Role of Catalase in Protection of Cancer Cells from Oxidative Stress induced by Binary Catalytic System “Teraphtal + Ascorbic acid”

EXPERIMENTAL STUDIES , , , ,

Т.А. Sidorova1, M.S. Vagida1, O.L. Kaliya2, G.K. Gerasimova1

1 N.N. Blokhin Russian Cancer Research Center of RAMS, Moscow, Russian Federation

2 State Scientific Center NIOPIC, Moscow, Russian Federation

For citation: Sidorova Т.А., Vagida M.S., Kaliya O.L., Gerasimova G.K. Role of Catalase in Protection of Cancer Cells from Oxidative Stress induced by Binary Catalytic System “Teraphtal + Ascorbic acid”. Klin. onkogematol. 2014; 7(3): 282–9. (In Russ.)

ABSTRACT

The efficacy of a novel anti-tumor agent binaric catalitic system “teraphtal + ascorbic acid” [BCS (T+A)], generating reactive oxygen species, may depend on the activity of enzymes of the cellular antioxidant defense system including catalase (CAT). To evaluate the role of CAT in cancer cell defense from oxidative stress induced by BCS (T+A), we studied the following biomarkers: the expression level and basal activity of CAT in cells, and its sensitivity to specific inhibitor, aminotriazole (3-AT). We found that functionally active CAT was expressed constitutively in cultures of human tumor cells of different hystogenesis grown in vitro; at that the basal levels of CAT-protein expression and CAT-enzyme activity depend on cell types. The efficacy of CAT inhibiting by 3-AT (the parameter IC50 3-АТ) is the same for cells of all tested cultures, it ranges from 20 to 25 mM and does not depend on the level of CAT protein expression in cells. No direct correlation was found between the biological CAT characteristics and their sensitivity to BCS (T+A) for cells of different hystogenesis. In case of pharmacological CAT inhibition, the cytotoxic activity of BCS (T+A) is doubled, whereas the human tumor cell sensitization degree (increased sensitivity) to BCS (T+A) depends on their type.

Keywords: human tumor cells, BCS (T+A), oxidative stress, catalase, aminotriazol.

