Overexpression of manganese-containing superoxide dismutase confers resistance to the cytotoxicity of tumor necrosis factor α and/or hyperthermia

Cancer Research

Volumn 57, Issue 10, 1997, Pages 1991-1998

  Li, Jian Jian ^a,b   Oberley, Larry W ^a  

^a UNIVERSITY OF IOWA   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SUPEROXIDE DISMUTASE; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; BREAST CANCER; CANCER CELL; CANCER RESISTANCE; CELL SURVIVAL; CONTROLLED STUDY; CYTOTOXICITY; DRUG SENSITIVITY; FEMALE; HUMAN; HUMAN CELL; HYPERTHERMIA; OXIDATIVE STRESS; PRIORITY JOURNAL; TUMOR NECROSIS;

BREAST NEOPLASMS; COMBINED MODALITY THERAPY; DNA, COMPLEMENTARY; DRUG RESISTANCE, NEOPLASM; HUMANS; HYPERTHERMIA, INDUCED; PYRUVATES; RNA, MESSENGER; SUPEROXIDE DISMUTASE; TRANSFECTION; TUMOR CELLS, CULTURED; TUMOR NECROSIS FACTOR-ALPHA;

EID: 0030968919     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (63)

1. McCord, J. M., Keele, B. B., and Fridovich, I. An enzyme bused theory of obligate anaerobiosis: the physiological function of superoxide dismutase. Proc. Natl. Acad. Sci. USA, 68: 1024-1027, 1971.
2. Watanabe, N., Niitsu, Y., Umeno, H., Sone, H., Nedam, H., Yamauchi, N., Maeda, M., and Urushizaki, I. Synergistic cytotoxic and antitumor effects of recombinant tumor necrosis factor and hyperthermia. Cancer Res., 48: 650-653, 1988.
3. Sugarman, B. J., Aggarwal, B. B., Hass, P. E., Figari, I. S., Palladino, M. A., and Shepard, H. M. Recombinant human tumor necrosis factor-α: effects on proliferation of normal and transformed cells in vitro. Science (Washington DC), 230: 943-945, 1985.
4. Beutler, B. Tumor Necrosis Factors: The Molecules and Their Emerging Role in Medicine. New York: Raven Press, 1992.
5. Yamauchi, N., Kuriyama, H., Watanabe, N., Neda, H., Maeda, M., and Niitsu, Y. Intracellular hydroxyl radical production induced by recombinant human tumor necrosis factor and its implication in the killing of tumor cells in vitro. Cancer Res., 49: 1671-1675, 1989.
6. Zimmerman, R. J., Chan, A., and Leadon S. A. Oxidative damage in murine tumor cells treated in vitro by recombinant tumor necrosis factor. Cancer Res., 49: 1644-1648, 1989.
7. Yamauchi, N., Kuriyama, Y. H., Watanabe, N., Neda, H., Maeda, M., Himeno, T., and Tsuji, Y. Suppressive effects of intracellular glutathione on hydroxyl radical production induced by tumor necrosis factor. Int. J. Cancer, 46: 884-888, 1990.
8. Schulze-Osthoff, K., Bakker, A. C., Vanhasebroeck, B., Beyaert, R., Jacob, W. A., and Fiers, W. Cytotoxic activity of tumor necrosis factor is mediated by early damage of mitochondrial functions. Evidence for the involvement of mitochondrial radical generation. J. Biol. Chem., 267: 5317-5323, 1992.
9. Schmid, D. S., Hornung, R., McGrath, K. M., Paul, N., and Ruddle, N. H. Target cell DNA fragmentation is mediated by lymphotoxin and tumor necrosis factor. Lymphokine Res., 6: 196-202, 1987.
10. Schulze-Osthoff, K., Beyaert, R., Vandevoorde, V., Haegerman, G., and Feirs, W. Depletion of the mitochondrial electron transport abrogates the cytotoxic and geneinducible effects of TNF. EMBO J., 12: 3095-3104, 1993.
11. Satomi, N., Sakurai, A., Haranaka, R., and Haranaka, K. Preventive effects of several chemicals against lethality of recombinant human tumor necrosis factor. J. Biol. Response Modif., 7: 54-63, 1988.
12. Matthews, N., Neale, M. L., Jackson, S. K., and Stark, J. M. Tumor cell killing by tumor necrosis factor: inhibition by anaerobic conditions, free-radical scavengers and inhibitors of arachidonate metabolism. Immunology. 62: 153-155, 1987.
