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Intracellular catalase activity instead of glutathione level dominates the resistance of cells to reactive oxygen species

  • Meng-Xin Zhao
  • Jun-Lin Wen
  • Lu Wang
  • Xiao-Ping WangEmail author
  • Tong-Sheng Chen
Original Paper
  • 12 Downloads

Abstract

Artesunate (ARS) induced significant reactive oxygen species (ROS) generation in HepG2, HeLa, and A549 lines. However, ARS induced ROS-dependent apoptosis in HeLa and A549 cell lines but ROS-independent apoptosis in HepG2 cells. A total of 200 μM hydrogen peroxide (H2O2) significantly induced cytotoxicity in HeLa cells, while H2O2 up to 300 μM did not induce cytotoxicity in HepG2 cells, further demonstrating the strong resistance of HepG2 cells to ROS. HeLa cells had much higher basic total glutathione (T-GSH) level than HepG2 cells, while the ratio of basic reduced glutathione (GSH)/oxidized glutathione (GSSG) in HepG2 cells was nearly twice than that in HeLa and A549 cells. Inhibition of glutathione markedly enhanced H2O2- or ARS-induced cytotoxicity in HeLa and A549 cell lines but modestly enhanced the cytotoxicity of H2O2 and even did not affect the cytotoxicity of ARS in HepG2 cells. Moreover, addition of GSH remarkably prevented H2O2- or ARS-induced cytotoxicity in HeLa and A549 cell lines, further indicating the involvement of GSH in scavenging ROS in the two cell lines. HepG2 cells exhibited higher catalase activity than HeLa cells, and inhibiting catalase activity by using 3-aminotriazole (3-AT, a specific inhibition of catalase) or catalase siRNA remarkably reduced the resistance of HepG2 cells to ROS, demonstrating the key roles of catalase for the strong resistance of HepG2 cells to ROS. Collectively, catalase activity instead of glutathione level dominates the resistance of cells to ROS.

Keywords

Catalase Reactive oxygen species Glutathione Resistance Hydrogen peroxide 

Notes

Funding

This work was supported by the National Natural Science Foundation of China (Grants 61527825, 81572184, and 81471699) and the Natural Science Foundation of Guangdong Province (Grant 2014A030313378).

