MnSOD in oxidative stress response-potential regulation via mitochondrial protein influx

Antioxidants and Redox Signaling

Volumn 20, Issue 10, 2014, Pages 1599-1617

  Candas, Demet ^a   Li, Jian Jian ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE; CYCLIN DEPENDENT KINASE; CYCLINE; GLUTATHIONE PEROXIDASE; HYDROGEN PEROXIDE; MANGANESE SUPEROXIDE DISMUTASE; MITOCHONDRIAL PROTEIN; PROTEIN P53; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE;

ACETYLATION; AEROBIC METABOLISM; ELECTRIC POTENTIAL; ENZYME ACTIVITY; GENE EXPRESSION REGULATION; HLUTATHIONYLATION; HUMAN; METAL BINDING; METHYLATION; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; NITRATION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN METHYLATION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN TRANSPORT; REVIEW; TRANSCRIPTION REGULATION;

ANIMALS; GENE EXPRESSION REGULATION; HUMANS; MITOCHONDRIAL PROTEINS; OXIDATIVE STRESS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; SUPEROXIDE DISMUTASE; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84895766266     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2013.5305     Document Type: Review

References (196)

1. Ahmed KM, Fan M, Nantajit D, Cao N, and Li JJ. Cyclin D1 in low-dose radiation-induced adaptive resistance. Oncogene 27: 6738-6748, 2008
2. Ahmed KM and Li JJ. NF-kappa B-mediated adaptive resistance to ionizing radiation. Free Radic Biol Med 44: 1-13, 2008
3. Ahmed KM, Nantajit D, Fan M, Murley JS, Grdina DJ, and Li JJ. Coactivation of ATM/ERK/NF-kappaB in the lowdose radiation-induced radioadaptive response in human skin keratinocytes. Free Radic Biol Med 46: 1543-1550, 2009
4. Ahn BH, Kim HS, Song S, Lee IH, Liu J, Vassilopoulos A, Deng CX, and Finkel T. A role for the mitochondrial deacetylase Sirt3 in regulating energy homeostasis. Proc Natl Acad Sci U S A 105: 14447-14452, 2008
5. Aitken A, Collinge DB, van Heusden BP, Isobe T, Roseboom PH, Rosenfeld G, and Soll J. 14-3-3 proteins: A highly conserved, widespread family of eukaryotic proteins. Trends Biochem Sci 17: 498-501, 1992
6. Alonso A, Sasin J, Bottini N, Friedberg I, Osterman A, Godzik A, Hunter T, Dixon J, and Mustelin T. Protein tyrosine phosphatases in the human genome. Cell 117: 699-711, 2004
7. Archambaud C, Nahori MA, Pizarro-Cerda J, Cossart P, and Dussurget O. Control of Listeria superoxide dismutase by phosphorylation. J Biol Chem 281: 31812-31822, 2006
8. Aulak KS, Miyagi M, Yan L, West KA, Massillon D, Crabb JW, and Stuehr DJ. Proteomic method identifies proteins nitrated in vivo during inflammatory challenge. Proc Natl Acad Sci U S A 98: 12056-12061, 2001
9. Azarashvili TS, Tyynela J, Odinokova IV, Grigorjev PA, Baumann M, Evtodienko YV, and Saris NE. Phosphorylation of a peptide related to subunit c of the F0F1-ATPase/ ATP synthase and relationship to permeability transition pore opening in mitochondria. J Bioenerg Biomembr 34: 279-284, 2002
10. Azzam EI, Jay-Gerin JP, and Pain D. Ionizing radiationinduced metabolic oxidative stress and prolonged cell injury. Cancer Lett 327: 48-60, 2012
11. Barra D, Schinina ME, Simmaco M, Bannister JV, Bannister WH, Rotilio G, and Bossa F. The primary structure of human liver manganese superoxide dismutase. J Biol Chem 259: 12595-12601, 1984
12. Beckman JS, Beckman TW, Chen J, Marshall PA, and Freeman BA. Apparent hydroxyl radical production by peroxynitrite: Implications for endothelial injury from nitric oxide and superoxide. Proc Natl Acad Sci U S A 87: 1620-1624, 1990
13. Bhattacharjee D. Role of radioadaptation on radiation-induced thymic lymphoma in mice. Mutat Res 358: 231-235, 1996
14. Bijur GN and Jope RS. Glycogen synthase kinase-3 beta is highly activated in nuclei and mitochondria. Neuroreport 14: 2415-2419, 2003
15. Bijur GN and Jope RS. Rapid accumulation of Akt in mitochondria following phosphatidylinositol 3-kinase activation. J Neurochem 87: 1427-1435, 2003
16. Bischoff JR, Friedman PN, Marshak DR, Prives C, and Beach D. Human p53 is phosphorylated by p60-cdc2 and cyclin B-cdc2. Proc Natl Acad Sci U S A 87: 4766-4770, 1990
17. Boerner JL, Demory ML, Silva C, and Parsons SJ. Phosphorylation of Y845 on the epidermal growth factor receptor mediates binding to the mitochondrial protein cytochrome c oxidase subunit II. Mol Cell Biol 24: 7059-7071, 2004
18. Boonstra J and Post JA. Molecular events associated with reactive oxygen species and cell cycle progression in mammalian cells. Gene 337: 1-13, 2004
19. Borgstahl GE, Parge HE, Hickey MJ, Beyer WF, Jr., Hallewell RA, and Tainer JA. The structure of human mitochondrial manganese superoxide dismutase reveals a novel tetrameric interface of two 4-helix bundles. Cell 71: 107-118, 1992
20. Bustamante E and Pedersen PL. High aerobic glycolysis of rat hepatoma cells in culture: Role of mitochondrial hexokinase. Proc Natl Acad Sci U S A 74: 3735-3739, 1977
21. Bykova NV, Egsgaard H, and Moller IM. Identification of 14 new phosphoproteins involved in important plant mitochondrial processes. FEBS Lett 540: 141-146, 2003
