Dissecting peroxiredoxin catalysis: Separating binding, peroxidation, and resolution for a bacterial AhpC

Biochemistry

Volumn 54, Issue 7, 2015, Pages 1567-1575

  Parsonage, Derek ^a   Nelson, Kimberly J ^a   Ferrer Sueta, Gerardo ^b   Alley, Samantha ^a   Karplus, P Andrew ^c   Furdui, Cristina M ^a   Poole, Leslie B ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

^b UNIVERSIDAD DE LA REPÚBLICA   (Uruguay)

^c OREGON STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; COVALENT BONDS; ENZYMES; OXIDATION; RECYCLING; SALMONELLA; SULFUR COMPOUNDS;

CATALYTIC CYCLES; DISULFIDE BOND FORMATION; DISULFIDE BONDS; PEROXIDE REDUCTION; PEROXIREDOXINS; REVERSIBLE BINDING; SALMONELLA TYPHIMURIUM; STRUCTURAL REARRANGEMENT;

RATE CONSTANTS;

ALKYL HYDROPEROXIDE REDUCTASE C; BACTERIAL ENZYME; HYDROGEN PEROXIDE; HYDROPEROXIDE; PEROXIREDOXIN; THIOREDOXIN REDUCTASE; TRYPTOPHAN; UNCLASSIFIED DRUG; PROTEIN BINDING;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CHEMICAL BINDING; CHEMICAL REACTION KINETICS; CONFORMATIONAL TRANSITION; ELECTRON TRANSPORT; MYCOBACTERIUM TUBERCULOSIS; OXIDATION REDUCTION POTENTIAL; PEROXIDATION; PRIORITY JOURNAL; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM; STEADY STATE; CHEMICAL STRUCTURE; ENZYME SPECIFICITY; ENZYMOLOGY; KINETICS; METABOLISM; OXIDATION REDUCTION REACTION;

BACTERIA (MICROORGANISMS); SALMONELLA TYPHIMURIUM;

HYDROGEN PEROXIDE; KINETICS; MODELS, MOLECULAR; OXIDATION-REDUCTION; PEROXIREDOXINS; PROTEIN BINDING; SALMONELLA TYPHIMURIUM; SUBSTRATE SPECIFICITY;

EID: 84923342260     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi501515w     Document Type: Article

References (45)

