How to make a glycopeptide: A synthetic biology approach to expand antibiotic chemical diversity

ACS Infectious Diseases

Volumn 2, Issue 9, 2016, Pages 642-650

  Yim, Grace ^a   Wang, Wenliang ^a   Thaker, Maulik N ^a,b   Tan, Stephanie ^a   Wright, Gerard D ^a  

^a MCMASTER UNIVERSITY   (Canada)

^b NOVARTIS INSTITUTES FOR BIOMEDICAL RESEARCH   (United States)

Author keywords

Antibiotic; Glycopeptide; Heterologous Expression; Synthetic Biosynthesis; Tailoring Enzymes

Indexed keywords

A 47934; DS A 47934; ISOENZYME; TEICOPLANIN DERIVATIVE; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT; GLYCOPEPTIDE; TEICOPLANIN;

ANTIBIOTIC RESISTANCE; ARTICLE; BIODIVERSITY; DRUG SYNTHESIS; ENZYME MODIFICATION; GENE CLUSTER; MICROBIAL DIVERSITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STREPTOMYCES COELICOLOR; SYNTHETIC BIOLOGY; BACTERIUM; BIOSYNTHESIS; CHEMISTRY; DRUG EFFECTS; GENETICS; METABOLISM; MULTIGENE FAMILY;

ANTI-BACTERIAL AGENTS; BACTERIA; BIOSYNTHETIC PATHWAYS; GLYCOPEPTIDES; MULTIGENE FAMILY; STREPTOMYCES COELICOLOR; SYNTHETIC BIOLOGY; TEICOPLANIN;

EID: 85009067210     PISSN: None     EISSN: 23738227     Source Type: Journal    
DOI: 10.1021/acsinfecdis.6b00105     Document Type: Article

References (42)

