Staphylococcus aureus peptidoglycan stem packing by rotational-echo double resonance NMR spectroscopy

Biochemistry

Volumn 52, Issue 21, 2013, Pages 3651-3659

  Kim, Sung Joon ^a   Singh, Manmilan ^b   Preobrazhenskaya, Maria ^c   Schaefer, Jacob ^b  

^a BAYLOR UNIVERSITY   (United States)

^b WASHINGTON UNIVERSITY   (United States)

^c GAUSE INSTITUTE OF NEW ANTIBIOTICS   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

AVERAGE DISTANCE; INTERNUCLEAR DISTANCES; NEAREST-NEIGHBORS; PEPTIDOGLYCANS; ROTATIONAL ECHO DOUBLE RESONANCE; STAPHYLOCOCCUS AUREUS; STRUCTURAL MOTIFS; TERTIARY STRUCTURES;

BACTERIA; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PEPTIDES;

AMINO ACIDS;

ALANINE; CARBON 13; NITROGEN 15; PEPTIDOGLYCAN;

ARTICLE; BACTERIAL CELL; BINDING AFFINITY; CONTROLLED STUDY; ISOTOPE LABELING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN MOTIF; PROTEIN TERTIARY STRUCTURE; ROTATIONAL ECHO DOUBLE RESONANCE NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; STAPHYLOCOCCUS AUREUS;

CELL DIVISION; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PEPTIDOGLYCAN; STAPHYLOCOCCUS AUREUS;

STAPHYLOCOCCUS AUREUS;

EID: 84878327682     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi4005039     Document Type: Article

References (36)

