Glycopeptide antibiotic biosynthesis

Journal of Antibiotics

Volumn 67, Issue 1, 2014, Pages 31-41

  Yim, Grace ^a   Thaker, Maulik N ^a   Koteva, Kalinka ^a   Wright, Gerard ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

Biosynthesis; Glycopeptide; Resistance; Teicoplanin; Vancomycin

Indexed keywords

A 40926; A47934; AMINO ACID; AZ 205; BALHIMYCIN; CA 37; CA 878; CA 915; CHLOROEREMOMYCIN; DALBAVANCIN; HEPTAPEPTIDE; PEKISKOMYCIN; POLYPEPTIDE ANTIBIOTIC AGENT; TEICOPLANIN; UK 68597; UNCLASSIFIED DRUG; VANCOMYCIN;

ACCESSORY RESISTANCE GENE; ACTINOBACTERIA; ACYLATION; ANTIBIOTIC BIOSYNTHESIS; ANTIBIOTIC RESISTANCE; BACTERIAL GENE; CHLORINATION; CORE RESISTANCE GENE; DRUG STRUCTURE; DRUG SULFATION; GLYCOSYLATION; METHYLATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN CROSS LINKING; REGULATOR GENE; REVIEW;

ANTI-BACTERIAL AGENTS; CELL WALL; DRUG DESIGN; DRUG RESISTANCE, BACTERIAL; GLYCOPEPTIDES; GRAM-POSITIVE BACTERIA; GRAM-POSITIVE BACTERIAL INFECTIONS; HUMANS; MOLECULAR TARGETED THERAPY;

EID: 84893142381     PISSN: 00218820     EISSN: 18811469     Source Type: Journal    
DOI: 10.1038/ja.2013.117     Document Type: Review

References (81)

