Decreased proteolysis caused by protein aggregates, inclusion bodies, plaques, lipofuscin, ceroid, and 'aggresomes' during oxidative stress, aging, and disease

International Journal of Biochemistry and Cell Biology

Volumn 36, Issue 12, 2004, Pages 2519-2530

  Grune, Tilman ^a   Jung, Tobias ^a   Merker, Katrin ^a   Davies, Kelvin J A ^b  

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Aging; Proteasome; Protein aggregates; Protein oxidation

Indexed keywords

CEROID; FRATAXIN; HUNTINGTIN; LIPOFUSCIN; PROTEASOME; PROTEIN; SYNUCLEIN; TAU PROTEIN;

AGING; AMINO ACID SEQUENCE; APOPTOSIS; CELL INCLUSION; CELL METABOLISM; CELL NUCLEUS; CROSS LINKING; CRYSTALLIZATION; CYTOPLASM; DEGENERATIVE DISEASE; EXTRACELLULAR MATRIX; GENERAL ASPECTS OF DISEASE; HUMAN; HYDROLYSIS; MITOCHONDRION; MUTATION; NONHUMAN; OXIDATION; OXIDATIVE STRESS; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN METABOLISM; PROTEIN MODIFICATION; REVIEW; SEQUENCE ANALYSIS; UBIQUITINATION;

AGING; ANIMALS; CEROID; HUMANS; INCLUSION BODIES; LIPOFUSCIN; NEURODEGENERATIVE DISEASES; OXIDATION-REDUCTION; OXIDATIVE STRESS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN STRUCTURE, QUATERNARY; PROTEINS;

EID: 4344677922     PISSN: 13572725     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biocel.2004.04.020     Document Type: Review

References (117)

1. Agarwal S., Sohal R.S. Aging and proteolysis of oxidized proteins. Arch. Biochem. Biophys. 309:1994;24-28
2. Aloj-Totaro E., Cuomo V., Pisanti F.A. Influence of environmental stress on lipofuscin production. Arch. Gerontol. Geriatr. 5:1986;343-349
3. Anselmi B., Conconi M., Veyrat-Durebex C., Turlin E., Biville F., Alliot J., Friguet B. Dietary self-selection can compensate an age-related decrease of rat liver 20S proteasome activity observed with standard diet. J. Gerontol. 53:1998;B173-B179
4. Baldwin A.S. The NF-κB and I-κB proteins: New discoveries and insights. Annu. Rev. Immunol. 14:1996;649-683
5. Beal T., Toscano-Cantaffa D., Young P., Rechsteiner M., Pickart C.M. The hydrophobic effect contributes to polyubiquitin chain recognition. Biochemistry. 37:1998;2925-2934
6. Bence D., Samapat R.M., Kopito R.R. Impairment of the Ubitquitin-Proteasome system by protein aggregation. Science. 292:2001;1552-1555
7. Berlett B.S., Stadtman E.R. Protein oxidation in aging disease, and oxidative stress. J. Biol. Chem. 272:1997;20313-20316
8. Brunk U.T., Jones C.B., Sohal R.S. A novel hypothesis of lipofuscinogenesis and cellular aging based on interactions between oxidative stress and autophagocytosis. Mutat. Res. 275:1992;395-403
9. Carmichael W., Schwartz J., Furlong R.A., Naranin Y., Rankin J., Rubinsztein D.C. Effects of heat shock, heat shock protein 40 (HDJ-2), and proteasome inhibition on protein aggregation in cellular models of Huntington's disease. Proc. Natl. Acad. Sci. U.S.A. 97:2000;2898-2903
10. Carney J.M., Starke-Reed P.E., Oliver C.N., Landrum R.W., Cheng M.S., Wu J.F., Floyd R.A. Reversal of age-related increase in brain protein oxidation, decrease in enzyme activity, and loss in temporal and spatial memory by chronic administration of the spin-trapping compound N-tert-butyl-a-phenylnitone. Proc. Natl. Acad. Sci. U.S.A. 88:1991;3633-3636
11. Carpenter, K. L. H., van der Veen, C., Taylor, S. E., Hardwick, S. J., Clare, K., Hegyi, L., & Mitchinson, M. J. (1995). Macrophages, lipid oxidation, ceroid accumulation and alpha-tocopherol depletion in human atherosclerotic lesions. In K. Kitani, G. O. Ivy, & H. Shimasaki (Eds.), Lipofuscin and ceroid pigments (pp. 53-64). Basel: S. Karger.
