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In vitro modulation of antioxidant enzymes in normal and malignant renal epithelium

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Summary

The activities of three antioxidant enzymes, superoxide dismutase, catalase, and glutathione peroxidase, were monitored in isolated human renal adenocarcinoma tissues and in cultured human renal adenocarcinoma cells. The results were compared to the activities of these enzymes in the proposed cell of origin, isolated human proximal tubular tissues, and cultured proximal tubular epithelial cells. Strong modulation of these enzymes by culture conditions was observed in normal cells but not in carcinoma cells. Low levels of cellular lipid peroxidation, as assessed by levels of malondialdehyde (MDA), were observed in adenocarcinoma cells under the culture conditions tested with one exception: greatly elevated MDA was observed in renal adenocarcinoma cells growth on plastic in serum-free, chemically defined medium. This increased lipid peroxidation correlated with a loss of cell viability under these conditions.

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References

  1. Allen, R. G.; Newton, R. K.; Sohal, R. S., et al. Alteration in superoxide dismutase, glutathione, and peroxidase in the plasmodial sline moldPhysarum polycephalum during differentiation. J. Cell. Physiol. 124: 413–419; 1985.

    Article  Google Scholar 

  2. Arneson, R. M.; Wander, J. D. Antioxidants in neoplastic cells: II. Isolation and partial characterization of a phenolic antioxidant from differentiated mouse neuroblastoma cells. Lipid 13: 391–398; 1977.

    Article  Google Scholar 

  3. Asayama, K.; Janco, R. L.; Burr, I. M. Selective induction of manganese superoxide dismutase in human monocytes. Am. J. Physiol. 294: C393-C397; 1985.

    Google Scholar 

  4. Aust, S. D.; Lipid peroxidation. In: Greenwald, R. A., ed. Handbook of methods for oxygen radical research. Boca Raton, FL: CRC Press; 1985: 203–207.

    Google Scholar 

  5. Beauchamp, C.; Fridovich, I. Superoxide dismutase: improved assay and an assay applicable to acrylamide gels. Anal. Biochem. 44: 276–287; 1971.

    Article  PubMed  CAS  Google Scholar 

  6. Belts, W. H. Detecting oxygen radicals by chemiluminescence. In: Greenwald, R. A., ed. Handbook of methods for oxygen radical research. Boca Raton, FL: CRC Press; 1985; 197–207.

    Google Scholar 

  7. Benedetti, A.; Malvaldi, G.; Fulceri, R., et al. Loss of lipid peroxidation as a histochemical marker for preneoplastic hepatocellular foci of rats. Cancer Res. 44: 5712–5717; 1984.

    PubMed  CAS  Google Scholar 

  8. Bensinger, R. E.; Johnson, C. M. Luminol assay for superoxide dismutase. Anal. Biochem. 116: 142–145; 1981.

    Article  PubMed  CAS  Google Scholar 

  9. Bishop, C. T.; Mizra, Z.; Crapo, J. D., et al. Free radical damage to cultured porcine aortic endothelial cells and lung fibroblasts: modulation by culture conditions. In Vitro 21: 229–236; 1985.

    CAS  Google Scholar 

  10. Bremner, T. A.; Reid, Y. A.; Harrington, G. Superoxide dismutase and peroxidase are coordinately regulated in differentiated and transformed tissues ofNicotiana tabacum. Differentiation 28: 200–204; 1985.

    Article  PubMed  CAS  Google Scholar 

  11. Cerutti, P. A. Prooxidant states and tumor promotion. Science 227: 375–381; 1985.

    Article  PubMed  CAS  Google Scholar 

  12. Cheeseman, K. H.; Collins, M.; Proudfoot, K., et al. Studies on lipid peroxidation in normal and tumor tissues. The Novikoff rat liver tumour. Biochem. J. 235: 507–514; 1986.

    PubMed  CAS  Google Scholar 

  13. Christman, M. F.; Morgan, R. W.; Jacobson, F. S., et al. Positive control of a regulon for defenses against oxidative stress and some heat-shock proteins inSalmonella typhimurium. Cell 41: 753–762; 1985.

    Article  PubMed  CAS  Google Scholar 

  14. Crivello, J. F. Interaction of bovine renal mitochondria cytochrome P-450 with antioxidants. Arch. Biochem. Biophys. 248: 551–561; 1986.

    Article  PubMed  CAS  Google Scholar 

  15. Dees, J. H.; Healfield, B. M.; Reuber, M. D. Adenocarcinoma of the kidney. III. Histogenesis of renal adenocarcinoma induced in rat byN-(4′ fluoro-4-biphenyl) acetamide. JNCI 64: 1537–1545; 1980.

