Reactive oxygen-mediated protein oxidation in aging and disease

Chemical Research in Toxicology

Volumn 10, Issue 5, 1997, Pages 485-494

  Stadtman, Earl R ^a   Berlett, Barbara S ^a  

^a NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FREE RADICAL; REACTIVE OXYGEN METABOLITE;

AGING; ALZHEIMER DISEASE; HUMAN; NEUROTOXICITY; OXIDATION; OXIDATIVE STRESS; PROTEIN CROSS LINKING; PROTEIN DEGRADATION; PROTEIN MODIFICATION; REVIEW;

AGING; ANIMALS; DISEASE; HUMANS; PROTEINS; REACTIVE OXYGEN SPECIES;

ANIMALIA;

EID: 0031010333     PISSN: 0893228X     EISSN: None     Source Type: Journal    
DOI: 10.1021/tx960133r     Document Type: Review

References (154)

1. Bovaris, A., Oshino, N., and Chance, B. (1972) The cellular production of hydrogen peroxide. Biochem. J. 128, 617-630.
2. Halliwell, B., and Gutteridge, J. M. C. (1989) Free Radicals in Biology and Medicine, Clarendon Press, Oxford.
3. Stadtman, E. R. (1986) Oxidation of proteins by mixed-function oxidation systems: Implication in protein turnover, ageing, and neutrophil function. Trends Biochem. Sci. 11, 11-12.
4. Stadtman, E. R. (1992) Protein oxidation and aging. Science 257, 1220-1224.
5. Dean, R. T. (1987) A mechanism for accelerated degradation of intracellular proteins after limited damage by free radicals. FEBS Lett. 220, 278-282.
6. Davies, K. J. A. (1987) Protein damage and degradation by oxygen radicals. I. General aspects. J. Biol. Chem. 262, 9895-9901.
7. Sohal, R. S., Ku, H.-H., Agarwal, S., Forster, M. J., and Lal, H. (1994) Oxidative damage, mitochondrial oxidant generation and antioxidant defenses during aging and in response to food restriction in the mouse. Mech. Ageing Dev. 74, 121-133.
8. Ames, B. N., Shingenaga, M. K., Park, E. M. (1991) DNA damage by endogenous oxidants as a cause of aging and cancer. In Oxidation Damage and Repair: Chemical, Biological, and Medical Aspects (Davies, K. J. A., Ed.) pp 181-187, Pergamon, Elmstad, New York.
9. Garrison, W. M. (1987) Reaction mechanisms in the radiolysis of peptide, polypeptides, and proteins. Chem. Rev. 87, 381-398.
10. Garrison, W. M., Jayko, M. E., and Bennett, W. (1962) Radiation-induced oxidation of proteins in aqueous solution. Radiat. Res. 16, 487-502.
11. Swallow, A. J. (1960) Effect of ionizing radiation on proteins. RCO groups, peptide bond cleavage, inactivation, -SH oxidation. In Radiation Chemistry of Organic Compounds (Swallow, A. J., Ed.) pp 211-224, Pergamon Press, New York.
12. Schuessler, H., and Schilling, K. (1984) Oxygen effect in radiolysis of proteins. Part 2. Bovine serum albumin. Int. J. Radiat. Biol. 45, 267-281.
13. 2O2 conversion of proline residue to 2-pyrrolidone. J. Biol. Chem. 267, 23646-23651.
14. Amici, A., Levine, R. L., Tsai, L., and Stadtman, E. R. (1989) Conversion of amino acid residues in proteins and amino acid homopolymers to carbonyl derivatives by metal-catalyzed reactions. J. Biol. Chem. 264, 3341-3346.
15. Zhou, J. Q., and Gafni, A. (1991) Exposure of rat muscle phosphoglycerate kinase to a nonenzymatic MFO system generates the old form of enzyme. J. Gerontol. 46, B217-B221.
16. Brodie, E., and Reed, D. J. (1990) Cellular recovery of glyceraldehyde-3-phosphate dehydrogenase activity and thiol status after exposure to hydroperoxide. Arch. Biochem. Biophys. 277, 228-233.
17. Takahashi, R., and Goto, S. (1990) Alteration of aminoacyl-tRNA synthetase with age: Heat labilization of the enzyme by oxidative damage. Arch. Biochem. Biophys. 277, 228-233.
18. Uchida, K., and Kawakishi, S. (1993) 2-Oxohistidine as a novel biological marker for oxidatively modified proteins. FEBS Lett. 332, 208-210.