12. Ciechanover P.B. The ubiquitin proteasome system in neurodegenerative diseases: Sometimes the chicken, sometimes the egg. Neuron. 40:2003;427-446
13. Conconi M., Friguet B. Proteasome inactivation upon aging and on oxidation-effect of HSP 90. Mol. Biol. Rep. 24:1997;45-50
14. Conconi M., Szweda L.I., Levine R.L., Stadtman E.R., Friguet B. Age-related decline of rat liver multicatalytic proteinase activity and protection from oxidative inactivation by heat-shock protein 90. Arch. Biochem. Biophys. 331:1996;232-240
15. Coux O., Tanaka K., Goldberg A.L. Structure and functions of the 20S and 26S proteasomes. Annu. Rev. Biochem. 65:1996;801-847
16. Cummings J., Reinstein E., Sun Y., Antalffy B., Jiang Y., Chiechanover A., Orr H.T., Beaudet A.L., Zoghbi H.Y. Mutation of the E6-AP ubiqutin ligase reduces nuclear inclusion frequency while accelerating polyglutamine-induced pathology in SCA 1 mice. Neuron. 24:1999;879-892
17. Davies, K. J. A., & Delsignore, M. E. (1987). Protein damage and degradation by oxygen radicals: III. Modification of secondary and tertiary structure. J. Biol. Chem. 9908-9913.
18. Davies K.J.A. Intracellular proteolytic systems may function as secondary antioxidant defenses: A hypothesis. Free Radic. Biol. Med. 2:1986;155-173
19. Davies K.J.A. Protein damage and degradation by oxygen radicals: I. General aspects. J. Biol. Chem. 262:1987;9895-9901
20. Davies K.J.A. Degradation of oxidized proteins by 20S proteasome. Biochimie. 83:2001;1-10
21. Davies K.J.A., Delsignore M.E., Lin S.W. Protein damage and degradation by oxygen radicals: II. Modification of amino acids. J. Biol. Chem. 262:1987;9902-9907
22. Davies, K. J. A., Lin, S. W., Pacifici, R. E. (1987). Protein damage and degradation by oxygen radicals: IV. Degradation of denatured proteins. J. Biol. Chem. 9914-9920.
23. Dean R.T., Fu S., Stocker R., Davies M.J. Biochemistry and pathology of radical-mediated proteinoxidation. Biochem. J. 324:1997;1-18
24. Fabunmi R.P., Wigley W.C., Thomas P.J., DeMartino G.N. Activity and regulation of the centrosome-associated proteasome. Nature. 404:2000;770-774
25. Falkenburg P.E., Haass C., Kloetzel P.M., Niedel B., Kopp F., Kuehn L., Dahlmann B. Drosophila small cytoplasmic 19S ribonucleoprotein is homologous to the rat multicatalytic proteinase. Nature. 331:1988;190-192
26. Fearnley I.M., Walker J.E., Martinus R.D., Jolly R.D., Kirkland K.B., Shaw G.J., Palmer D.N. The sequence of the major protein stored in ovine ceroid lipofuscinosis is identical with that of the dicyclohexylcarbodiimide-reactive proteolipid of mitochondrial ATP synthase. Biochem. J. 268:1990;751-758
27. Fink L. Protein aggregation: Folding aggregates, inclusion bodies and amyloid. Fold Des. 3:1998;R9-R23
28. Floyd R.A. Antioxidants, oxidative stress and degenerative neurological disorders. Proc. Soc. Exp. Biol. Med. 222:1999;236-245
29. Friedhoff P., van Bergen M., Mandelkow E.M., Mandelkow E. Structure of tau protein and assambly into paired helical filaments. Biochim. Biophys. Acta. 1502:2000;122-132
30. 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
31. Friguet B., Stadtman E.R., Szweda L.I. Modification of glucose-6-phosphate dehydrogenase by 4-hydroxy-2-nonenal. Formation of cross-linked protein that inhibits the multicatalytic protease. J. Biol. Chem. 269:1994;21639-21643
