Vitamin E therapy in Parkinson's disease

Toxicology

Volumn 189, Issue 1-2, 2003, Pages 129-146

  Fariss, Marc W ^a   Zhang, Jin Gang ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

Alpha tocopherol; Environment; Mitochondria; Oxidative stress; Parkinson's disease; Vitamin E; Vitamin E succinate

Indexed keywords

ADENOSINE TRIPHOSPHATE; ALPHA TOCOPHEROL; ALPHA TOCOPHEROL SUCCINATE; AMANTADINE; ASCORBIC ACID; BETA CARBOLINE DERIVATIVE; CHOLINERGIC RECEPTOR BLOCKING AGENT; COPPER; GLUTATHIONE; HERBICIDE; IRON; MANGANESE; METAL; PARAQUAT; PESTICIDE; REACTIVE OXYGEN METABOLITE;

BRAIN MITOCHONDRION; CELL PROTECTION; CLINICAL TRIAL; DIET SUPPLEMENTATION; DRUG EFFECT; DRUG EFFICACY; DRUG MECHANISM; HUMAN; NONHUMAN; OXIDATIVE STRESS; PARKINSON DISEASE; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; SUBSTANTIA NIGRA; TREATMENT OUTCOME;

EID: 0037735348     PISSN: 0300483X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0300-483X(03)00158-6     Document Type: Review

References (119)

1. Adams J.D. Jr, Wang B. Vitamin E uptake into the brain and 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine toxicity. J. Cereb. Blood Flow Metab. 14:1994;362-363.
2. Alam Z.I., Jenner A., Daniel S.E., Lees A.J., Cairns N., Marsden C.D., Jenner P., Halliwell B. Oxidative DNA damage in the Parkinsonian brain: an apparent selective increase in 8-hydroxyguanine levels in substantia nigra. J. Neurochem. 69:1997;1196-1203.
3. Barc S., Page G., Barrier L., Huguet F., Fauconneau B. Progressive alteration of neuronal dopamine transporter activity in a rat injured by an intranigral injection of MPP+. Brain Res. 941:2002;72-81.
4. Beal M.F., Matthews R.T., Tielman A., Shults C.W. Coenzyme Q10 attenuates the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) induced loss of striatal dopamine and dopaminergic axons in aged mice. Brain Res. 783:1998;109-114.
5. Berman S.B., Hastings T.G. Dopamine oxidation alters mitochondrial respiration and induces permeability transition in brain mitochondria: implications for Parkinson's disease. J. Neurochem. 73:1999;1127-1137.
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. Blatt D.H., Leonard S.W., Traber M.G. Vitamin E kinetics and the function of tocopherol regulatory proteins. Nutrition. 17:2001;799-805.
8. Burton G.W., Joyce A., Ingold K.U. Is vitamin E the only lipid-soluble, chain breaking antioxidant in human blood plasma and erythrocyte membranes? Arch. Biochem. Biophys. 221:1983;281-290.
9. Caparros-Lefebvre D., Elbaz A. Possible relation of atypical parkinsonism in the French West Indies with consumption of tropical plants: a case-control study. Caribbean Parkinsonism Study Group. Lancet. 354:1999;281-286.
10. Carini R., Giuseppe P., Dianzani M.U., Maddix S.P., Slater T.F., Cheeseman K.H. Comparative evaluation of activity of α-tocopherol, α-tocopherol polyethylene glycol 1000 succinate and α-tocopherol succinate in isolated hepatocytes and liver microsomal suspensions. Biochem. Pharmacol. 39:1990;1597-1601.
11. Cheeseman K.H., Emery S., Maddix S.P., Slater T.F., Burton G.W., Ingold K.U. Studies on lipid peroxidation in normal and tumor tissues. Biochem. J. 250:1988;247-252.
12. Chi D.S., Gong L., Daigneault E.A., Kostrzewa R.M. Effects of MPTP and vitamin E treatments on immune function in mice. Int. J. Immunopharmacol. 14:1992;739-746.