22. Candas D, Fan M, Nantajit D, Vaughan AT, Murley J, Woloschak G, Grdina DJ, and Li JJ. CyclinB1/Cdk1 phosphorylates mitochondrial antioxidant MnSOD in cell adaptive response to radiation stress. J Mol Cell Biol 2013 [Epub ahead of print]; DOI: 10.1093/jmcb/mjs062
23. Cardone L, Carlucci A, Affaitati A, Livigni A, DeCristofaro T, Garbi C, Varrone S, Ullrich A, Gottesman ME, Avvedimento EV, and Feliciello A. Mitochondrial AKAP121 binds and targets protein tyrosine phosphatase D1, a novel positive regulator of src signaling. Mol Cell Biol 24: 4613-4626, 2004
24. Cartwright P, Beilharz T, Hansen P, Garrett J, and Lithgow T. Mft52, an acid-bristle protein in the cytosol that delivers precursor proteins to yeast mitochondria. J Biol Chem 272: 5320-5325, 1997
25. Castellano I, Cecere F, De Vendittis A, Cotugno R, Chambery A, Di Maro A, Michniewicz A, Parlato G, Masullo M, Avvedimento EV, De Vendittis E, and Ruocco MR. Rat mitochondrial manganese superoxide dismutase: Amino acid positions involved in covalent modifications, activity, and heat stability. Biopolymers 91: 1215-1226, 2009
26. Castellano I, Ruocco MR, Cecere F, Di Maro A, Chambery A, Michniewicz A, Parlato G, Masullo M, and De Vendittis E. Glutathionylation of the iron superoxide dismutase from the psychrophilic eubacterium Pseudoalteromonas haloplanktis. Biochim Biophys Acta 1784: 816-826, 2008
27. Chang TS, Jeong W, Choi SY, Yu S, Kang SW, and Rhee SG. Regulation of peroxiredoxin I activity by Cdc2-mediated phosphorylation. J Biol Chem 277: 25370-25376, 2002
28. Chipuk JE, Kuwana T, Bouchier-Hayes L, Droin NM, Newmeyer DD, Schuler M, and Green DR. Direct activation of Bax by p53 mediates mitochondrial membrane permeabilization and apoptosis. Science 303: 1010-1014, 2004
29. Clerch LB and Massaro D. Tolerance of rats to hyperoxia. Lung antioxidant enzyme gene expression. J Clin Invest 91: 499-508, 1993
30. Curtis C, Landis GN, Folk D, Wehr NB, Hoe N, Waskar M, Abdueva D, Skvortsov D, Ford D, Luu A, Badrinath A, Levine RL, Bradley TJ, Tavare S, and Tower J. Transcriptional profiling of MnSOD-mediated lifespan extension in Drosophila reveals a species-general network of aging and metabolic genes. Genome Biol 8: R262, 2007
31. Dalle-Donne I, Rossi R, Colombo G, Giustarini D, and Milzani A. Protein S-glutathionylation: A regulatory device from bacteria to humans. Trends Biochem Sci 34: 85-96, 2009
32. Das KC, Lewis-Molock Y, and White CW. Thiol modulation of TNF alpha and IL-1 induced MnSOD gene expression and activation of NF-kappa B. Mol Cell Biochem 148: 45-57, 1995
33. de Diego-Otero Y, Romero-Zerbo Y, el Bekay R, Decara J, Sanchez L, Rodriguez-de Fonseca F, and del Arco-Herrera I. Alpha-Tocopherol protects against oxidative stress in the fragile X knockout mouse: An experimental therapeutic approach for the Fmr1 deficiency. Neuropsychopharmacology 34: 1011-1026, 2009
34. Dekker PJ, Martin F, Maarse AC, Bomer U, Muller H, Guiard B, Meijer M, Rassow J, and Pfanner N. The Tim core complex defines the number of mitochondrial translocation contact sites and can hold arrested preproteins in the absence of matrix Hsp70-Tim44. EMBO J 16: 5408-5419, 1997
35. Desai BN, Myers BR, and Schreiber SL. FKBP12-rapamycinassociated protein associates with mitochondria and senses osmotic stress via mitochondrial dysfunction. Proc Natl Acad Sci U S A 99: 4319-4324, 2002
36. Dhar SK, Xu Y, and St Clair DK. Nuclear factor kappaBand specificity protein 1-dependent p53-mediated bidirectional regulation of the human manganese superoxide dismutase gene. J Biol Chem 285: 9835-9846, 2010
37. Drane P, Bravard A, Bouvard V, and May E. Reciprocal down-regulation of p53 and SOD2 gene expressionimplication in p53 mediated apoptosis. Oncogene 20: 430-439, 2001
38. Droge W. Free radicals in the physiological control of cell function. Physiol Rev 82: 47-95, 2002
39. Dudley P, Wood CK, Pratt JR, and Moore AL. Developmental regulation of the plant mitochondrial matrix located HSP70 chaperone and its role in protein import. FEBS Lett 417: 321-324, 1997
40. Duttaroy A, Paul A, Kundu M, and Belton A. A Sod2 null mutation confers severely reduced adult life span in Drosophila. Genetics 165: 2295-2299, 2003
41. Eiserich JP, Patel RP, and O'Donnell VB. Pathophysiology of nitric oxide and related species: Free radical reactions and modification of biomolecules. Mol Aspects Med 19: 221-357, 1998
42. Eldridge A, Fan M, Woloschak G, Grdina DJ, Chromy BA, and Li JJ. Manganese superoxide dismutase interacts with a large scale of cellular and mitochondrial proteins in lowdose radiation-induced adaptive radioprotection. Free Radic Biol Med 53: 1838-1847, 2012
43. Epperly MW, Sikora C, Defilippi S, Bray J, Koe G, Liggitt D, Luketich JD, and Greenberger JS. Plasmid/liposome transfer of the human manganese superoxide dismutase transgene prevents ionizing irradiation-induced apoptosis in human esophagus organ explant culture. Int J Cancer 90: 128-137, 2000
