Moenomycin resistance mutations in Staphylococcus aureus reduce peptidoglycan chain length and cause aberrant cell division

ACS Chemical Biology

Volumn 9, Issue 2, 2014, Pages 459-467

  Rebets, Yuriy ^a,d   Lupoli, Tania ^a,b   Qiao, Yuan ^a,b   Schirner, Kathrin ^a   Villet, Regis ^c   Hooper, David ^c   Kahne, Daniel ^b   Walker, Suzanne ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b HARVARD UNIVERSITY   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d SAARLAND UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BAMBERMYCIN; GLYCOSYLTRANSFERASE; LYSOSTAPHIN; MOENOMYCIN A; PEPTIDOGLYCAN; PEPTIDOGLYCAN GLYCOSYLTRANSFERASE; POLYMER;

ANIMAL CELL; ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; AUTOLYSIS; BACTERIAL CELL; BACTERIAL MUTATION; BACTERIAL STRAIN; CELL DIVISION; CELL STRUCTURE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME SYNTHESIS; IN VITRO STUDY; MALE; MOUSE; MUTATION RATE; NONHUMAN; POINT MUTATION; POLYMERIZATION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; STAPHYLOCOCCUS AUREUS;

ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; DRUG RESISTANCE, BACTERIAL; HUMANS; MODELS, MOLECULAR; OLIGOSACCHARIDES; PEPTIDOGLYCAN; PEPTIDOGLYCAN GLYCOSYLTRANSFERASE; POINT MUTATION; PROTEIN STRUCTURE, TERTIARY; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS;

EID: 84896729018     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb4006744     Document Type: Article

References (51)

