Complete characterization of the seventeen step moenomycin biosynthetic pathway

Biochemistry

Volumn 48, Issue 37, 2009, Pages 8830-8841

  Ostash, Bohdan ^a,c   Doud, Emma H ^a,b   Lin, Cecilie ^a,b   Ostash, Iryna ^a,c   Perlstein, Deborah L ^a   Fuse, Shinichiro ^b,d   Wolpert, Manuel ^a   Kahne, Daniel ^b   Walker, Suzanne ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b HARVARD UNIVERSITY   (United States)

^c IVAN FRANKO NATIONAL UNIVERSITY OF LVIV   (Ukraine)

^d TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE; BACTERIAL CELLS; BIOSYNTHETIC GENE; BIOSYNTHETIC GENE CLUSTER; BIOSYNTHETIC PATHWAY; CHEMOENZYMATIC APPROACHES; CLINICAL USE; GLYCOSYLTRANSFERASES; IN-VITRO; MOLECULAR SCAFFOLDS; NATURAL PRODUCTS; PEPTIDOGLYCANS; POTENT ANTIBIOTIC ACTIVITY;

BIOCHEMISTRY; BIOSYNTHESIS; CELL MEMBRANES; ENZYMES; GENES; SCAFFOLDS;

ANTIBIOTICS;

BAMBERMYCIN; DIMETHYLALLYLTRANSFERASE; MOLECULAR SCAFFOLD;

ANTIMICROBIAL ACTIVITY; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; DRUG SYNTHESIS; GENE FUNCTION; NONHUMAN; PRIORITY JOURNAL;

ANTI-BACTERIAL AGENTS; BAMBERMYCINS; DRUG RESISTANCE, BACTERIAL; GENE DELETION; GENES, BACTERIAL; GLYCOLIPIDS; MULTIGENE FAMILY; PEPTIDOGLYCAN GLYCOSYLTRANSFERASE; PHOSPHOLIPIDS; STREPTOMYCES; STREPTOMYCES LIVIDANS;

BACTERIA (MICROORGANISMS); STREPTOMYCES GHANAENSIS;

EID: 70349088626     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi901018q     Document Type: Article

References (50)

