A two-plasmid system for the glycosylation of polyketide antibiotics: Bioconversion of ε-rhodomycinone to rhodomycin D

Chemistry and Biology

Volumn 6, Issue 12, 1999, Pages 845-855

  Olano, Carlos ^a   Lomovskaya, Natalia ^a   Fonstein, Leonid ^a   Roll, Jon T ^a   Hutchinson, C Richard ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Anthracycline antibiotics; Combinatorial biosynthesis; Daunorubicin; Deoxysugars; Streptomyces

Indexed keywords

ANTHRACYCLINE; ANTHRACYCLINE ANTIBIOTIC AGENT; ANTIBIOTIC AGENT; DAUNORUBICIN; DNA BINDING; DOXORUBICIN; DRUG ANALYSIS; GLYCOSYLATION; PLASMID; RHODOMYCINONE; STREPTOMYCES LIVIDANS;

EID: 0033485919     PISSN: 10745521     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1074-5521(00)80004-6     Document Type: Article

References (62)

1. Arcamone, F., et al., & Spalla, C. (1969). Adriamycin, 14- hydroxydaunomycin, a new antitumor antibiotic from Streptomyces peucetius var. caesius. Biotechnol. Bioeng. 11, 1101-1110.
2. Cassinelli, G. & Orezzi, P. (1963). Daunomycin, a new antibiotic with cytostatic activity. Isolation and properties. G. Microbiol. 11, 167-174.
3. D'bost, M., et al., & Werner, G.H. (1963). Un novel antibiotique a proprietes cytostatiques: La rubidomycine. C. R. Acad. Sci. Agric. Belg. 257, 1813-1815.
4. Arcamone, F. (1981). A novel antibiotic with cytostatic properties: Rubidomycin. Med. Chem. Ser. Monogr. 17, 25-31.
5. Arcamone, F.M. (1998). From the pigments of the actinomycetes to third generation antitumor anthracyclines. Biochimie 80, 201-206.
6. Fujiwara, A., & Hoshino, T. (1983). Anthracycline antibiotics. Crit. Rev. Biotechnol. 3, 133-157.
7. Hutchinson, C.R. (1997). Biosynthetic studies of daunorubicin and tetracenomycin C. Chem. Rev. 97, 2525-2535.
8. Hutchinson, C.R. (1999). Genetic engineering of doxorubicin production in Streptomyces peucetius. J. Industr. Microbiol. Biotechnol. 23, 647-652.
9. Summers, R.G., Donadio, S., Staver, M., Wendt-Pienkowski, E., Hutchinson, C.R. & Katz, L. (1997). Sequencing and mutagenesis of genes from the erythromycin biosynthetic gene cluster of Saccharopolyspora erythraea that are involved in L-mycarose and D-desosamine production. Microbiology 143, 3251-3262.
10. Gaisser, S., Böhm, G.A., Cortés, J, & Leadlay, P.F. (1997). Analysis of seven genes from the eryAI-eryK region of the erythromycin biosynthetic gene cluster in Saccharopolyspora erythraea. Mol. Gen. Genet. 256, 239-251.
11. Gaisser, S., et al., & Leadlay, P.F. (1998). Analysis of eryBI, eryBIII and eryBVII from the erythromycin biosynthetic gene cluster in Saccharopolyspora erythraea. Mol. Gen. Genet. 258, 78-88.
12. Salah-Bey, K., et al., & Raynal, M.C. (1998). Targeted gene inactivation for the elucidation of deoxysugar biosynthesis in the erythromycin producer Saccharopolyspora erythraea. Mol. Gen. Genet. 257, 542-553.
13. Olano, C., Rodriguez, A.M., Michel, J.M., Mendez, C., Raynal, M.C. & Salas, J.A. (1998). Analysis of a Streptomyces antibioticus chromosomal region involved in oleandomycin biosynthesis, which encodes two glycosyltranferases responsible for glycosylation of the macrolactone ring. Mol. Gen. Genet. 259, 299-308.
14. Quiros, L.M., Aguirrezabalaga, I., Olano, C., Mendez, C. & Salas, J.A. (1998). Two glycosyltransferases and a glycosidase are involved in oleandomycin modification during its biosynthesis by Streptomyces antiobioticus. Mol. Microbiol. 28, 1177-1185.