13. Chun H.S., Gibson G.E., De Giorgio L.A., Zhang H., Kidd V.J., Son J.H. Dopaminergic cell death induced by MPP(+), oxidant and specific neurotoxicants shares the common molecular mechanism. J. Neurochem. 76:2001;1010-10121.
14. Cleeter M.W., Copper J.M., Schapira A.H.V. Irreversible inhibition of mitochondrial complex I by MPTP: evidence for free radical involvement. J. Neurochem. 58:1992;786-789.
15. Cohen G., Kesler N. Monoamine oxidase and mitochondrial respiration. J. Neurochem. 73:1999;2310-2315.
16. Collins M. Alkaloids, alcohol and Parkinson's disease. Parkinsonism Relat. Disord. 8:2002;417.
17. Cox P.A., Sacks O.W. Cyad neurotoxins, consumption of flying foxes, and ALS-PDC disease in Guam. Neurology. 58:2002;956-959.
18. de Rijk M.C., Breteler M.M.B., den Breeijen J.H., Launer L.J., Grobbee D.E., van der Meche F.G.A., Hofman A. Dietary antioxidants and Parkinson's disease. The Rotterdam study. Arch. Neurol. 54:1997;762-765.
19. Duan W., Zhang Z., Gash D.M., Mattson M.P. Participation of prostate apoptosis response-4 in degeneration of dopaminergic neurons in models of Parkinson's disease. Ann. Neurol. 46:1999;587-597.
20. Eaton D., Klaassen C.D. Principles of toxicology. Klaassen C.D. Cassarett & Doull's Toxicology. 6th ed. 2001;20 McGraw-Hill, New York, NY.
21. Ebadi M., Srinivasan S.K., Baxi M.D. Oxidative stress and antioxidant therapy in Parkinson's disease. Progr. Neurobiol. 48:1996;1-19.
22. Engel L.S., Checkoway H., Keifer M.C., Seixas N.S., Longstreth W.T., Scott K.C., Hudnell K., Anger W.K., Camicioli R. Parkinsonism and occupational exposure to pesticides. Occup. Environ. Med. 58:2001;582-589.
23. Fahn S. A pilot trial of high-dose alpha-tocopherol and ascorbate in early Parkinson's disease. Ann. Neurol. 32:1992;S128-S132.
24. Fariss M.W. Oxygen toxicity: unique cytoprotective properties of vitamin E succinate in hepatocytes. Free Radic. Biol. Med. 9:1990;333-343.
25. Fariss M.W. Anionic tocopherol esters as antioxidants and cytoprotectants. Packer L., Cadenas E. Handbook of Synthetic Antioxidants. 1997;139-175 Marcel Dekker, New York.
26. Fariss M.W., Pascoe G.A., Reed D.J. Vitamin E reversal of the effect of extracellular calcium on chemically induced toxicity in hepatocytes. Science. 227:1985;751-754.
27. Fariss M.W., Merson M.H., O'Hara T.M. Alpha tocopheryl succinate protects hepatocytes from chemical-induced toxicity under physiological calcium conditions. Toxicol. Lett. 47:1989;61-75.
28. Fariss M.W., Fortuna M.B., Everett C.K., Smith J.D., Trent D.F., Djuric Z. The selective antiproliferative effects of α-tocopheryl hemisuccinate and cholesteryl hemisuccinate on murine leukemia cells result from the action of the intact compounds. Cancer Res. 54:1994;3346-3351.
29. Fariss M.W., Nicholls-Grzemski F.A., Tirmenstein M.A., Zhang J.G. Enhanced antioxidant and cytoprotective abilities of vitamin E succinate is associated with a rapid uptake advantage in rat hepatocytes and mitochondria. Free Radic. Biol. Med. 31:2001;530-541.
30. Fry M., Green D.E. Cardiolipin requirement for electron transfer in Complex I and III of the mitochondrial respiratory chains. J. Biol. Chem. 256:1981;1874-1880.
31. Gibson G.E., Park L.C.H., Sheu K.-F.R., Blass J.P., Calingasan N.Y. The alpha-ketoglutarate dehydrogenase complex in neurodegeneration. Neurochem. Int. 36:2000;97-112.
