NADH oxidase activity of Bacillus subtilis nitroreductase NfrA1: Insight into its biological role

FEBS Letters

Volumn 584, Issue 18, 2010, Pages 3916-3922

  Cortial, Sylvie ^a   Chaignon, Philippe ^b   Iorga, Bogdan I ^a   Aymerich, Stéphane ^c   Truan, Gilles ^d   Gueguen Chaignon, Virginie ^e   Meyer, Philippe ^e   Moréra, Solange ^e   Ouazzani, Jamal ^a  

^a INSTITUT DE CHIMIE DES SUBSTANCES NATURELLES   (France)

^b UNIVERSITÉ DE STRASBOURG   (France)

^c CNRS   (France)

^d CENTRE DE GÉNÉTIQUE MOLÉCULAIRE   (France)

^e LABORATOIRE D ENZYMOLOGIE ET BIOCHIMIE STRUCTURALES   (France)

Author keywords

Bacillus subtilis; Crystal structure; Hydrogen peroxide; NAD+ degradation; NADH oxidase; Nitroreductase

Indexed keywords

HYDROGEN PEROXIDE; NICOTINAMIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE; NITROREDUCTASE; PROTEIN NFRA1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; MULTIENZYME COMPLEX; NFRA1 PROTEIN, BACILLUS SUBTILIS; OXIDOREDUCTASE; SUPEROXIDE;

ARTICLE; BACILLUS SUBTILIS; BACTERIAL STRAIN; CRYSTALLOGRAPHY; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME KINETICS; ENZYME STRUCTURE; MOLECULAR CLONING; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; AMINO ACID SEQUENCE; BIOSYNTHESIS; CHEMISTRY; ENZYMOLOGY; GENETICS; METABOLISM; MOLECULAR GENETICS; OXIDATIVE STRESS; PHYSIOLOGY; PROTEIN CONFORMATION;

AMINO ACID SEQUENCE; BACILLUS SUBTILIS; BACTERIAL PROTEINS; CLONING, MOLECULAR; HYDROGEN PEROXIDE; MOLECULAR SEQUENCE DATA; MULTIENZYME COMPLEXES; NAD; NADH, NADPH OXIDOREDUCTASES; NIACINAMIDE; NITROREDUCTASES; OXIDATIVE STRESS; PROTEIN CONFORMATION; SUPEROXIDES;

BACILLUS SUBTILIS; POSIBACTERIA;

EID: 77956900968     PISSN: 00145793     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.febslet.2010.08.019     Document Type: Article

References (49)