    PubMed  CAS  Google Scholar 

  16. Del Rio, L. A.; Gomez-Ortega, M.; Lopez, A. L., et al. A more sensitive modification of the catalase assay with the Clark oxygen electrode. Application to the kinetic study of the pea leaf enzyme. Anal. Biochem. 80: 409–415; 1975.

    Google Scholar 

  17. Downs, T. R.; Wilfinger, W. W. Fluorometric quantification of DNA in cells and tissue. Anal. Biochem. 131: 538–547; 1983.

    Article  PubMed  CAS  Google Scholar 

  18. Eker, P.; Mossige, J.; Johannessen, J. V. Hereditary renal adenomas and adenocarcinomas in rats. Diagn. Histopathol. 4: 99–110; 1981.

    PubMed  CAS  Google Scholar 

  19. Fearon, E. R.; Vogelstein, B.; Feinberg, A. P. Somatic deletion and duplication of genes on chromosome 11 in Wilms’ tumor. Nature 309: 176–178; 1984.

    Article  PubMed  CAS  Google Scholar 

  20. Fernandez-Pol, J. A.; Hamilton, P. D.; Klos, D. J. Correlation betwen the loss of the transformed phenotype and an increase in superoxide dismutase activity in a revertant subclone of sarcoma virus-infected mammalian cells. Cancer Res. 42: 609–617; 1982.

    PubMed  CAS  Google Scholar 

  21. Gospodarowicz, D.; Lepine, J.; Massoglia, S., et al. Comparison of the ability of basement membrane produced by corneal endothelial and mouse-derived endodermal PFHR-9 cells to support the proliferation and differentiation of bovine kidney tubular epithelial cells in vitro. J. Cell. Biol. 99: 947–961; 1984.

    Article  PubMed  CAS  Google Scholar 

  22. Graf, J. D.; Ayala, F. J. Genetic variation for superoxide dismutase level inDrosophila melanogaster. Biochem. Genet. 24; 153–168; 1986.

    Article  PubMed  CAS  Google Scholar 

  23. Gunzler, W. A.; Kramers, H.; Flohe, L. An improved coupled test procedure for glutathione peroxidase in blood. Z. Klin. Chem. Klin. Biochem. 12: 444–451; 1974.

    PubMed  CAS  Google Scholar 

  24. Hames, B. D. An introduction to polyacrylamide gel elctrophoresis. In: Hames, B. D.; Rickwood, D. eds. Gel electrophoresis of proteins—A practical approach. Eynsham, Oxford: IRL Press; 1984: 8–41.

    Google Scholar 

  25. Hard, G. C. Identification of a high-frequency model for renal carcinoma by the induction of renal tumors in the mouse with a single dose of streptozotocin. Cancer Res. 45: 703–708; 1985.

    PubMed  CAS  Google Scholar 

  26. Hard, G. C.; Toh, B. H. Immunofluorescent characterization of rat kidney tumors according to the distribution of actin as revealed by specific antiactin antibody. Cancer Res. 37: 1618–1623; 1977.

    PubMed  CAS  Google Scholar 

  27. Iizuka, S.; Taniguchi, N.; Makita, A. Enzyme-liked immunosorbent assy for human manganese-containing superoxide dismutase and its content in lung cancer. JNCI 72: 1043–1049; 1984.

    PubMed  CAS  Google Scholar 

  28. Kaplan, P. L.; Ozanne, B. Transforming growth factors enable transformed and normal cells to grow in serum-free medium. In: Growth of cells in hormonally defined media. Sato, G. H.; Pardee, A. B.; Sirbasku, D. A. eds. New York: Cold Spring Harbor Laboratory Publications; 1982; 333–344.

    Google Scholar 

  29. Lechner, J. F.; McClendon, I. A.; LaVeck, M. A. et al. Differential control by platelet factors of squamous differentiation in normal and malignant human bronchial epithelial cells. Cancer Res. 43: 5915–5921; 1983.

    PubMed  CAS  Google Scholar 

  30. Li, J. J.; Li, S. A.; Klicka, J. K., et al. Relative carcinogenic activity of various synthetic and natural estrogen in the Syrian hamster kidney. Cancer Res. 43: 5200–5204; 1983.

    PubMed  CAS  Google Scholar 

  31. Loven, D. P.; Guernsey, D. L.; Oberley, L. W. Transformation affects superoxide dismutase activity. Int. J. Cancer 33: 783–786; 1984.

    Article  PubMed  CAS  Google Scholar 

  32. Loven, D. P.; Leeper, D. B.; Oberley, L. W.; Superoxide dismutase levels in Chinese hamster ovary cells and ovarian carcinoma cells after hyperthermia or exposure to cycloheximide. Cancer Res. 45: 3029–3033; 1985.