44. Epperly MW, Sikora CA, DeFilippi SJ, Gretton JA, Zhan Q, Kufe DW, and Greenberger JS. Manganese superoxide dismutase (SOD2) inhibits radiation-induced apoptosis by stabilization of the mitochondrial membrane. Radiat Res 157: 568-577, 2002
45. Evans MD, Dizdaroglu M, and Cooke MS. Oxidative DNA damage and disease: Induction, repair and significance. Mutat Res 567: 1-61, 2004
46. Fan J, Li Y, Levy RM, Fan JJ, Hackam DJ, Vodovotz Y, Yang H, Tracey KJ, Billiar TR, and Wilson MA. Hemorrhagic shock induces NAD(P)H oxidase activation in neutrophils: Role of HMGB1-TLR4 signaling. J Immunol 178: 6573-6580, 2007
47. Fan M, Ahmed KM, Coleman MC, Spitz DR, and Li JJ. Nuclear factor-kappaB and manganese superoxide dismutase mediate adaptive radioresistance in low-dose irradiated mouse skin epithelial cells. Cancer Res 67: 3220-3228, 2007
48. Farmer G, Friedlander P, Colgan J, Manley JL, and Prives C. Transcriptional repression by p53 involves molecular interactions distinct from those with the TATA box binding protein. Nucleic Acids Res 24: 4281-4288, 1996
49. Feinendegen LE, Bond VP, Sondhaus CA, and Muehlensiepen H. Radiation effects induced by low doses in complex tissue and their relation to cellular adaptive responses. Mutat Res 358: 199-205, 1996
50. Feng Y, Ariza ME, Goulet AC, Shi J, and Nelson MA. Death-signal-induced relocalization of cyclin-dependent kinase 11 to mitochondria. Biochem J 392: 65-73, 2005
51. Folz RJ and Crapo JD. Extracellular superoxide dismutase (SOD3): Tissue-specific expression, genomic characterization, and computer-Assisted sequence analysis of the human EC SOD gene. Genomics 22: 162-171, 1994
52. Forman HJ, Fukuto JM, and Torres M. Redox signaling: Thiol chemistry defines which reactive oxygen and nitrogen species can act as second messengers. Am J Physiol Cell Physiol 287: C246-C256, 2004
53. Freeman BA and Crapo JD. Hyperoxia increases oxygen radical production in rat lungs and lung mitochondria. J Biol Chem 256: 10986-10992, 1981
54. Frei B, Winterhalter KH, and Richter C. Menadione-(2-methyl-1,4- naphthoquinone-) dependent enzymatic redox cycling and calcium release by mitochondria. Biochemistry 25: 4438-4443, 1986
55. Fridovich I. The biology of oxygen radicals. Science 201: 875-880, 1978
56. Fridovich I. Superoxide radical and superoxide dismutases. Annu Rev Biochem 64: 97-112, 1995
57. Funfschilling U and Rospert S. Nascent polypeptideassociated complex stimulates protein import into yeast mitochondria. Mol Biol Cell 10: 3289-3299, 1999
58. Gius D and Spitz DR. Redox signaling in cancer biology. Antioxid Redox Signal 8: 1249-1252, 2006
59. Gonzalez FA, Raden DL, and Davis RJ. Identification of substrate recognition determinants for human ERK1 and ERK2 protein kinases. J Biol Chem 266: 22159-22163, 1991
60. Grdina DJ, Murley JS, Kataoka Y, and Calvin DP. Differential activation of nuclear transcription factor kappaB, gene expression, and proteins by amifostine's free thiol in human microvascular endothelial and glioma cells. Semin Radiat Oncol 12: 103-111, 2002
61. Gregory EM and Fridovich I. Oxygen toxicity and the superoxide dismutase. J Bacteriol 114: 1193-1197, 1973
62. Groves JT. Peroxynitrite: Reactive, invasive and enigmatic. Curr Opin Chem Biol 3: 226-235, 1999
63. Gudi R, Bowker-Kinley MM, Kedishvili NY, Zhao Y, and Popov KM. Diversity of the pyruvate dehydrogenase kinase gene family in humans. J Biol Chem 270: 28989-28994, 1995
64. Guo G, Yan-Sanders Y, Lyn-Cook BD, Wang T, Tamae D, Ogi J, Khaletskiy A, Li Z, Weydert C, Longmate JA, Huang TT, Spitz DR, Oberley LW, and Li JJ. Manganese superoxide dismutase-mediated gene expression in radiationinduced adaptive responses. Mol Cell Biol 23: 2362-2378, 2003
65. Guo W, Adachi T, Matsui R, Xu S, Jiang B, Zou MH, Kirber M, Lieberthal W, and Cohen RA. Quantitative assessment of tyrosine nitration of manganese superoxide dismutase in angiotensin II-infused rat kidney. Am J Physiol Heart Circ Physiol 285: H1396-H1403, 2003
66. Guo Y, Cheong N, Zhang Z, De Rose R, Deng Y, Farber SA, Fernandes-Alnemri T, and Alnemri ES. Tim50, a component of the mitochondrial translocator, regulates mitochondrial integrity and cell death. J Biol Chem 279: 24813-24825, 2004
67. Hachiya N, Alam R, Sakasegawa Y, Sakaguchi M, Mihara K, and Omura T. A mitochondrial import factor purified from rat liver cytosol is an ATP-dependent conformational modulator for precursor proteins. EMBO J 12: 1579-1586, 1993
68. Halliwell B. Oxidative stress and cancer: Have we moved forward? Biochem J 401: 1-11, 2007
69. Halliwell B and Gutteridge JMC. Free Radicals in Biology and Medicine. Oxford: Clarendon Press, 1989
70. Hass MA and Massaro D. Regulation of the synthesis of superoxide dismutases in rat lungs during oxidant and hyperthermic stresses. J Biol Chem 263: 776-781, 1988
71. Hawlitschek G, Schneider H, Schmidt B, Tropschug M, Hartl FU, and Neupert W. Mitochondrial protein import: Identification of processing peptidase and of PEP, a processing enhancing protein. Cell 53: 795-806, 1988