32. Gieche J., Mehlhase J., Licht A., Zacke T., Sitte N., Grune T. Protein oxidation and proteolysis in RAW264.7 macrophages: Effects of PMA activation. Biochim. Biophys. Acta. 1538:2001;321-328
33. Glickman M.H., Ciechanover A. The ubiquitin-proteasome proteolytic pathway: Destruction for the sake of construction. Physiol. Rev. 82:2002;373-428
34. Goldberg A.L. Protein degradation and protection against misfolded or damaged proteins. Nature. 426:2003;895-899
35. Gracia-Mata R., Bebock Z., Sorscher E.J., Sztul E.S. Characterization and dynamics of aggresome formation by a cytosolic GFP chimera. J. Cell Biol. 146:1999;1239-1254
36. Grune T., Blasig I.E., Sitte N., Roloff B., Haseloff R., Davies K.J.A. Peroxynitrite increases the degradation of aconitase and other cellular proteins by proteasome. J. Biol. Chem. 273:1998;10857-10862
37. Grune T., Klotz L.O., Gieche J., Rudeck M., Sies H. Protein oxidation and proteolysis by the nonradical oxidants singlet oxygen or peroxynitrite. Free Radic. Biol. Med. 30:2001;1243-1253
38. Grune T., Reinheckel T., Davies K.J.A. Degradation of oxidized proteins in K562 human hematopoietic cells by proteasome. J. Biol. Chem. 271:1996;15504-15509
39. Grune T., Reinheckel T., Davies K.J.A. Degradation of oxidized proteins in mammalian cells. FASEB J. 11:1997;526-534
40. Grune T., Reinheckel T., Joshi M., Davies K.J.A. Proteolysis in cultered liver epithelial cells during oxidative stress: Role of the multicatalytic proteinase complex, proteasome. J. Biol. Chem. 270:1995;2344-2351
41. Grune T., Shringarpure R., Sitte N., Davies K.J.A. Age related changes in Protein oxidation and Proteolysis in mammalian cells. J. Gerontol. Biol. Sci. 56A:2001;B459-B467
42. Hannover (1842). Mikroskopiske undersögelser af nervesystemet, Kgl. Danske Videsk. Kabernes Selskobs Naturv. Math. Afh. (Copenhagen) 10, 1-112.
43. Hendil K.B., Khan S., Tanaka K. Simultaneous binding of PA28 and PA700 activators to 20S proteasomes. Biochem. J. 332:1998;749-754
44. Hilt W., Wolf D.H. Proteasomes: Destruction as a programme. TIBS. 21:1996;96-102
45. Hunt J.V., Bottoms M.A., Clare K., Skarmarauskas J.T., Mitchinson M.J. Glucose oxidation and low-density lipoprotein-induced macrophage ceroid accumulation: Possible implications for diabetic atherosclerosis. Biochem. J. 300:1994;243-249
46. Ishida M., Lui G.M., Yamani A., Sugino I.K., Zarbin M.A. Culture of human retinal pigment epithelial cells from peripheral scleral flap biopsies. Cur. Eye Res. 17:1998;392-402
47. Jahngen-Hodge J., Obin M.S., Gong X., Shang F., Nowell T.R. Jr., Gong J., Abasi H., Blumberg J., Taylor A. Regulation of ubiquitin-conjugating enzymes by glutathione following oxidative stress. J. Biol. Chem. 272:1997;28218-28226
48. Johnston C.L., Ward C.L., Kopito R.R. Aggresomes: A cellular response to misfolded proteins. J. Cell Biol. 143:1998;1883-1898
49. Jolly, R. D., Douglas, B. V., Davey, P. M., & Roiri, J. E. (1995). Lipofuscin in bovine muscle and brain: A model for studying age pigment. In K. Kitani, G. O. Ivy, & H. Shimasaki (Eds.), Lipofuscin and ceroid pigments (pp. 283-293). Basel: S. Karger.
