Identification of NAD(P)H quinone oxidoreductase activity in azoreductases from P. aeruginosa: Azoreductases and NAD(P)H quinone oxidoreductases belong to the same FMN-dependent superfamily of enzymes

PLoS ONE

Volumn 9, Issue 6, 2014, Pages

  Ryan, Ali ^a,b   Kaplan, Elise ^a   Nebel, Jean Christophe ^b   Polycarpou, Elena ^b   Crescente, Vincenzo ^a,b   Lowe, Edward ^a   Preston, Gail M ^a   Sim, Edith ^a,b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b KINGSTON UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AZO REDUCTASE; FLAVINE MONONUCLEOTIDE; QUINONE DERIVATIVE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) DEHYDROGENASE (QUINONE); OXIDOREDUCTASE; PROTEIN BINDING;

AMINO ACID SEQUENCE; ARTICLE; ENZYME ACTIVITY; ENZYME MECHANISM; ENZYME SPECIFICITY; NONHUMAN; PSEUDOMONAS AERUGINOSA; REDUCTION; BIOLOGY; CHEMICAL STRUCTURE; CHEMISTRY; CLASSIFICATION; CONFORMATION; ENZYME ACTIVATION; GENETICS; METABOLISM; MULTIGENE FAMILY; OXIDATION REDUCTION REACTION; PHYLOGENY; STRUCTURE ACTIVITY RELATION;

COMPUTATIONAL BIOLOGY; ENZYME ACTIVATION; FLAVIN MONONUCLEOTIDE; MODELS, MOLECULAR; MOLECULAR CONFORMATION; MULTIGENE FAMILY; NADH, NADPH OXIDOREDUCTASES; OXIDATION-REDUCTION; PHYLOGENY; PROTEIN BINDING; PSEUDOMONAS AERUGINOSA; QUINONES; STRUCTURE-ACTIVITY RELATIONSHIP; SUBSTRATE SPECIFICITY;

EID: 84902590760     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0098551     Document Type: Article

References (87)

1. Bolton JL, Trush MA, Penning TM, Dryhurst G, Monks TJ (2000) Role of quinones in toxicology. Chem Res Toxicol 13: 135-160. (Pubitemid 30169958)
2. Cerenius L, Lee BL, Soderhall K (2008) The proPO-system: pros and cons for its role in invertebrate immunity. Trends Immunol 29: 263-271.
3. Mayer AM (2006) Polyphenol oxidases in plants and fungi: going places? A review. Phytochemistry 67: 2318-2331.
4. Shiao SH, Higgs S, Adelman Z, Christensen BM, Liu SH, et al. (2001) Effect of prophenoloxidase expression knockout on the melanization of microfilariae in the mosquito Armigeres subalbatus. Insect Molecular Biology 10: 315-321. (Pubitemid 32747948)
5. Inbaraj JJ, Chignell CF (2003) Cytotoxic Action of Juglone and Plumbagin: A Mechanistic Study Using HaCaT Keratinocytes. Chem Res Toxicol 17: 55-62. (Pubitemid 38134060)
6. Arcamone F, Cassinelli G, Fantini G, Grein A, Orezzi P, et al. (1969) Adriamycin, 14-hydroxydaimomycin, a new antitumor antibiotic from S. peucetius var. caesius. Biotech Bioeng 11: 1101-1110.
7. Chesis PL, Levin DE, Smith MT, Ernster L, Ames BN (1984) Mutagenicity of quinones: pathways of metabolic activation and detoxification. Proc Natl Acad Sci U S A 81: 1696-1700. (Pubitemid 14101208)
8. Nakanishi M, Yatome C, Ishida N, Kitade Y (2001) Putative ACP phosphodiesterase gene (acpD) encodes an azoreductase. J Biol Chem 276: 46394-46399.
9. Mendes S, Pereira L, Batista C, Martins L (2011) Molecular determinants of azo reduction activity in the strain Pseudomonas putida MET94. Appl Microb Biotechnol: 1-13.