15. Xue, Y., Zhao, L., Liu, H.W. & Sherman, D.H. (1998). A gene cluster for macrolide antibiotic biosynthesis in Streptomyces venezuelae: Architecture of metabolic diversity. Proc. Natl Acad. Sci. USA 95, 12111-12116.
16. Occi, J.L., Gerwain, K.M., Ruby, C.L. & MacNeil, D.L. (1991). Abstracts of the Annual Meeting of the Society for Industrial Microbiology. P49, p.93. Philadelphia, PA.
17. Kirschning, A., Bechthold, A.F.W., & Rhor, J. (1997). Chemical and biochemical aspects of deoxysugars and deoxysugar oligosaccharides. Top. Curr. Chem. 188, 1-84.
18. Liu, H.W., & Thorson, J.S. (1994). Pathways and mechanisms in the biogenesis of novel deoxysugars by bacteria. Annu. Rev. Microbiol. 48, 223-256.
19. Elling, L. (1997). Glycobiotechnology: Enzymes for the synthesis of nucleotide sugars. Advan. Biochem. Eng. Biotechnol. 58, 89-44.
20. Gallo, M.A., Ward, J. & Hutchinson, C.R. (1996). The dnrM gene in Streptomyces peucetius contains a naturally occurring frameshift mutation that is suppressed by another locus outside of the daunorubicin-production gene cluster. Microbiology 142, 269-275.
21. Thompson, M.W., Strohl, W.R. & Floss, H.G. (1992). Purification and characterization of TDP-D-glucose 4,6-dehydratase from anthracycline- Producing streptomycetes. J. Gen. Microbiol. 138, 779-786.
22. Scotti, C. & Hutchinson, C.R. (1996). Enhanced antibiotic production by manipulation of the Streptomyces peucetius dnrH and dnmT genes involved in doxorubicin (adriamycin) biosynthesis. J. Bacteriol. 178, 7316-7321.
23. Otten, S.L., Liu, X., Ferguson, J. & Hutchinson, C.R. (1995). Cloning and characterization of the Streptomyces peucetius dnrOS genes encoding a daunosamine biosynthesis enzyme and a glycosyl transferase involved in daunorubicin biosynthesis. J. Bacteriol. 177, 6688-6692.
24. Draeger, G., Park., S.H. & Floss, H.G. (1999). Mechanism of the 2-deoxygenation step in the biosynthesis of the deoxyhexose moieties of the antibiotics granaticin and oleandomycin. J. Am. Chem. Soc. 121, 2611-2612
25. Otten, S.L., Gallo, M.A., Madduri, K., Liu, X. & Hutchinson, C.R. (1997). Cloning and characterization of the Streptomyces peucetius dnmZUV genes encoding three enzymes required for biosynthesis of the daunorubicin precursor thymidine diphospho-L-daunosamine. J. Bacteriol. 179, 4446-4450.
26. Madduri, K., et al., & Hutchinson, C.R. (1998). Production of the antitumor drug epirubicin (4′-epidoxorubicin) and its precursor by a genetically engineered strain of Streptomyces peucetius. Nat. Biotechnol. 16, 69-74.
27. Stutzman-Engwall, K.J., Otten, S.L. & Hutchinson, C.R. (1992). Regulation of secondary metabolism in Streptomyces spp. and overproduction of daunorubicin in Streptomyces peucetius. J. Bacteriol. 174, 144-154.
28. 1 locus, which controls daunorubicin biosynthesis in Streptomyces peucetius. J. Bacteriol. 177, 1208-1215.
29. Tang, L., Grimm, A., Zhang, Y.X. & Hutchinson, C.R. (1996). Purification and characterization of the DNA-binding protein, Dnrl, a transcriptional factor of daunorubicin biosynthesis in Streptomyces peucetius. Mol. Microbiol. 22, 801-813.
30. Furuya, K. & Hutchinson, C.R. (1998). The DrrC protein of Streptomyces peucetius, a UvrA-like protein, is a DNA-binding protein whose gene is induced by daunorubicin. FEMS Microbiol. Lett. 168, 243-249.
