Peptidoglycan architecture of Gram-positive bacteria by solid-state NMR

Biochimica et Biophysica Acta - Biomembranes

Volumn 1848, Issue 1, 2015, Pages 350-362

  Kim, Sung Joon ^a   Chang, James ^a   Singh, Manmilan ^b  

^a BAYLOR UNIVERSITY   (United States)

^b WASHINGTON UNIVERSITY   (United States)

Author keywords

Architecture; Cell wall; Oritavancin; Peptidoglycan; REDOR; Staphylococcus aureus

Indexed keywords

ORITAVANCIN; PEPTIDOGLYCAN; POLYPEPTIDE ANTIBIOTIC AGENT; ANTIINFECTIVE AGENT;

ALPHA HELIX; ANTIBACTERIAL ACTIVITY; BACTERIAL CELL WALL; BACTERIUM MUTANT; CARBOXY TERMINAL SEQUENCE; CONFORMATIONAL TRANSITION; DRUG MECHANISM; DRUG PROTEIN BINDING; ENTEROCOCCUS FAECIUM; GRAM POSITIVE BACTERIUM; MOLECULAR MODEL; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PEPTIDOGLYCAN BACKBONE CONFORMATION; PEPTIDOGLYCAN BRIDGE LENGTH; PEPTIDOGLYCAN LATTICE STRUCTURE; PROTEIN CONFORMATION; PROTEIN CROSS LINKING; PROTEIN FOLDING; PROTEIN STRUCTURE; PSEUDO TESSERA STRUCTURE; REVIEW; ROTATIONAL ECHO DOUBLE RESONANCE; SOLID STATE NUCLEAR MAGNETIC RESONANCE; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS AUREUS FEM MUTANT; STRUCTURE ANALYSIS; TESSERA STRUCTURE; CELL WALL; CHEMISTRY; CONFORMATION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROCEDURES;

POSIBACTERIA; STAPHYLOCOCCUS AUREUS;

ANTI-BACTERIAL AGENTS; CELL WALL; GRAM-POSITIVE BACTERIA; MAGNETIC RESONANCE SPECTROSCOPY; MOLECULAR CONFORMATION; PEPTIDOGLYCAN; STAPHYLOCOCCUS AUREUS;

EID: 85028780557     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2014.05.031     Document Type: Review

References (56)