32. Gogu S.R., Lertora J.J.L., George W.J., Hyslop N.E., Agrawal K.C. Protection of zidovudine-induced toxicity against murine erythroid progenitor cells by vitamin E. Exp. Hematol. 19:1991;649-652.
33. Golbe L.I., Farrell T.M., Davis P.H. Case-control study of early life dietary factors in Parkinson's disease. Arch. Neurol. 45:1988;1350-1353.
34. Gomez C., Reiriz J., Pique M., Gil J., Ferrer I., Ambrosio S. Low concentrations of MPP ion induce caspase-mediated apoptosis in human SH-SY5Y neuroblastoma cells. J. Neurosci. Res. 63:2001;421-428.
35. Gong L., Daigneault E.A., Acuff R.V., Kostrzewa R.M. Vitamin E supplements fail to protect mice from acute MPTP neurotoxicity. NeuroReport. 2:1991;544-546.
36. Gorell J.M., Johnson C.C., Rybicki B.A., Peterson E.L., Kortsha G.X., Brown G.G., Richardson R.J. Occupational exposure to manganese, copper, lead, iron, mercury, and zinc and the risk of Parkinson's disease. Neurotoxicology. 20:1999;239-247.
37. Gorell J.M., Johnson C.C., Rybicki B.A., Peterson E.L., Richardson R.J. The risk of Parkinson's disease with exposure to pesticides, farming, well water, and rural living. Neurology. 50:1999;1346-1350.
38. Graham J.M., Paley M.N., Grunewald R.A., Hoggard N., Griffiths P.D. Brain iron deposition in Parkinson's disease imaged using the PRIME magnetic resonance sequence. Brain. 123:2000;2423-2431.
39. Hartley A., Stone J.M., Heron C., Cooper J.M., Schapira A.H.V. Complex I inhibitors induce dose-dependent apoptosis in PC12 cells: relevance to Parkinson's disease. J. Neurochem. 63:1994;1987-1990.
40. Hartmann A., Hunot S., Michel P.P., Muriel M.P., Vyas S., Faucheux B.A., Mouatt-Prigent A., Turmel H., Srinivasan A., Ruberg M., Evan G.I., et al. Caspase-3: a vulnerability factor and a final effector in the apoptotic death of dopaminergic neurons in Parkinson's disease. Proc. Natl. Acad. Sci. USA. 97:2000;2875-2880.
41. Hartmann A., Troadec J.D., Hunot S., Kikly K., Faucheux B.A., Mouatt-Prigent A., Ruberg M., Agid Y., Hirsch E.C. Caspase-8 is an effector in apoptotic death of dopaminergic neurons in Parkinson's disease, but pathway inhibition results in neuronal necrosis. J. Neurosci. 21:2001;2247-2255.
42. Hasegawa E., Takeshige K., Oishi T., Murai Y., Minakami S. MPP ion induces NADH-dependent superoxide formation and enhances NADH-dependent lipid peroxidation in bovine heart submitochondrial particles. Biochem. Biophys. Res. Commun. 170:1990;1049-1055.
43. Hellenbrand W., Boeing H., Robra B.P., Seidler A., Vieregge P., Nischan P., Joerg J., Oertel W.H., Schneider E., Ulm G. 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. 47:1996;644-650.
44. Hirai K., Ikeda K., Wang G.Y. Paraquat damage of rat liver mitochondria by superoxide production depends on extra-mitochondrial NADH. Toxicology. 72:1992;1-16.
45. Hirai K., Pahn J., Shimada H., Izuhara T., Moriguchi K. Cytochemical energy-filtering transmission electron microscopy of mitochondrial free radical formation in paraquat cytotoxicity. J. Electron Microsc. 48:1999;289-296.
46. Hovius R., Lambrechts H., Nicolay K., de Kruijff B. Improved methods to isolate and subfractionate rat liver mitochondria. Lipid composition of the inner and outer membrane. Biochim. Biophys. Acta. 1021:1990;217-226.
47. Huang C., Chu N., Lu C., Wang J., Tsai J., Tzeng J., Wolters E., Calne D. Chronic manganese intoxication. Arch. Neurol. 46:1989;1104-1106.
