Neurotoxicant-induced animal models of Parkinson's disease: Understanding the role of rotenone, maneb and paraquat in neurodegeneration

Cell and Tissue Research

Volumn 318, Issue 1, 2004, Pages 225-241

  Uversky, Vladimir N ^a,b  

^a INSTITUTE FOR BIOLOGICAL INSTRUMENTATION   (Russian Federation)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Synuclein; Agricultural chemicals; Animal models; Neurodegeneration; Neurotoxicity; Parkinson's disease

Indexed keywords

1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; AGRICULTURAL CHEMICAL; ALPHA SYNUCLEIN; ANTIPARKINSON AGENT; DOPAMINE RECEPTOR STIMULATING AGENT; HERBICIDE; HYDROGEN PEROXIDE; LEVODOPA; MANEB; NEUROTOXIN; OXIDOPAMINE; PARAQUAT; PESTICIDE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); ROTENONE;

ACUTE TOXICITY; ANIMAL MODEL; APOPTOSIS; CYTOTOXICITY; DEGENERATIVE DISEASE; ENVIRONMENTAL EXPOSURE; HUMAN; HUMAN CELL; MICROGLIA; NEUROLOGIC DISEASE; NEUROTOXICITY; NONHUMAN; OXIDATIVE STRESS; PARKINSON DISEASE; PATHOGENESIS; PRIORITY JOURNAL; REVIEW;

ANIMALS; DISEASE MODELS, ANIMAL; FUNGICIDES, INDUSTRIAL; HERBICIDES; MANEB; NERVE DEGENERATION; NEUROTOXINS; PARAQUAT; PARKINSON DISEASE; ROTENONE; UNCOUPLING AGENTS;

ANIMALIA; RODENTIA;

EID: 5444255433     PISSN: 0302766X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00441-004-0937-z     Document Type: Review

References (171)

1. Ahmadi FA, Linseman DA, Grammatopoulos TN, Jones SM, Bouchard RJ, Freed CR, Heidenreich KA, Zawada WM (2003) The pesticide rotenone induces caspase-3-mediated apoptosis in ventral mesencephalic dopaminergic neurons. J Neurochem 87:914-921
2. Alam M, Schmidt WJ (2002) Rotenone destroys dopaminergic neurons and induces parkinsonian symptoms in rats. Behav Brain Res 136:317-324
3. Alam ZI, Daniel SE, Lees AJ, Marsden DC, Jenner P, Halliwell B (1997a) A generalised increase in protein carbonyls in the brain in Parkinson's but not incidental Lewy body disease. J Neurochem 69:1326-1329
4. Alam ZI, Jenner A, Daniel SE, Lees AJ, Cairns N, Marsden CD, Jenner P, Halliwell B (1997b) Oxidative DNA damage in the parkinsonian brain: an apparent selective increase in 8-hydroxyguanine levels in substantia nigra. J Neurochem 69:1196-1203
5. Altschuler E (1999) Aluminum-containing antacids as a cause of idiopathic Parkinson's disease. Med Hypotheses 53:22-23
6. Armstrong JS, Hornung B, Lecane P, Jones DP, Knox SJ (2001) Rotenone-induced G2/M cell cycle arrest and apoptosis in a human B lymphoma cell line PW. Biochem Biophys Res Commun 289:973-978
7. Ascherio A, Zhang SMM, Hernan MA, Kawachi I, Colditz GA, Speizer FE, Willett WC (2001) Prospective study of caffeine consumption and risk of Parkinson's disease in men and women. Ann Neurol 50:56-63
8. Aschner M (2000) Manganese: brain transport and emerging research needs. Environ Health Perspect 108 (Suppl 3):429-432
9. Beal MF (2003) Mitochondria, oxidative damage, and inflammation in Parkinson's disease. Ann N Y Acad Sci 991:120-131
10. Betarbet R, Sherer TB, MacKenzie G, Garcia-Osuna M, Panov AV, Greenamyre JT (2000) Chronic systemic pesticide exposure reproduces features of Parkinson's disease. Nat Neurosci 3:1301-1306
11. Betarbet R, Sherer TB, Greenamyre JT (2002) Animal models of Parkinson's disease. Bioessays 24:308-318
12. Bismuth C, Garnier R, Baud FJ, Muszynski J, Keyes C (1990) Paraquat poisoning. An overview of the current status. Drug Saf 5:243-251
13. Bloem BR, Irwin I, Buruma OJ, Haan J, Roos RA, Tetrud JW, Langston JW (1990) The MPTP model: versatile contributions to the treatment of idiopathic Parkinson's disease. J Neurol Sci 97:273-293
14. Bonifati V, Rizzu P, Baren MJ van, Schaap O, Breedveld GJ, Krieger E, Dekker MC, Squitieri F, Ibanez P, Joosse M, Dongen JW van, Vanacore N, Swieten JC van, Brice A, Meco G, Duijn CM van, Oostra BA, Heutink P (2003) Mutations in the DJ-1 gene associated with autosomal recessive early-onset parkinsonism. Science 299:256-259
