Different consequences of reactions with hydrogen peroxide and t-butyl hydroperoxide in the hyperoxidative inactivation of rat peroxiredoxin-4

Journal of Biochemistry

Volumn 149, Issue 4, 2011, Pages 443-453

  Ikeda, Yoshitaka ^a,b   Nakano, Miyako ^b   Ihara, Hideyuki ^a   Ito, Ritsu ^a   Taniguchi, Naoyuki ^b,c   Fujii, Junichi ^d  

^a SAGA UNIVERSITY   (Japan)

^b OSAKA UNIVERSITY   (Japan)

^c RIKEN   (Japan)

^d YAMAGATA UNIVERSITY   (Japan)

Author keywords

ER; hyperoxidation; oxidative stress; peroxiredoxin; sulphinic acid

Indexed keywords

CYSTEINE; HYDROGEN PEROXIDE; ISOENZYME; PEROXIDASE; PEROXIREDOXIN 4; SULFINIC ACID DERIVATIVE; TERT BUTYL HYDROPEROXIDE;

ANIMAL CELL; ARTICLE; CATALYSIS; CONTROLLED STUDY; CYTOSOL; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; ENZYME INACTIVATION; ENZYME INHIBITION; MASS SPECTROMETRY; NONHUMAN; OXIDATIVE STRESS; PEROXIDATION;

EUKARYOTA; RATTUS;

EID: 79953229574     PISSN: 0021924X     EISSN: 17562651     Source Type: Journal    
DOI: 10.1093/jb/mvq156     Document Type: Article

References (50)

