Neurological mechanisms of green tea polyphenols in Alzheimer's and Parkinson's diseases

Journal of Nutritional Biochemistry

Volumn 15, Issue 9, 2004, Pages 506-516

  Weinreb, Orly ^a   Mandel, Silvia ^a   Amit, Tamar ^a   Youdim, Moussa B H ^a  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

( ) Epigallocatechin 3 gallate; Antioxidation; Green tea; Iron chelating; Neurodegenerative diseases; Neuroprotection

Indexed keywords

ANTIOXIDANT; CHELATING AGENT; COPPER; EPIGALLOCATECHIN GALLATE; GREEN TEA EXTRACT; IRON; POLYPHENOL DERIVATIVE; TRANSITION ELEMENT;

ALZHEIMER DISEASE; ANTIOXIDANT ACTIVITY; APOPTOSIS; CELL SURVIVAL; CORRELATION ANALYSIS; DIET SUPPLEMENTATION; DRUG EFFECT; DRUG MECHANISM; DRUG POTENCY; DRUG SCREENING; GENE EXPRESSION; HUMAN; MEDICINAL PLANT; NERVE DEGENERATION; NEUROMODULATION; NEUROPROTECTION; OXIDATIVE STRESS; PARKINSON DISEASE; REVIEW; SIGNAL TRANSDUCTION; TEA;

ALZHEIMER DISEASE; ANIMALS; ANTIOXIDANTS; APOPTOSIS; CATECHIN; DIETARY SUPPLEMENTS; DISEASE MODELS, ANIMAL; FLAVONOIDS; GENE EXPRESSION REGULATION; HUMANS; IRON CHELATING AGENTS; NEUROPROTECTIVE AGENTS; PARKINSON DISEASE; PHENOLS; SIGNAL TRANSDUCTION; TEA;

LETHRINIDAE;

EID: 4444226105     PISSN: 09552863     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2004.05.002     Document Type: Review

References (115)

1. Butterfield D., Castegna A., Pocernich C., Drake J., Scapagnini G., Calabrese V. Nutritional approaches to combat oxidative stress in Alzheimer's disease. J Nutr Biochem. 13:2002;444-461
2. van Acker S.A., van den Berg D.J., Tromp M.N., Griffioen D.H., van Bennekom W.P., van der Vijgh W.J., Bast A. Structural aspects of antioxidant activity of flavonoids. Free Radic Biol Med. 20:1996;331-342
3. Gotz M.E., Kunig G., Riederer P., Youdim M.B. Oxidative stress free radical production in neural degeneration. Pharmacol Ther. 63:1994;37-122
4. Halliwell B. Role of free radicals in the neurodegenerative diseases therapeutic implications for antioxidant treatment. Drugs Aging. 18:2001;685-716
5. Gotz M.E., Freyberger A., Riederer P. Oxidative stress a role in the pathogenesis of Parkinson's disease. J Neural Transm. 29:(Suppl):1990;241-249
6. Halliwell B. Reactive oxygen species and the central nervous system. J Neurochem. 59:1992;1609-1623
7. Riederer P., Sofic E., Rausch W.D., Schmidt B., Reynolds G.P., Jellinger K., Youdim M.B.H. Transition metals, ferritin, glutathione, and ascorbic acid in parkinsonian brains. J Neurochem. 52:1989;515-520
8. Linazasoro G. Neuroprotection in Parkinson's disease love story or mission impossible? Expert Rev Neurotherapeutics. 2:2002;403-416
9. Perry G., Cash A.D., Smith M.A. Alzheimer disease and oxidative stress. J Biomed Biotechnol. 2:2002;120-123
10. Perry G., Taddeo M.A., Nunomura A., Zhu X., Zenteno-Savin T., Drew K.L., Shimohama S., Avila J., Castellani R.J., Smith M.A. Comparative biology and pathology of oxidative stress in Alzheimer and other neurodegenerative diseases beyond damage and response. Comp Biochem Physiol C Toxicol Pharmacol. 133:2002;507-513
11. Hellenbrand W., Seidler A., Boeing H., Robra B.P., Vieregge P., Nischan P., Joerg J., Oertel W.H., Schneider E., Ulm G. Diet and Parkinson's disease. I A possible role for the past intake of specific foods and food groups. Results from a self-administered food-frequency questionnaire in a case-control study. Neurology. 47:1996;636-643
12. Higdon J.V., Frei B. Tea catechins and polyphenols health effects, metabolism, and antioxidant functions. Crit Rev Food Sci Nutr. 43:2003;89-143