1. Cashman J.R., Zhang J. Human flavin-containing monooxygenases. Annu. Rev. Pharmacol. Toxicol. 2006, 46:65-100.
2. Massey V. The chemical and biological versatility of riboflavin. Biochem. Soc. Trans. 2000, 28:283-296.
3. Karatani H., Izuta T., Hirayama S. Relationship between the redox change in yellow fluorescent protein of Vibrio fischeri strain Y1 and the reversible change in color of bioluminescence in vitro. Photochem. Photobiol. Sci. 2007, 6:566-570.
4. Jenks P.J., Ferrero R.L., Tankovic J., Thiberge J.M., Labigne A. Evaluation of nitrofurantoin combination therapy of metronidazole-sensitive and -resistant Helicobacter pylori infections in mice. Antimicrob. Agents Chemother. 2000, 44:2623-2629.
5. Rafii F., Hansen E.B. Isolation of nitrofurantoin-resistant mutants of nitroreductase-producing Clostridium sp. Strains from the human intestinal tract. Antimicrob. Agents Chemother. 1998, 42:1121-1126.
6. Spain J.C. Biodegradation of nitroaromatic compounds. Annu. Rev. Microbiol. 1995, 49:523-555.
7. Kwak Y.H., Lee D.S., Kim H.B. Vibrio harveyi nitroreductase is also a chromate reductase. Appl. Environ. Microbiol. 2003, 69:4390-4395.
8. Zenno S., Kobori T., Tanokura M., Saigo K. Purification and characterization of NfrA1, a Bacillus subtilis nitro/flavin reductase capable of interacting with the bacterial luciferase. Biosci. Biotechnol. Biochem. 1998, 62:1978-1987.
9. Searle P.F., Chen M.J., Hu L., Race P.R., Lovering A.L., Grove J.I., Guise C., Jaberipour M., James N.D., Mautner V., Young L.S., Kerr D.J., Mountain A., White S.A., Hyde E.I. Nitroreductase: a prodrug-activating enzyme for cancer gene therapy. Clin. Exp. Pharmacol. Physiol. 2004, 31:811-816.
10. Boyle R.G., Travers S. Hypoxia: targeting the tumour. Anti-Cancer Agents Med. Chem. 2006, 6:281-286.
11. Naal Z., Park J.H., Bernhard S., Shapleigh J.P., Batt C.A., Abruna H.D. Amperometric TNT biosensor based on the oriented immobilization of a nitroreductase maltose binding protein fusion. Anal. Chem. 2002, 74:140-148.
12. Chaignon P., Cortial S., Ventura A.P., Lopes P., Halgand F., Laprevote O., Ouazzani J. Purification and identification of a Bacillus nitroreductase: potential use in 3,5-DNBTF biosensoring system. Enzyme Microb. Technol. 2006, 39:1499-1506.
13. Moch C., Schrogel O., Allmansberger R. Transcription of the nfrA-ywcH operon from Bacillus subtilis is specifically induced in response to heat. J. Bacteriol. 2000, 182:4384-4393.
14. Morré D.M., James Morré D.J. Role of membrane redox in aging-related diseases. Acta Biologica Szegediensis 2006, 50:67-69.
15. Warnholtz A., Nickenig G., Schulz E., Macharzina R., Bräsen J.H., Skatchkov M., Heitzer T., Stasch J.P., Griendling K.K., Harrison D.G., Böhm M., Meinertz T., Münzel T. Increased NADH-oxidase-mediated superoxide production in the early stages of atherosclerosis: evidence for involvement of the renin-angiotensin system. Circulation 1999, 99:2027-2033.
16. Wolvetang E.J., Larm J.A., Moutsoulas P., Lawen A. Apoptosis induced by inhibitors of the plasma membrane NADH-oxidase involves Bcl-2 and calcineurin. Cell Growth Differ. 1996, 7:1315-1325.
17. Ellis E.A., Grant M.B., Murray F.T., Wachowski M.B., Guberski D.L., Kubilis P.S., Lutty G.A. Increased NADH oxidase activity in the retina of the BBZ/Wor diabetic rat. Free Radic. Biol. Med. 1998, 24:111-120.
18. 2-forming NADH oxidase is an alkyl hydroperoxide reductase protein. Free Radic. Biol. Med. 2000, 28:108-120.
19. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227:680-685.
20. Podczasy J.J., Wei R. Reduction of iodonitrotetrazolium violet by superoxide radicals. Biochem. Biophys. Res. Commun. 1988, 150:1294-1301.
21. Kabsch W.J. Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J. Appl. Crystallogr. 1993, 26:795-800.
22. The CCP4 suite: programs for protein crystallography (1994) Acta Crystallogr. D. Biol. Crystallogr. 50, 760-763.
23. Matthews B.W. Solvent content of protein crystals. J. Mol. Biol. 1968, 33:491-497.
24. Sheldrick G.M. A short history of SHELX. Acta Crystallogr., Sect. A: Found. Crystallogr. 2008, 64:112-122.
25. Terwilliger T.C. Automated structure solution, density modification and model building. Acta Crystallogr., Sect. D: Biol. Crystallogr. 2002, 58:1937-1940.