50. Kaltschmidt T.P., Uhereck M., Volk B., Baeuerle P.A., Kaltschmidt C. Transcription factor NF-Kappa B is activated in primary neurons by amyloid-ß peptides and in neurons surrounding early plaques from patients with Alzheimer's disease. Proc. Natl. Acad. Sci. U.S.A. 94:1997;2642-2647
51. Kato Y., Maruyama W., Naoi M., Hashizume Y., Osawa T. Immunohistochemical detection of dityrosine in lipofuscin pigments in the aged human brain. FEBS Lett. 439:1998;231-234
52. Katz M.L., Christianson J.S., Norbury N.E., Gao C.L., Siakos A.N., Koppang N. Lysine methylation of mitochondrial ATP synthase subunit c stored in tissues of dogs with hereditary ceroid lipofuscinosis. J. Biol. Chem. 269:1994;9906-9911
53. Keck S., Nitsch R., Grune T., Ullrich O. Proteasome inhibition by paired helical filament-tau in brains of patients with Alzheimer's disease. J. Neurochem. 85:2003;115-122
54. Keller J.N., Gee J., Ding Q. The proteasome in brain aging. Ageing Res. Rev. 1:2002;279-293
55. Kisselev A.F., Karganovich D., Goldberg A.L. Binding of hydrophobic peptides to several non-catalytic sites promotes peptide hydrolysis by all active sites of the 20S proteasomes. Evidence for peptide-induced channel opening in the alpha rings. J. Biol. Chem. 277:2002;22260-22270
56. Klikugawa, K., Beppu, M., & Sato, A. (1995). Extraction and purification of yellow-fluorescent lipofuscin in rat kidney. In K. Kitani, G. O. Ivy, & H. Shimasaki (Eds.), Lipofuscin and ceroid pigments (pp. 1-12). Basel: S. Karger.
57. Koneff J.H. Beiträge zur Kenntnis der Nervenzellen der peripheren Ganglien. Mitt. Naturforsch. Gesellsch. Bern. 44:1886;13-14
58. Kopito R.R. Aggresomes, inclusion bodies and protein aggregation. Trends Cell Biol. 10:2000;524-530
59. Lansbury P.T. Structural neurology: Are seeds at the root of neuronal degeneration? Neuron. 19:1997;1151-1154
60. Lasch P., Petras T., Ullrich O., Backmann J., Naumann D., Grune T. Hydrogen peroxide-induced structural alterations of RNaseA. J. Biol. Chem. 276:2001;9492-9502
61. Mehlhase J., Gieche J., Ullrich O., Sitte N., Grune T. LPS-induced protein oxidation and proteolysis in BV-2 microglial cells. IUBMB life. 50:2000;331-335
62. Merker K., Stolzing A., Grune T. Proteolysis, caloric restriction and aging. Mech. Aging Dev. 122:2001;595-615
63. Nagy, Z., Streiber, J., & Jeney, F. (1995). Induction of age pigment accumulation in the brain cells of young male rats through iron-injection into the cerebrospinal fluid. In K. Kitani, G. O. Ivy, & H. Shimasaki (Eds.), Lipofuscin and ceroid pigments (pp. 145-156). Basel: S. Karger.
64. Nakano, M., Oenzil, F., Mizuno, T., & Gotoh, S. (1995). Age-related changes in the lipofuscin accumulation of brain and heart. In K. Kitani, G. O. Ivy, & H. Shimasaki (Eds.), Lipofuscin and ceroid pigments (pp. 69-77). Basel: S. Karger.