15. Brooks AI, Chadwick CA, Gelbard HA, Cory-Slechta DA, Federoff HJ (1999) Paraquat elicited neurobehavioral syndrome caused by dopaminergic neuron loss. Brain Res 823:1-10
16. Burke RE (1999) Alpha-synuclein and Parkinson's disease. Brain Res Bull 50:465-466
17. Calne DB, Langston JW (1983) Aetiology of Parkinson's disease. Lancet II:1457-1459
18. Carpenter DO (2001) Effects of metals on the nervous system of humans and animals. Int J Occup Med Environ Health 14:209-218
19. Chauvin C, De Oliveira F, Ronot X, Mousseau M, Leverve X, Fontaine E (2001) Rotenone inhibits the mitochondrial permeability transition-induced cell death in U937 and KB cells. J Biol Chem 276:41394-41398
20. Corasaniti MT, Strongoli MC, Rotiroti D, Bagetta G, Nistico G (1998) Paraquat: a useful tool for the in vivo study of mechanisms of neuronal cell death. Pharmacol Toxicol 83:1-7
21. Davis GC, Williams AC, Markey SP, Ebert MH, Caine ED, Reichert CM, Kopin IJ (1979) Chronic Parkinsonism secondary to intravenous injection of meperidine analogues. Psychiatry Res 1:249-254
22. Davis LE, Adair JC (1999) Parkinsonism from methanol poisoning: benefit from treatment with anti-Parkinson drugs. Mov Disord 14:520-522
23. Dev KK, Hofele K, Barbieri S, Buchman VL, Putten H van der (2003) Part II: alpha-synuclein and its molecular pathophysiological role in neurodegenerative disease. Neuropharmacology 45:14-44
24. Dexter DT, Carter CJ, Wells FR, Javoy-Agid F, Agid Y, Lees A, Jenner P, Marsden CD (1989) Basal lipid peroxidation in substantia nigra is increased in Parkinson's disease. J Neurochem 52:381-389
25. Dickson DW (2001) Alpha-synuclein and the Lewy body disorders. Curr Opin Neurol 14:423-432
26. Di Monte DA (2001) The role of environmental agents in Parkinson's disease. Clin Neurosci Res 1:419-426
27. Di Monte DA (2003) The environment and Parkinson's disease: is the nigrostriatal system preferentially targeted by neurotoxins? Lancet Neurol 2:531-538
28. Di Monte D, Sandy MS, Ekstrom G, Smith MT (1986) Comparative-studies on the mechanisms of paraquat and 1-methyl-4-phenylpyridine (Mpp+) cytotoxicity. Biochem Biophys Res Commun 137:303-309
29. Di Monte DA, Lavasani M, Manning-Bog AB (2002) Environmental factors in Parkinson's disease. Neurotoxicology 23:487-502
30. Duan W, Rangnekar VM, Mattson MP (1999a) Prostate apoptosis response-4 production in synaptic compartments following apoptotic and excitotoxic insults: evidence for a pivotal role in mitochondrial dysfunction and neuronal degeneration. J Neurochem 72:2312-2322
31. Duan W, Zhang Z, Gash DM, Mattson MP (1999b) Participation of prostate apoptosis response-4 in degeneration of dopaminergic neurons in models of Parkinson's disease. Ann Neurol 46:587-597
32. Duda JE, Giasson BI, Chen Q, Gur TL, Hurtig HI, Stern MB, Gollomp SM, Ischiropoulos H, Lee VM, Trojanowski JQ (2000) Widespread nitration of pathological inclusions in neurodegenerative synucleinopathies. Am J Pathol 157:1439-1445
33. Fall PA, Fredrikson M, Axelson O, Granerus AK (1999) Nutritional and occupational factors influencing the risk of Parkinson's disease: a case-control study in southeastern Sweden. Mov Disord 14:28-37
34. Faull RL, Laverty R (1969) Changes in dopamine levels in the corpus striatum following lesions in the substantia nigra. Exp Neurol 23:332-340
35. Ferraz HB, Bertolucci PH, Pereira JS, Lima JG, Andrade LA (1988) Chronic exposure to the fungicide maneb may produce symptoms and signs of CNS manganese intoxication. Neurology 38:550-553
36. Floor E, Wetzel MG (1998) Increased protein oxidation in human substantia nigra pars compacta in comparison with basal ganglia and prefrontal cortex measured with an improved dinitrophenylhydrazine assay. J Neurochem 70:268-275
37. Floyd RA (1999) Antioxidants, oxidative stress, and degenerative neurological disorders. Proc Soc Exp Biol Med 222:236-245
