Biosynthetic conclusions from the functional dissection of oxygenases for biosynthesis of actinorhodin and related streptomyces antibiotics

Chemistry and Biology

Volumn 20, Issue 4, 2013, Pages 510-520

  Taguchi, Takaaki ^a   Yabe, Masaki ^b,c   Odaki, Hitomi ^a   Shinozaki, Miki ^a   Metsä Ketelä, Mikko ^d   Arai, Takao ^c   Okamoto, Susumu ^b   Ichinose, Koji ^a  

^a MUSASHINO UNIVERSITY   (Japan)

^b NATIONAL FOOD RESEARCH INSTITUTE   (Japan)

^c TOKYO UNIVERSITY OF SCIENCE   (Japan)

^d UNIVERSITY OF TURKU   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

ACTINORHODINE; ANTIBIOTIC AGENT; FLAVIN DEPENDENT MONOOXYGENASE; GRANATICIN; HYDROXYL GROUP; OXYGENASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; DRUG STRUCTURE; DRUG SYNTHESIS; GENE CLUSTER; HYDROXYLATION; NONHUMAN; PRIORITY JOURNAL; STREPTOMYCES COELICOLOR;

ANTHRAQUINONES; ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; MIXED FUNCTION OXYGENASES; MULTIGENE FAMILY; NADH, NADPH OXIDOREDUCTASES; NAPHTHOQUINONES; QUINONES; RECOMBINANT PROTEINS; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; STREPTOMYCES;

STREPTOMYCES; STREPTOMYCES COELICOLOR;

EID: 84876482861     PISSN: 10745521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chembiol.2013.03.007     Document Type: Article

References (41)

