Opportunities for synthetic biology in antibiotics: Expanding glycopeptide chemical diversity

ACS Synthetic Biology

Volumn 4, Issue 3, 2015, Pages 195-206

  Thaker, Maulik N ^a   Wright, Gerard D ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

antibiotic scaffold; glycopeptides; heterologous host; resistance; synthetic biology; tailoring enzymes

Indexed keywords

ANTIBIOTIC AGENT; NEW DRUG; POLYPEPTIDE ANTIBIOTIC AGENT; ANTIINFECTIVE AGENT; GLYCOPEPTIDE;

ANTIBIOTIC RESISTANCE; CHEMICAL MODIFICATION; DRUG MECHANISM; DRUG STRUCTURE; GLYCOSYLATION; HALOGENATION; METHYLATION; MOLECULE; NONHUMAN; PRIORITY JOURNAL; REVIEW; SULFATION; SYNTHETIC BIOLOGY; DRUG DEVELOPMENT; MOLECULAR BIOLOGY;

ANTI-BACTERIAL AGENTS; DRUG DISCOVERY; DRUG RESISTANCE, MICROBIAL; GLYCOPEPTIDES; MOLECULAR BIOLOGY; SYNTHETIC BIOLOGY;

EID: 84925633044     PISSN: None     EISSN: 21615063     Source Type: Journal    
DOI: 10.1021/sb300092n     Document Type: Review

References (67)

