Oxidative and nitrative protein modifications in Parkinson's disease

Free Radical Biology and Medicine

Volumn 44, Issue 10, 2008, Pages 1787-1794

  Danielson, Steven R ^a   Andersen, Julie K ^a  

^a BUCK INSTITUTE FOR RESEARCH ON AGING   (United States)

Author keywords

3NT; HNE; Nitration; Oxidation; Parkinson's disease; Posttranslational modification

Indexed keywords

ALPHA SYNUCLEIN; DJ 1 PROTEIN; DOPAMINE; LEVODOPA; PARKIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEASOME; PROTEIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); TYROSINE 3 MONOOXYGENASE;

DISEASE COURSE; HUMAN; NEUROPHYSIOLOGY; NITRATION; NITRATIVE STRESS; NONHUMAN; OXIDATION; OXIDATIVE STRESS; PARKINSON DISEASE; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN MODIFICATION; REVIEW;

BRAIN; DOPAMINE; HUMANS; NEURONS; NITRIC OXIDE; OXIDATION-REDUCTION; OXIDATIVE STRESS; PARKINSON DISEASE; PROTEIN PROCESSING, POST-TRANSLATIONAL;

EID: 42649144101     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2008.03.005     Document Type: Review

References (105)

1. Andersen J.K. Iron dysregulation and Parkinson's disease. J. Alzheimers Dis. 6 (2004) S47-S52
2. Farrer M.J. Genetics of Parkinson disease: paradigm shifts and future prospects. Nat. Rev. Genet. 7 (2006) 306-318
3. Jenner P., Dexter D.T., Sian J., Schapira A.H., and Marsden C.D. Oxidative stress as a cause of nigral cell death in Parkinson's disease and incidental Lewy body disease. The Royal Kings and Queens Parkinson's Disease Research Group. Ann. Neurol. 32 (1992) S82-S87 Suppl.
4. Perry T.L., Godin D.V., and Hansen S. Parkinson's disease: a disorder due to nigral glutathione deficiency?. Neurosci. Lett. 33 (1982) 305-310
5. Perry T.L., and Yong V.W. Idiopathic Parkinson's disease, progressive supranuclear palsy and glutathione metabolism in the substantia nigra of patients. Neurosci. Lett. 67 (1986) 269-274
6. Pearce R.K., Owen A., Daniel S., Jenner P., and Marsden C.D. Alterations in the distribution of glutathione in the substantia nigra in Parkinson's disease. J. Neural Transm. 104 (1997) 661-677
7. Dexter D.T., Carter C.J., Wells F.R., Javoy-Agid F., Agid Y., Lees A., Jenner P., and Marsden C.D. Basal lipid peroxidation in substantia nigra is increased in Parkinson's disease. J. Neurochem. 52 (1989) 381-389
8. Yoritaka A., Hattori N., Uchida K., Tanaka M., Stadtman E.R., and Mizuno Y. Immunohistochemical detection of 4-hydroxynonenal protein adducts in Parkinson disease. Proc. Natl. Acad. Sci. U. S. A. 93 (1996) 2696-2701
9. Alam Z.I., Jenner A., Daniel S.E., Lees A.J., Cairns N., Marsden C.D., Jenner P., and 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
10. Zhang J., Perry G., Smith M.A., Robertson D., Olson S.J., Graham D.G., and 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
11. Alam Z.I., Daniel S.E., Lees A.J., Marsden D.C., Jenner P., and Halliwell B. A generalised increase in protein carbonyls in the brain in Parkinson's but not incidental Lewy body disease. J. Neurochem. 69 (1997) 1326-1329
12. Floor E., and Wetzel M.G. 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 (1998) 268-275
13. Turko I.V., and Murad F. Protein nitration in cardiovascular diseases. Pharmacol. Rev. 54 (2002) 619-634
14. Good P.F., Hsu A., Werner P., Perl D.P., and Olanow C.W. Protein nitration in Parkinson's disease. J. Neuropathol. Exp. Neurol. 57 (1998) 338-342
15. Duda J.E., Giasson B.I., Chen Q., Gur T.L., Hurtig H.I., Stern M.B., Gollomp S.M., Ischiropoulos H., Lee V.M., and Trojanowski J.Q. Widespread nitration of pathological inclusions in neurodegenerative synucleinopathies. Am. J. Pathol. 157 (2000) 1439-1445
