Characterization of the mechanism of the NADH-dependent polysulfide reductase (Npsr) from Shewanella loihica PV-4: Formation of a productive NADH-enzyme complex and its role in the general mechanism of NADH and FAD-dependent enzymes

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1844, Issue 9, 2014, Pages 1708-1717

  Lee, Kyu Hyun ^a   Humbarger, Scott ^a   Bahnvadia, Raj ^a   Sazinsky, Matthew H ^a   Crane III, Edward J ^a  

^a POMONA COLLEGE   (United States)

Author keywords

Coenzyme A; NADH; Persulfide; Polysulfide; Shewanella; Sulfur

Indexed keywords

FLAVINE ADENINE NUCLEOTIDE; NICOTINAMIDE; NICOTINAMIDE ADENINE NUCLEOTIDE HYDRIDE DEPENDENT POLYSULFIDE REDUCTASE; OXIDOREDUCTASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; UNCLASSIFIED DRUG;

ABSORPTION SPECTROSCOPY; ARTICLE; BIOCATALYSIS; CHEMICAL INTERACTION; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; ELECTRON TRANSPORT; ENZYME ANALYSIS; ENZYME KINETICS; ENZYME MECHANISM; ENZYME METABOLISM; FLUORESCENCE SPECTROSCOPY; NONHUMAN; PRIORITY JOURNAL; REDUCTIVE HALF REACTION; SHEWANELLA; SHEWANELLA LOIHICA; WILD TYPE;

COENZYME A; NADH; PERSULFIDE; POLYSULFIDE; SHEWANELLA; SULFUR;

AMINO ACID SUBSTITUTION; BACTERIAL PROTEINS; BINDING SITES; BIOCATALYSIS; CRYSTALLOGRAPHY, X-RAY; ELECTRON TRANSPORT; FLAVIN-ADENINE DINUCLEOTIDE; KINETICS; MODELS, MOLECULAR; NAD; OXIDATION-REDUCTION; OXIDOREDUCTASES; PHENYLALANINE; PROTEIN BINDING; RECOMBINANT PROTEINS; SHEWANELLA; SUBSTRATE SPECIFICITY;

EID: 84904550133     PISSN: 15709639     EISSN: 18781454     Source Type: Journal    
DOI: 10.1016/j.bbapap.2014.06.013     Document Type: Article

References (32)

