Biosynthesis of glycopeptides: Prospects for improved antibacterials

Current Topics in Medicinal Chemistry

Volumn 8, Issue 8, 2008, Pages 654-666

  Donadio, Stefano ^a   Sosio, Margherita ^a  

^a Ktedogen Srl   (Italy)

Author keywords

Antibiotic; Combinatorial biosynthesis; Multi resistant pathogens; Natural product

Indexed keywords

A 40926; A 40926 DERIVATIVE; A47934; ANTIBIOTIC AGENT; AVOPARCIN; BALHIMYCIN; BALHIMYCIN AGLYCONE; CHLOROEREMOMYCIN; CHLOROPEPTIN; COMPLESTATIN; DALBAVANCIN; DECHLOROBALHIMYCIN; DECHLOROMANNOSYLAGLYCONE; FLUOROBALHIMYCIN DERIVATIVE; METHOXBALHIMYCIN DERIVATIVE; ORITAVANCIN; POLYPEPTIDE ANTIBIOTIC AGENT; RISTOCETIN; SULFOTEICOPLANIN; SULFOTEICOPLANIN AGLYCONE; TEICOPLANIN; TELAVANCIN; VANCOMYCIN;

ACTINOBACTERIA; ACYLATION; ANTIBACTERIAL ACTIVITY; ANTIBIOTIC RESISTANCE; BACTERIAL CELL WALL; BACTERIAL GROWTH; CHEMICAL MODIFICATION; CHLORINATION; COMBINATORIAL CHEMISTRY; CROSS LINKING; DRUG HALF LIFE; DRUG MECHANISM; DRUG STRUCTURE; DRUG SYNTHESIS; GENETIC MANIPULATION; GLYCOSYLATION; GRAM POSITIVE BACTERIUM; GROWTH INHIBITION; HALOGENATION; HUMAN; INFECTION; METHYLATION; MULTIDRUG RESISTANCE; NONHUMAN; REVIEW; STRUCTURE ACTIVITY RELATION; SULFATION;

AMINO ACIDS; ANIMALS; ANTI-BACTERIAL AGENTS; CROSS-LINKING REAGENTS; GLYCOPEPTIDES; HALOGENATION; HUMANS;

EID: 47249159015     PISSN: 15680266     EISSN: None     Source Type: Journal    
DOI: 10.2174/156802608784221541     Document Type: Review

References (71)

