Identification of the chelocardin biosynthetic gene cluster from Amycolatopsis sulphurea: A platform for producing novel tetracycline antibiotics

Microbiology (United Kingdom)

Volumn 159, Issue PART 12, 2013, Pages 2524-2532

  Lukežič, Tadeja ^a   Lešnik, Urška ^a,b   Podgoršek, Ajda ^a,f   Horvat, Jaka ^a   Polak, Tomaž ^b   Šala, Martin ^c   Jenko, Branko ^a,f   Raspor, Peter ^b   Herron, Paul R ^e   Hunter, Iain S ^e   Petković, Hrvoje ^a,d  

^a ACIES BIO D O O   (Slovenia)

^b UNIVERSITY OF LJUBLJANA   (Slovenia)

^c NATIONAL INSTITUTE OF CHEMISTRY   (Slovenia)

^d UNIVERSITY OF CANTABRIA   (Spain)

^e UNIVERSITY OF STRATHCLYDE   (United Kingdom)

^f Centre of Excellence for Integrated Approaches in Chemistry and Biology of Proteins (CIPKeBiP)   (Slovenia)

Author keywords

[No Author keywords available]

Indexed keywords

ACYL CARRIER PROTEIN; AMINOTRANSFERASE; AROMATASE; GLYCOSYLTRANSFERASE; LONG CHAIN FATTY ACID COENZYME A LIGASE; METHYLTRANSFERASE; OXYGENASE; POLYKETIDE SYNTHASE; TETRACYCLINE;

ACTINOBACTERIA; AMYCOLATOPSIS SULPHUREA; AROMATIZATION; ARTICLE; CYCLIZATION; DNA ISOLATION; DNA SEQUENCE; ESCHERICHIA COLI; GENE CLUSTER; GENE IDENTIFICATION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HYDROXYLATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OPEN READING FRAME; PRIORITY JOURNAL; SOUTHERN BLOTTING; STEREOCHEMISTRY;

ACTINOMYCETALES; ANTI-BACTERIAL AGENTS; BIOSYNTHETIC PATHWAYS; DNA, BACTERIAL; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; OPEN READING FRAMES; SEQUENCE ANALYSIS, DNA; TETRACYCLINES;

EID: 84888864591     PISSN: 13500872     EISSN: 14652080     Source Type: Journal    
DOI: 10.1099/mic.0.070995-0     Document Type: Article

References (51)