72. He H, Chen M, Scheffler NK, Gibson BW, Spremulli LL, and Gottlieb RA. Phosphorylation of mitochondrial elongation factor Tu in ischemic myocardium: Basis for chloramphenicol-mediated cardioprotection. Circ Res 89: 461-467, 2001
73. Hitchler MJ, Oberley LW, and Domann FE. Epigenetic silencing of SOD2 by histone modifications in human breast cancer cells. Free Radic Biol Med 45: 1573-1580, 2008
74. Holley AK, Bakthavatchalu V, Velez-Roman JM, and St Clair DK. Manganese superoxide dismutase: Guardian of the powerhouse. Int J Mol Sci 12: 7114-7162, 2011
75. Holley AK, Xu Y, St Clair DK, and St Clair WH. RelB regulates manganese superoxide dismutase gene and resistance to ionizing radiation of prostate cancer cells. AnnN Y Acad Sci 1201: 129-136, 2010
76. Holness MJ and Sugden MC. Regulation of pyruvate dehydrogenase complex activity by reversible phosphorylation. Biochem Soc Trans 31: 1143-1151, 2003
77. Hopper RK, Carroll S, Aponte AM, Johnson DT, French S, Shen RF, Witzmann FA, Harris RA, and Balaban RS. Mitochondrial matrix phosphoproteome: Effect of extra mitochondrial calcium. Biochemistry 45: 2524-2536, 2006
78. Horbinski C and Chu CT. Kinase signaling cascades in the mitochondrion: A matter of life or death. Free Radic Biol Med 38: 2-11, 2005
79. Hosoki A, Yonekura S, Zhao QL, Wei ZL, Takasaki I, Tabuchi Y, Wang LL, Hasuike S, Nomura T, Tachibana A, Hashiguchi K, Yonei S, Kondo T, and Zhang-Akiyama QM. Mitochondria-Targeted superoxide dismutase (SOD2) regulates radiation resistance and radiation stress response in HeLa cells. J Radiat Res 53: 58-71, 2012
80. Houten SM and Wanders RJ. A general introduction to the biochemistry of mitochondrial fatty acid beta-oxidation. J Inherit Metab Dis 33: 469-477, 2010
81. Huang P, Feng L, Oldham EA, Keating MJ, and Plunkett W. Superoxide dismutase as a target for the selective killing of cancer cells. Nature 407: 390-395, 2000
82. Hunt CR, Sim JE, Sullivan SJ, Featherstone T, Golden W, Von Kapp-Herr C, Hock RA, Gomez RA, Parsian AJ, and Spitz DR. Genomic instability and catalase gene amplification induced by chronic exposure to oxidative stress. Cancer Res 58: 3986-3992, 1998
83. Hurd TR, Costa NJ, Dahm CC, Beer SM, Brown SE, Filipovska A, and Murphy MP. Glutathionylation of mitochondrial proteins. Antioxid Redox Signal 7: 999-1010, 2005
84. Hurt EM, Thomas SB, Peng B, and Farrar WL. Molecular consequences of SOD2 expression in epigenetically silenced pancreatic carcinoma cell lines. Br J Cancer 97: 1116-1123, 2007
85. Hussain SP, Amstad P, He P, Robles A, Lupold S, Kaneko I, Ichimiya M, Sengupta S, Mechanic L, Okamura S, Hofseth LJ, Moake M, Nagashima M, Forrester KS, and Harris CC. p53-induced up-regulation of MnSOD and GPx but not catalase increases oxidative stress and apoptosis. Cancer Res 64: 2350-2356, 2004
86. Iglesias-Bartolome R, Patel V, Cotrim A, Leelahavanichkul K, Molinolo AA, Mitchell JB, and Gutkind JS. mTOR Inhibition Prevents Epithelial Stem Cell Senescence and Protects from Radiation-Induced Mucositis. Cell Stem Cell 11: 401-414, 2012
87. Kang BP, Urbonas A, Baddoo A, Baskin S, Malhotra A, and Meggs LG. IGF-1 inhibits the mitochondrial apoptosis program in mesangial cells exposed to high glucose. Am J Physiol Renal Physiol 285: F1013-F1024, 2003
88. Kennedy G, Spence VA, McLaren M, Hill A, Underwood C, and Belch JJ. Oxidative stress levels are raised in chronic fatigue syndrome and are associated with clinical symptoms. Free Radic Biol Med 39: 584-589, 2005
89. Kim A, Murphy MP, and Oberley TD. Mitochondrial redox state regulates transcription of the nuclear-encoded mitochondrial protein manganese superoxide dismutase: A proposed adaptive response to mitochondrial redox imbalance. Free Radic Biol Med 38: 644-654, 2005
90. Kim A, Zhong W, and Oberley TD. Reversible modulation of cell cycle kinetics in NIH/3T3 mouse fibroblasts by inducible overexpression of mitochondrial manganese superoxide dismutase. Antioxid Redox Signal 6: 489-500, 2004
91. Kiningham KK and St Clair DK. Overexpression of manganese superoxide dismutase selectively modulates the activity of Jun-Associated transcription factors in fibrosarcoma cells. Cancer Res 57: 5265-5271, 1997
92. Koehler CM, Beverly KN, and Leverich EP. Redox pathways of the mitochondrion. Antioxid Redox Signal 8: 813-822, 2006
93. Kumar S, Bharti A, Mishra NC, Raina D, Kharbanda S, Saxena S, and Kufe D. Targeting of the c-Abl tyrosine kinase to mitochondria in the necrotic cell death response to oxidative stress. J Biol Chem 276: 17281-17285, 2001
94. Li JJ, Oberley LW, St Clair DK, Ridnour LA, and Oberley TD. Phenotypic changes induced in human breast cancer cells by overexpression of manganese-containing superoxide dismutase. Oncogene 10: 1989-2000, 1995
95. This reference has been deleted
96. Li Z, Shi K, Guan L, Cao T, Jiang Q, Yang Y, and Xu C. ROS leads to MnSOD upregulation through ERK2 translocation and p53 activation in selenite-induced apoptosis of NB4 cells. FEBS Lett 584: 2291-2297, 2010
97. Lin T, Chao C, Saito S, Mazur SJ, Murphy ME, Appella E, and Xu Y. p53 induces differentiation of mouse embryonic stem cells by suppressing Nanog expression. Nat Cell Biol 7: 165-171, 2005
