Structural snapshots of yeast alkyl hydroperoxide reductase Ahp1 peroxiredoxin reveal a novel two-cysteine mechanism of electron transfer to eliminate reactive oxygen species

Journal of Biological Chemistry

Volumn 287, Issue 21, 2012, Pages 17077-17087

  Lian, Fu Ming ^a   Yu, Jiang ^a   Xiao Xiao, Ma ^a   Yu, Xiao Jie ^a   Chen, Yuxing ^a   Zhou, Cong Zhao ^a  

^a UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ALKYL HYDROPEROXIDE; CATALYTIC CYCLES; CELLULAR SIGNALING; CONFORMATIONAL CHANGE; COOPERATIVITY; DIMER INTERFACE; DISULFIDE BONDS; ELECTRON TRANSFER; ENZYMATIC ASSAY; HIGHER EFFICIENCY; HILL COEFFICIENT; HOMODIMERS; HYDROPEROXIDES; INTERMOLECULAR DISULFIDE BOND; PEROXIDASE ACTIVITIES; PEROXIDATIC CYSTEINE; PEROXIREDOXINS; PRIMARY SEQUENCES; REACTIVE OXYGEN SPECIES; SITE DIRECTED MUTAGENESIS; STRUCTURAL INSIGHTS; STRUCTURAL SNAPSHOTS; STRUCTURAL SUPERPOSITIONS; T-BUTYL HYDROPEROXIDE; THIOREDOXINS;

BIOINFORMATICS; COVALENT BONDS; ELECTRON TRANSITIONS; ENZYME ACTIVITY; OXYGEN; PIGMENTS; PROTEINS;

AMINO ACIDS;

ALKYL HYDROPEROXIDE REDUCTASE 1; PEROXIREDOXIN; REACTIVE OXYGEN METABOLITE; THIOREDOXIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; DISULFIDE BOND; ELECTRON TRANSPORT; ENZYME ACTIVITY; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SITE DIRECTED MUTAGENESIS; STRUCTURE ANALYSIS;

BINDING SITES; CRYSTALLOGRAPHY, X-RAY; CYSTEINE; ELECTRON TRANSPORT; MULTIENZYME COMPLEXES; OXIDATION-REDUCTION; PEROXIREDOXINS; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; REACTIVE OXYGEN SPECIES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TERT-BUTYLHYDROPEROXIDE; THIOREDOXINS;

EID: 84861219003     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.357368     Document Type: Article

References (53)