References

  1. Adeoye O, Olawumi J, Opeyemi A, Christiania O (2017) Review on the role of glutathione on oxidative stress and infertility. Jbra Assist Reprod 22:61–66Google Scholar
  2. Alía M, Ramos S, Mateos R, Bravo L, Goya L (2005) Response of the antioxidant defense system to tert-butyl hydroperoxide and hydrogen peroxide in a human hepatoma cell line (HepG2). J Biochem Toxic 19:119–128CrossRefGoogle Scholar
  3. Al-Qenaei A, Yiakouvaki A, Reelfs O, Santambrogio P, Levi S, Hall ND, Tyrrell RM, Pourzand C (2014) Role of intracellular labile iron, ferritin, and antioxidant defence in resistance of chronically adapted Jurkat T cells to hydrogen peroxide. Free Radic Biol Med 68:87–100CrossRefGoogle Scholar
  4. And JDL, Gallard H (1999) Catalytic decomposition of hydrogen peroxide by Fe(III) in homogeneous aqueous solution: mechanism and kinetic modeling. Environ Sci Technol 33:2726–2732CrossRefGoogle Scholar
  5. Andreoli SP, Mallett C, Mcateer JA, Williams LV (1992) Antioxidant defense mechanisms of endothelial cells and renal tubular epithelial cells in vitro: role of the glutathione redox cycle and catalase. Pediatr Res 32:360–365CrossRefGoogle Scholar
  6. Arrick BA, Nathan CF, Griffith OW, Cohn ZA (1982) Glutathione depletion sensitizes tumor cells to oxidative cytolysis. J Biol Chem 257:1231–1237Google Scholar
  7. Baud O, Greene AE, Li J, Wang H, Volpe JJ (2004) Glutathione peroxidase–catalase cooperativity is required for resistance to hydrogen peroxide by mature rat oligodendrocytes. J Neurosci 24:1531–1540CrossRefGoogle Scholar
  8. Cai X, Shen YL, Zhu Q, Jia PM, Yu Y, Zhou L, Huang Y, Zhang JW, Xiong SM, Chen SJ, Wang ZY, Chen Z, Chen GQ (2000) Arsenic trioxide- induced apoptosis and differentiation are associated respectively with mitochondrial transmembrane potential collapse and retinoic acid signaling pathways in acute promyelocytic leukemia. Leukemia 14:262–270CrossRefGoogle Scholar
  9. Chen T, Chen M, Chen J (2013) Ionizing radiation potentiates dihydroartemisinin- induced apoptosis of A549 cells via a caspase-8-dependent pathway. PLoS One 8:e59827CrossRefGoogle Scholar
  10. Cheng R, Li C, Li C, Wei L, Li L, Zhang Y, Yao Y, Gu X, Cai W, Yang Z, Ma J, Yang X, Gao G (2013) The artemisinin derivative artesunate inhibits corneal neovascularization by inducing ROS-dependent apoptosis in vascular endothelial cells. Invest Ophthalmol Vis Sci 54:3400–3409CrossRefGoogle Scholar
  11. Davison K, Cote S, Mader S, Miller WH (2003) Glutathione depletion overcomes resistance to arsenic trioxide in arsenic-resistant cell lines. Leukemia 17:931–940CrossRefGoogle Scholar
  12. Dejeans N, Glorieux C, Guenin S, Beck R, Sid B, Rousseau R, Bisig B, Delvenne P, Buc Calderon P, Verrax J (2012) Overexpression of GRP94 in breast cancer cells resistant to oxidative stress promotes high levels of cancer cell proliferation and migration: implications for tumor recurrence. Free Radic Biol Med 52:993–1002CrossRefGoogle Scholar
  13. Duthie SJ, Johnson W, Dobson VL (1997) The effect of dietary flavonoids on DNA damage (strand breaks and oxidised pyrimdines) and growth in human cells. Mutat Res 390:141–151CrossRefGoogle Scholar
  14. Fang J, Nakmura H, Iyer AK (2007) Tumor-targeted induction of oxystress for cancer therapy. J Drug Target 15:475–486CrossRefGoogle Scholar
  15. Gao F, Chen J, Ma T, Li H, Wang N, Li Z, Zhang Z, Zhou Y (2014) The glutathione peroxidase gene family in Thellungiella salsuginea: genome-wide identification, classification, and gene and protein expression analysis under stress conditions. Int J Mol Sci 15:3319–3335CrossRefGoogle Scholar
  16. Hou D, Uto T, Tong X, Takeshita T, Tanigawa S, Imamura I, Ose T, Fujii M (2004) Involvement of reactive oxygen species- independent mitochondrial pathway in gossypol-induced apoptosis. Arch Biochem Biophys 428:179–187CrossRefGoogle Scholar
  17. Jafri MS (2014) Mechanisms of myofascial pain. Int Sch Res Notices 156:4S10–4S14Google Scholar
  18. Kalaivani P, Saranya S, Poornima P, Prabhakaran R, Dallemer F, Vijaya PV, Natarajan K (2014) Biological evaluation of new nickel (II) metallates: synthesis, DNA/protein binding and mitochondrial mediated apoptosis in human lung cancer cells (A549) via ROS hypergeneration and depletion of cellular antioxidant pool. Eur J Med Chem 82:584–599CrossRefGoogle Scholar