48. Ithayarasi A.P., Shyamala D.C. Effect of alpha-tocopherol on mitochondrial electron transport in experimental myocardial infarction in rats. Indian J. Biochem. Biophys. 35:1998;115-119.
49. Jenner P. Parkinson's disease, pesticides and mitochondrial dysfunction. Trends Neurosci. 24:2001;245-246.
50. Kirby M.L., Barlow R.L., Bloomquist J.R. Neurotoxicity of the organochlorine insecticide Heptaclor to murine striatal dopaminergic pathways. Toxicol. Sci. 61:2001;100-106.
51. Kornburst D.J., Mavis R.D. Relative susceptibility of microsomes from lung heart, liver, kidney, brain and testes to lipid peroxidation: correlation with vitamin E content. Lipids. 15:1980;315-322.
52. Kristal B.S., Conway A.D., Brown A.M., Jain J.C., Ulluci P.A., Li S.W., Burke W.J. Selective dopaminergic vulnerability: 3,4-dihydroxyphenylacetaldehyde targets mitochondria. Free Radic. Biol. Med. 30:2001;924-931.
53. Lai C.-T., Yu P.H. Dopamine- and L-b-3,4-dihydroxyphenylalanine hydrochloride (L-Dopa)-induced cytotoxicity towards catecholaminergic neuroblastoma SH-SY5Y cells. Biochem. Pharmacol. 53:1997;363-372.
54. Lan J., Jiang D.H. Desferrioxamine and vitamin E protect against iron and MPTP-induced neurodegeneration in mice. J. Neural Transm. 104:1997;469-481.
55. Langston J.W., Ballard P., Tetrud J.W., Irwin I. Chronic parkinsonism in humans due to a product of merperidine-analog synthesis. Science. 219:1983;979-980.
56. Lee H.-J., Shin S.Y., Choi C., Lee Y.H., Lee S.-J. Formation and removal of α-synuclein aggregates in cells exposed to mitochondrial inhibitors. J. Biol. Chem. 277:2002;5411-5417.
57. Leedle R.A., Aust S.D. Importance of the polyunsaturated fatty acid to vitamin E ratio in the resistance of rat lung microsomes to lipid peroxidation. J. Free Radic. Biol. Med. 2:1986;397-403.
58. Leonard S.W., Terasawa Y., Farese R.V., Traber M.G. Incorporation of deuterated RRR- or all-rac-α-tocopherol in plasma and tissues of α-tocopherol transfer protein-null mice. Am. J. Clin. Nutr. 75:2002;555-560.
59. Lesnefsky E.J., Slabe T.J., Stoll M.S.K., Minkler P.E., Hoppel C.L. Myocardial ischemia selectively depletes cardiolipin in rabbit heart subsarcolemmal mitochondria. Am. J. Physiol. Heart Circ. Physiol. 280:2001;H2770-H2778.
60. Liebler D.C., Kling D.S., Reed D.J. Antioxidant protection of phospholipid bilayers by α-tocopherol. J. Biol. Chem. 261:1986;12114-12119.
61. 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.
62. Logroscino G., Marder K., Cote L., Tang M.-X., Shea S., Mayeux R. Dietary lipids and antioxidants in Parkinson's disease: a population-based case-control study. Ann. Neurol. 39:1996;89-94.
63. Lockwood A.H. Pesticides and Parkinsonism: is there an etiological link? Curr. Opin. Neurol. 13:2000;687-690.
64. Machlin L.J., Gabriel E. Kinetics of tissue alpha-tocopherol uptake and depletion following administration of high levels of vitamin E. Ann. New York Acad. Sci. 393:1982;48-60.
65. Maher N.E., Golbe L.I., Lazzarini A.M., et al. Epidemiological study of 203 sibling pairs with Parkinson's disease. Neurology. 58:2002;79-84.
66. Mandavilli B.S., Ali S.F., Van Houten B. DNA damage in brain mitochondria caused by aging and MPTP treatment. Brain Res. 885:2000;45-52.
67. Manning-Bog A.B., McCormack A.L., Li J., Uversky V.N., Fink A.L., DiMonte D.A. The herbicide paraquat causes up-regulation and aggregation of α-synuclein in mice. J. Biol. Chem. 277:2002;1641-1644.