1. Ames, B. D., Korman, T. P., Zhang, W., Smith, P., Vu, T., Tang, Y. & Tsai, S. C. (2008). Crystal structure and functional analysis of tetracenomycin ARO/CYC: implications for cyclization specificity of aromatic polyketides. Proc Natl Acad Sci U S A 105, 5349-5354.
2. Bao, W., Wendt-Pienkowski, E. & Hutchinson, C. R. (1998). Reconstitution of the iterative type II polyketide synthase for tetracenomycin F2 biosynthesis. Biochemistry 37, 8132-8138.
3. Bierman, M., Logan, R., O'Brien, K., Seno, E. T., Rao, R. N. & Schoner, B. E. (1992). Plasmid cloning vectors for the conjugal transfer of DNA from Escherichia coli to Streptomyces spp. Gene 116, 43-49.
4. Bisang, C., Long, P. F., Cortés, J., Westcott, J., Crosby, J., Matharu, A. L., Cox, R. J., Simpson, T. J., Staunton, J. & Leadlay, P. F. (1999). A chain initiation factor common to both modular and aromatic polyketide synthases. Nature 401, 502-505.
5. Carreras, C. W. & Khosla, C. (1998). Purification and in vitro reconstitution of the essential protein components of an aromatic polyketide synthase. Biochemistry 37, 2084-2088.
6. Chiba, K., Hoshino, Y., Ishino, K., Kogure, T., Mikami, Y., Uehara, Y. & Ishikawa, J. (2007). Construction of a pair of practical Nocardia-Escherichia coli shuttle vectors. Jpn J Infect Dis 60, 45-47.
7. Chopra, I. (1994). Tetracycline analogs whose primary target is not the bacterial ribosome. Antimicrob Agents Chemother 38, 637-640.
8. Chopra, I., Hawkey, P. M. & Hinton, M. (1992). Tetracyclines, molecular and clinical aspects. J Antimicrob Chemother 29, 245-277.
9. Chu, D. T. W., Huckin, S. N., Bernstein, E., Garmaise, D. L., Egan, R. S. & Stanaszek, R. S. (1981). Chemistry of chelocardin. V. Condensation with amino reagents. Can J Chem 59, 763-767.
10. Das, A. & Khosla, C. (2009). Biosynthesis of aromatic polyketides in bacteria. Acc Chem Res 42, 631-639.
11. Dhingra, G., Kumari, R., Bala, S., Majumdar, S., Malhotra, S., Sharma, P., Lal, S., Cullum, J. & Lal, R. (2003). Development of cloning vectors and transformation methods for Amycolatopsis. J Ind Microbiol Biotechnol 30, 195-204.
12. Fu, H., Ebert-Kkhosla, S., Hopwood, D. A. & Khosla, C. (1994). Relaxed specificity of the oxytetracycline polyketide synthase for an acetate primer in the absence of a malonamyl primer. J Am Chem Soc 116, 6443-6444.
13. Hertweck, C., Luzhetskyy, A., Rebets, Y. & Bechthold, A. (2007). Type II polyketide synthases: gaining a deeper insight into enzymatic teamwork. Nat Prod Rep 24, 162-190.
14. Hitchman, T. S., Crosby, J., Byrom, K. J., Cox, R. J. & Simpson, T. J. (1998). Catalytic self-acylation of type II polyketide synthase acyl carrier proteins. Chem Biol 5, 35-47.
15. Hopwood, D. A. (1997). Genetic contributions to understanding polyketide synthases. Chem Rev 97, 2465-2498.
16. Kieser, T., Bibb, M. J., Buttner, M. J., Chater, K. F. & Hopwood, D. A. (2000). Practical Streptomyces Genetics. Norwich: John Innes Foundation.
17. Lechevalier, M. P., Prauser, H., Labeda, D. P. & Ruan, J.-S. (1986). Two new genera of nocardioform Actinomycetes: Amycolata gen. nov. and Amycolatopsis gen. nov. Int J Syst Bacteriol 36, 29-37.
18. Lombó, F., Blanco, G., Fernández, E., Méndez, C. & Salas, J. A. (1996). Characterization of Streptomyces argillaceus genes encoding a polyketide synthase involved in the biosynthesis of the antitumor mithramycin. Gene 172, 87-91.
19. MacNeil, D. J., Gewain, K. M., Ruby, C. L., Dezeny, G., Gibbons, P. H. & MacNeil, T. (1992). Analysis of Streptomyces avermitilis genes required for avermectin biosynthesis utilizing a novel integration vector. Gene 111, 61-68.
20. Madon, J. & Hütter, R. (1991). Transformation system for Amycolatopsis (Nocardia) mediterranei: direct transformation of mycelium with plasmid DNA. J Bacteriol 173, 6325-6331.
21. Malhotra, S. & Lal, R. (2007). The genus Amycolatopsis: indigenous plasmids, cloning vectors and gene transfer systems. Indian J Microbiol 47, 3-14.
22. McCormick, J. R., Jensen, E. R., Arnold, N., Corey, H. S., Joachim, U. H., Johnson, S., Miller, P. A. & Sjolander, N. O. (1968). Biosynthesis of tetracyclines. XI. The methylanthrone analog of protetrone. J Am Chem Soc 90, 7127-7129.
23. McMurry, L. M. & Levy, S. B. (1998). Revised sequence of OtrB (tet347) tetracycline efflux protein from Streptomyces rimosus. Antimicrob Agents Chemother 42, 3050.
24. Medveczky, P., Chang, C.-W., Oste, C. C. & Mulder, C. (1987). Rapid vacuum driven transfer of DNA and RNA from gels to solid supports. Biotechniques 5, 242-246.
25. Menéndez, N., Nur-e-Alam, M., Braña, A. F., Rohr, J., Salas, J. A. & Méndez, C. (2004). Biosynthesis of the antitumor chromomycin A3 in Streptomyces griseus: analysis of the gene cluster and rational design of novel chromomycin analogs. Chem Biol 11, 21-32.
26. Metsä-Ketelä, M., Salo, V., Halo, L., Hautala, A., Hakala, J., Mäntsälä, P. & Ylihonko, K. (1999). An efficient approach for screening minimal PKS genes from Streptomyces. FEMS Microbiol Lett 180, 1-6.
