Insights into the catalytic mechanism of the Bcp family: Functional and structural analysis of Bcp1 from Sulfolobus solfataricus

Proteins: Structure, Function and Bioinformatics

Volumn 76, Issue 4, 2009, Pages 995-1006

  D'Ambrosio, Katia ^a   Limauro, Danila ^b   Pedone, Emilia ^a   Galdi, Ilaria ^b   Pedone, Carlo ^a   Bartolucci, Simonetta ^b   De Simone, Giuseppina ^a  

^a CNR   (Italy)

^b UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

Bacterioferritin comigratory protein; Crystal structure; Peroxiredoxin; Redox mechanism; Sulfolobus solfataricus

Indexed keywords

ARGININE; ASPARTIC ACID; BACTERIAL PROTEIN; CYSTEINE; PEROXIDASE; PROTEIN BCP1; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; DISULFIDE BOND; ENZYME ACTIVITY; ENZYME CONFORMATION; NONHUMAN; OXIDATION; PEROXIDATION; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN ISOLATION; PROTEIN MOTIF; REACTION ANALYSIS; STRUCTURE ANALYSIS; SULFOLOBUS SOLFATARICUS;

AMINO ACID SEQUENCE; ARCHAEAL PROTEINS; CRYSTALLOGRAPHY, X-RAY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; OXIDATION-REDUCTION; PEROXIREDOXINS; PROTEIN CONFORMATION; SEQUENCE ALIGNMENT; SULFOLOBUS SOLFATARICUS;

ARCHAEA; FUNGI; SULFOLOBUS SOLFATARICUS;

EID: 68149100376     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.22408     Document Type: Article

References (45)