68. Mansouri A., Demeilliers C., Amsellem S., Pessayre D., Fromenty B. Acute ethanol administration oxidatively damages and depletes mitochondrial DNA in mouse liver, brain, heart and skeletal muscles: protective effect of antioxidants. J. Pharmacol. Exp. Ther. 298:2001;737-743.
69. Martinovits G., Melamed E., Cohen O., Rosenthal J., Uzzan A. Systemic administration of antioxidants does not protect mice against the dopaminergic neurotoxicity of 1-methyl-4-phenyl-1,2,5,6-tetrahydropyridine (MPTP). Neurosci. Lett. 69:1986;192-197.
70. Maruyama W., Sango K., Iwasa K., Minami C., Dostert P., Kawai M., Moriyasu M., Naoi M. Dopaminergic neurotoxins cause different types of cell death in SH-SY5Y cells: apoptosis was induced by oxidized papaverolines and necrosis by reduced tetrahydropapaverolines. Neurosci. Lett. 291:2000;89-92.
71. Mayo J.C., Sainz R.M., Antolin I., Rodriguez C. Ultrastructural confirmation of neuronal protection by melatonin against the neurotoxin 6-hydroxydopamine cell damage. Brain Res. 818:1999;221-227.
72. McCormack A.L., Thiruchelvam M., Manning-Bog A.B., Thiffault C., Langston J.W., Cory-Slechta D.A., DiMonte 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.
73. Mizuno Y., Saitoh T., Sone N. Inhibition of mitochondrial alpha-ketoglutarate dehydrogenase by 1-methyl-4-phenylpyridinium ion. Biochem. Biophys. Res. Commun. 143:1987;971-976.
74. Mizuno Y., Matuda S., Yoshino H., Mori H., Hattori N., Ikebe S. An immunohistochemical study on alpha-ketoglutarate dehydrogenase complex in Parkinson's disease. Ann. Neurol. 35:1994;204-210.
75. Morens D.M., Grandinetti A., Waslien C.I., Park C.B., Ross G.W., White L.R. Case-control study of idiopathic Parkinson's disease and dietary vitamin E intake. Neurology. 46:1996;1270-1274.
76. Moussaoui S., Obinu M.C., Daniel N., Reibaud M., Blanchard V., Imperato A. The antioxidant ebselen prevents neurotoxicity and clinical symptoms in a primate model of Parkinson's disease. Exp. Neurol. 166:2000;235-245.
77. Nomura K., Imai H., Koumura T., Kobayashi T., Nakagawa Y. Mitochondrial phospholipid hydroperoxide glutathione peroxidase inhibits the release of cytochrome c from mitochondria by suppressing the peroxidation of cardiolipin in hypoglycaemia-induced apoptosis. Biochem. J. 351:2000;183-193.
78. Odunze I.N., Klaidman L.K., Adams J.D. Jr. MPTP toxicity in the mouse brain and vitamin E. Neurosci. Lett. 108:1990;346-349.
79. Offen D., Ziv I., Sternin H., Melamed E., Hochman A. Prevention of dopamine-induced cell death by thiol antioxidants: possible implications for treatment of Parkinson's disease. Exp. Neurol. 141:1996;32-39.
80. Pascoe G.A., Reed D.J. Vitamin E protection against chemical-induced cell injury. II. Evidence for the threshold effect of cellular α-tocopherol in prevention of adriamycin toxicity. Arch. Biochem. Biophys. 256:1987;159-166.
81. Payami H., Zareparsi S., James D., Nutt J. Familial aggregation of Parkinson's disease. A comparative study of early-onset and late-onset disease. Arch. Neurol. 59:2002;848-850.
82. 2+ homeostasis. Neurosci. Res. 37:2000;227-236.
83. Pereira C., Santos M.S., Oliveira C. Involvement of oxidative stress on the impairment of energy metabolism induced by Aβ peptides on PC12 cells: protection by antioxidants. Neurobiol. Dis. 6:1999;209-219.