13. Wiseman S.A., Balentine D.A., Frei B. Antioxidants in tea. Crit Rev Food Sci Nutr. 37:1997;705-718
14. Slikker W., Youdim M.B., Palmer G.C., Hall E., Williams C., Trembly B. The future of neuroprotection. Ann NY Acad Sci. 890:1999;529-533
15. Salah N., Miller N.J., Paganga G., Tijburg L., Bolwell G.P., Rice-Evans C. Polyphenolic flavanols as scavengers of aqueous phase radicals and as chain-breaking antioxidants. Arch Biochem Biophys. 322:1995;339-346
16. Nanjo F., Goto K., Seto R., Suzuki M., Sakai M., Hara Y. Scavenging effects of tea catechins and their derivatives on 1,1-diphenyl-2-picrylhydrazyl radical. Free Radic Biol Med. 21:1996;895-902
17. Ishige K., Schubert D., Sagara Y. Flavonoids protect neuronal cells from oxidative stress by three distinct mechanisms. Free Radic Biol Med. 30:2001;433-446
18. Schroeter H., Boyd C., Spencer J.P., Williams R.J., Cadenas E., Rice-Evans C. MAPK signaling in neurodegeneration influences of flavonoids and of nitric oxide. Neurobiol Aging. 23:2002;861-880
19. Levites Y., Amit T., Mandel S., Youdim M.B.H. Neuroprotection and neurorescue against amyloid beta toxicity and PKC-dependent release of non-amyloidogenic soluble precusor protein by green tea polyphenol (-)-epigallocatechin-3-gallate. FASEB J. 17:2003;952-954
20. Levites Y., Weinreb O., Maor G., Youdim M.B.H., Mandel S. Green tea polyphenol (-)-epigallocatechin-3-gallate prevents N-methyl-4-phenyl-1,2,3,6- tetrahydropyridine-induced dopaminergic neurodegeneration. J Neurochem. 78:2001;1073-1082
21. Chen C., Yu R., Owuor E.D., Kong A.N. Activation of antioxidant-response element (ARE), mitogen-activated protein kinases (MAPKs) and caspases by major green tea polyphenol components during cell survival and death. Arch Pharm Res. 23:2000;605-612
22. Levites Y., Amit T., Youdim M.B.H., Mandel S. Involvement of protein kinase C activation and cell survival/cell cycle genes in green tea polyphenol (-)-epigallocatechin-3-gallate neuroprotective action. J Biol Chem. 277:2002;30574-30580
23. Hollman P.C., Feskens E.J., Katan M.B. Tea flavonols in cardiovascular disease and cancer epidemiology. Proc Soc Exp Biol Med. 220:1999;198-202
24. Yang F., de Villiers W.J., McClain C.J., Varilek G.W. Green tea polyphenols block endotoxin-induced tumor necrosis factor-production and lethality in a murine model. J Nutr. 128:1998;2334-2340
25. Tedeschi E., Menegazzi M., Yao Y., Suzuki H., Forstermann U., Kleinert H. Green tea inhibits human inducible nitric-oxide synthase expression by down-regulating signal transducer and activator of transcription-1alpha activation. Mol Pharmacol. 65:2004;111-120
26. Weisburger J.H., Chung F.L. Mechanisms of chronic disease causation by nutritional factors and tobacco products and their prevention by tea polyphenols. Food Chem Toxicol. 40:2002;1145-1154
27. Pannala A.S., Rice-Evans C.A., Halliwell B., Singh S. Inhibition of peroxynitrite-mediated tyrosine nitration by catechin polyphenols. Biochem Biophys Res Commun. 232:1997;164-168
28. Nanjo F., Mori M., Goto K., Hara Y. Radical scavenging activity of tea catechins and their related compounds. Biosci Biotechnol Biochem. 63:1999;1621-1623
29. Khokhar S., Magnusdottir S.G. Total phenol, catechin, and caffeine contents of teas commonly consumed in the United Kingdom. J Agric Food Chem. 50:2002;565-570
30. Pietta P.G., Simonetti P., Gardana C., Brusamolino A., Morazzoni P., Bombardelli E. Catechin metabolites after intake of green tea infusions. Biofactors. 8:1998;111-118