13. Oberley, L. W., and Buettner, G. R. Role of superoxide dismutase in cancer: a review. Cancer Res., 39: 1141-1149, 1979.
14. Oberley, L. W., and Oberley, T. D. Role of antioxidant enzymes in cell immortalization and transformation. Mol. Cell. Biochem., 84: 147-153, 1988.
15. Oberley, E. W., McCormick M. L., Sierra-Rivera, E., and St. Clair, D. K. Manganese superoxide dismutase in normal and transformed human embryonic lung fibroblasts. Free Radical Biol. & Med., 6: 379-384, 1989.
16. Wong, G. H. W., Elwell, J. H., Oberley, E. W., and Goeddel, D. V. Manganous superoxide dismutase is essential for cellular resistance to cytotoxicity of tumor necrosis factor. Cell, 58: 923-931, 1989.
17. Ropp, M., Courgeon, A. M., Calvayrac R., and Best-Belpomme, M. The possible role of the superoxide ion in the induction of heat-shock and specific proteins in aerobic Drosophila cells during return to normoxia after a period of anaerobiosis. Can J. Biochem. Cell Biol. 61: 456-461, 1983.
18. Lee, P. C., Bochner, B. R., and Ames, B. N. AppppA, heat-shock stress, and cell oxidation. Proc. Natl. Acad. Sci. USA, 80: 7496-7500, 1983.
19. Yoshikawa, T., Kokura, S., Tainaka, K., Itani, K., Oyamada, H., Kaneko, T., Naito, Y., and Kondo, M. The role of active oxygen species and lipid peroxidation in the antitumor effect of hyperthermia. Cancer Res., 53: 2326-2329, 1993.
20. Wong, G. H. W., McHugh, T., Weber, R., and Goeddel, D. V. Tumor necrosis factor α selectively sensitizes human immunodeficiency cells to heat and radiation. Proc. Natl. Acad. Sci. USA, 88: 4372-4376, 1991.
21. Tsuji, Y., Watanabe, N., Okamoto, T., Tsuji, N., Sasaki, H., Akiyama, S., Yamauchi, N., and Niitsu, Y. Endogenous tumor necrosis factor functions as a resistant factor against hyperthermic cytotoxicity. Cancer Res., 52: 6258-6262, 1992.
22. Himeno, T., Watanabe, N., Yamauchi, N., Maeda, M., Tsuji, Y., Okamoto, T., Neda, H., and Niitsu, Y. Expression of endogenous tumor necrosis factor as a protective protein against the cytotoxicity of exogenous tumor necrosis factor. Cancer Res., 50: 4941-4945, 1990.
23. Himeno, T., Watanabe, N., Yamauchi, N., Maeda, M., Okamoto, T., Tsuji, N., Tsuji, Y., Akiyama, S., Sasaki, H., and Niitsu, Y. Induction of synthesis of manganous superoxide dismutase in L-M(pNTnF) cells carrying an inducible TNF gene. Int. J. Cancer, 59: 458-462, 1992.
24. Okamoto, T., Watanabe, N., Yamauchi, N., Tsuji, Y., Tsuji, N., Itoh, Y., Neda, H., and Niitsu, Y. Endogenous tumor necrosis factor exerts its protective function intracellularly against the cytotoxicity of exogenous tumor necrosis factor. Cancer Res., 52: 5278-5281, 1992.
25. Wong, G. H. W., and Goeddel, D. V. Induction of manganous superoxide dismutase by tumor necrosis factor: possible protective mechanism. Science, 242: 941-944, 1988.
26. Dubois, M-F., Ferrieux, C., and Lebon, P. Synergistic cytotoxic effects of recombinant human tumor necrosis factor, interferon, and heat-stress. Cancer Res., 49: 5618-5622, 1989.
27. Iizumi, T., Yazaki T., Waku M., and Soma, G-I. Immunochemotherapy for murine bladder tumor with a new human recombinant tumor necrosis factor (rTNF-S), VP-16 and hyperthermia. J. Urol., 142: 386-389, 1989.
28. Ohno, S., Stredel, F. R., Stephens, L. C., Siddik, Z. H., Makin, M., Klostergaard, J., Tomasovic, S. P., Khokhar, A. R., and Bull, J. M. C. Increased therapeutic efficacy induced by tumor necrosis factor-α combined with platinum complexes and whole-body hyperthermia in rats. Cancer Res., 52: 4096-4101, 1992.
29. Sakaguchi, Y., Makino, M., Kaneko, T., Stephens, L. C., Strebel, F. R., Danhauser. L. L., Jenkins, G. N., and Bull, J. M. C. Therapeutic efficacy of long duration-low temperature whole body hyperthermia when combined with tumor necrosis factor and carboplatin in rats. Cancer Res., 54: 2223-2227, 1994.