1. Trujillo, M., Clippe, A., Manta, B., Ferrer-Sueta, G., Smeets, A., Declercq, J. P., Knoops, B., and Radi, R. (2007) Pre-steady state kinetic characterization of human peroxiredoxin 5: Taking advantage of Trp84 fluorescence increase upon oxidation Arch. Biochem. Biophys. 467, 95-106
2. Trujillo, M., Mauri, P., Benazzi, L., Comini, M., De Palma, A., Flohe, L., Radi, R., Stehr, M., Singh, M., Ursini, F., and Jaeger, T. (2006) The mycobacterial thioredoxin peroxidase can act as a one-cysteine peroxiredoxin J. Biol. Chem. 281, 20555-20566
3. Hugo, M., Turell, L., Manta, B., Botti, H., Monteiro, G., Netto, L. E., Alvarez, B., Radi, R., and Trujillo, M. (2009) Thiol and sulfenic acid oxidation of AhpE, the one-cysteine peroxiredoxin from Mycobacterium tuberculosis: Kinetics, acidity constants, and conformational dynamics Biochemistry 48, 9416-9426
4. Horta, B. B., de Oliveira, M. A., Discola, K. F., Cussiol, J. R., and Netto, L. E. (2010) Structural and biochemical characterization of peroxiredoxin Qβ from Xylella fastidiosa: Catalytic mechanism and high reactivity J. Biol. Chem. 285, 16051-16065
5. Manta, B., Hugo, M., Ortiz, C., Ferrer-Sueta, G., Trujillo, M., and Denicola, A. (2009) The peroxidase and peroxynitrite reductase activity of human erythrocyte peroxiredoxin 2 Arch. Biochem. Biophys. 484, 146-154
6. 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
7. Peskin, A. V., Low, F. M., Paton, L. N., Maghzal, G. J., Hampton, M. B., and Winterbourn, C. C. (2007) The high reactivity of peroxiredoxin 2 with H2O2 is not reflected in its reaction with other oxidants and thiol reagents J. Biol. Chem. 282, 11885-11892
8. Hall, A., Parsonage, D., Poole, L. B., and Karplus, P. A. (2010) Structural evidence that peroxiredoxin catalytic power is based on transition-state stabilization J. Mol. Biol. 402, 194-209
9. Ferrer-Sueta, G., Manta, B., Botti, H., Radi, R., Trujillo, M., and Denicola, A. (2011) Factors affecting protein thiol reactivity and specificity in peroxide reduction Chem. Res. Toxicol. 24, 434-450
10. Zeida, A., Reyes, A. M., Lebrero, M. C., Radi, R., Trujillo, M., and Estrin, D. A. (2014) The extraordinary catalytic ability of peroxiredoxins: A combined experimental and QM/MM study on the fast thiol oxidation step Chem. Commun. 50, 10070-10073
11. Nelson, K. J., Parsonage, D., Hall, A., Karplus, P. A., and Poole, L. B. (2008) Cysteine p K a values for the bacterial peroxiredoxin AhpC Biochemistry 47, 12860-12868
12. Poole, L. B., Hall, A., and Nelson, K. J. (2011) Overview of peroxiredoxins in oxidant defense and redox regulation. Current Protocols in Toxicology, Chapter 7, pp 7.9.1-7.9.15, Wiley, New York.
13. Nagy, P., Karton, A., Betz, A., Peskin, A. V., Pace, P., OReilly, R. J., Hampton, M. B., Radom, L., and Winterbourn, C. C. (2011) Model for the exceptional reactivity of peroxiredoxins 2 and 3 with hydrogen peroxide: A kinetic and computational study J. Biol. Chem. 286, 18048-18055
14. 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 Signaling 15, 795-815
15. Salsbury, F. R., Jr., Yuan, Y., Knaggs, M. H., Poole, L. B., and Fetrow, J. S. (2012) Structural and electrostatic asymmetry at the active site in typical and atypical peroxiredoxin dimers J. Phys. Chem. B 116, 6832-6843
16. Portillo-Ledesma, S., Sardi, F., Manta, B., Tourn, M. V., Clippe, A., Knoops, B., Alvarez, B., Coitino, E. L., and Ferrer-Sueta, G. (2014) Deconstructing the catalytic efficiency of peroxiredoxin-5 peroxidatic cysteine Biochemistry 53, 6113-6125
17. Nelson, K. J., Knutson, S. T., Soito, L., Klomsiri, C., Poole, L. B., and Fetrow, J. S. (2011) Analysis of the peroxiredoxin family: Using active-site structure and sequence information for global classification and residue analysis Proteins 79, 947-964
18. Chae, H. Z., Robison, K., Poole, L. B., Church, G., Storz, G., and Rhee, S. G. (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. U.S.A. 91, 7017-7021
19. Wood, Z. A., Schröder, E., Harris, J. R., and Poole, L. B. (2003) Structure, mechanism and regulation of peroxiredoxins Trends Biochem. Sci. 28, 32-40
20. König, J., Lotte, K., Plessow, R., Brockhinke, A., Baier, M., and Dietz, K. J. (2003) Reaction mechanism of plant 2-Cys peroxiredoxin. Role of the C terminus and the quaternary structure J. Biol. Chem. 278, 24409-24420
21. Parsonage, D., Karplus, P. A., and Poole, L. B. (2008) Substrate specificity and redox potential of AhpC, a bacterial peroxiredoxin Proc. Natl. Acad. Sci. U.S.A. 105, 8209-8214
22. Baba, T., Ara, T., Hasegawa, M., Takai, Y., Okumura, Y., Baba, M., Datsenko, K. A., Tomita, M., Wanner, B. L., and Mori, H. (2006) Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: The Keio collection Mol. Syst. Biol. 2, 2006.0008