31. Lee M.J., Wang Z.Y., Li H., Chen L., Sun Y., Gobbo S., Balentine D.A., Yang C.S. Analysis of plasma and urinary tea polyphenols in human subjects. Cancer Epidemiol Biomarkers Prev. 4:1995;393-399
32. Harada M., Kan Y., Naoki H., Fukui Y., Kageyama N., Nakai M., Miki W., Kiso Y. Identification of the major antioxidative metabolites in biological fluids of the rat with ingested (+)-catechin and (-)-epicatechin. Biosci Biotechnol Biochem. 63:1999;973-977
33. Nakagawa K., Okuda S., Miyazawa T. Dose-dependent incorporation of tea catechins, (-)-epigallocatechin-3-gallate and (-)-epigallocatechin, into human plasma. Biosci Biotechnol Biochem. 61:1997;1981-1985
34. Yang C.S., Kim S., Yang G.Y., Lee M.J., Liao J., Chung J.Y., Ho C.T. Inhibition of carcinogenesis by tea bioavailability of tea polyphenols and mechanisms of actions. Proc Soc Exp Biol Med. 220:1999;213-217
35. Hong J.T., Ryu S.R., Kim H.J., Lee J.K., Lee S.H., Kim D.B., Yun Y.P., Ryu J.H., Lee B.M., Kim P.Y. Neuroprotective effect of green tea extract in experimental ischemia-reperfusion brain injury. Brain Res Bull. 53:2000;743-749
36. Abd El Mohsen M.M., Kuhnle G., Rechner A.R., Schroeter H., Rose S., Jenner P., Rice-Evans C.A. Uptake and metabolism of epicatechin and its access to the brain after oral ingestion. Free Radic Biol Med. 33:2002;1693-1702
37. Suganuma M., Okabe S., Oniyama M., Tada Y., Ito H., Fujiki H. Wide distribution of [3H](-)-epigallocatechin gallate, a cancer preventive tea polyphenol, in mouse tissue. Carcinogenesis. 19:1998;1771-1776
38. Checkoway H., Powers K., Smith-Weller T., Franklin G.M., Longstreth W.T. Jr, Swanson P.D. Parkinson's disease risks associated with cigarette smoking, alcohol consumption, and caffeine intake. Am J Epidemiol. 155:2002;732-738
39. Tan E.K., Tan C., Fook-Chong S.M., Lum S.Y., Chai A., Chung H., Shen H., Zhao Y., Teoh M.L., Yih Y., Pavanni R., Chandran V.R., Wong M.C. Dose-dependent protective effect of coffee, tea, and smoking in Parkinson's disease a study in ethnic Chinese. J Neurol Sci. 216:2003;163-167
40. Li S.C., Schoenberg B.S., Wang C.C., Cheng X.M., Rui D.Y., Bolis C.L., Schoenberg D.G. A prevalence survey of Parkinson's disease and other movement disorders in the People's Republic of China. Arch Neurol. 42:1985;655-657
41. Zhang Z.X., Roman G.C. Worldwide occurrence of Parkinson's disease an updated review. Neuroepidemiology. 12:1993;195-208
42. Le Bars P.L., Velasco F.M., Ferguson J.M., Dessain E.C., Kieser M., Hoerr R. Influence of the severity of cognitive impairment on the effect of the Ginkgo biloba extract EGb 761 in Alzheimer's disease. Neuropsychobiology. 45:2002;19-26
43. Orgogozo J.M., Dartigues J.F., Lafont S., Letenneur L., Commenges D., Salamon R., Renaud S., Breteler M.B. Wine consumption and dementia in the elderly a prospective community study in the Bordeaux area. Rev Neurol (Paris). 153:1997;185-192
44. Guo Q., Zhao B., Li M., Shen S., Xin W. Studies on protective mechanisms of four components of green tea polyphenols against lipid peroxidation in synaptosomes. Biochim Biophys Acta. 1304:1996;210-222
45. Grunblatt E., Mandel S., Maor G., Youdim M.B.H. Effects of R-apomorphine and S-apomorphine on MPTP-induced nigro-striatal doamine neuronal loss. J Neurochem. 77:2001;146-156
46. Grunblatt E., Mandel S., Berkuzki T., Youdim M.B.H. Apomorphine protects against MPTP-induced neurotoxicity in mice. Mov Disord. 14:1999;612-618
47. Pan T., Fei J., Zhou X., Jankovic J., Le W. Effects of green tea polyphenols on dopamine uptake and on MPP+ -induced dopamine neuron injury. Life Sci. 72:2003;1073-1083