1. Zmijewski, M. J., Jr.; Fayerman, J. T. Glycopeptides. In Genetics and Biochemistry of Antibiotic Prodiction; Vining, L. C.; Stuttard, C. ; Eds. Butterworth-Heinemann: Boston, 1995; pp. 269-281.
2. Pelzer, S.; Süßmuth, R. D.; Heckmann, D.; Recktenwald, J.; Huber, P.; Jung, G.; Wohlleben, W. Identification and analysis of the balhimycin biosynthetic gene cluster and its use for manipulating glycopeptide biosynthesis in Amycolatopsis mediterranei DSM5908. Antimicrob. Agents Chemother. 1999, 43, 1565-1573
3. Recktenwald, J.; Shawky, R.; Puk, O.; Pfenning, F.; Keller, U.; Wohlleben, W.; Pelzer, S. Nonribosomal biosynthesis of vancomycun-type antibiotics: A heptapeptide backbone and eight peptide synthetase modules. Microbiology 2002, 148, 1105-1118.
4. 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. Sequencing and analysis of genes involved in the biosynthesis of a vancomycin group antibiotic. Chem. Biol. 1998, 5, 155-162.
5. Chiu, H. T.; Hubbard, B. K.; Shah, A. N.; Eide, J.; Fredenburg, R. A.; Walsh, C. T.; Khosla, C. Molecular cloning and sequence analysis of the complestatin biosynthetic gene cluster. Proc. Natl. Acad. Sci. USA 2001, 98, 8548-8553.
6. Pootoolal, J.; Thomas, M. G.; Marshall, C. G.; Neu, J. M.; Hubbard, B. K.; Walsh, C.T.; Wright, G. D. Assembling the glycopeptide antibiotic scaffold: The biosynthesis of A47934 from Streptomyces toyocaensis NRRL15009. Proc. Natl. Acad. Sci. USA 2002, 99, 8962-8967.
7. 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. 2003, 10, 541-549.
8. Sosio, M.; Kloosterman, H.; Bianchi, A.; de Vreugd, P.; Dijkhuizen, L.; Donadio, S. Organization of the taicoplanin gene cluster in Actinoplanes teichomyceticus. Microbiology 2004, 150, 95-102.
9. Li, T. L.; Huang, F.; Haydock, S. F.; Mironenko, T.; Leadlay, P. F.; Spencer, J. B. Biosynthetic gene cluster of the glycopeptide antibiotic teicoplanin: Characterization of two glycosyltransferases and the key acyltransferase. Chem. Boil. 2004, 11, 107-119
10. Donadio, S.; Sosio, M.; Stegmann, E.; Weber, T.; Wofilleben, W. Comparative analysisi and insight into the evolution of gene clusters for glycopeptide antibiotic biosynthesis. Mol. Genet. Genomics 2005, 274, 40-50.
11. Nicolaou, K. C.; Boddy, C. N. C.; Brase, S.; Winssinger, N. Chemistry, biology and medicine of glycopeptide antibiotics. Angew. Chem. 1999, 111, 2230-2287.
12. Boger, D. L. Vancomycin, teicoplanin, and ramoplanin: Synthetic and mechanistic studies. Med. Res. Rev. 2001, 21, 356-381.
13. Malabarba, A.; Ciabatti, R. Glycopeptide derivatives. Curr. Med. Chem. 2001, 8, 1759-1773.
14. Hubbard, B. K.; Walsh, C. T. Vancomycin assembly: Nature's way. Angew. Chem. Int. Ed. 2002, 42, 730-765.
15. Allen, N. E.; Nicas, T. I. Mechanism of action of oritavancin and related glycopeptide antibiotics. FEMS Microbiol Rev. 2003, 26, 511-532.
16. Judice, J. K.; Pace, J. L. Semi-synthetic glycopeptide antibacterials. Bioorg. Med. Chem. Lett. 2003, 13, 4165-4168.
17. Süßmuth, R. D.; Wohlleben, W. The biosynthesis of glycopeptide antibiotics - a model for complex, non-ribosomally synthesized, peptidic secondary metabolites. Appl. Microbiol. Biotechnol. 2004, 63, 344-350.
18. Kahne, T.; Leimkuhler, C.; Lu, W.; Walsh, C. T. Glycopeptide and lipoglycopeptide antibiotics. Chem. Rev. 2005, 105, 425-448.
19. Stegmann, E.; Biscboff, D.; Kittel, C.; Pelzer, S.; Puk, O.; Recktenwald, J.; Weist, S.; Süßmuth, R. D.; Wohlleben, W. Precursor-directed biosynthesis for the generation of novel glycopetides. Ernst Schering Res. Found. Workshop 2005, 51, 215-232.
20. Pace, J. L.; Yang, G. Glycopeptides: Update on an old successful antibiotic class. Biochem. Pharmacol. 2006, 71, 968-980.
21. Sosio, M.; Donadio, S. Understanding and manipulating glycopeptide pathways: The example of the dalbavencin precursor A40926. J. Ind. Microbiol. Biotechnol. 2006, 33, 569-576.