65. Nakano, M., Oenzil, F., Mizuno, T., & Gotoh, S. (1995). Age-related changes in the lipofuscin accumulation of brain and heart. In K. Kitani, G. O. Ivy, & H. Shimasaki (Eds.), Lipofuscin and ceroid pigments (pp. 69-77). Basel: S. Karger.
66. Obin M.S., Shang F., Gong X., Handelman G., Blumberg J., Taylor A. Redox regulation of ubiquitin-conjugating enzymes: Mechanistic insights using the thiol-specific oxidant diamide. FASEB J. 12:1998;561-569
67. Pacifici R.E., Davies K.J.A. Protein degradation as an index of oxidative stress. Methods Enzym. 186:1990;485-502
68. Pacifici R.E., Kono Y., Davies K.J.A. Hydrophobicity as the signal for selective degradation of hydroxyl radical-modified hemoglobin by the multicatalytic proteinase complex, proteasome. J. Biol. Chem. 268(21):1993;15405-25411
69. Pacifici R.E., Salo D.C., Davies K.J.A. Macroxyproteinase (M.O.P.): A 670 kDa proteinase complex that degrades oxidatively denaturated proteins in red blood cells. Free Radic. Biol. Med. 7:1989;521-536
70. Passer B.J., Pellegrini L., Vito P., Ganjei J.K., D'Adamio L. Interaction of Alzheimer's presenilins with Bcl-XL: A potential role in modulating the threshold of cell death. J. Biol. Chem. 247:1999;24007-24013
71. Paulson H.L., Perez M.K., Trottier Y., Trojanowski J.Q., Subramony S.H., Das S.S., Vig P., Mandel J.L., Fishbeck K.H., Pittman R.N. Intranuclear inculsions of expanded polyglutamine protein in spinocerebellar ataxia type 3. Neuron. 19:1997;333-344
72. Pawelec G., Muller R., Rehbein A., Hahnel K., Ziegler B.L. Finite life spans of T cell clones derived from CD34+ human hematopoietic stem cells in vitro. Exp. Gerontol. 34:1999;69-77
73. Peters J.M. Proteasomes. Protein degradation machines of the cell. TIBS. 19:1994;377-382
74. Ravikumar B., Duden R., Rubinsztein D.C. Aggregate-prone proteins with polyglutamine and polyalanine expansions are degraded by autophagy. Hum. Mol. Genet. 11:2002;1107-1117
75. Ravikumar B., Stewart A., Kita H., Kato K., Duden R., Rubinsztein D.C. Raised intracellular glucose concentrations reduce aggregation and cell death caused by mutant huntingtin exon 1 by decreasing mTOR phosphorylation and inducing autophagy. Hum. Mol. Genet. 12:2003;985-994
76. Rechsteiner M., Hoffman L., Dubiel W. The multicatalytic and the 26S proteases. J. Biol. Chem. 268:1993;6065-6068
77. Reichel E., Holander J., Clark H.J., Strehler B.L. Lipofuscin pigment accumulation as a function of age and distribution in rodent brain. J. Gerontol. 23:1968;71-78
78. Reinheckel T., Sitte N., Ullrich O., Kuckelkorn U., Davies K.J.A., Grune T. Comparative resistance of the 20S and 26S proteasome to oxidative stress. Biochem. J. 335:1998;637-642
79. Reinheckel T., Ullrich O., Sitte N., Grune T. Differential impairment of 20S and 26S proteasome activities in human hematopoietic K562 cells during oxidative stress. Arch. Biochem. Biophys. 377:2000;65-68
80. Rivett A.J. Preferential degradation of the oxidatively modified form of glutamine synthetase by intracellular mammalian proteases. J. Biol. Chem. 260:1985;300-305
81. Rivett A.J. Purification of a liver alkaline protease which degrades oxidatively modified glutamine synthetase. Characterization as a high molecular weight cysteine proteinase. J. Biol. Chem. 260:1985;12600-12606
82. Rivett A.J. Proteasomes: Multicatalytic proteinase complexes. Biochem. J. 291:1993;1-10
83. Rivett A.J. Intracellular distribution of proteasomes. Curr. Opin. Immunol. 10:1998;110-114
84. Rock K.L., Gramm C., Rothstein L., Clark L.K., Stein R., Dick L., Hwang D., Goldberg A.L. Inhibitors of proteasome block the degradation of most cell proteins and the generation of peptides on MHC class I molecules. Cell. 78:1994;761-771
85. Sahakian, J. A., Szweda, L. I., Friguet, B., Kitani, K., Levine, R.L. (1995). Aging of the liver: Proteolysis of oxidatively modified glutamine synthetase. Arch. Biochem. Biophys. 318, 411-417.
