Aging, lipofuscin formation, and free radical-mediated inhibition of cellular proteolytic systems

Ageing Research Reviews

Volumn 2, Issue 4, 2003, Pages 383-405

  Szweda, Pamela A ^a   Camouse, Melissa ^a   Lundberg, Kathleen C ^a   Oberley, Terry D ^b   Szweda, Luke I ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

4 hydroxy 2 nonenal; Flourescent adduct; Free radicals; Lysosomes; Proteasome

Indexed keywords

CELL PROTEIN; FREE RADICAL; INHIBITOR PROTEIN; LIPOFUSCIN; MITOCHONDRIAL PROTEIN; PROTEASOME; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE;

AGING; ALPHA CHAIN; BRAIN CORTEX; CELL FUNCTION; CROSS LINKING; FLUORESCENCE; IMMUNOCHEMISTRY; LYSOSOME; MOLECULAR BIOLOGY; NONHUMAN; OXIDATION; OXIDATIVE STRESS; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW;

EID: 0141650806     PISSN: 15681637     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1568-1637(03)00028-X     Document Type: Review

References (140)

1. Adamec E., Mohan P.S., Cataldo A.M., Vonsattel J.P., Nixon R.A. Up-regulation of the lysosomal system in experimental models of neuronal injury: implications for Alzheimer's disease. Neuroscience. 100:2000;663-675.
2. Aksenova M.V., Aksenov M.Y., Carney J.M., Butterfield D.A. Protein oxidation and enzyme activity decline in old brown Norway rats are reduced by dietary restriction. Mech. Ageing Dev. 100:1998;157-168.
3. Alkalay I., Yaron A., Hatzubai A., Orian A., Ciechanover A., Ben-Neriah Y. Stimulation-dependent I kappa B alpha phosphorylation marks the NF-kappa B inhibitor for degradation via the ubiquitin-proteasome pathway. Proc. Natl. Acad. Sci. U.S.A. 92:1995;10599-10603.
4. Ambrosio G., Zweier J.L., Duilio C., Kuppusamy P., Santoro G., Elia P.P., Tritto I., Cirillo P., Condorelli M., Chiariello M.et al. Evidence that mitochondrial respiration is a source of potentially toxic oxygen free radicals in intact rabbit hearts subjected to ischemia and reflow. J. Biol. Chem. 268:1993;18532-18541.
5. Ames B.N., Shigenaga M.K., Hagen T.M. Oxidants, antioxidants and the degenerative diseases of aging. Proc. Natl. Acad. Sci. U.S.A. 90:1993;7915-7922.
6. 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. A Biol. Sci. Med. Sci. 53B:1998;173-179.
7. Beckman K.B., Ames B.N. Oxidative decay of DNA. J. Biol. Chem. 272:1997;19633-19636.
8. Beckman K.B., Ames B.N. The free radical theory of aging matures. Physiol. Rev. 78:1998;547-581.
9. Berlett B.S., Stadtman E.R. Protein oxidation in aging, disease, and oxidative stress. J. Biol. Chem. 272:1997;20313-20316.
10. Blanc E.M., Kelly J.F., Mark R.J., Mattson M.P. 4-Hydroxynonenal, an aldehydic product of lipid peroxidation, impairs signal transduction associated with muscarinic acetylcholine and metabotropic glutamate receptors: possible action on Gaq/11. J. Neurochem. 69:1997;570-580.
11. Braeckman B.P., Vanfleteren J.R. Stress-inducible mechanisms of life-span extension in yeast, eubacteria, and metazoans. Trends Microbiol. 7:1999;270-271.
12. Breitschopf K., Zeiher A.M., Dimmeler S. Ubiquitin-mediated degradation of the proapoptotic active form of bid. A functional consequence on apoptosis induction. J. Biol. Chem. 275:2000;21648-21652.
13. Brunk U.T., Terman A. Lipofuscin: mechanisms of age-related accumulation and influence on cell function. Free Radic. Biol. Med. 33:2002;611-619.
