruleus in Parkinson's disease. J Neuropathol Exp Neurol. 24:1965;398-414
16. 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
17. Enochs W.S., Sarna T., Zecca L., Riley P.A., Swartz H.M. The roles of neuromelanin, binding of metal ions, and oxidative cytotoxicity in the pathogenesis of Parkinson's disease: a hypothesis. J Neural Transm. 7:1994;83-100
18. Feany M.B., Bender W.W. A Drosophila model of Parkinson's disease. Nature. 404:2000;394-398
19. Forno L.S. The Lewy body in Parkinson's disease. J Neuropathol Exp Neurol. 45:1996;35-43
20. Forno L.S. Neuropathology of Parkinson's disease. J Neuropathol Exp Neurol. 55:1996;259-272
21. Forno L.S., DeLanney L.E., Irwin I., Langston J.W. Similarities and differences between MPTP-induced parkinsonism and Parkinson's disease: neuropathologic considerations. Adv Neurol. 60:1993;600-608
22. Gai W.P., Yuan H.X., Li X.Q., Power J.T.H., Blumbergs P.C., Jensen P.H. In situ and in vitro study of colocalization and segregation of α-synuclein, ubiquitin, and lipids in Lewy bodies. Exp Neurol. 166:2000;324-333
23. Hallman H., Lange J., Olson L., Strömberg, Jonsson G. Neurochemical and histochemical characterization of neurotoxic effects of MPTP on brain catecholamine neurons in the mouse. J Neurochem. 44:1985;117-127
24. Harman D. Lipofuscin and ceroid formation: the cellular recycling system. Porta E.A. Lipofuscin and ceroid pigments. 1990;3-15 Plenum Press, New York
25. Hashimoto M., Hsu L.J., Xia Y., Takeda A., Sisk A., Sundsmo M., Masliah E. Oxidative stress induces amyloid-like aggregate formation of NACP/alpha-synuclein in vitro. Neuroreport. 10:1999;717-721
26. Inoue H., Castagnoli K., Van Der Schyf C., Mabic S., Igarashi K., Castagnoli N. Jr. Species-dependent differences in monoamine oxidase A and B-catalyzed oxidation of various C4 substituted 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridinyl derivatives. J Pharmacol Exp Ther. 291:1999;856-864
27. Ischiropoulos H., Zhu L., Chen J., Tsai M., Martin J.C., Smith C.D., Beckman J.S. Peroxynitrite-mediated tyrosine nitration catalyzed by superoxide dismutase. Arch Biochem Biophys. 298:1992;431-437
28. Jellinger K. Cytoskeletal pathology of Parkinsonism and aging brain. Calne D., Crippa D., Comi G., Horowski R., Trabucchi M. Parkinsonism and aging. 1989;35-56 Raven Press, New York
29. Jenner P. Oxidative stress as a cause of Parkinson's disease. Acta Neurol Scand. 84:1991;6-15
30. Kahle P.J., Neumann M., Ozmen L., Müller V., Jacobsen H., Schindzielorz A., Okochi M., Leimer U., van der Putten H., Probst A., Kremmer E., Kretschman H.A., Haass C. Subcellular localization of wild-type and Parkinson's disease-associated mutant α-synuclein in human and transgenic mouse brain. J Neurosci. 20:2000;6365-6373
31. Kanda S., Bishop J.F., Eglitis M.A., Yang Y., Mouradian M.M. Enhanced vulnerability to oxidative stress by alpha-synuclein mutations and C-terminal truncation. Neuroscience. 97:2000;279-284
32. Katsuse O., Iseki E., Marui W., Kosaka K. Developmental stages of cortical Lewy bodies and their relation to axonal transport blockage in brains of patients with dementia with Lewy bodies. J Neurol Sci. 211:2003;29-35
33. Keller J.N., Gee J., Ding Q. The proteasome in brain aging. Ageing Res Rev. 1:2002;279-293
34. Kholodilov N.G., Oo T.F., Burke R.E. Synuclein expression is decreased in rat substantia nigra following induction of apoptosis by intrastriatal 6-hydroxydopamine. Neurosci Lett. 275:1999;105-108