30. Yamauchi, N., Watanabe, N., Naeda, M., Okamoto, T., Sasaki, H., Tsuji, N., Tsuji, Y., Umeno, H., Akiyama, S., and Niitsu, N. Mechanism of synergistic cytotoxic effect between tumor necrosis factor and hyperthermia. Jpn. J. Cancer Res., 83: 540-545, 1992.
31. 2-resistant Chinese hamster fibroblast cell lines. Arch. Biochem. Biophys., 279: 249-260, 1990.
32. St. Clair, D. K., Oberley, T. D., and Ho, Y-S. Overproduction of human Mn-superoxide dismutase modulates paraquat-mediated toxicity in mammalian cells. FEBS Lett., 293: 193-202, 1991.
33. r 100,000 human melanoma-associated cell surface glycoprotein. Cancer Res., 50: 1559-1565, 1990.
34. Gunning, P., Leavitt, J., Muscat, G., Ng, S-Y., and Kedes, L. A human β-actin expression vector system directs high-level accumulation of antisense transcripts. Proc. Natl. Acad. Sci. USA, 84: 4831-4835, 1987.
35. Li, J-J., Oberley, L. W., St. Clair, D. K., Ridnour, L. A., and Oberley, T. D. Phenotypic changes induced in human breast cancer cells by overexpression of manganese-containing superoxide dismutase. Oncogene, 10: 1989-2000, 1995.
36. Ho, Y-S., and Crapo, J. D. Isolation and characterization of complementary DNAs encoding human manganese-containing superoxide dismutase. FEBS Lett., 229: 256-260, 1988.
37. Church, S. L., Grant, J. W., Ridnour, L. A., Oberley L. W., Swanson, P. E., Meltzer, P. S., and Trent, J. M. Increased manganese superoxide dismutase expression suppresses the malignant phenotype of human melanoma cells. Proc. Natl. Acad. Sci. USA, 90: 3113-3117, 1993.
38. Tso, J. Y., Sun, X-H., Kao, T-H., Reece, K. S., and Wu, R. Isolation and characterization of rat and human glyceraldehyde-3-phosphate dehydrogenase cDNAs: genomic complexity and molecular evolution of the gene. Nucleic Acids Res., 13: 2485-2502, 1985.
39. Li. J-J., Domann, F., and Oberley, L. W. Determination of endogenous or exogenous human MnSOD mRNA by RT-PCR using plasmid cDNA primers. Biochem. Biophys. Res. Commun., 216: 610-618, 1995.
40. Lowry, O. H., Rosebrough, N. J., Farr, A. L., and Randall, R. J. Protein measurement with the Folin phenol reagent. J. Biol. Chem., 193: 265-275, 1951.
41. Beauchamp, G., and Fridovich, I. Superoxide dismutase: improved assays and assay applicable to polyacrylamide gel. Anal. Biochem., 44: 276-287, 1971.
42. Dewey, W. C. Interaction of heat with radiation and chemotherapy. Cancer Res., 44 (Suppl.): 4714s-4720s, 1984.
43. Li, J-J., and Dewey, W. C. Relationship between thermal tolerance and protein degradation in temperature-sensitive mouse cells. J. Cell. Physiol., 151: 310-317, 1992.
44. Gallemann, D., and Eyer, P. Formation of hydrogen peroxide during precipitation of red cells with perchloric acid. A cautionary note for precise determination of pyruvate. GSH, and NAD(P)H. Anal. Biochem., 191: 347-353, 1990.
45. O'Donnell-Tormey, J., Nathan, C. F., Lanks, K., DeBoer, C. J., and Harpe, J. D. L. Secretion of pyruvate. An antioxidant defense of mammalian cells. J. Exp. Med., 165: 500-514, 1987.
46. Niitsu, Y., Watanabe, N., Umeno, H., Sone, H., Neda, H., Yamauehi, N., Maeda, M., and Urushizaki, I. Synergistic effects of recombinant human tumor necrosis factor and hyperthermia on in vitro cytotoxicity and artificial metastasis. Cancer Res., 48: 654-657, 1988.
47. Smith, D. M., Tran, H. M., Soo, V. W., McQuiston, S. A., Tartaglia, L. A., Goeddel, D. V., and Epstein, L. B. Enhanced synthesis of tumor necrosis factor-induced proteins, plasminogen activator inhibitor-2, manganese superoxide dismutase, and protein 28/5.6 is selectively triggered by the 55-kDa tumor necrosis factor receptor in human melanoma cells. J. Biol. Chem., 269: 9898-9905, 1994.