48. Lu H., Meng X., Yang C.S. Enzymology of methylation of tea catechins and inhibition of catechol-O-methyltransferase by (-)-epigallocatechin gallate. Drug Metab Dispos. 31:2003;572-579
49. Deleu D., Northway M.G., Hanssens Y. Clinical pharmacokinetic and pharmacodynamic properties of drugs used in the treatment of Parkinson's disease. Clin Pharmacokinet. 41:2002;261-309
50. Monteiro H.P., Winterbourn C.C. 6-Hydroxydopamine releases iron from ferritin and promotes ferritin-dependent lipid peroxidation. Biochem Pharmacol. 38:1989;4177-4182
51. Mochizuki H., Imai H., Endo K., Yokomizo K., Murata Y., Hattori N., Mizuno Y. Iron accumulation in the substantia nigra of 1-methyl-4-phenyl-1,2,3, 6-tetrahydropyridine (MPTP)-induced hemiparkinsonian monkeys. Neurosci Lett. 168:1994;251-253
52. Oestreicher E., Sengstock G.J., Riederer P., Olanow C.W., Dunn A.J., Arendash G.W. Degeneration of nigrostriatal dopaminergic neurons increases iron within the substantia nigra a histochemical and neurochemical study. Brain Res. 660:1994;8-18
53. Temlett J.A., Landsberg J.P., Watt F., Grime G.W. Increased iron in the substantia nigra compacta of the MPTP-lesioned hemiparkinsonian African green monkey evidence from proton microprobe elemental microanalysis. J Neurochem. 62:1994;134-146
54. Senior K. New genes reveal major role for iron in neurodegeneration. Lancet. 358:2001;302
55. Bush A.I. The metallobiology of Alzheimer's disease. Trends Neurosci. 26:2003;207-214
56. Checler F. Processing of the beta-amyloid precursor protein and its regulation in Alzheimer's disease. J Neurochem. 65:1995;1431-1444
57. Nunan J., Small D.H. Regulation of APP cleavage by alpha-, beta- and gamma-secretases. FEBS Lett. 483:2000;6-10
58. Choi Y.T., Jung C.H., Lee S.R., Bae J.H., Baek W.K., Suh M.H., Park J., Park C.W., Suh S.I. The green tea polyphenol (-)-epigallocatechin gallate attenuates beta- amyloid-induced neurotoxicity in cultured hippocampal neurons. Life Sci. 70:2001;603-614
59. Ono K., Yoshiike Y., Takashima A., Hasegawa K., Naiki H., Yamada M. Potent anti-amyloidogenic and fibril-destabilizing effects of polyphenols in vitro implications for the prevention and therapeutics of Alzheimer's disease. J Neurochem. 87:2003;172-181
60. Mills J., Reiner P.B. Regulation of amyloid precursor protein cleavage. J Neurochem. 72:1999;443-460
61. Slack B.E., Nitsch R.M., Livneh E., Kunz G.M. Jr, Breu J., Eldar H., Wurtman R.J. Regulation by phorbol esters of amyloid precursor protein release from Swiss 3T3 fibroblasts overexpressing protein kinase C alpha. J Biol Chem. 268:1993;21097-21101
62. Benussi L., Govoni S., Gasparini L., Binetti G., Trabucchi M., Bianchetti A., Racchi M. Specific role for protein kinase C alpha in the constitutive and regulated secretion of amyloid precursor protein in human skin fibroblasts. Neurosci Lett. 240:1998;97-101
63. Matsushima H., Shimohama S., Chachin M., Taniguchi T., Kimura J. Ca2+-dependent and Ca2+-independent protein kinase C changes in the brain of patients with Alzheimer's disease. J Neurochem. 67:1996;317-323
64. Morel I., Lescoat G., Cogrel P., Sergent O., Pasdeloup N., Brissot P., Cillard P., Cillard J. Antioxidant and iron-chelating activities of the flavonoids catechin, quercetin and diosmetin on iron-loaded rat hepatocyte cultures. Biochem Pharmacol. 45:1999;13-19
65. Jeong J.H., Kim H.J., Lee T.J., Kim M.K., Park E.S., Choi B.S. Epigallocatechin 3-gallate attenuates neuronal damage induced by 3-hydroxykynurenine. Toxicology. 195:2004;53-60