16. Ferrante R.J., Hantraye P., Brouillet E., and Beal M.F. Increased nitrotyrosine immunoreactivity in substantia nigra neurons in MPTP treated baboons is blocked by inhibition of neuronal nitric oxide synthase. Brain Res. 823 (1999) 177-182
17. Pennathur S., Jackson-Lewis V., Przedborski S., and Heinecke J.W. Mass spectrometric quantification of 3-nitrotyrosine, ortho-tyrosine, and o,o′-dityrosine in brain tissue of 1-methyl-4-phenyl-1,2,3, 6-tetrahydropyridine-treated mice, a model of oxidative stress in Parkinson's disease. J. Biol. Chem. 274 (1999) 34621-34628
18. Hantraye P., Brouillet E., Ferrante R., Palfi S., Dolan R., Matthews R.T., and Beal M.F. Inhibition of neuronal nitric oxide synthase prevents MPTP-induced parkinsonism in baboons. Nat. Med. 2 (1996) 1017-1021
19. Liberatore G.T., Jackson-Lewis V., Vukosavic S., Mandir A.S., Vila M., McAuliffe W.G., Dawson V.L., Dawson T.M., and Przedborski S. Inducible nitric oxide synthase stimulates dopaminergic neurodegeneration in the MPTP model of Parkinson disease. Nat. Med. 5 (1999) 1403-1409
20. Wu D.C., Jackson-Lewis V., Vila M., Tieu K., Teismann P., Vadseth C., Choi D.K., Ischiropoulos H., and Przedborski S. Blockade of microglial activation is neuroprotective in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine mouse model of Parkinson disease. J. Neurosci. 22 (2002) 1763-1771
21. Youdim M.B., Ben-Shachar D., and Riederer P. Is Parkinson's disease a progressive siderosis of substantia nigra resulting in iron and melanin induced neurodegeneration?. Acta Neurol. Scand. 126 (1989) 47-54 Suppl.
22. Dexter D.T., Wells F.R., Lees A.J., Agid F., Agid Y., Jenner P., and Marsden C.D. Increased nigral iron content and alterations in other metal ions occurring in brain in Parkinson's disease. J. Neurochem. 52 (1989) 1830-1836
23. Sofic E., Paulus W., Jellinger K., Riederer P., and Youdim M.B. Selective increase of iron in substantia nigra zona compacta of parkinsonian brains. J. Neurochem. 56 (1991) 978-982
24. Turrens J.F., and Boveris A. Generation of superoxide anion by the NADH dehydrogenase of bovine heart mitochondria. Biochem. J. 191 (1980) 421-427
25. Hasegawa E., Takeshige K., Oishi T., Murai Y., and Minakami S. 1-Methyl-4-phenylpyridinium (MPP+) induces NADH-dependent superoxide formation and enhances NADH-dependent lipid peroxidation in bovine heart submitochondrial particles. Biochem. Biophys. Res. Commun. 170 (1990) 1049-1055
26. Ischiropoulos H., and Beckman J.S. Oxidative stress and nitration in neurodegeneration: cause, effect, or association?. J. Clin. Invest. 111 (2003) 163-169
27. Brissaud E. Nature et pathogenie de la maladie de Parkinson. Lecons Maladies Nerveuses (1895) 488-501
28. Lewy F. Paralysis agitans. I. Pathologiishe anatomie. In: Lewandowsky M. (Ed). Handbuch der neurology (1912), Springer, Berlin 920-933
29. Greenfield J.G., and Bosanquet F.D. The brain-stem lesions in Parkinsonism. J. Neurol. Neurosurg. Psychiatry 16 (1953) 213-226
30. Ehringer H., and Hornykiewicz O. [Distribution of noradrenaline and dopamine (3-hydroxytyramine) in the human brain and their behavior in diseases of the extrapyramidal system.]. Klin. Wochenschr. 38 (1960) 1236-1239
31. Poirier L.J., and Sourkes T.L. Influence of the substantia nigra on the catecholamine content of the striatum. Brain 88 (1965) 181-192
