Reaction mechanism of azoreductases suggests convergent evolution with quinone oxidoreductases

Protein and Cell

Volumn 1, Issue 8, 2010, Pages 780-790

  Ryan, Ali ^a   Wang, Chan ^a   Laurieri, Nicola ^a   Westwood, Isaac ^a   Sim, Edith ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Azoreductase; Convergent evolution; Enzyme characterisation; Enzyme mechanism; NAD(P)H quinone oxidoreductase

Indexed keywords

AZO REDUCTASE; BALSALAZIDE; MENADIONE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) DEHYDROGENASE (QUINONE);

ARTICLE; BACTERIAL GROWTH; CONTROLLED STUDY; CONVERGENT EVOLUTION; CRYSTAL STRUCTURE; ENZYME ANALYSIS; ENZYME KINETICS; ENZYME MECHANISM; ENZYME SPECIFICITY; ENZYME STABILITY; NONHUMAN; OXIDATION REDUCTION STATE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PSEUDOMONAS AERUGINOSA; SEQUENCE ANALYSIS;

BACTERIA (MICROORGANISMS);

EID: 79953133983     PISSN: 1674800X     EISSN: 16748018     Source Type: Journal    
DOI: 10.1007/s13238-010-0090-2     Document Type: Article

References (54)

1. Ackerley, D. F., Gonzalez, C. F., Park, C. H., Blake, R. 2nd, Keyhan, M., and Matin, A. (2004). Chromate-reducing properties of soluble flavoproteins from Pseudomonas putida and Escherichia coli. Appl Environ Microbiol 70, 873-882.
2. Adams, M. A., and Jia, Z. (2006). Modulator of drug activity B from Escherichia coli: crystal structure of a prokaryotic homologue of DT-diaphorase. J Mol Biol 359, 455-465.
3. Agarwal, R., Bonanno, J. B., Burley, S. K., and Swaminathan, S. (2006). Structure determination of an FMN reductase from Pseudomonas aeruginosa PA01 using sulfur anomalous signal. Acta Crystallogr D Biol Crystallogr 62, 383-391.
4. Alard, A., Fabre, B., Anesia, R., Marboeuf, C., Pierre, P., Susini, C., Bousquet, C., and Pyronnet, S. (2010). NAD(P)H quinoneoxydoreductase 1 protects eukaryotic translation initiation factor 4GI from degradation by the proteasome. Mol Cell Biol 30, 1097-1105.
5. Alves de Lima, R. O., Bazo, A. P., Salvadori, D. M. F., Rech, C. M., de Palma Oliveira, D., and de Arag̃o Umbuzeiro, G. (2007). Mutagenic and carcinogenic potential of a textile azo dye processing plant effluent that impacts a drinking water source. Mutat Res 626, 53-60.
6. Armougom, F., Moretti, S., Poirot, O., Audic, S., Dumas, P., Schaeli, B., Keduas, V., and Notredame, C. (2006). Expresso: automatic incorporation of structural information in multiple sequence alignments using 3D-Coffee. Nucleic Acids Res 34, W604-608.
7. Bin, Y., Jiti, Z., Jing, W., Cuihong, D., Hongman, H., Zhiyong, S., and Yongming, B. (2004). Expression and characteristics of the gene encoding azoreductase from Rhodobacter sphaeroides AS1. 1737. FEMS Microbiol Lett 236, 129-136.
8. Binter, A., Staunig, N., Jelesarov, I., Lohner, K., Palfey, B. A., Deller, S., Gruber, K., and Macheroux, P. (2009). A single intersubunit salt bridge affects oligomerization and catalytic activity in a bacterial quinone reductase. FEBS J 276, 5263-5274.
9. Chen, H., Wang, R. F., and Cerniglia, C. E. (2004). Molecular cloning, overexpression, purification, and characterization of an aerobic FMN-dependent azoreductase from Enterococcus faecalis. Protein Expr Purif 34, 302-310.
10. Cui, K., Lu, A. Y., and Yang, C. S. (1995). Subunit functional studies of NAD(P)H: quinone oxidoreductase with a heterodimer approach. Proc Natl Acad Sci U S A 92, 1043-1047.
11. Deller, S., Sollner, S., Trenker-El-Toukhy, R., Jelesarov, I., Gübitz, G. M., and Macheroux, P. (2006). Characterization of a thermostable NADPH: FMN oxidoreductase from the mesophilic bacterium Bacillus subtilis. Biochemistry 45, 7083-7091.
12. dos Santos, A. B., Cervantes, F. J., and van Lier, J. B. (2007). Review paper on current technologies for decolourisation of textile wastewaters: perspectives for anaerobic biotechnology. Bioresour Technol 98, 2369-2385.
13. Duurkens, R. H., Tol, M. B., Geertsma, E. R., Permentier, H. P., and Slotboom, D. J. (2007). Flavin binding to the high affinity riboflavin transporter RibU. J Biol Chem 282, 10380-10386.
