Overexpression of Manganese Superoxide Dismutase Promotes the Survival of Prostate Cancer Cells Exposed to Hyperthermia

References

• Flanagan, S.W., Moseley, EL. and Buettner, G.R. (1998) "Increased flux of free radicals in cells subjected to hyperthermia: detection by electron paramagnetic resonance spin trapping", FEBS Lett. 431, 285–286.
   PubMed Web of Science ®Google Scholar
• Frank, J., Kelleher, D.K., Pompella, A., Thews, 0., Biesalski, H.K. and Vaupel, P. (1998) "Enhancement of oxidative cell injury and antitumor effects of localized 44 degrees C hyperthermia upon combination with respiratory hypermda and xanthine oxidase", Cancer Res. 58, 2693–2698.
   PubMed Web of Science ®Google Scholar
• Hall, D.M., Buettner, G.R., Matthes, R.D. and Gisolfi, C.V. (1994) "Hyperthermia stimulates nitric oxide formation: electron paramagnetic resonance detection of.NO-heme in blood", J. Appl. Physiol. 77, 548–553.
   PubMed Web of Science ®Google Scholar
• Skibba, J.L., Powers, R.H., Stadnicka, A. and Kalbfleisch, J.H. (1990) "Lipid peroxidation caused by hyperthermic perfusion of rat liver", Biochem. Pharmacol. 40, 1411–1414.
   PubMed Web of Science ®Google Scholar
• Lord-Fontaine, S. and Averill-Bates, D.A. (2002) "Heat shock inactivates cellular antioxidant defenses against hydrogen peroxide: protection by glucose", Free Radic. Biol. Med. 32, 752–765.
   PubMed Web of Science ®Google Scholar
• Li, C.C. (1987) "Heat shock proteins: role in thermotolerance, drug resistance, and relationship to DNA topoisomerases", NCI Monogr., 99–103.
   PubMedGoogle Scholar
• Tanguay, R.M. (1983) "Genetic regulation during heat shock and function of heat-shock proteins: a review", Can. J Biochem. Cell Biol. 61, 387–394.
   PubMedGoogle Scholar
• Bardella, L., Cajone, F., Cairo, G., Schiaffonati, L. and Bernelli-Zazzera, A. (1986) "Synthesis of heat-shock proteins and tumor growth", Toxicol. Pathol. 14, 353–356.
   PubMedGoogle Scholar
• Omar, R. and Pappolla, M. (1993) "Oxygen free radicals as inducers of heat shock protein synthesis in cultured human neuroblastoma cells: relevance to neurodegenerative disease", Fur. Arch. Psychiatry Clin. Neurosci. 242, 262–267.
   PubMed Web of Science ®Google Scholar
• Privalle, CT. and Fridovich, I. (1987) "Induction of super-oxide dismutase in Escherichia coli by heat shock", Proc. Natl Acad. Sci. USA 84, 2723–2726.
   PubMed Web of Science ®Google Scholar
• Wallen, ES., Buettner, G.R. and Moseley, PL. (1997) "Oxidants differentially regulate the heat shock response", Int. J. Hyperthermia 13, 517–524.
   PubMed Web of Science ®Google Scholar
• Oberley, LW. and Buettner, G.R. (1979) "Role of superoxide dismutase in cancer: a review", Cancer Res. 39, 1141–1149.
   PubMed Web of Science ®Google Scholar
• Oberley, LW. and Oberley, T.D. (1986) Free radicals cancer and Aging, In: Johnson, J.E., Jr., Walford, R., Harmon, D. and Miguel, J., eds, Free Radicals, Aging, and Degenerative Disease (Alan R. Liss, New York), pp 352–371.
   Google Scholar
• Weydert, C., Roling, B., Liu, J., Hinkhouse, M.M., Ritchie, J.M., Oberley, LW. and Cullen, J.J. (2003) "Suppression of the malignant phenotype in human pancreatic cancer cells by the overexpression of manganese superoxide dismutase", Mol. Cancer Then 2, 361–369.
   PubMed Web of Science ®Google Scholar
• Zhang, H.J., Yan, T., Oberley, T.D. and Oberley, LW. (1999) "Comparison of effects of two polymorphic variants of manganese superoxide dismutase on human breast MCF-7 cancer cell phenotype", Cancer Res. 59, 6276–6283.