1. A. Alfieri, F. Fersini, N. Ruangchan, M. Prongjit, P. Chaiyen, and A. Mattevi Structure of the monooxygenase component of a two-component flavoprotein monooxygenase Proc. Natl. Acad. Sci. USA 104 2007 1177 1182
2. P. Beltran-Alvarez, R.J. Cox, J. Crosby, and T.J. Simpson Dissecting the component reactions catalyzed by the actinorhodin minimal polyketide synthase Biochemistry 46 2007 14672 14681
3. S.D. Bentley, K.F. Chater, A.M. Cerdeño-Tárraga, G.L. Challis, N.R. Thomson, K.D. James, D.E. Harris, M.A. Quail, H. Kieser, and D. Harper Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2) Nature 417 2002 141 147
4. J.L. Caballero, E. Martinez, F. Malpartida, and D.A. Hopwood Organisation and functions of the actVA region of the actinorhodin biosynthetic gene cluster of Streptomyces coelicolor Mol. Gen. Genet. 230 1991 401 412
5. A. Craney, C. Ozimok, S.M. Pimentel-Elardo, A. Capretta, and J.R. Nodwell Chemical perturbation of secondary metabolism demonstrates important links to primary metabolism Chem. Biol. 19 2012 1020 1027
6. A. Das, and C. Khosla Biosynthesis of aromatic polyketides in bacteria Acc. Chem. Res. 42 2009 631 639
7. B. Floriano, and M. Bibb afsR is a pleiotropic but conditionally required regulatory gene for antibiotic production in Streptomyces coelicolor A3(2) Mol. Microbiol. 21 1996 385 396
8. T. Grocholski, T. Oja, L. Humphrey, P. Mäntsälä, J. Niemi, and M. Metsä-Ketelä Characterization of the two-component monooxygenase system AlnT/AlnH reveals early timing of quinone formation in alnumycin biosynthesis J. Bacteriol. 194 2012 2829 2836
9. D.A. Hopwood, F. Malpartida, H.M. Kieser, H. Ikeda, J. Duncan, I. Fujii, B.A.M. Rudd, H.G. Floss, and S. Omura Production of 'hybrid' antibiotics by genetic engineering Nature 314 1985 642 644
10. J. Huang, C.J. Lih, K.H. Pan, and S.N. Cohen Global analysis of growth phase responsive gene expression and regulation antibiotic biosynthetic pathways in Streptomyces coelicolor using DNA microarrays Genes Dev. 15 2001 3183 3192
11. K. Ichinose, D.J. Bedford, D. Tornus, A. Bechthold, M.J. Bibb, W.P. Revill, H.G. Floss, and D.A. Hopwood The granaticin biosynthetic gene cluster of Streptomyces violaceoruber Tü22: sequence analysis and expression in a heterologous host Chem. Biol. 5 1998 647 659
12. K. Ichinose, C. Surti, T. Taguchi, F. Malpartida, K.I. Booker-Milburn, G.R. Stephenson, Y. Ebizuka, and D.A. Hopwood Proof that the ACTVI genetic region of Streptomyces coelicolor A3(2) is involved in stereospecific pyran ring formation in the biosynthesis of actinorhodin Bioorg. Med. Chem. Lett. 9 1999 395 400
13. K. Ichinose, M. Ozawa, K. Itou, K. Kunieda, and Y. Ebizuka Cloning, sequencing and heterologous expression of the medermycin biosynthetic gene cluster of Streptomyces sp. AM-7161: towards comparative analysis of the benzoisochromanequinone gene clusters Microbiology 149 2003 1633 1645
14. P. Javidpour, T.P. Korman, G. Shakya, and S.-C. Tsai Structural and biochemical analyses of regio- and stereospecificities observed in a type II polyketide ketoreductase Biochemistry 50 2011 4638 4649
15. P. Kallio, P. Patrikainen, J.-P. Suomela, P. Mäntsälä, M. Metsä-Ketelä, and J. Niemi Flavoprotein hydroxylase PgaE catalyzes two consecutive oxygen-dependent tailoring reactions in angucycline biosynthesis Biochemistry 50 2011 5535 5543
16. R. Kaspera, and R. Croteau Cytochrome P450 oxygenases of Taxol biosynthesis Phytochem. Rev. 5 2006 433 444
17. S.G. Kendrew, D.A. Hopwood, and E.N.G. Marsh Identification of a monooxygenase from Streptomyces coelicolor A3(2) involved in biosynthesis of actinorhodin: purification and characterization of the recombinant enzyme J. Bacteriol. 179 1997 4305 4310
18. T. Kieser, M.J. Bibb, M.J. Buttner, K.F. Chater, and D.A. Hopwood Practical Streptomyces Genetics 2000 The John Innes Foundation Norwich, UK
19. F. Malpartida, and D.A. Hopwood Molecular cloning of the whole biosynthetic pathway of a Streptomyces antibiotic and its expression in a heterologous host Nature 309 1984 462 464
20. R. McDaniel, S. Ebert-Khosla, D.A. Hopwood, and C. Khosla Engineered biosynthesis of novel polyketides Science 262 1993 1546 1550