35. Kirik D., Rosenblad C., Burger C., Lundberg C., Johansen T.E., Muzyczka N., Mandel R.J., Björklund A. Parkinson-like neurodegeneration induced by targeted overexpression of α-synuclein in the nigrostriatal system. J Neurosci. 22:2002;2780-2791
36. Kirik D., Annett L.E., Burger C., Muzyczka N., Mandel R.J., Björklund A. Nigrostriatal α-synucleinopathy induced by viral vector-mediated overexpression of human α-synuclein: a new primate model of Parkinson's disease. Proc Natl Acad Sci. 100:2003;2884-2889
37. 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
38. Kowall N.W., Hantraye P., Brouillet E., Beal M.F., McKee A.C., Ferrante R.J. MPTP induces alpha-synuclein aggregation in the substantia nigra of baboons. Clin Neurosci Neuropathol. 11:2000;211-213
39. Krüger R., Kuhn W., Müller T., Woitalla D., Graeber M., Kösel S., Pruntek H., Epplen J.T., Schöls L., Reiss O. Ala30Pro mutation in the gene encoding α-synuclein in Parkinson's disease. Nat Genet. 18:1998;106-108
40. Langston J.W., Forno L.S., Tetrud J., Reeves A.G., Kaplan J.A., Karluk D. Evidence of active nerve cell degeneration in the substantia nigra of humans years after 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine exposure. Ann Neurol. 46:1999;598-605
41. Lau Y.S., Trobough K.L., Crampton J.M., Wilson J.M. Effects of probenecid on striatal dopamine depletion in acute and long- term 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine (MPTP)-treated mice. Gen Pharmacol. 21:1990;181-187
42. Lim K.L., Dawson V.L., Dawson T.M. The cast of molecular characters in Parkinson's Disease. Felons, conspirators, and suspects. Ann NY Acad Sci. 991:2003;80-92
43. Liou H.-H., Tsai M.C., Chen C.J., Jeng J.S., Chang Y.C., Chen S.Y., Chen R.C. Environmental risk factors and Parkinson's disease: a case-control study in Taiwan. Neurology. 48:1997;1583-1588
44. Lo Bianco C., Ridet J.-L., Schneider B.L., Déglon, Aebischer P. α-synucleinopathy and selective dopaminergic neuron loss in a rat lentiviral-based model of Parkinson's disease. Proc Natl Acad Sci USA. 99:2002;10813-10818
45. Lotharius J., Brundin P. Pathogenesis of Parkinson's disease: dopamine, vesicles and alpha-synuclein. Nat Rev Neurosci. 3:2002;932-942
46. Manning-Bog A.B., McCormack A.L., Li J., Uversky V.N., Fink A.L., Di Monte D.A. The herbicide Paraquat causes upregulation and aggregation of α-synuclein in mice. J Biol Chem. 277:2001;1641-1644
47. Mash D.C., Ouyang Q., Pablo J., Basile M., Izenwasser S., Lieberman A., Perrin R.J. Cocaine abusers have an overexpression of alpha-synuclein in dopamine neurons. J Neurosci. 23:2003;2564-2571
48. 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 α-synuclein mice: implications for neurodegenerative disorders. Science. 287:2000;1265-1269
49. Matsuoka Y., Vila M., Lincoln S., McCormack A., Picciano M., LaFrancois J., Yu X., Dickson D., Langston W.J., McGowan E., Farrer M., Hardy J., Duff K., Przedborski S., Di Monte D.A. Lack of nigral pathology in transgenic mice expressing human α-synuclein driven by the tyrosine hydroxylase promoter. Neurobiol Dis. 8:2001;535-539
50. Mattson M.P., Chan S.L., Duan W. Modification of brain aging and neurodegenerative disorders by genes, diet, and behavior. Physiol Rev. 82:2002;637-672
51. Mayer R.J., Laszlo L., Landon M., Hope J., Lowe J. Ubiquitin, lysosomes, and neurodegenerative diseases. Ann NY Acad Sci. 674:1992;149-160
52. McCormack A.L., Thiruchelmvam M., Manning-Bog A.B., Thiffault C., Langston J.W., Cory-Slechta D.A., Di Monte D.A. Environmental risk factors and Parkinson's disease: selective degeneration of nigral dopaminergic neurons caused by the herbicide paraquat. Neurobiol Dis. 10:2002;119-127
