Structural Changes Common to Catalysis in the Tpx Peroxiredoxin Subfamily

Journal of Molecular Biology

Volumn 393, Issue 4, 2009, Pages 867-881

  Hall, Andrea ^a   Sankaran, Banumathi ^b   Poole, Leslie B ^c   Karplus, P Andrew ^a  

^a OREGON STATE UNIVERSITY   (United States)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^c WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

antioxidant; peroxiredoxin; structural transitions; thiol peroxidase; Tpx

Indexed keywords

HOMODIMER; PEROXIREDOXIN; THIOL PEROXIDASE; UNCLASSIFIED DRUG;

ALPHA HELIX; ARTICLE; BINDING SITE; CATALYSIS; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; DISULFIDE BOND; ENZYME ACTIVE SITE; ESCHERICHIA COLI; HYDROPHOBICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; SEQUENCE ANALYSIS; STRUCTURE ANALYSIS;

ESCHERICHIA COLI;

AMINO ACID SEQUENCE; CATALYSIS; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; ISOENZYMES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PERIPLASMIC PROTEINS; PEROXIDASES; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 70349840614     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2009.08.040     Document Type: Article

References (52)

1. Wood Z.A., Schroder E., Harris J.R., and Poole L.B. Structure, mechanism and regulation of peroxiredoxins. Trends Biochem. Sci. 28 (2003) 32-40
2. Bryk R., Griffin P., and Nathan C. Peroxynitrite reductase activity of bacterial peroxiredoxins. Nature 407 (2000) 211-215
3. Flohé L., Budde H., and Hofmann B. Peroxiredoxins in antioxidant defense and redox regulation. Biofactors 19 (2003) 3-10
4. Cha M.K., Kim H.K., and Kim I.H. Thioredoxin-linked "thiol peroxidase" from periplasmic space of Escherichia coli. J. Biol. Chem. 270 (1995) 28635-28641
5. Atack J.M., Harvey P., Jones M.A., and Kelly D.J. The Campylobacter jejuni thiol peroxidases Tpx and Bcp both contribute to aerotolerance and peroxide-mediated stress resistance but have distinct substrate specificities. J. Bacteriol. 190 (2008) 5279-5290
6. Cha M.K., Kim W.C., Lim C.J., Kim K., and Kim I.H. Escherichia coli periplasmic thiol peroxidase acts as lipid hydroperoxide peroxidase and the principal antioxidative function during anaerobic growth. J. Biol. Chem. 279 (2004) 8769-8778
7. Olczak A.A., Seyler Jr. R.W., Olson J.W., and Maier R.J. Association of Helicobacter pylori antioxidant activities with host colonization proficiency. Infect. Immun. 71 (2003) 580-583
8. Rho B.S., Hung L.W., Holton J.M., Vigil D., Kim S.I., Park M.S., et al. Functional and structural characterization of a thiol peroxidase from Mycobacterium tuberculosis. J. Mol. Biol. 361 (2006) 850-863
9. Karplus P.A., and Hall A. Structural survey of the peroxiredoxins. In: Flohé L., and Harris J.R. (Eds). Peroxiredoxin Systems (2007), Springer, New York, NY 41-60
10. Knoops B., Loumaye E., and Van Der Eecken V. Evolution of the peroxiredoxins. In: Flohé L., and Harris J.R. (Eds). Peroxiredoxin Systems (2007), Springer, New York, NY 27-40
11. Hofmann B., Hecht H.J., and Flohe L. Peroxiredoxins. Biol. Chem. 383 (2002) 347-364
12. Wan X.Y., Zhou Y., Yan Z.Y., Wang H.L., Hou Y.D., and Jin D.Y. Scavengase p20: a novel family of bacterial antioxidant enzymes. FEBS Lett. 407 (1997) 32-36