23. Studier, F. W. (2005) Protein production by auto-induction in high density shaking cultures Protein Expression Purif. 41, 207-234
24. Poole, L. B. and Ellis, H. R. (1996) Flavin-dependent alkyl hydroperoxide reductase from Salmonella typhimurium. 1. Purification and enzymatic activities of overexpressed AhpF and AhpC proteins Biochemistry 35, 56-64
25. Bailey, J. L. (1967) Techniques in Protein Chemistry, Elsevier Scientific Publishing Co., Inc., New York.
26. Janatova, J., Fuller, J. K., and Hunter, M. J. (1968) The heterogeneity of bovine albumin with respect to sulfhydryl and dimer content J. Biol. Chem. 243, 3612-3622
27. Nelson, K. J. and Parsonage, D. (2011) Measurement of peroxiredoxin activity. Current Protocols in Toxicology, Chapter 7, pp 7.10.11-7.10.28, Wiley, New York.
28. Mendes, P. (1993) GEPASI: A software package for modelling the dynamics, steady states and control of biochemical and other systems Comput. Appl. Biosci. 9, 563-571
29. Johnson, K. A., Simpson, Z. B., and Blom, T. (2009) Global kinetic explorer: A new computer program for dynamic simulation and fitting of kinetic data Anal. Biochem. 387, 20-29
30. Perkins, A., Nelson, K. J., Williams, J. R., Parsonage, D., Poole, L. B., and Karplus, P. A. (2013) The sensitive balance between the fully folded and locally unfolded conformations of a model peroxiredoxin Biochemistry 52, 8708-8721
31. Wood, Z. A., Poole, L. B., Hantgan, R. R., and Karplus, P. A. (2002) Dimers to doughnuts: Redox-sensitive oligomerization of 2-cysteine peroxiredoxins Biochemistry 41, 5493-5504
32. Jönsson, T. J., Ellis, H. R., and Poole, L. B. (2007) Cysteine reactivity and thiol-disulfide interchange pathways in AhpF and AhpC of the bacterial alkyl hydroperoxide reductase system Biochemistry 46, 5709-5721
33. Niimura, Y., Poole, L. B., and Massey, V. (1995) Amphibacillus xylanus NADH oxidase and Salmonella typhimurium alkyl-hydroperoxide reductase flavoprotein components show extremely high scavenging activity for both alkyl hydroperoxide and hydrogen peroxide in the presence of S. typhimurium alkyl-hydroperoxide reductase 22-kDa protein component J. Biol. Chem. 270, 25645-25650
34. Poole, L. B., Higuchi, M., Shimada, M., Calzi, M. L., and Kamio, Y. (2000) Streptococcus mutans H2O2-forming NADH oxidase is an alkyl hydroperoxide reductase protein Free Radical Biol. Med. 28, 108-120
35. Poole, L. B., Reynolds, C. M., Wood, Z. A., Karplus, P. A., Ellis, H. R., and Li Calzi, M. (2000) AhpF and other NADH:peroxiredoxin oxidoreductases, homologues of low Mr thioredoxin reductase Eur. J. Biochem. 267, 6126-6133
36. Reynolds, C. M. and Poole, L. B. (2000) Attachment of the N-terminal domain of Salmonella typhimurium AhpF to Escherichia coli thioredoxin reductase confers AhpC reductase activity but does not affect thioredoxin reductase activity Biochemistry 39, 8859-8869
37. Reynolds, C. M. and Poole, L. B. (2001) Activity of one of two engineered heterodimers of AhpF, the NADH:peroxiredoxin oxidoreductase from Salmonella typhimurium, reveals intrasubunit electron transfer between domains Biochemistry 40, 3912-3919
38. Wood, Z. A., Poole, L. B., and Karplus, P. A. (2001) Structure of intact AhpF reveals a mirrored thioredoxin-like active site and implies large domain rotations during catalysis Biochemistry 40, 3900-3911
39. Parsonage, D., Reeves, S. A., Karplus, P. A., and Poole, L. B. (2010) Engineering of fluorescent reporters into redox domains to monitor electron transfers Methods Enzymol. 474, 1-21
40. Trujillo, M., Ferrer-Sueta, G., Thomson, L., Flohe, L., and Radi, R. (2007) Kinetics of peroxiredoxins and their role in the decomposition of peroxynitrite Subcell. Biochem. 44, 83-113
41. Nelson, K. J., Parsonage, D., Karplus, P. A., and Poole, L. B. (2013) Evaluating peroxiredoxin sensitivity toward inactivation by peroxide substrates Methods Enzymol. 527, 21-40
42. Wood, Z. A., Poole, L. B., and Karplus, P. A. (2003) Peroxiredoxin evolution and the regulation of hydrogen peroxide signaling Science 300, 650-653
43. Heckel, A. and Pfleiderer, W. (1983) Lumazinesulfenates: A new class of stable sulfenic acids Tetrahedron Lett. 24, 5047-5050
44. Tripolt, R., Belaj, F., and Nachbaur, E. (1993) Unexpectedly stable sulfenic acid: 4,6-Dimethoxy-l,3,5-triazine-2-sulfenic acid; synthesis, properties, molecular and crystal structure Z. Naturforsch. 48b, 1212-1222
45. Peskin, A. V., Dickerhof, N., Poynton, R. A., Paton, L. N., Pace, P. E., Hampton, M. B., and Winterbourn, C. C. (2013) Hyperoxidation of peroxiredoxins 2 and 3: Rate constants for the reactions of the sulfenic acid of the peroxidatic cysteine J. Biol. Chem. 288, 14170-14177