Address correspondence to: tatsid@yahoo.com

Accepted: May 07, 2014

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REFERENCES

  1. Paletta-Silva R., Rocco-Machado N., Meyer-Fernandes J.R. NADPH oxidase biology and the regulation of tyrosine kinase receptor signaling and cancer drug cytotoxicity. Int. J. Mol. Sci. 2013; 14(2): 3683–704.
  2. Ray P.D., Huang B.W., Tsuji Y. Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cell Signal. 2012; 24(5): 981–90.
  3. Peus D., Vasa R.A., Meves A. et al. H2 O2 is an important mediator of UVB-induced EGF-receptor phosphorylation in cultured keratinocytes. J. Invest. Dermatol. 1998; 110(6): 966–71.
  4. Heck D., Vetrano A., Mariano T. et al. UVB light stimulates production of reactive oxygen species. J. Biol. Chem. 2003; 278(25): 22432–6.
  5. Saran M., Bors W. Radiation chemistry of physiological saline reinvestigated: evidence that chloride-derived intermediates play a key role in cytotoxicity. Radiat. Res. 1997; 147(1): 70–7.
  6. Buettner G.R., Need M.J. Hydrogen peroxide and hydroxyl free radical production by hematoporphyrin derivative, ascorbate and light. Cancer Lett. 1985; 25(3): 297–304.
  7. Arrick B.A., Griffo W., Cohn Z., Nathan C. Hydrogen peroxide from cellular metabolism of cystine. A requirement for lysis of murine tumor cells by vernolepin, a glutathione-depleting antineoplastic. J. Clin. Invest. 1985; 76(2): 567–74.
  8. Valko M., Leibfritz D., Moncol J. et al. Free radicals and antioxidants in normal physiological functions and human disease. Int. J. Biochem. Cell Biol. 2007; 39(1): 44–84.
  9. Cadenas E., Davies K.J.A. Mitochondrial free radical generation, oxidative stress, and aging. Free Radic. Biol. Med. 2000; 29: 222–30.
  10. Zhuang S., Yan Y., Daubert R.A. et al. ERK promotes hydrogen peroxideinduced apoptosis through caspase-3 activation and inhibition of Akt in renal epithelial cells. Am. J. Physiol. Renal. Physiol. 2007; 292(1): 440–7.
  11. Choi K., Kim J., Kim G.W., Choi C. Oxidative stress-induced necrotic cell death via mitochondira-dependent burst of reactive oxygen species. Curr. Neurovasc. Res. 2009; 6(4): 213–22.
  12. Marklund S.L., Westman N.G., Lundgren E., Roos G. Copper- and zinc-containing superoxide dismutase, manganese-containing superoxide dismutase, catalase, and glutathione peroxidase in normal and neoplastic human cell lines and normal human tissues. Cancer Res. 1982; 42(5): 1955–61.
  13. Chung-man Ho J., Zheng S., Comhair S.A. et al. Differential expression of manganese superoxide dismutase and catalase in lung cancer. Cancer Res. 2001; 61(23): 8578–85.
  14. Luczak M., Kazmierczak M., Handschuh L. et al. Comparative proteome analysis of acute myeloid leukemia with and without maturation. J. Proteomics 2012; 75(18): 5734–48.
  15. Zhong W., Yan T., Lim R., Oberley L.W. Expression of superoxide dismutases, catalase, and glutathione peroxidase in glioma cells. Free Radic. Biol. Med. 1999; 27: 1334–45.
  16. Smith P.S., Zhao W., Spitz D.R., Robbins M.E. Inhibiting catalase activity sensitizes 36 B10 rat glioma cells to oxidative stress. Free Radic. Biol. Med. 2007; 42(6): 787–97.
  17. Margoliash E., Novogrodsky A. A study of the inhibition of catalase by 3-amino-1:2:4: triazole. Biochem. J. 1958; 68(3): 468–75.
  18. Shevchuk I.N., Chekulayeva L.V., Chekulayev V.A. Active oxygen intermediates in the degradation of hematoporphyrin derivative in tumor cells subjected to photodynamic therapy. J. Photochem. Photobiol. 2008; 93(2): 94–107.
  19. Milton N.G. Inhibition of catalase activity with 3-amino-triazole enhances the cytotoxicity of the Alzheimer’s amyloid-beta peptide. Neurotoxicology 2001; 22(6): 767–74.
  20. Wagner B.A., Evig C.B., Reszka K.J. et al. Doxorubicin increases intracellular hydrogen peroxide in PC3 prostate cancer cells. Arch. Biochem. Biophys. 2005; 440(2): 181–90.
  21. Манзюк Л.В., Бредер В.В., Гершанович Л.М. и др. Результаты I-II фазы клинических испытаний каталитической системы «Терафтал + аскорбиновая кислота». РБЖ 2005; 1(4): 105–7. [Manzjuk L.V., Breder V.V., Gershanovich L.M. et al. Results of I-II phases of clinical trials of the catalytic system ‘teraphtal + ascorbic acid’. RBZh 2005; 1(4): 105–7. (In Russ.)].
  22. Петрова Е.Г., Борисенкова С.А., Калия О.Л. Окисление аскорбиновой кислоты в присутствии фталоцианиновых комплексов металлов и химические аспекты. Сообщение 2. Катализ октакарбоксифталоцианином кобальта. Продукты реакции. Известия АН (Серия химическая). 2004; 10: 2224–7. [Petrova E.G., Borisenkova S.A., Kaliya O.L. Oxidation of ascorbic acid in presence of phthalocyanine complexes of metals and chemical aspects. Report 2. Catalysis of cobalt with octacarboxy phthalocyanine. Reaction products. Izvestiya AN (Chemical series). 2004; 10: 2224–7. (In Russ.)].
  23. Bradford M.M. A rapid and sensitive for the quentitation of microgram quantitites of protein utilizing the principle of protein-dye binding. Analyt. Biochem. 1976; 72: 248–54.
  24. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970; 227(5259): 680–5.
  25. Ardestani A., Yazdanparast R., Nejad A.S. 2-Deoxy-D-ribose-induced oxidative stress causes apoptosis in human monocytic cells: prevention by pyridoxal-5’-phosphate. Toxicol. In Vitro. 2008; 22(4): 968–79. 26. Cole S.P. Rapid chemosensitivity testing of human lung tumor cells using the MTT assay Cancer Chemother. Pharmacol. 1986; 17: 259–63.
