Cloning, sequencing, and functional analysis of an iterative type I polyketide synthase gene cluster for biosynthesis of the antitumor chlorinated polyenone neocarzilin in "Streptomyces carzinostaticus"

Antimicrobial Agents and Chemotherapy

Volumn 48, Issue 9, 2004, Pages 3468-3476

  Otsuka, Miyuki ^a   Ichinose, Koji ^a   Fujii, Isao ^a   Ebizuka, Yutaka ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ACYLTRANSFERASE; AMINO ACID; ANTINEOPLASTIC AGENT; GENE PRODUCT; NEOCARZILIN A; NEOCARZILIN B; NEOCARZILIN C; POLYENE ANTIBIOTIC AGENT; POLYKETIDE SYNTHASE; POLYKETIDE SYNTHASE TYPE 1; PROTEIN ORF3; PROTEIN ORF4; PROTEIN ORF5; PROTEIN ORF6; THIOESTERASE TYPE II; THIOL ESTER HYDROLASE; UNCLASSIFIED DRUG; ZINOSTATIN;

AMINO ACID SEQUENCE; ARTICLE; CATALYSIS; CATALYST; DECARBOXYLATION; DNA SEQUENCE; DRUG STRUCTURE; DRUG SYNTHESIS; GENE CLUSTER; GENE DISRUPTION; GENE FUNCTION; GENE SEQUENCE; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; REACTION ANALYSIS; SEQUENCE ANALYSIS; STREPTOMYCES; STREPTOMYCES CARZINOSTATICUS;

ACETATES; ANTIBIOTICS, ANTINEOPLASTIC; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CLONING, MOLECULAR; COSMIDS; DNA, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; GENE LIBRARY; GENES, BACTERIAL; KETONES; MAGNETIC RESONANCE SPECTROSCOPY; MULTIENZYME COMPLEXES; MULTIGENE FAMILY; PLASMIDS; SPECTROPHOTOMETRY, ULTRAVIOLET; STREPTOMYCES;

EID: 4344691233     PISSN: 00664804     EISSN: None     Source Type: Journal    
DOI: 10.1128/AAC.48.9.3468-3476.2004     Document Type: Article

References (53)

