Expression and characterization of the isolated glycosyltransferase module of Escherichia coli PBP1b

Biochemistry

Volumn 43, Issue 38, 2004, Pages 12375-12381

  Barrett, Dianah S ^a   Chen, Lan ^a   Litterman, Nadia K ^a   Walker, Suzanne ^a  

^a PRINCETON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTICS; BIOCHEMISTRY; BIOSYNTHESIS; CATALYSIS; ESCHERICHIA COLI; MOLECULAR WEIGHT;

HIGH MOLECULAR WEIGHT (HMW); PENCILLIN-BINDING PROTEINS (PBP);

ENZYMES;

ANTIBIOTIC AGENT; GAMMA GLUTAMYLTRANSFERASE; GLYCOSYLTRANSFERASE; PENICILLIN BINDING PROTEIN; PEPTIDOGLYCAN;

ARTICLE; BIOSYNTHESIS; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CONTROLLED STUDY; DRUG DESIGN; DRUG TARGETING; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME LOCALIZATION; ENZYME MECHANISM; ENZYME STRUCTURE; ESCHERICHIA COLI; GENE OVEREXPRESSION; MOLECULAR WEIGHT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

BACTERIAL PROTEINS; CARRIER PROTEINS; CATALYSIS; DETERGENTS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GLYCOSYLTRANSFERASES; HEXOSYLTRANSFERASES; KINETICS; METALS; MOLECULAR STRUCTURE; MURAMOYLPENTAPEPTIDE CARBOXYPEPTIDASE; PENICILLIN-BINDING PROTEINS; PEPTIDOGLYCAN GLYCOSYLTRANSFERASE; PEPTIDYL TRANSFERASES; PROTEIN STRUCTURE, SECONDARY; SEQUENCE DELETION; SERINE-TYPE D-ALA-D-ALA CARBOXYPEPTIDASE;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; NEGIBACTERIA;

EID: 4644316620     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi049142m     Document Type: Article

References (44)