84. Perry T.L., Wee Yong V., Clavier R.M., Jones K., Wright J.M., Foulks J.G., Wall R.A. Partial protection from the dopaminergic neurotoxin N-methyl-4-phenyl-1,2,3,6-tetrahydropyridine by four different antioxidants in the mouse. Neurosci. Lett. 60:1985;109-114.
85. Perry G., Sayre L.M., Atwood C.S., Castellani R.J., Cash A.D., Rottkamp C.A., Smith M.A. The role of iron and copper in the aetiology of neurodegenerative disorders: therapeutic implications. CNS Drugs. 16:2002;339-352.
86. Prasad K.N., Cole W.C., Kumar B. Multiple antioxidants in the prevention and treatment of Parkinson's disease. J. Am. Coll. Nutr. 18:1999;413-423.
87. Priyadarshi A., Khuder S., Schaub E.A., Priyadarshi S.S. Environmental risk factors and Parkinson's disease: a metaanlaysis. Environ. Res. Sec. A. 86:2001;122-127.
88. Ray S.D., Fariss M.W. Role of cellular energy status in tocopheryl hemisuccinate cytoprotection against ethyl methanesulfonate-induced toxicity. Arch. Biochem. Biophys. 311:1994;180-190.
89. Roghani M., Behzadi G. Neuroprotective effect of vitamin E on the early model of Parkinson's disease in rat: behavioral and histochemical evidence. Brain Res. 892:2001;211-217.
90. Roth J.A., Horbinski C., Higgins L., Lein P., Garrick M.D. Mechanisms of manganese-induced rat pheochromocytoma (PC12) cell death and cell differentiation. Neurotoxicology. 23:2002;147-157.
91. Scott J.A., Fischman A.J., Khaw B.-A., Homcy C.J., Rabito C.A. Free radical-mediated membrane polarization in renal and cardiac cells. Biochim. Biophys. Acta. 899:1987;76-82.
92. Selley M.L. 4-Hydroxy-2-nonenal may be involved in the pathogenesis of Parkinson's disease. Free Radic. Biol. Med. 25:1998;169-174.
93. Sherer T.B., Betarbet R., Greenamyre J.T. Environment, mitochondria, and Parkinson's disease. Neuroscientist. 8:2002;192-197.
94. Spencer P.S., Nunn P.B., Hugon J., et al. Guam amyotrophic lateral sclerosis-parkinsonism-dementia linked to a plant excitant neurotoxin. Science. 237:1987;517-522.
95. Storch A., Kaftan A., Burkhardt K., Schwarz J. 6-Hydroxydopamine toxicity towards human SH-SY5Y dopaminergic neuroblastoma cells: independent of mitochondrial energy metabolism. J. Neural Transm. 107:2000;281-293.
96. Sukalski K.A., Pinto K.A., Berntson J.L. Decreased susceptibility of liver mitochondria from diabetic rats to oxidative damage and associated increase in α-tocopherol. Free Radic. Biol. Med. 14:1993;57-65.
97. Tanner C.M., Ottman R., Goldman S.M., Ellenberg J., Chan P., Mayeux R., Langston J.W. Parkinson disease in twins. An etiologic study. J. Am. Med. Assoc. 281:1999;341-346.
98. Tappel A.L. Vitamin E as the biological lipid antioxidant. Vitam. Horm. 20:1962;493-510.
99. Tatton N.A. Increased caspase-3 and bax immunoreactivity accompany nuclear GAPDH translocation and neuronal apoptosis in Parkinson's disease. Exp. Neurol. 166:2000;29-43.
100. Temlett J.A., Landsberg J.P., Watt F., Grime G.W. Increased iron in the substantia nigra compacta of the MPTP-lesioned hemiparkinsonian Africian Green Monkey: evidence from proton microprobe elemental microanalysis. J. Neurochem. 62:1994;134-146.
101. Parkinson Study Group, 1989. DATATOP: A multicenter controlled clinical trial in early Parkinson's disease, Arch. Neurol. 46:1052-1060.
102. Parkinson Study Group, 1993. Effects of tocopherol and deprenyl on the progression of disability in early Parkinson's disease, New Engl. J. Med. 328:176-183.
