Role of oxidative damage in protein aggregation associated with Parkinson's disease and related disorders

Antioxidants and Redox Signaling

Volumn 7, Issue 5-6, 2005, Pages 673-684

  Norris, Erin H ^a   Giasson, Benoit I ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3 NITROTYROSINE; ALPHA SYNUCLEIN; TAU PROTEIN; NERVE PROTEIN; NITRATE; SNCA PROTEIN, HUMAN; SYNUCLEIN;

ALZHEIMER DISEASE; BRAIN STEM; CELL INCLUSION; DEGENERATIVE DISEASE; DOPAMINERGIC NERVE CELL; GENE MUTATION; HUMAN; LEWY BODY; NITRATION; OLIGODENDROGLIA; OXIDATIVE STRESS; PARKINSON DISEASE; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN AGGREGATION; REVIEW; SHY DRAGER SYNDROME; SUBSTANTIA NIGRA; ANIMAL; CHEMISTRY; GENETICS; METABOLISM; PATHOLOGY;

ALPHA-SYNUCLEIN; ANIMALS; HUMANS; INCLUSION BODIES; LEWY BODIES; NERVE TISSUE PROTEINS; NITRATES; OXIDATIVE STRESS; PARKINSON DISEASE; SYNUCLEINS;

EID: 17644426350     PISSN: 15230864     EISSN: None     Source Type: Journal    
DOI: 10.1089/ars.2005.7.672     Document Type: Review

References (136)

1. Abeliovich A, Schmitz Y, Farinas I, Choi-Lundberg D, Ho WH, Castillo PE, Shirisky N, Verdugo JM, Armanini M, Ryan A, Hynes M, Phillips H, Sulzer D, and Rosenthal A. Mice lacking alpha-synuclein display functional deficits in the nigrostriatal dopamine system. Neuron 25: 239-252, 2000.
2. Arawaka S, Saito Y, Murayama S, and Mori H. Lewy body in neurodegenenition with brain iron accumulation type 1 is immunoreactive for alpha-synuclein. Neurology 51: 887-889, 1998.
3. Arima K, Murayama S, Mukoyama M, and Inose T. Immunocytochemical and ultrastructural studies of neuronal and oligodendroglial cytoplasmic inclusions in multiple system atrophy. 1. Neuronal cytoplasmic inclusions. Acta Neuropathol (Berl) 83: 453-460, 1992.
4. Athanassiadou A, Voutsinas G, Psiouri L, Leroy E, Polymeropoulos MH, Ilias A, Maniatis GM, and Papapetropoulos T. Genetic analysis of families with Parkinson disease that carry the Ala53Thr mutation in the gene encoding alpha-synuclein. Am J Hum Genet 65: 555-558, 1999.
5. Barbeau A, Roy M, Bernier G, Campanella G, and Paris S. Ecogenetics of Parkinson's disease: prevalence and environmental aspects in rural areas. Can J Neurol Sci 14: 36-41, 1987.
6. Barghorn S and Mandelkow E. Toward a unified scheme for the aggregation of tau into Alzheimer paired helical filaments. Biochemistry 41: 14885-14896, 2002.
7. Beal MF. Mitochondria, free radicals, and neurodegeneration. Curr Opin Neurobiol 6: 661-666, 1996.
8. Bhattacharya K, Rank KB, Evans DB, and Sharma SK. Role of cysteine-291 and cysteine-322 in the polymerization of human tau into Alzheimer-like filaments. Biochem Biophys Res Commun 285: 20-26, 2001.
9. Braak H, Braak E, Yilmazer D, de Vos RA, Jansen EN, Bohl J, and Jellinger K. Amygdala pathology in Parkinson's disease. Acta Neuropathol (Berl) 88: 493-500, 1994.
10. Brée L, Bussière T, Buée-Scherrer V, Delacourte A, and Hof PR. Tau protein isoforms, phosphorylation and role in neurodegenerative disorders. Brain Res Rev 33: 95-130, 2000.
11. Buchman VL, Hunter HJ, Pinon LG, Thompson J, Privalova EM, Ninkina NN, and Davies AM. Persyn, a member of the synuclein family, has a distinct pattern of expression in the developing nervous system. J Neurosci 18: 9335-9341, 1998.
12. Cabin DE, Shimazu K, Murphy D, Cole NB, Gottschalk W, McIlwain KL, Orrison B, Chen A, Ellis CE, Paylor R, Lu B, and Nussbaum PL. Synaptic vesicle depletion correlates with attenuated synaptic responses to prolonged repetitive stimuation in mice lacking α-synuclein. J Neurosci 22: 8797-8807, 2002.