14. Bulteau A.L., Lundberg K.C., Humphries K.M., Sadek H.A., Szweda P.A., Friguet B., Szweda L.I. Oxidative modification and inactivation of the proteasome during coronary occlusion/reperfusion. J. Biol. Chem. 276:2001;30057-30063.
15. Bulteau A.L., Petropoulos I., Friguet B. Age-related alterations of proteasome structure and function in aging epidermis. Exp. Gerontol. 35:2000;767-777.
16. Bulteau A.L., Szweda L.I., Friguet B. Age-dependent declines in proteasome activity in the heart. Arch. Biochem. Biophys. 397:2002;298-304.
17. Cabiscol E., Levine R.L. Carbonic anhydrase III. Oxidative modification in vivo and loss of phosphatase activity during aging. J. Biol. Chem. 270:1995;14742-14747.
18. Cadenas E., Davies K.J. Mitochondrial free radical generation, oxidative stress, and aging. Free Radic. Biol. Med. 29:2000;222-230.
19. Carney J.M., Starke-Reed P.E., Oliver C.N., Landum 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-alpha-phenylnitrone. Proc. Natl. Acad. Sci. U.S.A. 88:1991;3633-3636.
20. Castellani R.J., Perry G., Siedlak S.L., Nunomura A., Shimohama S., Zhang J., Montine T., Sayre L.M., Smith M.A. Hydroxynonenal adducts indicate a role for lipid peroxidation in neocortical and brainstem Lewy bodies in humans. Neurosci. Lett. 319:2002;25-28.
21. Cataldo A.M., Nixon R.A. Enzymatically active lysosomal proteases are associated with amyloid deposits in Alzheimer brain. Proc. Natl. Acad. Sci. U.S.A. 87:1990;3861-3865.
22. Cataldo A.M., Paskevich P.A., Kominami E., Nixon R.A. Lysosomal hydrolases of different classes are abnormally distributed in brains of patients with Alzheimer disease. Proc. Natl. Acad. Sci. U.S.A. 88:1991;10998-11002.
23. Cataldo A.M., Hamilton D.J., Nixon R.A. Lysosomal abnormalities in degenerating neurons link neuronal compromise to senile plaque development in Alzheimer disease. Brain Res. 640:1994;68-80.
24. Cataldo A.M., Barnett J.L., Berman S.A., Li J., Quarless S., Bursztajn S., Lippa C., Nixon R.A. Gene expression and cellular content of cathepsin D in Alzheimer's disease brain: evidence for early up-regulation of the endosomal-lysosomal system. Neuron. 14:1995;671-680.
25. Cataldo A.M., Hamilton D.J., Barnett J.L., Paskevich P.A., Nixon R.A. Properties of the endosomal-lysosomal system in the human central nervous system: disturbances mark most neurons in populations at risk to degenerate in Alzheimer's disease. J. Neurosci. 16:1996;186-199.
26. Cataldo A.M., Barnett J.L., Pieroni C., Nixon R.A. Increased neuronal endocytosis and protease delivery to early endosomes in sporadic Alzheimer's disease: neuropathologic evidence for a mechanism of increased beta-amyloidogenesis. J. Neurosci. 17:1997;6142-6151.
27. Cataldo A.M., Peterhoff C.M., Troncoso J.C., Gomez-Isla T., Hyman B.T., Nixon R.A. Endocytic pathway abnormalities precede amyloid beta deposition in sporadic Alzheimer's disease and Down syndrome: differential effects of APOE genotype and presenilin mutations. Am. J. Pathol. 157:2000;277-286.
28. Cavallini G., Donati A., Gori Z., Pollera M., Bergamini E. The protection of rat liver autophagic proteolysis from the age-related decline co-varies with the duration of anti-ageing food restriction. Exp. Gerontol. 36:2001;497-506.
29. Checler F., da Costa C.A., Ancolio K., Chevallier N., Lopez-Perez E., Marambaud P. Role of the proteasome in Alzheimer's disease. Biochim. Biophys. Acta. 1502:2000;133-138.