1. Walsh, C. T. (2003) Antibiotics: Actions, Origins, Resistance, ASM press, Washington, DC.
2. Lamb, S. S. and Wright, G. D. (2005) Accessorizing natural products: adding to nature's toolbox Proc. Natl. Acad. Sci. U.S.A. 102, 519-520
3. Miller, S. J. and Clardy, J. (2009) Natural products: Beyond grind and find Nat. Chem. 1, 261-263
4. Li, J. W. and Vederas, J. C. (2009) Drug discovery and natural products: end of an era or an endless frontier? Science 325, 161-165
5. Wright, G. D. (2007) The antibiotic resistome: the nexus of chemical and genetic diversity Nat. Rev. Microbiol. 5, 175-186
6. Fischbach, M. A. and Walsh, C. T. (2009) Antibiotics for emerging pathogens Science 325, 1089-1093
7. McAlpine, J. B., Bachmann, B. O., Piraee, M., Tremblay, S., Alarco, A. M., Zazopoulos, E., and Farnet, C. M. (2005) Microbial genomics as a guide to drug discovery and structural elucidation: ECO-02301, a novel antifungal agent, as an example J. Nat. Prod. 68, 493-496
8. Lautru, S., Deeth, R. J., Bailey, L. M., and Challis, G. L. (2005) Discovery of a new peptide natural product by Streptomyces coelicolor genome mining Nat. Chem. Biol. 1, 265-269
9. Sattely, E. S., Fischbach, M. A., and Walsh, C. T. (2008) Total biosynthesis: in vitro reconstitution of polyketide and nonribosomal peptide pathways Nat. Prod. Rep. 25, 757-793
10. Banik, J. J. and Brady, S. F. (2008) Cloning and characterization of new glycopeptide gene clusters found in an environmental DNA megalibrary Proc. Natl. Acad. Sci. U.S.A. 105, 17273-17277
11. Floss, H. G. (2006) Combinatorial biosynthesis-potential and problems J. Biotechnol. 124, 242-257
12. Hopwood, D. A., Malpartida, F., Kieser, H. M., Ikeda, H., Duncan, J., Fujii, I., Rudd, B. A., Floss, H. G., and Omura, S. (1985) Production of 'hybrid' antibiotics by genetic engineering Nature 314, 642-644
13. McCarthy, A. A. (2002) Kosan biosciences. Better chemistry through genetics Chem. Biol 9, 849-850
14. Koide, T., Pang, W. L., and Baliga, N. S. (2009) The role of predictive modelling in rationally re-engineering biological systems Nat. Rev. Microbiol. 7, 297-305
15. Komatsu, M., Uchiyama, T., Omura, S., Cane, D. E., and Ikeda, H. (2010) Genome-minimized Streptomyces host for the heterologous expression of secondary metabolism Proc. Natl. Acad. Sci. U.S.A. 107, 2646-2651
16. Martinez, A., Kolvek, S. J., Yip, C. L., Hopke, J., Brown, K. A., MacNeil, I. A., and Osburne, M. S. (2004) Genetically modified bacterial strains and novel bacterial artificial chromosome shuttle vectors for constructing environmental libraries and detecting heterologous natural products in multiple expression hosts Appl. Environ. Microbiol. 70, 2452-2463
17. Pfeifer, B., Hu, Z., Licari, P., and Khosla, C. (2002) Process and metabolic strategies for improved production of Escherichia coli -derived 6-deoxyerythronolide B Appl. Environ. Microbiol. 68, 3287-3292
18. 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
19. Lee, H. Y. and Khosla, C. (2007) Bioassay-guided evolution of glycosylated macrolide antibiotics in Escherichia coli PLoS Biol. 5, e45
20. Ro, D. K., Paradise, E. M., Ouellet, M., Fisher, K. J., Newman, K. L., Ndungu, J. M., Ho, K. A., Eachus, R. A., Ham, T. S., Kirby, J., Chang, M. C., Withers, S. T., Shiba, Y., Sarpong, R., and Keasling, J. D. (2006) Production of the antimalarial drug precursor artemisinic acid in engineered yeast Nature 440, 940-943
21. Solenberg, P. J., Matsushima, P., Stack, D. R., Wilkie, S. C., Thompson, R. C., and Baltz, R. H. (1997) Production of hybrid glycopeptide antibiotics in vitro and in Streptomyces toyocaensis Chem. Biol. 4, 195-202
22. Oberthur, M., Leimkuhler, C., Kruger, R. G., Lu, W., Walsh, C. T., and Kahne, D. (2005) A systematic investigation of the synthetic utility of glycopeptide glycosyltransferases J. Am. Chem. Soc. 127, 10747-10752
23. 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
24. 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
25. Michalodimitrakis, K. and Isalan, M. (2009) Engineering prokaryotic gene circuits FEMS Microbiol. Rev. 33, 27-37
26. Tahlan, K., Ahn, S. K., Sing, A., Bodnaruk, T. D., Willems, A. R., Davidson, A. R., and Nodwell, J. R. (2007) Initiation of actinorhodin export in Streptomyces coelicolor Mol. Microbiol. 63, 951-961
27. Morton, D., Leach, S., Cordier, C., Warriner, S., and Nelson, A. (2009) Synthesis of natural-product-like molecules with over eighty distinct scaffolds Angew. Chem. 48, 104-109
28. Lewis, C. A. and Miller, S. J. (2006) Site-selective derivatization and remodeling of erythromycin A by using simple peptide-based chiral catalysts Angew. Chem. 45, 5616-5619
29. Lewis, C. A., Merkel, J., and Miller, S. J. (2008) Catalytic site-selective synthesis and evaluation of a series of erythromycin analogs Bioorg. Med. Chem. Lett. 18, 6007-6011
30. Kennedy, J. (2008) Mutasynthesis, chemobiosynthesis, and back to semi-synthesis: combining synthetic chemistry and biosynthetic engineering for diversifying natural products Nat. Prod. Rep. 25, 25-34
31. Nicolaou, K. C., Boddy, C. N., Brase, S., and Winssinger, N. (1999) Chemistry, biology, and medicine of the glycopeptide antibiotics Angew. Chem. 38, 2096-2152
32. van Wageningen, A. A., Kirkpatrick, P. N., Williams, D. H., Harris, B. R., Kershaw, J. K., Lennard, N. J., Jones, M., Jones, S. J. M., and Solenberg, P. J. (1998) Sequencing and analysis of genes involved in the biosynthesis of a vancomycin group antibiotic Chem. Biol. 5, 155-162
33. 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
34. Grdadolnik, S. G., Pristovsek, P., and Mierke, D. F. (1998) Vancomycin: conformational consequences of the sugar substituent J. Med. Chem. 41, 2090-2099
35. Kannan, R., Harris, C. M., Harris, T. M., Waltho, J. P., Skelton, N. J., and Williams, D. H. (1988) Function of the amino sugar and N-terminal amino acid of the antibiotic vancomycin in its complexation with cell wall peptides J. Am. Chem. Soc. 110, 2946-2953