13. Conway KA, Harper JD, and Lansbury PT. Accelerated in vitro fibril formation by a mutant alpha-synuclein linked to early-onset Parkinson disease. Nat Med 4: 1318-1320, 1998.
14. Conway KA, Harper JD, and Lansbury PT. Fibrils formed in vitro from alpha-synuclein and two mutant forms linked to Parkinson's disease are typical amyloid. Biochemistry 39: 2552-2563, 2000.
15. Conway KA, Lee SJ, Rochet JC, Ding TT, Williamson RE, and Lansbury PT. 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 USA 97: 571-576, 2000.
16. Conway KA, Rochet JC, Bieganski RM, and Lansbury PT Jr. Kinetic stabilization of the alpha-synuclein protofibril by a dopamine-alpha-synuclein adduct. Science 294: 1346-1349, 2001.
17. Cronford ME, Chang L, and Miller BL. The neuropathology of parkinsonism: an overview. Brain Cogn 28: 321-341, 1995.
18. Crowther RA, Jakes R, Spillantini MG, and Goedert M. Synthetic filaments assembled from C-terminally truncated alpha-synuclein. FEBS Lett 436: 309-312, 1998.
19. Damier P, Hirsch EC, Agid Y, and Graybiel AM. The substantia nigra of the human brain. 11. Patterns of loss of dopamine-containing neurons in Parkinson's disease. Brain 122(Pt 8): 1437-1448, 1999.
20. Davidson WS, Jonas A, Clayton DF, and George JM. Stabilization of alpha-synuclein secondary structure upon binding to synthetic membranes. J Biol Chem 273: 9443-9449, 1998.
21. Dawson TM, Mandir AS, and Lee MK. Animal models of PD: pieces of the same puzzle? Neuron 35: 219-222, 2002.
22. Dickson DW, Ruan D, Crystal H, Mark MH, Davies P, Kress Y, and Yen SH. Hippocampal degeneration differentiates diffuse Lewy body disease (DLBD) from Alzheimer's disease: light and electron microscopic immunocytochemistry of CA2-3 neurites specific to DLBD. Neurology 41: 1402-1409, 1991.
23. Dooling EC, Schoene WC, and Richardson EP Jr. Hallervorden-Spatz syndrome. Arch Neurol 30: 70-83, 1974.
24. Du HN, Tang L, Luo XY, Li HT, Hu J, Zhou JW, and Hu HY. A peptide motif consisting of glycine, alanine, and valine is required for the fibrillization and cytotoxicity of human alpha-synuclein. Biochemistry 42: 8870-8878, 2003.
25. Duda JE, Giasson BI, Chen Q, Gur TL, Hurtig HI, Stern MB, Gollomp SM, Ischiropoulos H, Lee VM-Y, and Trojanowski JQ. Widespread nitration of pathological inclusions in neurodegenerative synucleinopathies. Am J Pathol 157: 1439-1445, 2000.
26. Duda JE, Giasson BI, Gur TL, Montine TJ, Robertson D, Biaggioni I, Hurtig HI, Stern MB, Gollomp SM, Grossman M, Lee VM-Y, and Trojanowski JQ. Immunohistochemical and biochemical studies demonstrate a distinct profile of alpha-synuclein permutations in multiple system atrophy. J Neuropathol Exp Neurol 59: 830-841, 2000.
27. Duda JE, Lee VM-Y, and Trojanowski JQ. Neuropathology of synuclein aggregates. J Neurosci Res 61: 121-127, 2000.
28. Duda JE, Giasson BI, Mabon ME, Lee VM-Y, and Trojanoswki JQ. Novel antibodies to oxidized α-synuclein reveal abundant neuritic pathology in Lewy body disease. Ann Neurol 52: 205-210, 2002.
29. Duda JE, Giasson BI, Mabon ME, Miller DC, Golbe LI, Lee VM-Y, and Trojanowski JQ. Concurrence of α-synuclein and tau brain pathology in the Contursi kindred. Acta Neuropathol (Berl) 104: 7-11, 2002.
30. Duffy PE and Tennyson VM. Phase and electron microscopy observations of Lewy bodies and melanin granules in the substantia nigra and locus ceruleus in Parkinson's disease. J Neuropathol Exp Neurol 24: 398-414, 1965.
31. El Agnaf OM, Jakes R, Curran MD, and Wallace A. Effects of the mutations Ala30 to Pro and Ala53 to Thr on the physical and morphological properties of alpha-synuclein protein implicated in Parkinson's disease. FEBS Lett 440: 67-70, 1998.