1. Kim, K., Kim, I.H., Lee, K.Y., Rhee, S.G., and Stadtman, E.R. (1988) The isolation and purification of a specific "protector" protein which inhibits enzyme in-activation by a thiol/Fe(III)/O2 mixed-function oxida-tion system. J. Biol. Chem. 263, 4704-4711
2. Chae, H.Z., Robison, K., Poole, L.B., Church, G., Storz, G., and Rhee, S.G. (1994) 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, 7017-7021 (Pubitemid 24226793)
3. Chae, H.Z., Kim, H.J., Kang, S.W., and Rhee, S.G. (1999) Characterization ofthree isoforms of mammalian peroxiredoxin that reduce peroxides in the presence of thioredoxin. Diabetes Res. Clin. Pract. 45, 101-112 (Pubitemid 29457756)
4. Chae, H.Z., Kang, S.W., and Rhee, S.G. (1999) Isoforms of mammalian peroxiredoxin that reduce peroxides in presence ofthioredoxin. Methods Enzymol. 300, 219-226
5. Chae, H.Z., Chung, S.J., and Rhee, S.G. (1994) Thioredoxin-dependent peroxide reductase from yeast. J. Biol. Chem. 269, 27670-27678 (Pubitemid 24346604)
6. Rhee, S.G., Kang, S.W., Chang, T.S., Jeong, W., and Kim, K. (2001) Peroxiredoxin, a novel family of perox-idases. IUBMB Life 52, 35-41
7. Fujii, J. and Ikeda, Y. (2002) Advances in our under-standing of peroxiredoxin, a multifunctional, mamma-lian redox protein. Redox Rep. 7, 123-130 (Pubitemid 34700435)
8. Ishii, T., Itoh, K., Akasaka, J., Yanagawa, T., Takahashi, S., Yoshida, H., Bannai, S., and Yamamoto, M. (2000) Induction of murine intestinal and hepatic peroxiredoxin MSP23 by dietary butylated hydroxyanisole. Carcinogenesis 21, 1013-1016 (Pubitemid 30265148)
9. Furuta, J., Nobeyama, Y., Umebayashi, Y., Otsuka, F., Kikuchi, K., and Ushijima, T. (2006) Silencing of Peroxiredoxin 2 and aberrant methylation of 33 CpG islands in putative promoter regions in human malignant melanomas. Cancer Res. 66, 6080-6086
10. Chang, X.Z., Li, D.Q., Hou, Y.F., Wu, J., Lu, J.S., Di, G.H., Jin, W., Ou, Z.L., Shen, Z.Z., and Shao, Z.M. (2007) Identification of the functional role of peroxire-doxin 6 in the progression of breast cancer. Breast Cancer Res. 9, R76
11. Iraqui, I., Faye, G., Ragu, S., Masurel-Heneman, A., Kolodner, R.D., and Huang, M.E. (2008) Human per-oxiredoxin PrxI is an orthologue ofyeast Tsa1, capable of suppressing genome instability in Saccharomyces cer-evisiae. Cancer Res. 68, 1055-1063 (Pubitemid 351272223)
12. Song, I.S., Kim, S.U., Oh, N.S., Kim, J., Yu, D.Y, Huang, S.M., Kim, J.M., Lee, D.S., and Kim, N.S. (2009) Peroxiredoxin I contributes to TRAIL resistance through suppression ofredox-sensitive caspase activation in human hepatoma cells. Carcinogenesis 30, 1106-1114
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 antioxi-dant defence and tumour suppression. Nature 424, 561-565 (Pubitemid 36975778)
14. Demasi, A.P., Ceratti, D., Furuse, C., Cury, P., Junqueira, J.L., and Araujo, V.C. (2007) Expression of peroxiredoxin I in plasma cells of oral inflammatory dis-eases. Eur. J. Oral Sci. 115, 334-337
15. Yang, C.S., Lee, D.S., Song, C.H., An, S.J., Li, S., Kim, J.M., Kim, C.S., Yoo, D.G., Jeon, B.H., Yang, H.Y., Lee, T.H., Lee, Z.W., El-Benna, J., Yu, D.Y., and Jo, E.K. (2007) Roles of peroxiredoxin II in the regulation of proinflammatory responses to LPS and protection against endotoxin-induced lethal shock. J. Exp. Med. 204, 583-594 (Pubitemid 46457081)
16. Li, L., Shoji, W., Takano, H., Nishimura, N., Aoki, Y., Takahashi, R., Goto, S., Kaifu, T., Takai, T., and Obinata, M. (2007) Increased susceptibility of MER5 (peroxiredoxin III) knockout mice to LPS-induced oxi-dative stress. Biochem. Biophys. Res. Commun. 355, 715-721 (Pubitemid 46330210)
