Structure of the quinoline N-hydroxylating cytochrome P450 RauA, an essential enzyme that confers antibiotic activity on aurachin alkaloids

FEBS Letters

Volumn 588, Issue 1, 2014, Pages 105-110

  Yasutake, Yoshiaki ^a   Kitagawa, Wataru ^a,b   Hata, Miyako ^a   Nishioka, Taiki ^b   Ozaki, Taro ^c,d   Nishiyama, Makoto ^c   Kuzuyama, Tomohisa ^c   Tamura, Tomohiro ^a,b  

^a NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

^b HOKKAIDO UNIVERSITY   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

^d UNIVERSITY OF TOKYO   (Japan)

Author keywords

Antibiotic; Aurachin; CYP; Cytochrome P450; Menaquinone; Rhodococcus erythropolis

Indexed keywords

ALKALOID; AURACHIN; QUINOLINE DERIVED ANTIINFECTIVE AGENT; RAUA ENZYME; UNCLASSIFIED DRUG;

ANTIMICROBIAL ACTIVITY; ARTICLE; BACTERIUM IDENTIFICATION; BINDING AFFINITY; BINDING SITE; CONTROLLED STUDY; DRUG BINDING; DRUG DETERMINATION; DRUG EFFICACY; DRUG HYDROXYLATION; DRUG SCREENING; DRUG STRUCTURE; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME SUBSTRATE COMPLEX; HYDROPHOBICITY; NONHUMAN; PRIORITY JOURNAL; RHODOCOCCUS ERYTHROPOLIS;

RHODOCOCCUS ERYTHROPOLIS;

EID: 84890998798     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2013.11.016     Document Type: Article

References (43)