32. Farrer M, Kachergus J, Forno L, Lincoln S, Wang DS, Hulihan M, Maraganore D, Gwinn-Hardy K, Wszolek Z, Dickson D, and Langston JW. Comparison of kindreds with parkinsonism and alpha-synuclein genomic multiplications. Ann Neurol 55: 174-179, 2004.
33. Fearnley J and Lees AJ. Parkinson's disease: neuropathology. Brain 114: 2283-2301, 1991.
34. Forno LS. Neuropathology of Parkinson's disease. J Neuropathol Exp Neurol 55: 259-272, 1996.
35. Fujiwara H, Hasegawa M, Dohmae N, Kawashima A, Masliah E, Goldberg MS, Shen J, Takio K, and Iwatsubo T. α-synuclein is phosphorylated in synucleinopathy lesions. Nat Cell Biol 4: 160-164, 2002.
36. Galvin JE, Giasson B, Hurtig HI, Lee VM-Y, and Trojanowski JQ. Neurodegeneration with brain iron accumulation, type 1 is characterized by alpha-, beta-, and gamma-synuclein neuropathology. Am J Pathol 157: 361-368, 2000.
37. Gamblin TC, King ME, Kuret J, Berry RW, and Binder LI. Oxidative regulation of fatty acid-induced tau polymerization. Biochemistry 39: 14203-14210, 2000.
38. George JM. The synucleins. Genome Biol 3: REVIEWS 3002, 2002.
39. George JM, Jin H, Woods WS, and Clayton DF. Characterization of a novel protein regulated during the critical period for song learning in the zebra finch. Neuron 15: 361-372, 1995.
40. Giasson BI, Uryu K, Trojanowski JQ, and Lee VM-Y. Mutant and wild type human alpha-synucleins assemble into elongated filaments with distinct morphologies in vitro. J Biol Chem 274: 7619-7622, 1999.
41. Giasson BI, Duda JE, Murray IV, Chen Q, Souza JM, Hurtig HI, Ischiropoulos H, Trojanowski JQ, and Lee VM-Y. Oxidative damage linked to neurodegeneration by selective alpha-synuclein nitration in synucleinopathy lesions. Science 290: 985-989, 2000.
42. Giasson BI, Murray IV, Trojanowski JQ, and Lee VM-Y. A hydrophobic stretch of 12 amino acid residues in the middle of alpha-synuclein is essential for filament assembly. J Biol Chem 276: 2380-2386, 2001.
43. Giasson BI, Duda JE, Quinn SM, Zhang B, Trojanoswki JQ, and Lee VM-Y. Neuronal α-synucleinopathy with severe movement disorder in mice expressing A53T human α-synuclein. Neuron 34: 521-533, 2002.
44. Giasson BI, Ischiropoulos H, Lee VM-Y, and Trojanoswki JQ. The relationship between oxidative/nitrative stress and pathological inclusions in Alzheimer's and Parkinson's diseases. Free Radic Biol Med 32: 1264-1275, 2002.
45. Giasson BI, Forman MS, Golbe LI, Graves CL, Kotzbauer PT, Trojanoswki JQ, and Lee VM-Y. Initiation and synergistic fibrillization of tau and alpha-synuclein, Science 300: 636-640, 2003.
46. Gilman S, Low PA, Quinn N, Albanese A, Ben Shlomo Y, Fowler CJ, Kaufmann H, Klockgether T, Lang AE, Lantos PL, Litvan I, Mathias CJ, Oliver E, Robertson D, Schatz I, and Wenning GK. Consensus statement on the diagnosis of multiple system atrophy. J Neural Sci 163: 94-98, 1999.
47. Goedert M. Alpha-synuclein and neurodegenerative diseases. Nat Rev Neurosci 2: 492-501, 2001.
48. Goedert M, Spillantini MG, Jakes R, Rutherford D, and Crowther RA. Multiple isoforms of human microtubule-associated protein tau: sequences and localization in neurofibrillary tangles of Alzheimer's disease. Neuron 3: 519-526, 1989.
49. Goedert M, Jakes R, Spillantini MG, Hasegawa M, Smith MJ, and Crowther RA. Assembly of microtubule-associated protein tau into Alzheimer-like filaments induced by sulphated glycosaminoglycans. Nature 383: 550-553, 1996.
50. Goldberg MS and Lansbury PT. Is there a cause-and-effect relationship between alpha-synuclein fibrillization and Parkinson's disease? Nat Cell Biol 2: E115-E119, 2000.