31. Guilfoile, P.G. & Hutchinson, C.R. (1991). A bacterial analog of the mdr gene of mammalian tumor cells is present in Streptomyces peucetius, the producer of daunorubicin and doxorubicin. Proc. Natl Acad. Sci. USA 88, 8553-8557.
32. Lombo, F., Siems, K., Bran̄a, A.F., Mendez, C., Bindseil, K. & Salas, J.A. (1997). Cloning and insertional inactivation of Streptomyces argillaceus genes involved in the earliest steps of biosynthesis of the sugar moieties of the antitumor polyketide mithramycin. J. Bacteriol. 179, 3354-3357.
33. Gerlitz, M., Meurer, G., Wendt-Pienkowski, E., Madduri, K. & Hutchinson, C.R. (1997). Effect of the daunorubicin dpsH gene on the choice of starter unit and cyclization pattern reveals that type II polyketide synthases can be unfaithful yet intriguing. J. Am. Chem. Soc. 119, 7392-7393.
34. Lomovskaya, N., et al., & Hutchinson, C.R. (1999). Doxorubicin overproduction in Streptomyces peucetius: Cloning and characterization of the dnrU ketoreductase and dnrV genes and the doxA cytochrome P-450 hydroxylase gene. J. Bacteriol. 181, 305-318.
35. Vara, J., Lewandowska-Skarbek, Wang, Y.G., Donadio, S. & Hutchinson, C.R. (1989). Cloning of genes governing the deoxysugar portion of the erythromycin biosynthetic pathway in Saccharopolyspora erythraea (Streptomyces erythreus). J. Bacteriol. 171, 5872-5881.
36. Lomovskaya, N., et al., & Hutchinson, C.R. (1998) The Streptomyces peucetius dpsY and dnrX genes govern early and late steps of daunorubicin and doxorubicin biosynthesis. J. Bacteriol. 180, 2379-2386.
37. Ho, C.C. & Chye, M.L. (1985). Construction of a genetic map of chromosomal auxotrophic markers in Streptomyces peucetius var. caesius. J. Gen. Appl. Microbiol. 31, 231-241.
38. Ho, C.C., Wright, M.H. & Hopwood, D.A. (1985). Transformation of protoplasts from Streptomyces peucetius var. caesius by plasmid cloning vectors. In Proceedings of the International Congress on Microbiology in the Eighties (Lim, G., & Nga, BH., eds.), pp. 275-289, Singapore Society for Microbiology, Singapore.
39. Bibb, M.J., White, J., Ward, J.M., & Janssen, G.R.. (1994). The mRNA for the 23S rRNA methylase encoded by the ermE gene of Saccharopolyspora erythraea is translated in the absence of a conventional ribosome-binding site. Mol. Microbiol. 14, 533-545.
40. Hopwood, D.A., et al., & Schrempf, H. (1985). Genetic Manipulation of Streptomyces: A Laboratory Manual. The John Innes Foundation, Norwich, United Kingdom.
41. Takano, E., Gramajo, H.C., Strauch, E., Andres, N., White, J. & Bibb, M.J. (1992). Transcriptional regulation of the redD transcriptional activator gene accounts for growth-phase-dependent production of the antibiotic undecylprodigiosin in Streptomyces coelicolor A3(2). Mol. Microbiol. 6, 2797-2804.
42. Otten, S.L., Stutzman-Engwall, K.J., & Hutchinson, C.R. (1990). Cloning and expression of daunorubicin biosynthesis genes from Streptomyces peucetius and S. peucetius subsp. caesius. J. Bacteriol. 172, 3427-3434.
43. Jacobsen, J.R., Hutchinson, C.R., Cane, D.E. & Khosla, C. (1997). Precursor-directed biosynthesis of erythromycin analogs by an engineered polyketide synthase. Science 277, 367-369.
44. Ruan, X., et al., & Katz, L. (1997). Acyltransferase domain substitutions in erythromycin polyketide synthase yield novel erythromycin derivatives. J. Bacteriol. 179, 6416-6425.