53. McLean P.J., Kawamata H., Shariff S., Hewett J., Sharma N., Ueda K., Breakefield X.O., Hyman B.T. Torsin A and heat shock proteins act as molecular chaperones: suppression of alpha-synuclein aggregation. J Neurochem. 83:2002;846-854
54. McNaught K.S.P., Olanow C.W., Halliwell B., Isaacson O., Jenner P. Failure of the ubiquitin-proteasome system in Parkinson's disease. Nature Rev Neurosci. 2:2001;589-594
55. Menegon A., Board P.G., Blackburn A.C., Mellick G.D., Le Couteur D.G. Parkinson's disease, pesticides, and glutathione transferase polymorphisms. Lancet. 352:1998;1344-1346
56. Meredith G.E., Totterdell S., Petroske E., Santa Cruz K., Callison R. Jr, Lau Y.-S. Lysosomal malfunction accompanies alpha-synuclein aggregation in a progressive mouse model of Parkinson's disease. Brain Res. 956:2002;156-165
57. Mitsumoto Y., Watanabe A., Mori A., Koga N. Spontaneous regeneration of nigrostriatal dopaminergic neurons in MPTP-treated C57BL/6 mice. Biochem Biophys Res Commun. 248:1998;660-663
58. Mori H., Oda M., Komori T., Arai N., Takanashi M., Mizutani T., Hirai S., Mizuno Y. Lewy bodies in progressive supranuclear palsy. Acta Neuropathol (Berl). 104:2002;273-278
59. Narhi L., Wood S.J., Stevenson S., Jiang Y., Wu G.M., Anafi D., Kaufman S.A., Martine F., Sitney K., Denis P., Louis J.C., Wypych J., Biere A.L., Citron M. Both familial Parkinson's disease mutations accelerate alpha-synuclein aggregation. J Biol Chem. 274:1999;9843-9846. Erratum in: J Biol Chem 1999; 274: 13728
60. Neystat M., Lynch T., Przedborski S., Kholodilov N., Rzhetskaya M., Burke R.E. Alpha-synuclein expression in substantia nigra and cortex in Parkinson's disease. Mov Disord. 14:1999;417-422
61. Nixon R.A., Cataldo A.M., Paskevich P.A., Hamilton D.J., Wheelock T.R., Kanaley-Andrews L. The lysosomal system in neurons. Involvement at multiple stages of Alzheimer's disease pathogenesis. Ann NY Acad Sci. 674:1992;65-88
62. Orth M., Tabrizi S. Models of Parkinson's disease. Movement Dis. 18:2003;729-737
63. Ostrerova-Golts N., Petrucelli L., Hardy J., Lee J.M., Fare M., Wolozin B. The A53T α-synuclein mutation increases iron-dependent aggregation and toxicity. J Neurosci. 20:2000;6048-6054
64. Parkkinen L., Soininen H., Alafuzoff I. Regional distribution of alpha-synuclein pathology in unimpaired aging and Alzheimer disease. J Neuropathol Exp Neurol. 62:2003;363-367
65. Parkkinen L., Soininen H., Laakso M., Alafuzoff I. Alpha-synuclein pathology is highly dependent on the case selection. Neuropathol Appl Neurobiol. 27:2001;314-325
66. Petroske E., Meredith G.E., Callen S., Totterdell S., Lau Y.-S. Mouse model of parkinsonism: a comparison between subacute MPTP and chronic MPTP/probenecid treatment. Neuroscience. 106:2001;589-601
67. Polymeropoulos M.H., Lavedan C., Leroy E., Ide S.E., Dehejia A., Dutr A., Pike B., Root H., Rubenstein J., Boyer R., Stenroos E.S., Chandrasekharapa S., Athanassiadou A., Papapetropoulos T., Johnson W.G., Lazzarini A., Duvoisin R.C., di Lorio G., Golbe L.I., Nussbaum R.L. Mutation in the α-synuclein gene identified in families with Parkinson's disease. Science. 276:1997;2045-2047
68. Przedborski S., Chen Q., Vila M., Giasson B.I., Djaldatti R., Vukosavic S., Souza J.M., Jackson-Lewis V.V., Lee V.M., Ischiropoulos H. Oxidative post-translational modifications of α-synuclein in the 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine (MPTP) mouse model of Parkinson's disease. J Neurochem. 76:2001;637-640
