Overexpression of human peroxiredoxin 5 in subcellular compartments of Chinese hamster ovary cells: Effects on cytotoxicity and DNA damage caused by peroxides

Free Radical Biology and Medicine

Volumn 36, Issue 1, 2004, Pages 65-77

  Banmeyer, Ingrid ^a   Marchand, Cécile ^a   Verhaeghe, Catherine ^a   Vucic, Bénédicte ^a   Rees, Jean François ^a   Knoops, Bernard ^a  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

Author keywords

Cytosol; DNA damage; Free radicals; Mitochondria; Nucleus; Oxidative stress; Peroxide; Peroxiredoxin; Thioredoxin peroxidase

Indexed keywords

CELL NUCLEUS DNA; HYDROGEN PEROXIDE; LACTATE DEHYDROGENASE; PEROXIDE; PEROXIREDOXIN; PEROXIREDOXIN 5; TERT BUTYL HYDROPEROXIDE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL COMPARTMENTALIZATION; CELL DEATH; CELL NUCLEUS; CELL ORGANELLE; CELL PROTECTION; CELLULAR DISTRIBUTION; CHO CELL; CLONOGENESIS; COMET ASSAY; CONTROLLED STUDY; CYTOSOL; CYTOTOXICITY; DNA DAMAGE; ENZYME ASSAY; EVALUATION; EXPOSURE; GENETIC TRANSFECTION; MITOCHONDRION; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; TIME;

CRICETINAE; CRICETULUS GRISEUS; MAMMALIA;

EID: 0346056899     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2003.10.019     Document Type: Article

References (63)

