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Oxidative Stress-dependent Structural and Functional Regulation of 2-cysteine Peroxiredoxins In Eukaryotes Including Plant Cells

산화 스트레스에 의존한 식물 및 진핵세포 2-시스테인 퍼록시레독신의 기능 조절

  • Jang, Ho-Hee (Environmental Biotechnology, National Core Research Center) ;
  • Kim, Sun-Young (Division of Applied Life Sciences (BK21 Program), Gyeongsang National University) ;
  • Lee, Sang-Yeol (Division of Applied Life Sciences (BK21 Program), Gyeongsang National University)
  • 장호희 (환경생명과학 국가핵심연구센터) ;
  • 김선영 (경상대학교 응용생명과학부) ;
  • 이상열 (경상대학교 응용생명과학부)
  • Published : 2006.03.01

Abstract

Peroxiredoxins (Prxs) are ubiquitously distributed and play important functions in diverse cellular signaling systems. The proteins are largely classified into three groups, such as typical 2-Cys Prx, atypical 2-Cys Prx, and 1-Cys Prx, that are distinguished by their catalytic mechanisms and number of Cys residues. From the three classes of Prxs, the typical 2-Cys Prx containing the two-conserved Cys residues at its N-terminus and C-terminus catalyzes $H_2O_2$ with the use of thioredoxin (Trx) as an electron donor. During the catalytic cycle, the N-terminal Cys residue undergoes a peroxide-dependent oxidation to sulfenic acid, which can be further oxidized to sulfinic acid at the presence of high concentrations of $H_2O_2$ and a Trx system containing Trx, Trx reductase, and NADPH. The sulfinic acid form of 2-Cys Prx is reduced by the action of sulfiredoxin which requires ATP as an energy source. Under the strong oxidative or heat shock stress conditions, 2-Cys Prx in eukaryotes rapidly switches its protein structure from low-molecular-weight species to high-molecular-weight protein structures. In accordance with its structural changes, the protein concomitantly triggers functional switching from a peroxidase to a molecular chaperone, which can protect its substrate denaturation from external stress. In addition to its N-terminal active site, the C-terminal domain including 'YF-motif' of 2-Cys Prx plays a critical role in the structural changes. Therefore, the C-terminal truncated 2-Cys Prxs are not able to regulate their protein structures and highly resistant to $H_2O_2$-dependent hyperoxidation, suggesting that the reaction is guided by the peroxidatic Cys residue. Based on the results, it may be concluded that the peroxidatic Cys of 2-Cys Prx acts as an '$H_2O_2$-sensor' in the cells. The oxidative stress-dependent regulation of 2-Cys Prx provides a means of defense systems in cells to adapt stress conditions by activating intracellular defense signaling pathways. Particularly, 2-Cys Prxs in plants are localized in chloroplasts with a dynamic protein structure. The protein undergoes conformational changes again oxidative stress. Depending on a redox-potential of the chloroplasts, the plant 2-Cys Prx forms super-molecular weight protein structures, which attach to the thylakoid membranes in a reversible manner.