1. 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)
2. Jacobson, F. S., Morgan, R. W., Christman, M. F., and Ames, B. N. (1989) An alkyl hydroperoxide reductase from Salmonella typhimurium involved in the defense of DNA against oxidative damage. Purification and properties. J. Biol. Chem. 264, 1488-1496
3. 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 (Pubitemid 36051004)
4. Winterbourn, C. C. (2008) Reconciling the chemistry and biology of reactive oxygen species. Nat. Chem. Biol. 4, 278-286
5. Veal, E. A., Day, A. M., and Morgan, B. A. (2007) Hydrogen peroxide sensing and signaling. Mol. Cell 26, 1-14 (Pubitemid 46578115)
6. Knoops, B., Loumaye, E., and Van Der Eecken, V. (2007) Evolution of the peroxiredoxins. Subcell. Biochem. 44, 27-40
7. Barranco-Medina, S., La'zaro, J. J., and Dietz, K. J. (2009) The oligomeric conformation of peroxiredoxins links redox state to function. FEBS Lett. 583, 1809-1816
8. Poole, L. B. (2007) The catalytic mechanism of peroxiredoxins. Subcell. Biochem. 44, 61-81
9. Hall, A., Karplus, P. A., and Poole, L. B. (2009) Typical 2-Cys peroxiredoxins-structures, mechanisms, and functions. FEBS J. 276, 2469-2477
10. Hall, A., Nelson, K., Poole, L. B., and Karplus, P. A. (2011) Structure-based insights into the catalytic power and conformational dexterity of peroxiredoxins. Antioxid. Redox Signal. 15, 795-815
11. Soito, L., Williamson, C., Knutson, S. T., Fetrow, J. S., Poole, L. B., and Nelson, K. J. (2011) PREX. PeroxiRedoxin classification indEX, a database of subfamily assignments across the diverse peroxiredoxin family. Nucleic Acids Res. 39, D332-D337
12. Seo, M. S., Kang, S. W., Kim, K., Baines, I. C., Lee, T. H., and Rhee, S. G. (2000) Identification of a new type of mammalian peroxiredoxin that forms an intramolecular disulfide as a reaction intermediate. J. Biol. Chem. 275, 20346-20354 (Pubitemid 30457609)
13. Manevich, Y., Feinstein, S. I., and Fisher, A. B. (2004) Activation of the antioxidant enzyme 1-CYS peroxiredoxin requires glutathionylation mediated by heterodimerization with pi GST. Proc. Natl. Acad. Sci. U.S.A. 101, 3780-3785 (Pubitemid 38381055)
14. Ralat, L. A., Manevich, Y., Fisher, A. B., and Colman, R. F. (2006) Direct evidence for the formation of a complex between 1-cysteine peroxiredoxin and glutathione S-transferase π with activity changes in both enzymes. Biochemistry 45, 360-372 (Pubitemid 43100403)
15. Biteau, B., Labarre, J., and Toledano, M. B. (2003) ATP-dependent reduction of cysteine-sulphinic acid by S. cerevisiae sulfiredoxin. Nature 425, 980-984 (Pubitemid 37376931)
16. Budanov, A. V., Sablina, A. A., Feinstein, E., Koonin, E. V., and Chumakov, P. M. (2004) Regeneration of peroxiredoxins by p53-regulated sestrins, homologs of bacterial AhpD. Science 304, 596-600 (Pubitemid 38541920)
17. Jönsson, T. J., and Lowther, W. T. (2007) The peroxiredoxin repair proteins. Subcell. Biochem. 44, 115-141
18. 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 peroxiredoxin through reduction of cysteine sulfinic acid in the active site to cysteine. J. Biol. Chem. 279, 50994-51001 (Pubitemid 40017840)
19. 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
20. 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 (Pubitemid 44878510)
21. Klomsiri, C., Karplus, P. A., and Poole, L. B. (2011) Cysteine-based redox switches in enzymes. Antioxid. Redox Signal. 14, 1065-1077
22. 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 (Pubitemid 38692528)
23. Chuang, M. H., Wu, M. S., Lo, W. L., Lin, J. T., Wong, C. H., and Chiou, S. H. (2006) The antioxidant protein alkylhydroperoxide reductase of Helicobacter pylori switches from a peroxide reductase to a molecular chaperone function. Proc. Natl. Acad. Sci. U.S.A. 103, 2552-2557
24. D'Autréaux, B., and Toledano, M. B. (2007) ROS as signaling molecules. Mechanisms that generate specificity in ROS homeostasis. Nat. Rev. Mol. Cell Biol. 8, 813-824 (Pubitemid 47462134)
25. Wong, C. M., Siu, K. L., and Jin, D. Y. (2004) Peroxiredoxin-null yeast cells are hypersensitive to oxidative stress and are genomically unstable. J. Biol. Chem. 279, 23207-23213
26. Jeong, J. S., Kwon, S. J., Kang, S. W., Rhee, S. G., and Kim, K. (1999) Purification and characterization of a second type thioredoxin peroxidase (type II TPx) from Saccharomyces cerevisiae. Biochemistry 38, 776-783
27. Lee, J., Spector, D., Godon, C., Labarre, J., and Toledano, M. B. (1999) A new antioxidant with alkyl hydroperoxide defense properties in yeast. J. Biol. Chem. 274, 4537-4544
28. Park, S. G., Cha, M. K., Jeong, W., and Kim, I. H. (2000) Distinct physiological functions of thiol peroxidase isoenzymes in Saccharomyces cerevisiae. J. Biol. Chem. 275, 5723-5732 (Pubitemid 30115214)