1. Ahlert, J., E. Shepard, N. Lomovskaya, E. Zazopoulos, A. Staffa, B. O. Bachmann, K. Huang, L. Fonstein, A. Czisny, R. E. Whitwam, C. M. Farnet, and J. S. Thornson. 2002. The calicheamicin gene cluster and its iterative type I enediyne PKS. Science 297:1173-1175.
2. Bibb, M. J., P. R. Findlay, and M. W. Johnson. 1984. The relationship between base composition and codon usage in bacterial genes and its use for the simple and reliable identification of protein-coding sequences. Gene 30:157-166.
3. Bierman, M., R. Logan, K. O'Brien, E. T. Seno, R. N. Rao, and B. E. Schoner. 1992. Plasmid cloning vectors for the conjugal transfer of DNA from Escherichia coli to Streptomyces spp. Gene 116:43-49.
4. Bisang, C., P. F. Long, J. Cortes, J. Westcott, J. Crosby, A. L. Matharu, R. Cox, T. J. Simpson, J. Staunton, and P. F. Leadlay. 1999. A chain initiation factor common to both modular and aromatic polyketide synthases. Nature 401:502-505.
5. Buller, A. R., N. Bate, and E. Cundliffe. 1999. Impact of thioesterase activity on tylosin biosynthesis in Streptomyces fradiae. Chem. Biol. 6:287-292.
6. Chang, Z., P. Flatt, W. H. Gerwick, V.-A. Nguyen, C. L. Willis, and D. H. Sherman. 2002. The barbamide biosynthetic gene cluster: a novel marine cyanobacterial system of mixed polyketide synthase (PKS)-non-ribosomal peptide synthase (NRPS) origin involving an unusual trichloroleucyl starter unit. Gene 296:235-247.
7. Cheng, Y.-Q., G.-L. Tang, and B. Shen. 2002. Identification and localization of the gene cluster encoding biosynthesis of the antitumor macrolactam leinamycin in Streptomyces atroolivaceus S-140. J. Bacteriol. 184:7013-7024.
8. Cheng, Y.-Q., G.-L. Tang, and B. Shen. 2003. Type I polyketide synthase requiring a discrete acyltransferase for polyketide biosynthesis. Proc. Natl. Acad. Sci. USA 100:3149-3154.
9. Dairi, T., T. Nakano, K. Aisaka, R. Katsumata, and M. Hasegawa. 1995. Cloning and nucleotide sequence of the gene responsible for chlorination of tetracycline. Biosci. Biotechnol. Biochem. 59:1099-1106.
10. Denoya, C. D., R. W. Fedechko, E. W. Hafner, A. I. McArthur, M. R. Morgenstern, D. D. Skinner, K. Stutzman-Engwall, R. G. Wax, and W. C. Wernau. 1995. A second branched-chain α-keto acid dehydrogenase gene cluster (bkdFGH) from Streptomyces avermitilis: its relationship to avermectin biosynthesis and the construction of a bkdF mutant suitable for the production of novel antiparasitic avermectins. J. Bacteriol. 177:3504-3511.
11. Duitman, E. H., L. W. Hamoen, M. Remhold, G. Venema, H. Seitz, W. Saenger, F. Bernhard, R. Reinhardt, M. Schmidt, C. Ullrich, T. Stein, F. Leenders, and J. Vater. 1999. The mycosubtilin synthetase of Bacillus subtilis ATCC6633: a multifunctional hybrid between a peptide synthetase, an amino transferase, and a fatty acid synthase. Proc. Natl. Acad. Sci. USA 96:13294-13299.
12. Edo, K., M. Mizugaki, Y. Koide, H. Seto, K. Furihata, N. Otake, and N. Ishida. 1985. The structure of neocarzinostatin chromophore possessing a novel bycyclo[7,3,0]dodecadiyne system. Tetrahedron Lett. 26:331-334.
13. El-Sayed, A. K., J. Hothersall, S. M. Cooper, E. Stephens, T. J. Simpson, and C. M. Thomas. 2003. Characterization of the mupirocin biosynthesis gene cluster from Pseudomonas fluorescent NCIMB 10586. Chem. Biol. 10:419-430.
14. Funa, N., Y. Ohnishi, I. Fujii, M. Shibuya, Y. Ebizuka, and S. Horinouchi. 1999. A new pathway for polyketide synthesis in microorganisms. Nature 400:897-899.
15. Gaisser, S., A. Trefzer, S. Stockert, A. Kirschning, and A. Bechthold. 1997. Cloning of an avilamycin biosynthetic gene cluster from Streptomyces viridochromogenes Tü57. J. Bacteriol. 179:6271-6278.
16. Gaitatzis, N., B. Silakowski, B. Kunze, G. Nordsiek, H. Blöcker, G. Höfle, and R. Müller. 2002. The biosynthesis of the aromatic myxobacterial electron transport inhibitor stigmatellin is directed by novel type of modular polyketide synthase. J. Biol. Chem. 277:13082-13090.
