The SOD2 mutant mouse as a model for oxidative stress: A functional proteomics perspective

Mass Spectrometry Reviews

Volumn 29, Issue 2, 2010, Pages 179-196

  Lee, Yie Hou ^a   Lin, Qingsong ^b   Boelsterli, Urs A ^c   Chung, Maxey C M ^a,b  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c UNIVERSITY OF CONNECTICUT   (United States)

Author keywords

Druginduced liver injury; Functional proteomics; Mass spectrometry; Mitochondria; Oxidative stress; SOD2

Indexed keywords

ANTIOXIDANT DEFENSE; BIO-MOLECULAR; BIOLOGICAL CHANGES; COMBINATORIAL APPROACH; DIVERSE RANGE; FUNCTIONAL PROTEOMICS; HUMAN DISEASE; LIVER INJURIES; MITOCHONDRIAL DYSFUNCTION; MITOCHONDRIAL STRESS; MUTANT MICE; PROTEIN DYNAMICS; PROTEOMICS; SYSTEMS APPROACH;

FREE RADICAL REACTIONS; FREE RADICALS; FUNCTIONAL GROUPS; LIVER; MASS SPECTROMETRY; MITOCHONDRIA; MOLECULAR BIOLOGY; OXIDATIVE STRESS;

PROTEINS;

MANGANESE SUPEROXIDE DISMUTASE; PROTEOME; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE;

ANIMAL; ANIMAL MODEL; BIOLOGICAL MODEL; GENE EXPRESSION PROFILING; GENETICS; HUMAN; MASS SPECTROMETRY; METABOLISM; METHODOLOGY; MITOCHONDRION; MOUSE; MOUSE MUTANT; MUTATION; OXIDATIVE STRESS; PEPTIDE MAPPING; PHYSIOLOGY; REVIEW;

ANIMALS; GENE EXPRESSION PROFILING; HUMANS; MASS SPECTROMETRY; MICE; MICE, KNOCKOUT; MITOCHONDRIA; MODELS, ANIMAL; MODELS, BIOLOGICAL; MUTATION; OXIDATIVE STRESS; PEPTIDE MAPPING; PROTEOME; REACTIVE OXYGEN SPECIES; SUPEROXIDE DISMUTASE;

EID: 77951230874     PISSN: 02777037     EISSN: 10982787     Source Type: Journal    
DOI: 10.1002/mas.20226     Document Type: Review

References (141)