  19. Kasugai I, Yamada M (1992) High production of catalase in hydrogen peroxide- resistant human leukemia HL-60 cell lines. Leuk Res 16:173–179CrossRefGoogle Scholar
  20. Keizer HG, Van RJ, Pinedo HM, Joenje H (1998) Effect of endogenous glutathione, superoxide dismutases, catalase, and glutathione peroxidase on adriamycin tolerance of Chinese hamster ovary cells. Cancer Res 48:4493Google Scholar
  21. Kiesslich T, Plaetzer K, Oberdanner CB, Berlanda J, Obermair FJ, Krammer B (2005) Differential effects of glucose deprivation on the cellular sensitivity towards photodynamic treatment- based production of reactive oxygen species and apoptosis-induction. FEBS Lett 579(1):185–190CrossRefGoogle Scholar
  22. Koppenol WH (2001) The haber-weiss cycle—70 years later. Redox Rep 6:229–234CrossRefGoogle Scholar
  23. Lardinois OM, Mestdagh MM, Rouxhet PG (1996) Reversible inhibitionand irreversible inactivation of catalase in presence of hydrogen peroxide. Biochim Biophys Acta 1295:222–238CrossRefGoogle Scholar
  24. Lee C (2015) Overexpression of Tyro3 receptor tyrosine kinase leads to the acquisition of taxol resistance in ovarian cancer cells. Mol Med Rep 12:1485–1492CrossRefGoogle Scholar
  25. Lenehan PF, Gutierrez PL, Wagner JL, Milak N, Fisher GR, Ross DD (1995) Ross resistance to oxidants associated with elevated catalase activity in HL-60 leukemia cells that overexpress multidrug-resistance protein does not contribute to the resistance to daunorubicin manifested by these cells. Cancer Chemother Pharmacol 35:377–386CrossRefGoogle Scholar
  26. Li L, Elkholy W, Rhodes CJ, Brubaker PL (2005) Glucagon- like peptide-1 protects beta cells from cytokine-induced apoptosis and necrosis: role of protein kinase B. Diabetologia 48(7):1339–1349CrossRefGoogle Scholar
  27. Lu JJ, Meng LH, Cai YJ, Chen Q, Tong LJ, Lin LP, Ding J (2008) Dihydroartemisinin induces apoptosis in HL-60 leukemia cells dependent of iron and p38 mitogenactivated protein kinase activation but independent of reactive oxygen species. Cancer Biol Ther 7:1017–1023CrossRefGoogle Scholar
  28. Lu YY, Chen TS, Qun JL, Pan WL, Sun L, Wei XB (2009) Dihydroartemisinin (DHA) induces caspase-3-dependent apoptosis in human lung adenocarcinoma ASTC-a-1 cells. J Biomed Sci 16:16CrossRefGoogle Scholar
  29. Madeo F, Frohlich E, Ligr M, Grey M, Sigrist SJ, Wolf DH, Frohlich KU (1999) Oxygen stress: a regulator of apoptosis in yeast. J Cell Biol 145:757–767CrossRefGoogle Scholar
  30. Martins D, English AM (2014) Catalase activity is stimulated by H2O2 in rich culture medium and is required for H2O2 resistance and adaptation in yeast. Redox Biol 2:308–313CrossRefGoogle Scholar
  31. Meshkini A, Yazdanparast R (2012) Involvement of oxidative stress in taxol-induced apoptosis in chronic myelogenous leukemia K562 cells. Exp Toxicol Pathol 64:357–365CrossRefGoogle Scholar
  32. Niess AM, Dickhuth HH, Northoff H, Fehrenbach E (1999) Free radicals and oxidative stress in exercise- immunological aspects. Exerc Immunol Rev 5:22–56Google Scholar
  33. Ogura Y, Yamazaki I (1983) Steady-state kinetics of the catalase reaction in the presence of cyanide. J Biomech 94(2):403–408Google Scholar
  34. Pang YL, Qin GQ, Wu LP, Wang XP, Chen TS (2016) Artesunate induces ROS-dependent apoptosis via a Bax-mediated intrinsic pathway in Huh-7 and Hep3B cells. Exp Cell Res 347(2):251–260CrossRefGoogle Scholar
  35. Park SJ, Wu CH, Gordon JD, Zhong X, Emami A, Safa AR (2004) Taxol Induces Caspase-10-dependent Apoptosis. J Biol Chem 279(49):51057–51067CrossRefGoogle Scholar
  36. Qin GQ, Wu LP, Liu YH, Pang YL, Zhao CB, Wu S, Wang XP, Chen TS (2015) Artesunate induces apoptosis via a ROS-independent and Bax-mediated intrinsic pathway in HepG2 cells. Exp Cell Res 336(2):308–317CrossRefGoogle Scholar
  37. Quan YY, Qin GQ, Huang H, Liu XH, Wang XP, Chen TS (2016) Dominant roles of Fenton reaction in sodium nitroprusside- induced chondrocyte apoptosis. Free Radic Biol Med 94:135–144CrossRefGoogle Scholar
  38. Ramyaa P, Krishnaswamy R, Padma VV (2014) Quercetin modulates OTA-induced oxidative stress and redox signalling in HepG2 cells—up regulation of Nrf2 expression and down regulation of NF-κB and COX-2. Biochim Biophys Acta 1840:681–692CrossRefGoogle Scholar