1. W.P. Jencks Economics of enzyme catalysis Cold Spring Harb. Symp. 52 1987 65 73 (Pubitemid 18262313)
2. D.P. Moser, and K.H. Nealson Growth of the facultative anaerobe Shewanella putrefaciens by elemental sulfur reduction Appl. Environ. Microbiol. 62 1996 2100 2105 (Pubitemid 26169007)
3. J.L. Burns, and T.J. DiChristina Anaerobic respiration of elemental sulfur and thiosulfate by Shewanella oneidensis MR-1 requires psrA, a homolog of the phsA gene of Salmonella enterica serovar typhimurium LT2 Appl. Environ. Microbiol. 75 2009 5209 5217
4. R. Hedderich, O. Klimmek, A. Kroger, R. Dirmeier, M. Keller, and K.O. Stetter Anaerobic respiration with elemental sulfur and with disulfides FEMS Microbiol. Rev. 22 1998 353 381 (Pubitemid 29074342)
5. M.D. Warner, V. Lukose, K.H. Lee, K. Lopez,and E.J. Crane Characterization of an NADH-dependent persulfide reductase from Shewanella loihica PV-4: implications for the mechanism of sulfur respiration via FAD-dependent enzymes Biochemistry-Us 50 2010 194 206
6. J.R. Wallen, C. Paige, T.C. Mallett, P.A. Karplus, and A. Claiborne Pyridine nucleotide complexes with Bacillus anthracis coenzyme A-disulfide reductase: a structural analysis of dual NAD(P)H specificity Biochemistry-Us 47 2008 5182 5193 (Pubitemid 351620755)
7. E.F. Pai, and G.E. Schulz The catalytic mechanism of glutathione reductase as derived from X-ray diffraction analyses of reaction intermediates J. Biol. Chem. 258 1983 1752 1757
8. D.S. Berkholz, H.R. Faber, S.N. Savvides, and P.A. Karplus Catalytic cycle of human glutathione reductase near 1 A resolution J. Mol. Biol. 382 2008 371 384
9. S. Bailey, K. Smith, A.H. Fairlamb, and W.N. Hunter Substrate interactions between trypanothione reductase and N(1)-glutathionylspermidine disulfide at 0.28-nm resolution Eur. J. Biochem. 213 1993 67 75 (Pubitemid 23106032)
10. Y.H. Zhang, C.S. Bond, S. Bailey, M.L. Cunningham, A.H. Fairlamb, and W.N. Hunter The crystal structure of trypanothione reductase from the human pathogen Trypanosoma cruzi at 2.3 Angstrom resolution Protein Sci. 5 1996 52 61
11. T. Stehle, S.A. Ahmed, A. Claiborne, and G.E. Schulz The structure of NADH peroxidase from Streptococcus faecalis at 3.3 A resolution FEBS Lett. 267 1990 186 188 (Pubitemid 20216685)
12. A. Claiborne, S.A. Ahmed, P. Ross, and H. Miller The streptococcal NADH peroxidase and NADH oxidase: structural and mechanistic aspects Flavins and Flavoproteins 1990 1991 Walter de Gruyter New York 639 646
13. S.B. delCardayre, and J.E. Davies Staphylococcus aureus coenzyme A disulfide reductase, a new subfamily of pyridine nucleotide-disulfide oxidoreductase. Sequence, expression, and analysis of CDR J. Biol. Chem. 273 1998 5752 5757 (Pubitemid 28124049)
14. D.R. Harris, D.E. Ward, J.M. Feasel, K.M. Lancaster, R.D. Murphy, T.C. Mallet, and E.J. Crane III Discovery and characterization of a Coenzyme A disulfide reductase from Pyrococcus horikoshii. Implications for this disulfide metabolism of anaerobic hyperthermophiles FEBS J. 272 2005 1189 1200 (Pubitemid 40314938)
15. J.A. Boylan, C.S. Hummel, S. Benoit, J. Garcia-Lara, J. Treglown-Downey, E.J. Crane III, and F.C. Gherardini Borrelia burgdorferi bb0728 encodes a coenzyme A disulphide reductase whose function suggests a role in intracellular redox and the oxidative stress response Mol. Microbiol. 59 2006 475 486
16. J.R. Peregrina, A. Sanchez-Azqueta, B. Herguedas, M. Martinez-Julvez, and M. Medina Role of specific residues in coenzyme binding, charge-transfer complex formation, and catalysis in Anabaena ferredoxin NADP(+)-reductase BBA Bioenerg. 1797 2010 1638 1646
17. Z. Deng, A. Aliverti, G. Zanetti, A.K. Arakaki, J. Ottado, E.G. Orellano, N.B. Calcaterra, E.A. Ceccarelli, N. Carrilli, and P.A. Karplus A productive NADP(+) binding mode of ferredoxin-NADP(+) reductase revealed by protein engineering and crystallographic studies Nat. Struct. Biol. 6 1999 847 853 (Pubitemid 29415177)
18. E.J. Crane III, D. Parsonage, L.B. Poole, and A. Claiborne Analysis of the kinetic mechanism of enterococcal NADH peroxidase reveals catalytic roles for NADH complexes with both oxidized and two-electron-reduced enzyme forms Biochemistry-Us 34 1995 14114 14124
19. P. Emsley, B. Lohkamp, W.G. Scott, and K. Cowtan Features and development of Coot Acta Crystallogr. D Biol. Crystallogr. 66 2010 486 501
20. A.A. Vagin, R.A. Steiner, A.A. Lebedev, L. Potterton, S. McNicholas, F. Long, and G.N. Murshudov REFMAC5 dictionary: organization of prior chemical knowledge and guidelines for its use Acta Crystallogr. D Biol. Crystallogr. 60 2004 2184 2195 (Pubitemid 41742770)
21. M.D. Winn, C.C. Ballard, K.D. Cowtan, E.J. Dodson, P. Emsley, P.R. Evans, R.M. Keegan, E.B. Krissinel, A.G. Leslie, A. McCoy, S.J. McNicholas, G.N. Murshudov, N.S. Pannu, E.A. Potterton, H.R. Powell, R.J. Read, A. Vagin, and K.S. Wilson Overview of the CCP4 suite and current developments Acta Crystallogr. D Biol. Crystallogr. 67 2011 235 242
22. L.B. Poole, and A. Claiborne Interactions of pyridine nucleotides with redox forms of the flavin-containing NADH peroxidase from Streptococcus faecalis J. Biol. Chem. 261 1986 14525 14533 (Pubitemid 17220238)
23. D.E. Ward, C.J. Donnelly, M.E. Mullendore, J. van der Oost, W.M. de Vos, and E.J. Crane III The NADH oxidase from Pyrococcus furiosus. Implications for the protection of anaerobic hyperthermophiles against oxidative stress Eur. J. Biochem. 268 2001 5816 5823 (Pubitemid 33079316)
24. D. Parsonage, H. Miller, R.P. Ross, and A. Claiborne Purification and analysis of streptococcal NADH peroxidase expressed in Eschericia coli J. Biol. Chem. 268 1993 3161 3167 (Pubitemid 23070940)
25. J.I. Yeh, A. Claiborne, and W.G. Hol Structure of the native cysteine-sulfenic acid redox center of enterococcal NADH peroxidase refined at 2.8 A resolution Biochemistry-Us 35 1996 9951 9957 (Pubitemid 26269909)
26. P. Rietveld, L.D. Arscott, A. Berry, N.S. Scrutton, M.P. Deonarain, R.N. Perham, and C.H. Williams Jr. Reductive and oxidative half-reactions of glutathione reductase from Escherichia coli Biochemistry-Us 33 1994 13888 13895 (Pubitemid 24381953)
27. I. Lans, J.R. Peregrina, M. Medina, M. Garcia-Viloca, A. Gonzalez-Lafont, and J.M. Lluch Mechanism of the hydride transfer between anabaena Tyr303Ser FNRrd/FNRox and NADP(+)/H. A combined pre-steady-state kinetic/ensemble-averaged transition-state theory with multidimensional tunneling study J. Phys. Chem. B 114 2010 3368 3379
28. C. Frieden Numerical integration of rate equations by computer TIBS 1993 58
29. + BMC Struct. Biol. 7 2007 69
30. S.L. Andrade, E.V. Patridge, J.G. Ferry, and O. Einsle Crystal structure of the NADH:quinone oxidoreductase WrbA from Escherichia coli J. Bacteriol. 189 2007 9101 9107
31. T. Stehle, A. Claiborne, and G.E. Schulz NADH binding site and catalysis of NADH peroxidase Eur. J. Biochem. 211 1993 221 226 (Pubitemid 23039516)
32. R.L. Krauth-Siegel, L.D. Arscott, A. Schonleben-Janas, R.H. Schirmer, and C.H. Williams Jr. Role of active site tyrosine residues in catalysis by human glutathione reductase Biochemistry-Us 37 1998 13968 13977 (Pubitemid 28471229)