51. Gomez-Tortosa E, Gonzalo I, Newell K, Garcia YJ, Vonsattel P, and Hyman BT. Patterns of protein nitration in dementia with Lewy bodies and striatonigral degeneration. Acta Neuropathol (Berl) 103: 495-500, 2002.
52. Graham DG. Oxidative pathways for catecholamines in the genesis of neuromelanin and cytotoxic quinones. Mol Pharmacol 14: 633-643, 1978.
53. Graham DG, Tiffany SM, Bell WR Jr, and Gutknecht WF. Autoxidation versus covalent binding of quinones as the mechanism of toxicity of dopamine, 6-hydroxydopamine, and related compounds toward C1300 neuroblastoma cells in vitro. Mol Pharmacol 14: 644-653, 1978.
54. Hansen L, Salmon D, Galasko D, Masliah E, Katzman R, DeTeresa R, Thai L, Pay MM, Hofstetter R, Klauber M, et al. The Lewy body variant of Alzheimer's disease: a clinical and pathologic entity. Neurology 40: 1-8, 1990.
55. Haroutunian V, Serby M, Purohit DP, Perl DP, Marin D, Lantz M, Mohs RC, and Davis KL. Contribution of Lewy body inclusions to dementia in patients with and without Alzheimer disease neuropathological conditions. Arch Neurol 57: 1145-1150, 2000.
56. Hashimoto M, Hsu LJ, Xia Y, Takeda A, Sisk A, Sundsmo M, and Masliah E. Oxidative stress induces amyloid-like aggregate formation of NACP/alpha-synuclein in vitro. Neuroreport 10: 717-721, 1999.
57. Hashimoto M, Takeda A, Hsu LJ, Takenouchi T, and Masliah E. Role of cytochrome c as a stimulator of alpha-synuclein aggregation in Lewy body disease. J Biol Chem 274: 28849-28852, 1999.
58. Hastings TG, Lewis DA, and Zigmond MJ. Role of oxidation in the neurotoxic effects of intrastriatal dopamine injections. Proc Natl Acad Sci U S A 93: 1956-1961, 1996.
59. Hill WD, Lee VM-Y, Hurtig HI, Murray JM, and Trojanowski JQ. Epitopes located in spatially separate domains of each neurofilament subunit are present in Parkinson's disease Lewy bodies. J Comp Neurol 309: 150-160, 1991.
60. Hoehn MM and Yahr MD. Parkinsonism: onset, progression and mortality. Neurology 17: 427-442, 1967.
61. Horiguchi T, Uryu K, Giasson BI, Ischiropoulos H, Lightfoot R, Bellmann C, Richter-Landsberg C, Lee VM-Y, and Trojanowski JQ. Nitration of tau protein is linked to neurodegeneration in tauopathies. Am J Pathol 163: 1021-1031, 2003.
62. Hurtig HI, Trojanowski JQ, Galvin J, Ewbank D, Schmidt ML, Lee VM, Clark CM, Glosser G, Stern MB, Gollomp SM, and Arnold SE. Alpha-synuclein cortical Lewy bodies correlate with dementia in Parkinson's disease. Neurology 54: 1916-1921, 2000.
63. Ingram EM and Spillantini MG. Tau gene mutations: dissecting the pathogenesis of FTDP-17. Trends Mol Med 8: 555-562, 2002.
64. Irizarry MC, Kim TW, McNamara M, Tanzi RE, George JM, Clayton DF, and Hyman BT. Characterization of the precursor protein of the non-A beta component of senile plaques (NACP) in the human central nervous system. J Neuropathol Exp Neurol 55: 889-895, 1996.
65. Irizarry MC, Growdon W, Gomez-Isla T, Newell K, George JM, Clayton DF, and Hyman BT. 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: 334-337, 1998.
66. Ishizawa T, Mattila P, Davies P, Wang D, and Dickson DW Colocalization of tau and alpha-synuclein epitopes in Lewy bodies. J Neuropathol Exp Neurol 62: 389-397, 2003.
67. Iwai A, Masliah E, Yoshimoto M, Ge N, Flanagan L, de Silva HA, Kittel A, and Saitoh T. The precursor protein of non-A beta component of Alzheimer's disease amyloid is a presynaptic protein of the central nervous system. Neuron 14:467-475, 1995.
68. Jakes R, Spillantini MG, and Goedert M. Identification of two distinct synucleins from human brain. FEBS Lett 345: 27-32, 1994.