38. Fontaine E, Eriksson O, Ichas F, Bernardi P (1998) Regulation of the permeability transition pore in skeletal muscle mitochondria. Modulation by electron flow through the respiratory chain complex I. J Biol Chem 273:12662-12668
39. Forno LS (1996) Neuropathology of Parkinson's disease. J Neuropathol Exp Neurol 55:259-272
40. Forno LS, Langston JW, DeLanney LE, Irwin I, Ricaurte GA (1986) Locus ceruleus lesions and eosinophilic inclusions in MPTP-treated monkeys. Ann Neurol 20:449-455
41. Gao HM, Hong JS, Zhang W, Liu B (2002) Distinct role for microglia in rotenone-induced degeneration of dopaminergic neurons. J Neurosci 22:782-790
42. Gao HM, Hong JS, Zhang W, Liu B (2003a) Synergistic dopaminergic neurotoxicity of the pesticide rotenone and inflammogen lipopolysaccharide: relevance to the etiology of Parkinson's disease. J Neurosci 23:1228-1236
43. Gao HM, Liu B, Hong JS (2003b) Critical role for microglial NADPH oxidase in rotenone-induced degeneration of dopaminergic neurons. J Neurosci 23:6181-6187
44. Gasser T (1998) Genetics of Parkinson's disease. Ann Neurol 44:53-57
45. Gasser T (2001) Genetics of Parkinson's disease. J Neurol 248:833-840
46. Gerber GB, Leonard A, Hantson P (2002) Carcinogenicity, mutagenicity and teratogenicity of manganese compounds. Crit Rev Oncol Hematol 42:25-34
47. Giasson BI, Duda JE, Murray IV, Chen Q, Souza JM, Hurtig HI, Ischiropoulos H, Trojanowski JQ, Lee VM (2000) Oxidative damage linked to neurodegeneration by selective alpha-synuclein nitration in synucleinopathy lesions. Science 290:985-989
48. Goedert M (2001a) Alpha-synuclein and neurodegenerative diseases. Nat Rev Neurosci 2:492-501
49. Goedert M (2001b) Parkinson's disease and other alpha-synucleinopathies. Clin Chem Lab Med 39:308-312
50. Good PF, Olanow CW, Perl DP (1992) Neuromelanin-containing neurons of the substantia nigra accumulate iron and aluminum in Parkinson's disease: a LAMMA study. Brain Res 593:343-346
51. Good PF, Hsu A, Werner P, Perl DP, Olanow CW (1998) Protein nitration in Parkinson's disease. J Neuropathol Exp Neurol 57:338-342
52. Gorell JM, Johnson CC, Rybicki BA, Peterson EL, Richardson RJ (1998) The risk of Parkinson's disease with exposure to pesticides, farming, well water, and rural living. Neurology 50:1346-1350
53. Gorell JM, Johnson CC, Rybicki BA, Peterson EL, Kortsha GX, Brown GG, Richardson RJ (1999) Occupational exposure to manganese, copper, lead, iron, mercury and zinc and the risk of Parkinson's disease. Neurotoxicology 20:239-247
54. Greenamyre JT, Sherer TB, Betarbet R, Panov AV (2001) Complex I and Parkinson's disease. IUBMB Life 52:135-141
55. Guenebaut V, Vincentelli R, Mills D, Weiss H, Leonard KR (1997) Three-dimensional structure of NADH-dehydrogenase from Neurospora crassa by electron microscopy and conical tilt reconstruction. J Mol Biol 265:409-418
56. Hageman G, Hoek JAF van der, Hout M van, Laan G van der, Steur EJ, Bruin W de, Herholz K (1999) Parkinsonism, pyramidal signs, polyneuropathy, and cognitive decline after long-term occupational solvent exposure. J Neurol 246:198-206
57. Kara S, Endo T, Kuriiwa F, Kano S (1991a) Different effects of paraquat on microsomal lipid peroxidation in mouse brain, lung and liver. Pharmacol Toxicol 68:260-265
58. Hara S, Endo T, Kuriiwa F, Kano S (1991b) Effects of MPTP, MPP +, and paraquat on NADPH-dependent lipid peroxidation in mouse brain and lung microsomes. Biochem Med Metab Biol 45:292-297
59. Hara S, Endo T, Kuriiwa F, Kano S (1991c) Interaction between dual NADPH-dependent reactions of paraquat in mouse brain microsomes. Res Commun Chem Pathol Pharmacol 73:119-122
60. Hara S, Endo T, Kuriiwa F, Kano S (1991d) Mechanism of paraquat-stimulated lipid peroxidation in mouse brain and pulmonary microsomes. J Pharm Pharmacol 43:731-733
61. Hashimoto M, Hsu LJ, Xia Y, Takeda A, Sisk A, Sundsmo M, Masliah E (1999) Oxidative stress induces amyloid-like aggregate formation of NACP/alpha-synuclein in vitro. Neuroreport 10:717-721
