Structural Analysis of Streptococcus pyogenes NADH Oxidase: Conformational Dynamics Involved in Formation of the C(4a)-Peroxyflavin Intermediate

Biochemistry

Volumn 54, Issue 45, 2015, Pages 6815-6829

  Wallen, Jamie R ^a   Mallett, T Conn ^b,d   Okuno, Takashi ^b,e   Parsonage, Derek ^b   Sakai, Hiroaki ^c   Tsukihara, Tomitake ^c   Claiborne, Al ^b  

^a WESTERN CAROLINA UNIVERSITY   (United States)

^b WAKE FOREST SCHOOL OF MEDICINE   (United States)

^c OSAKA UNIVERSITY   (Japan)

^d RIGAKU CORPORATION   (Japan)

^e YAMAGATA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CHAINS; CHARGE TRANSFER; CRYSTAL STRUCTURE; ELECTRON AFFINITY; ENZYMES; REACTION INTERMEDIATES; SULFUR DIOXIDE;

CHARGE TRANSFER INTERACTION; CONFORMATIONAL CHANGE; CONFORMATIONAL DYNAMICS; ENTEROCOCCUS FAECALIS; OXYGEN REACTIVITY; PROGRESSIVE DISPLACEMENT; STREPTOCOCCUS PYOGENES; STRUCTURAL MODELING;

CONFORMATIONS;

AZIDE; C(4A) PEROXYFLAVIN; QUERCETIN DERIVATIVE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; SULFINIC ACID DERIVATIVE; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; CYSTEINE; HYBRID PROTEIN; MULTIENZYME COMPLEX; NAD+ PEROXIDASE; OXIDOREDUCTASE; PEROXIDASE; RIBOFLAVIN DERIVATIVE;

ARTICLE; CRYSTALLIZATION; ENTEROCOCCUS FAECALIS; ENZYME CONFORMATION; ENZYME STRUCTURE; NONHUMAN; OXIDATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; STREPTOCOCCUS PYOGENES; AMINO ACID SEQUENCE; ANTAGONISTS AND INHIBITORS; CHEMICAL STRUCTURE; CHEMISTRY; COMPARATIVE STUDY; ENZYME ACTIVE SITE; ENZYMOLOGY; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MOLECULAR DYNAMICS; MOLECULAR GENETICS; OXIDATION REDUCTION REACTION; PROTEIN CONFORMATION; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; SPECIES DIFFERENCE; STRUCTURE ACTIVITY RELATION; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; AZIDES; BACTERIAL PROTEINS; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; CYSTEINE; ENTEROCOCCUS FAECALIS; FLAVINS; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; MULTIENZYME COMPLEXES; NADH, NADPH OXIDOREDUCTASES; OXIDATION-REDUCTION; OXIDOREDUCTASES; PEROXIDASES; PROTEIN CONFORMATION; RECOMBINANT FUSION PROTEINS; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; SPECIES SPECIFICITY; STREPTOCOCCUS PYOGENES; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84947253067     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/acs.biochem.5b00676     Document Type: Article

References (59)