   PubMed Web of Science ®Google Scholar
• Zhong, W., Oberley, L.W., Oberley, T.D. and St Clair, D.K. (1997) "Suppression of the malignant phenotype of human glioma cells by overexpression of manganese superoxide dismutase", Oncogene 14, 481–490.
   PubMed Web of Science ®Google Scholar
• Church, S.L., Grant, J.W., Ridnour, L.A., Oberley, L.W., Swanson, P.E., Meltzer, P.S. and Trent, J.M. (1993) "Increased manganese superoxide dismutase expression suppresses the malignant phenotype of human melanoma cells", Proc. Natl Acad. Sci. USA 90, 3113–3117.
   PubMed Web of Science ®Google Scholar
• Li, J.J., Oberley, L.W., St Clair, D.K., Ridnour, L.A. and Oberley, T.D. (1995) "Phenotypic changes induced in human breast cancer cells by overexpression of manganese-contain-ing superoxide dismutase", Oncogene 10, 1989–2000.
   PubMed Web of Science ®Google Scholar
• Yan, T., Oberley, L.W., Zhong, W. and St Clair, D.K. (1996) "Manganese-containing superoxide dismutase over-expression causes phenotypic reversion in SV40-transformed human lung fibroblasts", Cancer Res. 56, 2864–2871.
   PubMed Web of Science ®Google Scholar
• Li, J.J. and Oberley, L.W. (1997) "Overexpression of manganese-containing superoxide dismutase confers resist-ance to the cytotoxicity of tumor necrosis factor alpha and/or hyperthermia", Cancer Res. 57, 1991–1998.
   PubMed Web of Science ®Google Scholar
• Sun, J., Chen, Y, Li, M. and Ge, Z. (1998) "Role of antioxidant enzymes on ionizing radiation resistance", Free Radic. Biol. Med. 24, 586–593.
   PubMed Web of Science ®Google Scholar
• Suresh, A., Tung, E, Moreb, J. and Zucali, J.R. (1994) "Role of manganese superoxide dismutase in radioprotection using gene transfer studies", Cancer Gene Then 1, 85–90.
   PubMed Web of Science ®Google Scholar
• Wong, G.H., Elwell, J.H., Oberley, L.W. and Goeddel, D.V. (1989) "Manganous superoxide dismutase is essential for cellular resistance to cytotmdcity of tumor necrosis factor", Cell 58, 923–931.
   PubMed Web of Science ®Google Scholar
• Lin, P.S., Quamo, S., Ho, K.C. and Gladding, J. (1991) "Hyperthermia enhances the cytotoxic effects of reactive oxygen species to Chinese hamster cells and bovine endothelial cells in vitro", Radiat. Res. 126, 43–51.
   PubMed Web of Science ®Google Scholar
• Kokura, S., Nakagawa, S., Hara, T., Boku, Y, Naito, Y, Yoshida, N. and Yoshikawa, T. (2002) "Enhancement of lipid peroxidation and of the antitumor effect of hyperthermia upon combination with oral eicosapentaenoic acid", Cancer Lett. 185, 139–144.
   PubMed Web of Science ®Google Scholar
• Yoshikawa, T., Kokura, S., Tainaka, K., Itani, K., Oyamada, H., Kaneko, T., Naito, Y. and Kondo, M. (1993) "The role of active oxygen species and lipid permddation in the antitumor effect of hyperthermia", Cancer Res. 53, 2326–2329.
   PubMed Web of Science ®Google Scholar
• Alvarez, S., Valdez, L.B., Zaobornyj, T. and Boveris, A. (2003) "Oxygen dependence of mitochondrial nitric oxide synthase activity", Biochem. Biophys. Res. Commun. 305, 771–775.
   PubMed Web of Science ®Google Scholar
• Salo, D.C., Donovan, C.M. and Davies, K.J. (1991) "HSP70 and other possible heat shock or oxidative stress proteins are induced in skeletal muscle, heart, and liver during exercise", Free Radic. Biol. Med. 11, 239–246.
   PubMed Web of Science ®Google Scholar
• Bradford, M.M. (1976) "A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding", Anal. Biochem. 72,248–254.
   PubMed Web of Science ®Google Scholar
• Panus, P.C., Radi, R., Chumley, P.H., Lillard, R.H. and Freeman, B.A. (1993) "Detection of H202 release from vascular endothelial cells", Free Radic. Biol. Med. 14, 217–223.