1. Abdel-Aziz AF, El-Naggar MM. 1997. Superoxide dismutase activities in serum and white blood cells of patients with some malignancies. Cancer Lett 113:61-64.
2. Alban A, David SO, Bjorkesten L, Andersson C, Sloge E, Lewis S, Currie I. 2003. A novel experimental design for comparative two-dimensional gel analysis: Two-dimensional difference gel electrophoresis incorporating a pooled internal standard. Proteomics 3:36-44.
3. Ambrosone CB, Freudenheim JL, Thompson PA, Bowman E, Vena JE, Marshall JR, Graham S, Laughlin R, Nemoto T, Shields PG. 1999. Manganese superoxide dismutase (MnSOD) genetic polymorphisms, dietary antioxidants, and risk of breast cancer. Cancer Res 59:602-606.
4. Andersen JS, Mann M. 2006. Organellar proteomics: Turning inventories into insights. EMBO Rep 7:874-879.
5. Arbiser JL. 2004. Molecular regulation of angiogenesis and tumorigenesis by signal transduction pathways: Evidence of predictable and reproducible patterns of synergy in diverse neoplasms. Semin Cancer Biol 14:81-91.
6. Atkinson AJ, Colburn WA, DeGruttola VG, DeMets DL, Downing GJ, Hoth DF, Oates JAP, Carl C, Schooley RT, Spilker BA, Woodcock J, Zeger SL. 2001. Biomarkers and surrogate endpoints: Preferred definitions and conceptual framework. Clin Pharmacol Ther 69:89-95.
7. Bai Y, Markham K, Chen F, Weerasekera R, Watts J, Home P, Wakutani Y, Bagshaw R, Mathews PM, Fraser PE, Westaway D, St George-Hyslop P, Schmitt-Ulms G. 2008. The in vivo brain interactome of the amyloid precursor protein. Mol Cell Proteomics 7:15-34.
8. Bailey SM, Landar A, Darley-Usmar V. 2005. Mitochondrial proteomics in free radical research. Free Radic Biol Med 38:175-188.
9. Benchoua A, Trioulier Y, Zala D, Gaillard MC, Lefort N, Dufour N, Saudou F, Elalouf JM, Hirsch E, Hantraye P, Deglon N, Brouillet E. 2006. Involvement of mitochondrial complex II defects in neuronal death produced by N-terminus fragment of mutated huntingtin. Mol Biol Cell 17:1652-1663.
10. Bi X, Lin Q, Foo TW, Joshi S, You T, Shen HM, Ong CN, Cheah PY, Eu KW, Hew CL. 2006. Proteomic analysis of colorectal cancer reveals alterations in metabolic pathways: Mechanism of tumorigenesis. Mol Cell Proteomics 5:1119-1130.
11. Boelsterli UA. 2003. Animal models of human disease in drug safety assessment. J Toxicol Sci 28:109-121.
12. +/- mouse: mouse: Modeling the mitochondrial role in drug toxicity. Drug Discov Today 13:982-988.
13. Boelsterli UA, Lee YH. 2008. Development of animal models of drug-induced mitochondrial toxicity. In: Will Y, Dykens JA, editors. Mitochondrial dysfunction in drug-induced toxicity. Hoboken, NJ: Wiley, pp. 539-554.
14. Bonawitz ND, Shadel GS. 2007. Rethinking the mitochondrial theory of aging: The role of mitochondrial gene expression in lifespan determination. Cell Cycle 6:1574-1578.
15. Bota DA, Davies KJ. 2002. Lon protease preferentially degrades oxidized mitochondrial aconitase by an ATP-stimulated mechanism. Nat Cell Biol 4:674-680.
16. Braun RJ, Kinkl N, Beer M, Ueffing M. 2007. Two-dimensional electrophoresis of membrane proteins. Anal Bioanal Chem 389:1033-1045.
17. Brown GC, Borutaite V. 2002. Nitric oxide inhibition of mitochondrial respiration and its role in cell death. Free Radic Biol Med 33:1440-1450.
18. Bulteau AL, Ikeda-Saito M, Szweda LI. 2003. Redox-dependent modulation of aconitase activity in intact mitochondria. Biochemistry 42:14846-14855.
19. Bulteau AL, Lundberg KC, Ikeda-Saito M, Isaya G, Szweda LI. 2005. Reversible redox-dependent modulation of mitochondrial aconitase and proteolytic activity during in vivo cardiac ischemia/reperfusion. Proc Natl Acad Sci USA 102:5987-5991.
20. Butow RA, Avadhani NG. 2004. Mitochondrial signaling: The retrograde response. Mol Cell 14:1-15.