62. Hastings TG, Lewis DA, Zigmond MJ (1996) Role of oxidation in the neurotoxic effects of intrastriatal dopamine injections. Proc Natl Acad Sci USA 93:1956-1961
63. Hatefi Y (1985) The mitochondrial electron transport and oxidative phosphorylation system. Annu Rev Biochem 54:1015-1069
64. Hellenbrand W, Boeing H, Robra BP, Seidler A, Vieregge P, Nischan P, Joerg J, Oertel WH, Schneider E, Ulm G (1996) Diet and Parkinson's disease. II. A possible role for the past intake of specific nutrients. Results from a self-administered food-frequency questionnaire in a case-control study. Neurology 47:644-650
65. Hensley K, Pye QN, Maidt ML, Stewart CA, Robinson KA, Jaffrey F, Floyd RA (1998) Interaction of alpha-phenyl-N-tert-butyl nitrone and alternative electron acceptors with complex I indicates a substrate reduction site upstream from the rotenone binding site. J Neurochem 71:2549-2557
66. Hertzman C, Wiens M, Snow B, Kelly S, Calne D (1994) A case-control study of Parkinson's disease in a horticultural region of British Columbia. Mov Disord 9:69-75
67. Higgins DS Jr, Greenamyre JT (1996) [3H]Dihydrorotenone binding to NADH: ubiquinone reductase (complex I) of the electron transport chain: an autoradiographic study. J Neurosci 16:3807-3816
68. Hirsch EC, Brandel JP, Galle P, Javoy-Agid F, Agid Y (1991) Iron and aluminum increase in the substantia nigra of patients with Parkinson's disease: an X-ray microanalysis. J Neurochem 56:446-451
69. Hoglinger GU, Feger J, Prigent A, Michel PP, Parain K, Champy P, Ruberg M, Oertel WH, Hirsch EC (2003) Chronic systemic complex I inhibition induces a hypokinetic multisystem degeneration in rats. J Neurochem 84:491-502
70. Ischiropoulos H, Beckman JS (2003) Oxidative stress and nitration in neurodegeneration: cause, effect, or association? J Clin Invest 111:163-169
71. Isenberg JS, Klaunig JE (2000) Role of the mitochondrial membrane permeability transition (MPT) in rotenone-induced apoptosis in liver cells. Toxicol Sci 53:340-351
72. Jenner P (1998) Oxidative mechanisms in nigral cell death in Parkinson's disease. Mov Disord 13 (Suppl 1):24-34
73. Jenner P (2003) Oxidative stress in Parkinson's disease. Ann Neurol 53 (Suppl 3):S26-S36
74. Jones GM, Vale JA (2000) Mechanisms of toxicity, clinical features, and management of diquat poisoning: a review. J Toxicol Clin Toxicol 38:123-128
75. Jonsson G, Sachs C (1975) Actions of 6-hydroxydopamine quinones on catecholamine neurons. J Neurochem 25:509-516
76. Kiechle FL, Zhang X (2002) Apoptosis: biochemical aspects and clinical implications. Clin Chim Acta 326:27-45
77. Kim WG, Mohney RP, Wilson B, Jeohn GH, Liu B, Hong JS (2000) Regional difference in susceptibility to lipopolysaccharide-induced neurotoxicity in the rat brain: role of microglia. J Neurosci 20:6309-6316
78. Kitada T, Asakawa S, Hattori N, Matsumine H, Yamamura Y, Minoshima S, Yokochi M, Mizuno Y, Shimizu N (1998) Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature 392:605-608
79. Kitamura Y, Shimohama S, Akaike A, Taniguchi T (2000) The parkinsonian models: invertebrates to mammals. Jpn J Pharmacol 84:237-243
80. Klawans HL, Stein RW, Tanner CM, Goetz CG (1982) A pure parkinsonian syndrome following acute carbon monoxide intoxication. Arch Neurol 39:302-304
81. Kruger R, Kuhn W, Muller T, Woitalla D, Graeber M, Kosel S, Przuntek H, Epplen JT, Schols L, Riess O (1998) Ala30Pro mutation in the gene encoding alpha-synuclein in Parkinson's disease. Nat Genet 18:106-108
82. Kushnareva Y, Murphy AN, Andreyev A (2002) Complex I-mediated reactive oxygen species generation: modulation by cytochrome c and NAD(P)+oxidation- reduction state. Biochem J 368:545-553
83. Lang AE, Lozano AM (1998) Parkinson's disease-first of two parts. N Engl J Med 339:1044-1053
84. Langston JW (1996) The etiology of Parkinson's disease with emphasis on the MPTP story. Neurology 47:8153-8160
85. Langston JW, Ballard PA (1983) Parkinsons-disease in a chemist working with 1-methyl-4-phenyl-1,2,5,6-tetrahydropyridine. N Engl J Med 309:310