10. Chen H, Hopper SL, Cerniglia CE (2005) Biochemical and molecular characterization of an azoreductase from Staphylococcus aureus, a tetrameric NADPH-dependent flavoprotein. Microbiology 151: 1433-1441. (Pubitemid 40711790)
11. Wu K, Knox R, Sun XZ, Joseph P, Jaiswal AK, et al. (1997) Catalytic Properties of NAD(P)H: Quinone Oxidoreductase-2 (NQO2), a Dihydronicotinamide Riboside Dependent Oxidoreductase. Arch Biochem Biophys 347: 221-228. (Pubitemid 27492792)
12. Liu ZJ, Chen H, Shaw N, Hopper SL, Chen L, et al. (2007) Crystal structure of an aerobic FMN-dependent azoreductase (AzoA) from Enterococcus faecalis. Arch Biochem Biophys 463: 68-77. (Pubitemid 46879707)
13. Binter A, Staunig N, Jelesarov I, Lohner K, Palfey BA, et al. (2009) A single intersubunit salt bridge affects oligomerization and catalytic activity in a bacterial quinone reductase. FEBS J 276: 5263-5274.
14. Wang CJ, Laurieri N, Abuhammad A, Lowe E, Westwood I, et al. (2010) Role of Tyrosine 131 in the active site of paAzoR1, an azoreductase with specificity for the inflammatory bowel disease pro-drug balsalazide. Acta Crystallogr F 66: 2-7.
15. Ryan A, Laurieri N, Westwood I, Wang CJ, Lowe E, et al. (2010) A novel mechanism for azoreduction. J Mol Biol 400: 24-37.
16. Ryan A, Wang CJ, Laurieri N, Westwood I, Sim E (2010) Reaction mechanism of azoreductases suggests convergent evolution with quinone oxidoreductases. Protein Cell 1: 780-790.
17. Tedeschi G, Chen S, Massey V (1995) Active site studies of DT-diaphorase employing artificial flavins. J Biol Chem 270: 2512-2516.
18. Iyanagi T, Yamazaki I (1970) One-electron-transfer reactions in biochemical systems. V. Difference in the mechanism of quinone reduction by the NADH dehydrogenase and the NAD(P)H dehydrogenase (DT-diaphorase). Biochim Biophys Acta 216: 282-294.
19. Tan MW, Ausubel FM (2000) Caenorhabditis elegans: a model genetic host to study Pseudomonas aeruginosa pathogenesis. Curr Opin Microbiol 3: 29-34.
20. Rahme LG, Stevens EJ, Wolfort SF, Shao J, Tompkins RG, et al. (1995) Common virulence factors for bacterial pathogenicity in plants and animals. Science 268: 1899-1902.
21. Wang CJ, Hagemeier C, Rahman N, Lowe E, Noble M, et al. (2007) Molecular cloning, characterisation and ligand-bound structure of an azoreductase from Pseudomonas aeruginosa . J Mol Biol 373: 1213-1228. (Pubitemid 47539482)
22. Rakhimova E, Munder A, Wiehlmann L, Bredenbruch F, Tummler B (2008) Fitness of isogenic colony morphology variants of Pseudomonas aeruginosa in murine airway infection. PLoS One 3: e1685.
23. Thipyapong P, Hunt M, Steffens J (2004) Antisense downregulation of polyphenol oxidase results in enhanced disease susceptibility. Planta 220: 105-117. (Pubitemid 40033005)
24. Ding JL, Tan KC, Thangamani S, Kusuma N, Seow WK, et al. (2005) Spatial and temporal coordination of expression of immune response genes during Pseudomonas infection of horseshoe crab, Carcinoscorpius rotundicauda. Genes Immun 6: 557-574. (Pubitemid 41637663)
25. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402. (Pubitemid 27359211)
26. Stover CK, Pham XQ, Erwin AL, Mizoguchi SD, Warrener P, et al. (2000) Complete genome sequence of Pseudomonas aeruginosa PA01, an opportunistic pathogen. Nature 406: 959-964.
27. Prlić A, Bliven S, Rose PW, Bluhm WF, Bizon C, et al. (2010) Pre-calculated protein structure alignments at the RCSB PDB website. Bioinformatics 26: 2983-2985.
28. Burger S, Stolz A (2010) Characterisation of the flavin-free oxygen-tolerant azoreductase from Xenophilus azovorans KF46F in comparison to flavin-containing azoreductases. Appl Microbiol Biotechnol 87: 2067-2076.
29. Winter G (2010) xia2: an expert system for macromolecular crystallography data reduction. J Appl Crystallogr 43: 186-190.