21. Calvo S, Jain M, Xie X, Sheth SA, Chang B, Goldberger OA, Spinazzola A, Zeviani M, Carr SA, Mootha VK. 2006. Systematic identification of human mitochondrial disease genes through integrative genomics. Nat Genet 38:576-582.
22. Chance B, Sies H, Boveris A. 1979. Hydroperoxide metabolism in mammalian organs. Physiol Rev 59:527-605.
23. Chang TK, Abbott FS. 2006. Oxidative stress as a mechanism of valproic acid-associated hepatotoxicity. Drug Metab Rev 38:627-639.
24. Chang J, Van Remmen H, Ward WF, Regnier FE, Richardson A, Cornell J. 2004. Processing of data generated by 2-dimensional gel electrophoresis for statistical analysis: Missing data, normalization, and statistics. J Proteome Res 3:1210-1218.
25. Chen Q, Vazquez EJ, Moghaddas S, Hoppel CL, Lesnefsky EJ. 2003. Production of reactive oxygen species by mitochondria: Central role of complex III. J Biol Chem 278:36027-36031.
26. Chuang TC, Liu JY, Lin CT, Tang YT, Yeh MH, Chang SC, Li JW, Kao MC. 2007. Human manganese superoxide dismutase suppresses HER2/neumediated breast cancer malignancy. FEBS Lett 581:4443-4449.
27. Church SL, Grant JW, Ridnour LA, Oberley LW, Swanson PE, Meltzer PS, Trent JM. 1993. Increased manganese superoxide dismutase expression suppresses the malignant phenotype of human melanoma cells. Proc Natl Acad Sci USA 90:3113-3117.
28. Cohen AA, Geva-Zatorsky N, Eden E, Frenkel-Morgenstern M, Issaeva I, Sigal A, Milo R, Cohen-Saidon C, Liron Y, Kam Z, Cohen L, Danon T, Perzov N, Alon U. 2008. Dynamic proteomics of individual cancer cells in response to a drug. Science 322:1511-1516.
29. Cox J, Mann M. 2007. Is proteomics the new genomics? Cell 130:395-398.
30. Da Cruz S, Xenarios I, Langridge J, Vilbois F, Parone PA, Martinou JC. 2003. Proteomic analysis of the mouse liver mitochondrial inner membrane. J Biol Chem 278:41566-41571.
31. Dalle-Donne I, Scaloni A, Giustarini D, Cavarra E, Tell G, Lungarella G, Colombo R, Rossi R, Milzani A. 2005. Proteins as biomarkers of oxidative/nitrosative stress in diseases: The contribution of redox proteomics. Mass Spectrom Rev 24:55-99.
32. Danial NN, Gramm CF, Scorrano L, Zhang CY, Krauss S, Ranger AM, Datta SR, Greenberg ME, Licklider LJ, Lowell BB, Gygi SP, Korsmeyer SJ. 2003. BAD and glucokinase reside in a mitochondrial complex that integrates glycolysis and apoptosis. Nature 424:952-956.
33. Delaval E, Perichon M, Friguet B. 2004. Age-related impairment of mitochondrial matrix aconitase and ATP-stimulated protease in rat liver and heart. Eur J Biochem 271:4559-4564.
34. Dixit R, Boelsterli UA. 2007. Healthy animals and animal models of human disease(s) in safety assessment of human pharmaceuticals, including therapeutic antibodies. Drug Discov Today 12:336-342.
35. Doctrow SR, Baudry M, Huffman K, Malfroy B, Melov S. 2005. Salen manganese complexes: Multifunctional catalytic antioxidants protective in models for neurodegenerative diseases of aging. In: Sessler JL, Doctrow SR, McMurry TJ, Lippard SJ, editors. Medicinal inorganic chemistry. Washington, DC, New York: Oxford University Press, pp. 301-320.
36. Droge W. 2002. Free radicals in the physiological control of cell function. Physiol Rev 82:47-95.
37. Elrick MM, Walgren JL, Mitchell MD, Thompson DC. 2006. Proteomics: Recent applications and new technologies. Basic Clin Pharmacol Toxicol 98:432-441.
38. Faca VM, Song KS, Wang H, Zhang Q, Krasnoselsky AL, Newcomb LF, Plentz RR, Gurumurthy S, Redston MS, Pitteri SJ, Pereira-Faca SR, Ireton RC, Katayama H, Glukhova V, Phanstiel D, Brenner DE, Anderson MA, Misek D, Scholler N, Urban ND, Barnett MJ, Edelstein C, Goodman GE, Thornquist MD, Mcintosh MW, DePinho RA, Bardeesy N, Hanash SM. 2008. A mouse to human search for plasma proteome changes associated with pancreatic tumor development. PLoS Med5:e123.