32. Cotzias G.C., and Papavasiliou P.S. Gellene, R. Modification of Parkinsonism-chronic treatment with L-dopa. N. Engl. J. Med. 280 (1969) 337-345
33. Savitt J.M., Dawson V.L., and Dawson T.M. Diagnosis and treatment of Parkinson disease: molecules to medicine. J. Clin. Invest. 116 (2006) 1744-1754
34. LaVoie M.J., Ostaszewski B.L., Weihofen A., Schlossmacher M.G., and Selkoe D.J. Dopamine covalently modifies and functionally inactivates parkin. Nat. Med. 11 (2005) 1214-1221
35. Adams R.N., Murrill E., McCreery R., Blank L., and Karolczak M. 6-Hydroxydopamine, a new oxidation mechanism. Eur. J. Pharmacol. 17 (1972) 287-292
36. Stokes A.H., Hastings T.G., and Vrana K.E. Cytotoxic and genotoxic potential of dopamine. J. Neurosci. Res. 55 (1999) 659-665
37. Spencer J.P., Jenner P., Daniel S.E., Lees A.J., Marsden D.C., and Halliwell B. Conjugates of catecholamines with cysteine and GSH in Parkinson's disease: possible mechanisms of formation involving reactive oxygen species. J. Neurochem. 71 (1998) 2112-2122
38. Spencer J.P., Whiteman M., Jenner P., and Halliwell B. 5-s-Cysteinyl-conjugates of catecholamines induce cell damage, extensive DNA base modification and increases in caspase-3 activity in neurons. J. Neurochem. 81 (2002) 122-129
39. Li H., Shen X.M., and Dryhurst G. Brain mitochondria catalyze the oxidation of 7-(2-aminoethyl)-3,4-dihydro-5-hydroxy-2H-1,4-benzothiazine-3-carboxyli c acid (DHBT-1) to intermediates that irreversibly inhibit complex I and scavenge glutathione: potential relevance to the pathogenesis of Parkinson's disease. J. Neurochem. 71 (1998) 2049-2062
40. Polymeropoulos M.H., Lavedan C., Leroy E., Ide S.E., Dehejia A., Dutra A., Pike B., Root H., Rubenstein J., Boyer R., Stenroos E.S., Chandrasekharappa S., Athanassiadou A., Papapetropoulos T., Johnson W.G., Lazzarini A.M., Duvoisin R.C., Di Iorio G., Golbe L.I., and Nussbaum R.L. Mutation in the alpha-synuclein gene identified in families with Parkinson's disease. Science 276 (1997) 2045-2047
41. Baba M., Nakajo S., Tu P.H., Tomita T., Nakaya K., Lee V.M., Trojanowski J.Q., and Iwatsubo T. Aggregation of alpha-synuclein in Lewy bodies of sporadic Parkinson's disease and dementia with Lewy bodies. Am. J. Pathol. 152 (1998) 879-884
42. Lee H.J., Shin S.Y., Choi C., Lee Y.H., and Lee S.J. Formation and removal of alpha-synuclein aggregates in cells exposed to mitochondrial inhibitors. J. Biol. Chem. 277 (2002) 5411-5417
43. Manning-Bog A.B., McCormack A.L., Li J., Uversky V.N., Fink A.L., and Di Monte D.A. The herbicide paraquat causes up-regulation and aggregation of alpha-synuclein in mice: paraquat and alpha-synuclein. J. Biol. Chem. 277 (2002) 1641-1644
44. Ostrerova-Golts N., Petrucelli L., Hardy J., Lee J.M., Farer M., and Wolozin B. The A53T alpha-synuclein mutation increases iron-dependent aggregation and toxicity. J. Neurosci. 20 (2000) 6048-6054
45. Paxinou E., Chen Q., Weisse M., Giasson B.I., Norris E.H., Rueter S.M., Trojanowski J.Q., Lee V.M., and Ischiropoulos H. Induction of alpha-synuclein aggregation by intracellular nitrative insult. J. Neurosci. 21 (2001) 8053-8061
46. Przedborski S., Chen Q., Vila M., Giasson B.I., Djaldatti R., Vukosavic S., Souza J.M., Jackson-Lewis V., Lee V.M., and Ischiropoulos H. Oxidative post-translational modifications of alpha-synuclein in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) mouse model of Parkinson's disease. J. Neurochem. 76 (2001) 637-640
47. Souza J.M., Giasson B.I., Chen Q., Lee V.M., 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 (2000) 18344-18349