1. Rogers, H. J., Perkins, H. R., and Ward, J. B. (1980) in Microbial Cell Walls and Membranes (Rogers, H. J., Ed.) pp 239-297, Chapman and Hall, London, U.K.
2. Walsh, C. T. (2003) Antibiotics: Action, Origins, Resistance, ASM Press, Washington D.C.
3. Zoeiby, A. E., Sanschagrin, F., and Levesque, R. C. (2003) Structure and function of the Mur enzymes: Development of novel inhibitors, Mol. Microbiol. 47, 1-12.
4. van Heijenoort, J. (2001) Recent advances in the formation of the bacterial peptidoglycan monomer unit, Nat. Prod. Rep. 18, 503-519.
5. Suzuki, H., Nishimura, Y., and Hirota, Y. (1978) On the process of cellular division in Eschericia coli: A series of mutants of E. coli altered in the penicillin-binding proteins, Proc. Natl. Acad. Sci. U.S.A. 75, 664-668.
6. Tamaki, S., Nakajima, S., and Matsuhashi, M. (1977) Thermosensitive mutation in Eschericia coli simultaneously causing defects in penicillin-binding protein-1Bs and in enzyme activity for peptidoglycan synthesis in vitro, Proc. Natl. Acad. Sci. U.S.A. 74, 5472-5476.
7. Goffin, C., and Ghuysen, J.-M. (1998) Multimodular penicillin-binding proteins: An enigmatic family of orthologs and paralogs, Microbiol. Mol. Biol. Rev. 62, 1079-1093.
8. Adam, M., Fraipont, C., Rhazi, N., Nguyen-Disteche, M., Lakaye, B., Frere, J. M., Devreese, B., Van Beeumen, J., van Heijenoort, Y., van Heijenoort, J., and Ghuysen, J. M. (1997) The bimodular G57-V577 polypeptide chain of the class B penicillin-binding protein 3 of Escherichia coli catalyzes peptide bond formation from thiolesters and does not catalyze glycan chain polymerization from the lipid II intermediate, J. Bacteriol. 179, 6005-6009.
9. Popham, D. L., and Young, K. D. (2003) Role of penicillin-binding proteins in bacterial cell morphogenesis, Curr. Opin. Microbiol. 6, 594-599.
10. Di Berardino, M., Dijkstra, A., Stuber, D., Keck, W., and Gubler, M. (1996) The monofunctional glycosyltransferase of Escherichia coli is a member of a new class of peptidoglycan-synthesising enzymes, FEBS Lett. 392, 184-188.
11. Paik, J., Jendrossek, D., and Hakenbeck, R. (1997) A putative monofunctional glycosyltransferase is expressed in Ralstonia eutropha, J. Bacteriol. 179, 4061-4065.
12. Wang, Q. M., Peery, R. B., Johnson, R. B., Alborn, W. E., Yeh, W.-K., and Skatrud, P. L. (2001) Identification and characterization of a monofunctional glycosyltransferase from Staphylococcus aureus, J. Bacteriol. 183, 4779-4785.
13. Schonbrunn, E., Sack, S., Eschenburg, S., Perrakis, A., Krekel, F., Amrhein, N., and Mandelkow, E. (1996) Crystal structure of UDP-N- acetylglucosamine enolpyruvyltransferase, the target of the antibiotic fosfomycin, Structure 4, 1065-1075.
14. Benson, T. E., Harris, M. S., Choi, G. H., Cialdella, J. I., Herberg, J. T., Martin, J. P., Jr., and Baldwin, E. T. (2001) A structural variation for MurB: X-ray crystal structure of Staphylococcus aureus UDP-N- acetylenolpyruvylglucosamine reductase (MurB), Biochemistry 40, 2340-2350.
15. Mol, C. D., Brooun, A., Dougan, D. R., Hilgers, M. T., Tari, L. W., Wijnands, R. A., Knuth, M. W., McRee, D. E., and Swanson, R. V. (2003) Crystal structures of active fully assembled substrate- and product-bound complexes of UDP-N-acetylmuramic acid: L-alanine ligase (MurC) from Haemophilus influenzae, J. Bacteriol. 185, 4152-4162.
16. Bertrand, J. A., Auger, G., Fanchon, E., Martin, L., Blanot, D., van Heijenoort, J., and Dideberg, O. (1997) Crystal structure of UDP-N-acetylmuramoyl-L-alanine:D-glutamate ligase from Escherichia coli, EMBO J. 16, 3416-3425.
17. Gordon, E. J., Flouret, B., Chantalat, L., van Heijenoort, J., Mengin-Lecreulx, D., and Dideberg, O. (2001) Crystal structure of UDP-N-acetylmuramoyl-L-alanyl-D-glutamate:meso-diaminopimelate ligase from Escherichia coli, EMBO J. 276, 10999-11006.
18. Yan, Y., Munshi, S., Leiting, B., Anderson, M. S., Chrzas, J., and Chen, Z. (2000) Crystal structure of Escherichia coli UDPMurNAc-tripeptide D-alanyl-D-alanine-adding enzyme (MurF) at 2.3 Å resolution, J. Mol. Biol. 304, 435-445.
19. Ha, S., Walker, D., Shi, Y., and Walker, S. (2000) The 1.9 Å crystal structure of Escherichia coli MurG, a membrane-associated glycosyltransferase involved in peptidoglycan biosynthesis, Protein Sci. 9, 1045-1052.
20. Fonze, E., Vermeire, M., Nguyen-Disteche, M., Brasseur, R., and Charlier, P. (1999) The crystal structure of a penicilloyl-serine transferase of intermediate penicillin sensitivity. The DD-transpeptidase of Streptomyces K15, J. Biol. Chem. 274, 21853-21860.
21. Kelly, J. A., Knox, J. R., Moews, P. C., Hite, G. J., Bartolone, J. B., Zhao, H., Joris, B., Frere, J. M., and Ghuysen, J. M. (1985) 2.8-Å Structure of penicillin-sensitive D-alanyl carboxypeptidase-transpeptidase from Streptomyces R61 and complexes with β-lactams, J. Biol. Chem. 260, 6449-6458.
22. Davies, C., White, S. W., and Nicholas, R. A. (2001) Crystal structure of a deacylation-defective mutant of penicillin-binding protein 5 at 2.3-Å resolution, J. Biol. Chem. 276, 616-623.