    PubMed  CAS  Google Scholar 

  33. Marklund, S. L.; Westman, N. G.; Lundgren, E., et al. Copper and zinc-containing superoxide dismutase, manganese-containing superoxide dismutase, manganese-containing superoxide dismutase, catalase, and glutathione peroxidase in normal and neoplastic human cell lines and normal human tissues. Cancer Res. 42: 1955–1961; 1982.

    PubMed  CAS  Google Scholar 

  34. Masai, T.; Lechner, J. F.; Yookum, G. H., et al. Growth and differentiation of normal and transformed human bronchial epithelial cells. J. Cell Physiol. Supp. 4: 73–81; 1986.

    Article  Google Scholar 

  35. Mitelman, F.; Levan, G. Clustering of aberrations to specific chromosomes in human neoplasms. IV. A survey of 1,871 cases, Hereditas 95: 79–139; 1981.

    Article  PubMed  CAS  Google Scholar 

  36. Mohandas, J.; Marshall, J. J.; Duggin, G. G., et al. Low activities of glutathione-related enzymes as factors in the genesis of urinary bladder cancer. Cancer Res. 44; 5086–5091; 1984.

    PubMed  CAS  Google Scholar 

  37. Oberley, I. W.; Superoxide dismutase and cancer. In: Oberley, L. W., ed. Superoxide dismutase, vol. II. Boca Raton, FL: CRC Press; 1982; 127–165.

    Google Scholar 

  38. Oberley, L. W.; Oberley, T. D. Free radicals, cancer and aging. In: Johnson, J. E., ed. Free radicals, aging, and degenerative diseases. New York: Alan R. Liss, Inc.; 1986; 325–371.

    Google Scholar 

  39. Oberley, L. W.; Oberley, T. D.; Buettner, G. R. Cell differentiation, aging and cancer: The possible roles of superoxide and superoxide dismutase. Med. Hypotheses 6: 249–268; 1980.

    Article  PubMed  CAS  Google Scholar 

  40. Oberley, T. D.; Yang, A. H.; Gould-Kostka, J. Selection of kidney cell types in primary glomerular explant outgrowths by in vitro culture conditions. J. Cell Sci. 84: 69–92; 1986.

    PubMed  CAS  Google Scholar 

  41. Olshan, A. F.; Wilms’ tumor, overgrowth, and fetal growth factors: a hypothesis. Cancer Genet. Cytogenet. 21: 303–307; 1986.

    Article  PubMed  CAS  Google Scholar 

  42. Parshad, R.; Sanford, K. K.; Jones, G. M., et al. Susceptibility to fluorescent light-induced chromatid breaks associated with DNA repair deficiency and malignant transformation in culture. Cancer Res. 40: 4415–4419; 1980.

    PubMed  CAS  Google Scholar 

  43. Parshad, R.; Gantt, R.; Sanford, K. K. et al. Light-induced chromatid damage in human skin fibroblasts in culture in relation to their neoplastic potenial. Int. J. Cancer 28: 335–340; 1981.

    Article  PubMed  CAS  Google Scholar 

  44. Pathak, S.; Strong, L. C.; Ferrell, R. E., et al. Familial renal cell carcinoma with a 3,11 chromosome translocation limited to tumor cells. Science 217; 939–941; 1982.

    Article  PubMed  CAS  Google Scholar 

  45. Perchellet, J.-P.; Perchellet, E. M.; Orten, D. K., et al. Inhibition of the effects of 12-o-tetradecanoylphorbol-13-acetate on mouse epidermal glutathione peroxidase and ornithine decarboxylase activities by glutathione level-rising agents and selenium-containing compounds. Cancer Lett. 26: 283–293; 1985.

    Article  PubMed  CAS  Google Scholar 

  46. Qutzen, H. C.; Maguire, H. C., The etiology of renal-cell carcinoma. Semin. Oncol. 10: 379–384; 1983.

    Google Scholar 

  47. Ross, D. A.; Jackson, R. C.; Weber, G. et al. Decreased content of reduced and oxidized nicotinamide-adenine dinucleotide phosphate in rat hepatomas. Cancer Biochem. Biophys. 6: 61–64; 1982.

    PubMed  CAS  Google Scholar 

  48. Roswell, D. F.; White, E. H. The chemiluminescence of luminol and related hydrazides. In: DeLuca, M. A. ed. Methods in enzymology, vol. 57, Bioluminescence and chemiluminescence. New York: Academic Press; 1978; 409–423.

    Google Scholar 

  49. Saine, S. E.; Fang, W. F.; Strobel, H. W. Drug metabolism in the Novikoff hepatoma. Evidence for a mixed function oxidase system and partial purification of cytochrome P-450 reductase. Biochim. Biophys. Acta 526: 345–358; 1978.