48. Giasson B.I., Duda J.E., Murray I.V., Chen Q., Souza J.M., Hurtig H.I., Ischiropoulos H., Trojanowski J.Q., and Lee V.M. Oxidative damage linked to neurodegeneration by selective alpha-synuclein nitration in synucleinopathy lesions. Science 290 (2000) 985-989
49. Takahashi T., Yamashita H., Nakamura T., Nagano Y., and Nakamura S. Tyrosine 125 of alpha-synuclein plays a critical role for dimerization following nitrative stress. Brain Res. 938 (2002) 73-80
50. Hodara R., Norris E.H., Giasson B.I., Mishizen-Eberz A.J., Lynch D.R., and Lee V.M. Ischiropoulos, H. Functional consequences of alpha-synuclein tyrosine nitration: diminished binding to lipid vesicles and increased fibril formation. J. Biol. Chem. 279 (2004) 47746-47753
51. Mirzaei H., Schieler J.L., Rochet J.C., and Regnier F. Identification of rotenone-induced modifications in alpha-synuclein using affinity pull-down and tandem mass spectrometry. Anal. Chem. 78 (2006) 2422-2431
52. Benner E.J., Banerjee R., Reynolds A.D., Sherman S., Pisarev V.M., Tsiperson V., Nemachek C., Ciborowski P., Przedborski S., Mosley R.L., and Gendelman H.E. Nitrated alpha-synuclein immunity accelerates degeneration of nigral dopaminergic neurons. PLoS ONE 3 (2008) e1376
53. Wassef R., Haenold R., Hansel A., Brot N., Heinemann S.H., and Hoshi T. Methionine sulfoxide reductase A and a dietary supplement S-methyl-L-cysteine prevent Parkinson's-like symptoms. J. Neurosci. 27 (2007) 12808-12816
54. Anderson J.P., Walker D.E., Goldstein J.M., de Laat R., Banducci K., Caccavello R.J., Barbour R., Huang J., Kling K., Lee M., Diep L., Keim P.S., Shen X., Chataway T., Schlossmacher M.G., Seubert P., Schenk D., Sinha S., Gai W.P., and Chilcote T.J. Phosphorylation of Ser-129 is the dominant pathological modification of alpha-synuclein in familial and sporadic Lewy body disease. J. Biol. Chem. 281 (2006) 29739-29752
55. Smith W.W., Margolis R.L., Li X., Troncoso J.C., Lee M.K., Dawson V.L., Dawson T.M., Iwatsubo T., and Ross C.A. Alpha-synuclein phosphorylation enhances eosinophilic cytoplasmic inclusion formation in SH-SY5Y cells. J. Neurosci. 25 (2005) 5544-5552
56. Fujiwara H., Hasegawa M., Dohmae N., Kawashima A., Masliah E., Goldberg M.S., Shen J., Takio K., and Iwatsubo T. Alpha-synuclein is phosphorylated in synucleinopathy lesions. Nat. Cell Biol. 4 (2002) 160-164
57. Conway K.A., Rochet J.C., Bieganski R.M., and Lansbury Jr. P.T. Kinetic stabilization of the alpha-synuclein protofibril by a dopamine-alpha-synuclein adduct. Science 294 (2001) 1346-1349
58. Martinez-Vicente M., Talloczy Z., Kaushik S., Massey A.C., Mazzulli J., Mosharov E.V., Hodara R., Fredenburg R., Wu D.C., Follenzi A., Dauer W., Przedborski S., Ischiropoulos H., Lansbury P.T., Sulzer D., and Cuervo A.M. Dopamine-modified alpha-synuclein blocks chaperone-mediated autophagy. J. Clin. Invest. 118 (2008) 777-788
59. Norris E.H., Giasson B.I., Hodara R., Xu S., Trojanowski J.Q., Ischiropoulos H., and Lee V.M. Reversible inhibition of alpha-synuclein fibrillization by dopaminochrome-mediated conformational alterations. J. Biol. Chem. 280 (2005) 21212-21219
60. Mazzulli J.R., Armakola M., Dumoulin M., Parastatidis I., and Ischiropoulos H. Cellular oligomerization of alpha-synuclein is determined by the interaction of oxidized catechols with a C-terminal sequence. J. Biol. Chem. 282 (2007) 31621-31630
61. Dalfo E., and Ferrer I. Early alpha-synuclein lipoxidation in neocortex in lewy body diseases. Neurobiol. Aging (2006)