29. Iwai, K., Naganuma, A., and Kuge, S. (2010) Peroxiredoxin Ahp1 acts as a receptor for alkylhydroperoxides to induce disulfide bond formation in the Cad1 transcription factor. J. Biol. Chem. 285, 10597-10604
30. Goehring, A. S., Rivers, D. M., and Sprague, G. F., Jr. (2003) Attachment of the ubiquitin-related protein Urm1p to the antioxidant protein Ahp1p. Eukaryot. Cell 2, 930-936 (Pubitemid 37298706)
31. Van der Veen, A. G., Schorpp, K., Schlieker, C., Buti, L., Damon, J. R., Spooner, E., Ploegh, H. L., and Jentsch, S. (2011) Role of the ubiquitin-like protein Urm1 as a noncanonical lysine-directed protein modifier. Proc. Natl. Acad. Sci. U.S.A. 108, 1763-1770
32. Choi, H. J., Kang, S. W., Yang, C. H., Rhee, S. G., and Ryu, S. E. (1998) Crystal structure of a novel human peroxidase enzyme at 2.0 Å resolution. Nat. Struct. Biol. 5, 400-406 (Pubitemid 28211179)
33. Karplus, P. A., and Hall, A. (2007) Structural survey of the peroxiredoxins. Subcell. Biochem. 44, 41-60
34. Parsonage, D., Youngblood, D. S., Sarma, G. N., Wood, Z. A., Karplus, P. A., and Poole, L. B. (2005) Analysis of the link between enzymatic activity and oligomeric state in AhpC, a bacterial peroxiredoxin. Biochemistry 44, 10583-10592 (Pubitemid 41098235)
35. Kang, S. W., Baines, I. C., and Rhee, S. G. (1998) Characterization of a mammalian peroxiredoxin that contains one conserved cysteine. J. Biol. Chem. 273, 6303-6311 (Pubitemid 28144720)
36. Bao, R., Chen, Y., Tang, Y. J., Janin, J., and Zhou, C. Z. (2007) Crystal structure of the yeast cytoplasmic thioredoxin Trx2. Proteins 66, 246-249 (Pubitemid 44955996)
37. Zhang, Z., Bao, R., Zhang, Y., Yu, J., Zhou, C. Z., and Chen, Y. (2009) Crystal structure of Saccharomyces cerevisiae cytoplasmic thioredoxin reductase Trr1 reveals the structural basis for species-specific recognition of thioredoxin. Biochim. Biophys. Acta 1794, 124-128
38. Wang, P. F., Veine, D. M., Ahn, S. H., and Williams, C. H., Jr. (1996) A stable mixed disulfide between thioredoxin reductase and its substrate, thioredoxin. Preparation and characterization. Biochemistry 35, 4812-4819 (Pubitemid 26126699)
39. Ma, X. X., Guo, P. C., Shi, W. W., Luo, M., Tan, X. F., Chen, Y., and Zhou, C. Z. (2011) Structural plasticity of the thioredoxin recognition site of yeast methionine S-sulfoxide reductase Mxr1. J. Biol. Chem. 286, 13430-13437
40. Otwinowski, Z., and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (Pubitemid 27085611)
41. Vagin, A., and Teplyakov, A. (2010) Molecular replacement with MOLREP. Acta Crystallogr. D Biol. Crystallogr. 66, 22-25
42. Collaborative Computational Project, Number 4 (1994) The CCP4 suite. Programs for protein crystallography. Acta Crystallogr. D. Biol. Crystallogr. 50, 760-763
43. Echalier, A., Trivelli, X., Corbier, C., Rouhier, N., Walker, O., Tsan, P., Jacquot, J. P., Aubry, A., Krimm, I., and Lancelin, J. M. (2005) Crystal structure and solution NMR dynamics of a D (type II) peroxiredoxin glutaredoxin and thioredoxin-dependent. A new insight into the peroxiredoxin oligomerism. Biochemistry 44, 1755-1767 (Pubitemid 40223608)
44. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D. Biol. Crystallogr. 53, 240-255 (Pubitemid 27235885)
45. Emsley, P., and Cowtan, K. (2004) Coot. Model-building tools for molecular graphics. Acta Crystallogr. D. Biol. Crystallogr. 60, 2126-2132 (Pubitemid 41742764)
46. Chen, V. B., Arendall, W. B., 3rd, Headd, J. J., Keedy, D. A., Immormino, R. M., Kapral, G. J., Murray, L. W., Richardson, J. S., and Richardson, D. C. (2010) MolProbity. All-atom structure validation for macromolecular crystallography. Acta Crystallogr. D. Biol. Crystallogr. 66, 12-21
47. Laskowski, R. A., MacArthur, M. W., Moss, D. S., and Thornton, J. M. (1993) Procheck. A program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26, 283-291
48. DeLano, W. L. (2002) The PyMOL Molecular Graphics System, Version 0.99rc2, DeLano Scientific, Palo Alto, CA
49. Trivelli, X., Krimm, I., Ebel, C., Verdoucq, L., Prouzet-Mauléon, V., Chartier, Y., Tsan, P., Lauquin, G., Meyer, Y., and Lancelin, J. M. (2003) Characterization of the yeast peroxiredoxin Ahp1 in its reduced active and overoxidized inactive forms using NMR. Biochemistry 42, 14139-14149 (Pubitemid 37499410)
50. Janin, J., Bahadur, R. P., and Chakrabarti, P. (2008) Protein-protein interaction and quaternary structure. Q. Rev. Biophys. 41, 133-180
51. de Vries, S. J., van Dijk, M., and Bonvin, A. M. (2010) The HADDOCK web server for data-driven biomolecular docking. Nat. Protoc. 5, 883-897
52. Corpet, F. (1988) Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res. 16, 10881-10890
53. Gouet, P., Robert, X., and Courcelle, E. (2003) ESPript/ENDscript. Extracting and rendering sequence and 3D information from atomic structures of proteins. Nucleic Acids Res. 31, 3320-3323 (Pubitemid 37442149)