SimC7 is a novel NAD(P)H-dependent ketoreductase essential for the antibiotic activity of the DNA gyrase inhibitor simocyclinone

Journal of Molecular Biology

Volumn 427, Issue 12, 2015, Pages 2192-2204

  Schäfer, Martin ^a   Le, Tung B K ^a   Hearnshaw, Stephen J ^a   Maxwell, Anthony ^a   Challis, Gregory L ^b   Wilkinson, Barrie ^a   Buttner, Mark J ^a  

^a JOHN INNES CENTRE   (United Kingdom)

^b UNIVERSITY OF WARWICK   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALCOHOL DEHYDROGENASE; ANTIINFECTIVE AGENT; COUMARIN DERIVATIVE; DNA TOPOISOMERASE (ATP HYDROLYSING); ENZYME INHIBITOR; GLYCOSIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE; RECOMBINANT PROTEIN; SIMOCYCLINONE D8;

BIOSYNTHESIS; BIOTRANSFORMATION; ENZYMOLOGY; GENE DELETION; GENETICS; METABOLISM; MULTIGENE FAMILY; OXIDATION REDUCTION REACTION; STREPTOMYCES ANTIBIOTICUS; STREPTOMYCES COELICOLOR;

ALCOHOL OXIDOREDUCTASES; ANTI-BACTERIAL AGENTS; BIOSYNTHETIC PATHWAYS; BIOTRANSFORMATION; COUMARINS; DNA GYRASE; ENZYME INHIBITORS; GENE DELETION; GLYCOSIDES; MULTIGENE FAMILY; NAD; OXIDATION-REDUCTION; RECOMBINANT PROTEINS; STREPTOMYCES ANTIBIOTICUS; STREPTOMYCES COELICOLOR;

EID: 84937760452     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2015.03.019     Document Type: Article

References (41)