19. Berlett, B. S., Levine, R. L., and Stadtman, E. R. (1996) A comparison of the effects of ozone on the modification of amino acid residues in glutamine synthetase and bovine serum albumin. J. Biol. Chem. 271, 4177-4182.
20. Farber, J. M., and Levine, R. L. (1986) Sequence of a peptide susceptible to mixed-function oxidation: Probable cation binding site in glutamine synthetase. J. Biol. Chem. 261, 4574-4578.
21. Kopoldova, J., and Liebsier, J. (1963) The mechanism of radiation chemical degradation of amino acids V. Int. J. Appl. Radiat. Isot. 14, 493-498.
22. Vogt, W. (1995) Oxidation of methionine residues in proteins: Tools, targets, and reversal. Free Radical Biol. Med. 18, 93-105.
23. Pryor, W. A., Jin, X., and Squadrito, G. L. (1994) One- and two-electron oxidations of methionine by peroxynitrite. Proc. Natl. Acad. Sci. U.S.A. 91, 11173-11177.
24. Berlett, B. S., Friguet, B., Yim, M. B., Chock, P. B., and Stadtman, E. R. (1996) Peroxynitrite-mediated nitration of tyrosine residues of Escherichia coli glutamine synthetase mimic adenylylation: Relevance to signal transduction. Proc. Natl. Acad. Sci. U.S.A. 93, 1776-1780.
25. Berlett, B. S., and Stadtman, E. R. (1996) Carbon dioxide stimulates nitration of tyrosine residues and inhibits oxidation of methionine residues in Escherichia coli glutamine synthetase by peroxynitrite. FASEB J. 10, Abstract 585.
26. Maskos, Z., Rush, J. D., and Koppenol, W. H. (1992) The hydroxylation of phenylalanine and tyrosine: A comparison with salicylate and tryptophan. Arch. Biochem. Biophys. 296, 521-529.
27. Solar, S. (1985) Reactions of OH with phenylalanine in neutral aqueous solutions. Radiat. Phys. Chem. 26, 103-108.
28. Beckman, J. S., Ischiropoulos, H., Zhu, L., van der Woerd, M., Smith, C., Chen, J., Harrison, J., Martin, J. C., and Tsai, M. (1992) Kinetics of superoxide dismutase- and iron-catalyzed nitration of phenolics by peroxynitrite. Arch. Biochem. Biophys. 298, 438-445.
29. Fletcher, G. L., and Okada, S. (1961) Radiation-induced formation of dihydroxy phenylalanine from tyrosine and tyrosine-containing peptides in aqueous solution. Radiat. Res. 15, 349-351.
30. Gieseg, S. P., Simpson, J. A., Charlton, T. S., Duncan, M. W., and Dean, R. T. (1993) Protein-bound 3,4-dihydroxyphenylalanine is a major product formed during hydroxyl radical damage to proteins. Biochemistry 32, 4780-4786.
31. Davies, K. J. A., Delsignore, M. E., and Lin, S. W. (1987) Protein damage by oxygen radicals. II. Modification of amino acids. J. Biol. Chem. 262, 9902-9907.
32. Huggins, T. G., Wells-Knecht, M. C., Detorie, N. A., Baynes, J. W., and Thorpe, S. R. (1993) Formation of O-tyrosine and dityrosine in proteins during radiolytic and metal-catalyzed oxidation. J. Biol. Chem. 268, 12341-12347.
33. van der Vliet, A., Eiserich, J. P., O'Neill, C. A., Halliwell, B., and Cross, C. E. (1995) Tyrosine modification by reactive nitrogen species. A closer look. Arch. Biochem. Biophys. 319, 341-349.
34. Ischiropoulos, H., and Al-Medi, A. B. (1995) Peroxynitrite-mediated oxidative protein modifications. FEBS Lett. 364, 279-282.
35. Giulivi, C., and Davies, K. J. A. (1993) Dityrosine and tyrosine oxidation products are endogeneous markers for the selective proteolysis of oxidatively modified red blood cell hemoglobin by (the 19S) proteosome. J. Biol. Chem. 268, 8752-8759.
36. Heinecke, J. W., Li, W., Daehnke, H. L., III, and Goldstein, J. A. (1993) Dityrosine, a specific marker of oxidation, is synthesized by the myeloperoxidase-hydrogen peroxide system of human neutrophils and macrophages. J. Biol. Chem. 268, 4069-4077.
37. Dean, R. T., Gieseg, S., and Davies, M. J. (1993) Reactive species and their accumulation on radical-damaged proteins. Trends Biochem. Sci. 18, 437-441.