1. Vollmer, W., Blanot, D., and de Pedro, M. A. (2008) Peptidoglycan structure and architecture FEMS Microbiol. Rev. 32, 149-167
2. Sun, S. X. and Jiang, H. (2011) Physics of bacterial morphogenesis Microbiol. Mol. Biol. Rev. 75, 543-565
3. Typas, A., Banzhaf, M., Gross, C. A., and Vollmer, W. (2012) From the regulation of peptidoglycan synthesis to bacterial growth and morphology Nat. Rev. Microbiol. 10, 123-136
4. Sauvage, E., Kerff, F., Terrak, M., Ayala, J. A., and Charlier, P. (2008) The penicillin-binding proteins: structure and role in peptidoglycan biosynthesis FEMS Microbiol. Rev. 32, 234-258
5. Lovering, A. L., Gretes, M., and Strynadka, N. C. J. (2008) Structural details of the glycosyltransferase step of peptidoglycan assembly Curr. Opin. Struct. Biol. 18, 534-543
6. Terrak, M. and Nguyen-Distèche, M. (2006) Kinetic characterization of the monofunctional glycosyltransferase from Staphylococcus aureus J. Bacteriol. 188, 2528-2532
7. Reed, P., Veiga, H., Jorge, A. M., Terrak, M., and Pinho, M. G. (2011) Monofunctional Transglycosylases Are Not Essential for Staphylococcus aureus Cell Wall Synthesis J. Bacteriol. 193, 2549-2556
8. Pinho, M. G., de Lencastre, H., and Tomasz, A. (2001) An acquired and a native penicillin-binding protein cooperate in building the cell wall of drug-resistant staphylococci Proc. Natl. Acad. Sci. U.S.A. 98, 10886-10891
9. Pinho, M. G., Filipe, S. R., de Lencastre, H., and Tomasz, A. (2001) Complementation of the essential peptidoglycan transpeptidase function of penicillin-binding protein 2 (PBP2) by the drug resistance protein PBP2A in Staphylococcus aureus J. Bacteriol. 183, 6525-6531
10. Touhami, A., Jericho, M. H., and Beveridge, T. J. (2004) Atomic force microscopy of cell growth and division in Staphylococcus aureus J. Bacteriol. 186, 3286-3295
11. Turner, R. D., Ratcliffe, E. C., Wheeler, R., Golestanian, R., Hobbs, J. K., and Foster, S. J. (2010) Peptidoglycan architecture can specify division planes in Staphylococcus aureus Nat. Commun. 1, 1-9
12. Dmitriev, B. A., Toukach, F. V., Holst, O., Rietschel, E. T., and Ehlers, S. (2004) Tertiary structure of Staphylococcus aureus cell wall murein J. Bacteriol. 186, 7141-7148
13. van Heijenoort, Y., Derrien, M., and Van Heijenoort, J. (1978) Polymerization by transglycosylation in the biosynthesis of the peptidoglycan of Escherichia coli K 12 and its inhibition by antibiotics FEBS Lett. 89, 141-144
14. van Heijenoort, Y., Leduc, M., Singer, H., and Van Heijenoort, J. (1987) Effects of moenomycin on Escherichia coli J. Gen. Microbiol. 133, 667-674
15. 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
16. Welzel, P. (2005) Syntheses around the transglycosylation step in peptidoglycan biosynthesis Chem. Rev. 105, 4610-4660
17. Ostash, B. and Walker, S. (2010) Moenomycin family antibiotics: chemical synthesis, biosynthesis, and biological activity Nat. Prod. Rep. 27, 1594-1617
18. Perlstein, D. L., Zhang, Y., Wang, T. S., Kahne, D. E., and Walker, S. (2007) The direction of glycan chain elongation by peptidoglycan glycosyltransferases J. Am. Chem. Soc. 129, 12674-12675
19. Lovering, A. L., de Castro, L. H., Lim, D., and Strynadka, N. C. J. (2007) Structural insight into the transglycosylation step of bacterial cell-wall biosynthesis Science 315, 1402-1405
20. 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
21. 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
22. Fuse, S., Tsukamoto, H., Yuan, Y., Wang, T. S. A., Zhang, Y., Bolla, M., Walker, S., Sliz, P., and Kahne, D. (2010) Functional and structural analysis of a key region of the cell wall inhibitor moenomycin ACS Chem. Biol. 5, 701-711
23. Gampe, C. M., Tsukamoto, H., Doud, E. H., Walker, S., and Kahne, D. (2013) Tuning the moenomycin pharmacophore to enable discovery of bacterial cell wall synthesis inhibitors J. Am. Chem. Soc. 135, 3776-3779
24. Welzel, P. (2007) A long research story culminates in the first total synthesis of moenomycin A Angew. Chem., Int. Ed. 46, 4825-4829
25. Salzberg, L. I., Luo, Y., Hachmann, A.-B., Mascher, T., and Helmann, J. D. (2011) The Bacillus subtilis GntR family repressor YtrA responds to cell wall antibiotics J. Bacteriol. 193, 5793-5801
26. Novick, R. P. (1991) Genetic systems in staphylococci Methods Enzymol. 204, 587-636