69. Kampers T, Friedhoff P, Biernat J, Mandelkow EM, and Mandelkow E. RNA stimulates aggregation of microtubule-associated protein tau into Alzheimer-like paired helical filaments. FEBS Lett 399: 344-349, 1996.
70. Kato S, Nakamura H, Hirano A, Ito H, Llena JF, and Yen SH. Argyrophilic ubiquitinated cytoplasmic inclusions of Leu-7-positive glial cells in olivopontocerebellar atrophy (multiple system atrophy). Acta Neuropathol (Berl) 82: 488-493, 1991.
71. Kosaka K. Diffuse Lewy body disease in Japan. J Neurol 237: 197-204, 1990.
72. Krishnan S, Chi EY, Wood SJ, Kendrick BS, Li C, Garzon-Rodriguez W, Wypych J, Randolph TW, Narhi LO, Biere AL, Citron M, and Carpenter JF. Oxidative dimer formation is the critical rate-limiting step for Parkinson's disease alpha-synuclein fibrillogenesis. Biochemistry 42: 829-837, 2003.
73. Kruger R, Kuhn W, Muller T, Woitalla D, Graeber M, Kosel S, Przuntek H, Epplen JT, Schols L, and Riess O. Ala30Pro mutation in the gene encoding alpha-synuclein in Parkinson's disease. Nat Genet 18: 106-108, 1998.
74. Lang AE and Lozano AM. Parkinson's disease. First of two parts. N Engl J Med 339: 1044-1053, 1998.
75. Lantos PL. Multiple system atrophy. Brain Pathol 7: 1293-1297, 1997.
76. Lee MK, Stirling W, Xu Y, Xu X, Qui D, Mandir AS, Dawson TM, Copeland NG, Jenkins NA, and Price DL. Human alpha-synuclein-harboring familial Parkinson's disease-linked Ala-53 → Thr mutation causes neurodegenerative disease with alpha-synuclein aggregation in transgenic mice. Proc Natl Acad Sci U S A 99: 8968-8973, 2002.
77. Lee VM-Y, Goedert M, and Trojanowski JQ. Neurodegenerative tauopathies. Annu Rev Neurosci 24: 1121-1159, 2001.
78. Lee VM-Y, Giasson BI, and Trojanowski JQ. More than just two peas in a pod: common amyloidogenic properties of tau and alpha-synuclein in neurodegenerative diseases. Trends Neurosci 27: 129-134, 2004.
79. Lennox G, Lowe J, Landon M, Byrne EJ, Mayer RJ, and Godwin-Austen RB. Diffuse Lewy body disease: correlative neuropathology using anti-ubiquitin immunocytochemistry. J Neurol Neurosurg Psychiatry 52: 1236-1247, 1989.
80. Liou HH, Tsai MC, Chen CJ, Jeng JS, Chang YC, Chen SY, and Chen RC. Environmental risk factors and Parkinson's disease: a case-control study in Taiwan. Neurology 48: 1583-1588, 1997.
81. Lippa CF, Schmidt ML, Lee VM-Y, and Trojanowski JQ. Antibodies to alpha-synuclein detect Lewy bodies in many Down's syndrome brains with Alzheimer's disease. Ann Neurol 45: 353-357, 1999.
82. Markopoulou K and Langston JW. Candidate genes and Parkinson's disease: where to next? Neurology 53: 1382-1383, 1999.
83. Marui W, Iseki E, Ueda K, and Kosaka K. Occurrence of human alpha-synuclein immunoreactive neurons with neurofibrillary tangle formation in the limbic areas of patients with Alzheimer's disease. J Neurol Sci 174: 81-84, 2000.
84. Mattila PM, Röyttä M, Torikka H, Dickson DW, and Rinne JO. Cortical Lewy bodies and Alzheimer-type changes in patients with Parkinson's disease. Acta Neuropathol (Berl) 95: 576-582, 1998.
85. Mayeau R, Stern Y, Cote L, and Williams JB. Altered serotonin metabolism in depressed patients with Parkinson's disease. Neurology 34: 642-646, 1984.
86. McKeith IG, Galasko D, Kosaka K, Perry EK, Dickson DW, Hansen LA, Salmon DP, Lowe J, Mirra SS, Byrne EJ, Lennox G, Quinn NP, Edwardson JA, Ince PG, Bergeron C, Burns A, Miller BL, Lovestone S, Collerton D, Jansen EN, Ballard C, de Vos RA, Wilcock GK, Jellinger KA, and Perry RH. Consensus guidelines for the clinical and pathologic diagnosis of dementia with Lewy bodies (DLB): report of the consortium on DLB international workshop. Neurology 47: 1113-1124, 1996.