1. B. Kunze, G. Höfle, and H. Reichenbach Aurachins, new quinoline antibiotics from myxobacteria: production, physico-chemical and biochemical properties J. Antibiot. 40 1987 258 265
2. A. Sandmann, J. Dickschat, H. Jenke-Kodama, B. Kunze, E. Dittmann, and R. Müller A type II polyketide synthase from the gram-negative bacterium Stigmatella aurantiaca is involved in aurachin alkaloid biosynthesis Angew. Chem., Int. Ed. 46 2007 2712 2716
3. J. Nachtigall, K. Schneider, G. Nicholson, M. Goodfellow, H. Zinecker, J.F. Imhoff, R.D. Süssmuth, and H.P. Fiedler Two new aurachins from Rhodococcus sp. Acta 2259 J. Antibiot. 63 2010 567 569
4. D. Pistorius, Y. Li, A. Sandmanny, and R. Müller Completing the puzzle of aurachin biosynthesis in Stigmatella aurantiaca Sg a15 Mol. BioSyst. 7 2011 3308 3315
5. W. Kitagawa, and T. Tamura Three types of antibiotics produced from Rhodococcus erythropolis strains Microbes Environ. 23 2008 167 171
6. W. Kitagawa, and T. Tamura A quinoline antibiotic from Rhodococcus erythropolis JCM 6824 J. Antibiot. 61 2008 680 682
7. W. Kitagawa, T. Ozaki, T. Nishioka, Y. Yasutake, M. Hata, M. Nishiyama, T. Kuzuyama, and T. Tamura Cloning and heterologous expression of the aurachin RE biosynthesis gene cluster afford a novel cytochrome P-450 for quinoline N-hydroxylation ChemBioChem 14 2013 1085 1093
8. S. Romagnoli, W. Oettmeier, and D. Zannoni The effects of decyl aurachins C and D on the respiratory electron flow of facultative phototrophic bacteria Biochem. Mol. Biol. Int. 39 1996 671 678
9. 2 biosynthesis promising drug targets? Molecules 15 2010 1531 1553
10. M. Kurosu, P. Narayanasamy, K. Biswas, R. Dhiman, and D.C. Crick Discovery of 1,4-dihydroxy-2-naphthoate prenyltransferase inhibitors: new drug leads for multidrug-resistant Gram-positive pathogens J. Med. Chem. 50 2007 3973 3974
11. M. Kurosu, and D.C. Crick MenA is a promising drug target for developing novel lead molecules to combat Mycobacterium tuberculosis Med. Chem. 5 2009 197 207
12. J. Debnath, S. Siricilla, B. Wan, D.C. Crick, A.J. Lenaerts, S.G. Franzblau, and M. Kurosu Discovery of selective menaquinone biosynthesis inhibitors against Mycobacterium tuberculosis J. Med. Chem. 55 2012 3739 3755
13. M.J. Coon, X.X. Ding, S.J. Pernecky, and A.D. Vaz Cytochrome P450: progress and predictions FASEB J. 6 1992 669 673
14. A.W. Munro, H.M. Grivan, A.E. Mason, A.J. Dunford, and K.J. McLean What makes a P450 tick? Trends Biochem. Sci. 38 2013 140 150
15. D. Mansuy Cytochrome P-450 and model systems: great diversity of catalyzed reactions Pure Appl. Chem. 68 1994 737 744
16. D. Kim, and F.P. Guengerich Cytochrome P450 activation of arylamines and heterocyclic amines Annu. Rev. Pharmacol. Toxicol. 45 2005 27 49
17. 3 hydroxylase from Pseudonocardia autotrophica Biochem. Biophys. Res. Commun. 385 2009 170 175
18. T. Omura, and R. Sato The carbon monoxide-binding pigment of liver microsomes. I. Evidence for its hemoprotein nature J. Biol. Chem. 239 1964 2370 2378
19. P.-F. Chen, V. Berka, A.-L. Tsai, and K.K. Wu Effects of Asp-369 and Arg-372 mutations on heme environment and function in human endothelial nitric-oxide synthase J. Biol. Chem. 273 1998 34164 34170
20. T.G. Battye, L. Kontogiannis, O. Johnson, H.R. Powell, and A.G. Leslie IMOSFLM: a new graphical interface for diffraction-image processing with MOSFLM Acta Crystallogr., Sect. D: Biol. Crystallogr. 67 2011 271 281
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., Sect. D: Biol. Crystallogr. 67 2011 235 242
22. A.J. McCoy, R.W. Grosse-Kunstleve, P.D. Adams, M.D. Winn, L.C. Storoni, and R.J. Read Phaser crystallographic software J. Appl. Crystallogr. 40 2007 674 685
23. BioI ACP complex Proc. Natl. Acad. Sci. USA 105 2008 15696 15701
24. G.N. Murshudov, P. Skubak, A.A. Lebedev, N.S. Pannu, R.A. Steiner, R.A. Nicholls, M.D. Winn, F. Long, and A.A. Vagin REFMAC5 for the refinement of macromolecular crystal structures Acta Crystallogr., Sect. D: Biol. Crystallogr. 67 2011 355 367