86. Langston JW, Ballard P, Tetrud JW, Irwin I (1983) Chronic Parkinsonism in humans due to a product of meperidine-analog synthesis. Science 219:979-980
87. Langston JW, Forno LS, Tetrud J, Reeves AG, Kaplan JA, Karluk D (1999) 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 46:598-605
88. Lapointe N, St Hilaire M, Martinoli MG, Blanchet J, Gould P, Rouillard C, Cicchetti F (2004) Rotenone induces non-specific central nervous system and systemic toxicity. FASEB J 18:117-119
89. Levy BS, Nassetta WJ (2003) Neurologic effects of manganese in humans: a review. Int J Occup Environ Health 9:153-163
90. Lewy FH (1912) Paralysis agitans. Pathologische Anatomie. In: Lewandowski M (ed) Handbuch der Neurologie. Springer, Berlin Heidelberg New York, pp 920-933
91. Liou HH, Tsai MC, Chen CJ, Jeng JS, Chang YC, Chen SY, Chen RC (1997) Environmental risk factors and Parkinson's disease: a case-control study in Taiwan. Neurology 48:1583-1588
92. Lyras L, Perry RH, Perry EK, Ince PG, Jenner A, Jenner P, Halliwell B (1998) Oxidative damage to proteins, lipids, and DNA in cortical brain regions from patients with dementia with Lewy bodies. J Neurochem 71:302-312
93. Manning-Bog AB, McCormack AL, Li J, Uversky VN, Fink AL, Di Monte DA (2002) The herbicide paraquat causes up-regulation and aggregation of alpha-synuclein in mice-paraquat and alpha-synuclein. J Biol Chem 277:1641-1644
94. Marder K, Logroscino G, Alfaro B, Mejia H, Halim A, Louis E, Cote L, Mayeux R (1998) Environmental risk factors for Parkinson's disease in an urban multiethnic community. Neurology 50:279-281
95. Maries E, Dass B, Collier TJ, Kordower JH, Steece-Collier K (2003) The role of alpha-synuclein in Parkinson's disease: insights from animal models. Nat Rev Neurosci 4:727-738
96. Martyn C, Gale C (2003) Tobacco, coffee, and Parkinson's disease - caffeine and nicotine may improve the health of dopaminergic systems. BMJ 326:561-562
97. Mattson MP, Duan W (1999) "Apoptotic" biochemical cascades in synaptic compartments: roles in adaptive plasticity and neurodegenerative disorders. J Neurosci Res 58:152-166
98. McCormack AL, Thiruchelvam M, Manning-Bog AB, Thiffault C, Langston JW, Cory-Slechta DA, Di Monte DA (2002) Environmental risk factors and Parkinson's disease: selective degeneration of nigral dopaminergic neurons caused by the herbicide paraquat. Neurobiol Dis 10:119-127
99. McGeer PL, Itagaki S, Boyes BE, McGeer EG (1988) Reactive microglia are positive for HLA-DR in the substantia nigra of Parkinson's and Alzheimer's disease brains. Neurology 38:1285-1291
100. McGrew DM, Irwin I, Langston JW (2000) Ethylenebisdithiocarbamate enhances MPTP-induced striatal dopamine depletion in mice. Neurotoxicology 21:309-312
101. Meco G, Bonifati V, Vanacore N, Fabrizio E (1994) Parkinsonism after chronic exposure to the fungicide maneb (manganese ethylene-bis-dithiocarbamate) . Scand J Work Environ Health 20:301-305
102. Menegon A, Board PG, Blackburn AC, Mellick GD, Le Couteur DG (1998) Parkinson's disease, pesticides, and glutathione transferase polymorphisms. Lancet 352:1344-1346
103. Morano A, Jimenez-Jimenez FJ, Molina JA, Antolin MA (1994) Risk-factors for Parkinson's disease: case-control study in the province of Caceres, Spain. Acta Neurol Scand 89:164-170
104. Morato GS, Lemos T, Takahashi RN (1989) Acute exposure to maneb alters some behavioral functions in the mouse. Neurotoxicol Teratol 11:421-425
105. Nicklas WJ, Vyas I, Heikkila RE (1985) 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 36:2503-2508
106. Nicolaou K, Pfefferkorn J, Schuler F, Roecker A, Cao G, Casida J (2000) Combinatorial synthesis of novel and potent inhibitors of NADH:ubiquinone oxidoreductase. Chem Biol 7:979-992
107. Orth M, Tabrizi SJ (2003) Models of Parkinson's disease. Mov Disord 18:729-737
108. Paganini-Hill A (2001) Risk factors for Parkinson's disease: the Leisure World cohort study. Neuroepidemiology 20:118-124