17. Fang, J., Nakamura, T., Cho, D.H., Gu, Z., and Lipton, S.A. (2007) S-nitrosylation of peroxiredoxin 2 promotes oxidative stress-induced neuronal cell death in Parkinson's disease. Proc. Natl. Acad. Sci. USA 104, 18742-18747 (Pubitemid 350210767)
18. Yao, J., Taylor, M., Davey, F., Ren, Y., Aiton, J., Coote, P., Fang, F., Chen, J.X., Yan, S.D., and Gunn-Moore, F.J. (2007) Interaction of amyloid binding alcohol de-hydrogenase/Abeta mediates up-regulation of peroxire-doxin II in the brains of Alzheimer's disease patients and a transgenic Alzheimer's disease mouse model. Mol. Cell. Neurosci. 35, 377-382 (Pubitemid 46843572)
19. Qu, D., Rashidian, J., Mount, M.P., Aleyasin, H., Parsanejad, M., Lira, A., Haque, E., Zhang, Y., Callaghan, S., Daigle, M., Rousseaux, M.W., Slack, R.S., Albert, P.R., Vincent, I., and Woulfe, J.M. (2007) D.S. Park, Role of Cdk5-mediated phosphorylation of Prx2 in MPTP toxicity and Parkinson's disease. Neuron 55, 37-52 (Pubitemid 46990825)
20. Chae, H.Z., Uhm, T.B., and Rhee, S.G. (1994) Dimerization of thiol-specific antioxidant and the essen-tial role of cysteine 47. Proc. Natl. Acad. Sci. USA 91, 7022-7026 (Pubitemid 24226794)
21. Wood, Z.A., Schroder, E., Robin Harris, J., and Poole, L.B. (2003) Structure, mechanism and regulation of per-oxiredoxins. Trends Biochem. Sci. 28, 32-40
22. Watabe, S., Kohno, H., Kouyama, H., Hiroi, T., Yago, N., and Nakazawa, T. (1994) Purification and character-ization of a substrate protein for mitochondrial ATP-dependent protease in bovine adrenal cortex. J. Biochem. 115, 648-654 (Pubitemid 24119385)
23. Mitsumoto, A., Takanezawa, Y., Okawa, K., Iwamatsu, A., and Nakagawa, Y. (2001) Variants ofperoxiredoxins expression in response to hydroperoxide stress. Free Radic. Biol. Med. 30, 625-635 (Pubitemid 32280788)
24. Yang, K.S., Kang, S.W., Woo, H.A., Hwang, S.C., Chae, H.Z., Kim, K., and Rhee, S.G. (2002) Inactivation of human peroxiredoxin I during catalysis as the result of the oxidation of the catalytic site cysteine to cysteine-sulfinic acid. J. Biol. Chem. 277, 38029-38036 (Pubitemid 35154654)
25. Biteau, B., Labarre, J., and Toledano, M.B. (2003) ATP-dependent reduction of cysteine-sulphinic acid by S. cerevisiae sulphiredoxin. Nature 425, 980-984 (Pubitemid 37376931)
26. Chang, T.S., Jeong, W., Woo, H.A., Lee, S.M., Park, S., and Rhee, S.G. (2004) Characterization of mammalian sulfiredoxin and its reactivation of hyperoxidized perox-iredoxin through reduction of cysteine sulfinic acid in the active site to cysteine. J. Biol. Chem. 279, 50994-51001 (Pubitemid 40017840)
27. Rhee, S.G., Kang, S.W., Jeong, W., Chang, T.S., Yang, K.S., and Woo, H.A. (2005) Intracellular messenger function of hydrogen peroxide and its regulation by per-oxiredoxins. Curr. Opin. Cell. Biol. 17, 183-189 (Pubitemid 40380942)
28. Jonsson, T.J., Johnson, L.C., and Lowther, W.T. (2008) Structure of the sulphiredoxin-peroxiredoxin complex reveals an essential repair embrace. Nature 451, 98-101
29. Woo, H.A., Chae, H.Z., Hwang, S.C., Yang, K.S., Kang, S.W., Kim, K., and Rhee, S.G. (2003) Reversing the inactivation of peroxiredoxins caused by cysteine sul-finic acid formation. Science 300, 653-656 (Pubitemid 36520592)
30. Cox, A.G., Pearson, A.G., Pullar, J.M., Jonsson, T.J., Lowther, W.T., Winterbourn, C.C., and Hampton, M.B. (2009) Mitochondrial peroxiredoxin 3 is more resilient to hyperoxidation than cytoplasmic peroxiredoxins. Biochem. J. 421, 51-58
31. Bae, S.H., Woo, H.A., Sung, S.H., Lee, H.E., Lee, S.K., Kil, I.S., and Rhee, S.G. (2009) Induction of sulfiredoxin via an Nrf2-dependent pathway and hyperoxidation of peroxiredoxin III in the lungs of mice exposed to hyper-oxia. Antioxid. Redox Signal. 11, 937-948
