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Science 11 November 1988:
Vol. 242. no. 4880, pp. 941 - 944
DOI: 10.1126/science.3263703
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Articles

Science, Vol 242, Issue 4880, 941-944
Copyright © 1988 by American Association for the Advancement of Science

articles

Induction of manganous superoxide dismutase by tumor necrosis factor: possible protective mechanism

GH Wong and DV Goeddel

Department of Molecular Biology, Genentech, San Francisco, CA 94080.

Manganous superoxide dismutase (MnSOD) scavenges potentially toxic superoxide radicals produced in the mitochondria. Tumor necrosis factor-alpha (TNF-alpha) was found to induce the messenger RNA for MnSOD, but not the mRNAs for other antioxidant or mitochondrial enzymes tested. The increase in MnSOD mRNA occurred rapidly and was blocked by actinomycin D, but not by cycloheximide. Induction of MnSOD mRNA was also observed with TNF-beta, interleukin-1 alpha (IL-1 alpha), and IL-1 beta but not with other cytokines or agents tested. TNF-alpha induced MnSOD mRNA in all cell lines and normal cells examined in vitro and in various organs of mice in vivo. These effects of TNF-alpha and IL-1 on target cells may contribute to their reported protective activity against radiation as well as their ability to induce resistance to cell killing induced by the combination of TNF-alpha and cycloheximide.