1. Ojha, S., Meng, E. C., and Babbitt, P. C. (2007) Evolution of function in the "two dinucleotide binding domains" flavoproteins PLoS Comput. Biol. 3, e121 10.1371/journal.pcbi.0030121
2. Argyrou, A. and Blanchard, J. S. (2004) Flavoprotein disulfide reductases: advances in chemistry and function Prog. Nucleic Acid Res. Mol. Biol. 78, 89-142 10.1016/S0079-6603(04)78003-4
3. Mallett, T. C. and Claiborne, A. (1998) Oxygen reactivity of an NADH oxidase C42S mutant: evidence for a C(4a)-peroxyflavin intermediate and a rate-limiting conformational change Biochemistry 37, 8790-8802 10.1021/bi9803630
4. Mande, S. S., Parsonage, D., Claiborne, A., and Hol, W. G. (1995) Crystallographic analyses of NADH peroxidase Cys42Ala and Cys42Ser mutants: active site structures, mechanistic implications, and an unusual environment of Arg 303 Biochemistry 34, 6985-6992 10.1021/bi00021a010
5. Huijbers, M. M., Montersino, S., Westphal, A. H., Tischler, D., and van Berkel, W. J. (2014) Flavin dependent monooxygenases Arch. Biochem. Biophys. 544, 2-17 10.1016/j.abb.2013.12.005
6. van Berkel, W. J., Kamerbeek, N. M., and Fraaije, M. W. (2006) Flavoprotein monooxygenases, a diverse class of oxidative biocatalysts J. Biotechnol. 124, 670-689 10.1016/j.jbiotec.2006.03.044
7. Entsch, B., Cole, L. J., and Ballou, D. P. (2005) Protein dynamics and electrostatics in the function of p-hydroxybenzoate hydroxylase Arch. Biochem. Biophys. 433, 297-311 10.1016/j.abb.2004.09.029
8. Palfey, B. A., Entsch, B., Ballou, D. P., and Massey, V. (1994) Changes in the catalytic properties of p-hydroxybenzoate hydroxylase caused by the mutation Asn300Asp Biochemistry 33, 1545-1554 10.1021/bi00172a035
9. Entsch, B., Ballou, D. P., and Massey, V. (1976) Flavin-oxygen derivatives involved in hydroxylation by p-hydroxybenzoate hydroxylase J. Biol. Chem. 251, 2550-2563
10. Sheng, D., Ballou, D. P., and Massey, V. (2001) Mechanistic studies of cyclohexanone monooxygenase: chemical properties of intermediates involved in catalysis Biochemistry 40, 11156-11167 10.1021/bi011153h
11. Ahmed, S. A. and Claiborne, A. (1992) Catalytic properties of streptococcal NADH oxidase containing artificial flavins J. Biol. Chem. 267, 25822-25829
12. 2 into two water molecules by the flavoenzyme Biochemistry 45, 9648-9659 10.1021/bi060692p
13. Wallen, J. R., Paige, C., Mallett, T. C., Karplus, P. A., and Claiborne, A. (2008) Pyridine nucleotide complexes with Bacillus anthracis coenzyme A-disulfide reductase: a structural analysis of dual NAD(P)H specificity Biochemistry 47, 5182-5193 10.1021/bi8002204
14. Mallett, T. C., Parsonage, D., and Claiborne, A. (1999) Equilibrium analyses of the active-site asymmetry in enterococcal NADH oxidase: role of the cysteine-sulfenic acid redox center Biochemistry 38, 3000-3011 10.1021/bi9817717
15. Gibson, C. M., Mallett, T. C., Claiborne, A., and Caparon, M. G. (2000) Contribution of NADH oxidase to aerobic metabolism of Streptococcus pyogenes J. Bacteriol. 182, 448-455 10.1128/JB.182.2.448-455.2000
16. Ahmed, S. A. and Claiborne, A. (1989) The streptococcal flavoprotein NADH oxidase. I. Evidence linking NADH oxidase and NADH peroxidase cysteinyl redox centers J. Biol. Chem. 264, 19856-19863
17. Crane, E. J., 3rd, Yeh, J. I., Luba, J., and Claiborne, A. (2000) Analysis of the kinetic and redox properties of the NADH peroxidase R303M mutant: correlation with the crystal structure Biochemistry 39, 10353-10364 10.1021/bi000553m
18. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R., Thompson, J. D., Gibson, T. J., and Higgins, D. G. (2007) Clustal W and Clustal X version 2.0 Bioinformatics 23, 2947-2948 10.1093/bioinformatics/btm404
19. Robert, X. and Gouet, P. (2014) Deciphering key features in protein structures with the new ENDscript server Nucleic Acids Res. 42, W320-324 10.1093/nar/gku316
20. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol. 276, 307-326 10.1016/S0076-6879(97)76066-X
21. Yeh, J. I., Claiborne, A., and Hol, W. G. (1996) Structure of the native cysteine-sulfenic acid redox center of enterococcal NADH peroxidase refined at 2.8 Å resolution Biochemistry 35, 9951-9957 10.1021/bi961037s
22. Navaza, J. (1994) AMORE-an automated package for molecular replacement Acta Crystallogr., Sect. A: Found. Crystallogr. A50, 157-163 10.1107/S0108767393007597
23. Collaborative Computational Project Number 4 (1994) The CCP4 suite: programs for protein crystallography Acta Crystallogr., Sect. D: Biol. Crystallogr. D50, 760-763 10.1107/S0907444994003112
24. Cowtan, K. and Main, P. (1998) Miscellaneous algorithms for density modification Acta Crystallogr., Sect. D: Biol. Crystallogr. D54, 487-493 10.1107/S0907444997011980
25. Jones, T. A., Zou, J. Y., Cowan, S. W., and Kjeldgaard, M. (1991) Improved methods for building protein models in electron-density maps and the location of errors in these models Acta Crystallogr., Sect. A: Found. Crystallogr. A47, 110-119 10.1107/S0108767390010224
26. Brunger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J. S., Kuszewski, J., Nilges, M., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography & NMR system: a new software suite for macromolecular structure determination Acta Crystallogr., Sect. D: Biol. Crystallogr. D54, 905-921 10.1107/S0907444998003254
27. Ahmed, S. A. and Claiborne, A. (1989) The streptococcal flavoprotein NADH oxidase. II. Interactions of pyridine nucleotides with reduced and oxidized enzyme forms J. Biol. Chem. 264, 19863-19870
28. Müller, F. and Massey, V. (1969) Flavin-sulfite complexes and their structures J. Biol. Chem. 244, 4007-4016
29. Crane, E. J., 3rd, Parsonage, D., and Claiborne, A. (1996) The active-site histidine-10 of enterococcal NADH peroxidase is not essential for catalytic activity Biochemistry 35, 2380-2387 10.1021/bi952347y
30. Miller, H. and Claiborne, A. (1991) Peroxide modification of monoalkylated glutathione reductase. Stabilization of an active-site cysteine-sulfenic acid J. Biol. Chem. 266, 19342-19350
31. Stehle, T., Ahmed, S. A., Claiborne, A., and Schulz, G. E. (1991) Structure of NADH peroxidase from Streptococcus faecalis 10C1 refined at 2.16 Å resolution J. Mol. Biol. 221, 1325-1344 10.1016/0022-2836(91)90936-Z
32. Hooft, R. W., Vriend, G., Sander, C., and Abola, E. E. (1996) Errors in protein structures Nature 381, 272 10.1038/381272a0
33. Kleywegt, G. J. and Jones, T. A. (1996) Phi/psi-chology: Ramachandran revisited Structure 4, 1395-1400 10.1016/S0969-2126(96)00147-5
34. Holm, L. and Rosenstrom, P. (2010) Dali server: conservation mapping in 3D Nucleic Acids Res. 38, W545-549 10.1093/nar/gkq366
35. 13C NMR analysis of the cysteine-sulfenic acid redox center of enterococcal NADH peroxidase Biochemistry 36, 8611-8618 10.1021/bi9707990
36. Creighton, T. E. (1993) Proteins, 2 nd ed., W. H. Freeman and Co., New York.
37. 2O-forming NADH oxidase from Streptococcus faecalis Eur. J. Biochem. 156, 149-155 10.1111/j.1432-1033.1986.tb09560.x
38. 2O-forming oxidase induced in Streptococcus mutans J. Gen. Microbiol. 139, 2343-2351 10.1099/00221287-139-10-2343
39. Scrutton, N. S., Berry, A., and Perham, R. N. (1990) Redesign of the coenzyme specificity of a dehydrogenase by protein engineering Nature 343, 38-43 10.1038/343038a0
40. Miller, H., Mande, S. S., Parsonage, D., Sarfaty, S. H., Hol, W. G., and Claiborne, A. (1995) An L40C mutation converts the cysteine-sulfenic acid redox center in enterococcal NADH peroxidase to a disulfide Biochemistry 34, 5180-5190 10.1021/bi00015a032
41. Mittl, P. R. and Schulz, G. E. (1994) Structure of glutathione reductase from Escherichia coli at 1.86 Å resolution: comparison with the enzyme from human erythrocytes Protein Sci. 3, 799-809 10.1002/pro.5560030509