38. Guptasarma, P., Balasubramanian, D., Matsugo, S., and Saito, I. (1992) Hydroxyl radical mediated damage to proteins, with special reference to the crystallins. Biochemistry 31, 4296-4302.
39. Armstrong, R. C., and Swallow, A. J. (1969) Pulse- and gamma-radiolysis of aqueous solutions of tryptophan. Radiat. Res. 41, 563-579.
40. Winchester, R. V., and Lynn, K. R. (1970) X- and γ-radiolysis of some tryptophan dipeptides. Int. J. Radiat. Biol. 17, 541-549.
41. Pryor, W. A., and Uppu, R. M. (1993) A kinetic model for the competitive reactions of ozone with amino acid residues in proteins in reverse micelles. J. Biol. Chem. 268, 3120-3126.
42. Kikugawa, K., Kato, T., and Okamoto, Y. (1994) Damage of amino acids and proteins induced by nitrogen dioxide, a free radical toxin in air. Free Radical Biol. Med. 16, 373-382.
43. Maskos, Z., Rush, J. D., and Koppenol, W. H. (1992) The hydroxylation of tryptophan. Arch. Biochem. Biophys. 296, 514-520.
44. Taborsky, G. (1973) Oxidative modification of proteins in the presence of ferrous iron and air. Effect of ionic constituents of the reaction medium on the nature of the oxidation products. Biochemistry 12, 1341-1348.
45. Creeth, J. M., Cooper, B., Donald, A. S. R., and Clamp, J. R. (1983) Studies of the limited degradation of mucous glycoproteins. Biochem. J. 211, 323-332.
46. Poston, J. M. (1988) Detection of oxidized amino acid residues using P-aminobenzoic acid adducts. Fed. Proc. 46, 1979 (Abstract).
47. Uchida, K., Kato, Y., and Kawakishi, S. (1990) A novel mechanism for oxidative damage of prolyl peptides induced by hydroxyl radicals. Biochem. Biophys. Res. Commun. 169, 265-271.
48. Schuenstein, E., and Esterbauer, H. (1979) Formation and properties of reactive aldehydes. Submolecular Biology of Cancer, pp 225-244, CIBA Foundation Series 67, Excerpta Medica, Elsevier, Amsterdam.
49. Neuzil, J., Gebiki, J. M., and Stocker, R. (1993) Radical-induced chain oxidation of proteins and its inhibition by chain-breaking antioxidants. Biochem. J. 293, 601-606.
50. Uchida, K., and Stadtman, E. R. (1993) Covalent modification of 4-hydroxynonenal to glyceraldehyde-3-phosphate. J. Biol. Chem. 268, 6388-6393.
51. Friguet, B., Stadtman, E. R., and Szweda, L. (1994) Modification of glucose-6-phosphate dehydrogenase by 4-hydroxy-2-nonenal. J. Biol. Chem. 269, 21639-21643.
52. Nadkarni, D. V., and Sayre, L. M. (1995) Structural definition of early lysine and histidine adduction chemistry of 4-hydroxynonenal. Chem. Res. Toxicol. 8, 284-291.
53. Sayre, L. M., Arora, P. K., Iyer, R. S., and Salomon, R. G. (1993) Pyrrole formation from 4-hydroxynonenal and primary amines. Chem. Res. Toxicol. 6, 19-22.
54. Bruenner, B. A., Jones, A. D., and German, J. B. (1994) Maximum entropy deconvolution of heterogeneity in protein modification: Protein adducts of 4-hydroxy-2-nonenal. Rapid Commun. Mass Spectrom. 8, 509-512.
55. Bruenner, B. A., Jones, A. D., and German, J. B. (1995) Direct characterization of protein adducts of the lipid peroxidation product 4-hydroxy-2-nonenal using electrospray mass spectrometry. Chem. Res. Toxicol. 8, 552-559.
56. Monnier, V., Gerhardinger, C., Marion, M. S., and Taneda, S. (1995) Novel approaches toward inhibition of the Maillard reaction in vivo: Search, isolation, and characterization of prokaryotic enzymes which degrade glycated substrates. In Oxidative Stress and Aging (Cutler, R. G., Packer, L., Bertram, J., and Mori, A., Eds.) pp 141-149, Birkhauser Verlag, Basel, Switzerland.
57. Mullarkey, C. J., Edelstein, D., and Brownlee, M. (1990) Free radical generation by early glycation products. A mechanism for accelerated atherogenesis in diabetes. Biochem. Biophys. Res. Commun. 173, 932-939.