87. Murphy DD, Rueter SM, Trojanowski JQ, and Lee VM-Y. Synucleins are developmentally expressed, and alpha-synuclein regulates the size of the presynaptic vesicular pool in primary hippocampal neurons. J Neurosci 20: 3214-3220, 2000.
88. Murray IV, Giasson BI, Quinn SM, Koppaka V, Axelsen PH, Ischiropoulos H, Trojanowski JQ, and Lee VM-Y. Role of alpha-synuclein carboxy-terminus on fibril formation in vitro. Biochemistry 42: 8530-8540, 2003.
89. Narhi L, Wood SJ, Steavenson S, Jiang Y, Wu GM, Anafi D, Kaufman SA, Martin F, Sitney K, Denis P, Louis JC, Wypych J, Biere AL, and Citron M. Both familial Parkinson's disease mutations accelerate alpha-synuclein aggregation. J Biol Chem 274: 9843-9846, 1999.
90. Neumann M, Kahle PJ, Giasson BI, Ozmen L, Borroni E, Spooren W, Muller V, Odoy S, Fujiwara H, Hasegawa M, Iwatsubo T, Trojanowski JQ, Kretzschmar HA, and Haass C. Misfolded proteinase K-resistant hyperphosphorylated alpha-synuclein in aged transgenic mice with locomotor deterioration and in human alpha-synucleinopathies. J Clin Invest 110: 1429-1439, 2002.
91. Newell KL, Boyer P, Gomez-Tortosa E, Hobbs W, Hedley-Whyte ET, Vonsattel JP, and Hyman BT. Alpha-synuclein immunoreactivity is present in axonal swellings in neuroaxonal dystrophy and acute traumatic brain injury. J Neuropathol Exp Neurol 58: 1263-1268, 1999.
92. Norris EH, Giasson BI, Ischiropoulos H, and Lee VM-Y. Effects of oxidative and nitrative challenges on alpha-synuclein fibrillogenesis involve distinct mechanisms of protein modifications. J Biol Chem 278: 27230-27240, 2003.
93. Okazaki H, Lipkin LE, and Aronson SM. Diffuse intracytoplasmic inclusions (Lewy type) assocaited with progressive dementia and quadraparesis. J Neuropathol Exp Neurol 20: 237-244, 1961.
94. Paik SR, Shin HJ, Lee JH, Chang CS, and Kim J. Copper(II)-induced self-oligomerization of alpha-synuclein. Biochem J340(Pt3): 821-828, 1999.
95. Paik SR, Shin HJ, and Lee JH. Metal-catalyzed oxidation of alpha-synuclein in the presence of copper(II) and hydrogen peroxide. Arch Biochem Biophys 378: 269-277, 2000.
96. Pakkenberg B, Moller A, Gundersen HJ, Mouritzen DA, and Pakkenberg H. The absolute number of nerve cells in substantia nigra in normal subjects and in patients with Parkinson's disease estimated with an unbiased stereological method. J Neurol Neurosurg Psychiatry 54: 30-33, 1991.
97. Papadimitriou A, Veletza V, Hadjigeorgiou GM, Patrikiou A, Hirano M, and Anastasopoulos I. Mutated alpha-synuclein gene in two Greek kindreds with familial PD: incomplete penetrance? Neurology 52: 651-654, 1999.
98. Papp MI, Kahn JE, and Lantos PL. Glial cytoplasmic inclusions in the CNS of patients with multiple system atrophy (striatonigral degeneration, olivopontocerebellar atrophy and Shy-Drager syndrome). J Neurol Sci 94: 79-100, 1989.
99. Paxinou E, Chen Q, Weisse M, Giasson BI, Norris EH, Rueter SM, Trojanowski JQ, Lee VM-Y, and Ischiropoulos H. Induction of alpha-synuclein aggregation by intracellular nitrative insult. J Neurosci 21: 8053-8061, 2001.
100. Perez M, Cuadros R, Smith MA, Perry G, and Avila J. Phosphorylated, but not native, tau protein assembles following reaction with the lipid peroxidation product, 4-hydroxy-2-nonenal. FEBS Lett 486: 270-274, 2000.
101. Polymeropoulos MH, Lavedan C, Leroy E, Ide SE, Dehejia A, Dutra A, Pike B, Root H, Rubenstein J, Boyer R, Stenroos ES, Chandrasekharappa S, Athanassiadou A, Papapetropoulos T, Johnson WG, Lazzarini AM, Duvoisin RC, Di Iorio G, Golbe LI, and Nussbaum RL. Mutation in the alpha-synuclein gene identified in families with Parkinson's disease. Science 276: 2045-2047, 1997.