48. Mitchell, J. B., and Russo, A. Thiols, thiol depletion, and thermosensitivity. Radiat. Res., 95: 471-485, 1983.
49. Freeman, M. L., Spitz, D. R., and Meredith, M. J. Does heat shock enhance oxidative stress? Studies with ferrous and ferric ion. Radiat. Res., 124: 288-293, 1990.
50. Skibba, J. L., Powers, R. H., Stadnicka, A., Cullinane, D. W., Almagro, U. A., and Kalbfleisch, J. H. Oxidative stress as a precursor to the irreversible hepatocellular injury caused by hyperthermia. Int. J. Hyperthermia, 7: 749-761, 1991.
51. Lin, P. S., Quamo, S., Ho, K. C., and Gladding, J. Hyperthermia enhances the cytotoxic effects of reactive oxygen species to Chinese hamster cells and bovine endothelial cells in vitro. Radiat. Res., 126: 43-51, 1991.
52. Fujimoto, S., Konno, C., Kobayashi, K., Kokubun, M., Shrestha, R. D., Kiuchi. S., Takahashi, M., Ohta, M., and Okui, K. Augmented antitumour effects of combined treatment with hyperthermia and tumour necrosis factor on human gastric cancer xenotransplanted into nude mice. Int. J. Hyperthermia, 7: 511-518, 1991.
53. Fujimoto, S., Kobayashi, K., Takahashi, M., Konno, T. C., Kokubun, M., Ohta, M., Shrestha, R. D., and Kiuchi, S. Effects on tumour microcirculation in mice of misonidazole and tumour necrosis factor plus hyperthermia. Br. J. Cancer, 65: 33-36, 1992.
54. Klostergaard, J., Leroux E., Siddik, Z. H., Khodadadian, M., and Tomusovic, S. P. Enhanced sensitivity of human colon tumor cell lines in vitro in response to thermo-chemoimmuno-therapy. Cancer Res., 52: 5271-5277, 1992.
55. Calderwood, S. K., and Hahn, G. M. Thermal sensitivity and resistance of insulin-receptor binding in thermotolerant cells. Biochim. Biophys. Acta, 756: 1-8, 1983.
56. Kull, F. C., Jr., and Cuatrecasas, P. Possible requirement of internalization in the mechanism of in vitro cytotoxicity in tumor necrosis serum. Cancer Res., 41: 4885-4890, 1981.
57. Tomasovic, S. P., Khodadadian, M., Hung, M.-C., and Klostergaard, J. Hyperthermia enhances the cytotoxicity of NIH 3T3 cells transfected with a noncleavable transmembrane pro-tumor necrosis factor deletion mutant. J. Immunother. Emphasis Tumor Immunol., 16: 181-187, 1994.
58. Jäättelä, M., Saksela, K., and Saksela, E. Heat shock protects WEHI-164 target cells from the cytolysis by tumor necrosis factor α and β. Eur. J. Immunol., 19: 1413-1417, 1989.
59. Jäättelä, M., Wissing, D., Bauer, P. A., and Li, G. C. Major heat shock protein hsp70 protects tumor cells from tumor necrosis factor cytotoxicity. EMBO J., 11: 3507-3512, 1992.
60. Mehlen, P., Preville, X., Chareyron, P., Briolay, J., Klemenz, R., and Arrigo, A-P. Constitutive expression of human hsp27, Drosophila hsp27, or human alpha B-crystallin confers resistance to TNF-α and oxidative stress-induced cytotoxicity in stably transfected murine L929 fibroblasts. J. Immunol., 154: 363-374, 1995.
61. Lee, Y. J., Hou, Z., Curetty L., Cho, J. M., and Corry, P. M. Synergistic effects of cytokine and hyperthermia on cytotoxicity in HT-29 cells are not mediated by alteration of induced protein levels. J. Cell. Physiol., 155: 27-35, 1993.
62. Spitz, D. R., Dewey, W. C., and Li, G. C. Hydrogen peroxide or heat shock induces resistance to hydrogen peroxide in Chinese hamster fibroblasts. J. Cell. Physiol., 131: 364-373, 1987.
63. Spitz, D. R., Mackey, M. A., Li, G. C., Elwell, J. H., McCormick, M. L., and Oberley, L. W. The relationship between changes in ploidy and stable cellular resistance to hydrogen peroxide. J. Cell. Physiol., 139: 592-598, 1989.