1. Ostash, B., and Walker, S. (2005) Bacterial transglycosylase inhibitors. Curr. Opin. Chem. Biol. 9, 459-466.
2. Goldman, R. C., and Gange, D. (2000) Inhibition of transglycosylation involved in bacterial peptidoglycan synthesis. Curr. Med. Chem. 7, 801-820.
3. Halliday, J., McKeveney, D., Muldoon, C., Rajaratnam, P., and Meutermans, W. (2006) Targeting the forgotten transglycosylases. Biochem. Pharmacol. 71, 957-967.
4. Wright, G. D. (2007) A new target for antibiotic development. Science 315, 1373-1374.
5. Welzel, P. (2005) Syntheses around the transglycosylation step in peptidoglycan biosynthesis. Chem. Rev. 105, 4610-4660.
6. Adachi, M., Zhang, Y., Leimkuhler, C., Sun, B., LaTour, J. V., and Kahne, D. E. (2006) Degradation and reconstruction of moenomycin A and derivatives: dissecting the function of the isoprenoid chain. J. Am. Chem. Soc. 128, 14012-14013. (Pubitemid 44657478)
7. Lovering, A. L., De Castro, L., and Strynadka, N. C. J. (2008) Identification of dynamic structural motifs involved in peptidoglycan glycosyltransfer. J. Mol. Biol. 383, 167-177.
8. Lovering, A. L., de Castro, L. H., Lim, D., and Strynadka, N. C. (2007) Structural insight into the transglycosylation step of bacterial cell-wall biosynthesis. Science 315, 1402-1405. (Pubitemid 46399547)
9. Yuan, Y., Barrett, D., Zhang, Y., Kahne, D., Sliz, P., and Walker, S. (2007) Crystal structure of a peptidoglycan glycosyltransferase suggests a model for processive glycan chain synthesis. Proc. Natl. Acad. Sci. U.S.A. 104, 5348-5353. (Pubitemid 47175683)
10. Yuan, Y., Fuse, S., Ostash, B., Sliz, P., Kahne, D., and Walker, S. (2008) Structural analysis of the contacts anchoring moenomycin to peptidoglycan glycosyltransferases and implications for antibiotic design. ACS Chem. Biol. 3, 429-436.
11. Heaslet, H., Shaw, B., Mistry, A., and Miller, A. A. (2009) Characterization of the active site of S. aureus monofunctional glycosyltransferase (Mtg) by site-directed mutation and structural analysis of the protein complexed with moenomycin. J. Struct. Biol. 167, 129-135.
12. Sung, M. T., Lai, Y. T., Huang, C. Y., Chou, L. Y., Shih, H. W., Cheng, W. C., Wong, C. H., and Ma, C. (2009) Crystal structure of the membrane-bound bifunctional transglycosylase PBP1b from Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 106, 8824-8829.
13. Taylor, J. G., Li, X., Oberthur, M., Zhu, W., and Kahne, D. E. (2006) The total synthesis of moenomycin A. J. Am. Chem. Soc. 128, 15084-15085.
14. Ostash, B., Saghatelian, A., and Walker, S. (2007) A streamlined metabolic pathway for the biosynthesis of moenomycin A. Chem. Biol. 14, 257-267. (Pubitemid 46428142)
15. Flett, F., Mersinias, V., and Smith, C. P. (1997) High efficiency intergeneric conjugal transfer of plasmid DNA from Escherichia coli to methyl DNA-restricting streptomycetes. FEMS Microbiol. Lett. 155, 223-229. (Pubitemid 28248232)
16. Frirdich, E., and Whitfield, C. (2005) Characterization of Gla(KP), a UDP-galacturonic acid C4-epimerase from Klebsiella pneumoniae with extended substrate specificity. J. Bacteriol. 187, 4104-4115. (Pubitemid 40827794)
17. Sekurova, O. N., Brautaset, T., Sletta, H., Borgos, S. E. F., Jakobsen, O. M., Ellingsen, T. E., Strom, A. R., Valla, S., and Zotchev, S. B. (2004) In vivo analysis of the regulatory genes in the nystatin biosynthetic gene cluster of Streptomyces noursei ATCC 11455 reveals their differential control over antibiotic biosynthesis. J. Bacteriol. 186, 1345-1354. (Pubitemid 38248724)
18. 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.
19. BlondeletRouault, M. H., Weiser, J., Lebrihi, A., Branny, P., and Pernodet, J. L. (1997) Antibiotic resistance gene cassettes derived from the Omega interposon for use in E-coli and Streptomyces. Gene 190, 315-317. (Pubitemid 27220139)
20. Kieser, T., Bibb, M. J., Buttner, M. J., Chater, K. F., and Hopwood, D. A. (2000) Practical Streptomyces Genetics, The John Innes Foundation, Norwich, U.K.
21. Sambrook, J., and Russel, D. W. (2001) Molecular Cloning: A Laboratory Manual, 3rd ed., Cold Spring Harbor Laboratory Press, Cold Springs Harbor, NY.
22. Eichhorn, P., and Aga, D. S. (2005) Characterization of moenomycin antibiotics from medicated chicken feed by ion-trap mass spectrometry with electrospray ionization. Rapid Commun. Mass Spectrom. 19, 2179-2186. (Pubitemid 41059876)
23. Zehl, M., Pittenauer, E., Rizzi, A., and Allmaier, G. (2006) Characterization of moenomycin antibiotic complex by multistage MALDI-IT/RTOF-MS and ESI-IT-MS. J. Am. Soc. Mass. Spectrom. 17, 1081-1090. (Pubitemid 44094124)
24. Payandeh, J., Fujihashi, M., Gillon, W., and Pai, E. F. (2006) The crystal structure of (S)-3-O-geranylgeranylglyceryl phosphate synthase reveals an ancient fold for an ancient enzyme. J. Biol. Chem. 281, 6070-6078. (Pubitemid 43847708)
25. Zhang, D. L., and Poulter, C. D. (1993) Biosynthesis of archaebacterial ether lipids: Formation of ether linkages by prenyltransferases. J. Am. Chem. Soc. 115, 1270-1277.
26. Domingo, V., Arteaga, J. F., del Moral, J. F. Q., and Barrero, A. F. (2009) Unusually cyclized triterpenes: occurrence, biosynthesis and chemical synthesis. Nat. Prod. Rep. 26, 115-134.