30. Chen J.J., Bertrand H., Yu B.P. Inhibition of adenine nucleotide translocator by lipid peroxidation products. Free Radic. Biol. Med. 19:1995;583-590.
31. Chio K.S., Tappel A.L. Inactivation of ribonuclease and other enzymes by peroxidizing lipids and by malonaldehyde. Biochemistry. 8:1969a;2827-2832.
32. Chio K.S., Tappel A.L. Synthesis and characterization of the fluorescent products derived from malonaldehyde and amino acids. Biochemistry. 8:1969b;2821-2826.
33. Chondrogianni, N., Stratford, F.L., Trougakos, I.P., Friguet, B., Rivett, A.J., Gonos, E.S., et al. 2003. Central role of the proteasome in senescence and survival of human fibroblasts: induction of a senescence-like phenotype upon its inhibition and resistance to stress upon its activation. J. Biol. Chem., in press.
34. Ciechanover A., Laszlo A., Bercovich B., Stancovski I., Alkalay I., Ben-Neriah Y., Orian A. The ubiquitin-mediated proteolytic system: involvement of molecular chaperones, degradation of oncoproteins, and activation of transcriptional regulators. Cold Spring Harb. Symp. Quant. Biol. 60:1995;491-501.
35. Cohn J.A., Tsai L., Friguet B., Szweda L.I. Chemical characterization of a protein-4-hydroxy-2-nonenal cross-link: immunochemical detection in mitochondria exposed to oxidative stress. Arch. Biochem. Biophys. 328:1996;158-164.
36. Conconi M., Friguet B. Proteasome inactivation upon aging and on oxidation-effect of HSP 90. Mol. Biol. Rep. 24:1997;45-50.
37. Coux O., Tanaka K., Goldberg A.L. Structure and functions of the 20S and 26S proteasomes. Annu. Rev. Biochem. 65:1996;801-847.
38. Cuervo A.M., Dice J.F. How do intracellular proteolytic systems change with age? Front Biosci. 3:1998;D25-D43.
39. Cuervo A.M., Dice J.F. Age-related decline in chaperone-mediated autophagy. J. Biol. Chem. 275:2000a;31505-31513.
40. Cuervo A.M., Dice J.F. When lysosomes get old. Exp. Gerontol. 35:2000;119-131.
41. Cuervo A.M., Palmer A., Rivett A.J., Knecht E. Degradation of proteasomes by lysosomes in rat liver. Eur. J. Biochem. 227:1995;792-800.
42. Cuervo A.M., Hu W., Lim B., Dice J.F. I kappa B is a substrate for a selective pathway of lysosomal proteolysis. Mol. Biol. Cell. 9:1998;1995-2010.
43. Das N., Levine R.L., Orr W.C., Sohal R.S. Selectivity of protein oxidative damage during aging in Drosophila melanogaster. Biochem. J. 360:2001;209-216.
44. Davies K.J. Degradation of oxidized proteins by the 20S proteasome. Biochimie. 83:2001;301-310.
45. Deiss L.P., Galinka H., Berissi H., Cohen O., Kimchi A. Cathepsin D protease mediates programmed cell death induced by interferon-gamma, Fas/APO-1 and TNF-alpha. EMBO J. 15:1996;3861-3870.
46. DeMartino G.N., Slaughter C.A. The proteasome, a novel protease regulated by multiple mechanisms. J. Biol. Chem. 274:1999;22123-22126.
47. Dice J.F., 2000. Lysosomal Pathways of Protein Degradation. Landes Bioscience, Georgetown, TX.
48. Donati A., Cavallini G., Paradiso C., Vittorini S., Pollera M., Gori Z., Bergamini E. Age-related changes in the autophagic proteolysis of rat isolated liver cells: effects of antiaging dietary restrictions. J. Gerontol. A Biol. Sci. Med. Sci. 56:2001a;B375-B383.
49. Donati A., Cavallini G., Paradiso C., Vittorini S., Pollera M., Gori Z., Bergamini E. Age-related changes in the regulation of autophagic proteolysis in rat isolated hepatocytes. J. Gerontol. A. Biol. Sci. Med. Sci. 56:2001;288-293.