30. Kabsch W (2010) XDS. Acta Crystallogr D 66: 125-132.
31. Bailey S (1994) The CCP4 suit - programs for protein crystallography. Acta Crystallogr D 58: 760-763.
32. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, et al. (2007) Phaser crystallographic software. J Appl Crystallogr 40: 658-674. (Pubitemid 47080256)
33. Emsley P, Lohkamp B, Scott WG, Cowtan K (2010) Features and development of Coot. Acta Crystallogr D 66: 486-501.
34. Murshudov GN, Vagin AA, Dodson EJ (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D 53: 240-255. (Pubitemid 27235885)
35. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, et al. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D 66: 213-221.
36. Moriarty NW, Grosse-Kunstleve RW, Adams PD (2009) electronic Ligand Builder and Optimization Workbench (eLBOW): a tool for ligand coordinate and restraint generation. Acta Crystallogr D 65: 1074-1080.
37. Chen VB, Arendall WB 3rd, Headd JJ, Keedy DA, Immormino RM, et al. (2010) MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr D 66: 12-21.
38. Gonçalves AMD, Mendes S, de Sanctis D, Martins LO, Bento I (2013) The crystal structure of Pseudomonas putida AzoR: the active site revisited. FEBS J 280: 6643-6657.
39. Ito K, Nakanishi M, Lee WC, Zhi Y, Sasaki H, et al. (2008) Expansion of substrate specificity and catalytic mechanism of azoreductase by X-ray crystallography and site-directed mutagenesis. J Biol Chem 283: 13889-13896.
40. Miseviciene L, Anusevicius Z, Sarlauskas J, Cenas N (2006) Reduction of nitroaromatic compounds by NAD(P)H: quinone oxidoreductase (NQO1): the role of electron-accepting potency and structural parameters in the substrate specificity. Acta Biochim Pol 53: 569-576. (Pubitemid 44563726)
41. Clark WM (1960) Oxidation - Reduction potentials of organic systems London: Bailliere, Tindall & Cox.
42. Laurieri N, Crawford MHJ, Kawamura A, Westwood IM, Robinson J, et al. (2010) Small Molecule Colorimetric Probes for Specific Detection of Human Arylamine N-Acetyltransferase 1, a Potential Breast Cancer Biomarker. J Am Chem Soc 132: 3238-3239.
43. Butcher NJ, Minchin RF (2012) Arylamine N-acetyltransferase 1: a novel drug target in cancer development. Pharmacol Rev 64: 147-165.
44. Richter C, Dirks ME, Gronover CS, Prufer D, Moerschbacher BM (2012) Silencing and heterologous expression of ppo-2 indicate a specific function of a single polyphenol oxidase isoform in resistance of dandelion (Taraxacum officinale) against Pseudomonas syringae pv. tomato. Mol Plant Microbe Interact 25: 200-210.
45. Saravanakumar D, Lavanya N, Muthumeena B, Raguchander T, Suresh S, et al. (2008) Pseudomonas fluorescens enhances resistance and natural enemy population in rice plants against leaffolder pest. Journal of Applied Entomology 132: 469-479. (Pubitemid 351813472)
46. Soler-Rivas C, Arpin N, Olivier JM, Wichers HJ (1997) Activation of tyrosinase in Agaricus bisporus strains following infection by Pseudomonas tolaasii or treatment with a tolaasin-containing preparation. Mycological Research 101: 375-382. (Pubitemid 28199171)
47. Rompel A, Fischer H, Meiwes D, Buldt-Karentzopoulos K, Magrini A, et al. (1999) Substrate specificity of catechol oxidase from Lycopus europaeus and characterization of the bioproducts of enzymic caffeic acid oxidation. FEBS Lett 445: 103-110. (Pubitemid 29101543)
48. Tegos G, Stermitz FR, Lomovskaya O, Lewis K (2002) Multidrug pump inhibitors uncover remarkable activity of plant antimicrobials. Antimicrob Agents Chemother 46: 3133-3141.
49. Fischer TC, Gosch C, Mirbeth B, Gselmann M, Thallmair V, et al. (2012) Potent and specific bactericidal effect of juglone (5-hydroxy-1,4- naphthoquinone) on the fire blight pathogen Erwinia amylovora . J Agric Food Chem 60: 12074-12081.