86. Salo D.C., Pacifici R.E., Lin S.W., Giulivi C., Davies K.J.A. Superoxide dismutase undergoes proteolysis and fragmentation following oxidative modification and inactivation. J. Biol. Chem. 265:1990;11919-11927
87. Sanchez P., Xu C.J., Juo P., Kakizaka A., Blenis J., Yaun J. Caspase-8 is required for cell death induced by expanded polyglutamine repeats. Neuron. 22:1999;623-633
88. Shang F., Taylor A. Oxidative stress and recovery from oxidative stress are associated with altered ubiquitin conjugating and proteolytic activities in bovine lens epithelial cells. Biochem. J. 307:1995;297-303
89. Shang F., Gong X., Taylor A. Activity of ubiquitin-dependent pathway in response to oxidative stress. J. Biol. Chem. 272:1997;23086-23093
90. Sherman M.Y., Goldberg A.L. Cellular defenses against unfolded proteins: A cell biologist thinks about neurodegenerative diseases. Neuron. 29:2001;15-32
91. Shimasaki, H., Maeba, R., Tachibana, R., & Ueta, N. (1995). Lipid peroxidation and ceroid accumulation in macrophages cultured with oxidized low density lipoprotein. In K. Kitani, G. O. Ivy, & H. Shimasaki (Eds.), Lipofuscin and ceroid pigments (pp. 39-48). Basel: S. Karger.
92. Shringarpure R., Grune T., Mehlhase J., Davies K.J.A. Ubiquitin-conjugation is not required for the degradation of oxidized proteins by the proteasome. J. Biol. Chem. 278:2003;311-318
93. Shringarpure R., Grune T., Sitte N., Davies K.J.A. 4-Hydroxynonenal- modified amyloid-β peptide inhibits the proteasome: Possible importance for Alzheimer's disease. Cell. Mol. Life Sci. 57:2000;1802-1809
94. Sitte N., Huber M., Grune T., Ladhoff A., Doecke W.-D., von Zglinicki T., Davies K.J.A. Proteasome inhibition by lipofuscin/ceroid during postmitotic aging of fibroblasts. FASEB J. 14:2000;1490-1498
95. Sitte N., Merker K., Grune T. Proteasome-dependent degradation of oxidized proteins in MRC-5 fibroblasts. FEBS Lett. 440:1998;399-402
96. Sitte N., Merker K., von Zglinicki T., Davies K.J.A., Grune T. Protein oxidation and degradation during cellular senescence of human BJ fibroblasts: Part II - Aging of non-dividing fibroblasts. FASEB J. 14:2000;2502-2509
97. Sitte N., Merker K., von Zglinicki T., Grune T., Davies K.J.A. Protein oxidation and degradation during cellular senescence of human BJ fibroblasts: Part I - effects of proliferative senescence. FASEB J. 14:2000;2495-2502
98. Smith S.E., Koegl M., Jentsch S. Role of the ubiquitin/proteasome system in regulated protein degradation in Saccharomyces cerevistae. Biol. Chem. 377:1996;437-446
99. Sohal R.S., Brunk U.T. Lipofuscin as an indicator of oxidative stress and aging. Adv. Exp. Med. Biol. 266:1996;17-26
100. Sommerburg O., Ullrich O., Sitte N., von Zglinicki T., Siems W., Grune T. Dose- and wavelength-dependent oxidation of crystallins by UV light - selective recognition and degradation by the 20S proteasome. Free Radic. Biol. Med. 24:1998;1369-1374