98. Liu SZ, Cai L, and Sun SQ. Induction of a cytogenetic adaptive response by exposure of rabbits to very low doserate gamma-radiation. Int J Radiat Biol 62: 187-190, 1992
99. Lombard DB, Alt FW, Cheng HL, Bunkenborg J, Streeper RS, Mostoslavsky R, Kim J, Yancopoulos G, Valenzuela D, Murphy A, Yang Y, Chen Y, Hirschey MD, Bronson RT, Haigis M, Guarente LP, Farese RV, Jr., Weissman S, Verdin E, and Schwer B. Mammalian Sir2 homolog SIRT3 regulates global mitochondrial lysine acetylation. Mol Cell Biol 27: 8807-8814, 2007
100. Luk E, Carroll M, Baker M, and Culotta VC. Manganese activation of superoxide dismutase 2 in Saccharomyces cerevisiae requires MTM1, a member of the mitochondrial carrier family. Proc Natl Acad Sci U S A 100: 10353-10357, 2003
101. Luk EE and Culotta VC. Manganese superoxide dismutase in Saccharomyces cerevisiae acquires its metal co-factor through a pathway involving the Nramp metal transporter, Smf2p. J Biol Chem 276: 47556-47562, 2001
102. MacMillan-Crow LA, Crow JP, and Thompson JA. Peroxynitrite-mediated inactivation of manganese superoxide dismutase involves nitration and oxidation of critical tyrosine residues. Biochemistry 37: 1613-1622, 1998
103. Macmillan-Crow LA and Cruthirds DL. Invited review: Manganese superoxide dismutase in disease. Free Radic Res 34: 325-336, 2001
104. Maiorino M, Scapin M, Ursini F, Biasolo M, Bosello V, and Flohe L. Distinct promoters determine alternative transcription of gpx-4 into phospholipid-hydroperoxide glutathione peroxidase variants. J Biol Chem 278: 34286-34290, 2003
105. Mancuso M, Davidzon G, Kurlan RM, Tawil R, Bonilla E, Di Mauro S, and Powers JM. Hereditary ferritinopathy: A novel mutation, its cellular pathology, and pathogenetic insights. J Neuropathol Exp Neurol 64: 280-294, 2005
106. Martin J, Mahlke K, and Pfanner N. Role of an energized inner membrane in mitochondrial protein import. Delta psi drives the movement of presequences. J Biol Chem 266: 18051-18057, 1991
107. Martin RC, Li Y, Liu Q, Jensen NS, Barker DF, Doll MA, and Hein DW. Manganese superoxide dismutase V16A single-nucleotide polymorphism in the mitochondrial targeting sequence is associated with reduced enzymatic activity in cryopreserved human hepatocytes. DNA Cell Biol 28: 3-7, 2009
108. Matsuda Y, Higashiyama S, Kijima Y, Suzuki K, Kawano K, Akiyama M, Kawata S, Tarui S, Deutsch HF, and Taniguchi N. Human liver manganese superoxide dismutase. Purification and crystallization, subunit association and sulfhydryl reactivity. Eur J Biochem 194: 713-720, 1990
109. May T and Soll J. 14-3-3 proteins form a guidance complex with chloroplast precursor proteins in plants. Plant Cell 12: 53-64, 2000
110. Mettler FA. Medical Effects of Ionizing Radiation. Philadelphia: Saunders, 1985, p. 304
111. Mihara M, Erster S, Zaika A, Petrenko O, Chittenden T, Pancoska P, and Moll UM. p53 has a direct apoptogenic role at the mitochondria. Mol Cell 11: 577-590, 2003
112. Morgan DO. Cyclin-dependent kinases: Engines, clocks, and microprocessors. Annu Rev Cell Dev Biol 13: 261-291, 1997
113. Morgan DO. The Cell Cycle: Principles of Control. London: New Science Press, Ltd. 2007
114. Murakami K, Tanase S, Morino Y, and Mori M. Presequence binding factor-dependent and-independent import of proteins into mitochondria. J Biol Chem 267: 13119-13122, 1992
115. Murley JS, Baker KL, Miller RC, Darga TE, Weichselbaum RR, and Grdina DJ. SOD2-mediated adaptive responses induced by low-dose ionizing radiation via TNF signaling and amifostine. Free Radic Biol Med 51: 1918-1925, 2011
116. Murley JS, Kataoka Y, Baker KL, Diamond AM, Morgan WF, and Grdina DJ. Manganese superoxide dismutase (SOD2)-mediated delayed radioprotection induced by the free thiol form of amifostine and tumor necrosis factor alpha. Radiat Res 167: 465-474, 2007
117. Murley JS, Kataoka Y, Cao D, Li JJ, Oberley LW, and Grdina DJ. Delayed radioprotection by NFkappaBmediated induction of Sod2 (MnSOD) in SA-NH tumor cells after exposure to clinically used thiol-containing drugs. Radiat Res 162: 536-546, 2004
118. Murley JS, Kataoka Y, Weydert CJ, Oberley LW, and Grdina DJ. Delayed radioprotection by nuclear transcription factor kappaB-mediated induction of manganese superoxide dismutase in human microvascular endothelial cells after exposure to the free radical scavenger WR1065. Free Radic Biol Med 40: 1004-1016, 2006
119. Nabel GJ and Verma IM. Proposed NF-kappa B/I kappa B family nomenclature. Genes Dev 7: 2063, 1993
120. Nantajit D, Fan M, Duru N, Wen Y, Reed JC, and Li JJ. Cyclin B1/Cdk1 phosphorylation of mitochondrial p53 induces anti-Apoptotic response. PLoS One 5: E12341, 2010
121. Nulton-Persson AC and Szweda LI. Modulation of mitochondrial function by hydrogen peroxide. J Biol Chem 276: 23357-23361, 2001
122. Oberley LW. Mechanism of the tumor suppressive effect of MnSOD overexpression. Biomed Pharmacother 59: 143-148, 2005
123. Oberley LW, Lindgren LA, Baker SA, and Stevens RH. Superoxide lon as the cause of the oxygen effect. Radiat Res 68: 320-328, 1976