References

  1. Baier M, Dietz KJ (1997) The plant 2-Cys peroxiredoxin BAS1 is a nuclear-encoded chloroplast protein: its expressional regulation, phylogenetic origin, and implications for its specific physiological function in plants. Plant J 12: 179-190 https://doi.org/10.1046/j.1365-313X.1997.12010179.x
  2. Baier M, Dietz KJ (1999) Protective function of chloroplast 2-cysteine peroxiredoxin in photosynthesis. Evidence from transgenic Arabidopsis. Plant Physiol 119: 1407-1414 https://doi.org/10.1104/pp.119.4.1407
  3. Biteau B, Labarre J, Toledano MB (2003) ATP-dependent reduction of Cys-sulphinic acid by S. cerevisiae sulphiredoxin. Nature 425: 980-984 https://doi.org/10.1038/nature02075
  4. Broin M, Rey P (2003) Potato plants lacking the CDSP32 plastidic thioredoxin exhibit overoxidation of the BASl 2Cys peroxiredoxin and increased lipid peroxidation in thylakoids under photooxidative stress. Plant Physiol 132: 1335-1343 https://doi.org/10.1104/pp.103.021626
  5. Budanov AV, Sablina AA, Feinstein E, Koonin EV, Chumakov PM (2004) Regeneration of peroxiredoxins by p53-regulated sestrins, homologs of bacterial AhpD. Science 304: 596-600 https://doi.org/10.1126/science.1095569
  6. Burdon RH (1995) Superoxide and hydrogen peroxide in relation to mammalian cell proliferation. Free Radic Biol Med 18: 775-794 https://doi.org/10.1016/0891-5849(94)00198-S
  7. Butterfield DA, Yatin SM, Varadarajan S, Koppal T (1999) Amyloid beta-peptide-associated free radical oxidative stress, neurotoxicity, and Alzheimer's disease. Methods Enzymol 309: 746-768 https://doi.org/10.1016/S0076-6879(99)09050-3
  8. Cha MK, Yun CH, Kim IH (2000) Interaction of human thiol-specific antioxidant protein 1 with erythrocyte plasma membrane. Biochemistry 39: 6944-6950 https://doi.org/10.1021/bi000034j
  9. Chae HZ, Robison K, Poole LB, Church G, Storz G, Rhee SG (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
  10. Chang TS, Jeong W, Choi SY, Yu S, Kang SW, Rhee SG (2002) Regulation of peroxiredoxin I activity by Cdc2-mediated phosphorylation. J Biol Chem 277: 25370-25376 https://doi.org/10.1074/jbc.M110432200
  11. Chang TS, Jeong W, Woo HA, Lee SM, Park S, Rhee SG (2004) Characterization of mammalian sulfiredoxin and its reactivation of hyperoxidized peroxiredoxin through reduction of cysteine sulfinic acid in the active site to cysteine. J Biol Chem 279: 50994-51001 https://doi.org/10.1074/jbc.M409482200
  12. Cheong NE, Choi YO, Lee KO, Kim WY, Jung BG, Chi YH, Jeong JS, Kim K, Cho MJ, Lee SY (1999) Molecular cloning, expression, and functional characterization of a 2Cys-peroxiredoxin in Chinese cabbage. Plant Mol Biol 40: 825-834 https://doi.org/10.1023/A:1006271823973
  13. Choi YO, Cheong NE, Lee KO, Jung BG, Hong CH, Jeong JH, Chi YH, Kim K, Cho MJ, Lee SY (1999) Cloning and expression of a new isotype of the peroxiredoxin gene of Chinese cabbage and its comparison to 2Cys-peroxiredoxin isolated from the same plant. Biochem Biophys Res Commun 258: 768-771 https://doi.org/10.1006/bbrc.1999.0714
  14. Ellis HR, Poole LB (1997) Novel application of 7 -chloro4-nitrobenzo-2-oxa-l,3-diazole to identify Cys sulfenic acid in the AhpC component of alkyl hydroperoxide reductase. Biochemistry 36: 15013-15018 https://doi.org/10.1021/bi972191x
  15. Finkel T (2003) Oxidant signals and oxidative stress. Curr Opin Cell Biol 15: 247-254 https://doi.org/10.1016/S0955-0674(03)00002-4
  16. Finkel T, Holbrook NJ (2000) Oxidants, oxidative stress and the biology of ageing. Natrue 408: 239-247 https://doi.org/10.1038/35041687
  17. Fisher AB, Dodia C, Manevich Y, Chen JW, Feinstein SI (1999) Phospholipid hydroperoxides are substrates for non-selenium glutathione peroxidase. J Biol Chem 274: 21326-21334 https://doi.org/10.1074/jbc.274.30.21326
  18. Hendrick JP, Hartl FU (1993) Molecular chaperone functions of heat shock proteins. Annu Rev Biochem 62: 349-384 https://doi.org/10.1146/annurev.bi.62.070193.002025
  19. Hirotsu S, Abe Y, Okada K, Nagahara N, Hori H, Nishino T, Hakoshima T (1999) Crystal structure of a multifunctional 2-Cys peroxiredoxin heme-binding protein 23 kDa/ proliferation-associated gene product. Proc Natl Acad Sci USA 96: 12333-12338
  20. Jang HH, Lee KO, Chi YH, Jung BG, Park SK, Park JH, Lee JR, Lee SS, Moon JC, Yun JW, Choi YO, Kim WY, Kang JS, Cheong GW, Yun DJ, Rhee SG, Cho MJ, Lee SY (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
  21. Kim KS, Choi SY, Kwon HY, Won MH, Kang T-C, Kang JH (2002) Aggregation of $\alpha$ -synuclein induced by the Cu, Zn-superoxide dismutase and hydrogen peroxide system. Free Radic Biol Med 32: 544-550 https://doi.org/10.1016/S0891-5849(02)00741-4
  22. Konig J, Baier M, Horling F, Kahmann U, Harris G, Schurmann P, Dietz KJ (2002) The plant-specific function of 2-Cys peroxiredoxin-mediated detoxification of peroxides in the redox-hierarchy of photosynthetic electron flux. Proc Natl Acad Sci USA 99: 5738-5743
  23. Konig J, Lotte K, Plessow R, Brockhinke A, Baier M, Dietz KJ (2003) Reaction mechanism of plant 2-Cys peroxiredoxin. Role of the C terminus and the quaternary structure. J Biol Chem 278: 24409-24420 https://doi.org/10.1074/jbc.M301145200
  24. Koo KH, Lee S, Jeong SY, Kim ET, Kim HJ, Kim K, Song K, Chae HZ (2002) Regulation of thioredoxin peroxidase activity by C-terminal truncation. Arch Biochem Biophys 397: 312-318 https://doi.org/10.1006/abbi.2001.2700
  25. Lee KO, Jang HH, Jung BG, Chi YH, Lee JY, Choi YO, Lee JR, Urn CO, Cho MJ, Lee SY (2000) Rice lCys-peroxiredoxin over-expressed in transgenic tobacco does not maintain dormancy but enhances antioxidant activity. FEBS Lett 486: 103-106 https://doi.org/10.1016/S0014-5793(00)02230-4
  26. Martindale JL, Holbrook NJ (2002) Cellular response to oxidative stress: signaling for suicide and survival. J Cell Physiol 192: 1-15 https://doi.org/10.1002/jcp.10119
  27. Moon JC, Hah YS, Kim WY, Jung BG, Jang HH, Lee JR, Kim SY, Lee YM, Jeon MG, Kim CW, Cho MJ, Lee SY (2005) Oxidative stress-dependent structural and functional switching of a human 2-Cys peroxiredoxin isotype II that enhances HeLa cell resistance to $H_2O_2$-induced cell death. J Biol Chem 280: 28775-28784 https://doi.org/10.1074/jbc.M505362200
  28. Neumann CA, Krause DS, Carman CV, Das S, Dubey DP, Abraham JL, Bronson RT, Fujiwara Y, Orkin SH, van Etten RA (2003) Essential role for the peroxiredoxin Prdxl in erythrocyte antioxidant defence and tumour suppression. Nature 424: 561-565 https://doi.org/10.1038/nature01819
  29. Poole LB, Reynolds CM, Wood ZA, Karplus PA, Ellis HR, Li Calzi M (2000) AhpF and other NADH:peroxiredoxin oxidoreductases, homologues of low Mr thioredoxin reductase. Eur J Biochem 267: 6126-6133 https://doi.org/10.1046/j.1432-1327.2000.01704.x