25. P. Emsley, B. Lohkamp, W.G. Scott, and K. Cowtan Features and development of Coot Acta Crystallogr., Sect. D: Biol. Crystallogr. 66 2010 486 501
26. R.A. Laskowski, M.W. MacArthur, D.S. Moss, and J.M. Thornton procheck: a program to check the stereochemical quality of protein structures J. Appl. Crystallogr. 26 1993 283 291
27. A. Dereeper, V. Guignon, G. Blanc, S. Audic, S. Buffet, F. Chevenet, J.F. Dufayard, S. Guindon, V. Lefort, M. Lescot, J.M. Claverie, and O. Gascuel Phylogeny.fr: robust phylogenetic analysis for the nonspecialist Nucleic Acids Res. 36 2008 W465 W469
28. E. Uchida, N. Kagawa, T. Sakaki, N. Urushiro, N. Sawada, M. Kamakura, M. Ohta, S. Kato, and K. Inoue Purification and characterization of mouse CYP27B1overproduced by an Escherichia coli system coexpressing molecular chaperonins GroEL/ES Biochem. Biophy. Res. Commun. 323 2004 505 511
29. S. Han, S. Choi, Y.-J. Chun, C.-H. Yun, C.H. Lee, H.J. Shin, H.S. Na, M.W. Chung, and D. Kim Functional characterization of allelic variants of polymorphic human cytochrome P450 2A6 (CYP2A6a5a-a-19, and a5) Biol. Pharm. Bull. 35 2012 394 399
30. J. Guo, Y.J. Zhou, M.L. Hillwig, Y. Shen, L. Yang, Y. Wang, X. Zhang, W. Liu, R.J. Peters, X. Chen, Z.K. Zhao, and L. Huang CYP76AH1 catalyzes turnover of miltiradiene in tanshinones biosynthesis and enables heterologous production of ferruginol in yeasts Proc. Natl. Acad. Sci. USA 110 2013 12108 12113
31. 26-monooxygenase activity in Mycobacterium tuberculosis revealed by biochemical and genetic analyses J. Biol. Chem. 285 2010 36352 36360
32. Q. Wang, M.L. Hillwig, K. Okada, K. Yamazaki, Y. Wu, S. Swaminathan, H. Yamane, and R.J. Peters Characterization of CYP76M5-8 indicates metabolic plasticity within a plant biosynthetic gene cluster J. Biol. Chem. 287 2012 6159 6168
33. J.B. Schenkman, H. Remmer, and R.W. Estabrook Spectral studies of drug interaction with hepatic microsomal cytochrome Mol. Pharmacol. 3 1967 113 123
34. T. Beitlich, K. Kühnel, C. Schulze-Briese, R.L. Shoeman, and I. Schlichting Cryoradiolytic reduction of crystalline heme proteins: analysis by UV-Vis spectroscopy and X-ray crystallography J. Synchrotron Rad. 14 2007 11 23
35. S. Nagano, and L. Poulos Crystallographic study on the dioxygen complex of wild-type and mutant cytochrome P450cam: implications for the dioxygen activation mechanism J. Biol. Chem. 280 2005 31659 31663
36. L. Holm, and C. Sander Dali: a network tool for protein structure comparison Trends Biochem. Sci. 20 1995 478 480
37. 3 hydroxylase J. Biol. Chem. 285 2010 31193 31201
38. C. Savino, L.C. Montemiglio, G. Sciara, A.E. Miele, S.G. Kendrew, P. Jemth, S. Gianni, and B. Vallone Investigating the structural plasticity of a cytochrome P450: three-dimensional structures of P450 EryK and binding to its physiological substrate J. Biol. Chem. 284 2009 29170 29179
39. D.H. Sherman, S. Li, L.V. Yermalitskaya, Y. Kim, J.A. Smith, M.R. Waterman, and L.M. Podust The structural basis for substrate anchoring, active site selectivity, and product formation by P450 PikC from Streptomyces venezuelae J. Biol. Chem. 281 2006 26289 26297
40. C.R. Agnew, A.G. Warrilow, N.M. Burton, D.C. Lamb, S.L. Kelly, and R.L. Brady An enlarged, adaptable active site in CYP164 family P450 enzymes, the sole P450 in Mycobacterium leprae Antimicrob. Agents Chemother. 56 2012 391 402
41. D.R. Nelson The cytochrome P450 homepage Human Genomics 4 2009 59 65
42. I. Shamovsky, L. Ripa, L. Börjesson, C. Mee, B. Nordén, P. Hansen, C. Hasselgren, M. O'Donovan, and P. Sjö Explanation for main features of structure-genotoxicity relationships of aromatic amines by theoretical studies of their activation pathways in CYP1A2 J. Am. Chem. Soc. 133 2011 16168 16185
43. L. Ji, and G. Schüürmann Model and mechanism: N-hydroxylation of primary aromatic amines by cytochrome P450 Angew. Chem., Int. Ed. 52 2013 744 748