27. Maloy, S. R., Cronan, J. R., and Freiflder, D. (1994) Microbial Genetics, 2 nd ed., Jones and Bartlett, Boston.
28. Barrett, D., Leimkuhler, C., Chen, L., Walker, D., Kahne, D., and Walker, S. (2005) Kinetic characterization of the glycosyltransferase module of Staphylococcus aureus PBP2 J. Bacteriol. 187, 2215-2217
29. Wang, T. S. A., Lupoli, T. J., Sumida, Y., Tsukamoto, H., Wu, Y., Rebets, Y., Kahne, D. E., and Walker, S. (2011) Primer preactivation of peptidoglycan polymerases J. Am. Chem. Soc. 133, 8528-8530
30. Barrett, D., Wang, T.-S. A., Yuan, Y., Zhang, Y., Kahne, D., and Walker, S. (2007) Analysis of glycan polymers produced by peptidoglycan glycosyltransferases J. Biol. Chem. 282, 31964-31971
31. Wang, T. S. A., Manning, S. A., Walker, S., and Kahne, D. (2008) Isolated peptidoglycan glycosyltransferases from different organisms produce different glycan chain lengths J. Am. Chem. Soc. 130, 14068-14069
32. Bunce, C., Wheeler, L., Reed, G., Musser, J., and Barg, N. (1992) Murine model of cutaneous infection with gram-positive cocci Infect. Immun. 60, 2636-2640
33. Ford, C. W., Hamel, J. C., Stapert, D., and Yancey, R. J. (1989) Establishment of an experimental model of a Staphylococcus aureus abscess in mice by use of dextran and gelatin microcarriers J. Med. Microbiol. 28, 259-266
34. Steele, V. R., Bottomley, A. L., Garcia-Lara, J., Kasturiarachchi, J., and Foster, S. J. (2011) Multiple essential roles for EzrA in cell division of Staphylococcus aureus Mol. Microbiol. 80, 542-555
35. 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
36. Steidl, R., Pearson, S., Stephenson, R. E., Ledala, N., Sitthisak, S., Wilkinson, B. J., and Jayaswal, R. K. (2008) Staphylococcus aureus cell wall stress stimulon gene-lacZ fusion strains: potential for use in screening for cell wall-active antimicrobials Antimicrob. Agents Chemother. 52, 2923-2925
37. Balibar, C. J., Shen, X., McGuire, D., Yu, D., McKenney, D., and Tao, J. (2010) cwrA, a gene that specifically responds to cell wall damage in Staphylococcus aureus Microbiology 156, 1372-1383
38. Tzagoloff, H. and Novick, R. (1977) Geometry of cell division in Staphylococcus aureus J. Bacteriol. 129, 343-350
39. Pinho, M. G. and Errington, J. (2004) Recruitment of penicillin-binding protein PBP2 to the division site of Staphylococcus aureus is dependent on its transpeptidation substrates Mol. Microbiol. 55, 799-807
40. 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
41. 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. 123, 3155-3156
42. Truong-Bolduc, Q. C., Dunman, P. M., Strahilevitz, J., Projan, S. J., and Hooper, D. C. (2005) MgrA is a multiple regulator of two new efflux pumps in Staphylococcus aureus J. Bacteriol. 187, 2395-2405
43. Duthie, E. S. and Lorenz, L. L. (1952) Staphylococcal coagulase; mode of action and antigenicity J. Gen. Microbiol. 6, 95-107
44. Lee, C. Y., Buranen, S. L., and Ye, Z. H. (1991) Construction of single-copy integration vectors for Staphylococcus aureus Gene 103, 101-105
45. Schenk, S. and Laddaga, R. A. (1992) Improved method for electroporation of Staphylococcus aureus FEMS Microbiol. Lett. 73, 133-138
46. Campbell, J., Singh, A. K., Santa Maria, J. P. J., Kim, Y., Brown, S., Swoboda, J. G., Mylonakis, E., Wilkinson, B. J., and Walker, S. (2011) Synthetic lethal compound combinations reveal a fundamental connection between wall teichoic acid and peptidoglycan biosyntheses in Staphylococcus aureus ACS Chem. Biol. 6, 106-116
47. de Jonge, B. L., de Lencastre, H., and Tomasz, A. (1991) Suppression of autolysis and cell wall turnover in heterogeneous Tn551 mutants of a methicillin-resistant Staphylococcus aureus strain J. Bacteriol. 173, 1105-1110
48. Kusuma, C. M. and Kokai-Kun, J. F. (2005) Comparison of four methods for determining lysostaphin susceptibility of various strains of Staphylococcus aureus Antimicrob. Agents Chemother. 49, 3256-3263
49. Bae, T. and Schneewind, O. (2006) Allelic replacement in Staphylococcus aureus with inducible counter-selection Plasmid 55, 58-63
50. Attia, A. S., Benson, M. A., Stauff, D. L., Torres, V. J., and Skaar, E. P. (2010) Membrane damage elicits an immunomodulatory program in Staphylococcus aureus PLoS Pathog. 6, e1000802
51. Rasband, W. S. (1997-2012) ImageJ, U. S. National Institutes of Health, Bethesda, MD; imagej.nih.gov/ij/.