62. Kitada T., Asakawa S., Hattori N., Matsumine H., Yamamura Y., Minoshima S., Yokochi M., Mizuno Y., and Shimizu N. Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature 392 (1998) 605-608
63. Hyun D.H., Lee M., Hattori N., Kubo S., Mizuno Y., Halliwell B., and Jenner P. Effect of wild-type or mutant Parkin on oxidative damage, nitric oxide, antioxidant defenses, and the proteasome. J. Biol. Chem. 277 (2002) 28572-28577
64. Palacino J.J., Sagi D., Goldberg M.S., Krauss S., Motz C., Wacker M., Klose J., and Shen J. Mitochondrial dysfunction and oxidative damage in parkin-deficient mice. J. Biol. Chem. 279 (2004) 18614-18622
65. Chung K.K., Thomas B., Li X., Pletnikova O., Troncoso J.C., Marsh L., Dawson V.L., and Dawson T.M. S-nitrosylation of parkin regulates ubiquitination and compromises parkin's protective function. Science 304 (2004) 1328-1331
66. Bonifati V., Rizzu P., van Baren M.J., Schaap O., Breedveld G.J., Krieger E., Dekker M.C., Squitieri F., Ibanez P., Joosse M., van Dongen J.W., Vanacore N., van Swieten J.C., Brice A., Meco G., van Duijn C.M., Oostra B.A., and Heutink P. Mutations in the DJ-1 gene associated with autosomal recessive early-onset parkinsonism. Science 299 (2003) 256-259
67. Cookson M.R. The biochemistry of Parkinson's disease. Annu. Rev. Biochem. 74 (2005) 29-52
68. Mitsumoto A., Nakagawa Y., Takeuchi A., Okawa K., Iwamatsu A., and Takanezawa Y. Oxidized forms of peroxiredoxins and DJ-1 on two-dimensional gels increased in response to sublethal levels of paraquat. Free Radic. Res. 35 (2001) 301-310
69. Yokota T., Sugawara K., Ito K., Takahashi R., Ariga H., and Mizusawa H. Down regulation of DJ-1 enhances cell death by oxidative stress, ER stress, and proteasome inhibition. Biochem. Biophys. Res. Commun. 312 (2003) 1342-1348
70. Choi J., Sullards M.C., Olzmann J.A., Rees H.D., Weintraub S.T., Bostwick D.E., Gearing M., Levey A.I., Chin L.S., and Li L. Oxidative damage of DJ-1 is linked to sporadic Parkinson and Alzheimer diseases. J. Biol. Chem. 281 (2006) 10816-10824
71. Bandopadhyay R., Kingsbury A.E., Cookson M.R., Reid A.R., Evans I.M., Hope A.D., Pittman A.M., Lashley T., Canet-Aviles R., Miller D.W., McLendon C., Strand C., Leonard A.J., Abou-Sleiman P.M., Healy D.G., Ariga H., Wood N.W., de Silva R., Revesz T., Hardy J.A., and Lees A.J. The expression of DJ-1 (PARK7) in normal human CNS and idiopathic Parkinson's disease. Brain 127 (2004) 420-430
72. Meulener M.C., Xu K., Thomson L., Ischiropoulos H., and Bonini N.M. Mutational analysis of DJ-1 in Drosophila implicates functional inactivation by oxidative damage and aging. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 12517-12522
73. Kinumi T., Kimata J., Taira T., Ariga H., and Niki E. Cysteine-106 of DJ-1 is the most sensitive cysteine residue to hydrogen peroxide-mediated oxidation in vivo in human umbilical vein endothelial cells. Biochem. Biophys. Res. Commun. 317 (2004) 722-728
74. Ooe H., Maita C., Maita H., Iguchi-Ariga S.M., and Ariga H. Specific cleavage of DJ-1 under an oxidative condition. Neurosci. Lett. 406 (2006) 165-168
75. Canet-Aviles R.M., Wilson M.A., Miller D.W., Ahmad R., McLendon C., Bandyopadhyay S., Baptista M.J., Ringe D., Petsko G.A., and Cookson M.R. The Parkinson's disease protein DJ-1 is neuroprotective due to cysteine-sulfinic acid-driven mitochondrial localization. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 9103-9108