69. Ricaurte G.A., Langston J.W., Delanney L.E., Irwin I., Peroutka S.J., Forno L.S. Fate of nigrostriatal neurons in young mature mice given 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine: a neurochemical and morphological reassessment. Brain Res. 376:1986;117-124
70. 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 α-synuclein in transgenic mice. Exp Neurol. 175:2002;35-48
71. Rideout H.J., Larsen K.E., Sulzer D., Stefanis L. Proteosomal inhibition leads to formation of ubiquitin/alpha-synuclein-immunoreactive inclusions in PC12 cells. J Neurochem. 78:2001;899-908
72. Saito Y., Kawashima A., Ruberu N.N., Fujiwara H., Koyama S., Sawabe M., Arai T., Nagura H., Yamanouchi H., Hasegawa M., Iwatsubo T., Murayama S. Accumulation of phosphorylated alpha-synuclein in aging human brain. J Neuropathol Exp Neurol. 62:2003;644-654
73. Sherer T.B., Betarbet R., Stout A.K., Lund S., Baptista M., Panov A.V., Cookson M.R., Greenamyre J.T. An in vitro model of Parkinson's disease: linking mitochondrial impairment to altered α-synuclein metabolism and oxidative damage. J Neurosci. 22:2002;7006-7015
74. Song D.D., Haber S.N. Striatal responses to partial dopaminergic lesion: evidence for compensatory sprouting. J Neurosci. 20:2000;5102-5114
75. Sonsalla P.K., Heikkila R.E. The influence of dose and dosing interval on MPTP-induced dopaminergic neurotoxicity in mice. Eur J Pharmacol. 12:1986;339-345
76. Spillantini M.G., Schmidt M.L., Lee V.M., Trojanowski J.Q., Jakes R., Goedert M. Alpha-synuclein in Lewy bodies. Nature. 388:1997;839-840
77. Thiruchelvam M., Brockel B.J., Richfield E.K., Baggs R.B., Cory-Slechta D.A. Potentiated and preferential effects of combined paraquat and maneb on nigrostriatal dopamine systems: environmental risk factors for Parkinson's disease? Brain Res. 873:2000;225-234
78. Tofaris G.K., Layfield R., Spillantini M.G. α-Synuclein metabolism and aggregation is linked to ubiquitin-independent degradation by the proteasome. FEBS Lett. 509:2001;22-26
79. Totterdell S., Hanger D., Meredith G.E. The ultrastructural distribution of alpha-synuclein-like protein in normal mouse brain: implications for Parkinson's disease. Brain Res. 2004;. in press
80. Uversky V.N., Li J., Souillac P., Millett I.S., Doniach S., Jakes R., Goedert M., Finck A.L. Biophysical properties of the synucleins and their propensities to fibrillate. J Biol Chem. 277:2002;11970-11978
81. Van der Putten H., Wiederhold K.-H., Probst A., Barbieri S., Mistl C., Danner S., Kauffmann S., Hofele K., Spooren W.P.J.M., Ruegg M.A., Lin S., Caroni P., Sommer B., Tolnay M., Bilbe G. Neuropathology in mice expressing human α-synuclein. J Neurosci. 20:2000;6021-6029
82. 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
83. Widdowson P.S., Farnworth M.J., Simpson M.G., Lock E.A. Influence of age on the passage of paraquat through the blood-brain barrier in rats: a distribution and pathological examination. Hum Exp Toxicol. 15:1996;231-236
84. Widdowson P.S., Farnworth M.J., Upton R., Simpson M.G. No changes in behaviour, nigro-striatal system neurochemistry or neuronal cell death following toxic multiple oral paraquat administration to rats. Hum Exp Toxicol. 15:1996;583-591
85. Zecca L., Tampellini D., Gerlach M., Riederer P., Fariello R.G., Sulzer D. Substantia nigra neuromelanin: structure, synthesis, and molecular behaviour. Mol Pathol. 54:2001;414-418
86. Zhang I., Dawson V.L., Dawson T.M. Oxidative stress and genetics in the pathogenesis of Parkinson's disease. Neurobiol Dis. 7:2000;240-250