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Peroxiredoxin I deficiency attenuates phagocytic capacity of macrophage in clearance of the red blood cells damaged by oxidative stress

  • Han, Ying-Hao (Aging Research Center) ;
  • Kwon, Tae-Ho (Aging Research Center) ;
  • Kim, Sun-Uk (Aging Research Center) ;
  • Ha, Hye-Lin (Aging Research Center) ;
  • Lee, Tae-Hoon (Aging Research Center) ;
  • Kim, Jin-Man (Department of Pathology, College of Medicine, Chungnam National University) ;
  • Jo, Eun-Kyeong (Department of Microbiology, College of Medicine, Chungnam National University) ;
  • Kim, Bo-Yeon (Chemical Biology Research Center and World Class Institute, Korea Research Institute of Bioscience and Biotechnology) ;
  • Yoon, Do-Young (Department of Bioscience and Biotechnology, Bio/Molecular Informatics Center, Konkuk University) ;
  • Yu, Dae-Yeul (Aging Research Center)
  • Received : 2012.04.18
  • Accepted : 2012.06.09
  • Published : 2012.10.31

Abstract

The role of peroxiredoxin (Prx) I as an erythrocyte antioxidant defense in red blood cells (RBCs) is controversial. Here we investigated the function of Prx I by using Prx $I^{-/-}$ and Prx I/$II^{-/-}$ mice. Prx $I^{-/-}$ mice exhibited a normal blood profile. However, Prx I/$II^{-/-}$ mice showed more significantly increased Heinz body formation as compared with Prx $II^{-/-}$ mice. The clearance rate of Heinz body-containing RBCs in Prx $I^{-/-}$ mice decreased significantly through the treatment of aniline hydrochloride (AH) compared with wild-type mice. Prx I deficiency decreased the phagocytic capacity of macrophage in clearing Heinz body-containing RBCs. Our data demonstrate that Prx I deficiency did not cause hemolytic anemia, but showed that further increased hemolytic anemia symptoms in Prx $II^{-/-}$ mice by attenuating phagocytic capacity of macrophage in oxidative stress damaged RBCs, suggesting a novel role of Prx I in phagocytosis of macrophage.