58. Wolf, S. P., and Dean, R. T. (1987) Glucose autoxidation and protein modification. Biochem. J. 245, 243-250.
59. Kristal, B. S., and Yu, B. P. (1992) An emerging hypothesis: Synergistic induction of aging by free radicals and Maillard reactions. J. Gerontol. 47, B104-B107.
60. Cohn, J. A., Tsai, L., Friguet, B., and Szweda, L. I. (1996) Chemical characterization of a protein-4-hydroxy-2-nonenal cross-link: Immunochemical detection in mitochondria exposed to oxidative stress. Arch. Biochem. Biophys. 328, 158-164.
61. Grune, T., Reinheckel, T., Joshi, M., and Davies, K. J. A. (1995) Proteolysis in cultured liver epithelial cells during oxidative stress. J. Biol. Chem. 270, 2344-2351.
62. Friguet, B., Szweda, L., and Stadtman, E. R. (1994) 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, 168-173.
63. Stadtman, E. R. (1990) Metal ion-catalyzed oxidation of proteins: Biochemical mechanism and biological consequences. Free Radical Biol. Med. 9, 315-325.
64. Chevion, M. (1988) A site-specific mechanism for free radical induced biological damage: The essential role of redox-active transition metals. Free Radical Biol. Med. 5, 27-37.
65. Fucci, L., Oliver, C. N., Coon, M. J., and Stadtman, E. R. (1983) Inactivation of key metabolic enzymes by mixed-function oxidation reactions: Possible implications in protein turnover and aging. Proc. Natl. Acad. Sci. U.S.A. 80, 1521-1525.
66. Levine, R. L., Oliver, C. N., Fulks, R. M., and Stadtman, E. R. (1981) Turnover of bacterial glutamine synthetase: Oxidative inactivation precedes proteolysis. Proc. Natl. Acad. Sci. U.S.A. 78, 2120-2124, 1981.
67. Rivett, A. J., and Levine, R. L. (1990) Metal-catalyzed oxidation of Escherichia coli glutamine synthetase: Correlation of structural and functional changes. Arch. Biochem. Biophys. 278, 26-34.
68. Sahakian, J. A., Shames, B. D., and Levine, R. L. (1991) Metal-catalyzed oxidation of glutamine synthetase. Susceptibility to proteolysis requires oxidation of histidine residue at both metal binding sites. FASEB J. 5, A1177 (Abstract).
69. Stadtman, E. R., and Wittenberger, M. E. (1985) Inactivation of Escherichia coli glutamine synthetase by xanthine oxidase, nicotinate hydroxylase, horseradish peroxidase, or glucose oxidase: Effects of ferreodoxin, putidaredoxin, and menadione. Arch. Biochem. Biophys. 239, 379-387.
70. Oliver, C. N., Fucci, L., Levine, R. L., Wittenberger, M. E., and Stadtman, E. R. (1982) Inactivation of key metabolic enzymes by P450 linked mixed function oxidation systems. In Cytochrome P-450, Biochemistry, Biophysics, and Environmental Implications (Heitanen, E., Laitinen, M., and Hanninen, O., Eds.) pp 531-539, Elsevier Biomedical Press, Amsterdam.
71. Levine, R. L. (1983) Oxidation of glutamine synthetase. II. Characterization of the ascorbate model system. J. Biol. Chem. 258, 11828-11833.
72. Kim, K., Rhee, S. G., and Stadtman, E. R. (1985) Nonenzymatic cleavage of proteins by reactive oxygen species generated by dithiothreitol and iron. J. Biol. Chem. 260, 15394-15397.
73. Starke-Reed, P. E., and Oliver, C. N. (1989) Protein Oxidation and proteolysis during aging and oxidative stress. Arch. Biochem. Biophys. 275, 559-567.
74. 3H]hydride reduction. J. Biol. Chem. 266, 14446-14450.
75. Sohal, R. S., Agarwal, S., Dubey, A., and Orr, W. C. (1993) Protein oxidative damage is associated with life expectancy of houseflies. Proc. Natl. Acad. Sci. U.S.A. 90, 7255-7259.
76. Witt, E. H., Reznick, A. Z., Viguie, C. A., Starke-Reed, P. E., and Packer, L. (1992) Exercise, oxidative damage, and effects of antioxidant manipulation. J. Nutr. 122, 766-773.
77. Reznick, A. Z., Witt, E., Matsumoto, M., and Packer, L. (1992) Vitamin E inhibits protein oxidation in skeletal muscle of resting and exercised rats. Biochem. Biophys. Res. Commun. 189, 801-806.