1. H.J. Rogers, J.B. Ward, and H.R. Perkins Microbial Cell Walls and Membranes 1980 Chapman and Hall London, New York
2. P. Giesbrecht, T. Kersten, H. Maidhof, and J. Wecke Staphylococcal cell wall: morphogenesis and fatal variations in the presence of penicillin Microbiol. Mol. Biol. Rev. 62 1998 1371 1414
3. W.W. Navarre, and O. Schneewind Surface proteins of Gram-positive bacteria and mechanisms of their targeting to the cell wall envelope Microbiol. Mol. Biol. Rev. 63 1999 174 229
4. 15N REDOR NMR Biochemistry 36 1997 9859 9866
5. S. Bellais, M. Arthur, L. Dubost, J.E. Hugonnet, L. Gutmann, J. van Heijenoort, R. Legrand, J.P. Brouard, L. Rice, and J.L. Mainardi Aslfm, the d-aspartate ligase responsible for the addition of d-aspartic acid onto the peptidoglycan precursor of Enterococcus faecium J. Biol. Chem. 281 2006 11586 11594
6. A.L. Lovering, S.S. Safadi, and N.C. Strynadka Structural perspective of peptidoglycan biosynthesis and assembly Annu. Rev. Biochem. 81 2012 451 478
7. I.G. Boneca, Z.H. Huang, D.A. Gage, and A. Tomasz Characterization of Staphylococcus aureus cell wall glycan strands, evidence for a new beta-N-acetylglucosaminidase activity J. Biol. Chem. 275 2000 9910 9918
8. B. Glauner, and J.V. Holtje Growth pattern of the murein sacculus of Escherichia coli J. Biol. Chem. 265 1990 18988 18996
9. E.J. Hayhurst, L. Kailas, J.K. Hobbs, and S.J. Foster Cell wall peptidoglycan architecture in Bacillus subtilis Proc. Natl. Acad. Sci. U. S. A. 105 2008 14603 14608
10. D. Gally, and A.R. Archibald Cell wall assembly in Staphylococcus aureus: proposed absence of secondary crosslinking reactions J. Gen. Microbiol. 139 1993 1907 1913
11. W. Vollmer, and S.J. Seligman Architecture of peptidoglycan: more data and more models Trends Microbiol. 18 2010 59 66
12. M.S. Gilmore The Enterococci: Pathogenesis, Molecular Biology, and Antibiotic Resistance 2002 ASM Press Washington, D.C.
13. M. Beeby, J.C. Gumbart, B. Roux, and G.J. Jensen Architecture and assembly of the Gram-positive cell wall Mol. Microbiol. 88 2013 664 672
14. L. Gan, S. Chen, and G.J. Jensen Molecular organization of Gram-negative peptidoglycan Proc. Natl. Acad. Sci. U. S. A. 105 2008 18953 18957
15. E.I. Tocheva, J. Lopez-Garrido, H.V. Hughes, J. Fredlund, E. Kuru, M.S. Vannieuwenhze, Y.V. Brun, K. Pogliano, and G.J. Jensen Peptidoglycan transformations during Bacillus subtilis sporulation Mol. Microbiol. 88 9 2013 673 686
16. R.D. Turner, A.F. Hurd, A. Cadby, J.K. Hobbs, and S.J. Foster Cell wall elongation mode in Gram-negative bacteria is determined by peptidoglycan architecture Nat. Commun. 4 2013 1496
17. R.D. Turner, E.C. Ratcliffe, R. Wheeler, R. Golestanian, J.K. Hobbs, and S.J. Foster Peptidoglycan architecture can specify division planes in Staphylococcus aureus Nat. Commun. 1 2010 26
18. R.D. Turner, W. Vollmer, and S.J. Foster Different walls for rods and balls: the diversity of peptidoglycan Mol. Microbiol. 92 5 2014 862 874
19. W. Vollmer, and J.V. Holtje The architecture of the murein (peptidoglycan) in gram-negative bacteria: vertical scaffold or horizontal layer(s)? J. Bacteriol. 186 2004 5978 5987
20. X. Yao, M. Jericho, D. Pink, and T. Beveridge Thickness and elasticity of gram-negative murein sacculi measured by atomic force microscopy J. Bacteriol. 181 1999 6865 6875
21. B.A. Dmitriev, F.V. Toukach, K.J. Schaper, O. Holst, E.T. Rietschel, and S. Ehlers Tertiary structure of bacterial murein: the scaffold model J. Bacteriol. 185 2003 3458 3468
22. T.J. Beveridge Ultrastructure, chemistry, and function of the bacterial wall Int. Rev. Cytol. 72 1981 229 317
23. S.J. Kim, L. Cegelski, D.R. Studelska, R.D. O'Connor, A.K. Mehta, and J. Schaefer Rotational-echo double resonance characterization of vancomycin binding sites in Staphylococcus aureus Biochemistry 41 2002 6967 6977
24. M.V. Kelemen, and H.J. Rogers Three-dimensional molecular models of bacterial cell wall mucopeptides (peptidoglycans) Proc. Natl. Acad. Sci. U. S. A. 68 1971 992 996
25. V. Braun, H. Gnirke, U. Henning, and K. Rehn Model for the structure of the shape-maintaining layer of the Escherichia coli cell envelope J. Bacteriol. 114 1973 1264 1270
26. R.E. Burge, A.G. Fowler, and D.A. Reaveley Structure of the peptidoglycan of bacterial cell walls. I J. Mol. Biol. 117 1977 927 953
27. H. Labischinski, G. Barnickel, H. Bradaczek, and P. Giesbrecht 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 1979 147 155
28. S.O. Meroueh, K.Z. Bencze, D. Hesek, M. Lee, J.F. Fisher, T.L. Stemmler, and S. Mobashery Three-dimensional structure of the bacterial cell wall peptidoglycan Proc. Natl. Acad. Sci. U. S. A. 103 2006 4404 4409
29. S. Sharif, M. Singh, S.J. Kim, and J. Schaefer Staphylococcus aureus peptidoglycan tertiary structure from carbon-13 spin diffusion J. Am. Chem. Soc. 131 2009 7023 7030
30. S. Sharif, S.J. Kim, H. Labischinski, and J. Schaefer Characterization of peptidoglycan in fem-deletion mutants of methicillin-resistant Staphylococcus aureus by solid-state NMR Biochemistry 48 2009 3100 3108