124. Oberley LW, St Clair DK, Autor AP, and Oberley TD. Increase in manganese superoxide dismutase activity in the mouse heart after X-irradiation. Arch Biochem Biophys 254: 69-80, 1987
125. Oberley TD, Verwiebe E, Zhong W, Kang SW, and Rhee SG. Localization of the thioredoxin system in normal rat kidney. Free Radic Biol Med 30: 412-424, 2001
126. Oda K, Arakawa H, Tanaka T, Matsuda K, Tanikawa C, Mori T, Nishimori H, Tamai K, Tokino T, Nakamura Y, and Taya Y. p53AIP1, a potential mediator of p53-dependent apoptosis, and its regulation by Ser-46-phosphorylated p53. Cell 102: 849-862, 2000
127. Ohman T, Parish G, and Jackson RM. Hypoxic modulation of manganese superoxide dismutase promoter activity and gene expression in lung epithelial cells. Am J Respir Cell Mol Biol 21: 119-127, 1999
128. Okado-Matsumoto A and Fridovich I. Subcellular distribution of superoxide dismutases (SOD) in rat liver: Cu,Zn-SOD in mitochondria. J Biol Chem 276: 38388-38393, 2001
129. Ozden O, Park SH, Kim HS, Jiang H, Coleman MC, Spitz DR, and Gius D. Acetylation of MnSOD directs enzymatic activity responding to cellular nutrient status or oxidative stress. Aging (Albany, NY) 3: 102-107, 2011
130. Ozeki M, Tamae D, Hou DX, Wang T, Lebon T, Spitz DR, and Li JJ. Response of cyclin B1 to ionizing radiation: Regulation by NF-kappaB and mitochondrial antioxidant enzyme MnSOD. Anticancer Res 24: 2657-2663, 2004
131. Pagliarini DJ and Dixon JE. Mitochondrial modulation: Reversible phosphorylation takes center stage? Trends Biochem Sci 31: 26-34, 2006
132. Pagliarini DJ, Wiley SE, Kimple ME, Dixon JR, Kelly P, Worby CA, Casey PJ, and Dixon JE. Involvement of a mitochondrial phosphatase in the regulation of ATP production and insulin secretion in pancreatic beta cells. Mol Cell 19: 197-207, 2005
133. Pan S and Berk BC. Glutathiolation regulates tumor necrosis factor-Alpha-induced caspase-3 cleavage and apoptosis: Key role for glutaredoxin in the death pathway. Circ Res 100: 213-219, 2007
134. Pandey BN, Gordon DM, De Toledo SM, Pain D, and Azzam EI. Normal human fibroblasts exposed to high-or low-dose ionizing radiation: Differential effects on mitochondrial protein import and membrane potential. Antioxid Redox Signal 8: 1253-1261, 2006
135. Pfanner N and Geissler A. Versatility of the mitochondrial protein import machinery. Nat Rev Mol Cell Biol 2: 339-349, 2001
136. Qiu X, Brown K, Hirschey MD, Verdin E, and Chen D. Calorie restriction reduces oxidative stress by SIRT3-mediated SOD2 activation. Cell Metab 12: 662-667, 2010
137. Quijano C, Hernandez-Saavedra D, Castro L, McCord JM, Freeman BA, and Radi R. Reaction of peroxynitrite with Mn-superoxide dismutase. Role of the metal center in decomposition kinetics and nitration. J Biol Chem 276: 11631-11638, 2001
138. Radi R, Cassina A, Hodara R, Quijano C, and Castro L. Peroxynitrite reactions and formation in mitochondria. Free Radic Biol Med 33: 1451-1464, 2002
139. Ramond A, Godin-Ribuot D, Ribuot C, Totoson P, Koritchneva I, Cachot S, Levy P, and Joyeux-Faure M. Oxidative stress mediates cardiac infarction aggravation induced by intermittent hypoxia. Fundam Clin Pharmacol 2011 [Epub ahead of print]; DOI: 10.1111/j.1472-8206.2011.01015.x.
140. Ravindranath SD and Fridovich I. Isolation and characterization of a manganese-containing superoxide dismutase from yeast. J Biol Chem 250: 6107-6112, 1975
141. Redondo-Horcajo M, Romero N, Martinez-Acedo P, Martinez-Ruiz A, Quijano C, Lourenco CF, Movilla N, Enriquez JA, Rodriguez-Pascual F, Rial E, Radi R, Vazquez J, and Lamas S. Cyclosporine A-induced nitration of tyrosine 34 MnSOD in endothelial cells: Role of mitochondrial superoxide. Cardiovasc Res 87: 356-365, 2010
142. Rhee SG, Kang SW, Chang TS, Jeong W, and Kim K. Peroxiredoxin, a novel family of peroxidases. IUBMB Life 52: 35-41, 2001
143. Ridnour LA, Sim JE, Choi J, Dickinson DA, Forman HJ, Ahmad IM, Coleman MC, Hunt CR, Goswami PC, and Spitz DR. Nitric oxide-induced resistance to hydrogen peroxide stress is a glutamate cysteine ligase activitydependent process. Free Radic Biol Med 38: 1361-1371, 2005
144. Robinson KM and Lemire BD. Covalent attachment of FAD to the yeast succinate dehydrogenase flavoprotein requires import into mitochondria, presequence removal, and folding. J Biol Chem 271: 4055-4060, 1996
145. Roise D, Horvath SJ, Tomich JM, Richards JH, and Schatz G. A chemically synthesized pre-sequence of an imported mitochondrial protein can form an amphiphilic helix and perturb natural and artificial phospholipid bilayers. EMBO J 5: 1327-1334, 1986
146. Roise D and Schatz G. Mitochondrial presequences. J Biol Chem 263: 4509-4511, 1988
147. Rosini P, De Chiara G, Bonini P, Lucibello M, Marcocci ME, Garaci E, Cozzolino F, and Torcia M. Nerve growth factordependent survival of CESS B cell line is mediated by increased expression and decreased degradation of MAPK phosphatase 1. J Biol Chem 279: 14016-14023, 2004