50. Buell CR, Joardar V, Lindeberg M, Selengut J, Paulsen IT, et al. (2003) The complete genome sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000. Proc Natl Acad Sci U S A 100: 10181-10186. (Pubitemid 37071853)
51. Salgado A, Blázquez J (2006) Determination of the structure of a hybrid between 2-(1,4-benzoquinone) acetic acid and a linear peptide by electrospray ionization mass spectrometry. Rapid Comm Mass Spectrom 20: 512-516. (Pubitemid 43200378)
52. Rodriguez-Rojas A, Mena A, Martin S, Borrell N, Oliver A, et al. (2009) Inactivation of the hmgA gene of Pseudomonas aeruginosa leads to pyomelanin hyperproduction, stress resistance and increased persistence in chronic lung infection. Microbiology 155: 1050-1057.
53. Arias-Barrau E, Olivera ER, Luengo JM, Fernandez C, Galan B, et al. (2004) The homogentisate pathway: a central catabolic pathway involved in the degradation of L-phenylalanine, L-tyrosine, and 3-hydroxyphenylacetate in Pseudomonas putida. J Bacteriol 186: 5062-5077. (Pubitemid 38970833)
54. Ryan A, Kaplan E, Laurieri N, Lowe E, Sim E (2011) Activation of nitrofurazone by azoreductases: multiple activities in one enzyme. Sci Rep 1: DOI:10.1038/srep00063.
55. Neyt C, Iriarte M, Thi VH, Cornelis GR (1997) Virulence and arsenic resistance in Yersiniae. J Bacteriol 179: 612-619. (Pubitemid 27051811)
56. Cai J, Salmon K, DuBow MS (1998) A chromosomal ars operon homologue of Pseudomonas aeruginosa confers increased resistance to arsenic and antimony in Escherichia coli. Microbiology 144 (Pt 10): 2705-2713. (Pubitemid 28486420)
57. Mao F, Dam P, Chou J, Olman V, Xu Y (2009) DOOR: a database for prokaryotic operons. Nucleic Acids Res 37: D459-463.
58. Ye J, Yang HC, Rosen BP, Bhattacharjee H (2007) Crystal structure of the flavoprotein ArsH from Sinorhizobium meliloti. FEBS Lett 581: 3996-4000. (Pubitemid 47212107)
59. Hervás M, López-Maury L, León P, Sánchez-Riego AM, Florencio FJ, et al. (2012) ArsH from the cyanobacterium Synechocystis sp. PCC 6803 is an efficient NADPH-dependent quinone reductase. Biochemistry 51: 1178-1187.
60. Yang Z, Lu CD (2007) Functional genomics enables identification of genes of the arginine transaminase pathway in Pseudomonas aeruginosa. J Bacteriol 189: 3945-3953. (Pubitemid 46847340)
61. Gong X, Kole L, Iskander K, Jaiswal AK (2007) NRH: Quinone Oxidoreductase 2 and NAD(P)H: Quinone Oxidoreductase 1 Protect Tumor Suppressor p53 against 20S Proteasomal Degradation Leading to Stabilization and Activation of p53. Cancer Res 67: 5380-5388. (Pubitemid 46997278)
62. Ahn KS, Gong X, Sethi G, Chaturvedi MM, Jaiswal AK, et al. (2007) Deficiency of NRH: quinone oxidoreductase 2 differentially regulates TNF signaling in keratinocytes: up-regulation of apoptosis correlates with downregulation of cell survival kinases. Cancer Res 67: 10004-10011. (Pubitemid 47621251)
63. Xu J, Jaiswal AK (2012) NAD(P)H: quinone oxidoreductase 1 (NQO1) competes with 20S proteasome for binding with C/EBPa leading to its stabilization and protection against radiation-induced myeloproliferative disease. J Biol Chem 287: 41608-41618.
64. Skelly JV, Sanderson MR, Suter DA, Baumann U, Read MA, et al. (1999) Crystal structure of human DT-diaphorase: a model for interaction with the cytotoxic prodrug 5-(aziridin-1-yl)-2,4-dinitrobenzamide (CB1954). J Med Chem 42: 4325-4330. (Pubitemid 29504136)
65. Chatterjee PK, Sternberg NL (1995) A general genetic approach in Escherichia coli for determining the mechanism(s) of action of tumoricidal agents: application to DMP 840, a tumoricidal agent. Proc Natl Acad Sci U S A 92: 8950-8954.
66. Hayashi M, Ohzeki H, Shimada H, Unemoto T (1996) NADPH-specific quinone reductase is induced by 2-methylene-4-butyrolactone in Escherichia coli. Biochim Biophys Acta 1273: 165-170. (Pubitemid 26072616)
67. Wang G, Maier RJ (2004) An NADPH quinone reductase of Helicobacter pylori plays an important role in oxidative stress resistance and host colonization. Infect Immun 72: 1391-1396. (Pubitemid 38263760)
68. Turner KH, Vallet-Gely I, Dove SL (2009) Epigenetic control of virulence gene expression in Pseudomonas aeruginosa by a LysR-type transcription regulator. PLoS genetics 5: e1000779.