66. Levites Y., Youdim M.B.H., Maor G., Mandel S. Attenuation of 6-hydroxydopamine (6-OHDA)-induced nuclear factor-kappaB (NF-kappaB) activation and cell death by tea extracts in neuronal cultures. Biochem Pharmacol. 63:2002;21-29
67. Higuchi A., Yonemitsu K., Koreeda A., Tsunenari S. Inhibitory activity of epigallocatechin gallate (EGCg) in paraquat-induced microsomal lipid peroxidation - a mechanism of protective effects of EGCg against paraquat toxicity. Toxicology. 183:2003;143-149
68. Liou H.H., Chen R.C., Chen T.H., Tsai Y.F., Tsai M.C. Attenuation of paraquat-induced dopaminergic toxicity on the substantia nigra by (-)-deprenyl in vivo. Toxicol Appl Pharmacol. 172:2001;37-43
69. Thompson M., Williams C.R., Elliot G.E. Stability of flavonoid complexes of copper(II) and flavonoid antioxidant activity. Anal Chim Acta. 85:1976;375-381
70. Grinberg L.N., Newmark H., Kitrossky N., Rahamim E., Chevion M., Rachmilewitz E.A. Protective effects of tea polyphenols against oxidative damage to red blood cells. Biochem Pharmacol. 54:1997;973-978
71. Jellinger K., Paulus W., Grundke-Iqbal I., Riederer P., Youdim M.B.H. Brain iron and ferritin in Parkinson's and Alzheimer's diseases. J Neural Transm Park Dis Dement Sect. 2:1990;327-340
72. Sofic E., Paulus W., Jellinger K., Riederer P., Youdim M.B.H. Selective increase of iron in substantia nigra zona compacta of parkinsonian brains. J Neurochem. 56:1991;978-982
73. Mogi M., Harada M., Riederer P., Narabayashi H., Fujita K., Nagatsu T. Tumor necrosis factor-alpha (TNF-alpha) increases both in the brain and in the cerebrospinal fluid from parkinsonian patients. Neurosci Lett. 165:1994;208-210
74. Blum-Degen D., Muller T., Kuhn W., Gerlach M., Przuntek H., Riederer P. Interleukin-1 beta and interleukin-6 are elevated in the cerebrospinal fluid of Alzheimer's and de novo Parkinson's disease patients. Neurosci Lett. 202:1995;17-20
75. McGeer P.L., McGeer E.G. The inflammatory response system of brain implications for therapy of Alzheimer and other neurodegenerative diseases. Brain Res Brain Res Rev. 21:1995;195-218
76. Sakaguchi S., Furusawa S., Yokota K., Sasaki K., Takayanagi M., Takayanagi Y. The enhancing effect of tumour necrosis factor-alpha on oxidative stress in endotoxemia. Pharmacol Toxicol. 79:1996;259-265
77. Lin Y.L., Lin J.K. (-)-Epigallocatechin-3-gallate blocks the induction of nitric oxide synthase by down-regulating lipopolysaccharide-induced activity of transcription factor nuclear factor-kappaB. Mol Pharmacol. 52:1997;465-472
78. Schreck R., Rieber P., Baeuerle P.A. Reactive oxygen intermediates as apparently widely used messengers in the activation of the NF-kappa B transcription factor and HIV-1. EMBO J. 10:1991;2247-2258
79. Hunot S., Brugg B., Ricard D., Michel P.P., Muriel M.P., Ruberg M., Faucheux B.A., Agid Y., Hirsch E.C. Nuclear translocation of NF-kappaB is increased in dopaminergic neurons of patients with parkinson disease. Proc Natl Acad Sci USA. 94:1997;7531-7536
80. Lin Y.L., Tsai S.H., Lin-Shiau S.Y., Ho C.T., Lin J.K. Theaflavin-3,3′-digallate from black tea blocks the nitric oxide synthase by down-regulating the activation of NF-kappaB in macrophages. Eur J Pharmacol. 367:1999;379-388
81. Xia Z., Dickens M., Raingeaud J., Davis R.J., Greenberg M.E. Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science. 270:1995;1326-1331
82. Singer C.A., Figueroa-Masot X.A., Batchelor R.H., Dorsa D.M. The mitogen-activated protein kinase pathway mediates estrogen neuroprotection after glutamate toxicity in primary cortical neurons. J Neurosci. 19:1999;2455-2463