102. Saito Y, Kawai M, Inoue K, Sasaki R, Arai H, Nanba E, Kuzuhara S, Ihara Y, Kanazawa I, and Murayama S. Widespread expression of alpha-synuclein and tau immunoreactivity in Hallervorden-Spatz syndrome with protracted clinical course. J Neurol Sci 177: 48-59, 2000.
103. Samuel W Galasko D, Masliah E, and Hansen LA. Neocortical Lewy body counts correlate with dementia in the Lewy body variant of Alzheimer's disease. J Neuropathol Exp Neurol 55: 44-52, 1996.
104. Schmidt ML, Murray J, Lee VM-Y, Hill WD, Wertkin A, and Trojanowski JQ. Epitope map of neurofilament protein domains in cortical and peripheral nervous system Lewy bodies. Am J Pathol 139: 53-65, 1991.
105. Schmidt ML, Martin JA, Lee VM-Y, and Trojanowski JQ. Convergence of Lewy bodies and neurofibrillary tangles in amygdala neurons of Alzheimer's disease and Lewy body disorders. Acta Neuropathol (Berl) 91: 475-481, 1996.
106. Schweers O, Mandelkow EM, Biernat J, and Mandelkow E. Oxidation of cysteine-322 in the repeat domain of microtubule-associated protein tau controls the in vitro assembly of paired helical filaments. Proc Natl Acad Sci U S A 92: 8463-8467, 1995.
107. Semchuk KM, Love EJ, and Lee RG. Parkinson's disease: a test of the multifactorial etiologic hypothesis. Neurology 43: 1173-1180, 1993.
108. Serpell LC, Berriman J, Jakes R, Goedert M, and Crowther RA. Fiber diffraction of synthetic alpha-synuclein filaments shows amyloid-like cross-beta conformation. Proc Natl Acad Sci U S A 97: 4897-4902, 2000.
109. Simuni T and Hurtig HI. Parkinson's disease: the clinical picture. In: Neurodegenerative Dementias, edited by Clark CM and Trojanoswki JQ. New York: McGraw-Hill, 2000, pp. 193-203.
110. Singleton AB, Farrer M, Johnson J, Singleton A, Hague S, Kachergus J, Hulihan M, Peuralinna T, Dutra A, Nussbaum R, Lincoln S, Crawley A, Hanson M, Maraganore D, Adler C, Cookson MR, Muenter M, Baptista M, Miller D, Blancato J, Hardy J, and Gwinn-Hardy K. Alpha-synuclein locus triplication causes Parkinson's disease. Science 302: 841, 2003.
111. Smith MA, Richey Harris PL, Sayre LM, Beckman JS, and Perry G. Widespread peroxynitrite-mediated damage in Alzheimer's disease. J Neurosci 17: 2653-2657, 1997.
112. Smythies J and Galzigna L. The oxidative metabolism of catecholamines in the brain: a review. Biochim Biophys Acta 1380: 159-162, 1998.
113. Souza JM, Giasson BI, Chen Q, Lee VM-Y, and Ischiropoulos H. Dityrosine cross-linking promotes formation of stable alpha-synuclein polymers. Implication of nitrative and oxidative stress in the pathogenesis of neurodegenerative synucleinopathies. J Biol Chem 275: 18344-18349, 2000.
114. Spillantini MG, Schmidt ML, Lee VM-Y, Trojanowski JQ, Jakes R, and Goedert M. Alpha-synuclein in Lewy bodies. Nature 388: 839-840, 1997.
115. Spillantini MG, Crowther RA, Jakes R, Cairns NJ, Lantos PL, and Goedert M. Filamentous alpha-synuclein inclusions link multiple system atrophy with Parkinson's disease and dementia with Lewy bodies. Neurosci Lett 251: 205-208, 1998.
116. Spillantini MG, Crowther RA, Jakes R, Hasegawa M, and Goedert M. Alpha-synuclein in filamentous inclusions of Lewy bodies from Parkinson's disease and dementia with Lewy bodies. Proc Natl Acad Sci U S A 95: 6469-6473, 1998.
117. Spira PJ, Sharpe DM, Halliday G, Cavanagh J, and Nicholson GA. Clinical and pathological features of a parkinsonian syndrome in a family with an Ala53Thr alpha-synuclein mutation. Ann Neurol 49: 313-319, 2001.