78. Oliver, C. N., Starke-Reed, P. E., Stadtman, E. R., Liu, G. J., Carney, J. M., and Floyd, R. A. (1990) Oxidative damage to brain proteins, loss of glutamine synthetase activity, and production of free radicals during ischemia-reperfusion-induced injury to gerbil brain. Proc. Natl. Acad. Sci. U.S.A. 87, 5144-5147.
79. Poston, J. M., and Parenteau, G. L. (1992) Biochemical effects of ischemia on isolated perfused rat heart tissues. Arch. Biochem. Biophys. 295, 35-41.
80. Oliver, C. N. (1987) Inactivation of enzymes and oxidative modification of proteins by stimulated neutrophils. Arch. Biochem. Biophys. 253, 62-72.
81. Karsek-Staples, J. A., and Webster, R. O. (1993) Ceroplasmin inhibits carbonyl formation in endogenous cell proteins. Free Radical Biol. Med. 14, 115-125.
82. Mickel, H. S., Oliver, C. N., and Starke-Reed, P. E. (1990) Protein oxidation and myelinolysis occur in brain following rapid correction of hyponatremia. Biochem. Biophys. Res. Commun. 172, 92-97.
83. Stafford, R. E., Mak, T. M., Kramer, J. H., and Weglicki, W. B. (1993) Protein oxidation in magnesium deficient rat brains and kidneys. Biochem. Biophys. Res. Commun. 196, 596-600.
84. Cross, C. E., Reznick, A. Z., Packer, L., Davis, P. A., Suzuki, Y. J., and Halliwell, B. (1992) Oxidative damage to human plasma proteins by ozone. Free Radical Res. Commun. 15, 347-352.
85. Kelley, F. J., and Birch, S. (1993) Ozone exposure inhibits cardiac protein synthesis in the mouse. Free Radical Biol. Med. 14, 443-446.
86. Reznick, A. Z., Cross, C. E., Hu, M.-L., Suzuki, Y. J., Khwaja, S., Safadi, A., Motchnik, P. A., Packer, L., and Halliwell, B. (1992) Modification of plasma proteins by cigarette smoke as measured by protein carbonyl formation. Biochem. J. 286, 607-611.
87. Sohal, R. S., and Dubey, A. (1994) Mitochondrial oxidative damage, hydrogen peroxide release, and aging. Free Radical Biol. Med. 16, 621-626.
88. Sohal, R. S., Ku, H.-H., and Agarwal, S. (1993) Biochemical correlates of longevity in two closely related rodent species. Biochem. Biophys. Res. Commun. 196, 7-11.
89. Shacter, E., Williams, J. A., Lim, M., and Levine, R. L. (1994) Differential susceptibility of plasma proteins to oxidative modification: Examination by Western blot immunoassay. Free Radical Biol. Med. 17, 429-437.
90. Troncoso, J. C., Costello, A. C., Kim, J. H., and Johnson, G. V. W. (1995) Metal-catalyzed oxidation of bovine neurofilaments in vitro. Free Radical Biol. Med. 18, 891-899.
91. Wieland, P., and Lauterburg, B. H. (1995) Oxidation of mitochondrial proteins, DNA following administration of ethanol. Biochem. Biophys. Res. Commun. 213, 815-819.
92. Dreyfus, J. C., Kahn, A., and Schapira, F. (1978) Post translational modifications of enzymes. Curr. Top. Cell. Regul. 14, 243-297.
93. Rothstein, M. (1977) Recent developments in age-related alteration of enzymes. Mech. Ageing Dev. 6, 241-257.
94. Oliver, C. N., Ahn, B.-W., Moerman, E. J., Goldstein, S., and Stadtman, E. R. (1987) Age-related changes in oxidized proteins. J. Biol. Chem. 262, 5488-5491.
95. Smith, C. D., Carney, J. M., Starke-Reed, P. E., Oliver, C. N., Stadtman, E. R., and Floyd, R. A. (1991) Excess brain protein oxidation and enzyme dysfunction in normal and Alzheimer's disease. Proc. Natl. Acad. Sci. U.S.A. 88, 10540-10543.
96. Smith, C. D., Carney, J. M., Tatsuno, T., Stadtman, E. R., Floyd, R. A., and Marksbery, W. R. (1994) Protein oxidation in aging brain. In Aging and Cellular Defense Mechanisms (Franceschi, C., Cerpaldi, G., Cristofalo, V. G., and Vijg, J., Eds.) pp 110-119, Vol. 663, New York Academy of Science, New York.