1. Butterfield LH, Merino A, Golub SD, Shau H. From cytoprotection to tumor suppression: the multifactorial role of peroxiredoxins. Antioxid Redox Signal 1999;1:385-402. (Pubitemid 129628306)
2. Rhee SG, Kang SW, Chang TS, Jeong W, Kim K. Peroxiredoxins, a novel family of peroxidases. IUBMB Life 2001;52:35-41.
3. Fujii J, Ikeda Y. Advances in our understanding of peroxiredoxin, a multifunctional, mammalian redox protein. Redox Rep 2002;7:123-130. (Pubitemid 34700435)
4. Hofmann B, Hecht HJ, Flohé L. Peroxiredoxins. Biol Chem 2002; 383:347-364.
5. Wood ZA, Schröder E, Harris JR, Poole LB. Structure, mechanisms and regulation of peroxiredoxins. Trends Biochem Sci 2003;28:32-40.
6. Poole LB. The catalytic mechanism of peroxiredoxins. Subcell Biochem 2007;44:61-81.
7. Konig J, Baier M, Horling F, Kahmann U, Harris G, Schurmann P, Dietz KJ. 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 2002;99:5738-5743. (Pubitemid 34411620)
8. Neumann CA, Krause DS, Carman CV, Das S, Dubey DP, Abraham JL, Bronson RT, Fujiwara Y, Orkin SH, Van Etten RA. Essential role for the peroxiredoxin Prdx1 in erythrocyte antioxidant defence and tumour suppression. Nature 2003;424:561-565. (Pubitemid 36975778)
9. Limauro D, Pedone E, Pirone L, Bartolucci S. Identification and characterization of 1-Cys peroxiredoxin from Sulfolobus solfataricus and its involvement in the response to oxidative stress. FEBS J 2006;273:721-731.
10. Sherman DR, Mdluli K, Hickey MJ, Arain TM, Morris SL, Barry III CE, Stover CK. Compensatory AhpC gene expression in isoniazid-resistant Mycobacterium tuberculosis. Science 1996;272:1641-1643. (Pubitemid 26200020)
11. Park SH, Chung YM, Lee YS, Kim HJ, Kim JS, Chae HZ, Yoo YD. Antisense of human peroxiredoxin II enhances radiation-induced cell death. Clin Cancer Res 2000;6:4915-4920.
12. Chung YM, Yoo YD, Park JK, Kim YT, Kim HJ. Increased expression of peroxiredoxin II confers resistance to cisplatin. Anticancer Res 2001;21:1129-1133.
13. Choi MH, Lee IK, Kim GW, Kim BU, Han YH, Yu DY, Park HS, Kim KY, Lee JS, Choi C, Bae YS, Lee BI, Rhee SG, Kang SW. Regulation of PDGF- signaling and vascular remodeling by peroxiredoxin II. Nature 2005;435:347-353. (Pubitemid 40745544)
14. 2-sensing by the antioxidant Pap1 pathway. Proc Natl Acad Sci USA 2005;102:8875-8880.
15. Limauro D, Pedone E, Galdi I, Bartolucci S. Peroxiredoxins as cellular guardians in Sulfolobus solfataricus - characterization of Bcp1, Bcp3 and Bcp4. FEBS J 2008;275:2067-2077. (Pubitemid 351569548)
16. Monteiro G, Horta BB, Pimenta DC, Augusto O, Netto LE. Reduction of 1-Cys peroxiredoxins by ascorbate changes the thiol-specific antioxidant paradigm, revealing another function of vitamin C. Proc Natl Acad Sci USA 2007;104:4886-4891. (Pubitemid 47186146)
17. Mizohata E, Sakai H, Fusatomi E, Terada T, Murayama K, Shirouzu M, Yokoyama S. Crystal structure of an archaeal peroxiredoxin from the aerobic hyperthermophilic crenarchaeon Aeropyrum pernix K1. J Mol Biol 2005;354:317-329. (Pubitemid 41579849)
18. Li S, Peterson NA, Kim MY, Kim CY, Hung LW, Yu M, Lekin T, Segelke BW, Lott JS, Baker EN. Crystal structure of AhpE from Mycobacterium tuberculosis, a 1-Cys peroxiredoxin. J Mol Biol 2005; 346:1035-1046. (Pubitemid 40215528)
19. Wood ZA, Poole LB, Hantgan RR, Karplus PA. Dimers to doughnuts: redox-sensitive oligomerization of 2-cysteine peroxiredoxins. Biochemistry 2002;41:5493-5504.
20. Wood ZA, Poole LB Karplus PA. Peroxiredoxin evolution and the regulation of hydrogen peroxide signaling. Science 2003;300:650-653. (Pubitemid 36520591)
21. Jeong W, Cha MK, Kim IH. Thioredoxin-dependent hydroperoxide peroxidase activity of bacterioferritin comigratory protein (BCP) as a new member of the thiol-specific antioxidant protein (TSA)/alkyl hydroperoxide peroxidase C (AhpC) family. J Biol Chem 2000;275: 2924-2930. (Pubitemid 30082068)
22. Wakita M, Masuda S, Motohashi K, Hisabori T, Ohta H, Takamiya K. The significance of type II and PrxQ peroxiredoxins for antioxidative stress response in the purple bacterium Rhodobacter sphaeroides. J Biol Chem 2007;282:27792-27801. (Pubitemid 47529504)
23. Rouhier N, Gelhaye E, Gualberto JM, Jordy MN, De Fay E, Hirasawa M, Duplessis S, Lemaire SD, Frey P, Martin F, Manieri W, Knaff DB, Jacquot JP. Poplar peroxiredoxin Q. A thioredoxin-linked chloroplast antioxidant functional in pathogen defense. Plant Physiol 2004;134:1027-1038.