39. Forner F, Arriaga EA, Mann M. 2006. Mild protease treatment as a small-scale biochemical method for mitochondria purification and proteomic mapping of cytoplasm-exposed mitochondrial proteins. J Proteome Res 5:3277-3287.
40. Foster LJ, de Hoog CL, Zhang Y, Zhang Y, Xie X, Mootha VK, Mann M. 2006. A mammalian organelle map by protein correlation profiling. Cell 125:187-199.
41. Frank R, Hargreaves R. 2003. Clinical biomarkers in drug discovery and development. Nat Rev Drug Discov 2:566-580.
42. Gao X, Zhang P. 2007. Transgenic RNA interference in mice. Physiology 22:161-166.
43. Gardner PR, Raineri I, Epstein LB, White CW. 1995. Superoxide radical and iron modulate aconitase activity in mammalian cells. J Biol Chem 270: 13399-13405.
44. Gaucher SP, Taylor SW, Fahy E, Zhang B, Warnock DE, Ghosh SS, Gibson BW. 2004. Expanded coverage of the human heart mitochondrial proteome using multidimensional liquid chromatography coupled with tandem mass spectrometry. J Proteome Res 3:495-505.
45. Gibson GE, Park LCH, Sheu K-FR, Blass JP, Calingasan NY 2000. The a-ketoglutarate dehydrogenase complex in neurodegeneration. Neurochem Int 36:97-112.
46. Godovac-Zimmermann J, Kleiner O, Brown LR, Drukier AK. 2005. Perspectives in spicing up proteomics with splicing. Proteomics 5:699-709.
47. Golden TR, Hubbard A, Morten KJ, Hinerfeld D, Melov S. 2005. Pharmacogenomic profiling of an oxidative stress-mediated spongiform encephalopathy. Free Radic Biol Med 39:152-163.
48. Graham DJ, Green L, Senior JR, Nourjah P. 2002. Troglitazone-induced liver failure: A case study. Am J Med 114:299-306.
49. Griffin JL. 2006. Understanding mouse models of disease through metabolomics. Curr Opin Chem Biol 10:309-315.
50. Gu M, Gash MT, Mann VM, Javoy-Agid F, Cooper JM, Schapira AH. 1996. Mitochondrial defect in Huntington's disease caudate nucleus. Ann Neurol 39:385-389.
51. Guengerich FP, MacDonald JS. 2007. Applying mechanisms of chemical toxicity to predict drug safety. Chem Res Toxicol 20:344-369.
52. Gunay-Aygun M. 2005. 3-Methylglutaconic aciduria: A common biochemical marker in various syndromes with diverse clinical features. Mol Genet Metab 84:1-3.
53. Halliwell B, Gutteridge JM, Aruoma OI. 1987. The deoxyribose method: A simple "test-tube" assay for determination of rate constants for reactions of hydroxyl radicals. Anal Biochem 165:215-219.
54. Hamdan M, Righetti PG. 2002. Modern strategies for protein quantification in proteome analysis: Advantages and limitations. Mass Spectrom Rev 21:287-302.
55. Hanash S. 2003. Disease proteomics. Nature 422:226-232.
56. Hanash SM, Pitteri SJ, Faca VM. 2008. Mining the plasma proteome for cancer biomarkers. Nature 452:571-579.
57. 2 formation by rat heart mitochondria on substrate availability and donor age. J Bioenerg Biomembr 29:89-95.
58. Hinerfeld D, Traini MD, Weinberger RP, Cochran B, Doctrow SR, Harry J, Melov S. 2004. Endogenous mitochondrial oxidative stress: Neurodegeneration, proteomic analysis, specific respiratory chain defects, and efficacious antioxidant therapy in superoxide dismutase 2 null mice. J Neurochem 88:657-667.
59. Huang TT, Carlson EJ, Kozy HM, Mantha S, Goodman SI, Ursell PC, Epstein CJ. 2001. Genetic modification of prenatal lethality and dilated cardiomyopathy in Mn superoxide dismutase mutant mice. Free Radic Biol Med 31:1101-1110.
60. Humphries KM, Szweda LI. 1998. Selective inactivation of alpha-ketoglutarate dehydrogenase and pyruvate dehydrogenase: Reaction of lipoic acid with 4-hydroxy-2-nonenal. Biochemistry 37:15835-15841.
61. Hunzinger C, Wozny W, Schwall GP, Poznanovic S, Stegmann W, Zengerling H, Schoepf R, Groebe K, Cahill MA, Osiewacz HD, Jagemann N, Bloch M, Dencher NA, Krause F, Schrattenholz A. 2006. Comparative profiling of the mammalian mitochondrial proteome: Multiple aconitase-2 isoforms including N-formylkynurenine modifications as part of a protein biomarker signature for reactive oxidative species. J Proteome Res 5:625-633.