97. Garland, D., Russell, P., and Zigler, J. S. (1988) The oxidative modification of lens proteins. In Oxygen Radicals in Biology and Medicine (Simic, M. G., Taylor, K. S., Ward, J. F., and von Sontag, V., Eds.) pp 347-353, Plenum, New York.
98. Starke-Reed, P. E., and Oliver, C. N. (1989) Protein oxidation and proteolysis during aging and oxidative stress. Arch. Biochem. Biophys. 275, 559-567.
99. Starke, P. E., Oliver, C. N., and Stadtman, E. R. (1987) Modification of hepatic proteins in rats exposed to high oxygen concentration. FASEB J. 1, 36-39.
100. Sohal, R. S., Agarwal, S., and Sohal, B. H. (1995) Oxidative stress and aging in the Mongolian gerbil (Meriones unguiculatus). Mech. Ageing Dev. 81, 15-25.
101. Gordillo, E., Ayala, A., F-Lobato, M., Bautista, J., and Machada, A. (1988) Possible involvement of histidine residues in loss of enyzmatic activity of rat liver malic enzyme during aging. J. Biol. Chem. 263, 8053-8057.
102. De La Cruz, C. P., Revilla, E., Venero, J. L., Ayala, A., Cano, J., and Machado, A. (1996) Oxidative inactivation of tyrosine hydroxylase in Substantia nigra of aged rat. Free Radical Biol. Med. 20, 53-61.
103. Musci, G., Bonaccorsi di Patti, M. C., Fagiolo, U., and Calabrese, L. (1993) Age-related changes in human ceruloplasmin. J. Biol. Chem. 268, 13388-13395.
104. Mordente, A., Martorana, G. E., Miggiano, G. A. D., Meucci, E., Santini, S. A., and Castelli, A. (1988) Mixed function oxidation and enzymes: Kinetic and structural properties of oxidatively modified alkaline phosphatase. Arch. Biochem. Biophys. 264, 502-509.
105. Agarwal, S., and Sohal, R. S. (1993) Relationship between aging and susceptibility to protein oxidative damage. Biochem. Biophys. Res. Commun. 194, 1203-1206.
106. Youngman, L. D., Park, J.-Y. K., and Ames, B. (1992) Protein oxidation associated with aging is reduced by dietary restriction of protein calories. Proc. Natl. Acad. Sci. U.S.A. 89, 9112-9116.
107. Chapman, M. L., Rubin, B. R., and Gracy, R. W. (1989) Increased carbonyl content of proteins in synovial fluid from patients with rheumatoid arthritis. J. Rheumatol. 16, 15-18.
108. Murphy, M. E., and Kherer, J. P. (1989) Oxidation state of tissue thiol groups and content of protein carbonyl groups in chickens with inherited muscular dystrophy. Biochem. J. 260, 359-364.
109. Bowling, A. C., Schultz, J. B., Brown, R. H., Jr., and Beal, M. F. (1993) Superoxide dismutase activity, oxidative damage, and mitochondrial energy metabolism I familial and sporadic amyotrophic lateral sclerosis. J. Neurochem. 61, 2322-2325.
110. Carney, J. M., Smith, C. D., Carney, A. M., and Butterfield, D. A. (1994) Aging- and oxygen-induced modifications in brain biochemistry and behavior. In Aging and Cellular Defense Mechanisms (Franceschi, C., Crepaldi, G., Cristofalo, V. J., and Vijg, J., Eds.) pp 110-119, Vol. 63, New York Academy of Science, New York.
111. Harris, M., Hensley, K., Butterfield, D. A., Leedle, R. A., and Carney, J. M. (1995) Direct evidence of oxidative injury produced by Alzheimer's β-amyloid peptide (1-40) in cultured hippocampal neurons. Exp. Neurol. 131, 193-202.
112. Chauhan, A., Chauhan, V. P. S., Brockerhoff, H., and Wisniewski, H. M. (1991) Action of amyloid β-protein on protein kinase C activity. Life Sci. 49, 1555-1556.
113. Gladstone, I. M., and Levine, R. L. (1994) Oxidation of proteins in neonatal lungs. Pediatrics 93, 764-768.
114. Steinberg, D., Parthasarathy, S., Carew, T. E., Koo, J. C., and Witzum, J. W. (1989) Beyond cholesterol modifications of low-density lipoprotein that increase athrogenicity. N. Engl. J. Med. 320, 915-924.
115. Steinbrecher, U. P. (1987) Oxidation of human low density lipoprotein results in derivatization of lysine residues of apoliprotein B by lipid peroxide decomposition products. J. Biol. Chem. 262, 3603-3608.