109. Pearce RK, Owen A, Daniel S, Jenner P, Marsden CD (1997) Alterations in the distribution of glutathione in the substantia nigra in Parkinson's disease. J Neural Transm 104:661-677
110. Perier C, Bove J, Vila M, Przedborski S (2003) The rotenone model of Parkinson's disease. Trends Neurosci 26:345-346
111. Perry TL, Yong VW, Wall RA, Jones K (1986) Paraquat and two endogenous analogues of the neurotoxic substance N-methyl-4-phenyl-1,2,3,6- tetrahydropyridine do not damage dopaminergic nigrostriatal neurons in the mouse. Neurosci Lett 69:285-289
112. Pezzoli G, Strada O, Silani V, Zecchinelli A, Perbellini L, Javoy-Agid F, Ghidoni P, Motti ED, Masini T, Scarlato G, Agid Y, Hirsch EC (1996) Clinical and pathological features in hydrocarbon-induced parkinsonism. Ann Neurol 40:922-925
113. Piccini P, Burn DJ, Ceravolo R, Maraganore D, Brooks DJ (1999) The role of inheritance in sporadic Parkinson's disease: evidence from a longitudinal study of dopaminergic function in twins. Ann Neurol 45:577-582
114. 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, Nussbaum RL (1997) Mutation in the alpha-synuclein gene identified in families with Parkinson's disease. Science 276:2045-2047
115. Ragonese P, Salemi G, Morgante L, Aridon P, Epifanio A, Buffa D, Scoppa F, Savettieri G (2003) A case-control study on cigarette, alcohol, and coffee consumption preceding Parkinson's disease. Neuroepidemiology 22:297-304
116. Raivich G, Jones LL, Werner A, Bluthmann H, Doetschmann T, Kreutzberg GW (1999) Molecular signals for glial activation: pro- and anti-inflammatory cytokines in the injured brain. Acta Neurochir Suppl (Wien) 73:21-30
117. Robinson BH (1998) Human complex I deficiency: clinical spectrum and involvement of oxygen free radicals in the pathogenicity of the defect. Biochim Biophys Acta 1364:271-286
118. Ross GW, Petrovitch H (2001) Current evidence for neuroprotective effects of nicotine and caffeine against Parkinson's disease. Drugs Aging 18:797-806
119. Ross GW, Abbott RD, Petrovitch H, Morens DM, Grandinetti A, Tung KH, Tanner CM, Masaki KH, Blanchette PL, Curb JD, Popper JS, White LR (2000) Association of coffee and caffeine intake with the risk of Parkinson disease. J Am Med Assoc 283:2674-2679
120. Sachs C, Jonsson G (1975) Mechanisms of action of 6-hydroxydopamine. Biochem Pharmacol 24:1-8
121. Sakka N, Sawada H, Izumi Y, Kume T, Katsuki H, Kaneko S, Shimohama S, Akaike A (2003) Dopamine is involved in selectivity of dopaminergic neuronal death by rotenone. Neuroreport 14:2425-2428
122. Schapira AH (1994) Mitochondrial function and neurotoxicity. Curr Opin Neurol 7:531-534
123. Schapira AH, Cooper JM, Dexter D, Clark JB, Jenner P, Marsden CD (1990) Mitochondrial complex I deficiency in Parkinson's disease. J Neurochem 54:823-827
124. Schuler F, Casida JE (2001) Functional coupling of PSST and ND1 subunits in NADH:ubiquinone oxidoreductase established by photoaffinity labeling. Biochim Biophys Acta 1506:79-87
125. Schwarzschild MA, Chen JF, Tennis M, Messing S, Kamp C, Ascherio A, Holloway RG, Marek K, Tanner CM, McDermott M, Lang AE (2003) Relating caffeine consumption to Parkinson's disease progression and dyskinesias development. Mov Disord 18:1082-1083
126. Seidler A, Hellenbrand W, Robra BP, Vieregge P, Nischan P, Joerg J, Oertel WH, Ulm G, Schneider E (1996) Possible environmental, occupational, and other etiologic factors for Parkinson's disease: a case-control study in Germany. Neurology 46:1275-1284
127. Semchuk KM, Love EJ, Lee RG (1992) Parkinson's disease and exposure to agricultural work and pesticide chemicals. Neurology 42:1328-1335
128. Semchuk KM, Love EJ, Lee RG (1993) Parkinson's disease: a test of the multifactorial etiologic hypothesis. Neurology 43:1173-1180
129. Sherer TB, Betarbet R, Kim JH, Greenamyre JT (2003a) Selective microglial activation in the rat rotenone model of Parkinson's disease. Neurosci Lett 341:87-90