31. T. Gullion, and J. Schaefer Detection of weak heteronuclear dipolar coupling by rotational-echo double-resonance nuclear magnetic resonance Adv. Magn. Opt. Reson. 13 1989 57 83
32. T. Gullion, and J. Schaefer Rotational-echo double-resonance NMR J. Magn. Reson. 81 1989 196 200
33. S.J. Kim, M. Preobrazhenskaya, and J. Schaefer Characterization of Staphylococcus aureus peptidoglycan tertiary structure using glycopeptides as probe by solid-state NMR Interscience Conference on Antimicrobial Agents and Chemotherapy Washington DC 2008 F2 F2073
34. 19F} rotational-echo double resonance Biochemistry 45 2006 5235 5250
35. S.J. Kim, M. Singh, M. Preobrazhenskaya, and J. Schaefer Staphylococcus aureus peptidoglycan stem packing by rotational-echo double resonance NMR spectroscopy Biochemistry 52 2013 3651 3659
36. 15N labeling J. Mol. Biol. 357 2006 1253 1262
37. A.L. Koch The three-for-one model for gram-negative wall growth: a problem and a possible solution FEMS Microbiol. Lett. 162 1998 127 134
38. G.J. Patti, S.J. Kim, and J. Schaefer Characterization of the peptidoglycan of vancomycin-susceptible Enterococcus faecium Biochemistry 47 2008 8378 8385
39. G.J. Patti, S.J. Kim, T.Y. Yu, E. Dietrich, K.S. Tanaka, T.R. Parr Jr., A.R. Far, and J. Schaefer Vancomycin and oritavancin have different modes of action in Enterococcus faecium J. Mol. Biol. 392 2009 1178 1191
40. K.H. Schleifer, and O. Kandler Peptidoglycan types of bacterial cell walls and their taxonomic implications Bacteriol. Rev. 36 1972 407 477
41. S. Sharif, S.J. Kim, H. Labischinski, J. Chen, and J. Schaefer Uniformity of glycyl bridge lengths in the mature cell walls of Fem mutants of methicillin-resistant Staphylococcus aureus J. Bacteriol. 195 2013 1421 1427
42. S.J. Kim, M. Singh, S. Sharif, and J. Schaefer Cross-link formation and peptidoglycan lattice assembly in the FemA mutant of Staphylococcus aureus Biochemistry 53 2014 1420 1427
43. S.J. Kim, M. Singh, and J. Schaefer Oritavancin binds to isolated protoplast membranes but not intact protoplasts of Staphylococcus aureus J. Mol. Biol. 391 2009 414 425
44. A. Grundling, and O. Schneewind Cross-linked peptidoglycan mediates lysostaphin binding to the cell wall envelope of Staphylococcus aureus J. Bacteriol. 188 2006 2463 2472
45. N.E. Allen, D.L. LeTourneau, and J.N. Hobbs Jr. The role of hydrophobic side chains as determinants of antibacterial activity of semisynthetic glycopeptide antibiotics J. Antibiot. 50 1997 677 684
46. D.L. LeTourneau, and N.E. Allen Use of capillary electrophoresis to measure dimerization of glycopeptide antibiotics Anal. Biochem. 246 1997 62 66
47. S.J. Kim, and J. Schaefer Hydrophobic side-chain length determines activity and conformational heterogeneity of a vancomycin derivative bound to the cell wall of Staphylococcus aureus Biochemistry 47 2008 10155 10161
48. S.J. Kim, K.S. Tanaka, E. Dietrich, A. Rafai Far, and J. Schaefer Locations of the hydrophobic side chains of lipoglycopeptides bound to the peptidoglycan of Staphylococcus aureus Biochemistry 52 2013 3405 3414
49. K.C. Nicolaou, R. Hughes, S.Y. Cho, N. Winssinger, H. Labischinski, and R. Endermann Synthesis and biological evaluation of vancomycin dimers with potent activity against vancomycin-resistant bacteria: target-accelerated combinatorial synthesis Chemistry 7 2001 3824 3843
50. L. Cui, H. Murakami, K. Kuwahara-Arai, H. Hanaki, and K. Hiramatsu Contribution of a thickened cell wall and its glutamine nonamidated component to the vancomycin resistance expressed by Staphylococcus aureus Mu50 Antimicrob. Agents Chemother. 44 2000 2276 2285
51. S.J. Kim, S. Matsuoka, G.J. Patti, and J. Schaefer Vancomycin derivative with damaged D-Ala-D-Ala binding cleft binds to cross-linked peptidoglycan in the cell wall of Staphylococcus aureus Biochemistry 47 2008 3822 3831
52. L. Cegelski, S.J. Kim, A.W. Hing, D.R. Studelska, R.D. O'Connor, A.K. Mehta, and J. Schaefer Rotational-echo double resonance characterization of the effects of vancomycin on cell wall synthesis in Staphylococcus aureus Biochemistry 41 2002 13053 13058
53. T. Kern, M. Giffard, S. Hediger, A. Amoroso, C. Giustini, N.K. Bui, B. Joris, C. Bougault, W. Vollmer, and J.P. Simorre Dynamics characterization of fully hydrated bacterial cell walls by solid-state NMR: evidence for cooperative binding of metal ions J. Am. Chem. Soc. 132 2010 10911 10919
54. H. Takahashi, I. Ayala, M. Bardet, G. De Paepe, J.P. Simorre, and S. Hediger Solid-State NMR on bacterial cells: selective cell wall signal enhancement and resolution improvement using dynamic nuclear polarization J. Am. Chem. Soc. 135 2013 5105 5110
55. M. Renault, R. Tommassen-van Boxtel, M.P. Bos, J.A. Post, J. Tommassen, and M. Baldus Cellular solid-state nuclear magnetic resonance spectroscopy Proc. Natl. Acad. Sci. U. S. A. 109 2014 4863 4868
56. G.J. Patti, J. Chen, J. Schaefer, and M.L. Gross Characterization of structural variations in the peptidoglycan of vancomycin-susceptible Enterococcus faecium: understanding glycopeptide-antibiotic binding sites using mass spectrometry J. Am. Soc. Mass Spectrom. 19 2008 1467 1475