101. Stadtman E.R. Oxidation of free amino acids and amino acid residues in proteins by radiolysis and by metal-catalyzed reactions. Annu. Rev. Biochem. 62:1993;797-821
102. Stadtman E.R., Starke-Reed P.E., Oliver C.N., Carney J.M., Floyd R.A. Protein modification in aging. Exs. 62:1992;64-72
103. Starke-Reed P.E., Oliver C.N. Protein oxidation and proteolysis during aging and oxidative stress. Arch. Biochem. Biophys. 275:1989;559-567
104. Strehler B.L., Mark D.D., Mildvan A.S., Gee M.V. Rate of magnitude of age pigment accumulation in the human myocardium. J. Gerontol. 14:1959;430-439
105. Tanahashi N., Murakami Y., Minami Y., Shimbara N., Hendil K.B., Tanaka K. Hybrid proteasomes. Induction by interferon-gamma and contribution to ATP-dependent proteolysis. J. Biol. Chem. 275:2000;14336-14345
106. Ullrich O., Reinheckel T., Sitte N., Hass R., Grune T., Davies K.J.A. Poly-ADP ribose polymerase activates nuclear proteasome to degrade oxidatively damaged histones. Proc. Natl. Acad. Sci. U.S.A. 96:1999;6223-6228
107. Ullrich O., Sitte N., Sommerburg O., Sandig V., Davies K.J.A., Grune T. Influence of DNA binding on the degradation of oxidized histones by the 20S proteasome. Arch. Biochem. Biophys. 362:1999;211-216
108. Voges D., Zwickl P., Baumeister W. The 26S proteasome: A molecular machine designed for controlled proteolysis. Annu. Rev. Biochem. 68:1999;1015-1068
109. Waelter S., Bodderich A., Lurz R., Scherzinger E., Lueder G., Lehrach H., Wanker E.E. Accumulation of mutant huntingtin fragments in aggresome-like inclusion bodies as a result of insufficient protein degradation. Mol. Biol. Cell. 12:2001;1393-1407
110. Webb J.L., Ravikumar B., Atkins J., Skepper J.N., Rubinsztein D.C. Alpha-Synuclein is degraded by both autophagy and the proteasome. J. Biol. Chem. 278:2003;25009-25013
111. Wetzel R., Behl C. Mutations off-pathway aggregation of proteins. Trends Biotechnol. 12:1994;193-198
112. Wickner S., Maurizi M.R., Gottesman S. Posttranslational quality control: Folding, refolding, and degrading proteins. Science. 286:1999;1888-1893
113. Wojcik C., DeMartino G.N. Intracellular localization of proteasomes. Int. J. Biochem. Cell Biol. 35:2003;579-589
114. Wolozin B., Behl C. Mechanism of neurodegenerative disorders. Arch. Neurol. 57:2000;793-804
115. Yin D. Lipofuscin-like fluorophores can result from reactions between oxidized ascorbic acid and glutamine. Carbonylprotein cross-linking may represent a common reaction in oxygen radical and glycosylation-related ageing processes. Mech. Aging Dev. 62:1992;35-46
116. Yin, D. (1995). Studies on age pigments evolving into a new theory of biological aging. In K. Kitani, G. O. Ivy, & H. Shimasaki (Eds.), Lipofuscin and ceroid pigments (pp. 159-170). Basel: S. Karger.
117. Yin D. Biochemical basis of lipofuscin, ceroid, and age pigment-like fluorophores. Free Radic. Biol. Med. 21:1996;871-888