130. Sherer TB, Betarbet R, Testa CM, Seo BB, Richardson JR, Kim JH, Miller GW, Yagi T, Matsuno-Yagi A, Greenamyre JT (2003b) Mechanism of toxicity in rotenone models of Parkinson's disease. J Neurosci 23:10756-10764
131. Sherer TB, Kim JH, Betarbet R, Greenamyre JT (2003c) Subcutaneous rotenone exposure causes highly selective dopaminergic degeneration and alpha-synuclein aggregation. Exp Neurol 179:9-16
132. Shimizu K, Matsubara K, Ohtaki K, Fujimaru S, Saito O, Shiono H (2003a) Paraquat induces long-lasting dopamine overflow through the excitotoxic pathway in the striatum of freely moving rats. Brain Res 976:243-252
133. Shimizu K, Matsubara K, Ohtaki K, Shiono H (2003b) Paraquat leads to dopaminergic neural vulnerability in organotypic midbrain culture. Neurosci Res 46:523-532
134. 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, Gwinn-Hardy K (2003) Alpha-synuclein locus triplication causes Parkinson's disease. Science 302:841
135. Sjoerdsma A, Engelman K, Specter S, Udenfriend S (1965) Inhibition of catecholamine synthesis in man with alpha-methyl-tyrosine, an inhibitor of tyrosine hydroxylase. Lancet II:1092-1094
136. Soleo L, Defazio G, Scarselli R, Zefferino R, Livrea P, Foa V (1996) Toxicity of fungicides containing ethylene-bis-dithiocarbamate in serumless dissociated mesencephalic-striatal primary coculture. Arch Toxicol 70:678-682
137. Spector S, Sjoerdsma A, Udenfriend S (1965) Blokade of endogenous norepinephrine synthesis by alpha-methyl-tyrosine, an inhibitor of tyrosine hydrolase. J Pharmacol Exp Ther 147:86-95
138. Spillantini MG, Schmidt ML, Lee VM, Trojanowski JQ, Jakes R, Goedert M (1997) Alpha-synuclein in Lewy bodies. Nature 388:839-840
139. Spillantini MG, Crowther RA, Jakes R, Hasegawa M, Goedert M (1998) α-Synuclein in filamentous inclusions of Lewy bodies from Parkinson's disease and dementia with Lewy bodies. Proc Natl Acad Sci USA 95:6469-6473
140. Stokes AH, Hastings TG, Vrana KE (1999) Cytotoxic and genotoxic potential of dopamine. J Neurosci Res 55:659-665
141. Sveinbjornsdottir S, Hicks AA, Jonsson T, Petursson H, Gugmundsson G, Frigge ML, Kong A, Gulcher JR, Stefansson K (2000) Familial aggregation of Parkinson's disease in Iceland. N Engl J Med 343:1765-1770
142. Tada-Oikawa S, Hiraku Y, Kawanishi M, Kawanishi S (2003) Mechanism for generation of hydrogen peroxide and change of mitochondrial membrane potential during rotenone-induced apoptosis. Life Sci 73:3277-3288
143. Takahashi RN, Rogerio R, Zanin M (1989) Maneb enhances MPTP neurotoxicity in mice. Res Commun Chem Pathol Pharmacol 66:167-170
144. Takeda A (2003) Manganese action in brain function. Brain Res Brain Res Rev 41:79-87
145. Talpade DJ, Greene JG, Higgins DS Jr, Greenamyre JT (2000) In vivo labeling of mitochondrial complex I (NADH:ubiquinone oxidoreductase) in rat brain using [(3)H]dihydrorotenone. J Neurochem 75:2611-2621
146. Tan EK, Tan C, Fook-Chong SMC, Lum SY, Chai A, Chung H, Shen H, Zhao Y, Teoh ML, Yih Y, Pavanni R, Chandran VR, Wong MC (2003) Dose-dependent protective effect of coffee, tea, and smoking in Parkinson's disease: a study in ethnic Chinese. J Neurol Sci 216:163-167
147. Tanner CM (1989) The role of environmental toxins in the etiology of Parkinson's disease. Trends Neurosci 12:49-54
148. Tanner CM, Ottman R, Goldman SM, Ellenberg J, Chan P, Mayeux R, Langston JW (1999) Parkinson disease in twins: an etiologic study. J Am Med Assoc 281:341-346
149. Thiruchelvam M, Brockel BJ, Richfield EK, Baggs RB, Cory-Slechta DA (2000a) Potentiated and preferential effects of combined paraquat and maneb on nigrostriatal dopamine systems: environmental risk factors for Parkinson's disease? Brain Res 873:225-234
150. Thiruchelvam M, Richfield EK, Baggs RB, Tank AW, Cory-Slechta DA (2000b) The nigrostriatal dopaminergic system as a preferential target of repeated exposures to combined paraquat and maneb: implications for Parkinson's disease. J Neurosci 20:9207-9214