1. Levine, D. P. Vancomycin: A history. Clin. Infect. Dis. 42 (Suppl 1), S5-12 (2006
2. Kirst, H. A., Thompson, D. G. & Nicas, T. I. Historical yearly usage of vancomycin. Antimicrob. Agents Chemother. 42, 1303-1304 (1998
3. Williams, A. H. & Gruneberg, R. N. Teicoplanin. J. Antimicrob. Chemother. 14, 441-445 (1984
4. Cynamon, M. H. & Granato, P. A. Comparison of the in vitro activities of teichomycin A2 and vancomycin against staphylococci and enterococci. Antimicrob. Agents Chemother. 21, 504-505 (1982
5. Pelzer, S. et al. 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 (1999
6. van Wageningen, A. M. et al. Sequencing and analysis of genes involved in the biosynthesis of a vancomycin group antibiotic. Chem. Biol. 5, 155-162 (1998
7. Woertz, T., Dietz, S., Zerbe, K. & Robinson, J. A. Amycolatopsis orientalis vancomycin biosynthesis cluster, strain ATCC19795. Accession no. HE589771. GenBank (2011
8. Jeong, H et al. Genome sequence of the vancomycin-producing Amycolatopsis orientalis subsp. orientalis strain KCTC 9412T. Genome Announc. 1, e00408-13 (2013
9. Sosio, M., Stinchi, S., Beltrametti, F., Lazzarini, A. & Donadio, S. The gene cluster for the biosynthesis of the glycopeptide antibiotic A40926 by nonomuraea species. Chem. Biol. 10, 541-549 (2003
10. Pootoolal, J. et al. Assembling the glycopeptide antibiotic scaffold: The biosynthesis of A47934 from Streptomyces toyocaensis NRRL15009. Proc. Natl Acad. Sci. USA 99, 8962-8967 (2002
11. Sosio, M. et al. Organization of the teicoplanin gene cluster in Actinoplanes teichomyceticus. Microbiology 150 (Pt 1), 95-102 (2004
12. Li, T. L. et al. Biosynthetic gene cluster of the glycopeptide antibiotic teicoplanin: Characterization of two glycosyltransferases and the key acyltransferase. Chem. Biol. 11, 107-119 (2004
13. Thaker, M. N. et al. Identifying producers of antibacterial compounds by screening for antibiotic resistance. Nat. Biotechnol. 31, 922-927 (2013
14. Yim, G. et al. Characterization of the UK-68,597 biosynthetic cluster: Harnessing the synthetic capabilities of glycopeptide tailoring enzymes Unpublished
15. Banik, J. J., Craig, J. W., Calle, P. Y. & Brady, S. F. Tailoring enzyme-rich environmental DNA clones: A source of enzymes for generating libraries of unnatural natural products. J. Am. Chem. Soc. 132, 15661-15670 (2010
16. Banik, J. J. & Brady, S. F. Cloning and characterization of new glycopeptide gene clusters found in an environmental DNA megalibrary. Proc. Natl Acad. Sci. USA 105, 17273-17277 (2008
17. Owen, J. G. et al. Mapping gene clusters within arrayed metagenomic libraries to expand the structural diversity of biomedically relevant natural products. Proc. Natl Acad. Sci. USA 110, 11797-11802 (2013
18. Marahiel, M. A. & Essen, L. O. Chapter 13Nonribosomal peptide synthetases mechanistic and structural aspects of essential domains. Methods Enzymol. 458, 337-351 (2009
19. Hahn, M. & Stachelhaus, T. Harnessing the potential of communication-mediating domains for the biocombinatorial synthesis of nonribosomal peptides. Proc. Natl Acad. Sci. USA 103, 275-280 (2006
20. Stachelhaus, T., Mootz, H. D. & Marahiel, M. A. The specificity-conferring code of adenylation domains in nonribosomal peptide synthetases. Chem. Biol. 6, 493-505 (1999
21. Linne, U., Doekel, S. & Marahiel, M. A. Portability of epimerization domain and role of peptidyl carrier protein on epimerization activity in nonribosomal peptide synthetases. Biochemistry 40, 15824-15834 (2001
22. Stachelhaus, T. & Walsh, C. T. Mutational analysis of the epimerization domain in the initiation module PheATE of gramicidin S synthetase. Biochemistry 39, 5775-5787 (2000