50. Essner E., Novikoff A.V. Human heptocellular pigments and lysosomes. J. Ultrastruct. Res. 3:1960;374-391.
51. Esterbauer H., Schaur R.J., Zollner H. Chemistry and biochemistry of 4-hydroxynonenal malonaldehyde and related aldehydes. Free Radic. Biol. Med. 11:1991;81-128.
52. Ferri K.F., Kroemer G. Organelle-specific initiation of cell death pathways. Nat. Cell Biol. 3:2001;E255-E263.
53. 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.
54. 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. 269:1994a;21639-21643.
55. Friguet B., Szweda L.I., Stadtman E.R. Susceptibility of glucose-6-phosphate dehydrogenase modified by 4-hydroxy-2-nonenal and metal-catalyzed oxidation to proteolysis by the multicatalytic protease. Arch. Biochem. Biophys. 311:1994;168-173.
56. Friguet B., Bulteau A.L., Chondrogianni N., Conconi M., Petropoulos I. Protein degradation by the proteasome and its implications in aging. Ann. N. Y. Acad. Sci. 908:2000;143-154.
57. Giulivi C., Pacifici R.E., Davies K.J. Exposure of hydrophobic moieties promotes the selective degradation of hydrogen peroxide-modified hemoglobin by the multicatalytic proteinase complex, proteasome. Arch. Biochem. Biophys. 311:1994;329-341.
58. Halestrap A.P., McStay G.P., Clarke S.J. The permeability transition pore complex: another view. Biochimie. 84:2002;153-166.
59. Harman D. Lipofuscin and ceroid formation: the cellular recycling system. Adv. Exp. Med. Biol. 266:1989;3-15.
60. Hoppe G., O'Neil J., Hoff H.F. Inactivation of lysosomal proteases by oxidized low density lipoprotein is partially responsible for its poor degradation by mouse peritoneal macrophages. J. Clin. Invest. 94:1994;1506-1512.
61. Itakura K., Uchida K. Evidence that malondialdehyde-derived aminoenimine is not a fluorescent age pigment. Chem. Res. Toxicol. 14:2001;473-475.
62. Itakura K., Osawa T., Uchida K. Structure of a fluorescent compound formed from 4-hydroxy-2-nonenal and N(alpha)-hippuryllysine: a model for fluorophores derived from protein modifications by lipid peroxidation. J. Org. Chem. 63:1998;185-187.
63. Itakura K., Oya-Ito T., Osawa T., Yamada S., Toyokuni S., Shibata N., Kobayashi M., Uchida K. Detection of lipofuscin-like fluorophore in oxidized human low-density lipoprotein. 4-hydroxy-2-nonenal as a potential source of fluorescent chromophore. FEBS Lett. 473:2000;249-253.
64. Ivy G.O., Schottler F., Wenzel J., Baudry M., Lynch G. Inhibitors of lysosomal enzymes: accumulation of lipofuscin-like dense bodies in the brain. Science. 226:1984;985-987.
65. Ivy G.O., Kanai S., Ohta M., Smith G., Sato Y., Kobayashi M., Kitani K. Lipofuscin-like substances accumulate rapidly in brain, retina, and internal organs with cysteine protease inhibition. Adv. Exp. Med. Biol. 266:1989;31-45. (Discussion 37-45).
66. Ivy G.O., Kanai S., Ohta M., Sato Y., Otsubo K., Kitani K. Leupeptin causes an accumulation of lipofuscin-like substances in liver cells of young rats. Mech. Ageing Dev. 57:1991;213-231.
67. Ivy G.O., Roopsingh R., Kanai S., Ohta M., Sato Y. Kitani K. Ann. N. Y. Acad. Sci. 786:1996;12-23.
68. Jung H., Lee E.Y., Lee S.I. Age-related changes in ultrastructural features of cathepsin B- and D-containing neurons in rat cerebral cortex. Brain Res. 844:1999;43-54.