26. Langer G., Cohen S.X., Lamzin V.S., Perrakis A. Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7. Nat. Protoc. 2008, 3:1171-1179.
27. Roussel, A. and Cambillau, C. (1989) Turbo-Frodo. In Silicon Graphics Geometry Partners Directory. Ed. Silicon Graphics Silicon Graphics, Mountain View, CA, 77-78.
28. Brunger A.T., et al. Crystallography and NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr., Sect. D: Biol. Crystallogr. 1998, 54:905-921.
29. Blanc E., Roversi P., Vonrhein C., Flensburg C., Lea S.M., Bricogne G. Refinement of severely incomplete structures with maximum likelihood in BUSTER-TNT. Acta Crystallogr., Sect. D. Biol. Crystallogr. 2004, 60:2210-2221.
30. Friesner R.A., et al. Glide: a new approach for rapid, accurate docking and scoring. 1. Method and assessment of docking accuracy. J. Med. Chem. 2004, 47:1739-1749.
31. Halgren T.A., Murphy R.B., Friesner R.A., Beard H.S., Frye L.L., Pollard W.T., Banks J.L. Glide: a new approach for rapid, accurate docking and scoring. 2. Enrichment factors in database screening. J. Med. Chem. 2004, 47:1750-1759.
32. Pettersen E.F., Goddard T.D., Huang C.C., Couch G.S., Greenblatt D.M., Meng E.C., Ferrin T.E. UCSF chimera - a visualization system for exploratory research and analysis. J. Comput. Chem. 2004, 25:1605-1612.
33. Tanner J.J., Lei B., Tu S.C., Krause K.L. Flavin reductase P: structure of a dimeric enzyme that reduces flavin. Biochemistry 1996, 35:13531-13539.
34. Tanner J.J., Tu S.C., Barbour L.J., Barnes C.L., Krause K.L. Unusual folded conformation of nicotinamide adenine dinucleotide bound to flavin reductase P. Protein Sci. 1999, 8:1725-1732.
35. Kobori T., Sasaki H., Lee W.C., Zenno S., Saigo K., Murphy M.E., Tanokura M. Structure and site-directed mutagenesis of a flavoprotein from Escherichia coli that reduces nitrocompounds: alteration of pyridine nucleotide binding by a single amino acid substitution. J. Biol. Chem. 2001, 276:2816-2823.
36. Morokutti A., Lyskowski A., Sollner S., Pointner E., Fitzpatrick T.B., Kratky C., Gruber K., Macheroux P. Structure and function of YcnD from Bacillus subtilis, a flavin-containing oxidoreductase. Biochemistry 2005, 44:13724-13733.
37. Hecht H.J., Erdmann H., Park H.J., Sprinzl M., Schmid R.D. Crystal structure of NADH oxidase from Thermus thermophilus. Nat. Struct. Biol. 1995, 2:1109-1114.
38. Koike H., Sasaki H., Tanokura M., Zenno S., Saigo K. Crystallization and preliminary crystallographic analysis of the major NAD(P)H: FMN oxidoreductase of Vibrio fischeri ATCC 7744. J. Struct. Biol. 1996, 117:70-72.
39. Gouet P., Courcelle E., Stuart D.I., Metoz F. ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics 1999, 15:305-308.
40. Clifford D.P., Repine J.E. Hydrogen peroxide mediated killing of bacteria. Mol. Cell. Biochem. 1982, 49:143-149.
41. Gomaa O.M., Azab K.S.H. Resistance to hydrogen peroxide in textile waste water Bacillus sp. Int. J. Agri. Biol. 2007, 9:347-351.
42. Luo S., Levine R.L. Methionine in proteins defends against oxidative stress. FASEB J. 2009, 23:464-472.
43. Oppenheimer N.J. NAD hydrolysis: chemical and enzymatic mechanisms. Mol. Cell. Biochem. 1994, 138:245-251.
44. Berti P.J., Blanke S.R., Schramm V.L. Transition state structure for the hydrolysis of NAD catalyzed by Diphtheria toxin. J. Am. Chem. Soc. 1997, 119:12079-12088.
45. Zhao K., Harshaw R., Chai X., Marmorstein R. Structural basis for nicotinamide cleavage and ADP-ribose transfer by NAD(+)-dependent Sir2 histone/protein deacetylases. Proc. Natl Acad. Sci. USA 2004, 101:8563-8568.
46. Lund F.E. Signaling properties of CD38 in the mouse immune system: enzyme-dependent and -independent roles in immunity. Mol. Med. 2006, 12:328-333.
47. Bourgeois C., Okazaki I., Cavanaugh E., Nightingale M., Moss J. Identification of regulatory domains in ADP-ribosyltransferase-1 that determine transferase and NAD glycohydrolase activities. J. Biol. Chem. 2003, 278:26351-26355.
48. Tavazzi B., Di Pierro D., Amorini A.M., Fazzina G., Galvano M., Lupi A., Giardina B., Lazzarino G. Direct NAD(P)H hydrolysis into ADP-ribose(P) and nicotinamide induced by reactive oxygen species: a new mechanism of oxygen radical toxicity. Free Radic. Res. 2000, 33:1-12.
49. Huie R.E., Padmaja S. The reaction of NO with superoxide. Free Radical Res. Commun. 1993, 18:195-199.