24. Choi J, Choi S, Chon JK, Choi J, Cha MK, Kim IH, Shin W. Crystal structure of the C107S/C112S mutant of yeast nuclear 2-Cys peroxiredoxin. Proteins 2005;61:1146-1149. (Pubitemid 41753187)
25. Choi J, Choi S, Choi J, Cha MK, Kim IH, Shin W. Crystal structure of Escherichia coli thiol peroxidase in the oxidized state: insights into intramolecular disulfide formation and substrate binding in atypical 2-Cys peroxiredoxins. J Biol Chem 2003;278:49478-54986
26. Kim SJ, Woo JR, Hwang YS, Jeong DG, Shin DH, Kim K, Ryu SE. The tetrameric structure of Haemophilus influenza hybrid Prx5 reveals interactions between electron donor and acceptor proteins. J Biol Chem 2003;278:10790-10798. (Pubitemid 36800352)
27. Evrard C, Capron A, Marchand C, Clippe A, Smeets A, Wattiez R, Soumillion P, Knoops B, Declercq JP. Crystal structure of a dimeric oxidized form of human peroxiredoxin 5. J Mol Biol 2004; 337: 1079-1090. (Pubitemid 38445052)
28. Kong W, Shiota S, Shi Y, Nakayama H, Nakayama K. A novel peroxiredoxin of the plant Sedum lineare is a homologue of Escherichia coli bacterioferritin co-migratory protein (Bcp). Biochem J 2000; 351:107-114. (Pubitemid 30781562)
29. Pedone E, Limauro D, D'Alterio R, Rossi M, Bartolucci S. Characterization of a multifunctional protein disulfide oxidoreductase from Sulfolobus solfataricus. FEBS J 2006;273:5407-5420. (Pubitemid 44772397)
30. Pedone E, Limauro D, Bartolucci S. The machinery for oxidative protein folding in thermophiles. Antioxid Redox Signal 2008;10: 157-170. (Pubitemid 350115988)
31. McPherson A. Current approaches to macromolecular crystallization. Eur J Biochem 1990;189:1-23.
32. Jancarik J, Kim SH. Sparse matrix sampling: a screening method for crystallisation of proteins. J Appl Crystallogr 1991;24: 409-411. (Pubitemid 21679358)
33. Cudney R, Patel S, Weisgraber K, Newhouse Y, McPherson A. Screening and optimization strategies for macromolecular crystal growth. Acta Crystallogr D 1994;50:414-423.
34. Otwinowsky Z, Minor W. Processing of X-Ray diffraction data collected in oscillation mode. Methods Enzymol 1997;276:307-326. (Pubitemid 27085611)
35. Brünger AT, Adams PD, Clore GM, DeLano WL, Gros P, Grosse-Kunsteleve RW, Jiang JS, Kuszewski J, Nilges M, Pannu NS, Read RJ, Rice LM, Simonson T, Warren GL. Crystallography and NMR system (CNS): a new software system for macromolecular structure determination. Acta Crystallogr D 1998;54:905-921. (Pubitemid 28443603)
36. Jones TA, Zou JY, Cowan SW, Kjeldgaard M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr A 1991;47: 110-119.
37. Laskowsky RA, MacArthur MW, Moss DS, Thornton JM. PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Crystallogr 1993;26:283-291.
38. Declercq JP, Evrard C, Clippe A, Vander Stricht D, Bernard A, Knoops B. Crystal structure of human peroxiredoxin 5, a novel type of mammalian peroxiredoxin at 1.5 Å resolution. J Mol Biol 2001;311:751-759. (Pubitemid 32803733)
39. Choi HJ, Kang SW, Yang CH, Rhee SG, Ryu SE. Crystal structure of a novel human peroxidase enzyme at 2.0 Å resolution. Nat Struct Biol 1998;5:400-406. (Pubitemid 28211179)
40. Hirotsu S, Abe Y, Okada K, Nagahara N, Hori H, Nishino TS, Hakoshima T. Crystal structure of a multifunctional 2-Cys peroxiredoxin heme-binding protein 23 kDa/proliferationassociated gene product. Proc Natl Acad Sci USA 1999;96:12333-12338. (Pubitemid 29513502)
41. Evrard C, Smeets A, Knoops B, Declercq JP. Crystal structure of the C47S mutant of human peroxiredoxin 5. J Chem Crystallogr 2004; 34:553-558. (Pubitemid 39237813)
42. Stehr M, Hecht JH, Jäger T, Flohé L, Singh M. Structure of the inactive variant C60S of Mycobacterium tuberculosis thiol peroxidase. Acta Crystallogr A 2006;62:563-567.
43. Sarma GN, Nickel C, Rahlfs S, Fischer M, Becker K, Karplus PA. Crystal structure of a novel Plasmodium falciparum 1-Cys peroxiredoxin. J Mol Biol 2005;346:1021-1034. (Pubitemid 40215527)
44. Latifi A, Ruiz M, Jeanjean R, Zhang CC. PrxQ-A, a member of the peroxiredoxin Q family, plays a major role in defense against oxidative stress in the cyanobacterium Anabaena sp. strain PCC7120. Free Radical Biol Med 2007;42:424-431. (Pubitemid 46038050)
45. Koh CS, Didierjean C, Navrot N, Panjikar S, Mulliert G, Rouhier N, Jacquot JP, Aubry A, Shawkataly O, Corbier C. Crystal structures of a poplar thioredoxin peroxidase that exhibits the structure of glutathione peroxidases: insights into redox-driven conformational changes. J Mol Biol 2007;370:512-529. (Pubitemid 46915399)