17. Gribble, G. W. 2003. The diversity of naturally produced organohalogens. Chemosphere 52:289-297.
18. Hammer, P. E., D. S. Hill, S. T. Lam, K.-H. van Pee, and J. M. Ligon. 1997. Four genes from Pseudomonas fluorescens that encode the biosynthesis of pyrrolnitrin. Appl. Environ. Microbiol. 63:2147-2154.
19. Heathcote, M. L., J. Staunton, and P. F. Leadlay. 2001. Role of type II thioesterases: evidence for removal of short acyl chains produced by aberrant decarboxylation of chain extender units. Chem. Biol. 8:207-220.
20. Hohaus, K., A. Altmann, W. Burd, I. Fischer, P. E. Hammer, D. S. Hill, J. M. Ligon, and K.-H. van Pée. 1997. NADH-dependent halogenases are more likely to be involved in halometabolite biosynthesis than haloperoxidases. Angew. Chem. Int. Engl. Ed. 36:2012-2013.
21. Hopwood, D. A. 1997. Genetic contributions to understanding polyketide synthases. Chem. Rev. 97:2465-2497.
22. Ikeda, H., T. Nonomiya, M. Usami, T. Ohta, and S. Omura. 1999. Organization of the biosynthetic gene cluster for the polyketide anthelmintic macrolide avermectin in Streptomyces avermitilis. Proc. Natl. Acad. Sci. USA 96:9509-9514.
23. Ishida, N., K. Miyazaki, K. M. Kumagai, and M. Rikimaru. 1965. Neocarzinostatin, an antitumor antibiotic of high molecular weight. J. Antibiot. 18:68-76.
24. Ishikawa, J., and K. Hotta. 1999. FramePlot: a new implementation of the frame analysis for predicting protein-coding regions in bacterial DNA with a high G+C content. FEMS Microbiol. Lett. 174:251-253.
25. Ishikawa, J., N. Tsuchizaki, M. Yoshida, D. Ishijama, and K. Hotta. 2000. Colony PCR for detection of specific DNA sequences in actinomycetes. Actinomycetologica 14:1-5.
26. Kaneda, T. 1991. Iso- and anteoiso-fatty acids in bacteria: biosynthesis, function, and taxonomic significance. Microbiol. Rev. 55:288-302.
27. Keller, S., T. Wage, K. Hohaus, M. Hölzer, E. Eichhorn, and K.-H. van Pée. 2000. Purification and partial characterization of tryptophan 7-halogenase (PrnA) from Pseudomonas fluorescens. Angew. Chem. Int. Ed. 39:2300-2302.
28. Kieser, T., M. J. Bibb, M. J. Buttner, K. F. Chater, and D. A. Hopwood. 2000. Practical Streptomyces genetics. The John Innes Foundation, Norwich, England.
29. Lau, J., D. E. Cane, and C. Khosla. 2000. Substrate specificity of the loading didomain of the erythromycin polyketide synthase. Biochemistry 39:10514-10520.
30. Liu, W., S. D. Christenson, S. Standage, and B. Shen. 2002. Biosynthesis of the enediyne antitumor antibiotic C-1027. Science 297:1170-1173.
31. Lomoskaya, N. D., K. F. Chater, and N. M. Mkrtumian. 1980. Genetics and molecular biology of Streptomyces bacteriophages. Microbiol. Rev. 44:206-229.
32. McDaniel, R., S. E. Khosla, D. A. Hopwood, and C. Khosla. 1993. Engineered biosynthesis of novel polyketides. Science 262:1546-1550.
33. Nowak-Thompson, B., N. Chaney, J. S. Wing, S. J. Gould, and J. E. Loper. 1999. Characterization of the pyoluteorin biosynthetic gene cluster of Pseudomonas fluorescens Pf-5. J. Bacteriol. 181:2166-2174.
34. Nozoe, S., N. Ishii, G. Kusano, K. Kikuchi, and T. Ohta. 1992. Neocarzilins A and B, novel polyenones from Streptomyces carzinostaticus. Tetrahedron Lett. 33:7547-7550.
35. Nozoe, S., K. Kikuchi, N. Ishii, and T. Ohta. 1992. Synthesis of neocarzilin A: an absolute stereochemistry. Tetrahedron Lett. 33:7551-7552.
36. Onaka, H., S. Taniguchi, Y. Igarashi, and T. Furumai. 2003. Characterization of the biosynthetic gene cluster of rebeccamycin from Lechevaleria aerocolonigenes ATCC 39243. Biosci. Biotechnol. Biochem. 67:127-138.
37. Paitan, Y., G. Alon, E. Orr, E. Z. Ron, and E. Rosenberg. 1999. The first gene in the biosynthesis of the polyketide antibiotic TA of Myxococcus xanthus codes for a unique PKS module coupled to a peptide synthetase. J. Mol. Biol. 286:465-474.
