Oritavancin Binds to Isolated Protoplast Membranes but not Intact Protoplasts of Staphylococcus aureus

Journal of Molecular Biology

Volumn 391, Issue 2, 2009, Pages 414-425

  Kim, Sung Joon ^a   Singh, Manmilan ^a   Schaefer, Jacob ^a  

^a WASHINGTON UNIVERSITY   (United States)

Author keywords

bacterial cell wall; glycopeptide antibiotic; rotational echo double resonance; solid state NMR; transglycosylase

Indexed keywords

CARBON 13; EREMOMYCIN; FLUORINE; GLYCINE; LYSINE; NITROGEN 15; ORITAVANCIN; PEPTIDOGLYCAN; PHOSPHORUS 31; POLYPEPTIDE ANTIBIOTIC AGENT; SUCROSE; VANCOMYCIN;

ARTICLE; BACTERIAL CELL WALL; DRUG STRUCTURE; HYDROPHOBICITY; MEMBRANE BINDING; MEMBRANE STABILIZATION; NONHUMAN; PHOSPHOLIPID BILAYER; PRIORITY JOURNAL; PROTOPLAST; STAPHYLOCOCCUS AUREUS; WHOLE CELL;

BACTERIA (MICROORGANISMS); STAPHYLOCOCCUS AUREUS;

EID: 67650692249     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2009.06.033     Document Type: Article

References (41)

1. van Heijenoort J. Formation of the glycan chains in the synthesis of bacterial peptidoglycan. Glycobiology 11 (2001) 25R-36R
2. Rogers H.J., Ward J.B., and Perkins H.R. Microbial Cell Walls and Membranes (1980), Chapman and Hall, London, UK
3. Cegelski L., Kim S.J., Hing A.W., Studelska D.R., O'Connor R.D., Mehta A.K., and Schaefer J. Rotational-echo double resonance characterization of the effects of vancomycin on cell wall synthesis in Staphylococcus aureus. Biochemistry 41 (2002) 13053-13058
4. Cooper R.D., Snyder N.J., Zweifel M.J., Staszak M.A., Wilkie S.C., Nicas T.I., et al. Reductive alkylation of glycopeptide antibiotics: synthesis and antibacterial activity. J. Antibiot. 49 (1996) 575-581
5. Allen N.E., LeTourneau D.L., and Hobbs Jr. J.N. The role of hydrophobic side chains as determinants of antibacterial activity of semisynthetic glycopeptide antibiotics. J. Antibiot. 50 (1997) 677-684
6. Sharman G.J., Try A.C., Dancer R.J., Cho Y.R., Staroske T., Bardsley B., et al. The roles of dimerization and membrane anchoring in activity of glycopeptide antibiotics against vancomycin-resistant bacteria. J. Am. Chem. Soc. 119 (1997) 12041-12047
7. Cooper M.A., and Williams D.H. Binding of glycopeptide antibiotics to a model of a vancomycin-resistant bacterium. Chem. Biol. 6 (1999) 891-899
8. Rao J., Yan L., Lahiri J., Whitesides G.M., Weis R.M., and Warren H.S. Binding of a dimeric derivative of vancomycin to l-Lys-D-Ala-d-lactate in solution and at a surface. Chem. Biol. 6 (1999) 353-359
9. Beauregard D.A., Williams D.H., Gwynn M.N., and Knowles D.J. Dimerization and membrane anchors in extracellular targeting of vancomycin group antibiotics. Antimicrob. Agents Chemother. 39 (1995) 781-785
10. Kim S.J., Cegelski L., Studelska D.R., O'Connor R.D., Mehta A.K., and Schaefer J. Rotational-echo double resonance characterization of vancomycin binding sites in Staphylococcus aureus. Biochemistry 41 (2002) 6967-6977
11. 19F} rotational-echo double resonance. Biochemistry 45 (2006) 5235-5250
12. Grundling A., Missiakas D.M., and Schneewind O. Staphylococcus aureus mutants with increased lysostaphin resistance. J. Bacteriol. 188 (2006) 6286-6297
13. Beining P.R., Huff E., Prescott B., and Theodore T.S. Characterization of the lipids of mesosomal vesicles and plasma membranes from Staphylococcus aureus. J. Bacteriol. 121 (1975) 137-143
14. Theodore T.S., and Weinbach E.C. Respiratory activities associated with mesosomal vesicles and protoplast membranes of Staphylococcus aureus. J. Bacteriol. 120 (1974) 562-564
15. Popkin T.J., Theodore T.S., and Cole R.M. Electron microscopy during release and purification of mesosomal vesicles and protoplast membranes from Staphylococcus aureus. J. Bacteriol. 107 (1971) 907-917
16. Theodore T.S., and Panos C. Protein and fatty acid composition of mesosomal vesicles and plasma membranes of Staphylococcus aureus. J. Bacteriol. 116 (1973) 571-576
17. Huber T.W., and Schuhardt V.T. Lysostaphin-induced, osmotically fragile Staphylococcus aureus cells. J. Bacteriol. 103 (1970) 116-119
18. Reynolds P.E. Peptidoglycan synthesis in bacilli. II. Characteristics of protoplast membrane preparations. Biochim. Biophys. Acta 237 (1971) 255-272
19. Rodriguez M.J., Snyder N.J., Zweifel M.J., Wilkie S.C., Stack D.R., Cooper R.D., et al. Novel glycopeptide antibiotics: N-alkylated derivatives active against vancomycin-resistant enterococci. J. Antibiot. 51 (1998) 560-569
20. Gullion T., and Schaefer J. