Peroxiredoxin 1 functions as a signal peroxidase to receive, transduce, and transmit peroxide signals in mammalian cells

Free Radical Biology and Medicine

Volumn 53, Issue 7, 2012, Pages 1522-1530

  Jarvis, Reagan M ^a,b   Hughes, Stephanie M ^a   Ledgerwood, Elizabeth C ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

^b GERMAN CANCER RESEARCH CENTER   (Germany)

Author keywords

ASK1; Disulfide; H2O2; Peroxiredoxin; Redox signaling

Indexed keywords

HYDROGEN PEROXIDE; PEROXIREDOXIN 1; PEROXIREDOXIN 2; PEROXIREDOXIN 3; SYNAPTOPHYSIN;

ARTICLE; CYTOSOL; DISULFIDE BOND; ENZYME METABOLISM; GENE SILENCING; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

CELL LINE; DISULFIDES; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; HUMANS; HYDROGEN PEROXIDE; MACROPHAGES; MAP KINASE KINASE KINASE 5; OXIDATION-REDUCTION; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PEROXIREDOXIN III; PEROXIREDOXINS; PHOSPHORYLATION; SIGNAL TRANSDUCTION;

MAMMALIA;

EID: 84866357593     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2012.08.001     Document Type: Article

References (48)

1. C. Nathan Specificity of a third kind: reactive oxygen and nitrogen intermediates in cell signaling J. Clin. Invest 111 2003 769 778
2. Rudolph, T. K.; Freeman, B. A. Transduction of redox signaling by electrophile-protein reactions. Sci. Signaling 2:re7; 2009.
3. 2 scavenging and signaling Antioxid. Redox Signaling 10 2008 1565 1576
4. C.C. Winterbourn Reconciling the chemistry and biology of reactive oxygen species Nat. Chem. Biol. 4 2008 278 286
5. H.J. Forman, M. Maiorino, and F. Ursini Signaling functions of reactive oxygen species Biochemistry 49 2010 835 842
6. 2, and protein chaperones Antioxid. Redox Signaling 15 2011 781 794
7. A. Hall, P.A. Karplus, and L.B. Poole Typical 2-Cys peroxiredoxins - structures, mechanisms and functions FEBS J 276 2009 2469 2477
8. S.W. Kang, H.Z. Chae, M.S. Seo, K. Kim, I.C. Baines, and S.G. Rhee Mammalian peroxiredoxin isoforms can reduce hydrogen peroxide generated in response to growth factors and tumor necrosis factor-alpha J. Biol. Chem. 273 1998 6297 6302
9. Z.A. Wood, L.B. Poole, and P.A. Karplus Peroxiredoxin evolution and the regulation of hydrogen peroxide signaling Science 300 2003 650 653
10. 2-sensing by the antioxidant Pap1 pathway Proc. Natl. Acad. Sci. USA 102 2005 8875 8880
11. M. Jara, A.P. Vivancos, and E. Hidalgo C-terminal truncation of the peroxiredoxin Tpx1 decreases its sensitivity for hydrogen peroxide without compromising its role in signal transduction Genes Cells 13 2008 171 179
12. K.-S. Yang, S.W. Kang, H.A. Woo, S.C. Hwang, H.Z. Chae, K. Kim, and S.G. Rhee 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 2002 38029 38036
13. H.A. Woo, H.Z. Chae, S.C. Hwang, K.-S. Yang, S.W. Kang, K. Kim, and S.G. Rhee Reversing the inactivation of peroxiredoxins caused by cysteine sulfinic acid formation Science 300 2003 653 656
14. 2-induced cell death J. Biol. Chem. 280 2005 28775 28784