83. Cordey M., Gundimeda U., Gopalakrishna R., Pike C.J. Estrogen activates protein kinase C in neurons role in neuroprotection. J Neurochem. 84:2003;1340-1348
84. Kaplan D.R., Miller F.D. Neurotrophin signal transduction in the nervous system. Curr Opin Neurobiol. 10:2000;381-391
85. Koh S.H., Kim S.H., Kwon H., Park Y., Kim K.S., Song C.W., Kim J., Kim M.H., Yu H.J., Henkel J.S., Jung H.K. Epigallocatechin gallate protects nerve growth factor differentiated PC12 cells from oxidative-radical-stress-induced apoptosis through its effect on phosphoinositide 3-kinase/Akt and glycogen synthase kinase-3. Brain Res Mol Brain Res. 118:2003;72-81
86. Mandel S., Reznichenko L., Amit T., Youdim M. Green tea polyphenol (-)-epigallocatechin-3-gallate protects rat PC12 cells from apoptosis induced by serum withdrawal independent of P13-Akt pathway. Neurotoxocity Research. 5:2003;419-424
87. Vaudry D., Stork P.J., Lazarovici P., Eiden L.E. Signaling pathways for PC12 cell differentiation making the right connections. Science. 296:2002;1648-1649
88. Harris C.A., Deshmukh M., Tsui-Pierchala B., Maroney A.C., Johnson E.M. Jr. Inhibition of the c-Jun N-terminal kinase signaling pathway by the mixed lineage kinase inhibitor CEP-1347 (KT7515) preserves metabolism and growth of trophic factor-deprived neurons. J Neurosci. 22:2002;103-113
89. Johnson G.L., Lapadat R. Mitogen-activated protein kinase pathways mediated by ERK, JNK, and p38 protein kinases. Science. 298:2002;1911-1912
90. Owuor E.D., Kong A.N. Antioxidants and oxidants regulated signal transduction pathways. Biochem Pharmacol. 64:2002;765-770
91. Satoh T., Nakatsuka D., Watanabe Y., Nagata I., Kikuchi H., Namura S. Neuroprotection by MAPK/ERK kinase inhibition with U0126 against oxidative stress in a mouse neuronal cell line and rat primary cultured cortical neurons. Neurosci Lett. 288:2000;163-166
92. Schroeter H., Spencer J.P., Rice-Evans C., Williams R.J. Flavonoids protect neurons from oxidized low-density-lipoprotein-induced apoptosis involving c-Jun N-terminal kinase (JNK), c-Jun and caspase-3. Biochem J. 358:2001;547-557
93. Dempsey E.C., Newton A.C., Mochly-Rosen D., Fields A.P., Reyland M.E., Insel P.A., Messing R.O. Protein kinase C isozymes and the regulation of diverse cell responses. Am J Physiol Lung Cell Mol Physiol. 279:2000;L429-L438
94. Maher P. How protein kinase C activation protects nerve cells from oxidative stress-induced cell death. J Neurosci. 21:2001;2929-2938
95. Cardell M., Wieloch T. Time course of the translocation and inhibition of protein kinase C during complete cerebral ischemia in the rat. J Neurochem. 61:1993;1308-1314
96. Busto R., Globus M.Y., Neary J.T., Ginsberg M.D. Regional alterations of protein kinase C activity following transient cerebral ischemia effects of intraischemic brain temperature modulation. J Neurochem. 63:1994;1095-1103
97. Nishino N., Kitamura N., Nakai T., Hashimoto T., Tanaka C. Phorbol ester binding sites in human brain characterization, regional distribution, age-correlation, and alterations in Parkinson's disease. J Mol Neurosci. 1:1989;19-26
98. Gubina E., Rinaudo M.S., Szallasi Z., Blumberg P.M., Mufson R.A. Overexpression of protein kinase C isoform epsilon but not delta in human interleukin-3-dependent cells suppresses apoptosis and induces bcl-2 expression. Blood. 91:1998;823-829
99. Whelan R.D., Parker P.J. Loss of protein kinase C function induces an apoptotic response. Oncogene. 16:1998;1939-1944