23. Deka, R. K., Machius, M., Norgard, M. V., and Tomchick, D. R. (2002) Crystal structure of the 47-kDa lipoprotein of Treponema pallidum reveals a novel penicillin-binding protein, J. Biol. Chem. 277, 41857-41864.
24. Bompard-Gilles, C., Remaut, H., Villeret, V., Prange, T., Fanuel, L., Delmarcelle, M., Joris, B., Frere, J., and Van Beeumen, J. (2000) Crystal structure of a D-aminopeptidase from Ochrobactrum anthropi, a new member of the "penicillin-recognizing enzyme" family, Structure 8, 971-980.
25. Pares, S., Mouz, N., Petillot, Y., Hakenbeck, R., and Dideberg, O. (1996) X-ray structure of Streptococcus pneumoniae PBP2x, a primary penicillin target enzyme, Nat. Struct. Biol. 3, 284-289.
26. Charlier, P., Buisson, G., Dideberg, O., Wierenga, J., Keck, W., Laible, G., and Hakenbeck, R. (1993) Crystallization of a genetically engineered water-soluble primary penicillin target enzyme. The high molecular mass PBP2x of Streptococcus pneumoniae, J. Mol. Biol. 232, 1007-1009.
27. Dessen, A., Mouz, N., Gordon, E., Hopkins, J., and Dideberg, O. (2001) Crystal structure of PBP2x from a highly penicillin-resistant Streptococcus pneumoniae clinical isolate: A mosaic framework containing 83 mutations, J. Biol. Chem. 276, 45106-45112.
28. Lim, D., and Strynadka, N. C. (2002) Structural basis for the β-lactam resistance of PBP2a from methicillin-resistant Staphylococcus aureus, Nat. Struct. Biol. 9, 870-876.
29. Bouhss, A., Mengin-Lecreulx, D., Le Beller, D., and van Heijenoort, J. (1999) Topological analysis of the MraY protein catalysing the first membrane step of peptidoglycan synthesis, Mol. Microbiol. 34, 576-585.
30. Ye, X.-Y., Lo, M.-C., Brunner, L., Walker, D., Kahne, D., and Walker, S. (2001) Better substrates for bacterial transglycosylases, J. Am. Chem. Soc. 125, 8736-8737.
31. Schwartz, B., Markwalder, J. A., and Wang, Y. (2001) Lipid II: Total synthesis of the bacterial cell wall precursor and utilization as a substrate for glycosyltransfer and transpeptidation by penicillin binding protein (PBP) 1b of Eschericia coli, J. Am. Chem. Soc. 123, 11638-11643.
32. VanNieuwenhze, M. S., Mauldin, S. C., Zia-Ebrahimi, M., Winger, B. E., Hornback, W. J., Saha, S. L., Aikins, J. A., and Blaszczak, L. C. (2002) The first total synthesis of lipid II: The final monomeric intermediate in bacterial cell wall biosynthesis, J. Am. Chem. Soc. 124, 3656-3660.
33. Breukink, E., van Heusden, H. E., Vollmerhaus, P. J., Swiezewska, E., Brunner, L., Walker, S., Heck, A. J., and de Kruijff, B. (2003) Lipid II is an intrinsic component of the pore induced by nisin in bacterial membranes, J. Biol. Chem. 278, 19898-19903.
34. Terrak, M., Ghosh, T. K., van Heijenoort, J., Beeumen, J. V., Lampilas, M., Aszodi, J., Ayala, J. A., Ghuysen, J.-M., and Nguyen-Distèche, M. (1999) The catalytic, glycosyl transferase and acyl transferase modules of the cell wall peptidoglycan-polymerizing penicillin-binding protein 1b of Escherichia coli, Mol. Microbiol. 34, 350-364.
35. Chen, L., Walker, D., Sun, B., Hu, Y., Walker, S., and Kahne, D. (2003) Vancomycin analogues active against vanA-resistant strains inhibit bacterial transglycosylase without binding substrate, Proc. Natl. Acad. Sci. U.S.A. 100, 5658-5663.
36. Lefevre, F., Remy, M. H., and Masson, J. M. (1997) Topographical and functional investigation of Escherichia coli penicillin-binding protein 1 b by alanine stretch scanning mutagenesis, J. Bacteriol. 179, 4761-4767.
37. Zijderveld, C., Waisfisz, Q., Aarsman, M., and Nanninga, N. (1995) Hybrid proteins of the transglycosylase and the transpeptidase domains of PBP1B and PBP3 of Escherichia coli, J. Bacteriol. 177, 6290-6293.
38. Schwartz, B., Markwalder, J. A., Seitz, S. P., Wang, Y., and Stein, R. L. (2002) A kinetic characterization of the glycosyltransferase activity of Eschericia coli PBP1b and development of a continuous fluorescence assay, Biochemistry 41, 12552-12561.
39. Nakagawa, J., Tamaki, S., Tomioka, S., and Matsuhashi, M. (1984) Functional biosynthesis of cell wall peptidoglycan by polymorphic bifunctional polypeptides. Penicillin-binding protein 1Bs of Escherichia coli with activities of transglycosylase and transpeptidase, J. Biol. Chem. 259, 13937-13946.
40. Unligil, U. M., and Rini, J. M. (2000) Glycosyltransferase structure and mechanism, Curr. Opin. Struct. Biol. 10, 510-517.
41. 2+ between the periplasm and the cytosol of Escherichia coli, Cell Calcium 32, 183-192.
42. van Asselt, E. J., and Dijkstra, B. W. (1999) Binding of calcium in the EF-hand of Escherichia coli lytic transglycosylase Slt35 is important for stability, FEBS Lett. 458, 429-435.
43. Anderson, J. S., Meadow, P. M., Haskin, M. A., and Strominger, J. L. (1966) Biosynthesis of the peptidoglycan of bacterial cell walls. I. Utilization of uridine diphosphate acetylmuramyl pentapeptide and uridine diphosphate acetylglucosamine for peptidoglycan synthesis by particulate enzymes from Staphylococcus aureus and Micrococcus lysodeikticus, Arch. Biochem. Biophys. 116, 487-515.
44. Wang, C. C., Schultz, D. E., and Nicholas, R. A. (1996) Localization of a putative second membrane association site in penicillin-binding protein 1B of Escherichia coli, Biochem. J. 316, 149-156.