32. 2-de-pendent hyperoxidation of peroxiredoxin 6 (Prdx6) plays a role in cellular toxicity via up-regulation of iPLA2 activity. J. Biol. Chem. 283, 33563-33568
33. 2-induced cell death. J. Biol. Chem. 280, 28775-28784 (Pubitemid 41105779)
34. 2 produced during disulphide formation. J. Cell Sci. 123, 2672-2679
35. Wood, Z.A., Poole, L.B., and Karplus, P.A. (2003) Peroxiredoxin evolution and the regulation of hydrogen peroxide signaling. Science 300, 650-653 (Pubitemid 36520591)
36. 2, a necessary evil for cell signaling. Science 312, 1882-1883 (Pubitemid 43993698)
37. Jara, M., Vivancos, A.P., and Hidalgo, E. (2008) C-terminal truncation of the peroxiredoxin Tpx1 de-creases its sensitivity for hydrogen peroxide without compromising its role in signal transduction. Genes Cells 13, 171-179 (Pubitemid 351188987)
38. Koo, K.H., Lee, S., Jeong, S.Y., Kim, E.T., Kim, H.J., Kim, K., Song, K., and Chae, H.Z. (2002) Regulation of thioredoxin peroxidase activity by C-terminal truncation. Arch. Biochem. Biophys. 397, 312-318 (Pubitemid 34852297)
39. Okado-Matsumoto, A., Matsumoto, A., Fujii, J., and Taniguchi, N. (2000) Peroxiredoxin IV is a secretable protein with heparin-binding properties under reduced conditions. J. Biochem. 127, 493-501 (Pubitemid 30185255)
40. Tavender, T.J., Sheppard, A.M., and Bulleid, N.J. (2008) Peroxiredoxin IV is an endoplasmic reticulum-localized enzyme forming oligomeric complexes in human cells. Biochem. J. 411, 191-199 (Pubitemid 351482361)
41. Ikeda, Y., Ito, R., Ihara, H., Okada, T., and Fujii, J. (2010) Expression of N-terminally truncated forms of rat peroxiredoxin-4 in insect cells. Protein Expr. Purif. 72, 1-7
42. Matsumoto, A., Okado, A., Fujii, T., Fujii, J., Egashira, M., Niikawa, N., and Taniguchi, N. (1999) Cloning of the peroxiredoxin gene family in rats and characteriza-tion of the fourth member. FEBS Lett. 443, 246-250 (Pubitemid 29080804)
43. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685
44. Manta, B., Hugo, M., Ortiz, C., Ferrer-Sueta, G., Trujillo, M., and Denicola, A. (2009) The peroxidase and peroxynitrite reductase activity of human erythro-cyte peroxiredoxin 2. Arch. Biochem. Biophys. 484, 146-154
45. Lee, C.K., Kim, H.J., Lee, Y.R., So, H.H., Park, H.J., Won, K.J., Park, T., Lee, K.Y., Lee, H.M., and Kim, B. (2007) Analysis of peroxiredoxin decreasing oxidative stress in hypertensive aortic smooth muscle. Biochim. Biophys. Acta 1774, 848-855 (Pubitemid 46977838)
46. Lim, J.C., Choi, H.I., Park, Y.S., Nam, H.W., Woo, H.A., Kwon, K.S., Kim, Y.S., Rhee, S.G., Kim, K., and Chae, H.Z. (2008) Irreversible oxidation of the active-site cysteine of peroxiredoxin to cysteine sulfonic acid for enhanced molecular chaperone activity. J. Biol. Chem. 283, 28873-28880
47. Bertolotti, M., Yim, S.H., Garcia-Manteiga, J.M., Masciarelli, S., Kim, Y.J., Kang, M.H., Iuchi, Y., Fujii, J., Vene, R., Rubartelli, A., Rhee, S.G., and Sitia, R. (2010) B-to plasma-cell terminal differentiation entails oxidative stress and profound reshaping of the antioxidant responses. Antioxid. Redox Signal. 13, 1133-1144
48. Iuchi, Y., Okada, F., Tsunoda, S., Kibe, N., Shirasawa, N., Ikawa, M., Okabe, M., Ikeda, Y., and Fujii, J. (2009) Peroxiredoxin 4 knockout results in elevated spermato-genic cell death via oxidative stress. Biochem. J. 419, 149-158
49. van Anken, E., Romijn, E.P., Maggioni, C., Mezghrani, A., Sitia, R., Braakman, I., and Heck, A.J. (2003) Sequential waves of functionally related proteins are ex-pressed when B cells prepare for antibody secretion. Immunity 18, 243-253 (Pubitemid 36262999)
50. Enyedi, B., Varnai, P., and Geiszt, M. (2010) Redox state of the endoplasmic reticulum is controlled by Ero1L-alpha and intraluminal calcium. Antioxid. Redox Signal. 13, 721-729