62. Hurt EM, Thomas SB, Peng B, Farrar WL. 2007a. Integrated molecular profiling of SOD2 expression in multiple myeloma. Blood 109:3953-3962.
63. Hurt EM, Thomas SB, Peng B, Farrar WL. 2007b. Molecular consequences of SOD2 expression in epigenetically silenced pancreatic carcinoma cell lines. Br J Cancer 97:1116-1123.
64. Ikegami T, Suzuki Y, Shimizu T, Isono K, Koseki H, Shirasawa T. 2002. Model mice for tissue-specific deletion of the manganese superoxide dismutase (MnSOD) gene. Biochem Biophys Res Commun 296:729-736.
65. Inarrea P, Moini H, Rettori D, Han D, Martinez J, Garcia I, Fernandez-Vizarra E, Iturralde M, Cadenas E. 2005. Redox activation of mitochondrial intermembrane space Cu,Zn-superoxide dismutase. Biochem J 387: 203-209.
66. Jiang X-S, Dai J, Sheng Q-H, Zhang L, Xia Q-C, Wu J-R, Zeng R. 2005. A comparative proteomic strategy for subcellular proteome research. Mol Cell Proteomics 4:12-34.
67. Jungblut P, Thiede B. 1997. Protein identification from 2-DE gels by MALDI mass spectrometry. Mass Spectrom Rev 16:145-162.
68. Kaplowitz N. 2005. Idiosyncratic drug hepatotoxicity. Nature Rev Drug Discov 4:489-499.
69. Kato M, Minakami H, Kuroiwa M, Kobayashi Y, Oshima S, Kozawa K, Morikawa A, Kimura H. 2003. Superoxide radical generation and Mnand Cu-Zn superoxide dismutases activities in human leukemic cells. Hematol Oncol 21:11-16.
70. Kennedy S. 2002. The role of proteomics in toxicology: Identification of biomarkers of toxicity by protein expression analysis. Biomarkers 7:269-290.
71. Kirkwood TBL. 2008. A systematic look at an old problem. Nature 451:644-647.
72. Kislinger T, Cox B, Kannan A, Chung C, Hu P, Ignatchenko A, Scott MS, Gramolini AO, Morris Q, Hallett MT, Rossant J, Hughes TR, Frey B, Emili A. 2006. Global survey of organ and organelle protein expression in mouse: Combined proteomic and transcriptomic profiling. Cell 125:173-186.
73. Klaunig JE, Kamendulis LM. 2004. The role of oxidative stress in carcinogenesis. Annu Rev Pharmacol Toxicol 44:239-267.
74. Klungland A, Rosewell I, Hollenbach S, Larsen E, Daly G, Epe B, Seeberg E, Lindahl T, Barnes DE. 1999. Accumulation of premutagenic DNA lesions in mice defective in removal of oxidative base damage. Proc Natl Acad Sci USA 96:13300-13305.
75. +/- mouse results in the age-related decline of mitochondrial function culminating in increased apoptosis. Proc Natl Acad Sci USA 98:2278-2283.
76. Krishnan KJ, Greaves LC, Reeve AK, Turnbull D. 2007. The ageing mitochondrial genome. Nucleic Acids Res 35:7399-7405.
77. Kuhn E, Wu J, Karl J, Liao H, Zolg W, Guild B. 2004. Quantification of C-reactive protein in the serum of patients with rheumatoid arthritis using multiple reaction monitoring mass spectrometry and 13C-labeled peptide standards. Proteomics 4:1175-1186.
78. Lai KK, Kolippakkam D, Beretta L. 2008. Comprehensive and quantitative proteome profiling of the mouse liver and plasma. Hepatology 47: 1043-1051.
79. Larsson R, Cerutti P. 1989. Translocation and enhancement of phosphotransferase activity of protein kinase C following exposure in mouse epidermal cells to oxidants. Cancer Res 49:5627-5632.
80. Lebovitz RM, Zhang H, Vogel H, Cartwright J, Dionne L, Lu N, Huang S, Matzuk MM. 1996. Neurodegeneration, myocardial injury, and perinatal death in mitochondrial superoxide dismutase-deficient mice. Proc Natl Acad Sci USA 93:9782-9787.
81. Lee YH, Boelsterli UA, Lin Q, Chung MC. 2008a. Proteomics profiling of hepatic mitochondria in heterozygous Sod2(+/-) mice, an animal model of discreet mitochondrial oxidative stress. Proteomics 8:555-568.
82. +/- mice: Two-stage oxidative injury. Toxicol Appl Pharmacol 231:43-51.
83. Lei XG. 2002. In vivo antioxidant role of glutathione peroxidase: Evidence from knockout mice. Methods Enzymol 347:213-225.