    PubMed  CAS  Google Scholar 

  50. Sanford, K. K.; Parshad, R.; Gantl, R. Responses of human cells in culture to hydrogen peroxide and ralated free radicals generated by visible light: relationship to cancer susceptibility. In: Johnson, J. E. eds. Free radicals, aging, and degenerative diseases, New York, Alan R. Liss, Inc. 1986; 373–394.

    Google Scholar 

  51. Simon, L. M.; Robin, E. D.; Theodore, J. Difference in oxygen-dependent regulation of enzymes between tumor and normal cell systems in culture. J. Cell Physiol. 108: 393–400; 1981.

    Article  PubMed  CAS  Google Scholar 

  52. Sohal, R. S. Relationship between oxygen metabolism, aging and development. Adv. Free. Radical. Biol. Med. 2: 117–160; 1986.

    CAS  Google Scholar 

  53. Steinert, B. W.; Anderson, P. J.; Oberley, L. W., et al. Kidney glomerular explants in serum-free media: demonstration of intracellular antioxidant enzymes and active oxygen metabolites. In Vitro 22: 285–294; 1986.

    CAS  Google Scholar 

  54. Swann, P. F.; Kaufman, D. G.; Magee, P. N., et al. Induction of kidney tumors by a single dose of dimethylnitrosamine: dose response and influence of diet and benzo[a]pyrene pretreatment. Br. J. Cancer 41: 285–294; 1980.

    PubMed  CAS  Google Scholar 

  55. Thoenes, W.; Storkel, S. T.; Rumpelt, H. J. Histopathology and classification on renal cell tumors (adenomas, oncocytomas and carcinomas). The basic cytological and histopathological elements and their use for diagnostics. Pathol. Res Pract. 181; 125–143; 1986.

    PubMed  CAS  Google Scholar 

  56. Tisdale, M. J.; Malmound, M. B. Activities of free radiacal metabolizing enzymes in tumours. Br. J. Cancer 47; 809–812; 1983.

    PubMed  CAS  Google Scholar 

  57. Tsuda, H.; Sakata, T.; Masui, T. et al. Modifying effects of butylated hydroxyanisole, ethoxyquin and acetaminophen on induction of neoplastic lesions in rat liver and kidney initiated byN-ethyl-N-hydroxyethylnitrosamine. Carcinogenesis 5: 525–531; 1984.

    Article  PubMed  CAS  Google Scholar 

  58. Utsumi, K.; Goto, N.; Kanemasa, Y., et al. Inhibition of mitochondrial lipid peroxidation by an agent in cancer cells. Physiol. Chem. Physics 3: 467–480; 1971.

    CAS  Google Scholar 

  59. Van Der Valk, P.; Gille, J. J. P.; Oostra, A. B., et al. Characterization of an oxygen-tolerant cell line derived from Chinese hamster ovary. Cell Tissue Res. 239: 61–68; 1985.

    Article  PubMed  Google Scholar 

  60. Weekes, U. Y. Metabolism of dimethylnitrosamine to mutagenic intermediates by kidney microsomal enzymes and correlation with reported host susceptibility to kidney tumors. JNCI 55: 1199–1208; 1975.

    PubMed  CAS  Google Scholar 

  61. Yang, A. H.; Gould-Kostka, J.; Oberley, T. D. In vitro growth and differentiation of human kidney tubular cells on a basement membrane substrate. In Vitro 23: 34–46; 1987.

    CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Pathology, University of Wisconsin Medical School, 53706, Madison, Wisconsin

    An Hang Yang & Terry D. Oberley

  2. Laboratory Service, Electron Microscopy Section, William S. Middleton Memorial Veterans Hospital, 2500 Overlook Terrace, 53705, Madison, Wisconsin

    Terry D. Oberley

  3. Radiation Research Laboratory, University of Iowa College of Medicine, 52242, Iowa City, Iowa

    Larry W. Oberley

  4. Department of Human Oncology, University of Wisconsin Medical School, 53706, Madison, Wisconsin

    Steven M. Schmid & Kenneth B. Cummings

  5. Department of Surgery, University of Wisconsin Medical School, 53706, Madison, Wisconsin

    Kenneth B. Cummings

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  1. An Hang Yang
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  2. Terry D. Oberley
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  3. Larry W. Oberley
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  5. Kenneth B. Cummings
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This work was supported by a grant from the Veterans Adminsitration (T. D. O.) and by grant 1 R01 CA 41267 from the National Institutes of Health (L. W. O.), Bethesda, MD.

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Yang, A.H., Oberley, T.D., Oberley, L.W. et al. In vitro modulation of antioxidant enzymes in normal and malignant renal epithelium. In Vitro Cell Dev Biol 23, 546–558 (1987). https://doi.org/10.1007/BF02620972

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