23. Luo, L et al. Timing of epimerization and condensation reactions in nonribosomal peptide assembly lines: Kinetic analysis of phenylalanine activating elongation modules of tyrocidine synthetase B. Biochemistry 41, 9184-9196 (2002
24. Medema, M. H. et al. antiSMASH: Rapid identification, annotation and analysis of secondary metabolite biosynthesis gene clusters in bacterial and fungal genome sequences. Nucleic Acids Res. 39 (Web Server issue), W339-W346 (2011
25. Pootoolal, J., Neu, J. & Wright, G. D. Glycopeptide antibiotic resistance. Annu. Rev. Pharmacol. Toxicol. 42, 381-408 (2002
26. Nicolaou, K. C., Boddy, C. N., Brase, S. & Winssinger, N. Chemistry, biology, and medicine of the glycopeptide antibiotics. Angew. Chem. Int. Ed. Engl. 38, 2096-2152 (1999
27. Stegmann, E. et al. Genetic analysis of the balhimycin (vancomycin-type) oxygenase genes. J. Biotechnol. 124, 640-653 (2006
28. Hadatsch, B. et al. The biosynthesis of teicoplanin-type glycopeptide antibiotics: Assignment of p450 mono-oxygenases to side chain cyclizations of glycopeptide a47934. Chem. Biol. 14, 1078-1089 (2007
29. Cryle, M. J., Staaden, J. & Schlichting, I. Structural characterization of CYP165D3, a cytochrome P450 involved in phenolic coupling in teicoplanin biosynthesis. Arch. Biochem. Biophys. 507, 163-173 (2011
30. Li, Z., Rupasinghe, S. G., Schuler, M. A. & Nair, S. K. Crystal structure of a phenolcoupling P450 monooxygenase involved in teicoplanin biosynthesis. Proteins 79, 1728-1738 (2011
31. Woithe, K. et al. Oxidative phenol coupling reactions catalyzed by OxyB: A cytochrome P450 from the vancomycin producing organism. implications for vancomycin biosynthesis. J. Am. Chem. Soc. 129, 6887-6895 (2007
32. Chen, H., Tseng, C. C., Hubbard, B. K. & Walsh, C. T. Glycopeptide antibiotic biosynthesis: Enzymatic assembly of the dedicated amino acid monomer (S)-3, 5-dihydroxyphenylglycine. Proc. Natl Acad. Sci. USA 98, 14901-14906 (2001
33. Pfeifer, V. et al. A polyketide synthase in glycopeptide biosynthesis: The biosynthesis of the non-proteinogenic amino acid (S)-3,5- dihydroxyphenylglycine. J. Biol. Chem. 276, 38370-38377 (2001
34. Sandercock, A. M. et al. Biosynthesis of the di-hydroxyphenylglycine constituent of the vancomycin-group antibiotic chloroeremomycin. Chem. Commun. 14, 1252-1253 (2001
35. Hubbard, B. K., Thomas, M. G. & Walsh, C. T. Biosynthesis of L-p-hydroxyphenylglycine, a non-proteinogenic amino acid constituent of peptide antibiotics. Chem. Biol. 7, 931-942 (2000
36. Chen, H. & Walsh, C. T. Coumarin formation in novobiocin biosynthesis: Betahydroxylation of the aminoacyl enzyme tyrosyl-S-NovH by a cytochrome P450 NovI. Chem. Biol. 8, 301-312 (2001
37. Chen, H., Hubbard, B. K., O'Connor, S. E. & Walsh, C. T. Formation of beta-hydroxy histidine in the biosynthesis of nikkomycin antibiotics. Chem. Biol. 9, 103-112 (2002
38. Donadio, S., Sosio, M., Stegmann, E., Weber, T. & Wohlleben, W. Comparative analysis and insights into the evolution of gene clusters for glycopeptide antibiotic biosynthesis. Mol. Genet. Genomics 274, 40-50 (2005
39. Puk, O. et al. Biosynthesis of chloro-beta-hydroxytyrosine, a nonproteinogenic amino acid of the peptidic backbone of glycopeptide antibiotics. J. Bacteriol. 186, 6093-6100 (2004
40. Recktenwald, J. et al. Nonribosomal biosynthesis of vancomycin-type antibiotics: A heptapeptide backbone and eight peptide synthetase modules. Microbiology 148 (Pt 4), 1105-1118 (2002
41. Puk, O. et al. Glycopeptide biosynthesis in Amycolatopsis mediterranei DSM5908: Function of a halogenase and a haloperoxidase/perhydrolase. Chem. Biol. 9, 225-235 (2002