69. Keller J.N., Pang Z., Geddes J.W., Begley J.G., Germeyer A., Waeg G., Mattson M.P. Impairment of glucose and glutamate transport and induction of mitochondrial oxidative stress and dysfunction in synaptosomes by amyloid ß-peptide: role of the lipid peroxidation product 4-hydroxynonenal. J. Neurochem. 69:1997;273-284.
70. Keller J.N., Hanni K.B., Markesbery W.R. Possible involvement of proteasome inhibition in aging: implications for oxidative stress. Mech. Ageing Dev. 113:2000a;61-70.
71. Keller J.N., Huang F.F., Markesbery W.R. Decreased levels of proteasome activity and proteasome expression in aging spinal cord. Neuroscience. 98:2000;149-156.
72. Kikugawa K., Kato T., Beppu M., Hayasaka A. Fluorescent and cross-linked proteins formed by free radical and aldehyde species generated during lipid oxidation. Adv. Exp. Med. Biol. 266:1989;345-356. (Disucussion 357).
73. Kitani K., Ohta M., Kanai S., Nokubo M., Sato Y., Otsubo K., Ivy G.O. Morphological, physiological and biochemical alterations in livers of rodents induced by protease inhibitors: a comparison with old livers. Adv. Exp. Med. Biol. 266:1989;75-92.
74. Kowaltowski A.J., Castilho R.F., Vercesi A.E. Mitochondrial permeability transition and oxidative stress. FEBS Lett. 495:2001;12-15.
75. Kurz D.J., Decary S., Hong Y., Erusalimsky J.D. Senescence-associated (beta)-galactosidase reflects an increase in lysosomal mass during replicative ageing of human endothelial cells. J. Cell Sci. 113(20):2000;3613-3622.
76. Lee C.K., Klopp R.G., Weindruch R., Prolla T.A. Gene expression profile of aging and its retardation by caloric restriction. Science. 285:1999;1390-1393.
77. Li B., Dou Q.P. Bax degradation by the ubiquitin/proteasome-dependent pathway: involvement in tumor survival and progression. Proc. Natl. Acad. Sci. U.S.A. 97:2000;3850-3855.
78. Lougheed M., Zhang H.F., Steinbrecher U.P. Oxidized low density lipoprotein is resistant to cathepsins and accumulates within macrophages. J. Biol. Chem. 266:1991;14519-14525.
79. Lucas D.T., Szweda L.I. Cardiac reperfusion injury: aging, lipid peroxidation, and mitochondrial dysfunction. Proc. Natl. Acad. Sci. U.S.A. 95:1998;510-514.
80. Lucas D.T., Szweda L.I. Declines in mitochondrial respiration during cardiac reperfusion: age-dependent inactivation of alpha-ketoglutarate dehydrogenase. Proc. Natl. Acad. Sci. U.S.A. 96:1999;6689-6693.
81. Ly D.H., Lockhart D.J., Lerner R.A., Schultz P.G. Mitotic misregulation and human aging. Science. 287:2000;2486-2492.
82. Mark R.J., Lovell M.A., Markesbery W.R., Uchida K., Mattson M.P. A role for 4-hydroxynonenal in disruption of ion homeostasis and neuronal death induced by amyloid β-peptide. J. Neurochem. 68:1997a;255-264.
83. Mark R.J., Pang Z., Geddes J.W., Uchida K., Mattson M.P. Amyloid β-peptide impairs glucose uptake in hippocampal and cortical neurons: involvement of membrane lipid peroxidation. J. Neurosci. 17:1997;1046-1054.
84. Mathews P.M., Guerra C.B., Jiang Y., Grbovic O.M., Kao B.H., Schmidt S.D., Dinakar R., Mercken M., Hille-Rehfeld A., Rohrer J., Mehta P., Cataldo A.M., Nixon R.A. Alzheimer's disease-related overexpression of the cation-dependent mannose 6-phosphate receptor increases Abeta secretion: role for altered lysosomal hydrolase distribution in beta-amyloidogenesis. J. Biol. Chem. 277:2002;5299-5307.