   PubMed Web of Science ®Google Scholar
• Gardner, P.R., Nguyen, D.D. and White, C.W. (1994) "Aconitase is a sensitive and critical target of oxygen poisoning in cultured mammalian cells and in rat lungs", Proc. Natl Acad. Sci. USA 91, 12248–12252.
   PubMed Web of Science ®Google Scholar
• Laemmli, U.K. (1970) "Cleavage of structural proteins during the assembly of the head of bacteriophage T4", Nature 227, 680–685.
   PubMed Web of Science ®Google Scholar
• Oberley, T.D., Oberley, L.W., Slattery, A.F., Lauchner, L.J. and Elwell, J.H. (1990) "Immunohistochemical localization of antioxidant enzymes in adult Syrian hamster tissues and during kidney development", Am. J. Pathol. 137, 199–214.
   PubMed Web of Science ®Google Scholar
• Beauchamp, C. and Fridovich, I. (1971) "Superoxide dismutase: improved assays and an assay applicable to acrylamide gels", Anal. Biochem. 44, 276–287.
   PubMed Web of Science ®Google Scholar
• Folch, J., Lees, M. and Sloane Stanley, G.H. (1957) "A simple method for the isolation and purification of total lipids from animal tissues", J. Biol. Chem. 226, 497–509.
   PubMed Web of Science ®Google Scholar
• Qian, S.Y., Wang, H.P., Schafer, F.Q. and Buettner, G.R. (2000) "EPR detection of lipid-derived free radicals from PUFA, LDL, and cell oxidations", Free Radic. Biol. Med. 29, 568–579.
   PubMed Web of Science ®Google Scholar
• Duling, D.R. (1994) "Simulation of multiple isotropic spin-trap EPR spectra", J. Magn. Reson. B 104, 105–110.
   PubMedGoogle Scholar
• Li ASW, Cummings KB, Roethling HP, Buettner GR, Chignell CE (1988) "A spin trapping data base implemented on the IBM PC/AT", J. Mag. Resonance 79: 140–142. NIH. Software database page. Available at: http://epr.niehs.nih.gov/. Accessed January 14, 2004.
   Google Scholar
• Dikalov, S.I. and Mason, R.P. (1999) "Reassignment of organic peroxyl radical adducts", Free Radic. Biol. Med. 27, 864–872.
   PubMedGoogle Scholar
• Dikalov, S.I. and Mason, R.P. (2001) "Spin trapping of polyunsaturated fatty acid-derived peroxyl radicals: reassignment to alkoxyl radical adducts", Free Radic. Biol. Med. 30, 187–197.
   PubMed Web of Science ®Google Scholar
• Kalyanaraman, B., Mottley, C. and Mason, R.P. (1984) "On the use of organic extraction in the spin-trapping technique as applied to biological systems", J. Biochem. Biophys. Methods 9, 27–31.
   PubMedGoogle Scholar
• Schaich, K.M. and Borg, D.C. (1988) "Fenton reactions in lipid phases", Lipids 23, 570–579.
   PubMed Web of Science ®Google Scholar
• Venkataraman, S., Martin, S.M., Schafer, F.Q. and Buettner, G.R. (2000) "Detailed methods for the quantification of nitric oxide in aqueous solutions using either an oxygen monitor or EPR", Free Radic. Biol. Med. 29, 580–585.
   PubMed Web of Science ®Google Scholar
• Wagner, B.A., Buettner, G.R. and Burns, C.P. (1994) "Free radical-mediated lipid permddation in cells: oxidizability is a function of cell lipid bis-allylic hydrogen content", Biochem-istry 33, 4449–4453.
   PubMed Web of Science ®Google Scholar
• Palmeira, C.M., Moreno, A.J., Madeira, V.M. and Wallace, K.B. (1996) "Continuous monitoring of mitochondrial membrane potential in hepatocyte cell suspensions", J. Pharmacol. Toxicol. Methods 35, 35–43.
   PubMed Web of Science ®Google Scholar
• Littell, R.C., Milliken, G.A., Stroup, W.W. and Wolfinger, R.D. (1996) SAS System for Mixed Models (SAS Institute Inc., Cary, NC).