27. Dewick, P. M. (2002) The biosynthesis of C-5-C-25 terpenoid compounds. Nat. Prod. Rep. 19, 181-222.
28. Liang, P. H., Ko, T. P., and Wang, A. H. J. (2002) Structure, mechanism and function of prenyltransferases. Eur. J. Biochem. 269, 3339-3354.
29. Anantharaman, V., Aravind, L., and Koonin, E. V. (2003) Emergence of diverse biochemical activities in evolutionarily conserved structural scaffolds of proteins. Curr. Opin. Chem. Biol. 7, 12-20. (Pubitemid 36126487)
30. Nagano, N., Orengo, C. A., and Thornton, J. M. (2002) One fold with many functions: The evolutionary relationships between TIM barrel families based on their sequences, structures and functions. J. Mol. Biol. 321, 741-765.
31. Caetano-Anolles, G., Yafremava, L. S., Gee, H., Caetano-Anolles, D., Kim, H. S., and Mittenthal, J. E. (2009) The origin and evolution of modern metabolism. Int. J. Biochem. Cell Biol. 41, 285-297.
32. Wierenga, R. K. (2001) The TIM-barrel fold: a versatile framework for efficient enzymes. FEBS Lett. 492, 193-198.
33. Neundorf, I., Kohler, C., Hennig, L., Findeisen, M., Arigoni, D., and Welzel, P. (2003) Evidence for the combined participation of a C-10 and a C-15 precursor in the biosynthesis of moenocinol, the lipid part of the moenomycin antibiotics. ChemBioChem 4, 1201-1205. (Pubitemid 37462822)
34. Hu, Y. D., and Floss, H. G. (2004) Further studies on the biosynthesis of the manumycin-type antibiotic, asukamycin, and the chemical synthesis of protoasukamycin. J. Am. Chem. Soc. 126, 3837-3844.
35. Cho, H., Beale, J. M., Graff, C., Mocek, U., Nakagawa, A., Omura, S., and Floss, H. G. (1993) Studies on the biosynthesis of the antibiotic reductiomycin in Streptomyces xanthochromogenus. J. Am. Chem. Soc. 115, 12296-12304. (Pubitemid 24077502)
36. 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. (Pubitemid 40586306)
37. Petricek, M., Petrickova, K., Havlicek, L., and Felsberg, J. (2006) Occurrence of two 5-aminolevulinate biosynthetic pathways in Streptomyces nodosus subsp asukaensis is linked with the production of asukamycin. J. Bacteriol. 188, 5113-5123. (Pubitemid 44051477)
38. Schuricht, U., Endler, K., Hennig, L., Findeisen, M., and Welzel, P. (2000) Studies on the biosynthesis of the antibiotic moenomycin A. J. Prakt. Chem. 342, 761-772.
39. Woodyer, R. D., Li, G. Y., Zhao, H. M., and van der Donk, W. A. (2007) New insight into the mechanism of methyl transfer during the biosynthesis of fosfomycin. Chem. Commun. 359-361.
40. Kudo, F., Kasama, Y., Hirayama, T., and Eguchi, T. (2007) Cloning of the pactamycin biosynthetic gene cluster and characterization of a crucial glycosyltransferase prior to a unique cyclopentane ring formation. J. Antibiot. 60, 492-503.
41. Unwin, J., Standage, S., Alexander, D., Hosted, T., Horan, A. C., and Wellington, E. M. H. (2004) Gene cluster in Micromonospora echinospora ATCC15835 for the biosynthesis of the gentamicin C complex. J. Antibiot. 57, 436-445. (Pubitemid 39162300)
42. Nunez, L. E., Mendez, C., Brana, A. F., Blanco, G., and Salas, J. A. (2003) The biosynthetic gene cluster for the beta-lactam carbapenem thienamycin in Streptomyces cattleya. Chem. Biol. 10, 301-311. (Pubitemid 36516648)
43. Kuzuyama, T., Seki, T., Dairi, T., Hidaka, T., and Seto, H. (1995) Nucleotide-sequence of fortimicin Kl1 methyltransferase gene isolated from Micromonospora olivasterospora, and comparison of its deduced amino-acid-sequence with those of methyltransferases involved in the biosynthesis of bialaphos and fosfomycin. J. Antibiot. 48, 1191-1193.
44. Hidaka, T., Hidaka, M., Kuzuyama, T., and Seto, H. (1995) Sequence of a P-methyltransferase-encoding gene isolated from a bialaphos-producing Streptomyces hygroscopius. Gene 158, 149-150.
45. Kuzuyama, T., Hidaka, T., Kamigiri, K., Imai, S., and Seto, H. (1992) Studies on the biosynthesis of fosfomycin. 4. The biosynthetic origin of the methyl-group of fosfomycin. J. Antibiot. 45, 1812-1814.
46. El-Abadla, N., Lampilas, M., Hennig, L., Findeisen, M., Welzel, P., Muller, D., Markus, A., and van Heijenoort, J. (1999) Moenomycin A: The role of the methyl group in the moenuronamide unit and a general discussion of structure-activity relationships. Tetrahedron 55, 699-722. (Pubitemid 29023317)
47. Welzel, P., Kunisch, F., Kruggel, F., Stein, H., Scherkenbeck, J., Hiltmann, A., Duddeck, H., Muller, D., Maggio, J. E., Fehlhaber, H. W., Seibert, G., Vanheijenoort, Y., and Vanheijenoort, J. (1987) Moenomycin-A: Minimum structural requirements for biological-activity. Tetrahedron 43, 585-598.
48. Ritzeler, O., Hennig, L., Findeisen, M., Welzel, P., and Muller, D. (1997) Search for new moenomycin structure-activity relationships. Synthesis of a trisaccharide precursor of a moenomycin analogue. Tetrahedron 53, 5357-5357
49. Hennig, L., Findeisen, M., Welzel, P., and Haessner, R. (1998) H-1 NMR spectroscopic studies of the moenomycins. Magn. Reson. Chem. 36, 615-620. (Pubitemid 128112291)
50. Donnerstag, A., Hennig, L., Findeisen, M., Welzel, P., and Haessner, R. (1996) H-1 NMR as a tool for the structure elucidation of moenomycin antibiotics. Magn. Reson. Chem. 34, 1031-1035. (Pubitemid 126324848)