1. Van Boeckel, T. P., Gandra, S., Ashok, A., Caudron, Q., Grenfell, B. T., Levin, S. A., and Laxminarayan, R. (2014) Global antibiotic consumption 2000 to 2010: An analysis of national pharmaceutical sales data. Lancet Infect. Dis. 14, 742-750.
2. Fu, X., Albermann, C., Jiang, J., Liao, J., Zhang, C., and Thorson, J. S. (2003) Antibiotic optimization via in vitro glycorandomization. Nat. Biotechnol. 21, 1467-1469.
3. Losey, H. C., Jiang, J., Biggins, J. B., Oberthur, M., Ye, X. Y., Dong, S. D., Kahne, D., Thorson, J. S., and Walsh, C. T. (2002) Incorporation of glucose analogs by GtfE and GtfD from the vancomycin biosynthetic pathway to generate variant glycopeptides. Chem. Biol. 9, 1305-1314.
4. Ho, J. Y., Huang, Y. T., Wu, C. J., Li, Y. S., Tsai, M. D., and Li, T. L. (2006) Glycopeptide biosynthesis: Dbv21/Orf2 from dbv/tcp gene clusters are N-Ac-Glm teicoplanin pseudoaglycone deacetylases and Orf15 from cep gene cluster is a Glc-1-P thymidyltransferase. J. Am. Chem. Soc. 128, 13694-13695.
5. Kruger, R. G., Lu, W., Oberthur, M., Tao, J., Kahne, D., and Walsh, C. T. (2005) Tailoring of glycopeptide scaffolds by the acyltransferases from the teicoplanin and A-40, 926 biosynthetic operons. Chem. Biol. 12, 131-140.
6. Puk, O., Huber, P., Bischoff, D., Recktenwald, J., Jung, G., Sussmuth, R. D., van Pee, K. H., Wohlleben, W., and Pelzer, S. (2002) Glycopeptide biosynthesis in Amycolatopsis mediterranei DSM5908: function of a halogenase and a haloperoxidase/perhydrolase. Chem. Biol. 9, 225-235.
7. Lamb, S. S., Patel, T., Koteva, K. P., and Wright, G. D. (2006) Biosynthesis of sulfated glycopeptide antibiotics by using the sulfotransferase StaL. Chem. Biol. 13, 171-181.
8. Shi, R., Lamb, S. S., Zakeri, B., Proteau, A., Cui, Q., Sulea, T., Matte, A., Wright, G. D., and Cygler, M. (2009) Structure and function of the glycopeptide N-methyltransferase MtfA, a tool for the biosynthesis of modified glycopeptide antibiotics. Chem. Biol. 16, 401-410.
9. Yushchuk, O., Ostash, B., Pham, T. H., Luzhetskyy, A., Fedorenko, V., Truman, A. W., and Horbal, L. (2016) Characterization of the post-Assembly line tailoring processes in teicoplanin biosynthesis. ACS Chem. Biol., DOI: 10.1021/acschembio.6b00018.
10. Banik, J. J., Craig, J. W., Calle, P. Y., and Brady, S. F. (2010) Tailoring enzyme-rich environmental DNA clones: A source of enzymes for generating libraries of unnatural natural products. J. Am. Chem. Soc. 132, 15661-15670.
11. Yim, G., Thaker, M. N., Koteva, K., and Wright, G. (2014) Glycopeptide antibiotic biosynthesis. J. Antibiot. 67, 31-41.
12. World Health Organization. (2014) Antimicrobial Resistance: Global Report on Surveillance, Geneva, Switzerland.
13. Lunde, C. S., Hartouni, S. R., Janc, J. W., Mammen, M., Humphrey, P. P., and Benton, B. M. (2009) Telavancin disrupts the functional integrity of the bacterial membrane through targeted interaction with the cell wall precursor lipid II. Antimicrob. Agents Chemother. 53, 3375-3383.
14. Weber, T., Blin, K., Duddela, S., Krug, D., Kim, H. U., Bruccoleri, R., Lee, S. Y., Fischbach, M. A., Muller, R., Wohlleben, W., Breitling, R., Takano, E., and Medema, M. H. (2015) antiSMASH 3.0-A comprehensive resource for the genome mining of biosynthetic gene clusters. Nucleic Acids Res. 43, W237-243.
15. Thaker, M. N., and Wright, G. D. (2015) Opportunities for synthetic biology in antibiotics: expanding glycopeptide chemical diversity. ACS Synth. Biol. 4, 195-206.
16. Gomez-Escribano, J. P., and Bibb, M. J. (2011) Engineering Streptomyces coelicolor for heterologous expression of secondary metabolite gene clusters. Microb. Biotechnol. 4, 207-215.
17. Gregory, M. A., Till, R., and Smith, M. C. (2003) Integration site for Streptomyces phage phiBT1 and development of site-specific integrating vectors. J. Bacteriol. 185, 5320-5323.
18. Fayed, B., Younger, E., Taylor, G., and Smith, M. C. (2014) A novel Streptomyces spp. integration vector derived from the S. venezuelae phage, SV1. BMC Biotechnol. 14, 51.
19. Combes, P., Till, R., Bee, S., and Smith, M. C. (2002) The streptomyces genome contains multiple pseudo-AttB sites for the (phi)C31-encoded site-specific recombination system. J. Bacteriol. 184, 5746-5752.
20. Pootoolal, J., Thomas, M. G., Marshall, C. G., Neu, J. M., Hubbard, B. K., Walsh, C. T., and Wright, G. D. (2002) Assembling the glycopeptide antibiotic scaffold: The biosynthesis of A47934 from Streptomyces toyocaensis NRRL15009. Proc. Natl. Acad. Sci. U. S. A. 99, 8962-8967.
21. Jones, A. C., Gust, B., Kulik, A., Heide, L., Buttner, M. J., and Bibb, M. J. (2013) Phage p1-derived artificial chromosomes facilitate heterologous expression of the FK506 gene cluster. PLoS One 8, e69319.