84. LiJJ, Oberley LW, St Clair DK, Ridnour LA, Oberley TD. 1995a. Phenotypic changes induced in human breast cancer cells by overexpression of manganese-containing superoxide dismutase. Oncogene 10:1989-2000.
85. Li Y, Huang TT, Carlson EJ, Melov S, Ursell PC, Olson JL, Noble LJ, Yoshimura MP, Berger C, Chan PH, Wallace DC, Epstein CJ. 1995b. Dilated cardiomyopathy and neonatal lethality in mutant mice lacking manganese superoxide dismutase. Nat Genet 11:376-381.
86. -/+ mice. Free Radic Biol Med 36:542-554.
87. Lim MS, Lim PL, Gupta R, Boelsterli UA. 2006. Critical role of free cytosolic calcium, but not uncoupling, in mitochondrial permeability transition and cell death induced by diclofenac oxidative metabolites in immortalized human hepatocytes. Toxicol Appl Pharmacol 217:322-331.
88. Lin MT, Beal MF. 2006. Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 443:787-795.
89. Lynn S, Huang EJ, Elchuri S, Naeemuddin M, Nishinaka Y, Yodoi J, Ferriero DM, Epstein CJ, Huang TT. 2005. Selective neuronal vulnerability and inadequate stress response in superoxide dismutase mutant mice. Free Radic Biol Med 38:817-828.
90. Mansouri A, Muller FL, Liu Y, Ng R, Faulkner J, Hamilton M, Richardson A, Huang TT, Epstein CJ, Van Remmen H. 2006. Alterations in mitochondrial function, hydrogen peroxide release and oxidative damage in mouse hind-limb skeletal muscle during aging. Mech Ageing Dev 127:298-306.
91. McDonald T, Sheng S, Stanley B, Chen D, Ko Y, Cole RN, Pedersen P, Van Eyk JE. 2006. Expanding the subproteome of the inner mitochondria using protein separation technologies: One- and two-dimensional liquid chromatography and two-dimensional gel electrophoresis. Mol Cell Proteomics 5:2392-2411.
92. Melov S, Schneider JA, Day BJ, Hinerfeld D, Coskun P, Mirra SS, Crapo JD, Wallace DC. 1998. A novel neurological phenotype in mice lacking mitochondrial manganese superoxide dismutase. Nat Genet 18:159-163.
93. Melov S, Coskun P, Patel M, Tuinstra R, Cottrell B, Jun AS, Zastawny TH, Dizdaroglu M, Goodman SI, Huang TT, Miziorko H, Epstein CJ, Wallace DC. 1999a. Mitochondrial disease in superoxide dismutase 2 mutant mice. Proc Natl Acad Sci USA 96:846-851.
94. Melov S, Coskun PE, Wallace DC. 1999b. Mouse models of mitochondrial disease, oxidative stress, and senescence. Mutat Res 434:233-242.
95. Melov S, Doctrow SR, Schneider JA, Haberson J, Patel M, Coskun PE, Huffman K, Wallace DC, Malfroy B. 2001. Lifespan extension and rescue of spongiform encephalopathy in superoxide dismutase 2 nullizygous mice treated with superoxide dismutase-catalase mimetics. J Neurosci 21:8348-8353.
96. Melov S, Adlard PA, Morten K, Johnson F, Golden TR, Hinerfeld D, Schilling B, Mavros C, Masters CL, Volitakis I, Li QX, Laughton K, Hubbard A, Cherny RA, Gibson B, Bush AI. 2007. Mitochondrial oxidative stress causes hyperphosphorylation of tau. PLoS ONE 2:e536.
97. Mootha VK, Bunkenborg J, Olsen JV, Hjerrild M, Wisniewski JR, Stahl EB, Ray HN, Sihag S, Kamal M, Patterson N, Lander ES, Mann M. 2003. Integrated analysis of protein composition, tissue diversity, and gene regulation in mouse mitochondria. Cell 115:629-640.
98. Morten KJ, Ackrell BA, Melov S. 2006. Mitochondrial reactive oxygen species in mice lacking superoxide dismutase 2: Attenuation via antioxidant treatment. J Biol Chem 281:3354-3359.
99. Muller JM, Cahill MA, Rupec RA, Baeuerle PA, Nordheim A. 1997. Antioxidants as well as oxidants activate c-fos via Ras-dependent activation of extracellular-signal-regulated kinase 2 and EIk-1. Eur J Biochem 244:45-52.
100. Muller FL, Liu Y, Van Remmen H. 2004. Complex III releases superoxide to both sides of the inner mitochondrial membrane. J Biol Chem 279: 49064-49073.
