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Over-expressed Peroxiredoxin I Protects against Oxidative Damage in Mouse Embryonic Fibroblasts Lacking Peroxiredoxin II

  • Kim, Seong-Gon (School of Life Science and Biotechnology, Kyungpook National University) ;
  • Kim, Jae-Young (Department of Biochemistry, School of Dentistry, IHBR, Kyungpook National University) ;
  • Ryoo, Zae-Young (School of Life Science and Biotechnology, Kyungpook National University) ;
  • Lee, Sang-Gyu (School of Life Science and Biotechnology, Kyungpook National University)
  • Received : 2011.07.29
  • Accepted : 2011.10.05
  • Published : 2011.10.30

Abstract

Peroxiredoxins (Prxs) have a critical role in protecting cells against oxidative damage generated by reactive oxygen species (ROS). PrxI and PrxII are more than 90% homologous in their amino acid sequences, and both proteins reduce $H_2O_2$. In this study, an over-expression plasmid carrying PrxI was transfected into $PrxII^{-/-}$ mouse embryonic fibroblasts (MEFs) to investigate potential compensatory relationships between PrxI and PrxII. ROS levels induced by oxidative stress were increased in $PrxII^{-/-}$ MEFs as compared to wild-type MEFs. Moreover, exposure of $PrxII^{-/-}$ MEFs to $H_2O_2$ caused a reduction in cell viability of about 10%, and the proportion of cell death was increased compared to mock-treated $PrxII^{-/-}$ MEFs. However, transient over-expression of PrxI in $PrxII^{-/-}$ MEFs conferred increased resistance against the oxidative damage, as evidenced by increased cell viability and reduced intracellular ROS levels under $H_2O_2$ stress conditions. The findings suggest that over-expressed PrxI can partly compensate for the loss of PrxII function in PrxII-deficient MEFs.