118. Stadtman ER. Protein oxidation and aging. Science 257: 1220-1224, 1992.
119. Takeda A, Hashimoto M, Mallory M, Sundsumo M, Hansen L, and Masliah E. C-terminal alpha-synuclein immunoreactivity in structures other than Lewy bodies in neurodegenerative disorders. Acta Neuropathol (Berl) 99: 296-304, 2000.
120. Tanner CM and Goldman SM. Epidemiology of Parkinson's disease. Neurol Clin 14: 317-335, 1996.
121. Tu PH, Calvin JE, Baba M, Giasson B, Tomita T, Leight S, Nakajo S, Iwatsubo T, Trojanowski JQ, and Lee VM-Y. Glial cytoplasmic inclusions in white matter oligodendrocytes of multiple system atrophy brains contain insoluble alpha-synuclein. Ann Neurol 44: 415-422, 1998.
122. Uversky VN, Li J, and Fink AL. Metal-triggered structural transformations, aggregation, and fibrillation of human alpha-synuclein. J Biol Chem 276: 44284-44296, 2001.
123. Uversky VN, Yamin G, Souillac PO, Goers J, Glaser CB, and Fink AL. Methionine oxidation inhibits fibrillation of human α-synuclein in vitro. FEBS Lett 517: 239-244, 2002.
124. Volles MJ, Lee S-J, Rochet J-C, Shtilerman MD, Ding TT, Kessler JC, and Lansbury, PT. Vesicle permeabilization by protofibrillar α-synuclein: implications for the pathogenesis and treatment of Parkinson's disease. Biochemistry 40: 7812-7819, 2001.
125. Wakabayashi K, Yoshimoto M, Tsuji S, and Takahashi H. Alpha-synuclein immunoreactivity in glial cytoplasmic inclusions in multiple system atrophy. Neurosci Lett 249: 180-182, 1998.
126. Weinreb PH, Zhen W, Poon AW, Conway KA, and Lansbury PT. NACP, a protein implicated in Alzheimer's disease and learning, is natively unfolded. Biochemistry 35: 13709-13715, 1996.
127. Wenning GK, Ben Shlomo Y, Magalhaes M, Daniel SE, and Quinn NP. Clinical features and natural history of multiple system atrophy. An analysis of 100 cases. Brain 117 (Pt 4): 835-845, 1994.
128. Wenning GK, Tison F, Ben Shlomo Y, Daniel SE, and Quinn NP. Multiple system atrophy: a review of 203 pathologically proven cases. Mov Disord 12: 133-147, 1997.
129. Whitehouse PJ, Hedreen JC, White CL, and Price DL. Basal forebrain neurons in the dementia of Parkinson's disease. Ann Neurol 13: 243-248, 1983.
130. Wilson DM and Binder LI. Free fatty acids stimulate the polymerization of tau and amyloid beta peptides. In vitro evidence for a common effector of pathogenesis in Alzheimer's disease. Am J Pathol 150: 2181-2195, 1997.
131. Withers GS, George JM, Banker GA, and Clayton DF. Delayed localization of synelfin (synuclein, NACP) to presynaptic terminals in cultured rat hippocampal neurons. Brain Res Dev Brain Res 99: 87-94, 1997.
132. Wood SJ, Wypych J, Steavenson S, Louis JC, Citron M, and Biere AL. Alpha-synuclein fibrillogenesis is nucleation-dependent. Implications for the pathogenesis of Parkinson's disease. J Biol Chem 274: 19509-19512, 1999.
133. Yamin G, Glaser CB, Uversky VN, and Fink AL. Certain metals trigger fibrillation of methionine-oxidized alpha-synuclein. J Biol Chem 278: 27630-27635, 2003.
134. Yamin G, Uversky VN, and Fink AL. Nitration inhibits fibrillation of human alpha-synuclein in vitro by formation of soluble oligomers. FEBS Lett 542: 147-152, 2003.
135. Zarranz JJ, Alegre J, Gomez-Esteban JC, Lezcano E, Ros R, Ampuero I, Vidal L, Hoenicka J, Rodriguez O, Atares B, Llorens V, Gomez TE, del Ser T, Munoz DG, and de Yebenes JG. The new mutation, E46K, of alpha-synuclein causes Parkinson and Lewy body dementia. Ann Neurol 55: 164-173, 2004.
136. Zhou B, Westaway SK, Levinson B, Johnson MA, Gitschier J, and Hayflick SJ. A novel pantothenate kinase gene (PANK.2) is defective in Hallervorden-Spatz syndrome. Nat Genet 28: 345-349, 2001.