1. Halliwell B., Gutteridge J.M.C. Free radicals in biology and medicine. 2nd ed. 1998;Oxford University Press, London.
2. Chae H.Z., Robison K., Poole L.B., Church G., Storz G., Rhee S.G. Cloning and sequencing of thiol-specific antioxidant from mammalian brain: alkyl hydroperoxide reductase and thiol-specific antioxidant define a large family of antioxidant enzymes. Proc. Natl. Acad. Sci. USA. 91:1994;7017-7021.
3. Rhee S.G., Kang S.W., Chang T.S., Jeong W., Kim K. Peroxiredoxin, a novel family of peroxidases. IUBMB Life. 52:2001;35-41.
4. Hofmann B., Hecht H.J., Flohe L. Peroxiredoxins. Biol. Chem. 383:2002;347-364.
5. Fujii J., Ikeda Y. Advances in our understanding of peroxiredoxin, a multifunctional, mammalian redox protein. Redox Rep. 7:2002;123-130.
6. Wood Z.A., Schroder E., Robin Harris J., Poole L.B. Structure, mechanism and regulation of peroxiredoxins. Trends Biochem. Sci. 28:2003;32-40.
7. Knoops B., Clippe A., Bogard C., Arsalane K., Wattiez R., Hermans C., Duconseille E., Falmagne P., Bernard A. Cloning and characterization of AOEB166, a novel mammalian antioxidant enzyme of the peroxiredoxin family. J. Biol. Chem. 274:1999;30451-30458.
8. Yamashita H., Avraham S., Jiang S., London R., Van Veldhoven P.P., Subramani S., Rogers R.A., Avraham H. Characterization of human and murine PMP20 peroxisomal proteins that exhibit antioxidant activity in vitro. J. Biol. Chem. 274:1999;29897-29904.
9. Seo M.S., Kang S.W., Kim K., Baines I.C., Lee T.H., Rhee S.G. Identification of a new type of mammalian peroxiredoxin that forms an intramolecular disulfide as a reaction intermediate. J. Biol. Chem. 275:2000;20346-20354.
10. Kropotov A., Sedova V., Ivanov V., Sazeeva N., Tomilin A., Krutilina R., Oei S.L., Griesenbeck J., Buchlow G., Tomilin N. A novel human DNA-binding protein with sequence similarity to a subfamily of redox proteins which is able to repress RNA-polymerase-III-driven transcription of the Alu-family retroposons in vitro. Eur. J. Biochem. 260:1999;336-346.
11. Oberley T.D., Verwiebe E., Zhong W., Kang S.W., Rhee S.G. Localization of the thioredoxin system in normal rat kidney. Free Radic. Biol. Med. 30:2001;412-424.
12. Lee S.P., Hwang Y.S., Kim Y.J., Kwon K.S., Kim H.J., Kim K., Chae H.Z. Cyclophilin a binds to peroxiredoxins and activates its peroxidase activity. J. Biol. Chem. 276:2001;29826-29832.
13. Powis G., Montfort W.R. Properties and biological activities of thioredoxins. Annu. Rev. Pharmacol. Toxicol. 41:2001;261-295.
14. Damdimopoulos A.E., Miranda-Vizuete A., Pelto-Huikko M., Gustafsson J.A., Spyrou G. Human mitochondrial thioredoxin: involvement in mitochondrial membrane potential and cell death. J. Biol. Chem. 277:2002;33249-33257.
15. Nordberg J., Arner E.S. Reactive oxygen species, antioxidants, and the mammalian thioredoxin system. Free Radic. Biol. Med. 31:2001;1287-1312.
16. Le Hir M., Su Q., Weber L., Woerly G., Granelli-Piperno A., Ryffel B. In situ detection of cyclosporin A: evidence for nuclear localization of cyclosporine and cyclophilins. Lab. Invest. 73:1995;727-733.
17. Krummrei U., Bang R., Schmidtchen R., Brune K., Bang H. Cyclophilin-A is a zinc-dependent DNA binding protein in macrophages. FEBS Lett. 371:1995;47-51.
18. Landtmeters M., Alzate L., Clippe A., Duconseille E., Bernard A., Knoops B. PRDX5 is a novel mammalian antioxidant enzyme of the peroxiredoxin family with antiapoptotic properties (abstract). Anticancer Res. 21:2001;A1569.
19. Zhou Y., Kok K.H., Chun A.C., Wong C.M., Wu H.W., Lin M.C., Fung P.C., Kung H., Jin D.Y. Mouse peroxiredoxin V is a thioredoxin peroxidase that inhibits p53-induced apoptosis. Biochem. Biophys. Res. Commun. 268:2000;921-927.
20. Nguyen-nhu T.N., Knoops B. Mitochondrial and cytosolic expression of human peroxiredoxin 5 in Saccharomyces cerevisiae protect yeast cells from oxidative stress induced by paraquat. FEBS Lett. 544:2003;148-152.
21. Wang M.X., Wei A., Yuan J., Clippe A., Bernard A., Knoops B., Murrell G.A. Antioxidant enzyme peroxiredoxin 5 is upregulated in degenerative human tendon. Biochem. Biophys. Res. Commun. 284:2001;667-673.