  30. Quinn J, Findlay VJ, Dawson K, Millar JB, Jones N, Morgan BA, Toone WM (2002) Distinct regulatory proteins control the graded transcriptional response to increasing $H_2O_2$ levels in fission yeast Schizosaccharomyces pombe. Mol Biol Cell 13: 805-816 https://doi.org/10.1091/mbc.01-06-0288
  31. Rabilloud T, Heller M, Gasnier F, Luche S, Rey C, Aebersold R, Benahmed M, Louisot P, Lunardi J (2002) Proteomics analysis of cellular response to oxidative stress. Evidence for in vivo overoxidation of peroxiredoxins at their active site. J Biol Chem 277: 19396-19401 https://doi.org/10.1074/jbc.M106585200
  32. Rhee SG, Chae HZ, 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
  33. Rhee SG, Yang K-S, Kang SW, Woo HA, Chang T-S (2005b) Controlled elimination of intracellular $H_2O_2$: Regulation of peroxiredoxin, catalase, and glutathione peroxidase via post-translational modification. Antioxid Redox Signal 7: 619-626 https://doi.org/10.1089/ars.2005.7.619
  34. Sayed AA, Williams DL (2004) Biochemical characterization of 2-Cys peroxiredoxins from Schistosoma mansoni. J Biol Chem 279: 26159-26166 https://doi.org/10.1074/jbc.M401748200
  35. Schroder E, Panting CP (1998) Evidence that peroxiredoxins are novel members of the thioredoxin fold superfamily. Protein Sci 7: 2465-2468 https://doi.org/10.1002/pro.5560071125
  36. Schroder E, Littlechild JA, Lebedev M, Errington N, Vagin AA, lsupov MN (2000) Crystal structure of decameric 2-Cys peroxiredoxin from human erythrocytes at 1.7 A resolution. Structure Fold Des 8: 605-615 https://doi.org/10.1016/S0969-2126(00)00147-7
  37. Storz G, Tartaglia LA, Farr SB, Ames BN (1990) Bacterial defenses against oxidative stress. Trends Genet 6: 363-368 https://doi.org/10.1016/0168-9525(90)90278-E
  38. Sundaresan M, Yu ZX, Ferrans VJ, Irani K, Finkel T (1995) Requirement for generation of $H_2O_2$ for platelet-derived growth factor signal transduction. Science 270: 296-299 https://doi.org/10.1126/science.270.5234.296
  39. Ushio-Fukai M, Alexander RW, Akers M, Yin Q, Fujio Y, Walsh K, Griendling KK (1999) Reactive oxygen species mediate the activation of Akt/protein kinase B by angiotensin II in vascular smooth muscle cells. J Biol Chem 274: 22699-22704 https://doi.org/10.1074/jbc.274.32.22699
  40. Veal EA, Findlay VJ, Day AM, Bozonet SM, Evans JM, Quinn J, Morgan BA (2004) A 2-Cys peroxiredoxin regulates peroxide-induced oxidation and activation of a stressactivated MAP kinase. Mol Cell 15: 129-139 https://doi.org/10.1016/j.molcel.2004.06.021
  41. Vivancos AP, Castillo EA, Biteau B, Nicot C, Ayte J, Toledano MB, Hidalgo E (2005) A Cys-sulfinic acid in peroxiredoxin regulates $H_2O_2$-sensing by the antioxidant Pap 1 pathway. Proc Natl Acad Sci USA 102: 8875-8880
  42. Wood ZA, Schroder E, Robin Harris J, Poole LB (2003a) Structure, mechanism and regulation of peroxiredoxins. Trends Biochem Sci 28: 32-40 https://doi.org/10.1016/S0968-0004(02)00003-8
  43. Wood ZA, Poole LB, Karplus PA (2003b) Peroxiredoxin evolution and the regulation of hydrogen peroxide signaling. Science 300: 650-653 https://doi.org/10.1126/science.1080405
  44. Yang KS, Kang SW, Woo HA, Hwang SC, Chae HZ, Kim K, Rhee SG (2002) Inactivation of human peroxiredoxin I during catalysis as the result of the oxidation of the catalytic site Cys to Cys-sulfinic acid. J Biol Chem 277: 38029-38036 https://doi.org/10.1074/jbc.M206626200

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