85. Mattson M.P., Fu W., Waeg G., Uchida K. 4-Hydroxynonenal, a product of lipid peroxidation inhibits dephosphorylation of the microtubule-associated protein tau. NeuroReport. 8:1997;2275-2281.
86. Mattson M.P., Chan S.L., Duan W. Modification of brain, aging, and neurodegenerative disorders by genes, diet, and behavior. Physiol. Rev. 82:2002;637-672.
87. Meredith G.E., Totterdell S., Petroske E., Santa Cruz K., Callison R.C. Jr., Lau Y.S. Lysosomal malfunction accompanies alpha-synuclein aggregation in a progressive mouse model of Parkinson's disease. Brain Res. 956:2002;156-165.
88. Miyagishi T., Takahata N., Iizuka R. Electron microscopic studies on the lipo-pigments in the cerebral cortex nerve cells of senile and Vitamin E deficient rats. Acta Neuropathol. (Berl.). 9:1967;7-17.
89. Monserrat A.J., Benavides S.H., Berra A., Farina S., Vicario S.C., Porta E.A. Lectin histochemistry of lipofuscin and certain ceroid pigments. Histochem. Cell Biol. 103:1995;435-445.
90. Muratani M., Tansey W.P. How the ubiquitin-proteasome system controls transcription. Nat. Rev. Mol. Cell Biol. 4:2003;192-201.
91. Muse K.E., Oberley T.D., Sempf J.M., Oberley L.W. Immunolocalization of antioxidant enzymes in adult hamster kidney. Histochem. J. 26:1994;734-753.
92. Nixon R.A., Cataldo A.M., Mathews P.M. The endosomal-lysosomal system of neurons in Alzheimer's disease pathogenesis: a review. Neurochem. Res. 25:2000;1161-1172.
93. Okada K., Wangpoengtrakul C., Osawa T., Toyokuni S., Tanaka K., 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.
94. Pacifici R.E., Kono Y., Davies K.J. Hydrophobicity as the signal for selective degradation of hydroxyl radical-modified hemoglobin by the multicatalytic proteinase complex, proteasome. J. Biol. Chem. 268:1993;15405-15411.
95. Palmer D.N., Barns G., Husbands D.R., Jolly R.D. Ceroid lipofuscinosis in sheep. II. The major component of the lipopigment in liver, kidney, pancreas, and brain is low molecular weight protein. J. Biol. Chem. 261:1986;1773-1777.
96. Palmer, D.N., Fearnley, I.M., Medd, S.M., Walker, J.E., Martinus, R.D., Bayliss, S.L., Hall, N.A., Lake, B.D., Wolfe, L.S., Jolly, R.D., 1990. In: Porta, E. (Ed.), Lipofuscin and Ceroid Pigments. Plenum Press, New York, pp. 211-223.
97. Pedersen W.A., Fu W., Keller J.N., Markesbery W.R., Appel S.H., Smith R.G., Kasarskis E., Mattson M.P. Protein modification by the lipid peroxidation product 4-hydroxynonenal in spinal cord tissue of ALS patients. Ann. Neurol. 44:1998;819-824.
98. Porta E.A. Advances in age pigment research. Arch. Gerontol. Geriatr. 212:1991;303-320.
99. Porta E.A. Pigments in aging: an overview. Ann. N. Y. Acad. Sci. 959:2002;57-65.
100. Reinheckel T., Sitte N., Ullrich O., Kuckelkorn U., Davies K.J., Grune T. Comparative resistance of the 20S and 26S proteasome to oxidative stress. Biochem. J. 335(3):1998;637-642.
101. 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.
102. Rivett A.J. Preferential degradation of the oxidatively modified form of glutamine synthetase by intracellular mammalian proteases. J. Biol. Chem. 260:1985;300-305.
103. Roberg K. Relocalization of cathepsin D and cytochrome c early in apoptosis revealed by immunoelectron microscopy. Lab. Invest. 81:2001;149-158.
104. Rock K.L., York I.A., Saric T., Goldberg A.L. Protein degradation and the generation of MHC class I-presented peptides. Adv. Immunol. 80:2002;1-70.