  26. Gaspar T., Domok F., Lenti L. et al. Neuroprotective effect of adenoviral catalase gene transfer in cortical neuronal cultures. Brain Res. 2009; 1270: 1–9.
  27. Chilumuri A., Odell M., Milton N. The neuroprotective role of catalase overexpression in SH-SY5Y cells against beta-amyloid and H2 O2 toxicity. Alzheimer’s Dementia. 2013; 9(4 Suppl.): 6.
  28. Bai J., Cederbaum A.I. Catalase protects HepG2 cells from apoptosis induced by DNA-damaging agents agents by accelerating the degradation of p53. J. Biol. Chem. 2003; 278: 4660–7.
  29. Smith P.S., Zhao W., Spitz D.R., Robbins M.E. Inhibititing catalase activity sensitizes 36B10 rat glioma cells to oxidative stress. Free Radic. Biol. Med. 2007; 42: 787–97.
  30. Glorieux C., Dejeans N., Sid B. et al. Catalase overexpression in mammary cancer-cells leads to a less aggressive phenotype and an altered response to chemotherapy. Biochem. Pharmacol. 2011; 82: 1384–90.
  31. Ho J.C., Zheng S., Comhair S.A. Differential expression of manganese superoxide dismutase and catalase in lung cancer. Cancer Res. 2001; 61: 8578–85.
  32. Coursin D.B., Cihla H.P., Sempf J. et al. An immunohistochemical analysis of antioxidant and glutathione S-transferase enzyme levels in normal and neoplastic human lung. Histol. Histopathol. 1996; 11(4): 851–60.
  33. Oshino N., Oshino R., Chance B. The characteristics of the “peroxidatic” reaction of catalase in ethanol oxidation. Biochem. J. 1973; 131(3): 555–63.
  34. Margoliash E., Novogrodsky A. A study of catalase by 3-amino-1:2:4- triazole. Biochem. J. 1958; 68: 468–75.
  35. Margoliash E., Novogrodsky A., Schejter A. Irreversible reaction of 3-amino-1:2:4-triazole and related inhibitors with the protein of catalase. Biochem. J. 1960; 74: 339–48.
  36. Kinnula V.L., Everitt J.I., Mangum J.B. et al. Antioxidant defense mechanisms in cultured pleural mesothelial cells. Am. J. Respir. Cell Mol. Biol. 1992; 7(1): 95–103.
  37. Switala J., Loewen C. Diversity of properties among catalases. Arch. Biochem. Biophys. 2002; 401: 145–54.
  38. Williams R.N., Delamere N.A., Paterson C.A. Inactivation of catalase with 3-amino-1,2,4-triazole: an indirect irreversible mechanism. Biochem. Pharmacol. 1985; 34(18): 3386–9.
  39. Nathan C.F., Arrick B.A., Murray H.W. et al. Tumor cell anti-oxidant defenses. Inhibition of the glutathione redox cycle enhances macrophagemediated cytolysis. J. Exp. Med. 1981; 153(4): 766–82.
  40. Кашкина Л.М., Матвеева В.А., Дьякова Н.А. и др. Приобретение НР-фенотипа и изменение активности каталазы в трансформированных клетках различного происхождения в динамике опухолевой прогрессии in vivo. ДАН 2003; 394: 830–4. [Kashkina L.M., Matveeva V.A., D’yakova N.A. et al. Acquisition of HPphenotype and changes in the activity of catalase in transformed cells of different origin in dynamics of tumor progression in vivo. DAN 2003; 394: 830–4. (In Russ.)].
  41. Deichman G.I., Kashkina L.M., Mizenina O.A. et al. Mechanisms of unusually high antioxidant activity of RSV-SR-transformed cells and of its suppression by activated p21ras. Int. J. Cancer. 1996; 66(6): 747–52.
  42. Szumiel I. L5178Y sublines: a look back from 40 years. Part 1: general characteristics. Int. J. Radiat. Biol. 2005; 81(5): 339–52.
  43. Wang W., Adachi M., Kawamura R. et al. Parthenolide-induced apoptosis in multiple myeloma cells involves reactive oxygen species generation and cell sensitivity depends on catalase activity. Apoptosis 2006; 11(12): 2225–35.
  44. Klingelhoeffer C., Kammerer U., Koospal M. et al. Natural resistance to ascorbic acid induced oxidative stress is mainly mediated by catalase activity in human cancer cells and catalase-silencing sensitizes to oxidative stress. BMC Complem. Alter. Med. 2012; 12: 61.
  45. Bouzyk E., Iwanenko T., Jarocewicz N. et al. Antioxidant defense system in differentially hydrogen peroxide sensitive L5178Y sublines. Free Radic. Biol. Med. 1997; 22(4): 697–704.
  46. Kinnula K., Linnainmaa K., Raivio K.O., Kinnula V.L. Endogenous antioxidant enzymes and glutathione S-transferase in protection of mesothelioma cells against hydrogen peroxide and epirubicin toxicity. Br. J. Cancer. 1998; 77(7): 1097–102.
  47. Hata Y., Kawabe T., Hiraishi H. et al. Antioxidant defenses of cultured colonic epithelial cells against reactive oxygen metabolites. Eur. J. Pharmacol. 1997; 321(1): 113–9.
  48. Hachiya M., Akashi M. Catalase regulates cell growth in HL60 human promyelocytic cells: evidence for growth regulation by H2 O2 . Radiat. Res. 2005; 163(3): 271–82.
  49. Myzak M.C., Carr A.C. Myeloperoxidase-dependent caspase-3 activation and apoptosis in HL-60 cells: protection by the antioxidants ascorbate and (dihydro)lipoic acid. Redox. Rep. 2002; 7(1): 47–53.
  50. Duthie S.J., Grant M.H. The role of reductive and oxidative metabolism in the toxicity of mitoxantrone, adriamycin and menadione in human liver derived Hep G2 hepatoma cells. Br. J. Cancer 1989; 60(4): 566–71.
  51. Heim W.G., Appleman D., Pyfrom H.T. Production of catalase changes in animals with 3-amino-1,2,4-triazole. Science 1955; 122(3172): 693–4. 53. Juul T., Malolepszy A., Dybkaer K. et al. The in vivo toxicity of hydroxyurea depends on its direct target catalase. J. Biol. Chem. 2010; 285(28): 21411–5.