148. Salvi M, Brunati AM, and Toninello A. Tyrosine phosphorylation in mitochondria: A new frontier in mitochondrial signaling. Free Radic Biol Med 38: 1267-1277, 2005
149. Salvi M, Stringaro A, Brunati AM, Agostinelli E, Arancia G, Clari G, and Toninello A. Tyrosine phosphatase activity in mitochondria: Presence of Shp-2 phosphatase in mitochondria. Cell Mol Life Sci 61: 2393-2404, 2004
150. Sarsour EH, Kalen AL, Xiao Z, Veenstra TD, Chaudhuri L, Venkataraman S, Reigan P, Buettner GR, and Goswami PC. Manganese Superoxide Dismutase Regulates a Metabolic Switch during the Mammalian Cell Cycle. Cancer Res 72: 3807-3816, 2012
151. Schatz G. Mitochondria: Beyond oxidative phosphorylation. Biochim Biophys Acta 1271: 123-126, 1995
152. Schatz G. The protein import system of mitochondria. J Biol Chem 271: 31763-31766, 1996
153. Scheffler IE. Mitochondria. In: Mitochondria. New York: John Wiley & Sons, Inc., 2002, pp. 345-351
154. Schwoch G, Trinczek B, and Bode C. Localization of catalytic and regulatory subunits of cyclic AMP-dependent protein kinases in mitochondria from various rat tissues. Biochem J 270: 181-188, 1990
155. Seo MS, Kang SW, Kim K, Baines IC, Lee TH, and Rhee SG. Identification of a new type of mammalian peroxiredoxin that forms an intramolecular disulfide as a reaction intermediate. J Biol Chem 275: 20346-20354, 2000
156. Shadley JD and Wolff S. Very low doses of X-rays can cause human lymphocytes to become less susceptible to ionizing radiation. Mutagenesis 2: 95-96, 1987
157. Shi T, Wang F, Stieren E, and Tong Q. SIRT3, a mitochondrial sirtuin deacetylase, regulates mitochondrial function and thermogenesis in brown adipocytes. J Biol Chem 280: 13560-13567, 2005
158. Shimoda-Matsubayashi S, Matsumine H, Kobayashi T, Nakagawa-Hattori Y, Shimizu Y, and Mizuno Y. Structural dimorphism in the mitochondrial targeting sequence in the human manganese superoxide dismutase gene. A predictive evidence for conformational change to influence mitochondrial transport and a study of allelic association in Parkinson's disease. Biochem Biophys Res Commun 226: 561-565, 1996
159. Slot JW, Geuze HJ, Freeman BA, and Crapo JD. Intracellular localization of the copper-zinc and manganese superoxide dismutases in rat liver parenchymal cells. Lab Invest 55: 363-371, 1986
160. Spitz DR and Sullivan SJ. The generation of stable oxidative stress-resistant phenotypes in Chinese hamster fibroblasts chronically exposed to hydrogen peroxide or hyperoxia. Methods Mol Biol 610: 183-199, 2010
161. St Clair DK, Wan XS, Oberley TD, Muse KE, and St Clair WH. Suppression of radiation-induced neoplastic transformation by overexpression of mitochondrial superoxide dismutase. Mol Carcinog 6: 238-242, 1992
162. Stojanovic S, Stanic D, Nikolic M, Raicevic S, Spasic M, and Niketic V. Manganese superoxide dismutase (MnSOD) catalyzes NO-dependent tyrosine residue nitration. J Serb Chem Soc 70: 601-608, 2005
163. Stroupe ME, DiDonato M, and Tainer JA. Manganese superoxide dismutase. In: Handbook of Metalloproteins, edited by Messerschmidt A, Huber R, Poulas T, and Wieghardt K. Chichester, UK: John Wiley & Sons, Ltd., 2006
164. Sui D and Wilson JE. Structural determinants for the intracellular localization of the isozymes of mammalian hexokinase: Intracellular localization of fusion constructs incorporating structural elements from the hexokinase isozymes and the green fluorescent protein. Arch Biochem Biophys 345: 111-125, 1997
165. Sutton A, Imbert A, Igoudjil A, Descatoire V, Cazanave S, Pessayre D, and Degoul F. The manganese superoxide dismutase Ala16Val dimorphism modulates both mitochondrial import and mRNA stability. Pharmacogenet Genomics 15: 311-319, 2005
166. Sutton A, Khoury H, Prip-Buus C, Cepanec C, Pessayre D, and Degoul F. The Ala16Val genetic dimorphism modulates the import of human manganese superoxide dismutase into rat liver mitochondria. Pharmacogenetics 13: 145-157, 2003
167. Takada Y, Hachiya M, Park SH, Osawa Y, Ozawa T, and Akashi M. Role of reactive oxygen species in cells overexpressing manganese superoxide dismutase: Mechanism for induction of radioresistance. Mol Cancer Res 1: 137-146, 2002
168. Tao R, Coleman MC, Pennington JD, Ozden O, Park SH, Jiang H, Kim HS, Flynn CR, Hill S, Hayes McDonald W, Olivier AK, Spitz DR, and Gius D. Sirt3-mediated deacetylation of evolutionarily conserved lysine 122 regulates MnSOD activity in response to stress. Mol Cell 40: 893-904, 2010
169. Tsan MF. Superoxide dismutase and pulmonary oxygen toxicity: Lessons from transgenic and knockout mice (Review). Int J Mol Med 7: 13-19, 2001
170. Ubersax JA, Woodbury EL, Quang PN, Paraz M, Blethrow JD, Shah K, Shokat KM, and Morgan DO. Targets of the cyclin-dependent kinase Cdk1. Nature 425: 859-864, 2003
171. 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, and Richardson A. 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, 2003
172. Verma IM, Stevenson JK, Schwarz EM, Van Antwerp D, and Miyamoto S. Rel/NF-kappa B/I kappa B family: Intimate tales of association and dissociation. Genes Dev 9: 2723-2735, 1995