116. Kumar, K. V., and Das, U. N. (1993) Pathobiology of human essential hypertension. Free Radical Res. Commun. 19, 59-66.
117. Kubisch H. M., Wang, J., Luche, R., Carlson, E., Bray, T. M., Epstein, C. J., and Phillips, J. P. (1994) Transgenetic copper/zinc superoxide dismutase modulates susceptibility to type 1 diabetes. Proc. Natl. Acad. Sci. U.S.A. 91, 9956-9959.
118. Adams, J. D., Jr. (1991) Oxygen free radicals and Parkinsons disease. Free Radical Biol. Med. 10, 161-169.
119. Riederer P., Sofic, E., Rausch, W.-D., Schmidt, B., Reynolds, G. P., Jellinger, K., and Youdin, B. H. (1989) Transition metals, ferritin, glutathione, and ascorbic acid in Parkinsonian brains. J. Neurochem. 52, 515-520.
120. Brown, R. K., and Kelly, F. (1994) Evidence for increased oxidative damage in patients with cystic fibrosis. Pediatr. Res. 36, 487-493.
121. Winklhofer-Roob, B. M., Ziouzenkova, O., Puhl, H., Ellemunter, H., Greiner, P., Müller, G., Van't Hof, M. A., Esterbauer, H., and Shmerling, O. H. (1995) Impaired resistance to oxidation of low density lipoprotein in cystic fibrosis: Improvement during vitamin E supplements. Free Radical Biol. Med. 19, 725-733.
122. Babbs, C. F. (1992) Oxygen radicals in ulcerative colitis. Free Radical Biol. Med. 13, 169-181.
123. Babbs, C. F. (1990) Free radicals and the etiology of colon cancer. Free Radical Biol. Med. 8, 191-200.
124. Sun, Y. (1990) Free radicals, antioxidants, enzymes, and carcinogenesis. Free Radical Biol. Med. 8, 583-599.
125. Halliwell, B. (1987) Oxidants and human disease: Some new concepts. FASEB J. 1, 358-364.
126. Harmon, D. (1990) Free radical theory of aging: A hypothesis on pathogenesis of senile dementia of the Alzheimer's type. Age 16, 23-30.
127. Katzman, R., and Saitoh, T. (1991) Advances in Alzheimers disease. FASEB J. 5, 278-286.
128. Giaccone, G., Pedrotti, B., Migheli, A., Verga, L., Perez, J., Racaghi, G., Smith, M. A., Perry, G., De Giola, L., Selvaggni, C., Salmona, M., Ghiso, J., Frangione, B., Islam, K., Bugiani, O., and Tagliavini, F. (1996) βPP and tau interaction: A possible link between amyloid and neurofibrillary tangles in Alzheimer's disease. Am. J. Pathol. 148, 79-87.
129. Good, P. F., Werner, P., Hsu, A., Olanow, C. W., and Perl, D. P. (1996) Evidence of neuronal oxidative damage in Alzheimer's disease. Am. J. Pathol. 149 (1), 21-28.
130. Smith, M. A., Rudnicka-Nawrot, M., Richey, P. L., Praprotnik, D., Mulvihill, P., Miller, C. A., Sayre, L. M., and Perry, G. (1995) Carbonyl-related posttranslational modification of neurofilament protein in the neurofibrillary pathology of Alzheimer's disease. J. Neurochem. 64, 2660-2666.
131. Smith, M. A., Perry, G., Richey, P. L., Sayre, L. M., Anderson, V. E., Beal, M. F., and Kowall, N. (1996) Oxidative damage in Alzheimer's disease. Nature 382, 120-121.
132. Balaze, L., and Leon, M. (1994) Evidence of an oxidative challenge in Alzheimer's brain. Neurochem. Res. 19, 1131-1137.
133. Behl, C., Davis, J. B., Lesley, R., and Schubert, D. (1994) Hydrogen peroxide mediates amyloid β protein toxicity. Cell 77, 817-827.
134. Hensley, K., Carney, J. M., Mattson, M. P., Askenova, M., Harris, M., Wu, J. F., Floyd, R. A., and Butterfield, D. A. (1994) A model for β-amyloid aggregation and neurotoxicity based on free radical generation by the peptide: Relevance to Alzheimer's disease. Proc Natl. Acad. Sci. U.S.A. 91, 3270-3274.