103. Tirmenstein M.A., Pierce C.A., Leraas T.L., Fariss M.W. A fluorescence plate reader assay for monitoring the susceptibility of biological samples to lipid peroxidation. Anal. Biochem. 265:1998;246-253.
104. Tirmenstein M.A., Nicholls-Grzemski F.A., Zhang J.-G., Fariss M.W. Glutathione depletion and the production of reactive oxygen species in isolated hepatocyte suspensions. Chemico-Biol. Interact. 127:2000;201-217.
105. Traber M.G. Vitamin E in humans: demand and delivery. Annu. Rev. Nutr. 16:1996;321-347.
106. Trizna Z., Hsu T.C., Schantz S.P. Protective effects of vitamin E against bleomycin-induced genotoxicity in head and neck cancer patients in vitro. Anticancer Res. 12:1992;325-328.
107. Umansky V., Ratter F., Lampel S., Bucur M., Schirrmacher V., Ushmorov A. Inhibition of nitric-oxide mediated apoptosis in Jurkat leukemia cells despite cytochrome c release. Exp. Cell Res. 265:2001;274-282.
108. Vatassery G.T. Oxidation of alpha-tocopherol in subcellular fractions from rat brain and its possible involvement in nerve function. Biochem. Pharmacol. 45:1993;2295-2301.
109. Vatassery G.T., Brin M.F., Fahn S., Kayden H.J., Traber M.G. Effect of high dose of dietary vitamin E on the concentration of vitamin E in several brain regions, plasma, liver, and adipose tissue of rats. J. Neurochem. 51:1988;621-623.
110. Vatassery G.T., Fahn S., Kuskowski M.A. Alpha tocopherol in CSF of subjects taking high-dose vitamin E in the DATATOP study. Neurology. 50:1998;1900-1902.
111. Vatassery G.T., Bauer T., Dysken M. High doses of vitamin E in the treatment of disorders of the central nervous system in the aged. Am. J. Clin. Nutr. 70:1999;793-801.
112. Vila M., Jackson-Lewis V., Vukosavic S., Djaldetti R., Liberatore G., Offen D., Korsmeyer S.J., Przedborski S. Bax ablation prevents dopaminegic neurodegeneration in the MPTP mouse model of Parkinson's disease. Proc. Natl. Acad. Sci. USA. 98:2001;2837-2842.
113. Wei Q., Yeung M., Jurma O.P., Anderson J.K. Genetic elevation of monoamine oxidase levels in dopaminergic PC12 cells results in increased free radical damage and sensitivity to MPTP. J. Neurosci. Res. 46:1996;666-673.
114. Wey H.E., Pyron L., Woolery M. Essential fatty acid deficiency in cultured human keratinocytes attenuates toxicity due to lipid peroxidation. Toxicol. Appl. Pharmacol. 120:1993;72-79.
115. Yang N.Y.J., Desai I.D. Effect of high levels of dietary vitamin E on liver and plasma lipids and fat soluble vitamins in rats. J. Nutr. 107:1977;1418-1426.
116. Yoritaka A., Hattori N., Uchida K., Tanaka M., Stadtman E.R., Mizuno Y. Immunohistochemical detection of 4-hydroxynonenal-protein adducts in Parkinson's disease. Proc. Natl. Acad. Sci. USA. 93:1996;2696-2701.
117. Zhang J., Pery G., Smith M.A., Robertson D., Olson S.J., Graham D.G., Montine T.J. Parkinson's disease is associated with oxidative damage to cytoplasmic DNA and RNA in substantia nigra neurons. Am. J. Pathol. 154:1999;1423-1429.
118. Zhang J.G., Tirmenstein M.A., Nicholls-Grzemski F.A., Fariss M.W. Mitochondrial electron transport inhibitors cause lipid peroxidation-dependent and -independent cell death: protective role of antioxidants. Arch. Biochem. Biophys. 393:2001;87-96.
119. Zhang J.G., Nicholls-Grzemski F.A., Tirmenstein M.A., Fariss M.W. Vitamin E succinate protects hepatocytes against the toxic effect of reactive oxygen species generated at mitochondrial complexes I and III by alkylating agents. Chemico-Biol. Interact. 138:2001;267-284.