69. Agarwal R, Bonanno JB, Burley SK, Swaminathan S (2006) Structure determination of an FMN reductase from Pseudomonas aeruginosa PA01 using sulfur anomalous signal. Acta Crystallogr D 62: 383-391.
70. Sparla F, Tedeschi G, Pupillo P, Trost P (1999) Cloning and heterologous expression of NAD(P)H: quinone reductase of Arabidopsis thaliana, a functional homologue of animal DT-diaphorase. FEBS Lett 463: 382-386. (Pubitemid 30001955)
71. Yang W, Ni L, Somerville RL (1993) A stationary-phase protein of Escherichia coli that affects the mode of association between the trp repressor protein and operator-bearing DNA. Proc Natl Acad Sci USA 90: 5796-5800. (Pubitemid 23176249)
72. Gooderham WJ, Gellatly SL, Sanschagrin F, McPhee JB, Bains M, et al. (2009) The sensor kinase PhoQ mediates virulence in Pseudomonas aeruginosa. Microbiology 155: 699-711.
73. Gorman J, Shapiro L (2005) Crystal structures of the tryptophan repressor binding protein WrbA and complexes with flavin mononucleotide. Protein Sci 14: 3004-3012. (Pubitemid 41770141)
74. Patridge EV, Ferry JG (2006) WrbA from Escherichia coli and Archaeoglobus fulgidus is an NAD(P)H: quinone oxidoreductase. J Bacteriol 188: 3498-3506. (Pubitemid 43726214)
75. Green L (2012) in vitro and in vivo characterisation of P. aeruginosa oxidoreductase enzymes in pathogenesis and therapy. Wellington, NZ: Victoria University of Wellington. 205 p.
76. Lyngberg L, Healy J, Bartlett W, Miller S, Conway SJ, et al. (2011) KefF, the regulatory subunit of the potassium efflux system KefC, shows quinone oxidoreductase activity. J Bacteriol 193: 4925-4932.
77. Roosild TP, Castronovo S, Miller S, Li C, Rasmussen T, et al. (2009) KTN (RCK) domains regulate K+ channels and transporters by controlling the dimerhinge conformation. Structure 17: 893-903.
78. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30: 2725-2729.
79. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792-1797.
80. Vasiliou V, Ross D, Nebert DW (2006) Update of the NAD(P)H: quinone oxidoreductase (NQO) gene family. Hum Genomics 2: 329-335.
81. Chen H, Feng J, Kweon O, Xu H, Cerniglia CE (2010) Identification and molecular characterization of a novel flavin-free NADPH preferred azoreductase encoded by azoB in Pigmentiphaga kullae K24. BMC Biochem 11: 13.
82. McNicholas S, Potterton E, Wilson KS, Noble MEM (2011) Presenting your structures: the CCP4 mg molecular-graphics software. Acta Crystallogr D 67: 386-394.
83. Prosser GA, Copp JN, Syddall SP, Williams EM, Smaill JB, et al. (2010) Discovery and evaluation of Escherichia coli nitroreductases that activate the anti-cancer prodrug CB1954. Biochem Pharmacol 79: 678-687.
84. Ackerley DF, Gonzalez CF, Park CH, Blake R 2nd, Keyhan M, et al. (2004) Chromate-reducing properties of soluble flavoproteins from Pseudomonas putida and Escherichia coli. Appl Environ Microbiol 70: 873-882. (Pubitemid 38568211)
85. Liu G, Zhou J, Wang J, Yan B, Li J, et al. (2008) Site-directed mutagenesis of substrate binding sites of azoreductase from Rhodobacter sphaeroides. Biotechnol Lett 30: 869-875.
86. Liu G, Zhou J, Jin R, Zhou M, Wang J, et al. (2008) Enhancing survival of Escherichia coli by expression of azoreductase AZR possessing quinone reductase activity. Appl Microbiol Biotechnol 80: 409-416.
87. Sedlacek V, van Spanning RJ, Kucera I (2009) Characterization of the quinone reductase activity of the ferric reductase B protein from Paracoccus denitrificans. Arch Biochem Biophys 483: 29-36.