135. Hensley, K., Carney, J., Hal, N., Shaw, W., and Butterfield, D. A. (1994) Electron paramagnetic resonance investigations of free radical-induced alterations in neocortical synaptosomal membrane protein infrastructure. Free Radical Biol. Med. 17, 321-331
136. Hensley, K., Hall, N., Subramanian, R., Cole, P., Harris, M., Askenova, M., Gabbita, P., Wu, J. F., Carney, J. M., Lovell, M., Marksbery, W. R., and Butterfield, D. A. (1995) Brain regional correspondence between Alzheimer's disease histopathology and biomarkers of protein oxidation. J. Neurochem. 65, 2146-2156.
137. Pryor, W. A., and Squadrito, G. L. (1995) The chemistry of peroxynitrite: A product from the reaction of nitric oxide with superoxide. Am. J. Physiol. L699-L722.
138. Karoui, H., Hogg, N., Fréjaville, C., Tordo, P., and Kalyanaraman, B. (1996) Characterization of sulfur-centered radical intermediates formed during the oxidation of thiols and sulfite by peroxynitrite. J. Biol. Chem. 271, 6000-6009.
139. Mohr, S., Stamler, J. S., and Brune, B. (1994) Mechanism of covalent modification of glyceraldehyde-3-phosphate dehydrogenase at its active site thiol by nitric oxide, peroxynitrite, and related nitrosating agents. FEBS Lett. 348, 223-227.
140. Gatti, R. M., Radi, R., and Augusto, O. (1994) Peroxynitrite-mediated oxidation of albumin to the protein-thiyl free radical. FEBS Lett. 348, 287-290.
141. Stadtman, E. R., Chock, P. B., and Rhee, S. G. (1981) Interconvertible enzyme cycles in cellular regulation. Curr. Top. Cell. Regul. 18, 79-83.
142. Hunter, T. (1995) Protein kinases and phosphatases: The Yin and Yang of protein phosphorylation and signaling. Cell 80, 225-236.
143. 2 peptide. Proc. Natl. Acad. Sci. U.S.A. 93, 3377-3382.
144. Lymar, S. V., and Hurst, J. K. (1995) Rapid reaction betwen peroxynitrite ion and carbon dioxide: Implications for biological activity. J. Am. Chem. Soc. 117, 8867-8868.
145. Uppu, R. M., Squadrito, G. L., and Pryor, W. A. (1996) Acceleration of peroxynitrite oxidations by carbon dioxide. Arch. Biochem. Biophys. 327, 335-343.
146. Denicola, A., Freeman, B. A., Trujillo, M., and Radi, R. (1996) Peroxynitrite reaction with carbon dioxide/bicarbonate: Kinetics and influence on peroxynitrite-mediated oxidations. Arch. Biochem. Biophys. 333, 49-58.
147. Lymar, S. V., Jiang, Q., and Hurst, J. K. (1996) Mechanism of carbon-dioxide-catalyzed oxidation of tyrosine by peroxynitrite. Biochemistry 35, 7855-7861.
148. Lymar, S. V., and Hurst, J. K. (1996) Carbon dioxide: Physiological catalyst for peroxynitrite-mediated cellular damage or cellular protectant? Chem. Res. Toxicol. 9, 845-850.
149. Rivett, A. J. (1986) Regulation of intracellular protein turnover: Covalent modification as a mechanism of marking proteins for degradation. Curr. Top. Cell. Regul. 28, 291-337.
150. Pacifici, R. E., Salo, D. C., and Davies, K. J. A. (1989) Macro-proteinase (M.O.P.): A 670 kDA proteinase complex that degrades oxidatively denatured proteins in red blood cells. Free Radical Biol. Med. 7, 521-536.
151. Levine, R. L. (1989) Proteolysis induced by metal-catalyzed oxidation. Cell. Biol. Rev. 21, 347-360.
152. Grant, A. J., Jessup, W., and Dean, R. J. (1993) Inefficient degradation of oxidized regions of protein molecules. Free Radical Res. Commun. 18, 259-267.
153. Carney, J. M., Starke-Reed, P. E., Oliver, C. N., Landum, R. W., Cheng, M. S., Wu, J. F., and Floyd, R. A. (1991) Reversal of age-related increase in brain protein oxidation, decrease in enzyme activity loss and loss of temporal and spatial memory by chronic administration of the spin-trapping compound N-terf-butyl-α-phenylnitrone. Proc. Natl. Acad. Sci. U.S.A. 88, 3633-3636.
154. Forster, M. J., Dubey, A., Dawson, K. M., Stutts, W. A., Lal, H., and Sohal, R. S. (1996) Age-related losses of cognitive function and motor skills in mice are associated with oxidative protein damage in the brain. Proc. Natl. Acad. Sci. U.S.A. 93, 4765-4769.