22. Declercq J.P., Evrard C., Clippe A., Vander Stricht D., Bernard A., Knoops B. Crystal structure of human peroxiredoxin 5, a novel type of mammalian peroxiredoxin at 1.5 A resolution. J. Mol. Biol. 311:2001;751-759.
23. Plaisant F., Clippe A., Vander Stricht D., Knoops B., Gressens P. Recombinant peroxiredoxin 5 protects against excitotoxic brain lesions in newborn mice. Free Radic. Biol. Med. 34:2003;862-872.
24. Mizushima S., Nagata S. pEF-BOS, a powerful mammalian expression vector. Nucleic Acids Res. 18:1990;5322.
25. Demoulin J.B., Uyttenhove C., Van Roost E., DeLestre B., Donckers D., Van Snick J., Renauld J.C. A single tyrosine of the interleukin-9 (IL-9) receptor is required for STAT activation, antiapoptotic activity, and growth regulation by IL-9. Mol. Cell. Biol. 16:1996;4710-4716.
26. Kalderon D., Richardson W.D., Markham A.F., Smith A.E. Sequence requirements for nuclear location of simian virus 40 large-T antigen. Nature. 311:1984;33-38.
27. Chae H.Z., Kang S.W., Rhee S.G. Isoforms of mammalian peroxiredoxin that reduce peroxides in presence of thioredoxin. Methods Enzymol. 300:1999;219-226.
28. Rickwood D., Harris J.R. Cell biology: essential techniques. 1997;Wiley, New York.
29. Paglia D.E., Valentine W.N. Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J. Lab. Clin. Med. 70:1967;158-169.
30. Collins A.R., Ma A.G., Duthie S.J. The kinetics of repair of oxidative DNA damage (strand breaks and oxidised pyrimidines) in human cells. Mutat. Res. 336:1995;69-77.
31. Breeuwer M., Goldfarb D.S. Facilitated nuclear transport of histone H1 and other small nucleophilic proteins. Cell. 60:1990;999-1008.
32. Wang M.X., Wei A., Yuan J., Trickett A., Knoops B., Murrell G.A. Expression and regulation of peroxiredoxin 5 in human osteoarthritis. FEBS Lett. 531:2002;359-362.
33. Wattiez R., Hermans C., Cruyt C., Bernard A., Falmagne P. Human bronchoalveolar lavage fluid protein two-dimensional database: study of interstitial lung diseases. Electrophoresis. 21:2000;2703-2712.
34. Bjornstedt M., Xue J., Huang W., Akesson B., Holmgren A. The thioredoxin and glutaredoxin systems are efficient electron donors to human plasma glutathione peroxidase. J. Biol. Chem. 269:1994;29382-29384.
35. Gelvan D., Moreno V., Clopton D.A., Chen Q., Saltman P. Sites and mechanisms of low-level oxidative stress in cultured cells. Biochem. Biophys. Res. Commun. 206:1995;421-428.
36. Sanchez-Gongora E., Pastorino J.G., Alvarez L., Pajares M.A., Garcia C., Vina J.R., Mato J.M., Farber J.L. Increased sensitivity to oxidative injury in Chinese hamster ovary cells stably transfected with rat liver S-adenosylmethionine synthetase cDNA. Biochem. J. 319:1996;767-773.
37. Tonoki H. Establishment of Chinese hamster ovary cell lines with reduced expression of glutathione reductase after antisense-oriented gene transfection and assessment of the sensitivity to oxidant injury. Hokkaido Igaku Zasshi. 69:1994;1261-1274.
38. Keizer H.G., van Rijn J., Pinedo H.M., Joenje H. Effect of endogenous glutathione, superoxide dismutases, catalase, and glutathione peroxidase on adriamycin tolerance of Chinese hamster ovary cells. Cancer Res. 48:1988;4493-4497.
39. Anuszewska E.L., Gruber B.M., Koziorowska J.H. Studies on adaptation to adriamycin in cells pretreated with hydrogen peroxide. Biochem. Pharmacol. 54:1997;597-603.
40. Arai M., Imai H., Koumura T., Yoshida M., Emoto K., Umeda M., Chiba N., Nakagawa Y. Mitochondrial phospholipid hydroperoxide glutathione peroxidase plays a major role in preventing oxidative injury to cells. J. Biol. Chem. 274:1999;4924-4933.
41. Tamura T., McMicken H.W., Smith C.V., Hansen T.N. Overexpression of human glutathione reductase in Chinese hamster ovary cells protects cells from oxidant injury (abstract). Pediatr. Res. 39:1997;A248.
42. Zhang Y., Marcillat O., Giulivi C., Ernster L., Davies K.J. The oxidative inactivation of mitochondrial electron transport chain components and ATPase. J. Biol. Chem. 265:1990;16330-16336.