13. Link A.J., Robison K., and Church G.M. Comparing the predicted and observed properties of proteins encoded in the genome of Escherichia coli K-12. Electrophoresis 18 (1997) 1259-1313
14. Tao K. Subcellular localization and in vivo oxidation-reduction kinetics of thiol peroxidase in Escherichia coli. FEMS Microbiol. Lett. 289 (2008) 41-45
15. Baker L.M., and Poole L.B. Catalytic mechanism of thiol peroxidase from Escherichia coli. Sulfenic acid formation and overoxidation of essential CYS61. J. Biol. Chem. 278 (2003) 9203-9211
16. Dubbs J.M., and Mongkolsuk S. Peroxiredoxins in bacterial antioxidant defense. In: Flohé L., and Harris J.R. (Eds). Peroxiredoxin Systems (2007), Springer, New York, NY 143-193
17. Jaeger T., Budde H., Flohé L., Menge U., Singh M., Trujillo M., and Radi R. Multiple thioredoxin-mediated routes to detoxify hydroperoxides in Mycobacterium tuberculosis. Arch. Biochem. Biophys. 423 (2004) 182-191
18. Choi J., Choi S., Cha M.K., Kim I.H., and 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. 278 (2003) 49478-49486
19. Zhou Y., Wan X.Y., Wang H.L., Yan Z.Y., Hou Y.D., and Jin D.Y. Bacterial scavengase p20 is structurally and functionally related to peroxiredoxins. Biochem. Biophys. Res. Commun. 233 (1997) 848-852
20. Sarma G.N., Nickel C., Rahlfs S., Fischer M., Becker K., and Karplus P.A. Crystal structure of a novel Plasmodium falciparum 1-Cys peroxiredoxin. J. Mol. Biol. 346 (2005) 1021-1034
21. Stehr M., Hecht H.J., Jager T., Flohe L., and Singh M. Structure of the inactive variant C60S of Mycobacterium tuberculosis thiol peroxidase. Acta Crystallogr., Sect. D: Biol. Crystallogr. 62 (2006) 563-567
22. Lu J., Yang F., Li Y., Zhang X., Xia B., and Jin C. Reversible conformational switch revealed by the redox structures of Bacillus subtilis thiol peroxidase. Biochem. Biophys. Res. Commun. 373 (2008) 414-418
23. Diederichs K., and Karplus P.A. Improved R-factors for diffraction data analysis in macromolecular crystallography. Nat. Struct. Biol. 4 (1997) 269-275
24. Weiss M.S., and Hilgenfeld R. On the use of the merging R factor as a quality indicator for X-ray data. J. Appl. Crystallogr. 30 (1997) 203-205
25. Davis I.W., Leaver-Fay A., Chen V.B., Block J.N., Kapral G.J., Wang X., et al. MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res. 35 (2007) W375-W383
26. Burmeister W.P. Structural changes in a cryo-cooled protein crystal owing to radiation damage. Acta Crystallogr., Sect. D: Biol. Crystallogr. 56 (2000) 328-341
27. Ravelli R.B., and Garman E.F. Radiation damage in macromolecular cryocrystallography. Curr. Opin. Struct. Biol. 16 (2006) 624-629
28. Ravelli R.B., and McSweeney S.M. The 'fingerprint' that X-rays can leave on structures. Structure 8 (2000) 315-328
29. Weik M., Ravelli R.B., Kryger G., McSweeney S., Raves M.L., Harel M., et al. Specific chemical and structural damage to proteins produced by synchrotron radiation. Proc. Natl Acad. Sci. USA 97 (2000) 623-628
30. Declercq J.P., Evrard C., Clippe A., Stricht D.V., Bernard A., and Knoops B. Crystal structure of human peroxiredoxin 5, a novel type of mammalian peroxiredoxin at 1.5 Å resolution. J. Mol. Biol. 311 (2001) 751-759
31. Smeets A., Loumaye E., Clippe A., Rees J.F., Knoops B., and Declercq J.P. The crystal structure of the C45S mutant of annelid Arenicola marina peroxiredoxin 6 supports its assignment to the mechanistically typical 2-Cys subfamily without any formation of toroid-shaped decamers. Protein Sci. 17 (2008) 700-710