173. Voisin S, Watson DC, Tessier L, Ding W, Foote S, Bhatia S, Kelly JF, and Young NM. The cytoplasmic phosphoproteome of the Gram-negative bacterium Campylobacter jejuni: Evidence for modification by unidentified protein kinases. Proteomics 7: 4338-4348, 2007
174. Wan XS, Devalaraja MN, and St Clair DK. Molecular structure and organization of the human manganese superoxide dismutase gene. DNA Cell Biol 13: 1127-1136, 1994
175. Wang F, Liu J, Robbins D, Morris K, Sit A, Liu YY, and Zhao Y. Mutant p53 exhibits trivial effects on mitochondrial functions which can be reactivated by ellipticine in lymphoma cells. Apoptosis 16: 301-310, 2011
176. Wang HG, Rapp UR, and Reed JC. Bcl-2 targets the protein kinase Raf-1 to mitochondria. Cell 87: 629-638, 1996
177. Wang X, Martindale JL, Liu Y, and Holbrook NJ. The cellular response to oxidative stress: Influences of mitogenactivated protein kinase signalling pathways on cell survival. Biochem J 333 (Pt 2): 291-300, 1998
178. Waris G and Ahsan H. Reactive oxygen species: Role in the development of cancer and various chronic conditions. J Carcinog 5: 14, 2006
179. Weisiger RA and Fridovich I. Mitochondrial superoxide simutase. Site of synthesis and intramitochondrial localization. J Biol Chem 248: 4793-4796, 1973
180. Wiedemann N, Frazier AE, and Pfanner N. The protein import machinery of mitochondria. J Biol Chem 279: 14473-14476, 2004
181. Wilcox KC, Zhou L, Jordon JK, Huang Y, Yu Y, Redler RL, Chen X, Caplow M, and Dokholyan NV. Modifications of superoxide dismutase (SOD1) in human erythrocytes: A possible role in amyotrophic lateral sclerosis. J Biol Chem 284: 13940-13947, 2009
182. Williams MD, Van Remmen H, Conrad CC, Huang TT, Epstein CJ, and Richardson A. Increased oxidative damage is correlated to altered mitochondrial function in heterozygous manganese superoxide dismutase knockout mice. J Biol Chem 273: 28510-28515, 1998
183. Wispe JR, Clark JC, Burhans MS, Kropp KE, Korfhagen TR, and Whitsett JA. Synthesis and processing of the precursor for human mangano-superoxide dismutase. Biochim Biophys Acta 994: 30-36, 1989
184. Wong GH. Protective roles of cytokines against radiation: Induction of mitochondrial MnSOD. Biochim Biophys Acta 1271: 205-209, 1995
185. Wright G and Reichenbecher V. The effects of superoxide and the peripheral benzodiazepine receptor ligands on the mitochondrial processing of manganese-dependent superoxide dismutase. Exp Cell Res 246: 443-450, 1999
186. Wright G, Reichenbecher V, Green T, Wright GL, and Wang S. Paraquat inhibits the processing of human manganese-dependent superoxide dismutase by SF-9 insect cell mitochondria. Exp Cell Res 234: 78-84, 1997
187. Wright G, Terada K, Yano M, Sergeev I, and Mori M. Oxidative stress inhibits the mitochondrial import of preproteins and leads to their degradation. Exp Cell Res 263: 107-117, 2001
188. Wynn RM, Kato M, Machius M, Chuang JL, Li J, Tomchick DR, and Chuang DT. Molecular mechanism for regulation of the human mitochondrial branched-chain alpha-ketoacid dehydrogenase complex by phosphorylation. Structure 12: 2185-2196, 2004
189. Xu S, Ying J, Jiang B, Guo W, Adachi T, Sharov V, Lazar H, Menzoian J, Knyushko TV, Bigelow D, Schoneich C, and Cohen RA. Detection of sequence-specific tyrosine nitration of manganese SOD and SERCA in cardiovascular disease and aging. Am J Physiol Heart Circ Physiol 290: H2220-H2227, 2006
190. Xu Y, Kiningham KK, Devalaraja MN, Yeh CC, Majima H, Kasarskis EJ, and St Clair DK. An intronic NF-kappaB element is essential for induction of the human manganese superoxide dismutase gene by tumor necrosis factoralpha and interleukin-1beta. DNA Cell Biol 18: 709-722, 1999
191. Yamakura F, Kobayashi K, Furukawa S, and Suzuki Y. In vitro preparation of iron-substituted human manganese superoxide dismutase: Possible toxic properties for mitochondria. Free Radic Biol Med 43: 423-430, 2007
192. Yang M, Cobine PA, Molik S, Naranuntarat A, Lill R, Winge DR, and Culotta VC. The effects of mitochondrial iron homeostasis on cofactor specificity of superoxide dismutase 2. EMBO J 25: 1775-1783, 2006
193. Young JC, Hoogenraad NJ, and Hartl FU. Molecular chaperones Hsp90 and Hsp70 deliver preproteins to the mitochondrial import receptor Tom70. Cell 112: 41-50, 2003
194. Zacchi P, Gostissa M, Uchida T, Salvagno C, Avolio F, Volinia S, Ronai Z, Blandino G, Schneider C, and Del Sal G. The prolyl isomerase Pin1 reveals a mechanism to control p53 functions after genotoxic insults. Nature 419: 853-857, 2002
195. Zhao Y, Chaiswing L, Velez JM, Batinic-Haberle I, Colburn NH, Oberley TD, and St Clair DK. p53 translocation to mitochondria precedes its nuclear translocation and targets mitochondrial oxidative defense protein-manganese superoxide dismutase. Cancer Res 65: 3745-3750, 2005
196. Zorov DB, Filburn CR, Klotz LO, Zweier JL, and Sollott SJ. Reactive oxygen species (ROS)-induced ROS release: A new phenomenon accompanying induction of the mitochondrial permeability transition in cardiac myocytes. J Exp Med 192: 1001-1014, 2000