1. Rogers, H. J., Ward, J. B., and Perkins, H. R. (1980) Microbial Cell Walls and Membranes, Chapman and Hall, London.
2. van Heijenoort, J. (2001) Formation of the glycan chains in the synthesis of bacterial peptidoglycan Glycobiology 11, 25R-36R
3. Gan, L., Chen, S., and Jensen, G. J. (2008) Molecular organization of Gram-negative peptidoglycan Proc. Natl. Acad. Sci. U. S. A. 105, 18953-18957
4. Turner, R. D., Hurd, A. F., Cadby, A., Hobbs, J. K., and Foster, S. J. (2013) Cell wall elongation mode in Gram-negative bacteria is determined by peptidoglycan architecture Nat. Commun. 4, 1496
5. Dmitriev, B. A., Toukach, F. V., Schaper, K. J., Holst, O., Rietschel, E. T., and Ehlers, S. (2003) Tertiary structure of bacterial murein: the scaffold model J. Bacteriol. 185, 3458-3468
6. Hayhurst, E. J., Kailas, L., Hobbs, J. K., and Foster, S. J. (2008) Cell wall peptidoglycan architecture in Bacillus subtilis Proc. Natl. Acad. Sci. U. S. A. 105, 14603-14608
7. Turner, R. D., Ratcliffe, E. C., Wheeler, R., Golestanian, R., Hobbs, J. K., and Foster, S. J. (2013) Peptidoglycan architecture can specify division planes in Staphylococcus aureus Nat. Commun. 1, 26
8. Tocheva, E. I., Lopez-Garrido, J., Hughes, H. V., Fredlund, J., Kuru, E., Vannieuwenhze, M. S., Brun, Y. V., Pogliano, K., and Jensen, G. J. (2013) Peptidoglycan transformations during Bacillus subtilis sporulation Mol. Microbiol. 10.1111/mmi.12201
9. Kelemen, M. V. and Rogers, H. J. (1971) Three-dimensional molecular models of bacterial cell wall mucopeptides (peptidoglycans) Proc. Natl. Acad. Sci. U. S. A. 68, 992-996
10. Braun, V., Gnirke, H., Henning, U., and Rehn, K. (1973) Model for the structure of the shape-maintaining layer of the Escherichia coli cell envelope J. Bacteriol. 114, 1264-1270
11. Burge, R. E., Fowler, A. G., and Reaveley, D. A. (1977) Structure of the peptidogylcan of bacterial cell walls. I J. Mol. Biol. 117, 927-953
12. Labischinski, H., Barnickel, G., Bradaczek, H., and Giesbrecht, P. (1979) On the secondary and tertiary structure of murein. Low and medium-angle X-ray evidence against chitin-based conformations of bacterial peptidoglycan Eur. J. Biochem. 95, 147-155
13. Meroueh, S. O., Bencze, K. Z., Hesek, D., Lee, M., Fisher, J. F., Stemmler, T. L., and Mobashery, S. (2006) Three-dimensional structure of the bacterial cell wall peptidoglycan Proc. Natl. Acad. Sci. U. S. A. 103, 4404-4409
14. Sharif, S., Kim, S. J., and Schaefer, J. (2009) Staphylococcus aureus peptidoglycan tertiary structure from carbon-13 spin diffusion J. Am. Chem. Soc. 131, 7023-7030
15. Kim, S. J. and Schaefer, J. (2008) Hydrophobic side-chain length determines activity and conformational heterogeneity of a vancomycin derivative bound to the cell wall of Staphylococcus aureus Biochemistry 47, 10155-10161
16. Giesbrecht, P., Kersten, T., Maidhof, H., and Wecke, J. (1998) Staphylococcal cell wall: morphogenesis and fatal variations in the presence of penicillin Microbiol. Mol. Biol. Rev. 62, 1371-1414
17. Kim, S. J., Matsuoka, S., Patti, G. J., and Schaefer, J. (2008) Vancomycin derivative with damaged D-Ala-D-Ala binding cleft binds to cross-linked peptidoglycan in the cell wall of Staphylococcus aureus Biochemistry 47, 3822-3831
18. Toke, O., Maloy, W. L., Kim, S. J., Blazyk, J., and Schaefer, J. (2004) Secondary Structure and Lipid Contact of a Peptide Antibiotic in Phospholipid Bilayers by REDOR Biophys. J. 87, 662-674
19. Gullion, T. and Schaefer, J. (1989) Rotational-echo double-resonance NMR J. Magn. Reson. 81, 196-200
20. 19F} Rotational-Echo Double-Resonance NMR J. Polym. Sci., Part B: Polym. Phys. 44, 2760-2775
21. Gullion, T., Baker, D. B., and Conradi, M. S. (1990) New, compensated Carr-Purcell sequences J. Magn. Reson. 89, 479-484
22. Mueller, K. T., Jarvie, T. P., Aurentz, D. J., and Roberts, B. W. (1995) The REDOR transform: direct calculation of internuclear couplings from dipolar-dephasing NMR data Chem. Phys. Lett. 242, 535-542
23. de la Caillerie, J.-B. d. E. and Fretigny, C. (1998) Analysis of the REDOR signal and inversion J. Magn. Reson. 133, 273-280
24. O'Connor, R. D. and Schaefer, J. (2002) Relative CSA-dipolar orientation from REDOR sidebands J. Magn. Reson. 154, 46-52
25. 15N labeling J. Mol. Biol. 357, 1253-1262
26. Kim, S. J., Cegelski, L., Studelska, D. R., O'Connor, R. D., Mehta, A. K., and Schaefer, J. (2002) Rotational-echo double resonance characterization of vancomycin binding sites in Staphylococcus aureus Biochemistry 41, 6967-6977
27. Kim, S. J., Cegelski, L., Stueber, D., Singh, M., Dietrich, E., Tanaka, K. S., Parr, T. R., Far, A. R., and Schaefer, J. (2008) Oritavancin exhibits dual mode of action to inhibit cell-wall biosynthesis in Staphylococcus aureus J. Mol. Biol. 377, 281-293
28. Sharif, S., Kim, S. J., Labischinski, H., and Schaefer, J. (2009) Characterization of peptidoglycan in fem-deletion mutants of methicillin-resistant Staphylococcus aureus by solid-state NMR Biochemistry 48, 3100-3108
29. Rohrer, S., Ehlert, K., Tschierske, M., Labischinski, H., and Berger-Bachi, B. (1999) The essential Staphylococcus aureus gene fmhB is involved in the first step of peptidoglycan pentaglycine interpeptide formation Proc. Natl. Acad. Sci. U. S. A. 96, 9351-9356
30. Snowden, M. A. and Perkins, H. R. (1990) Peptidoglycan cross-linking in Staphylococcus aureus. An apparent random polymerization process Eur. J. Biochem. 191, 373-377
31. Sharif, S., Singh, M., Kim, S. J., and Schaefer, J. (2009) Staphylococcus aureus peptidoglycan tertiary structure from carbon-13 spin diffusion J. Am. Chem. Soc. 131, 7023-7030
32. 19F} rotational-echo double resonance Biochemistry 45, 5235-5250
33. Koch, A. L. (1998) The three-for-one model for gram-negative wall growth: a problem and a possible solution FEMS Microbiol. Lett. 162, 127-134
34. Vollmer, W. and Seligman, S. J. (2010) Architecture of peptidoglycan: more data and more models Trends Microbiol. 18, 59-66
35. Boneca, I. G., Huang, Z. H., Gage, D. A., and Tomasz, A. (2000) Characterization of Staphylococcus aureus cell wall glycan strands, evidence for a new beta-N-acetylglucosaminidase activity J. Biol. Chem. 275, 9910-9918
36. Vollmer, W. and Holtje, J. V. (2004) The architecture of the murein (peptidoglycan) in gram-negative bacteria: vertical scaffold or horizontal layer(s)? J. Bacteriol. 186, 5978-5987