76. Andres-Mateos E., Perier C., Zhang L., Blanchard-Fillion B., Greco T.M., Thomas B., Ko H.S., Sasaki M., Ischiropoulos H., Przedborski S., Dawson T.M., and Dawson V.L. DJ-1 gene deletion reveals that DJ-1 is an atypical peroxiredoxin-like peroxidase. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 14807-14812
77. Ito G., Ariga H., Nakagawa Y., and Iwatsubo T. Roles of distinct cysteine residues in S-nitrosylation and dimerization of DJ-1. Biochem. Biophys. Res. Commun. 339 (2006) 667-672
78. Hoepken H.H., Gispert S., Morales B., Wingerter O., Del Turco D., Mulsch A., Nussbaum R.L., Muller K., Drose S., Brandt U., Deller T., Wirth B., Kudin A.P., Kunz W.S., and Auburger G. Mitochondrial dysfunction, peroxidation damage and changes in glutathione metabolism in PARK6. Neurobiol. Dis. 25 (2007) 401-411
79. Wang D., Qian L., Xiong H., Liu J., Neckameyer W.S., Oldham S., Xia K., Wang J., Bodmer R., and Zhang Z. Antioxidants protect PINK1-dependent dopaminergic neurons in Drosophila. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 13520-13525
80. Pridgeon J.W., Olzmann J.A., Chin L.S., and Li L. PINK1 protects against oxidative stress by phosphorylating mitochondrial chaperone TRAP1. PLoS Biol. 5 (2007) e172
81. Nicklas W.J., Vyas I., and Heikkila R.E. 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 (1985) 2503-2508
82. Heikkila R.E., Nicklas W.J., Vyas I., and Duvoisin R.C. Dopaminergic toxicity of rotenone and the 1-methyl-4-phenylpyridinium ion after their stereotaxic administration to rats: implication for the mechanism of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine toxicity. Neurosci. Lett. 62 (1985) 389-394
83. Schapira A.H., Cooper J.M., Dexter D., Jenner P., Clark J.B., and Marsden C.D. Mitochondrial complex I deficiency in Parkinson's disease. Lancet 1 (1989) 1269
84. Jenner P. Altered mitochondrial function, iron metabolism and glutathione levels in Parkinson's disease. Acta Neurol. Scand. 146 (1993) 6-13 Suppl.
85. Jha N., Jurma O., Lalli G., Liu Y., Pettus E.H., Greenamyre J.T., Liu R.M., Forman H.J., and Andersen J.K. Glutathione depletion in PC12 results in selective inhibition of mitochondrial complex I activity. Implications for Parkinson's disease. J. Biol. Chem. 275 (2000) 26096-26101
86. Taylor E.R., Hurrell F., Shannon R.J., Lin T.K., Hirst J., and Murphy M.P. Reversible glutathionylation of complex I increases mitochondrial superoxide formation. J. Biol. Chem. 278 (2003) 19603-19610
87. Beer S.M., Taylor E.R., Brown S.E., Dahm C.C., Costa N.J., Runswick M.J., and Murphy M.P. Glutaredoxin 2 catalyzes the reversible oxidation and glutathionylation of mitochondrial membrane thiol proteins: implications for mitochondrial redox regulation and antioxidant DEFENSE. J. Biol. Chem. 279 (2004) 47939-47951
88. Hsu M., Srinivas B., Kumar J., Subramanian R., and Andersen J. Glutathione depletion resulting in selective mitochondrial complex I inhibition in dopaminergic cells is via an NO-mediated pathway not involving peroxynitrite: implications for Parkinson's disease. J. Neurochem. 92 (2005) 1091-1103
89. Chinta S.J., Kumar J.M., Zhang H., Forman H.J., and Andersen J.K. Up-regulation of gamma-glutamyl transpeptidase activity following glutathione depletion has a compensatory rather than an inhibitory effect on mitochondrial complex I activity: implications for Parkinson's disease. Free Radic. Biol. Med. 40 (2006) 1557-1563
90. Murray J., Taylor S.W., Zhang B., Ghosh S.S., and Capaldi R.A. Oxidative damage to mitochondrial complex I due to peroxynitrite: identification of reactive tyrosines by mass spectrometry. J. Biol. Chem. 278 (2003) 37223-37230