  39. Rogalska A, Gajek A, Szwed M, Jóźwia Z, Marczak A (2011) The role of reactive oxygen species in WP 631-induced death of human ovarian cancer cells: a comparison with the effect of doxorubicin. Toxicol in Vitro 25(8):1712–1720CrossRefGoogle Scholar
  40. Rudin CM, Yang Z, Schumaker LM, Vanderweele DJ, Newkirk K, Egorin MJ, Zuhowski EG, Cullen KJ (2003) Inhibition of glutathione synthesis reverses Bcl-2-mediated cisplatin resistance. Cancer Res 63:312–318Google Scholar
  41. Schnelldorfer T, Gansauge S, Gansauge F, Schlosser S, Beger HG, Nussler AK (2000) Glutathione depletion causes cell growth inhibition and enhanced apoptosis in pancreatic cancer cells. Cancer 89:1440–1447CrossRefGoogle Scholar
  42. Smith PS, Zhao WL, Robbins ME (2007) Inhibiting catalase activity sensitizes 36B10 rat glioma cells to oxidative stress. Free Radic Biol Med 42:787–797CrossRefGoogle Scholar
  43. Sokolova T, Gutterer JM, Hirrlinger J, Hamprecht B, Dringen R (2001) Catalase in astroglia-rich primary cultures from rat brain: immunocytochemical localization and inactivation during the disposal of hydrogen peroxide. Neurosci Lett 297:129–132CrossRefGoogle Scholar
  44. Spitz DR, Li GC, McCormick ML, Sun Y, Oberley LW (1988) Stable H2O2-resistant variants of Chinese hamster fibro- blasts demonstrate increases in catalase activity. Radiat Res 114:114–124CrossRefGoogle Scholar
  45. Spitz DR, Adams DT, Sherman CM, Roberts RJ (1992) Mechanisms of cellular resistance to hydrogen peroxide, hyperoxia, and 4-hydroxy-2-nonenal toxicity: the significance of increased catalase activity in H2O2-resistant fibroblasts. Arch Biochem Biophys 292:221–227CrossRefGoogle Scholar
  46. Spitz DR, Kinter MT, Roberts RJ (1995) Contribution of increased glutathione content to mechanisms of oxidative stress resistance in hydrogen peroxide resistant hamster fibroblasts. J Cell Physiol 165(3):600–609CrossRefGoogle Scholar
  47. Sun QL, Sha HF, Yang XH, Bao GL, Lu J, Xie YY (2011) Comparative proteomic analysis of paclitaxel sensitive A549 lung adenocarcinoma cell line and its resistant counterpart A549-Taxol. J Cancer Res Clin Oncol 137(3):521–532CrossRefGoogle Scholar
  48. Vetrano AM, Heck DE, Mariano TM, Mishin V, Laskin DL (2005) Characterization of the oxidase activity in mammalian catalase. J Biol Chem 280(42):35372–35381CrossRefGoogle Scholar
  49. Wang J, Yi J (2008) Cancer cell killing via ROS: to increase or decrease, that is the question. Cancer Biol Ther 7(12):1875–1884CrossRefGoogle Scholar
  50. Wang YF, Chen CY, Chung SF, Chiou YH, Lo HR (2004) Involvement of oxidative stress and caspase activation in paclitaxel-induced apoptosis of primary effusion lymphoma cells. Cancer Chemother Pharmacol 54:322–330CrossRefGoogle Scholar
  51. Winterbourn CC, Metodiewa D (1999) Reactivity of biologically important thiol compounds with superoxide and hydrogen peroxide. Free Radic Biol Med 27:322–328CrossRefGoogle Scholar
  52. Woo SH, Park IC, Park MJ, Lee HC, Lee SJ (2002) Arsenic trioxide induces apoptosis through a reactive oxygen species-dependent pathway and loss of mitochondrial membrane potential in HeLa cells. Int J Oncol 21:57Google Scholar
  53. Wu G, Fang YZ, Yang S, Lupton JR, Turner ND (2004) Glutathione metabolism and its implications for health. J Nutr 134(3):489–492CrossRefGoogle Scholar
  54. Yae T, Tsuchihashi K (2012) Alternative splicing of CD44 mRNA by EsRP1 enhances lung colonization of metastatic cancer cell. Nat Commun 3(2):883CrossRefGoogle Scholar
  55. Zhuo CJ, Pan WL, Wang XP, Chen TS (2012) Artesunate induces apoptosis via a Bak-mediated caspase-independent intrinsic pathway in human lung adenocarcinoma cells. J Cell Physiol 227(12):3778–3786CrossRefGoogle Scholar

Copyright information

© Cell Stress Society International 2019

Authors and Affiliations

  • Meng-Xin Zhao
    • 1
  • Jun-Lin Wen
    • 1
  • Lu Wang
    • 2
  • Xiao-Ping Wang
    • 1
    Email author
  • Tong-Sheng Chen
    • 2
  1. 1.Department of Pain Management, the First Affiliated HospitalJinan UniversityGuangzhouChina
  2. 2.MOE Key Laboratory of Laser Life Science & College of Life ScienceSouth China Normal UniversityGuangzhouChina

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