Keywords

References

  1. Chae, H. Z., Kim, H. J., Kang, S. W. and Rhee, S. G. (1999) Characterization of three isoforms of mammalian peroxiredoxin that reduce peroxides in the presence of thioredoxin. Diabetes Res. Clin. Pract. 45, 101-112. https://doi.org/10.1016/S0168-8227(99)00037-6
  2. Chae, H. Z., Kim, I. H., Kim, K. and Rhee, S. G. (1993) Cloning, sequencing, and mutation of thiol-specifi c antioxidant gene of Saccharomyces cerevisiae. J. Biol. Chem. 268, 16815-16821.
  3. Claiborne, A., Mallett, T. C., Yeh, J. I., Luba, J. and Parsonage, D. (2001) Structural, redox, and mechanistic parameters for cysteine- sulfenic acid function in catalysis and regulation. Adv. Protein Chem. 58, 215-276. https://doi.org/10.1016/S0065-3233(01)58006-7
  4. Han, Y. H., Kim, H. S., Kim, J. M., Kim, S. K., Yu, D. Y. and Moon, E. Y. (2005) Inhibitory role of peroxiredoxin II (Prx II) on cellular senescence. FEBS Lett. 579, 4897-4902. https://doi.org/10.1016/j.febslet.2005.07.049
  5. Iwahara, S., Satoh, H., Song, D. X., Webb, J., Burlingame, A. L., Nagae, Y. and Muller-Eberhard, U. (1995) Purifi cation, characterization, and cloning of a heme-binding protein (23 kDa) in rat liver cytosol. Biochemistry 34, 13398-13406. https://doi.org/10.1021/bi00041a017
  6. Jang, H. H., Lee, K. O., Chi, Y. H., Jung, B. G., Park, S. K., Park, J. H., Lee, J. R., Lee, S. S., Moon, J. C., Yun, J. W., Choi, Y. O., Kim, W. Y., Kang, J. S., Cheong, G. W., Yun, D. J., Rhee, S. G., Cho, M. J. and Lee, S. Y. (2004) Two enzymes in one; two yeast peroxiredoxins display oxidative stress-dependent switching from a peroxidase to a molecular chaperone function. Cell 117, 625-635. https://doi.org/10.1016/j.cell.2004.05.002
  7. Kang, S. W., Chae, H. Z., Seo, M. S., Kim, K., Baines, I. C. and Rhee, S. G. (1998) Mammalian peroxiredoxin isoforms can reduce hydrogen peroxide generated in response to growth factors and tumor necrosis factor-alpha. J. Biol. Chem. 273, 6297-6302. https://doi.org/10.1074/jbc.273.11.6297
  8. Kim, H., Lee, T. H., Park, E. S., Suh, J. M., Park, S. J., Chung, H. K., Kwon, O. Y., Kim, Y. K., Ro, H. K. and Shong, M. (2000) Role of peroxiredoxins in regulating intracellular hydrogen peroxide and hydrogen peroxide-induced apoptosis in thyroid cells. J. Biol. Chem. 275, 18266-18270. https://doi.org/10.1074/jbc.275.24.18266
  9. Kim, K., Kim, I. H., Lee, K. Y., Rhee, S. G. and Stadtman, E. R. (1988) The isolation and purifi cation of a specifi c "protector" protein which inhibits enzyme inactivation by a thiol/Fe(III)/O2 mixed-function oxidation system. J. Biol. Chem. 263, 4704-4711.
  10. Knoops, B., Clippe, A., Bogard, C., Arsalane, K., Wattiez, R., Hermans, C., Duconseille, E., Falmagne, P. and Bernard, A. (1999) Cloning and characterization of AOEB166, a novel mammalian antioxidant enzyme of the peroxiredoxin family. J. Biol. Chem. 274, 30451-30458. https://doi.org/10.1074/jbc.274.43.30451
  11. Lee, T. H., Kim, S. U., Yu, S. L., Kim, S. H., Park, D. S., Moon, H. B., Dho, S. H., Kwon, K. S., Kwon, H. J., Han, Y. H., Jeong, S., Kang, S. W., Shin, H. S., Lee, K. K., Rhee, S. G. and Yu, D. Y. (2003) Peroxiredoxin II is essential for sustaining life span of erythrocytes in mice. Blood 101, 5033-5038. https://doi.org/10.1182/blood-2002-08-2548
  12. Lee, W., Choi, K. S., Riddell, J., Ip, C., Ghosh, D., Park, J. H. and Park, Y. M. (2007) Human peroxiredoxin 1 and 2 are not duplicate proteins: the unique presence of CYS83 in Prx1 underscores the structural and functional differences between Prx1 and Prx2. J. Biol. Chem. 282, 22011-22022. https://doi.org/10.1074/jbc.M610330200
  13. Ma, D., Warabi, E., Yanagawa, T., Kimura, S., Harada, H., Yamagata, K. and Ishii, T. (2009) Peroxiredoxin I plays a protective role against cisplatin cytotoxicity through mitogen activated kinase signals. Oral Oncol. 45, 1037-1043. https://doi.org/10.1016/j.oraloncology.2009.07.002
  14. Moon, E. Y., Han, Y. H., Lee, D. S., Han, Y. M. and Yu, D. Y. (2004) Reactive oxygen species induced by the deletion of peroxiredoxin II (PrxII) increases the number of thymocytes resulting in the enlargement of PrxII-null thymus. Eur. J. Immunol. 34, 2119-2128. https://doi.org/10.1002/eji.200424962
  15. Nemoto, Y., Yamamoto, T., Takada, S., Matsui, Y. and Obinata, M. (1990) Antisense RNA of the latent period gene (MER5) inhibits the differentiation of murine erythroleukemia cells. Gene 91, 261-265. https://doi.org/10.1016/0378-1119(90)90097-B
  16. Neumann, C. A., Krause, D. S., Carman, C. V., Das, S., Dubey, D. P., Abraham, J. L., Bronson, R. T., Fujiwara, Y., Orkin, S. H. and Van Etten, R. A. (2003) Essential role for the peroxiredoxin Prdx1 in erythrocyte antioxidant defence and tumour suppression. Nature 424, 561-565. https://doi.org/10.1038/nature01819
  17. Phalen, T. J., Weirather, K., Deming, P. B., Anathy, V., Howe, A. K., van der Vliet, A., Jonsson, T. J., Poole, L. B. and Heintz, N. H. (2006) Oxidation state governs structural transitions in peroxiredoxin II that correlate with cell cycle arrest and recovery. J. Cell Biol. 175, 779-789. https://doi.org/10.1083/jcb.200606005
  18. Rhee, S. G., Chae, H. Z. and Kim, K. (2005a) Peroxiredoxins: a historical overview and speculative preview of novel mechanisms and emerging concepts in cell signaling. Free Radic. Biol. Med. 38, 1543-1552. https://doi.org/10.1016/j.freeradbiomed.2005.02.026
  19. Rhee, S. G., Kang, S. W., Chang, T. S., Jeong, W. and Kim, K. (2001) Peroxiredoxin, a novel family of peroxidases. IUBMB Life 52, 35-41. https://doi.org/10.1080/15216540252774748
  20. Rhee, S. G., Kang, S. W., Jeong, W., Chang, T. S., Yang, K. S. and Woo, H. A. (2005b) Intracellular messenger function of hydrogen peroxide and its regulation by peroxiredoxins. Curr. Opin. Cell Biol. 17, 183-189. https://doi.org/10.1016/j.ceb.2005.02.004
  21. Seo, M. S., Kang, S. W., Kim, K., Baines, I. C., Lee, T. H. and Rhee, S. G. (2000) Identifi cation of a new type of mammalian peroxiredoxin that forms an intramolecular disulfi de as a reaction intermediate. J. Biol. Chem. 275, 20346-20354. https://doi.org/10.1074/jbc.M001943200
  22. Shau, H., Butterfi eld, L. H., Chiu, R. and Kim, A. (1994) Cloning and sequence analysis of candidate human natural killer-enhancing factor genes. Immunogenetics 40, 129-134.
  23. Tsuji, K., Copeland, N. G., Jenkins, N. A. and Obinata, M. (1995) Mammalian antioxidant protein complements alkylhydroperoxide reductase (ahpC) mutation in Escherichia coli. Biochem. J. 307 (Pt 2), 377-381.
  24. Wang, X., Phelan, S. A., Forsman-Semb, K., Taylor, E. F., Petros, C., Brown, A., Lerner, C. P. and Paigen, B. (2003) Mice with targeted mutation of peroxiredoxin 6 develop normally but are susceptible to oxidative stress. J. Biol. Chem. 278, 25179-25190. https://doi.org/10.1074/jbc.M302706200
  25. Wen, S. T. and Van Etten, R. A. (1997) The PAG gene product, a stress-induced protein with antioxidant properties, is an Abl SH3-binding protein and a physiological inhibitor of c-Abl tyrosine kinase activity. Genes Dev. 11, 2456-2467. https://doi.org/10.1101/gad.11.19.2456
  26. Wood, Z. A., Schroder, E., Robin Harris, J. and Poole, L. B. (2003) Structure, mechanism and regulation of peroxiredoxins. Trends Biochem. Sci. 28, 32-40. https://doi.org/10.1016/S0968-0004(02)00003-8
  27. Zhang, B., Wang, Y., Liu, K., Yang, X., Song, M. and Bai, Y. (2008) Adenovirus-mediated transfer of siRNA against peroxiredoxin I enhances the radiosensitivity of human intestinal cancer. Biochem. Pharmacol. 75, 660-667. https://doi.org/10.1016/j.bcp.2007.09.016

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