151. Thiruchelvam M, Richfield EK, Goodman BM, Baggs RB, Cory-Slechta DA (2002) Developmental exposure to the pesticides paraquat and maneb and the Parkinson's disease phenotype. Neurotoxicology 23:621-633
152. Thiruchelvam M, McCormack A, Richfield EK, Baggs RB, Tank AW, Di Monte DA, Cory-Slechta DA (2003) Age-related irreversible progressive nigrostriatal dopaminergic neurotoxicity in the paraquat and maneb model of the Parkinson's disease phenotype. Eur J Neurosci 18:589-600
153. Tieu K, Ischiropoulos H, Przedborski S (2003) Nitric oxide and reactive oxygen species in Parkinson's disease. IUBMB Life 55:329-335
154. Trojanowski JQ (2003) Rotenone neurotoxicity: a new window on environmental causes of Parkinson's disease and related brain amyloidoses. Exp Neurol 179:6-8
155. Trojanowski JQ, Lee VM (2002) Parkinson's disease and related synucleinopathies are a new class of nervous system amyloidoses. Neurotoxicology 23:457-460
156. Turrens JF, Boveris A (1980) Generation of Superoxide anion by the NADH dehydrogenase of bovine heart mitochondria. Biochem J 191:421-427
157. Ueda S, Masutani H, Nakamura H, Tanaka T, Ueno M, Yodoi J (2002) Redox control of cell death. Antioxid Redox Signal 4:405-414
158. Uitti RJ, Snow BJ, Shinotoh H, Vingerhoets FJG, Hayward M, Hashimoto S, Richmond J, Markey SP, Markey CJ, Calne DB (1994) Parkinsonism induced by solvent abuse. Ann Neurol 35:616-619
159. Ungerstedt U (1968) 6-Hydroxy-dopamine induced degeneration of central monoamine neurons. Eur J Pharmacol 5:107-110
160. Uversky VN (2003) A protein-chameleon: conformational plasticity of α-synuclein, a disordered protein involved in neurodegenerative disorders. J Biomol Struct Dyn 21:211-234
161. Uversky VN, Fink AL (2002) Biophysical properties of human α-synuclein and its role in Parkinson's disease. In: Pandalai SG (ed) Recent research developments in proteins. Transworld Research Network, Kerala, India, pp 153-186
162. Uversky VN, Li J, Fink AL (2001) Pesticides directly accelerate the rate of alpha-synuclein fibril formation: a possible factor in Parkinson's disease. FEBS Lett 500:105-108
163. Uversky VN, Li J, Bower K, Fink AL (2002) Synergistic effects of pesticides and metals on the fibrillation of α-synuclein: implications for Parkinson's disease. Neurotoxicology 23:527-536
164. Vanacore N, Nappo A, Gentile M, Brustolin A, Palange S, Liberati A, Di Rezze S, Caldora G, Gasparini M, Benedetti F, Bonifati V, Forastiere F, Quercia A, Meco G (2002) Evaluation of risk of Parkinson's disease in a cohort of licensed pesticide users. Neurol Sci 23 (Suppl 2):S119-S120
165. Vila M, Vukosavic S, Jackson-Lewis V, Neystat M, Jakowec M, Przedborski S (2000) Alpha-synuclein up-regulation in substantia nigra dopaminergic neurons following administration of the parkinsonian toxin MPTP. J Neurochem 74:721-729
166. Weiss H, Friedrich T, Hofhaus G, Preis D (1991) The respiratory-chain NADH dehydrogenase (complex I) of mitochondria. Eur J Biochem 197:563-576
167. Wooten GF (1997) Neurochemistry and neuropharmacology of Parkinson's disease. In: Watts RL (ed) Movement disorders: neurologic principles and practice. McGraw-Hill, New York, pp 153-160
168. Yasui M, Kihira T, Ota K (1992) Calcium, magnesium and aluminum concentrations in Parkinson's disease. Neurotoxicology 13:593-600
169. Yumino K, Kawakami I, Tamura M, Hayashi T, Nakamura M (2002) Paraquat- and diquat-induced oxygen radical generation and lipid peroxidation in rat brain microsomes. J Biochem (Tokyo) 131:565-570
170. 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, Ser T del, Munoz DG, Yebenes JG de (2004) The new mutation, E46K, of alpha-synuclein causes Parkinson and Lewy body dementia. Ann Neurol 55:164-173
171. Zhang J, Fitsanakis VA, Gu G, Jing D, Ao M, Amarnath V, Montine TJ (2003) Manganese ethylene-bis-dithiocarbamate and selective dopaminergic neurodegeneration in rat: a link through mitochondrial dysfunction. J Neurochem 84:336-346