42. Cryle, M. J., Meinhart, A. & Schlichting, I. Structural characterization of OxyD, a cytochrome P450 involved in beta-hydroxytyrosine formation in vancomycin biosynthesis. J. Biol. Chem. 285, 24562-24574 (2010
43. Mulyani, S. et al. The thioesterase Bhp is involved in the formation of betahydroxytyrosine during balhimycin biosynthesis in Amycolatopsis balhimycina. Chembiochem. 11, 266-271 (2010
44. Stinchi, S. et al. A derivative of the glycopeptide A40926 produced by inactivation of the beta-hydroxylase gene in Nonomuraea sp. ATCC39727. FEMS Microbiol. Lett. 256, 229-235 (2006
45. Truman, A. W. et al. Chimeric glycosyltransferases for the generation of hybrid glycopeptides. Chem. Biol. 16, 676-685 (2009
46. Losey, H. C. et al. Incorporation of glucose analogs by GtfE and GtfD from the vancomycin biosynthetic pathway to generate variant glycopeptides. Chem. Biol. 9, 1305-1314 (2002
47. Lu, W. et al. Characterization of a regiospecific epivancosaminyl transferase GtfA and enzymatic reconstitution of the antibiotic chloroeremomycin. Proc. Natl Acad. Sci. USA 101, 4390-4395 (2004
48. Losey, H. C. et al. Tandem action of glycosyltransferases in the maturation of vancomycin and teicoplanin aglycones: Novel glycopeptides. Biochemistry 40, 4745-4755 (2001
49. Mulichak, A. M. et al. Structure of the TDP-epi-vancosaminyltransferase GtfA from the chloroeremomycin biosynthetic pathway. Proc. Natl Acad. Sci. USA 100, 9238-9243 (2003
50. Chen, H. et al. Deoxysugars in glycopeptide antibiotics: Enzymatic synthesis of TDP-Lepivancosamine in chloroeremomycin biosynthesis. Proc. Natl Acad. Sci. USA 97, 11942-11947 (2000
51. Kahne, D., Leimkuhler, C., Lu, W. & Walsh, C. Glycopeptide and lipoglycopeptide antibiotics. Chem. Rev. 105, 425-448 (2005
52. Kruger, R. G. et al. Tailoring of glycopeptide scaffolds by the acyltransferases from the teicoplanin and A-40,926 biosynthetic operons. Chem. Biol. 12, 131-140 (2005
53. Howard-Jones, A. R. et al. Kinetic analysis of teicoplanin glycosyltransferases and acyltransferase reveal ordered tailoring of aglycone scaffold to reconstitute mature teicoplanin. J. Am. Chem. Soc. 129, 10082-10083 (2007
54. Ho, J. Y. et al. 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 (2006
55. Gerhard, U., Mackay, J. P., Maplestone, R. A. & Williams, D. H. The role of the sugar and chlorine substituents in the dimerization of vancomycin antibiotics. J. Am. Chem. Soc. 115, 232-237 (1993
56. Williams, D. H. & Bardsley, B. The vancomycin group of antibiotics and the fight against resistant bacteria. Ange. Chem. Int. Ed. 38, 1172-1193 (1999
57. Schmartz, P. C. et al. Substituent effects on the phenol coupling reaction catalyzed by the vancomycin biosynthetic P450 enzyme OxyB. Angew. Chem. Int. Ed. Engl. 51, 11468-11472 (2012
58. Bischoff, D. et al. The biosynthesis of vancomycin-type glycopeptide antibiotics-A model for oxidative side-chain cross-linking by oxygenases coupled to the action of peptide synthetases. Chembiochem. 6, 267-272 (2005
59. Lamb, S. S., Patel, T., Koteva, K. P. & Wright, G. D. Biosynthesis of sulfated glycopeptide antibiotics by using the sulfotransferase StaL. Chem. Biol. 13, 171-181 (2006
60. Shi, R. et al. Sulfonation of glycopeptide antibiotics by sulfotransferase StaL depends on conformational flexibility of aglycone scaffold. Proc. Natl Acad. Sci. USA 109, 11824-11829 (2012
61. Bick, M. J., Banik, J. J., Darst, S. A. & Brady, S. F. The 2.7 A resolution structure of the glycopeptide sulfotransferase Teg14. Acta. Crystallogr. D Biol. Crystallogr. 66 (Pt 12), 1278-1286 (2010