42. Stehle, T., Claiborne, A., and Schulz, G. E. (1993) NADH binding site and catalysis of NADH peroxidase Eur. J. Biochem. 211, 221-226 10.1111/j.1432-1033.1993.tb19889.x
43. Karplus, P. A. and Schulz, G. E. (1989) Substrate binding and catalysis by glutathione reductase as derived from refined enzyme: substrate crystal structures at 2 Å resolution J. Mol. Biol. 210, 163-180 10.1016/0022-2836(89)90298-2
44. Schreuder, H. A., Hol, W. G., and Drenth, J. (1988) Molecular modeling reveals the possible importance of a carbonyl oxygen binding pocket for the catalytic mechanism of p-hydroxybenzoate hydroxylase J. Biol. Chem. 263, 3131-3136
45. Schreuder, H. A., Hol, W. G., and Drenth, J. (1990) Analysis of the active site of the flavoprotein p-hydroxybenzoate hydroxylase and some ideas with respect to its reaction mechanism Biochemistry 29, 3101-3108 10.1021/bi00464a029
46. Wilkinson, K. D. and Williams, C. H., Jr. (1979) Evidence for multiple electronic forms of two-electron-reduced lipoamide dehydrogenase from Escherichia coli J. Biol. Chem. 254, 852-862
47. Mallett, T. C., Wallen, J. R., Karplus, P. A., Sakai, H., Tsukihara, T., and Claiborne, A. (2006) Structure of coenzyme A-disulfide reductase from Staphylococcus aureus at 1.54 Å resolution Biochemistry 45, 11278-11289 10.1021/bi061139a
48. Wallen, J. R., Mallett, T. C., Boles, W., Parsonage, D., Furdui, C. M., Karplus, P. A., and Claiborne, A. (2009) Crystal structure and catalytic properties of Bacillus anthracis CoADR-RHD: implications for flavin-linked sulfur trafficking Biochemistry 48, 9650-9667 10.1021/bi900887k
49. Warner, M. D., Lukose, V., Lee, K. H., Lopez, K., Sazinsky, M. H., and Crane, E. J., 3rd (2011) Characterization of an NADH-dependent persulfide reductase from Shewanella loihica PV-4: implications for the mechanism of sulfur respiration via FAD-dependent enzymes Biochemistry 50, 194-206 10.1021/bi101232y
50. Atkinson, H. J. and Babbitt, P. C. (2009) An atlas of the thioredoxin fold class reveals the complexity of function-enabling adaptations PLoS Comput. Biol. 5, e1000541 10.1371/journal.pcbi.1000541
51. Shoun, H., Arima, K., and Beppu, T. (1983) Inhibition of p-hydroxybenzoate hydroxylase by anions: possible existence of two anion-binding sites in the site for reduced nicotinamide adenine dinucleotide phosphate J. Biochem. 93, 169-176
52. Gatti, D. L., Palfey, B. A., Lah, M. S., Entsch, B., Massey, V., Ballou, D. P., and Ludwig, M. L. (1994) The mobile flavin of 4-OH benzoate hydroxylase Science 266, 110-114 10.1126/science.7939628
53. Steennis, P. J., Cordes, M. M., Hilkens, J. H., and Müller, F. (1973) On the interaction of para-hydroxybenzoate hydroxylase from Pseudomonas fluorescens with halogen ions FEBS Lett. 36, 177-180 10.1016/0014-5793(73)80363-1
54. Ghisla, S. and Massey, V. (1989) Mechanisms of flavoprotein-catalyzed reactions Eur. J. Biochem. 181, 1-17 10.1111/j.1432-1033.1989.tb14688.x
55. Tierney, D. L., Fee, J. A., Ludwig, M. L., and Penner-Hahn, J. E. (1995) X-ray absorption spectroscopy of the iron site in Escherichia coli Fe(III) superoxide dismutase Biochemistry 34, 1661-1668 10.1021/bi00005a022
56. Gutman, C. T., Guzei, I. A., and Brunold, T. C. (2013) Structural, spectroscopic, and computational characterization of the azide adduct of Fe(III)(2,6-diacetylpyridinebis(semioxamazide)), a functional analogue of iron superoxide dismutase Inorg. Chem. 52, 8909-8918 10.1021/ic401098x
57. Gutfreund, H. (1972) Enzymes: Physical Principles, John Wiley & Sons, New York.
58. Segel, I. H. (1975) Enzyme Kinetics, John Wiley & Sons, New York.
59. Frieden, C. (1979) Slow transitions and hysteretic behavior in enzymes Annu. Rev. Biochem. 48, 471-489 10.1146/annurev.bi.48.070179.002351