15. T.J. Phalen, K. Weirather, P.B. Deming, V. Anathy, A.K. Howe, A. van der Vliet, T.J. Jonsson, L.B. Poole, and N.H. Heintz Oxidation state governs structural transitions in peroxiredoxin II that correlate with cell cycle arrest and recovery J. Cell Biol. 175 2006 779 789
16. A.M. Day, J.D. Brown, S.R. Taylor, J.D. Rand, B.A. Morgan, and E.A. Veal Inactivation of a peroxiredoxin by hydrogen peroxide is critical for thioredoxin-mediated repair of oxidized proteins and cell survival Mol. Cell 45 2012 398 408
17. A.G. Cox, A.G. Pearson, J.M. Pullar, T.J. Jonsson, W.T. Lowther, C.C. Winterbourn, and M.B. Hampton Mitochondrial peroxiredoxin 3 is more resilient to hyperoxidation than cytoplasmic peroxiredoxins Biochem. J. 421 2009 51 58
18. C.C. Winterbourn, and D. Metodiewa Reactivity of biologically important thiol compounds with superoxide and hydrogen peroxide Free Radic. Biol. Med. 27 1999 322 328
19. 2 receptor and redox-transducer in gene activation Cell 111 2002 471 481
20. D.E. Fomenko, A. Koc, N. Agisheva, M. Jacobsen, A. Kaya, M. Malinouski, J.C. Rutherford, K.L. Siu, D.Y. Jin, D.R. Winge, and V.N. Gladyshev Thiol peroxidases mediate specific genome-wide regulation of gene expression in response to hydrogen peroxide Proc. Natl. Acad. Sci. USA 108 2011 2729 2734
21. E.A. Veal, V.J. Findlay, A.M. Day, S.M. Bozonet, J.M. Evans, J. Quinn, and B.A. Morgan A 2-Cys peroxiredoxin regulates peroxide-induced oxidation and activation of a stress-activated MAP kinase Mol. Cell 15 2004 129 139
22. T. Tachibana, S. Okazaki, A. Murayama, A. Naganuma, A. Nomoto, and S. Kuge A major peroxiredoxin-induced activation of Yap1 transcription factor is mediated by reduction-sensitive disulfide bonds and reveals a low level of transcriptional activation J. Biol. Chem 284 2009 4464 4472
23. K. Iwai, A. Naganuma, and S. Kuge Peroxiredoxin Ahp1 acts as a receptor for alkylhydroperoxides to induce disulfide bond formation in the Cad1 transcription factor J. Biol. Chem 285 2010 10597 10604
24. 2-terminal kinase activation and apoptosis Mol. Biol. Cell 18 2007 3903 3913
25. 2 J. Biol. Chem. 277 2002 20336 20342
26. Y. Jung, H. Kim, S.H. Min, S.G. Rhee, and W. Jeong Dynein light chain LC8 negatively regulates NF-κB through the redox-dependent interaction with IκBα J. Biol. Chem. 283 2008 23863 23871
27. Y. Yan, P. Sabharwal, M. Rao, and S. Sockanathan The antioxidant enzyme Prdx1 controls neuronal differentiation by thiol-redox-dependent activation of GDE2 Cell 138 2009 1209 1221
28. 2 involves KEAP1 disulfide formation J. Biol. Chem. 285 2010 8463 8471
29. H. Ichijo, E. Nishida, K. Irie, P. ten Dijke, M. Saitoh, T. Moriguchi, M. Takagi, K. Matsumoto, K. Miyazono, and Y. Gotoh Induction of apoptosis by ASK1, a mammalian MAPKKK that activates SAPK/JNK and p38 signaling pathways Science 275 1997 90 94
30. N.J. Adimora, D.P. Jones, and M.L. Kemp A model of redox kinetics implicates the thiol proteome in cellular hydrogen peroxide responses Antioxid. Redox Signaling 13 2010 731 743
31. 2 accumulation for cell signaling Cell 140 2010 517 528
32. J.P. Conway, and M. Kinter Dual role of peroxiredoxin I in macrophage-derived foam cells J. Biol. Chem. 281 2006 27991 28001