101. Nesvizhskii AI, Aebersold R. 2005. Interpretation of shotgun proteomic data: The protein inference problem. Mol Cell Proteomics 4:1419-1440.
102. New LS, Saha S, Ong MM, Boelsterli UA, Chan EC. 2007. Pharmacokinetic study of intraperitoneally administered troglitazone in mice using ultraperformance liquid chromatography/tandem mass spectrometry. Rapid Commun Mass Spectrom 21:982-988.
103. Nierkens S, Pieters R. 2005. Murine models of drug hypersensitivity. Curr Opin Allergy Clin Immunol 5:331-335.
104. Nojiri H, Shimizu T, Funakoshi M, Yamaguchi O, Zhou H, Kawakami S, Ohta Y, Sami M, Tachibana T, Ishikawa H, Kurosawa H, Kahn RC, Otsu K, Shirasawa T. 2006. Oxidative stress causes heart failure with impaired mitochondrial respiration. J Biol Chem 281:33789-33801.
105. Okado-Matsumoto A, Fridovich I. 2001. Subcellular distribution of superoxide dismutases (SOD) in rat liver: Cu, Zn-SOD in mitochondria. J Biol Chem 276:38388-38393.
106. +/- mice. Free Radic Biol Med 40:420-429.
107. Ong MMK, Latchoumycandane C, Boelsterli UA. 2007. Troglitazoneinduced hepatic necrosis in an animal model of silent mitochondrial abnormalities. Toxicol Sci 97:205-213.
108. Orrenius S, Gogvadze V, Zhivotovsky B. 2007. Mitochondrial oxidative stress: Implications for cell death. Annu Rev Pharmacol Toxicol 47: 143-183.
109. Pagliarini DJ, Calvo SE, Chang B, Sheth SA, Vafai SB, Ong SE, Walford GA, Sugiana C, Boneh A, Chen WK, Hill DE, Vidal M, Evans JG, Thorburn DR, Carr SA, Mootha VK. 2008. A mitochondrial protein compendium elucidates complex I disease biology. Cell 134:112-123.
110. Pessayre D, Mansouri A, Haouzi D, Fromenty B. 1999. Hepatotoxicity due to mitochondrial dysfunction. Cell Biol Toxicol 15:367-373.
111. Pryor WA, HoukKN, Foote CS, Fukuto JM, Ignarro LJ, Squadrito GL, Davies KJ. 2006. Free radical biology and medicine: It's a gas, man. Am J Physiol Regul Integr Comp Physiol 291:R491-R511.
112. Quij ano C, Hernandez-Saavedra D, Castro L, McCord JM, Freeman BA, Radi R. 2001. Reaction of peroxynitrite with Mn-superoxide dismutase. Role of the metal center in decomposition kinetics and nitration. J Biol Chem 276:11631-11638.
113. Radi R, Turrensll JF, Chang LY, Bush KM, Crapo JD, Freeman BA. 1991. Detection of catalase in rat heart mitochondria. J Biol Chem 266: 22028-22034.
114. Ratain MJ, Glassman RH. 2007. Biomarkers in phase I oncology trials: Signal, noise, or expensive distraction? Clin Cancer Res 13:6545-6548.
115. Richter C. 1995. Oxidative damage to mitochondrial DNA and its relationship to ageing. Int J Biochem Cell Biol 27:647-653.
116. Salvi M, Battaglia V, Brunati AM, La Rocca N, Tibaldi E, Pietrangeli P, Marcocci L, Mondovi B, Rossi CA, Toninello A. 2007. Catalase takes part in rat liver mitochondria oxidative stress defense. J Biol Chem 282:24407-24415.
117. Sandbach JM, Coscun PE, Grossnikiaus HE, Kokoszka JE, Newman NJ, Wallace DC. 2001. Ocular pathology in mitochondrial superoxide dismutase (Sod2)-deficient mice. Invest Ophthalmol Vis Sci 42:2173-2178.
118. Schapira AH. 2006. Mitochondrial disease. Lancet 368:70-82.
119. Shenton JM, Chen J, Uetrecht JP. 2004. Animal models of idiosyncratic drug reactions. Chem Biol Interact 150:53-70.
120. Shull S, Heintz NH, Periasamy M, Manohar M, Janssen YM, Marsh JP, Mossman BT. 1991. Differential regulation of antioxidant enzymes in response to oxidants. J Biol Chem 266:24398-24403.
121. Slaughter MR, Thakkar H, O'Brien PJ. 2003. Differential expression of the lenticular antioxidant system in laboratory animals: A determinant of species predilection to oxidative stress-induced ocular toxicity? Curr Eye Res 26:15-23.
122. Smith MA, Hirai K, Hsiao K, Pappolla MA, Harris PL, Siedlak SL, Tabaton M, Perry G. 1998. Amyloid-beta deposition in Alzheimer transgenic mice is associated with oxidative stress. J Neurochem 70:2212-2215.