105. Sanchez-Martin M.M., Cabezas J.A. Evaluation of the activities of eight lysosomal hydrolases in sera of humans, rats, and pigs of different ages. Mech. Ageing Dev. 99:1997;95-107.
106. Sayre L.M., Zelasko D.A., Harris P.L., Perry G., Salomon R.G., Smith M.A. 4-Hydroxynonenal-derived advanced lipid peroxidation end products are increased in Alzheimer's disease. J. Neurochem. 68:1997;2092-2097.
107. Scarlett J.L., Murphy M.P. Release of apoptogenic proteins from the mitochondrial intermembrane space during the mitochondrial permeability transition. FEBS Lett. 418:1997;282-286.
108. Shringarpure R., Grune T., Davies K.J. Protein oxidation and 20S proteasome-dependent proteolysis in mammalian cells. Cell Mol. Life Sci. 58:2001;1442-1450.
109. +)-ATPase. Free Radic. Biol. Med. 20:1996;215-223.
110. Sitte N., Huber M., Grune T., Ladhoff A., Doecke W.D., Von Zglinicki T., Davies K.J. Proteasome inhibition by lipofuscin/ceroid during postmitotic aging of fibroblasts. FASEB J. 14:2000a;1490-1498.
111. Sitte N., Merker K., Von Zglinicki T., Davies K.J., Grune T. Protein oxidation and degradation during cellular senescence of human BJ fibroblasts. Part II. Aging of nondividing cells. FASEB J. 14:2000b;2503-2510.
112. Sitte N., Merker K., Von Zglinicki T., Grune T., Davies K.J. Protein oxidation and degradation during cellular senescence of human BJ fibroblasts. Part I. Effects of proliferative senescence. FASEB J. 14:2000c;2495-2502.
113. Stadtman E.R. Protein oxidation in aging and age-related diseases. Ann. N. Y. Acad. Sci. 928:2001;22-38.
114. Strickland E., Hakala K., Thomas P.J., DeMartino G.N. Recognition of misfolding proteins by PA700, the regulatory subcomplex of the 26 S proteasome. J. Biol. Chem. 275:2000;5565-5572.
115. Strous G.J., van Kerkhof P., Govers R., Ciechanover A., Schwartz A.L. The ubiquitin conjugation system is required for ligand-induced endocytosis and degradation of the growth hormone receptor. EMBO J. 15:1996;3806-3812.
116. Szweda L.I., Uchida K., Tsai L., Stadtman E.R. Inactivation of glucose-6-phosphate dehydrogenase by 4-hydroxy-2-nonenal. Selective modification of an active-site lysine. J. Biol. Chem. 268:1993;3342-3347.
117. Szweda P.A., Friguet B., Szweda L.I. Proteolysis free radicals and aging. Free Radic. Biol. Med. 33:2002;29-36.
118. +-free calmodulin and calmodulin damaged by in vitro aging are selectively degraded by 26 S proteasomes without ubiquitination. J. Biol. Chem. 275:2000;20295-20301.
119. Terman A. The effect of age on formation and elimination of autophagic vacuoles in mouse hepatocytes. Gerontology. 41(Suppl. 2):1995;319-326.
120. Terman A., Brunk U.T. Ceroid/lipofuscin formation in cultured human fibroblasts: the role of oxidative stress and lysosomal proteolysis. Mech. Ageing Dev. 104:1998a;277-291.
121. Terman A., Brunk U.T. Lipofuscin: mechanisms of formation and increase with age. APMIS. 106:1998b;265-276.
122. Terman A., Brunk U.T. On the degradability and exocytosis of ceroid/lipofuscin in cultured rat cardiac myocytes. Mech. Ageing Dev. 100:1998c;145-156.
123. Terman A., Sandberg S. Proteasome inhibition enhances lipofuscin formation. Ann. N. Y. Acad. Sci. 973:2002;309-312.
124. Terman A., Abrahamsson N., Brunk U.T. Ceroid/lipofuscin-loaded human fibroblasts show increased susceptibility to oxidative stress. Exp. Gerontol. 34:1999;755-770.