22. Hong, H. J., Hutchings, M. I., Hill, L. M., and Buttner, M. J. (2005) The role of the novel Fem protein VanK in vancomycin resistance in Streptomyces coelicolor. J. Biol. Chem. 280, 13055-13061.
23. Beltrametti, F., Lazzarini, A., Brunati, C., Marazzi, A., Jovetic, S., Selva, E., and Marinelli, F. (2003) Production and characterization of monochlorinated and dechlorinated A40926 derivatives. J. Antibiot. 56, 773-782.
24. Losey, H. C., Peczuh, M. W., Chen, Z., Eggert, U. S., Dong, S. D., Pelczer, I., Kahne, D., and Walsh, C. T. (2001) Tandem action of glycosyltransferases in the maturation of vancomycin and teicoplanin aglycones: novel glycopeptides. Biochemistry 40, 4745-4755.
25. Butler, M. S., Hansford, K. A., Blaskovich, M. A., Halai, R., and Cooper, M. A. (2014) Glycopeptide antibiotics: back to the future. J. Antibiot. 67, 631-644.
26. Liu, Y. C., Li, Y. S., Lyu, S. Y., Hsu, L. J., Chen, Y. H., Huang, Y. T., Chan, H. C., Huang, C. J., Chen, G. H., Chou, C. C., Tsai, M. D., and Li, T. L. (2011) Interception of teicoplanin oxidation intermediates yields new antimicrobial scaffolds. Nat. Chem. Biol. 7, 304-309.
27. Hadatsch, B., Butz, D., Schmiederer, T., Steudle, J., Wohlleben, W., Sussmuth, R., and Stegmann, E. (2007) The biosynthesis of teicoplanin-Type glycopeptide antibiotics: Assignment of p450 monooxygenases to side chain cyclizations of glycopeptide a47934. Chem. Biol. 14, 1078-1089.
28. Stegmann, E., Pelzer, S., Bischoff, D., Puk, O., Stockert, S., Butz, D., Zerbe, K., Robinson, J., Sussmuth, R. D., and Wohlleben, W. (2006) Genetic analysis of the balhimycin (vancomycin-Type) oxygenase genes. J. Biotechnol. 124, 640-653.
29. Schmartz, P. C., Wolfel, K., Zerbe, K., Gad, E., El Tamany el, S., Ibrahim, H. K., Abou-Hadeed, K., and Robinson, J. A. (2012) Substituent effects on the phenol coupling reaction catalyzed by the vancomycin biosynthetic P450 enzyme OxyB. Angew. Chem., Int. Ed. 51, 11468-11472.
30. Lu, W., Oberthur, M., Leimkuhler, C., Tao, J., Kahne, D., and Walsh, C. T. (2004) Characterization of a regiospecific epivancosaminyl transferase GtfA and enzymatic reconstitution of the antibiotic chloroeremomycin. Proc. Natl. Acad. Sci. U. S. A. 101, 4390-4395.
31. Howard-Jones, A. R., Kruger, R. G., Lu, W., Tao, J., Leimkuhler, C., Kahne, D., and Walsh, C. T. (2007) Kinetic analysis of teicoplanin glycosyltransferases and acyltransferase reveal ordered tailoring of aglycone scaffold to reconstitute mature teicoplanin. J. Am. Chem. Soc. 129, 10082-10083.
32. Fischbach, M. A., and Clardy, J. (2007) One pathway, many products. Nat. Chem. Biol. 3, 353-355.
33. Klein, J., Heal, J. R., Hamilton, W. D., Boussemghoune, T., Tange, T. O., Delegrange, F., Jaeschke, G., Hatsch, A., and Heim, J. (2014) Yeast synthetic biology platform generates novel chemical structures as scaffolds for drug discovery. ACS Synth. Biol. 3, 314-323.
34. Kalan, L., Perry, J., Koteva, K., Thaker, M., and Wright, G. (2013) Glycopeptide sulfation evades resistance. J. Bacteriol. 195, 167-171.
35. Kwun, M. J., Novotna, G., Hesketh, A. R., Hill, L., and Hong, H. J. (2013) In vivo studies suggest that induction of VanS-dependent vancomycin resistance requires binding of the drug to D-Ala-D-Ala termini in the peptidoglycan cell wall. Antimicrob. Agents Chemother. 57, 4470-4480.
36. Hong, H. J., Hutchings, M. I., Neu, J. M., Wright, G. D., Paget, M. S., and Buttner, M. J. (2004) Characterization of an inducible vancomycin resistance system in Streptomyces coelicolor reveals a novel gene (vanK) required for drug resistance. Mol. Microbiol. 52, 1107-1121.
37. Yim, G., Kalan, L., Koteva, K., Thaker, M. N., Waglechner, N., Tang, I., and Wright, G. D. (2014) Harnessing the synthetic capabilities of glycopeptide antibiotic tailoring enzymes: characterization of the UK-68, 597 biosynthetic cluster. ChemBioChem 15, 2613-2623.
38. Hopwood, D. A., Kieser, T., Bibb, M. J., Buttner, M. J., and Chater, K. (2000) Practical Streptomyces Genetics, John Innes Foundation, Norwich, UK.
39. Datsenko, K. A., and Wanner, B. L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U. S. A. 97, 6640-6645.
40. Sherwood, E. J., and Bibb, M. J. (2013) The antibiotic planosporicin coordinates its own production in the actinomycete Planomonospora alba. Proc. Natl. Acad. Sci. U. S. A. 110, E2500-2509.
41. Sitrin, R. D., and Wasserman, G. F. (1989) Affinity and HPLC purification of glycopeptide antibiotics. J. Chromatogr. Libr. 43, 111-152.
42. D'Costa, V. M., McGrann, K. M., Hughes, D. W., and Wright, G. D. (2006) Sampling the antibiotic resistome. Science 311, 374-377.