22. Anderson, J. S.; Matsuhashi, M.; Haskin, M. A.; Strominger, J. L. Lipid-phosphoacetylmuramyl-pentapeptide and lipid-phosphodisaccharide-pentapeptide: Presumed membrane transport intermediates in cell wall synthesis. Proc. Natl. Acad. Sci. USA 1965, 53, 881-889.
23. Williams, D. H.; Williamson, M. P.; Butcher, D. W.; Hammond, S. J. Detailed binding sites of the antibiotics vancomycin and ristocetin A: determination of intermolecular distances in antibiotic/substrate complexes by use of the time-dependent NOE. J. Am. Chem. Soc. 1983, 105, 1332-1339.
24. Sharman, G. J.; Try, A. C.; Dancer, R. J.; Cho, Y. R.; Staroske, T.; Bardsley, B.; Maguire, A. J.; Cooper, M. A.; O'Brien, D. P.; William , D. H. The roles of dimerization and membrane anchoring in activity of glycopeptide antibiotics against vancomycin-resistant bacteria. J. Am. Chem. Soc. 1997, 119, 12041-12047.
25. Ge M.; Chen, Z.; Onishi, H. R.; Kohler, J.; Silver, L. L.; Kerns, R.; Fukuzawa, S.; Thompson, C.; Kahne, D. Vancomycin derivatives that inhibit peptidoglycan biosynthesis without binding D-Ala-D-Ala. Science 1999, 284, 442-443.
26. Chen, L.; Walker. D.; Sun, B.; Hu, Y.; Walker, S.; Kahne, D. Vancomycin analogues active against vanA-resistant strains inhibit bacterial transglycosylase without binding substrate. Proc. Natl. Acad. Sci. USA 2003, 100, 5658-5663.
27. Leimkuhler, C.; Chen, L.; Barrett, D.; Panzone, G.; Sun, B.; Falcone, B.; Oberthur, M.; Donadio, S.; Walker, S.; Kahne, D. (2005) Differential inhibition of Staphylococcus aureus PBP2 by glycopeptide antibiotics. J. Am. Chem. Soc. 2005, 127, 3250-3251
28. Breukink, E.; de Kruijff, B. Lipid II as a target for antibiotics. Nat. Rev. Drug Discov. 2006, 5, 321-332.
29. Cetinkaya, Y.; Falk, P.; Mayhall, C. G. Vancomycin-resistant enterococci. Clin. Microbiol. Rev. 2000, 13, 686-707.
30. Weigel, L. M.; Clewell, D. B.; Gill, S. R.; Clark, N. C.; McDougal, L. K.; Flannagan, S. E.; Kolonay, J. F.; Shetty, J.; Killgore, G. E.; Tenover. F. C. Genetic analysis of a high-level vancomycin-resistant isolate of Staphylococcus aureus. Science 2003, 302, 1569-1571.
31. Hubbard, B. K.; Thomas, M. G.; Walsh, C. T. Biosynthesis of L-phydroxyphenylglycine, a non-proteinogenic amino acid constituent of peptide antibiotics. Chem. Biol. 2000, 7, 931-942
32. Choroba, O. W.; Williams, D. H.; Spencer, J. B. Biosynthesis of the vancomycin group of antibiotics: Involvement of an unusual dioxygmase in the pathway to (S)-4-hydroxyphenylglycine. J. Am. Chem. Soc. 2000, 122, 5389-5390.
33. Li, T. L.; Choroba, O. W.; Charles, E. H.; Sandercock, A.M.; Williams, D. H.; Spencer, J. B. Characterisation of a hydroxymandelate oxidase involved in the biosynthesis of two unusual amino acids occurring in the vancomycin group of antibiotics. Chem. Commun. 2001, 1752-1753.
34. 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-dihydroxyphenylglycinc. Proc. Natl. Acad. Sci. USA 2001, 98, 14901-14906.
35. Li, T. L.; Choroba, O. W.; Hong, H.; Williams, D. H.; Spencer, J. B. Biosynthesis of the vancomycin group of antibiotics: Characterisation of a type III polyketide synthase in the pathway to (S)-3,5-duhydroxyphenylglycine. Chem. Commun. 2001, 2156-2157.
36. Pfeifer, V.; Nicholson, G. J.; Ries, J.; Recktenwald, J.; Schefer, A. B.; Shawky, R. M.; Schroder, J.; Wohlleben, W.; Pelzer, S. A polyketide synthase in glycopeptide biosynthesis: The biosynthesis of the non-proteinogenic amino acid (S)-3,5-dihydroxyphenylglycine. J. Biol. Chem. 2001, 276, 38370-38377.
37. Tseng, C. C.; Vaillancourt, F. H.; Bruner, S. D.; Walsh, C. T. DpgC is a metal- and cofactor-free 3,5-dihydroxyphenylacetyl-CoA 1,2-dioxygenase in the vancomycin biosynthetic pathway. Chem. Biol. 2004, 11, 1195-1203.
38. Chen, H.; Walsh, C. T. Coumarin formation in novobiocin biosynthesis: beta-hydroxylation of the aminoacyl enzyme tyrosyl-S-NovH by a cytochrome P450 Nov1. Chem. Biol. 2001, 8, 301-312.