32. Evrard C., Capron A., Marchand C., Clippe A., Wattiez R., Soumillion P., et al. Crystal structure of a dimeric oxidized form of human peroxiredoxin 5. J. Mol. Biol. 337 (2004) 1079-1090
33. Evrard C., Smeets A., Knoops B., and Declercq J.P. Crystal structure of the C47S mutant of human peroxiredoxin 5. J. Chem. Cryst. 34 (2004) 553-558
34. Nakamura T., Yamamoto T., Inoue T., Matsumura H., Kobayashi A., Hagihara Y., et al. Crystal structure of thioredoxin peroxidase from aerobic hyperthermophilic archaeon Aeropyrum pernix K1. Proteins 62 (2006) 822-826
35. Trujillo M., Mauri P., Benazzi L., Comini M., De Palma A., Flohe L., et al. The mycobacterial thioredoxin peroxidase can act as a one-cysteine peroxiredoxin. J. Biol. Chem. 281 (2006) 20555-20566
36. Wood Z.A., Poole L.B., Hantgan R.R., and Karplus P.A. Dimers to doughnuts: redox-sensitive oligomerization of 2-cysteine peroxiredoxins. Biochemistry 41 (2002) 5493-5504
37. Leslie A.G.W. Recent changes to the MOSFLM package for processing film and image plate data. Joint CCP4 + ESF-EAMCB Newsletter on Protein Crystallography 26 (1992)
38. Evans P.R. Recent advances in phasing. Proceedings of the CCP4 Study Weekend (1997) 97-102
39. Otwinowski Z., and Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276 (1997) 307-326
40. Collaborative Computational Project, Number 4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr., Sect. D: Biol. Crystallogr. 50 (1994) 760-763
41. Vagin A., and Teplyakov A. MOLREP: an Automated Program for Molecular Replacement. J. Appl. Crystallogr. 30 (1997) 1022-1025
42. Emsley P., and Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr., Sect. D: Biol. Crystallogr. 60 (2004) 2126-2132
43. Murshudov G.N., Vagin A.A., and Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr., Sect. D: Biol. Crystallogr. 53 (1997) 240-255
44. Howlin B., Butler S.A., Moss D.S., Harris G.W., and Driessen H.P.C. TLSANL: TLS parameter-analysis program for segmented anisotropic refinement of macromolecular structures. J. Appl. Crystallogr. 26 (1993) 622-624
45. Kabsch W., and Sander C. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22 (1983) 2577-2637
46. Krebs W.G., and Gerstein M. The morph server: a standardized system for analyzing and visualizing macromolecular motions in a database framework. Nucleic Acids Res. 28 (2000) 1665-1675
47. Altschul S.F., Gish W., Miller W., Myers E.W., and Lipman D.J. Basic local alignment search tool. J. Mol. Biol. 215 (1990) 403-410
48. Thompson J.D., Higgins D.G., and Gibson T.J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22 (1994) 4673-4680
49. Landau M., Mayrose I., Rosenberg Y., Glaser F., Martz E., Pupko T., and Ben-Tal N. ConSurf 2005: the projection of evolutionary conservation scores of residues on protein structures. Nucleic Acids Res. 33 (2005) W299-W302
50. Crooks G.E., Hon G., Chandonia J.M., and Brenner S.E. WebLogo: a sequence logo generator. Genome Res. 14 (2004) 1188-1190
51. Rozwarski D.A., Gronenborn A.M., Clore G.M., Bazan J.F., Bohm A., Wlodawer A., et al. Structural comparisons among the short-chain helical cytokines. Structure 2 (1994) 159-173
52. DeLano W.L. The PyMOL Molecular Graphics System (2002), DeLano Scientific, San Carlos, CA