123. Sohal RS, Weindruch R. 1996. Oxidative stress, caloric restriction, and aging. Science 273:59-63.
124. Strassburger M, Bloch W, Sulyok S, Schuller J, Keist AF, Schmidt A, Wenk J, Peters T, Wlaschek M, Lenart J, Krieg T, Hafner M, Kumin A, Werner S, Muller W, Scharffetter-Kochanek K. 2005. Heterozygous deficiency of manganese superoxide dismutase results in severe lipid peroxidation and spontaneous apoptosis in murine myocardium in vivo. Free Radic Biol Med 38:1458-1470.
125. Sturtz LA, Diekert K, Jensen LT, Lill R, Culotta VC. 2001. A fraction of yeast Cu.Zn-superoxide dismutase and its metallochaperone, CCS, localize to the intermembrane space of mitochondria. A physiological role for SOD1 in guarding against mitochondrial oxidative damage. J Biol Chem 276:38084-38089.
126. Suter L, Babiss LE, Wheeldon EB. 2004. Toxicogenomics in predictive toxicology in drug development. Chem Biol 11:161-171.
127. Taylor SW, Fahy E, Zhang B, Glenn GM, Warnock DE, Wiley S, Murphy AN, Gaucher SP, Capaldi RA, Gibson BW, Ghosh SS. 2003. Characterization of the human heart mitochondrial proteome. Nat Biotechnol 21:281-286.
128. Tennant RW. 2002. The National Center for Toxicogenomics: Using new technologies to inform mechanistic toxicology. Environ Health Perspect 110:A8-A10.
129. Van Remmen H, Salvador C, Yang H, Huang TT, Epstein CJ, Richardson A. 1999. Characterization of the antioxidant status of the heterozygous manganese superoxide dismutase knockout mouse. Arch Biochem Biophys 363:91-97.
130. Van Remmen H, Williams MD, Guo Z, Estlack L, Yang H, Carlson EJ, Epstein CJ, Huang TT, Richardson A. 2001. Knockout mice heterozygous for Sod2 show alterations in cardiac mitochondrial function and apoptosis. Am J Physiol Heart Circ Physiol 281:H1422-H1432.
131. Van Remmen H, Ikeno Y, Hamilton M, Pahlavani M, Wolf N, Thorpe SR, Alderson NL, Baynes JW, Epstein CJ, Huang TT, Nelson J, Strong R, Richardson A. 2003. Life-long reduction in MnSOD activity results in increased DNA damage and higher incidence of cancer but does not accelerate aging. Physiol Genomics 16:29-37.
132. Veenstra TD, Prieto DA, Conrads TP. 2004. Proteomic patterns for early cancer detection. Drug Discov Today 9:889-897.
133. Vijayvergiya C, Beal MF, Buck J, Manfredi G. 2005. Mutant superoxide dismutase 1 forms aggregates in the brain mitochondrial matrix of amyotrophic lateral sclerosis mice. J Neurosci 25:2463-2470.
134. Wallace DC. 1999. Mitochondrial diseases in man and mouse. Science 283:1482-1488.
135. Wetmore BA, Merrick BA. 2004. Toxicoproteomics: Proteomics applied to toxicology and pathology. Toxicol Pathol 32:619-642.
136. Williams MD, Van Remmen H, Conrad CC, Huang TT, Epstein CJ, Richardson A. 1998. Increased oxidative damage is correlated to altered mitochondrial function in heterozygous manganese superoxide dismutase knockout mice. J Biol Chem 273:28510-28515.
137. Yamakura F, Taka H, Fujimura T, Murayama K. 1998. Inactivation of human manganese-superoxide dismutase by peroxynitrite is caused by exclusive nitration of tyrosine 34 to 3-nitrotyrosine. J Biol Chem 273:14085-14089.
138. Yan L-J, Levine RL, Sohal RS. 1997. Oxidative damage during aging targets mitochondrial aconitase. Proc Natl Acad Sci USA 94:11168-11172.
139. Yates JR III, Gilchrist A, Howell KE, Bergeron JJ. 2005. Proteomics of organelles and large cellular structures. Nat Rev Mol Cell Biol 6:702-714.
140. Zhang L, Yu L, Yu CA. 1998. Generation of superoxide anion by succinatecytochrome c reductase from bovine heart mitochondria. J Biol Chem 273:33972-33976.
141. Zhao Y Oberley TD, Chaiswing L, Lin SM, Epstein CJ, Huang TT, St Clair D. 2002. Manganese superoxide dismutase deficiency enhances cell turnover via tumor promoter-induced alterations in AP-1 and p53-mediated pathways in a skin cancer model. Oncogene 21:3836-3846.