39. Puk, O.; Bischoff, D.; Kittel, C.; Pelzer, S.; Weist, S.; Stegmann, E.; Süßmuth, R. D.; Wohlleben, W. Biosynthesis of chloro-beta-hydroxytyrosine, a nonproteinogenic amino acid of the peptidic backbone of glycopeptide antibiotics. J. Bacteriol. 2004, 186, 6093-6100.
40. Puk, 0.; Huber, P.; Bischoff, D.; Recktenwald, J.; Jung, G.; Süßmuth, R. D.; van Pee, K. H.; Wohlleben, W.; Pelzer, S. Glycopeptide biosynthesis in Amycolatopsis mediterranel: Function of a halogenase and a haloperoxidase/perhydrolase. Chem. Biol. 2002, 9, 225-235.
41. Stinchi, S.; Carrano, L.; Lazzarini, A.; Feroggio, M.; Grigoletto, A.; Sosio, M.; Donadio, S. A derivative of the glycopeptide A40926 produced by inactivation of the beta-hydroxylase gene in Nonomuraea sp. ATCC39727. FEMS Microbiol. Lett. 2006, 256, 229-235.
42. Trauger, J. W.; Walsh, C. T. Heterologous expression in Escherichia coli of the first module of the nonribosomal peptide synthetase for chloroeremomycin, a vancomycin-type glycopeptide antibiotic. Proc. Natl. Acad. Sci. USA 2000, 97, 3112-3117.
43. Bischoff, D.; Bister, B.; Bertazzo, M.; Pfeifer, V.; Stegmann, E.; Nicholson, G. J.; Keller, S.; Pelzer, S.; Wohlleben, W.; Süßmuth, R. D. 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. 2005, 6, 267-272.
44. Bischoff, D.; Pelzer, S.; Bister, B.; Nicholson, G. J.; Stockert, S.; Schirle, M.; Wohlleben, W.; Jung, G.; Süßmuth, R. D. The biosynthesis of vancomycin-type glycopeptide antibiotics - the order of the cyclization steps. Angew. Chem. Int. Ed. Engl. 2001, 40, 4688-4691.
45. Zerbe, K.; Pylypenko, O.; Vitali, F.; Zhang, W.; Rouset, S.; Heck, M.; Vrijbloed, J. W.; Bischoff, D.; Bister, B.; Süßmuth, R. D.; Pelzer, S.; Wohlleben, W.; Robinson. J. A.; Schlichting, I. Crystal structure of OxyB, a cytochrome P450 implicated in an oxidative phenol coupling reaction during vancomycin biosynthesis. J. Biol. Chem. 2002, 277, 47476-47485.
46. Zerbe, K.; Woithe, K.; Li, D. B.; Vitali, F.; Bigler, L.; Robinson, J. A. An oxidative phenol coupling reaction catalyzed by oxyB, a cytochrome P450 from the vancomycin-producing microorganism. Angew. Chem. Int. Ed. Engl. 2004, 43, 6709-6713.
47. Pylypenko, O.; Vitali, F.; Zerbe, K.; Robinson, J. A.; Schlichting, I. Crystal structure of OxyC, a cytochrome P450 implicated in an oxidative C-C coupling reaction during vancomycin biosynthesis. J. Biol. Chem. 2003, 278, 46727-46733.
48. Chen, H.; Thomas, M. G.; Hubbard, B. K.; Losey, H. C.; Walsh, C. T.; Burkart, M. D. Deoxysugars in glycopotide antibiotics: Enzymatic synthesis of TDP-L-epivancosamine in chloroeremomycin biosynthesis. Proc. Natl. Acad Sci. USA 2000, 97, 11942-11947.
49. Kirkpatrick, P. N.; Scaife, W.; Hallis, T. M.; Liu, H.-w.; Spencer, J. B.; Williams, D. H. Characterisation of a sugar epimentse enzyme involved in the biosynthesis of a vancomycin-group antibiotic. Chem. Commun. 2000, 1565-1566.
50. Solenberg, P. J.; Matsushima, P.; Stack, D. R.; Wilkie, S. C.; Thompson, R. C.; Baltz, R. H. Production of hybrid glycopeptide antibiotics in vitro and in Streptomyces toyocaensis. Chem. Biol. 1997, 4, 195-202.
51. Losey, H. C.; Peczuh, M. W.; Chen, Z.; Eggert, U. S.; Dong, S. D.; Pelczer, I.; Kalme, D.; Walsh, C. T. Tandem action of glycosyltransferases in the maturation of vancomycin and teicoplanin aglycones: Novel glycopeptides. Biochemistry 2001, 40, 4745-4755.
52. Mulichak, A. M.; Losey, H. C.; Walsh, C. T.; Garavito, R. M. Structure of the UDP-glucosyltransferase GtfB that modifies the heptapeptide aglycone in the biosyrithesis of vancomycin group antibiotics. Structure 2001, 9, 547-557.
53. Mulichak, A. M.; Losey, H. C.; Lu, W.; Wawrzak, Z.; Walsh, C. T.; Garavito, R. M. Structure of the TDP-epi-vancosaminyltransferase GtfA from the chloroeremomycin biosynthetic pathway. Proc. Natl. Acad. Sci. USA 2003, 100, 9238-9243.