1. J. Schimana, H.-P. Fiedler, I. Groth, R. Sussmuth, W. Beil, and M. Walker Simocyclinones, novel cytostatic angucyclinone antibiotics produced by Streptomyces antibioticus Tu 6040. I. Taxonomy, fermentation, isolation and biological activities J Antibiot (Tokyo) 53 2000 779 787
2. M.I. Andersson, and A.P. MacGowan Development of the quinolones J Antimicrob Chemother 51 2003 1 11
3. K. Drlica, H. Hiasa, R. Kerns, M. Malik, A. Mustaev, and X. Zhao Quinolones: action and resistance updated Curr Top Med Chem 9 2009 981 998
4. F. Collin, S. Karkare, and A. Maxwell Exploiting bacterial DNA gyrase as a drug target: current state and perspectives Appl Microbiol Biotechnol 92 2011 479 497
5. N.A. Gormley, G. Orphanides, A. Meyer, P.M. Cullis, and A. Maxwell The interaction of coumarin antibiotics with fragments of DNA gyrase B protein Biochemistry 35 1996 5083 5092
6. R.H. Flatman, A.J. Howells, L. Heide, H.-P. Fiedler, and A. Maxwell Simocyclinone D8: an inhibitor of DNA gyrase with a novel mode of action Antimicrob Agents Chemother 49 2005 1093 1100
7. M.J. Edwards, R.H. Flatman, L.A. Mitchenall, C.E. Stevenson, T.B.K. Le, and H.-P. Fiedler A crystal structure of the bifunctional antibiotic, simocyclinone D8, bound to DNA gyrase Science 326 2009 1415 1418
8. S.J. Hearnshaw, M.J. Edwards, C.E. Stevenson, D.M. Lawson, and A. Maxwell A new crystal structure of the bifunctional antibiotic simocyclinone D8 bound to DNA gyrase gives fresh insight into the mechanism of inhibition J Mol Biol 426 2014 2023 2033
9. M.J. Edwards, M.A. Williams, A. Maxwell, and A.R. McKay Mass spectrometry reveals that the antibiotic simocyclinone D8 binds to DNA gyrase in a "bent-over" conformation: evidence of positive cooperativity in binding Biochemistry 50 2011 3432 3440
10. J. Schimana, M. Walker, A. Zeeck, and H.-P. Fiedler Simocyclinones: diversity of metabolites is dependent on fermentation conditions J Ind Microbiol Biotechnol 27 2001 144 148
11. A. Trefzer, S. Pelzer, J. Schimana, S. Stockert, C. Bihlmaier, and H.-P. Fiedler Biosynthetic gene cluster of simocyclinone, a natural multihybrid antibiotic Antimicrob Agents Chemother 46 2002 1174 1182
12. U. Galm, J. Schimana, H.-P. Fiedler, J. Schmidt, S.M. Li, and L. Heide Cloning and analysis of the simocyclinone biosynthetic gene cluster of Streptomyces antibioticus Tu 6040 Arch Microbiol 178 2002 102 114
13. T.B.K. Le, H.-P. Fiedler, C.D. den Hengst, S.K. Ahn, A. Maxwell, and M.J. Buttner Coupling of the biosynthesis and export of the DNA gyrase inhibitor simocyclinone in Streptomyces antibioticus Mol Microbiol 72 2009 1462 1474
14. T.B.K. Le, C.E.M. Stevenson, H.-P. Fiedler, A. Maxwell, D.M. Lawson, and M.J. Buttner Structures of the TetR-like simocyclinone efflux pump repressor, SimR, and the mechanism of ligand-mediated derepression J Mol Biol 408 2011 40 56
15. T.B.K. Le, M.A. Schumacher, D.M. Lawson, R.G. Brennan, and M.J. Buttner The crystal structure of the TetR family transcriptional repressor SimR bound to DNA and the role of a flexible N-terminal extension in minor groove binding Nucleic Acids Res 39 2011 9433 9447
16. L. Horbal, Y. Rebets, M. Rabyk, R. Makitrynskyy, A. Luzhetskyy, and V. Fedorenko SimReg1 is a master switch for biosynthesis and export of simocyclinone D8 and its precursors AMB Express 2 2012 1
17. T. Luft, S.M. Li, H. Scheible, B. Kammerer, and L. Heide Overexpression, purification and characterization of SimL, an amide synthetase involved in simocyclinone biosynthesis Arch Microbiol 183 2005 277 285
18. M. Pacholec, C.L. Freel Meyers, M. Oberthur, D. Kahne, and C.T. Walsh Characterization of the aminocoumarin ligase SimL from the simocyclinone pathway and tandem incubation with NovM, P, N from the novobiocin pathway Biochemistry 44 2005 4949 4956
19. C. Anderle, S. Hennig, B. Kammerer, S.M. Li, L. Wessjohann, and B. Gust Improved mutasynthetic approaches for the production of modified aminocoumarin antibiotics Chem Biol 14 2007 955 967
20. A.C. Jones, B. Gust, A. Kulik, L. Heide, M.J. Buttner, and M.J. Bibb Phage P1-derived artificial chromosomes facilitate heterologous expression of the FK506 gene cluster PLoS One 8 2013 e69319