   Google Scholar
• Venkataraman, S., Jiang, X., Weydert, C., Zhang, Y., Zhang, H., Goswami, P.C., Ritchie, J.M., Oberley, L.W. and Buettner, G.R. (2004) "Manganese superoxide dismutase overexpres-sion inhibits the growth of androgen-independent prostate cancer cells", Oncogene (in press).
   Google Scholar
• Buckler, K.J. and Vaughan-Jones, R.D. (1998) "Effects of mitochondrial uncouplers on intracellular calcium, pH and membrane potential in rat carotid body type I cells", J. Physiol. 513(Pt 3), 819–833.
   PubMed Web of Science ®Google Scholar
• Tretter, L. and Adam-Vizi, V. (2000) "Inhibition of Krebs cycle enzymes by hydrogen peroxide: a key role of [alpha]-ketoglutarate dehydrogenase in limiting NADH production under oxidative stress", J. Neurosci. 20, 8972–8979.
   PubMed Web of Science ®Google Scholar
• Fridovich, I. (1997) "Superoxide anion radical (02-.), super-oxide dismutases, and related matters", J. Biol. Chem. 272, 18515–18517.
   PubMed Web of Science ®Google Scholar
• Gardner, P.R. and Fridovich, I. (1991) "Superoxide sensitivity of the Escherichia coli aconitase", J. Biol. Chem. 266, 19328–19333.
   PubMed Web of Science ®Google Scholar
• Liochev, S.L. (1996) "The role of iron-sulfur clusters in in vivo hydroxyl radical production", Free Radic. Res. 25, 369–384.
   PubMed Web of Science ®Google Scholar
• Loschen, G., Azzi, A. and Flohe, L. (1973) "Mitochondrial H202 formation: relationship with energy conservation", FEBS Lett. 33, 84–87.
   PubMed Web of Science ®Google Scholar
• Girotti, A.W. (1985) "Mechanisms of lipid permddation", J. Free Radic. Biol. Med. 1, 87–95.
   PubMedGoogle Scholar
• Wilcox, A.L. and Marnett, L.J. (1993) "Polyunsaturated fatty acid alkoxyl radicals exist as carbon-centered epoxyallylic radicals: a key step in hydroperoxide-amplified lipid permddation", Chem. Res. Toxicol. 6, 413–416.
   PubMed Web of Science ®Google Scholar
• Takahashi, I., Emi, Y., Hasuda, S., Kakeji, Y, Maehara, Y. and Sugimachi, K. (2002) "Clinical application of hyperthermia combined with anticancer drugs for the treatment of solid tumors", Surgery 131, S78–S84.
   Web of Science ®Google Scholar
• Armour, E.P., McEachern, D., Wang, Z., Corry, P.M. and Martinez, A. (1993) "Sensitivity of human cells to mild hyperthermia", Cancer Res. 53, 2740–2744.
   PubMed Web of Science ®Google Scholar
• Jung, K., Seidel, B., Rudolph, B., Lein, M., Cronauer, M.V., Henke, W., Hampel, G., Schnorr, D. and Loening, S.A. (1997) "Antioxidant enzymes in malignant prostate cell lines and in primary cultured prostatic cells", Free Radic. Biol. Med. 23, 127–133.
   PubMed Web of Science ®Google Scholar
• Oberley, T.D., Schultz, J.L., Li, N. and Oberley, L.W. (1995) "Antioxidant enzyme levels as a function of growth state in cell culture", Free Radic. Biol. Med. 19, 53–65.
   PubMed Web of Science ®Google Scholar
• Hoshida, S., Yamashita, N., Otsu, K. and Hon, M. (2002) "The importance of manganese superoxide dismutase in delayed preconditioning: involvement of reactive oxygen species and cytokines", Cardiovasc. Res. 55, 495–505.
   PubMed Web of Science ®Google Scholar
• Oberley, LW., St Clair, D.K., Autor, A.P. and Oberley, T.D. (1987) "Increase in manganese superoxide dismutase activity in the mouse heart after X-irradiation", Arch. Biochem. Biophys. 254, 69–80.
   PubMed Web of Science ®Google Scholar
• Orrenius, S., Burgess, D.H., Hampton, M.B. and Zhivotovsky, B. (1997) "Mitochondria as the focus of apoptosis research", Cell Death Differ. 4, 427–428.
   PubMed Web of Science ®Google Scholar
• Krajcovicova-Kudlackova, M., Paukova, V, Bacekova, M. and Dusinska, M. (2004) "Lipid peroxidation in relation to vitamin C and vitamin E levels", Cent. Fur. J. Public Health 12, 46–48.