43. Kaneko M., Kodama M., Inoue F., Terasaki T. Mitochondrial biosynthesis controls the sensitivity of Chinese hamster cells to hydrogen peroxide. Free Radic. Res. 24:1996;299-309.
44. Bryszewska M., Piasecka A., Zavodnik L.B., Distel L., Schussler H. Oxidative damage of Chinese hamster fibroblasts induced by t-butyl hydroperoxide and by X-rays. Biochim. Biophys. Acta. 1621:2003;285-291.
45. Halestrap A.P., Woodfield K.Y., Connern C.P. Oxidative stress, thiol reagents, and membrane potential modulate the mitochondrial permeability transition by affecting nucleotide binding to the adenine nucleotide translocase. J. Biol. Chem. 272:1997;3346-3354.
46. Cabiscol E., Piulats E., Echave P., Herrero E., Ros J. Oxidative stress promotes specific protein damage in Saccharomyces cerevisiae. J. Biol. Chem. 275:2000;27393-27398.
47. Munoz C.M., van Meeteren L.A., Post J.A., Verkleij A.J., Verrips C.T., Boonstra J. Hydrogen peroxide inhibits cell cycle progression by inhibition of the spreading of mitotic CHO cells. Free Radic. Biol. Med. 33:2002;1061-1072.
48. Henle E.S., Linn S. Formation, prevention, and repair of DNA damage by iron/hydrogen peroxide. J. Biol. Chem. 272:1997;19095-19098.
49. Aruoma O.I., Halliwell B., Gajewski E., Dizdaroglu M. Copper-ion-dependent damage to the bases in DNA in the presence of hydrogen peroxide. Biochem. J. 273:1991;601-604.
50. Termini J. Hydroperoxide-induced DNA damage and mutations. Mutat. Res. 450:2000;107-124.
51. Dahm-Daphi J., Sass C., Alberti W. Comparison of biological effects of DNA damage induced by ionizing radiation and hydrogen peroxide in CHO cells. Int. J. Radiat. Biol. 76:2000;67-75.
52. Kaneko M., Inoue F. The sensitivity to DNA single strand breakage in mitochondria, but not in nuclei, of Chinese hamster V79 and variant cells correlates with their cellular sensitivity to hydrogen peroxide. Toxicol. Lett. 99:1998;15-22.
53. Wiese A.G., Pacifici R.E., Davies K.J. Transient adaptation of oxidative stress in mammalian cells. Arch. Biochem. Biophys. 318:1995;231-240.
54. Cantoni O., Sestili P., Palomba L., Guidarelli A., Cattabeni F., Murray D. Isolation and preliminary characterization of a Chinese hamster ovary cell line with high-degree resistance to hydrogen peroxide. Biochem. Pharmacol. 51:1996;1021-1029.
55. Guidarelli A., Cattabeni F., Cantoni O. Alternative mechanisms for hydroperoxide-induced DNA single strand breakage. Free Radic. Res. 26:1997;537-547.
56. Cooke M.S., Evans M.D., Dizdaroglu M., Lunec J. Oxidative DNA damage: mechanisms, mutation and disease. FASEB J. 17:2003;1195-1214.
57. Cha M.K., Choi Y.S., Hong S.K., Kim W.C., No K.T., Kim I.H. Nuclear thiol peroxidase as a functional alkyl-hydroperoxide reductase necessary for stationary phase growth of Saccharomyces cerevisiae. J. Biol. Chem. 278:2003;24636-24643.
58. Bai J., Cederbaum A.I. Overexpression of catalase in the mitochondrial or cytosolic compartment increases sensitivity of HepG2 cells to tumor necrosis factor-alpha-induced apoptosis. J. Biol. Chem. 275:2000;19241-19249.
59. Wenk J., Brenneisen P., Wlaschek M., Poswig A., Briviba K., Oberley T.D., Scharffetter-Kochanek K. Stable overexpression of manganese superoxide dismutase in mitochondria identifies hydrogen peroxide as a major oxidant in the AP-1-mediated induction of matrix-degrading metalloprotease-1. J. Biol. Chem. 274:1999;25869-25876.
60. Wang X., Phelan S.A., Forsman-Semb K., Taylor E.F., Petros C., Brown A., Lerner C.P., Paigen B. Mice with targeted mutation of peroxiredoxin 6 develop normally but are susceptible to oxidative stress. J. Biol. Chem. 278:2003;25179-25190.
61. Rohrdanz E., Schmuck G., Ohler S., Kahl R. The influence of oxidative stress on catalase and MnSOD gene transcription in astrocytes. Brain Res. 900:2001;128-236.
62. Kirkman H.N., Gaetani G.F. Catalase: a tetrameric enzyme with four tightly bound molecules of NADPH. Proc. Natl. Acad. Sci. USA. 81:1984;4343-4347.
63. Tabatabaie T., Floyd R.A. Susceptibility of glutathione peroxidase and glutathione reductase to oxidative damage and the protective effect of spin trapping agents. Arch. Biochem. Biophys. 314:1994;112-119.