91. Bharath S., and Andersen J.K. Glutathione depletion in a midbrain-derived immortalized dopaminergic cell line results in limited tyrosine nitration of mitochondrial complex I subunits: implications for Parkinson's disease. Antioxid. Redox Signal. 7 (2005) 900-910
92. Chinta S.J., Kumar M.J., Hsu M., Rajagopalan S., Kaur D., Rane A., Nicholls D.G., Choi J., and Andersen J.K. Inducible alterations of glutathione levels in adult dopaminergic midbrain neurons result in nigrostriatal degeneration. J. Neurosci. 27 (2007) 13997-14006
93. Keeney P.M., Xie J., Capaldi R.A., and Bennett Jr. J.P. Parkinson's disease brain mitochondrial complex I has oxidatively damaged subunits and is functionally impaired and misassembled. J. Neurosci. 26 (2006) 5256-5264
94. Sherer T.B., Betarbet R., Testa C.M., Seo B.B., Richardson J.R., Kim J.H., Miller G.W., Yagi T., Matsuno-Yagi A., and Greenamyre J.T. Mechanism of toxicity in rotenone models of Parkinson's disease. J. Neurosci. 23 (2003) 10756-10764
95. Kweon G.R., Marks J.D., Krencik R., Leung E.H., Schumacker P.T., Hyland K., and Kang U.J. Distinct mechanisms of neurodegeneration induced by chronic complex I inhibition in dopaminergic and non-dopaminergic cells. J. Biol. Chem. 279 (2004) 51783-51792
96. Halliwell B. Hypothesis: proteasomal dysfunction: a primary event in neurogeneration that leads to nitrative and oxidative stress and subsequent cell death. Ann. N. Y. Acad. Sci. 962 (2002) 182-194
97. Friguet, B.; Szweda, L. I. Inhibition of the multicatalytic proteinase (proteasome) by 4-hydroxy-2-nonenal cross-linked protein. FEBS Lett. 405 (1997) 21-25
98. Okada K., Wangpoengtrakul C., Osawa T., Toyokuni S., Tanaka K., and Uchida K. 4-Hydroxy-2-nonenal-mediated impairment of intracellular proteolysis during oxidative stress. Identification of proteasomes as target molecules. J. Biol. Chem. 274 (1999) 23787-23793
99. Grune T., and Davies K.J. The proteasomal system and HNE-modified proteins. Mol. Aspects Med. 24 (2003) 195-204
100. Bennett M.C., Bishop J.F., Leng Y., Chock P.B., Chase T.N., and Mouradian M.M. Degradation of alpha-synuclein by proteasome. J. Biol. Chem. 274 (1999) 33855-33858
101. Lee M.H., Hyun D.H., Jenner P., and Halliwell B. Effect of proteasome inhibition on cellular oxidative damage, antioxidant defences and nitric oxide production. J. Neurochem. 78 (2001) 32-41
102. Ara J., Przedborski S., Naini A.B., Jackson-Lewis V., Trifiletti R.R., Horwitz J., and Ischiropoulos H. Inactivation of tyrosine hydroxylase by nitration following exposure to peroxynitrite and 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP). Proc Natl. Acad. Sci. U. S. A. 95 (1998) 7659-7663
103. Blanchard-Fillion B., Souza J.M., Friel T., Jiang G.C., Vrana K., Sharov V., Barron L., Schoneich C., Quijano C., Alvarez B., Radi R., Przedborski S., Fernando G.S., Horwitz J., and Ischiropoulos H. Nitration and inactivation of tyrosine hydroxylase by peroxynitrite. J. Biol. Chem. 276 (2001) 46017-46023
104. Kuhn D.M., Sadidi M., Liu X., Kreipke C., Geddes T., Borges C., and Watson J.T. Peroxynitrite-induced nitration of tyrosine hydroxylase: identification of tyrosines 423, 428, and 432 as sites of modification by matrix-assisted laser desorption ionization time-of-flight mass spectrometry and tyrosine-scanning mutagenesis. J. Biol. Chem. 277 (2002) 14336-14342
105. Sadidi M., Geddes T.J., and Kuhn D.M. S-thiolation of tyrosine hydroxylase by reactive nitrogen species in the presence of cysteine or glutathione. Antioxid. Redox Signal. 7 (2005) 863-869