14. El-Shafei, A., Fadda, A. A., Khalil, A. M., Ameen, T. A., and Badria, F. A. (2009). Synthesis, antitumor evaluation, molecular modeling and quantitative structure-activity relationship (QSAR) of some novel arylazopyrazolodiazine and triazine analogs. Bioorg Med Chem 17, 5096-5105.
15. Environmental Protection Agency. (1997). Profile of the Textile Industry. In Sector Notebook Project (Washington, DC).
16. Farghaly, T. A., and Abdalla, M. M. (2009). Synthesis, tautomerism, and antimicrobial, anti-HCV, anti-SSPE, antioxidant, and antitumor activities of arylazobenzosuberones. Bioorg Med Chem 17, 8012-8019.
17. Fetzner, S., Müller, R., and Lingens, F. (1992). Purification and some properties of 2-halobenzoate 1, 2-dioxygenase, a two-component enzyme system from Pseudomonas cepacia 2CBS. J Bacteriol 174, 279-290.
18. Foster, C. E., Bianchet, M. A., Talalay, P., Zhao, Q., and Amzel, L. M. (1999). Crystal structure of human quinone reductase type 2, a metalloflavoprotein. Biochemistry 38, 9881-9886.
19. Gorman, J., and Shapiro, L. (2005). Crystal structures of the tryptophan repressor binding protein WrbA and complexes with flavin mononucleotide. Protein Sci 14, 3004-3012.
20. Ito, K., Nakanishi, M., Lee, W. C., Sasaki, H., Zenno, S., Saigo, K., Kitade, Y., and Tanokura, M. (2006). Three-dimensional structure of AzoR from Escherichia coli. An oxidereductase conserved in microorganisms. J Biol Chem 281, 20567-20576.
21. Lewis, D. F. V. (2001). Guide to Cytochromes P450: Structure and Function (New York, US, Taylor and Francis).
22. Li, R., Bianchet, M. A., Talalay, P., and Amzel, L. M. (1995). The three-dimensional structure of NAD(P)H: quinone reductase, a flavoprotein involved in cancer chemoprotection and chemotherapy: mechanism of the two-electron reduction. Proc Natl Acad Sci U S A 92, 8846-8850.
23. Lichtenstein, G. R., Kamm, M. A. (2008). Review article: 5-aminosalicylate formulations for the treatment of ulcerative colitis-methods of comparing release rates and delivery of 5-aminosalicylate to the colonic mucosa. Aliment Pharmacol Ther 28, 663-673.
24. Liger, D., Graille, M., Zhou, C. Z., Leulliot, N., Quevillon-Cheruel, S., Blondeau, K., Janin, J., and van Tilbeurgh, H. (2004). Crystal structure and functional characterization of yeast YLR011wp, an enzyme with NAD(P)H-FMN and ferric iron reductase activities. J Biol Chem 279, 34890-34897.
25. Liu, G., Zhou, J., Jin, R., Zhou, M., Wang, J., Lu, H., and Qu, Y. (2008). Enhancing survival of Escherichia coli by expression of azoreductase AZR possessing quinone reductase activity. Appl Microbiol Biotechnol 80, 409-416.
26. Liu, G., Zhou, J., Fu, Q. S., and Wang, J. (2009). The Escherichia coli azoreductase AzoR Is involved in resistance to thiol-specific stress caused by electrophilic quinones. J Bacteriol 191, 6394-6400.
27. Long, D. J., 2nd, Gaikwad, A., Multani, A., Pathak, S., Montgomery, C. A., Gonzalez, F. J., Jaiswal, A. K. (2002). Disruption of the NAD(P) H: quinone oxidoreductase 1 (NQO1) gene in mice causes myelogenous hyperplasia. Cancer Res 62, 3030-3036.
28. Nakanishi, M., Yatome, C., Ishida, N., and Kitade, Y. (2001). Putative ACP phosphodiesterase gene (acpD) encodes an azoreductase. J Biol Chem 276, 46394-46399.
29. Nissen, M. S., Youn, B., Knowles, B. D., Ballinger, J. W., Jun, S. Y., Belchik, S. M., Xun, L., and Kang, C. (2008). Crystal structures of NADH: FMN oxidoreductase (EmoB) at different stages of catalysis. J Biol Chem 283, 28710-28720.
30. Patridge, E. V., and Ferry, J. G. (2006). WrbA from Escherichia coli and Archaeoglobus fulgidus is an NAD(P)H: quinone oxidoreductase. J Bacteriol 188, 3498-3506.
31. Peppercorn, M. A., and Goldman, P. (1972). The role of intestinal bacteria in the metabolism of salicylazosulfapyridine. J Pharmacol Exp Ther 181, 555-562.
32. Potterton, L., McNicholas, S., Krissinel, E., Gruber, J., Cowtan, K., Emsley, P., Murshudov, G. N., Cohen, S., Perrakis, A., and Noble, M. (2004). Developments in the CCP4 molecular-graphics project. Acta Crystallogr D Biol Crystallogr 60, 2288-2294.