125. Tsai L., Sokoloski E.A. The reaction of 4-hydroxy-2-nonenal with N alpha-acetyl-L-histidine. Free Radic. Biol. Med. 19:1995;39-44.
126. Tsai L., Szweda P.A., Vinogradova O., Szweda L.I. Structural characterization and immunochemical detection of a fluorophore derived from 4-hydroxy-2-nonenal and lysine. Proc. Natl. Acad. Sci. U.S.A. 95:1998;7975-7980.
127. Uchida K., Stadtman E.R. Covalent attachment of 4-hydroxynonenal to glyceraldehyde-3-phosphate dehydrogenase. A possible involvement of intra- and intermolecular cross-linking reaction. J. Biol. Chem. 268:1993;6388-6393.
128. Uchida K., Szweda L.I., Chae H.Z., Stadtman E.R. Immunochemical detection of 4-hydroxynonenal protein adducts in oxidized hepatocytes. Proc. Natl. Acad. Sci. U.S.A. 90:1993;8742-8746.
129. Vanfleteren J.R., Braeckman B.P. Mechanisms of life span determination in Caenorhabditis elegans. Neurobiol. Aging. 20:1999;487-502.
130. Wataya T., Nunomura A., Smith M.A., Siedlak S.L., Harris P.L., Shimohama S., Szweda L.I., Kaminski M.A., Avila J., Price D.L., Cleveland D.W., Sayre L.M., Perry G. High molecular weight neurofilament proteins are physiological substrates of adduction by the lipid peroxidation product hydroxynonenal. J. Biol. Chem. 277:2002;4644-4648.
131. Wehrle J.P., Cintron N.M., Pedersen P.L. Phosphate transport in rat liver mitochondria energy-dependent accumulation of phosphate by inverted inner membrane vesicles. J. Biol. Chem. 253:1978;8598-8603.
132. Whitby F.G., Masters E.I., Kramer L., Knowlton J.R., Yao Y., Wang C.C., Hill C.P. Structural basis for the activation of 20S proteasomes by 11S regulators. Nature. 408:2000;115-120.
133. Yan L.J., Sohal R.S. Prevention of flight activity prolongs the life span of the housefly, Musca domestica, and attenuates the age-associated oxidative damamge to specific mitochondrial proteins. Free Radic. Biol. Med. 29:2000;1143-1150.
134. Yan L.J., Levine R.L., Sohal R.S. Oxidative damage during aging targets mitochondrial aconitase. Proc. Natl. Acad. Sci. U.S.A. 94:1997;11168-11172.
135. Yao Y., Huang L., Krutchinsky A., Wong M.L., Standing K.G., Burlingame A.L., Wang C.C. Structural and functional characterizations of the proteasome-activating protein PA26 from Trypanosoma brucei. J. Biol. Chem. 274:1999;33921-33930.
136. Yin D. Biochemical basis of lipofuscin, ceroid, and age pigment-like fluorophores. Free Radic. Biol. Med. 21:1996;871-888.
137. Yoritaka A., Hattori N., Uchida K., Tanaka M., Stadtman E.R., Mizuno Y. Immunohistochemical detection of 4-hydroxynonenal protein adducts in Parkinson disease. Proc. Natl. Acad. Sci. U.S.A. 93:1996;2696-2701.
138. Zainal T.A., Weindruch R., Szweda L.I., Oberley T.D. Localization of 4-hydroxy-2-nonenal-modified proteins in kidney following iron overload. Free Radic. Biol. Med. 26:1999;1181-1193.
139. Zainal T.A., Oberley T.D., Allison D.B., Szweda L.I., Weindruch R. Caloric restriction of rhesus monkeys lowers oxidative damage in skeletal muscle. FASEB J. 14:2000;1825-1836.
140. Zweier J.L., Kuppusamy P., Williams R., Rayburn B.K., Smith D., Weisfeldt M.L., Flaherty J.T. Measurement and characterization of postischemic free radical generation in the isolated perfused heart. J. Biol. Chem. 264:1989;18890-18895.