   PubMedGoogle Scholar
• Liu, X., Zhao, J. and Zheng, R. (2003) "DNA damage of tumor-associated lymphocytes and total antioxidant capacity in cancerous patients", Mutat. Res. 539, 1–8.
   PubMed Web of Science ®Google Scholar
• Anderstam, B., Vaca, C. and Harms-Ringdahl, M. (1992) "Lipid peroxide levels in a murine adenocarcinoma exposed to hyperthermia: the role of glutathione depletion", Radiat. Res. 132, 296–300.
   PubMed Web of Science ®Google Scholar
• Powers, R.H., Stadnicka, A., Kalbfleish, J.H. and Sldbba, J.L. (1992) "Involvement of xanthine oxidase in oxidative stress and iron release during hyperthermic rat liver perfusion", Cancer Res. 52, 1699–1703.
   PubMed Web of Science ®Google Scholar
• Gardner, P.R. and Fridovich, I. (1992) "Inactivation-reacti-vation of aconitase in Escherichia coli. A sensitive measure of superoxide radical", J. Biol. Chem. 267, 8757–8763.
   PubMed Web of Science ®Google Scholar
• Gardner, P.R., Raineri, I., Epstein, LB. and White, C.W. (1995) "Superoxide radical and iron modulate aconitase activity in mammalian cells", J. Biol. Chem. 270, 13399–13405.
   PubMed Web of Science ®Google Scholar
• Liochev, S.I. and Fridovich, I. (1997) "How does superoxide dismutase protect against tumor necrosis factor: a hypothesis informed by effect of superoxide on 'free' iron", Free Radic. Biol. Med. 23, 668–671.
   PubMed Web of Science ®Google Scholar
• Brehmer, M. and Svensson, I. (2000) "Heat-induced apoptosis in human prostatic stromal cells", BJU Int. 85, 535–541.
   PubMed Web of Science ®Google Scholar
• Rong, Y. and Mack, P. (2000) "Apoptosis induced by hyperthermia in Dunn osteosarcoma cell line in vitro", Int. J. Hyperthermia 16, 19–27.
   PubMed Web of Science ®Google Scholar
• Liu, F.F., Miller, N., Levin, W., Zanke, B., Cooper, B., Henry, M., Sherar, M.D., Pintilie, M., Hunt, J.W. and Hill, R.P. (1996) "The potential role of HSP70 as an indicator of response to radiation and hyperthermia treatments for recurrent breast cancer", Int. J. Hyperthermia 12, 197–208.
   PubMed Web of Science ®Google Scholar
• Duan, H., Zhang, H.J., Yang, J.Q., Oberley, LW., Futscher, B.W. and Domann, F.E. (2003) "MnSOD up-regulates maspin tumor suppressor gene expression in human breast and prostate cancer cells", Antioxid. Redox Signal. 5, 677–688.
   PubMed Web of Science ®Google Scholar
• Epperly, MW., Gretton, J.E., Sikora, CA., Jefferson, M., Bernarding, M., Nie, S. and Greenberger, J.S. (2003) "Mitochondrial localization of superoxide dismutase is required for decreasing radiation-induced cellular damage", Radiat. Res. 160, 568–578.
   PubMed Web of Science ®Google Scholar
• Rodriguez, A.M., Carrico, P.M., Mazurkiewicz, J.E. and Melendez, J.A. (2000) "Mitochondrial or cytosolic catalase reverses the MnSOD-dependent inhibition of proliferation by enhancing respiratory chain activity, net ATP production, and decreasing the steady state levels of H202", Free Radic. Biol. Med. 29, 801–813.
   PubMed Web of Science ®Google Scholar
• Krall, J., Bagley, AC., Mullenbach, G.T., Hallewell, R.A. and Lynch, R.E. (1988) "Superoxide mediates the toxicity of paraquat for cultured mammalian cells", J. Biol. Chem. 263, 1910–1914.
   PubMed Web of Science ®Google Scholar
• Scott, M.D., Meshnick, S.R. and Eaton, J.W. (1989) "Super-oxide dismutase amplifies organismal sensitivity to ionizing radiation", J. Biol. Chem. 264, 2498–2501.
   PubMed Web of Science ®Google Scholar