54. Lu, W.; Oberthur, M.; Leimkuhler, C.; Tao, J.; Kahne, D.; Walsh, C. T. Characterization of a regiospecific epivancosaminyl transferase GtfA and enzymatic reconstitution of the antibiotic chloroeremomycin. Proc. Natl. Acad. Sci. USA 2004, 101, 4390-4395.
55. Mulichak, A. M.; Lu, W.; Losey, H. C.; Walsh, C. T.; Garavito, R. M. Crystal structure of vancosaminyltransferase GtfD from the vancomycin biosynthetic pathway: Interactions with acceptor and nucleotide ligands. Biochemistry 2004, 43, 5170-5180.
56. O'Brien, D. P.; Kirkpatrick, P.N.; O'Brien, S. W.; Staroske, T.; Richardson, T. I.; Evans, D. A.; Hopkinson,'A.; Spencer, J. B.; Williams, D. H. Expression and assay of an N-methyltransferase involved in the biosynthesis of a vancomycin group antibiotic. Chem. Commun. 2000, 103-104.
57. Ho, J. Y.; Huang, Y. T.; Wu, C. J.; Li, Y. S.; Tsai, M. D.; Li, T. L. 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-l-P thymidyltransferase. J. Am. Chem. Soc. 2006, 128, 13694-13695.
58. Truman, A. W.; Robinson, L.; Spencer, J. B. Identification of a deacetylase involved in the maturation of teicoplanin. Chembiochem. 2006, 7, 1670-1675.
59. Borghi, A.; Edwaeds, D.; Zerilli, L. F.; Lancini, G. C. Factors affecting the normal and branched-chain acyl moieties of teicoplanin components produced by Actinoplanes teichomyceticus. J. Gen. Microbiol. 1991, 137, 587-592.
60. Lamb, S. S.; Patel, T.; Koteva, K P.; Wright, G. D. Biosynthesis of sulfated glycopeptide antibiotics by using the sulfotransferase StaL. Chem. Biol. 2006, 13, 171-181.
61. Shi, R.; Lamb, S. S.; Bhat, S.; Sulea, T.; Wright, G. D.; Matte, A.; Cygler, M. Crystal structure of StaL, a glycopeptide antibiotic sulfotransferase from Streptomyces toyocaensis. J. Biol. Chem. 2007, 282, 13073-13086.
62. Weist, S.; Bister, B.; Puk, O.; Bischoff, D.; Pelzer, S.; Nicholson, G. J.; Wohlleben, W.; Jung, G.; Sussmuth, R. D.. Fluorobalhimycin - a new chapter in glycopeptide antibiotic research. Angew. Chem. Int. Ed. Engl. 2002, 41, 3383-3385.
63. Weist, S.; Kittel, C.; Bischoff, D.; Bister, B.; Pfeifer, V.; Nicholson, G. J.; Wohlleben, W.; Süßmuth, R. D. Mutasynthesis of glycopeptide antibiotics: Variations of vancomycin's AB-ring amino acid 3,5-dihydroxyphenylglycine. J. Am. Chem. Soc. 2004, 126, 5942-5943.
64. Lin, H.; Walsh, C. T. A chemoenzymatic approach to glycopeptide antibiotics. J. Am. Chem. Soc. 2004, 126, 13998-14003.
65. Oberthur, M.; Leimkuhler, C.; Kruger, R. G.; Lu, W.; Walsh, C. T.; Kahne, D. A systematic investigation of the synthetic utility of glycopeptide glycosyltransferases. J. Am. Chem. Soc. 2005, 127, 10747-10752.
66. Walsh, C.; Freel Meyers, C. L.; Losey, H. C. Antibiotic glycosyltransferases: Antibiotic maturation and prospects for reprogramming. J. Med. Chem. 2003, 46, 3425-3436
67. Fu, X.; Albermann, C.; Jiang, J.; Liao, J.; Zhang, C.; Thorson, J. S. Antibiotic optimization via in vitro glycorandomization. Nat. Biotechnol. 2003, 21, 1467-1469.
68. Losey, H. C.; Jiang, J.; Biggins, J. B.; Oberthur, M.; Ye, X. Y.; Dong, S. D.; Kahne, D.; Thorson, J. S.; Walsh, C. T. Incorporation of glucose analogs by GtfE and GtfD from the vancomycin biosynthetic pathway to generate variant glycopeptides. Chem. Biol. 2002, 9, 1305-1514.
69. Kruger, R. G.; Lu, W.; Oberthur, M.; Tao, J.; Kahne, D.; Walsh, C. T. Tailoring of glycopeptide scaffolds by the acyltransferases from the teicoplanin and A-40,926 biosynthetic operons. Chem. Biol. 2005, 12, 131-140.
70. Zhang, C.; Griffeth, B. R.; Fu, Q.; Albermann, C.; Fu, X.; Lee, I. K.; Li, L.; Thorson, J. S. Exploiting the reversibility of natural product glycosyltransferase-catalyzed reactions. Science 2006, 313, 1291-1294.
71. Lancini, G. Forty years of antibiotic research at Lepetit: A personal journey. SIM News 2006, 56, 192-212.