33. T.-S. Chang, W. Jeong, S.Y. Choi, S. Yu, S.W. Kang, and S.G. Rhee Regulation of peroxiredoxin I activity by Cdc2-mediated phosphorylation J. Biol. Chem. 277 2002 25370 25376
34. T. Zykova, F. Zhu, T. Vakorina, J. Zhang, L. Higgins, D. Urusova, A. Bode, and Z. Dong TOPK phosphorylation of Prx1 at Ser32 prevents UVB-induced apoptosis in RPMI7951 melanoma cells through the regulation of Prx1 peroxidase activity J. Biol. Chem. 285 2010 29138 29146
35. J. Cao, J. Schulte, A. Knight, N.R. Leslie, A. Zagozdzon, R. Bronson, Y. Manevich, C. Beeson, and C.A. Neumann Prdx1 inhibits tumorigenesis via regulating PTEN/AKT activity EMBO J 28 2009 1505 1517
36. R. Chang, and E. Wang Mouse translation elongation factor eEF1A-2 interacts with Prdx-I to protect cells against apoptotic death induced by oxidative stress J. Cell. Biochem 100 2007 267 278
37. S.-Y. Park, X. Yu, C. Ip, J.L. Mohler, P.N. Bogner, and Y.-M. Park Peroxiredoxin 1 interacts with androgen receptor and enhances its transactivation Cancer Res. 67 2007 9294 9303
38. 2-terminal kinase complex Cancer Res 66 2006 7136 7142
39. R.A. Egler, E. Fernandes, K. Rothermund, S. Sereika, N. de Souza-Pinto, P. Jaruga, M. Dizdaroglu, and E.V. Prochownik Regulation of reactive oxygen species, DNA damage, and c-Myc function by peroxiredoxin 1 Oncogene 24 2005 8038 8050
40. Z.M. Mu, X.Y. Yin, and E.V. Prochownik Pag, a putative tumor suppressor, interacts with the Myc Box II domain of c-Myc and selectively alters its biological function and target gene expression J. Biol. Chem 277 2002 43175 43184
41. S.T. Wen, and R.A. Van Etten 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 1997 2456 2467
42. A.M. Day, and E.A. Veal Hydrogen peroxide-sensitive cysteines in the Sty1 MAPK regulate the transcriptional response to oxidative stress J. Biol. Chem. 285 2010 7505 7516
43. S.M. Bozonet, V.J. Findlay, A.M. Day, J. Cameron, E.A. Veal, and B.A. Morgan Oxidation of a eukaryotic 2-Cys peroxiredoxin is a molecular switch controlling the transcriptional response to increasing levels of hydrogen peroxide J. Biol. Chem. 280 2005 23319 23327
44. S. Okazaki, A. Naganuma, and S. Kuge Peroxiredoxin-mediated redox regulation of the nuclear localization of Yap1, a transcription factor in budding yeast. Antioxid. Redox Signaling 7 2005 327s-334
45. E. Zito, E.P. Melo, Y. Yang, A. Wahlander, T.A. Neubert, and D. Ron Oxidative protein folding by an endoplasmic reticulum-localized peroxiredoxin Mol. Cell 40 2010 787 797
46. R.E. Rosenfield Jr, R. Parthasarathy, and J.D. Dunitz Directional preferences of nonbonded atomic contacts with divalent sulfur. 1. Electrophiles and nucleophiles J. Am. Chem. Soc. 99 1977 4860 4862
47. A.P. Wiita, R. Perez-Jimenez, K.A. Walther, F. Grater, B.J. Berne, A. Holmgren, J.M. Sanchez-Ruiz, and J.M. Fernandez Probing the chemistry of thioredoxin catalysis with force Nature 450 2007 124 127
48. H. Nishitoh, M. Saitoh, Y. Mochida, K. Takeda, H. Nakano, M. Rothe, K. Miyazono, and H. Ichijo ASK1 is essential for JNK/SAPK activation by TRAF2 Mol. Cell 2 1998 389 395