100. Ruvolo P.P., Deng X., Carr B.K., May W.S. A functional role for mitochondrial protein kinase Calpha in Bcl2 phosphorylation and suppression of apoptosis. J Biol Chem. 273:1998;25436-25442
101. Chung JH, Han JH, Hwang EJ, Seo JY, Cho KH, Kim KH, Youn JI, Eun HC. Dual mechanisms of green tea extract-induced cell survival in human epidermal keratinocytes. FASEB J 2003;17:1913-5
102. Sah JF, Balasubramanian S, Eckert RL, Rorke EA. Epigallocatechin-3- gallate inhibits epidermal growth factor receptor signaling pathway: evidence for direct inhibition of ERK1/2 and Akt kinases. J Biol Chem 2004;279:12755-62
103. Hastak K., Gupta S., Ahmad N., Agarwal M.K., Agarwal M.L., Mukhtar H. Role of p53 and NF-kappaB in epigallocatechin-3-gallate-induced apoptosis of LNCaP cells. Oncogene. 22:2003;4851-4859
104. Halliwell B. Vitamin C antioxidant or pro-oxidant in vivo? Free Radi Res. 25:1996;439-454
105. Gassen M., Gross A., Youdim M.B. Apomorphine enantiomers protect cultured pheochromocytoma (PC12) cells from oxidative stress induced by H2O2 and 6-hydroxydopamine. Mov Disord. 13:1998;242-248
106. Mandel S., Grunblatt E., Maor G., Youdim M.B.H. Early and late gene changes in MPTP mice model of Parkinson's disease employing cDNA microarray. Neurochem Res. 27:2002;1231-1243
107. Weinreb O, Mandel S, Youdim MB. Gene and protein expression profiles of anti- and pro-apoptotic actions of dopamine, R-apomorphine, green tea polyphenol (-)-epigallocatechine-3-gallate and melatonin. Ann NY Acad Sci 2003;993:351-61, discussion 87-93
108. Weinreb O., Mandel S., Youdim M.B.H. CDNA gene expression profile homology of antioxidants and their anti-apoptotic and pro-apoptotic activities in human neuroblastoma cells. FASEB J. 17:2003;935-937
109. Gassen M., Youdim M.B.H. Free radical scavengers chemical concepts and clinical relevance. J Neural Transm. 56:(Suppl):1999;193-210
110. Mandel S., Grunblatt E., Riederer P., Gerlach M., Levites Y., Youdim M.B.H. Neuroprotective strategies in Parkinson's disease an update on progress. CNS Drugs. 17:2003;729-762
111. Maruyama W., Takahashi T., Youdim M.B.H., Naoi M. The anti-parkinson drug, rasagiline, prevents apoptotic DNA damage induced by peroxynitrite in human dopaminergic neuroblastoma SH-SY5Y cells. J Neural Transm. 109:2002;467-481
112. Maruyama W., Akao Y., Youdim M.B.H., Boulton A.A., Davis B.A., Naoi M. Transfection-enforced Bcl-2 overexpression and an anti-Parkinson drug, rasagiline, prevent nuclear accumulation of glyceraldehyde-3 phosphate dehydrogenase induced by an endogenous dopaminergic neurotoxin, N-methyl(R)salsolinol. J Neurochem. 78:2001;727-735
113. Bates T.E., Heales S.J., Davies S.E., Boakye P., Clark J.B. Effects of 1-methyl-4-phenylpyridinium on isolated rat brain mitochondria evidence for a primary involvement of energy depletion. J Neurochem. 63:1994;640-648
114. Kalivendi SV, Cunningham S, Kotamraju S, Joseph J, Hillard CJ, Kalyanaraman B. a-Synuclein up-regulation and aggregation during MPP+-induced apoptosis in neuroblastoma cells: intermediacy of transferrin receptor iron and hydrogen peroxide. J Biol Chem 2004;279:15240-7
115. Rogers J.T., Randall J.D., Cahill C.M., Eder P.S., Huang X., Gunshin H., Leiter L., McPhee J., Sarang S.S., Utsuki T., Greig N.H., Lahiri D.K., Tanzi R.F., Bush A.I., Giordano T., Gullans S.R. An iron-responsive element type II in the 5′-untranslated region of the Alzheimer's amyloid precursor protein transcript. J Biol Chem. 277:2002;45518-45528