36. Mackay, J. P., Gerhard, U., Beauregard, D. A., Maplestone, R. A., and Williams, D. H. (1994) Dissection of the contributions toward dimerization of glycopeptide antibiotics J. Am. Chem. Soc. 116, 4573-4580
37. Chan, H. C., Huang, Y. T., Lyu, S. Y., Huang, C. J., Li, Y. S., Liu, Y. C., Chou, C. C., Tsai, M. D., and Li, T. L. (2011) Regioselective deacetylation based on teicoplanin-complexed Orf2∗ crystal structures Mol. Biosyst. 7, 1224-1231
38. 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
39. Bister, B., Bischoff, D., Nicholson, G. J., Stockert, S., Wink, J., Brunati, C., Donadio, S., Pelzer, S., Wohlleben, W., and Sussmuth, R. D. (2003) Bromobalhimycin and chlorobromobalhimycins-illuminating the potential of halogenases in glycopeptide antibiotic biosyntheses ChemBioChem 4, 658-662
40. Kalan, L., Perry, J., Koteva, K., Thaker, M. N., and Wright, G. (2012) Glycopeptide sulfation evades resistance J. Bacteriol. 195, 167-171
41. 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
42. Shi, R., Lamb, S. S., Bhat, S., Sulea, T., Wright, G. D., Matte, A., and Cygler, M. (2007) Crystal structure of StaL, a glycopeptide antibiotic sulfotransferase from Streptomyces toyocaensis J. Biol. Chem. 282, 13073-13086
43. Bick, M. J., Banik, J. J., Darst, S. A., and Brady, S. F. (2010) Crystal structures of the glycopeptide sulfotransferase Teg12 in a complex with the teicoplanin aglycone Biochemistry 49, 4159-4168
44. Bick, M. J., Banik, J. J., Darst, S. A., and Brady, S. F. (2010) The 2.7 A resolution structure of the glycopeptide sulfotransferase Teg14 Acta Crystallogr., Sect. D 66, 1278-1286
45. Shi, R., Munger, C., Kalan, L., Sulea, T., Wright, G. D., and Cygler, M. (2012) Sulfonation of glycopeptide antibiotics by sulfotransferase StaL depends on conformational flexibility of aglycone scaffold Proc. Natl. Acad. Sci. U.S.A. 109, 11824-11829
46. 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
47. Nagarajan, R., Merkel, K. E., Michel, K. H., Higgins, H. M., Hoehn, M. M., Hunt, A. H., Jones, N. D., Occolowitz, J. L., Schabel, A. A., and Swartzendruber, J. K. (1988) M43 antibiotics: methylated vancomycins and unrearranged CDP-I analogs J. Am. Chem. Soc. 110, 7896-7897
48. Malabarba, A. and Goldstein, B. P. (2005) Origin, structure, and activity in vitro and in vivo of dalbavancin J. Antimicrob. Chemother. 55, ii15-ii20
49. Mulichak, A. M., Losey, H. C., Walsh, C. T., and Garavito, R. M. (2001) Structure of the UDP-glucosyltransferase GtfB that modifies the heptapeptide aglycone in the biosynthesis of vancomycin group antibiotics Structure 9, 547-557
50. 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
51. Hubbard, B. K. and Walsh, C. T. (2003) Vancomycin assembly: Nature's way Angew. Chem., Int. Ed. 42, 730-765
52. Losey, H. C., Jiang, J., Biggins, J. B., Oberthür, 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
53. 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
54. Chen, H., Thomas, M. G., Hubbard, B. K., Losey, H. C., Walsh, C. T., and Burkart, M. D. (2000) Deoxysugars in glycopeptide antibiotics: Enzymatic synthesis of TDP-l-epivancosamine in chloroeremomycin biosynthesis Proc. Natl. Acad. Sci. U.S.A. 97, 11942-11947
55. 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
56. Li, T. L., Huang, F., Haydock, S. F., Mironenko, T., Leadlay, P. F., and Spencer, J. B. (2004) Biosynthetic gene cluster of the glycopeptide antibiotic teicoplanin: characterization of two glycosyltransferases and the key acyltransferase Chem. Biol. 11, 107-119
57. Zou, Y., Brunzelle, J. S., and Nair, S. K. (2008) Crystal structures of lipoglycopeptide antibiotic deacetylases: Implications for the biosynthesis of A40926 and teicoplanin Chem. Biol. 15, 533-545
58. 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
59. Mulichak, A. M., Lu, W., Losey, H. C., Walsh, C. T., and Garavito, R. M. (2004) Crystal structure of vancosaminyltransferase GtfD from the vancomycin biosynthetic pathway: interactions with acceptor and nucleotide ligands Biochemistry 43, 5170-5180
60. Sosio, M., Giusino, F., Cappellano, C., Bossi, E., Puglia, A. M., and Donadio, S. (2000) Artificial chromosomes for antibiotic-producing actinomycetes Nat. Biotechnol. 18, 343-345
61. Gust, B., Chandra, G., Jakimowicz, D., Yuqing, T., Bruton, C. J., and Chater, K. F. (2004) λ Red-mediated genetic manipulation of antibiotic-producing Streptomyces, In Advances in Applied Microbiology, pp 107-128, Academic Press, New York.
62. Kim, J. H., Feng, Z., Bauer, J. D., Kallifidas, D., Calle, P. Y., and Brady, S. F. (2010) Cloning large natural product gene clusters from the environment: piecing environmental DNA gene clusters back together with TAR Biopolymers 93, 833-844
63. Pfeifer, B. A., Admiraal, S. J., Gramajo, H., Cane, D. E., and Khosla, C. (2001) Biosynthesis of complex polyketides in a metabolically engineered strain of E. Coli Science 291, 1790-1792
64. Zhang, H., Wang, Y., and Pfeifer, B. A. (2008) Bacterial hosts for natural product production Mol. Pharm. 5, 212-225
65. Hosaka, T., Ohnishi-Kameyama, M., Muramatsu, H., Murakami, K., Tsurumi, Y., Kodani, S., Yoshida, M., Fujie, A., and Ochi, K. (2009) Antibacterial discovery in actinomycetes strains with mutations in RNA polymerase or ribosomal protein S12 Nat. Biotechnol. 27, 462-464
66. Zhou, M., Jing, X., Xie, P., Chen, W., Wang, T., Xia, H., and Qin, Z. (2012) Sequential deletion of all the polyketide synthase and nonribosomal peptide synthetase biosynthetic gene clusters and a 900-kb subtelomeric sequence of the linear chromosome of Streptomyces coelicolor FEMS Microbiol. Lett. 333, 169-179
67. Alduina, R. and Gallo, G. (2012) Artificial chromosomes to explore and to exploit biosynthetic capabilities of actinomycetes J. Biomed. Biotechnol. 2012, 462049