38. Pelzer, S., R. Süßmuth, D. Heckmann, J. Recktenwald, P. Huber, G. Jung, and W. Wohlleben. 1999. Identification and analysis of the balhimycin biosynthetic gene cluster and its use for manipulating glycopeptide biosynthesis in Amycolatopsis mediterranei DSM5908. Antimicrob. Agents Chemother. 43:1565-1573.
39. Pereda, A., R. G. Summers, D. L. Stassi, X. A. Ruan, and L. Katz. 1998. The loading domain of the erythromycin polyketide synthase is not essential for erythromycin biosynthesis in Saccharopolyspora erythraea. Microbiology 144: 543-553.
40. Piel, J. 2002. A polyketide synthase-peptide synthase gene cluster from an uncultured bacterial symbiont of Paederus beetles. Proc. Natl. Acad. Sci. USA 99:14002-14007.
41. Piraee, M., and L. C. Vining. 2002. Use of degenerate primers and touchdown PCR to amplify a halogenase gene fragment from Streptomyces venezuelae ISP5230. J. Ind. Microbiol. Biotechnol. 29:1-5.
42. Sanchez, C., I. A. Butovich, A. F. Brana, J. Rohr, C. Mendez, and J. A. Salas. 2002. The biosynthetic gene cluster for the antitumor rebeccamycin: characterization and generation of indolocarbazole derivatives. Chem. Biol. 9:519-531.
43. Scrutton, N. S., A. Berry, and R. N. Perham. 1990. Redesign of the coenzyme specificity of a dehydrogenase by protein engineering. Nature 343:38-43.
44. Shima, J., A. Hesketh, S. Okamoto, S. Kawamoto, and K. Ochi. 1996. Induction of actinorhodin production by rpsL (encoding ribosomal protein S12) mutations that confer streptomycin resistance in Streptomyces lividans and Streptomyces coelicolor A3(2). J. Bacteriol. 178:7276-7284.
45. Silakowski, B., G. Nordsiek, B. Kunze, H. Blöcker, and R. Müller. 2001. Novel features in a combined polyketide synthase/non- ribosomal peptide synthetase: the myxalamid biosynthetic gene cluster of the myxobacterium Stigmatella aurantiaca Sga15. Chem. Biol. 8:59-64.
46. Sitachitta, N., B. L. Márquez, R. T. Williamson, J. Rossi, M. A. Roberts, W. H. Gerwick, V.-A. Nguyen, and C. L. Willis. 2000. Biosynthetic pathway and origin of the chlorinated methyl group in barbamide and dechlorobarbamide, metabolites from marine cyanobacterium Lyngbya majuscula. Tetrahedron 56:9103-9113.
47. Skinner, D. D., M. R. Morgenstern, R. W. Fedechko, and C. D. Denova. 1995. Cloning and sequencing of a cluster of genes encoding branched-chain alpha-keto acid dehydrogenase from Streptomyces avermitilis and the production of a functional E1 [αβ] component in Escherichia coli. J. Bacteriol. 177:183-190.
48. Smokvina, T., P. Mazodier, F. Boccard, C. J. Thompson, and M. Guérieneau. 1990. Construction of a series of pSAM2-based integrative vectors for use in actinomycetes. Gene 94:53-59.
49. Strohl, W. R. 1992. Compilation and analysis of DNA sequences associated with apparent streptomycete promoters. Nucleic Acids Res. 20:961-974.
50. Taguchi, T., K. Itou, Y. Ebizuka, F. Malpartida, D. A. Hopwood, C. M. Surti, K. I. Booker-Milburn, G. R. Stephenson, and K. Ichinose. 2000. Chemical characterisation of disruptants of the Streptomyces coelicolor A3(2) actVI genes involved in actinorhodin biosynthesis. J. Antibiot. 53:144-152.
51. Tang, L., S. Shah, L. Chung, J. Carney, L. Katz, C. Khosla, and B. Julien. 2000. Cloning and heterologous expression of the epothilone gene cluster. Science 287:640-642.
52. Van Wageningen, A. M. A., P. N. Kirkpatrick, D. H. Williams, B. R. Harris, J. K. Kershaw, N. J. Lennard, M. Jones, S. J. M. Jones, and P. J. Solenberg. 1998. Sequencing and analysis of genes involved in the biosynthesis of a vancomycin group antibiotic. Chem. Biol. 5:155-162.
53. Xue, Y., L. Zhao, H.-W. Liu, and D. H. Sherman. 1998. A gene cluster for macrolide antibiotic biosynthesis in Streptomyces venezuelae: architecture of metabolic diversity. Proc. Natl. Acad. Sci. USA 95:12111-12116.