21. G.L. Newton, and R.C. Fahey Mycothiol biochemistry Arch. Microbiol. 178 2002 388 394
22. K. Ochi, and S. Okamoto A magic bullet for antibiotic discovery Chem. Biol. 19 2012 932 934
23. T. Oja, K. Palmu, H. Lehmussola, O. Leppäranta, K. Hännikäinen, J. Niemi, P. Mäntsälä, and M. Metsä-Ketelä Characterization of the alnumycin gene cluster reveals unusual gene products for pyran ring formation and dioxan biosynthesis Chem. Biol. 15 2008 1046 1057
24. S. Okamoto, T. Taguchi, K. Ochi, and K. Ichinose Biosynthesis of actinorhodin and related antibiotics: discovery of alternative routes for quinone formation encoded in the act gene cluster Chem. Biol. 16 2009 226 236
25. H. Onaka, M. Nakaho, K. Hayashi, Y. Igarashi, and T. Furumai Cloning and characterization of the goadsporin biosynthetic gene cluster from Streptomyces sp. TP-A0584 Microbiology 151 2005 3923 3933
26. R) in Streptomyces coelicolor Mol. Microbiol. 68 2008 861 870
27. J.-H. Park, C.-J. Cha, and J.-H. Roe Identification of genes for mycothiol biosynthesis in Streptomyces coelicolor A3(2) J. Microbiol. 44 2006 121 125
28. P. Patrikainen, P. Kallio, K. Fan, K.D. Klika, K.A. Shaaban, P. Mäntsälä, J. Rohr, K. Yang, J. Niemi, and M. Metsä- Ketelä Tailoring enzymes involved in the biosynthesis of angucyclines contain latent context-dependent catalytic activities Chem. Biol. 19 2012 647 655
29. 2)O Org. Lett. 2 2000 3225 3227
30. J. Sambrook, E.F. Fritsch, and T. Maniatis Molecular Cloning: A Laboratory Manual Second Edition 1989 Cold Spring Harbor Laboratory Cold Spring Harbor, NY
31. G. Sciara, S.G. Kendrew, A.E. Miele, N.G. Marsh, L. Federici, F. Malatesta, G. Schimperna, C. Savino, and B. Vallone The structure of ActVA-Orf6, a novel type of monooxygenase involved in actinorhodin biosynthesis EMBO J. 22 2003 205 215
32. T. Taguchi, Y. Ebizuka, D.A. Hopwood, and K. Ichinose A new mode of stereochemical control revealed by analysis of the biosynthesis of dihydrogranaticin in Streptomyces violaceoruber Tü22 J. Am. Chem. Soc. 123 2001 11376 11380
33. T. Taguchi, S. Okamoto, T. Itoh, Y. Ebizuka, K. Ochi, and K. Ichinose Actinoperylone, a novel perylenequinone-type shunt product, from a deletion mutant of the actVA-ORF5 and ORF6 genes for actinorhodin biosynthesis in Streptomyces coelicolor A3(2) Tetrahedron Lett. 49 2008 1208 1211
34. T. Taguchi, S. Okamoto, K. Hasegawa, and K. Ichinose Epoxyquinone formation catalyzed by a two-component flavin-dependent monooxygenase involved in biosynthesis of the antibiotic actinorhodin ChemBioChem 12 2011 2767 2773
35. T. Taguchi, T. Ebihara, A. Furukawa, Y. Hidaka, R. Ariga, S. Okamoto, and K. Ichinose Identification of the actinorhodin monomer and its related compound from a deletion mutant of the actVA-ORF4 gene of Streptomyces coelicolor A3(2) Bioorg. Med. Chem. Lett. 22 2012 5041 5045
36. K. Thotsaporn, J. Sucharitakul, J. Wongratana, C. Suadee, and P. Chaiyen Cloning and expression of p-hydroxyphenylacetate 3-hydroxylase from Acinetobacter baumannii: evidence of the divergence of enzymes in the class of two-protein component aromatic hydroxylases Biochim. Biophys. Acta 1680 2004 60 66
37. N. Tibrewal, P. Pahari, G. Wang, M.K. Kharel, C. Morris, T. Downey, Y. Hou, T.S. Bugni, and J. Rohr Baeyer-Villiger C-C bond cleavage reaction in gilvocarcin and jadomycin biosynthesis J. Am. Chem. Soc. 134 2012 18181 18184
38. J. Valton, L. Filisetti, M. Fontecave, and V. Nivière A two-component flavin-dependent monooxygenase involved in actinorhodin biosynthesis in Streptomyces coelicolor J. Biol. Chem. 279 2004 44362 44369
39. J. Valton, M. Fontecave, T. Douki, S.G. Kendrew, and V. Nivière An aromatic hydroxylation reaction catalyzed by a two-component FMN-dependent Monooxygenase. The ActVA-ActVB system from Streptomyces coelicolor J. Biol. Chem. 281 2006 27 35
40. J. Valton, C. Mathevon, M. Fontecave, V. Nivière, and D.P. Ballou Mechanism and regulation of the Two-component FMN-dependent monooxygenase ActVA-ActVB from Streptomyces coelicolor J. Biol. Chem. 283 2008 10287 10296
41. W.J.H. van Berkel, N.M. Kamerbeek, and M.W. Fraaije Flavoprotein monooxygenases, a diverse class of oxidative biocatalysts J. Biotechnol. 124 2006 670 689