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Superoxide Dismutases in Gastric and Esophageal Cancer and the Prognostic Impact in Gastric Cancer.
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Increased Tumor Necrosis Factor-{{alpha}} Sensitivity of MCF-7 Cells Transfected with NAD(P)H:Quinone Reductase.
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Adenosine A1 Receptor Activation Induces Delayed Preconditioning in Rats Mediated by Manganese Superoxide Dismutase.
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Immunolocalization and Adenoviral Vector-mediated Manganese Superoxide Dismutase Gene Transfer to Experimental Oral Tumors.
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Journal of Dental Research 79, 1410-1417
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Interleukin-6-Induced Protection in Hyperoxic Acute Lung Injury.
N. S. Ward, A. B. Waxman, R. J. Homer, L. L. Mantell, O. Einarsson, Y. Du, and J. A. Elias (2000)
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Antioxidant defense mechanisms of human mesothelioma and lung adenocarcinoma cells.
K. Jarvinen, P. Pietarinen-Runtti, K. Linnainmaa, K. O. Raivio, C. M. Krejsa, T. Kavanagh, and V. L. Kinnula (2000)
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Specificity of endogenous fatty acid release during tumor necrosis factor-induced apoptosis in WEHI 164 fibrosarcoma cells.
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I. Rahman and W. MacNee (1999)
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E. S. Berleth, S. Nadadur, A. D. Henn, C. Eppolito, S. Shiojiri, H. L. Gurtoo, M. J. Ehrke, and E. Mihich (1999)
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Y. Liu, V. Tergaonkar, S. Krishna, and E. J. Androphy (1999)
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Y. HONDA and S. HONDA (1999)
FASEB J 13, 1385-1393
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T. Ohman, G. Parish, and R. M. Jackson (1999)
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Mitochondrial disease in mouse results in increased oxidative stress.
L. A. Esposito, S. Melov, A. Panov, B. A. Cottrell, and D. C. Wallace (1999)
PNAS 96, 4820-4825
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Modulation of tumor necrosis factor-{alpha}-mediated cytotoxicity by changes of the cellular methylation state: mechanism and in vivo relevance.
F. Ratter, C. Gaßner, V. Shatrov, and V. Lehmann (1999)
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Molecular Mechanism of the Regulation of Glutathione Synthesis by Tumor Necrosis Factor-alpha and Dexamethasone in Human Alveolar Epithelial Cells.
I. Rahman, F. Antonicelli, and W. MacNee (1999)
J. Biol. Chem. 274, 5088-5096
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In Vivo Architecture of the Manganese Superoxide Dismutase Promoter.
S. Kuo, S. E. Chesrown, J. K. Mellott, R. J. Rogers, J.-L. Hsu, and H. S. Nick (1999)
J. Biol. Chem. 274, 3345-3354
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Antioxidant Function of the Mitochondrial Protein SP-22 in the Cardiovascular System.
M. Araki, H. Nanri, K. Ejima, Y. Murasato, T. Fujiwara, Y. Nakashima, and M. Ikeda (1999)
J. Biol. Chem. 274, 2271-2278
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Protein Kinase Cdelta -dependent Induction of Manganese Superoxide Dismutase Gene Expression by Microtubule-active Anticancer Drugs.
K. C. Das, X.-l. Guo, and C. W. White (1998)
J. Biol. Chem. 273, 34639-34645
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Expression and Developmental Profile of Antioxidant Enzymes in Human Lung and Liver.
T. M. Asikainen, K. O. Raivio, M. Saksela, and V. L. Kinnula (1998)
Am. J. Respir. Cell Mol. Biol. 19, 942-949
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M. Ameyar, A. Atfi, Z. Cai, R. Stancou, V. Shatrov, A. Bettaieb, and S. Chouaib (1998)
J. Biol. Chem. 273, 29002-29008
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Induction of Mn SOD in human monocytes without inflammatory cytokine production by a mutant endotoxin.
L. Tian, J. E. White, H.-Y. Lin, V. S. Haran, J. Sacco, G. Chikkappa, F. B. Davis, P. J. Davis, and M.-F. Tsan (1998)
Am J Physiol Cell Physiol 275, C740-C747
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Antioxidant Enzyme Regulation and Resistance to Oxidants of Human Bronchial Epithelial Cells Cultured under Hyperoxic Conditions.
P. Pietarinen-Runtti, K. O. Raivio, M. Saksela, T. M. Asikainen, and V. L. Kinnula (1998)
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E. LAKARI, P. PAAKKO, and V. L. KINNULA (1998)
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Differential Regulation of Copper-Zinc Superoxide Dismutase and Manganese Superoxide Dismutase in the Rat Corpus Luteum: Induction of Manganese Superoxide Dismutase Messenger Ribonucleic Acid by Inflammatory Cytokines.
N. Sugino, C. M. Telleria, and G. Gibori (1998)
Biol Reprod 59, 208-215
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Trypanosoma cruzi Infection in Tumor Necrosis Factor Receptor p55-Deficient Mice.
E. Castanos-Velez, S. Maerlan, L. M. Osorio, F. Aberg, P. Biberfeld, A. Orn, and M. E. Rottenberg (1998)
Infect. Immun. 66, 2960-2968
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Overexpression of Manganese Superoxide Dismutase Suppresses Tumor Necrosis Factor-induced Apoptosis and Activation of Nuclear Transcription Factor-kappa B and Activated Protein-1.
S. K. Manna, H. J. Zhang, T. Yan, L. W. Oberley, and B. B. Aggarwal (1998)
J. Biol. Chem. 273, 13245-13254
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Early Activation of c-Jun N-terminal Kinase and p38 Kinase Regulate Cell Survival in Response to Tumor Necrosis Factor alpha.
A. Roulston, C. Reinhard, P. Amiri, and L. T. Williams (1998)
J. Biol. Chem. 273, 10232-10239
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Tumor Necrosis Factor-{alpha} Confers Resistance to Hypoxic Injury in the Adult Mammalian Cardiac Myocyte.
M. Nakano, A. A. Knowlton, Z. Dibbs, and D. L. Mann (1998)
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Prevention of Mitochondrial Injury by Manganese Superoxide Dismutase Reveals a Primary Mechanism for Alkaline-induced Cell Death.
H. J. Majima, T. D. Oberley, K. Furukawa, M. P. Mattson, H.-C. Yen, L. I. Szweda, and D. K. St. Clair (1998)
J. Biol. Chem. 273, 8217-8224
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Manganese Superoxide Dismutase in Healthy Human Pleural Mesothelium and in Malignant Pleural Mesothelioma.
K. Kahlos, S. Anttila, T. Asikainen, K. Kinnula, K. O. Raivio, K. Mattson, K. Linnainmaa, and V. L. Kinnula (1998)
Am. J. Respir. Cell Mol. Biol. 18, 570-580
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Apoptosis caused by oxidized LDL is manganese superoxide dismutase and p53 dependent.
R. Kinscherf, R. Claus, M. Wagner, C. Gehrke, H. Kamencic, D. Hou, O. Nauen, W. Schmiedt, G. Kovacs, J. Pill, et al. (1998)
FASEB J 12, 461-467
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Interaction of an Adenovirus E3 14.7-Kilodalton Protein with a Novel Tumor Necrosis Factor Alpha-Inducible Cellular Protein Containing Leucine Zipper Domains.
Y. Li, J. Kang, and M. S. Horwitz (1998)
Mol. Cell. Biol. 18, 1601-1610
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Mitochondrial Manganese Superoxide Dismutase Prevents Neural Apoptosis and Reduces Ischemic Brain Injury: Suppression of Peroxynitrite Production, Lipid Peroxidation, and Mitochondrial Dysfunction.
J. N. Keller, M. S. Kindy, F. W. Holtsberg, D. K. St. Clair, H.-C. Yen, A. Germeyer, S. M. Steiner, A. J. Bruce-Keller, J. B. Hutchins, and M. P. Mattson (1998)
J. Neurosci. 18, 687-697
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Role of oxidants in influenza virus-induced gene expression.
K. Knobil, A. M. K. Choi, G. W. Weigand, and D. B. Jacoby (1998)
Am J Physiol Lung Cell Mol Physiol 274, L134-L142
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Elevation of Manganese Superoxide Dismutase Gene Expression by Thioredoxin.
K. C. Das, Y. Lewis-Molock, and C. W. White (1997)
Am. J. Respir. Cell Mol. Biol. 17, 713-726
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Tumor Necrosis Factor Increases Hepatocellular Glutathione by Transcriptional Regulation of the Heavy Subunit Chain of gamma -Glutamylcysteine Synthetase.
A. Morales, C. Garcia-Ruiz, M. Miranda, M. Mari, A. Colell, E. Ardite, and J. C. Fernandez-Checa (1997)
J. Biol. Chem. 272, 30371-30379
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Cloning, Expression, and Characterization of Two Manganese Superoxide Dismutases from Caenorhabditis elegans.
T. Hunter, W. H. Bannister, and G. J. Hunter (1997)
J. Biol. Chem. 272, 28652-28659
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Mouse Extracellular Superoxide Dismutase: Primary Structure, Tissue-specific Gene Expression, Chromosomal Localization, and Lung In Situ Hybridization.
R. J. Folz, J. Guan, M. F. Seldin, T. D. Oury, J. J. Enghild, and J. D. Crapo (1997)
Am. J. Respir. Cell Mol. Biol. 17, 393-403
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Late preconditioning against stunning is not mediated by increased antioxidant defenses in conscious pigs.
X.-L. Tang, Y. Qiu, J. F. Turrens, J.-Z. Sun, and R. Bolli (1997)
Am J Physiol Heart Circ Physiol 273, H1651-H1657
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