Keywords

References

  1. 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
  2. Park, J. G. and Oh, G. T. (2011) The role of peroxidases in the pathogenesis of atherosclerosis. BMB Rep. 44, 497-505. https://doi.org/10.5483/BMBRep.2011.44.8.497
  3. Kim, J. S., Bang, M. A., Lee, S., Chae, H. Z. and Kim, K. (2010) Distinct functional roles of peroxiredoxin isozymes and glutathione peroxidase from fission yeast, Schizosaccharomyces pombe. BMB Rep. 43, 170-175. https://doi.org/10.5483/BMBRep.2010.43.3.170
  4. 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
  5. Jacob, H. and Winterhalter, K. (1970) Unstable hemoglobins: the role of heme loss in Heinz body formation. Proc. Natl. Acad. Sci. U.S.A. 65, 697-701. https://doi.org/10.1073/pnas.65.3.697
  6. 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
  7. Neumann, C. A., Cao, J. and Manevich, Y. (2009) Peroxiredoxin 1 and its role in cell signaling. Cell Cycle. 8, 4072-4078. https://doi.org/10.4161/cc.8.24.10242
  8. Kim, S. U., Hwang, C. N., Sun, H. N., Jin, M. H., Han, Y. H., Lee, H., Kim, J. M., Kim, S. K., Yu, D. Y., Lee, D. S. and Lee, S. H. (2008) Peroxiredoxin I is an indicator of microglia activation and protects against hydrogen peroxide- mediated microglial death. Biol. Pharm. Bull. 31, 820-825. https://doi.org/10.1248/bpb.31.820
  9. Bae, J. Y., Ahn, S. J., Han, W. and Noh, D. Y. (2007) Peroxiredoxin I and II inhibit H2O2-induced cell death in MCF-7 cell lines. J. Biol. Chem. 101, 1038-1045.
  10. Woo, H. A., Yim, S. H., Shin, D. H., Kang, D., Yu, D. Y. and Rhee, S. G. (2010) Inactivation of peroxiredoxin I by phosphorylation allows localized H(2)O(2) accumulation for cell signaling. Cell 140, 517-528. https://doi.org/10.1016/j.cell.2010.01.009
  11. Yan, Y., Sabharwal, P., Rao, M. and Sockanathan, S. (2009) The antioxidant enzyme Prdx1 controls neuronal differentiation by thiol-redox-dependent activation of GDE2. Cell 138, 1209-1221. https://doi.org/10.1016/j.cell.2009.06.042
  12. Cao, J., Schulte, J., Knight, A., Leslie, N. R., Zagozdzon, A., Bronson, R., Manevich, Y., Beeson, C. and Neumann, C. A. (2009) Prdx1 inhibits tumorigenesis via regulating PTEN/AKT activity. EMBO J. 28, 1505-1517. https://doi.org/10.1038/emboj.2009.101
  13. 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
  14. Egler, R. A., Fernandes, E., Rothermund, K., Sereika, S., de Souza-Pinto, N., Jaruga, P., Dizdaroglu, M. and Prochownik, E. V. (2005) Regulation of reactive oxygen species, DNA damage, and c-Myc function by peroxiredoxin 1. Oncogene 24, 8038-8050. https://doi.org/10.1038/sj.onc.1208821
  15. Uwayama, J., Hirayama, A., Yanagawa, T., Warabi, E., Sugimoto, R., Itoh, K., Yamamoto, M., Yoshida, H., Koyama, A. and Ishii, T. (2006) Tissue Prx I in the protection against Fe-NTA and the reduction of nitroxyl radicals. Biochem. Biophys. Res. Commun. 339, 226-231. https://doi.org/10.1016/j.bbrc.2005.10.192
  16. Friedman, J. S., Lopez, M. F., Fleming, M. D., Rivera, A., Martin, F. M., Welsh, M. L., Boyd, A., Doctrow, S. R. and Burakoff, S. J. (2004) SOD2-deficiency anemia: protein oxidation and altered protein expression reveal targets of damage, stress response, and antioxidant responsiveness. Blood 104, 2565-2573. https://doi.org/10.1182/blood-2003-11-3858
  17. Ho, Y. S., Xiong, Y., Ma, W., Spector, A. and Ho, D. S. (2004) Mice lacking catalase develop normally but show differential sensitivity to oxidant tissue injury. J. Biol. Chem. 279, 32804-32812. https://doi.org/10.1074/jbc.M404800200
  18. Johnson, R. M., Goyette, G. Jr., Ravindranath, Y. and Ho, Y. S. (2000) Red cells from glutathione peroxidase-1-deficient mice have nearly normal defenses against exogenous peroxides. Blood 96, 1985-1988.
  19. Low, F. M., Hampton, M. B., Peskin, A. V. and Winterbourn, C. C. (2007) Peroxiredoxin 2 functions as a noncatalytic scavenger of low-level hydrogen peroxide in the erythrocyte. Blood 109, 2611-2617. https://doi.org/10.1182/blood-2006-09-048728
  20. Bokoch, G. M. (1995) Regulation of the phagocyte respiratory burst by small GTP-binding proteins. Trends. Cell Biol. 5, 109-113. https://doi.org/10.1016/S0962-8924(00)88960-6
  21. Brown, K. L., Christenson, K., Karlsson, A., Dahlgren, C. and Bylund, J. (2009) Divergent effects on phagocytosis by macrophage-derived oxygen radicals. J. Innate. Immun. 1, 592-598. https://doi.org/10.1159/000235583
  22. Ishii, T., Itoh, K., Takahashi, S., Sato, H., Yanagawa, T., Katoh, Y., Bannai, S. and Yamamoto, M. (2000) Transcription factor Nrf2 coordinately regulates a group of oxidative stress-inducible genes in macrophages. J. Biol. Chem. 275, 16023-16029. https://doi.org/10.1074/jbc.275.21.16023
  23. Yamaguchi, M., Sato, H. and Bannai, S. (1993) Induction of stress proteins in mouse peritoneal macrophages by oxidized low-density lipoprotein. Biochem. Biophys. Res. Commun. 193, 1198-1201. https://doi.org/10.1006/bbrc.1993.1752

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