27. Mitscher, L. A., Juvarkar, J. V., Rosenbrook, W., Jr, Andres, W. W., Schenk, J. & Egan, R. S. (1970). Structure of chelocardin, a novel tetracycline antibiotic. J Am Chem Soc 92, 6070-6071.
28. Mitscher, L. A., Swayze, J. K., Högberg, T., Khanna, I., Rao, G. S., Theriault, R. J., Kohl, W., Hanson, C. & Egan, R. (1983). Biosynthesis of cetocycline. J Antibiot (Tokyo) 36, 1405-1407.
29. Moore, B. S. & Hertweck, C. (2002). Biosynthesis and attachment of novel bacterial polyketide synthase starter units. Nat Prod Rep 19, 70-99.
30. Oliva, B. & Chopra, I. (1992). Tet determinants provide poor protection against some tetracyclines: further evidence for division of tetracyclines into two classes. Antimicrob Agents Chemother 36, 876-878.
31. Oliva, B., Gordon, G., McNicholas, P., Ellestad, G. & Chopra, I. (1992). Evidence that tetracycline analogs whose primary target is not the bacterial ribosome cause lysis of Escherichia coli. Antimicrob Agents Chemother 36, 913-919.
32. Oliver, T. J. & Sinclair, A. C. (1964). Antibiotic M-319. United States Patent US3155582.
33. Olszewska, E. & Jones, K. (1988). Vacuum blotting enhances nucleic acid transfer. Trends Genet 4, 92-94.
34. Petersen, P. J., Jacobus, N. V., Weiss, W. J., Sum, P. E. & Testa, R. T. (1999). In vitro and in vivo antibacterial activities of a novel glycylcycline, the 9-t-butylglycylamido derivative of minocycline (GAR-936). Antimicrob Agents Chemother 43, 738-744.
35. Petkovic, H., Thamchaipenet, A., Zhou, L. H., Hranueli, D., Raspor, P., Waterman, P. G. & Hunter, I. S. (1999). Disruption of an aromatase/ cyclase from the oxytetracycline gene cluster of Streptomyces rimosus results in production of novel polyketides with shorter chain lengths. J Biol Chem 274, 32829-32834.
36. Petković, H., Cullum, J., Hranueli, D., Hunter, I. S., Perić-Concha, N., Pigac, J., Thamchaipenet, A., Vujaklija, D. & Long, P. F. (2006). Genetics of Streptomyces rimosus, the oxytetracycline producer. Microbiol Mol Biol Rev 70, 704-728.
37. Petkovic, H., Raspor, P. & Lesnik, U. (2013). Genes for biosynthesis of tetracycline compounds and uses thereof. United States Patent US8361777 B2.
38. Pickens, L. B. & Tang, Y. (2010). Oxytetracycline biosynthesis. J Biol Chem 285, 27509-27515.
39. Pioletti, M., Schlünzen, F., Harms, J., Zarivach, R., Glühmann, M., Avila, H., Bashan, A., Bartels, H., Auerbach, T. & other authors (2001). Crystal structures of complexes of the small ribosomal subunit with tetracycline, edeine and IF3. EMBO J 20, 1829-1839.
40. Proctor, R., Craig, W. & Kunin, C. (1978). Cetocycline, tetracycline analog: in vitro studies of antimicrobial activity, serum binding, lipid solubility, and uptake by bacteria. Antimicrob Agents Chemother 13, 598-604.
41. Rasmussen, B., Noller, H. F., Daubresse, G., Oliva, B., Misulovin, Z., Rothstein, D. M., Ellestad, G. A., Gluzman, Y., Tally, F. P. & Chopra, I. (1991). Molecular basis of tetracycline action: identification of analogs whose primary target is not the bacterial ribosome. Antimicrob Agents Chemother 35, 2306-2311.
42. Sambrook, J. & Russell, D. W. (2001). Molecular Cloning: a Laboratory Manual, 3rd edn. Cold Spring Harbor, N: Cold Spring Harbor Laboratory Press.
43. Saraste, M., Sibbald, P. R. & Wittinghofer, A. (1990). The P-loop-a common motif in ATP-and GTP-binding proteins. Trends Biochem Sci 15, 430-434.
44. Taylor, W. R. & Green, N. M. (1989). The predicted secondary structures of the nucleotide-binding sites of six cation-transporting ATPases lead to a probable tertiary fold. Eur J Biochem 179, 241-248.
45. Uchiyama, H. & Weisblum, B. (1985). N-Methyl transferase of Streptomyces erythraeus that confers resistance to the macrolidelincosamide-streptogramin B antibiotics: amino acid sequence and its homology to cognate R-factor enzymes from pathogenic bacilli and cocci. Gene 38, 103-110.
46. van Wageningen, A. M., Kirkpatrick, P. N., Williams, D. H., Harris, B. R., Kershaw, J. K., Lennard, N. J., Jones, M., Jones, S. J. & Solenberg, P. J. (1998). Sequencing and analysis of genes involved in the biosynthesis of a vancomycin group antibiotic. Chem Biol 5, 155-162.
47. Wang, P., Zhang, W., Zhan, J. & Tang, Y. (2009). Identification of OxyE as an ancillary oxygenase during tetracycline biosynthesis. ChemBioChem 10, 1544-1550.
48. Wilson, D. N. (2009). The A-Z of bacterial translation inhibitors. Crit Rev Biochem Mol Biol 44, 393-433.
49. Wu, H., Qu, S., Lu, C., Zheng, H., Zhou, X., Bai, L. & Deng, Z. (2012). Genomic and transcriptomic insights into the thermo-regulated biosynthesis of validamycin in Streptomyces hygroscopicus 5008. BMC Genomics 13, 337.
50. Zhang, W., Ames, B. D., Tsai, S. C. & Tang, Y. (2006). Engineered biosynthesis of a novel amidated polyketide, using the malonamylspecific initiation module from the oxytetracycline polyketide synthase. Appl Environ Microbiol 72, 2573-2580.
51. Zhang, W., Watanabe, K., Wang, C. C. & Tang, Y. (2007). Investigation of early tailoring reactions in the oxytetracycline biosynthetic pathway. J Biol Chem 282, 25717-25725.