21. J.P. Gomez-Escribano, and M.J. Bibb Engineering Streptomyces coelicolor for heterologous expression of secondary metabolite gene clusters Microbial Biotechnol 4 2011 207 215
22. N. Ruiz, B. Falcone, D. Kahne, and T.J. Silhavy Chemical conditionality: a genetic strategy to probe organelle assembly Cell 121 2005 307 317
23. L.M. Oppegard, B.L. Hamann, K.R. Streck, K.C. Ellis, H.-P. Fiedler, and A.B. Khodursky In vivo and in vitro patterns of the activity of simocyclinone D8, an angucyclinone antibiotic from Streptomyces antibioticus Antimicrob Agents Chemother 53 2009 2110 2119
24. S. Alt, L.A. Mitchenall, A. Maxwell, and L. Heide Inhibition of DNA gyrase and DNA topoisomerase IV of Staphylococcus aureus and Escherichia coli by aminocoumarin antibiotics J Antimicrob Chemother 66 2011 2061 2069
25. M. Komatsu, T. Uchiyama, S. Omura, D.E. Cane, and H. Ikeda Genome-minimized Streptomyces host for the heterologous expression of secondary metabolism Proc Natl Acad Sci USA 107 2010 2646 2651
26. M. Komatsu, K. Komatsu, H. Koiwai, Y. Yamada, I. Kozone, and M. Izumikawa Engineered Streptomyces avermitilis host for heterologous expression of biosynthetic gene cluster for secondary metabolites ACS Synth Biol 2 2013 384 396
27. P. Cimermancic, M.H. Medema, J. Claesen, K. Kurita, L.C. Wieland Brown, and K. Mavrommatis Insights into secondary metabolism from a global analysis of prokaryotic biosynthetic gene clusters Cell 158 2014 412 421
28. M.H. Medema, P. Cimermancic, A. Sali, E. Takano, and M.A. Fischbach A systematic computational analysis of biosynthetic gene cluster evolution: lessons for engineering biosynthesis PLoS Comput Biol 10 2014 e1004016
29. Y. Kallberg, U. Oppermann, and B. Persson Classification of the short-chain dehydrogenase/reductase superfamily using hidden Markov models FEBS J 277 2010 2375 2386
30. B. Persson, and Y. Kallberg Classification and nomenclature of the superfamily of short-chain dehydrogenases/reductases (SDRs) Chem Biol Interact 202 2013 111 115
31. L.A. Kelley, and M.J. Sternberg Protein structure prediction on the Web: a case study using the Phyre server Nat Protoc 4 2009 363 371
32. K. Kulowski, E. Wendt-Pienkowski, L. Han, K.Q. Yang, L.C. Vining, and C.R. Hutchinson Functional characterization of the jadI gene as a cyclase forming angucyclinones J Am Chem Soc 121 1999 1786 1794
33. P. Javidpour, A. Das, C. Khosla, and S.C. Tsai Structural and biochemical studies of the hedamycin type II polyketide ketoreductase (HedKR): molecular basis of stereo- and regiospecificities Biochemistry 50 2011 7426 7439
34. T.P. Korman, Y.H. Tan, J. Wong, R. Luo, and S.C. Tsai Inhibition kinetics and emodin cocrystal structure of a type II polyketide ketoreductase Biochemistry 47 2008 1837 1847
35. P. Paananen, P. Patrikainen, P. Kallio, P. Mäntsälä, J. Niemi, and L. Niiranen Structural and functional analysis of angucycline C-6 ketoreductase LanV involved in landomycin biosynthesis Biochemistry 52 2013 5304 5314
36. M. Sosio, F. Giusino, C. Cappellano, E. Bossi, A.M. Puglia, and S. Donadio Artificial chromosomes for antibiotic-producing actinomycetes Nat Biotechnol 18 2000 343 345
37. B. Gust, G.L. Challis, K. Fowler, T. Kieser, and K.F. Chater PCR-targeted Streptomyces gene replacement identifies a protein domain needed for biosynthesis of the sesquiterpene soil odor geosmin Proc Natl Acad Sci USA 100 2003 1541 1546
38. B. Gust, G. Chandra, D. Jakimowicz, T. Yuqing, C.J. Bruton, and K.F. Chater Lambda red-mediated genetic manipulation of antibiotic-producing Streptomyces Adv Appl Microbiol 54 2004 107 128
39. T. Kieser, M.J. Bibb, M.J. Buttner, K.F. Chater, and D.A. Hopwood Practical Streptomyces Genetics 2000 The John Innes Foundation Norwich
40. M. Holzenkampfer, M. Walker, A. Zeeck, J. Schimana, and H.-P. Fiedler Simocyclinones, novel cytostatic angucyclinone antibiotics produced by Streptomyces antibioticus Tu 6040 II. Structure elucidation and biosynthesis J Antibiot (Tokyo) 55 2002 301 307
41. I. Wiegand, K. Hilpert, and R.E. Hancock Agar and broth dilution methods to determine the minimal inhibitory concentration (MIC) of antimicrobial substances Nat Protoc 3 2008 163 175