62. Bick, M. J., Banik, J. J., Darst, S. A. & Brady, S. F. Crystal structures of the glycopeptide sulfotransferase Teg12 in a complex with the teicoplanin aglycone. Biochemistry 49, 4159-4168 (2010
63. Shi, R. et al. Structure and function of the glycopeptide N-methyltransferase MtfA, a tool for the biosynthesis of modified glycopeptide antibiotics. Chem. Biol. 16, 401-410 (2009
64. O'Brien, D. P. et al. Expression and assay of an -methyltransferase involved in the biosynthesis of a vancomycin group antibiotic. Chem. Commun. 1, 103-104 (2000
65. Courvalin, P. Vancomycin resistance in gram-positive cocci. Clin. Infect. Dis. 42 (Suppl 1), S25-S34 (2006
66. Cundliffe, E. & Demain, A. L. Avoidance of suicide in antibiotic-producing microbes. J. Ind. Microbiol. Biotechnol. 37, 643-672 (2010
67. McComas, C. C., Crowley, B. M. & Boger, D. L. Partitioning the loss in vancomycin binding affinity for D-Ala-D-Lac into lost H-bond and repulsive lone pair contributions. J. Am. Chem. Soc. 125, 9314-9315 (2003
68. Bugg, T. D. et al. Molecular basis for vancomycin resistance in Enterococcus faecium BM4147: Biosynthesis of a depsipeptide peptidoglycan precursor by vancomycin resistance proteins VanH and VanA. Biochemistry 30, 10408-10415 (1991
69. Schaberle, T. F. et al. Self-resistance and cell wall composition in the glycopeptide producer Amycolatopsis balhimycina. Antimicrob. Agents Chemother. 55, 4283-4289 (2011
70. Baptista, M., Depardieu, F., Courvalin, P. & Arthur, M. Specificity of induction of glycopeptide resistance genes in Enterococcus faecalis. Antimicrob. Agents Chemother. 40, 2291-2295 (1996
71. Koteva, K. et al. A vancomycin photoprobe identifies the histidine kinase VanSsc as a vancomycin receptor. Nat. Chem. Biol. 6, 327-329 (2010
72. Kwun, M. J., Novotna, G., Hesketh, A. R., Hill, L. & Hong, H. J. 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 (2013
73. Arthur, M., Molinas, C. & Courvalin, P. The VanS-VanR two-component regulatory system controls synthesis of depsipeptide peptidoglycan precursors in Enterococcus faecium BM4147. J. Bacteriol. 174, 2582-2591 (1992
74. Kalan, L., Perry, J., Koteva, K., Thaker, M. & Wright, G. Glycopeptide sulfation evades resistance. J. Bacteriol. 195, 167-171 (2013
75. Beltrametti, F. et al. Resistance to glycopeptide antibiotics in the teicoplanin producer is mediated by van gene homologue expression directing the synthesis of a modified cell wall peptidoglycan. Antimicrob. Agents Chemother. 51, 1135-1141 (2007
76. Wright, G. D., Molinas, C., Arthur, M., Courvalin, P. & Walsh, C. T. Characterization of vanY, a DD-carboxypeptidase from vancomycin-resistant Enterococcus faecium BM4147. Antimicrob. Agents Chemother. 36, 1514-1518 (1992
77. Marcone, G. L. et al. Novel mechanism of glycopeptide resistance in the A40926 producer Nonomuraea sp. ATCC 39727. Antimicrob. Agents Chemother. 54, 2465-2472 (2010
78. Hong, H. J. et al. Characterization of an inducible vancomycin resistance system in Streptomyces coelicolor reveals a novel gene (vanK) required for drug resistance. Mol. Microbiol. 52, 1107-1121 (2004
79. Novotna, G., Hill, C., Vincent, K., Liu, C. & Hong, H. J. A novel membrane protein, VanJ, conferring resistance to teicoplanin. Antimicrob. Agents Chemother. 56, 1784-1796 (2012
80. Serina, S., Radice, F., Maffioli, S., Donadio, S. & Sosio, M. Glycopeptide resistance determinants from the teicoplanin producer Actinoplanes teichomyceticus. FEMS Microbiol. Lett. 240, 69-74 (2004
81. Thaker, M. N. & Wright, G. D. Opportunities for synthetic biology in antibiotics: Expanding glycopeptide chemical diversity. ACS Synth. Biol. (e-pub ahead of print 28 December 2013; doi:10.1021/sb300092n