33. Poulos, T. L., Finzel, B. C., Gunsalus, I. C., Wagner, G. C., and Kraut, J. (1985). The 2. 6-A crystal structure of Pseudomonas putida cytochrome P-450. J Biol Chem 260, 16122-16130.
34. + channels and transporters by controlling the dimer-hinge conformation. Structure 17, 893-903.
35. Ryan, A., Laurieri, N., Westwood, I., Wang, C.J., Lowe, E., and Sim, E. (2010). A novel mechanism for azoreduction. J Mol Biol 400, 24-37.
36. Sandy, J., Mushtaq, A., Holton, S. J., Schartau, P., Noble, M. E., and Sim, E. (2005). Investigation of the catalytic triad of arylamine Nacetyltransferases: essential residues required for acetyl transfer to arylamines. Biochem J 390, 115-123.
37. Savli, H., Karadenizli, A., Kolayli, F., Gundes, S., Ozbek, U., and Vahaboglu, H. (2003). Expression stability of six housekeeping genes: A proposal for resistance gene quantification studies of Pseudomonas aeruginosa by real-time quantitative RT-PCR. J Med Microbiol 52, 403-408.
38. Sherma, J. F. B. (2003). Handbook of thin layer chromatography, 3rd edn (New York, Marcel Dekker).
39. Shore, J. (1995). Dyeing with reactive dyes. In cellulosics dyeing, J. Shore, ed. (Manchester, UK, The Alden Press).
40. Sinclair, J. C., Sandy, J., Delgoda, R., Sim, E., and Noble, M. E. (2000). Structure of arylamine N-acetyltransferase reveals a catalytic triad. Nat Struct Biol 7, 560-564.
41. Sollner, S., Nebauer, R., Ehammer, H., Prem, A., Deller, S., Palfey, B. A., Daum, G., and Macheroux, P. (2007). Lot6p from Saccharomyces cerevisiae is a FMN-dependent reductase with a potential role in quinone detoxification. FEBS J 274, 1328-1339.
42. Sollner, S., Deller, S., Macheroux, P., and Palfey, B. A. (2009a). Mechanism of flavin reduction and oxidation in the redox-sensing quinone reductase Lot6p from Saccharomyces cerevisiae. Biochemistry 48, 8636-8643.
43. Sollner, S., Schober, M., Wagner, A., Prem, A., Lorkova, L., Palfey, B. A., Groll, M., and Macheroux, P. (2009b). Quinone reductase acts as a redox switch of the 20S yeast proteasome. EMBO Rep 10, 65-70.
44. Sparla, F., Tedeschi, G., Pupillo, P., and 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.
45. Stolz, A. (2001). Basic and applied aspects in the microbial degradation of azo dyes. Appl Microbiol Biotechnol 56, 69-80.
46. Tomasz, M., and Palom, Y. (1997). The mitomycin bioreductive antitumor agents: cross-linking and alkylation of DNA as the molecular basis of their activity. Pharmacol Ther 76, 73-87.
47. Töwe, S., Leelakriangsak, M., Kobayashi, K., van Duy, N., Hecker, M., Zuber, P., and Antelmann, H. (2007). The MarR-type repressor MhqR (YkvE) regulates multiple dioxygenases/glyoxalases and an azoreductase which confer resistance to 2-methylhydroquinone and catechol in Bacillus subtilis. Mol Microbiol 66, 40-54.
48. Wang, C. J. (2008). Characterisation of azoreductases from Pseudomonas aeruginosa In Pharmacology (Oxford, University of Oxford), pp. 229.
49. Wang, C. J., Hagemeier, C., Rahman, N., Lowe, E., Noble, M., Coughtrie, M., Sim, E., and Westwood, I. (2007). Molecular cloning, characterisation and ligand-bound structure of an azoreductase from Pseudomonas aeruginosa. J Mol Biol 373, 1213-1228.
50. Wang, C. J., Laurieri, N., Abuhammad, A., Lowe, E., Westwood, I., Ryan, A., and Sim, E. (2010a). Role of Tyrosine 131 in the active site of paAzoR1, an azoreductase with specificity for the inflammatory bowel disease pro-drug balsalazide. Acta Crystallogr Sect F Struct Biol Cryst Commun 66, 2-7.
51. Wang, X., Jia, J., and Wang, Y. (2010b). Electrochemical degradation of reactive dye in the presence of water jet cavitation. Ultrason Sonochem 17, 515-520.
52. Ye, J., Yang, H. C., Rosen, B. P., and Bhattacharjee, H. (2007). Crystal structure of the flavoprotein ArsH from Sinorhizobium meliloti. FEBS Lett 581, 3996-4000.
53. You, S. J., Tseng, D. H., Ou, S. H., and Chang, W. K. (2007). Performance and microbial diversity of a membrane bioreactor treating real textile dyeing wastewater. Environ Technol 28, 935-941.
54. Zhang, J., Sun, Z., Li, Y., Peng, X., Li, W., Yan, Y. (2009). Biodegradation of p-nitrophenol by Rhodococcus sp. CN6 with high cell surface hydrophobicity. J Hazard Mater 163, 723-728.