45. Stassi, D.L., et al., & Katz, L. (1998). Ethyl-substituted erythromycin derivatives produced by directed metabolic engineering. Proc. Natl Acad. Sci. USA 95, 7305-7309.
46. Marsden, A.F., Wilkinson, B., Cortés, J., Dinster, N.J., Stauton, J. & Leadlay, P.F. (1998). Engineering broader specificity into an antibiotic-producing polyketide synthase. Science 279, 199-202.
47. McDaniel, R., Thamchaipenet, A., Gustafsson, C., Fu, H., Betlach, M. & Ashley, G. (1999). Multiple genetic modifications of the erythromycin polyketide synthase to produce a library of novel 'unnatural' natural products. Proc. Natl Acad. Sci. USA 96, 1846-51.
48. Gokhale, R.S., Tsuji, S.Y., Cane, D.E. & Khosla, C. (1999). Dissecting and exploiting intermodular communication in polyketide synthases. Science 284, 482-485.
49. Stachelhaus, T., Schneider, A. & Marahiel, M.A. (1995). Rational design of peptide antibiotics by targeted replacement of bacterial and fungal domains. Science 269, 69-72.
50. Belshaw, P., Walsh, C.T. & Stachelhaus, T. (1999). Aminoacyl-CoAs as probes of condensation domain selectivity in nonribosomal peptide synthesis. Science 284, 486-489.
51. Decker, H., Haag, S., Udvarnoki, G. & Rohr, J. (1995). Novel genetically engineered tetracenomycins. Angew. Chem. Int. Ed. Engl. 34, 1107-1110.
52. Solenberg, P.J., Matsushima, P., Stack, D.R., Wilkie, S.C., Thompson, R.C., & Baltz, R.H. (1997). Production of hybrid glycopeptide antibiotics in vitro and in Streptomyces toyocaensis. Chem. Biol. 4, 195-202.
53. Wohlert, S.E., et al., & Rohr, J. (1998). Novel hybrid tetracenomycins through combinatorial biosynthesis using a glycosyltransferase encoded by the elm genes in cosmid 16F4 and which shows a broad sugar substrate specificity. J. Am. Chem. Soc. 120, 10596-10601.
54. Johnson, D.A. & Liu, H. (1998). Mechanisms and pathways from recent deoxysugar biosynthesis research. Curr. Opin. Chem. Biol. 2, 642-649.
55. Zhao, L., Sherman, D.H. & Liu, H.W. (1998). Biosynthesis of desosamine: Construction of a new methymycin/neomethymycin analogue by deletion of a desosamine biosynthetic gene. J. Am. Chem. Soc. 120, 10256-10257.
56. Zhao, L., Que, N.L.S., Xue, Y., Sherman, D.H. & Liu, H.W. (1998). Mechanistic studies of desosamine biosynthesis: C-4 deoxygenation precedes C-3 transamination. J. Am. Chem. Soc. 120, 12159-12160.
57. Hopwood, D.A., Kiesser, T., Wright, H.M. & Bibb, M.J. (1983). Plasmids, recombination and chromosome mapping in Streptomyces lividans 66. J. Gen. Microbiol. 129, 2257-2269.
58. Sambrook, J., Fritsch, E.F. & Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual, (2nd Edn), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
59. Yanisch-Perron, C., Vieira, J., & Messing, J. (1985). Improved M13 phage cloning vectors and host strains: Nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33, 103-119.
60. Lomovskaya, N.D., Chater, K.F. & Mkrtumian, N.M. (1980). Genetics and molecular biology of Streptomyces bacteriophage. Microbiol. Rev. 44, 206-229.
61. Grimm, A., Madduri, K., Ali, A. & Hutchinson, CR. (1994). Characterization of the Streptomyces peucetius ATCC 29050 genes encoding doxorubicin polyketide synthase. Gene 151, 1-10.
62. Lomovskaya, N., Fonstein, L., Ruan, X., Stassi, D., Katz, L. & Hutchinson, C.R. (1997). Gene disruption and replacement in the rapamycin-producing Streptomyces hygroscopicus strain ATCC 29253. Microbiology 143, 875-883.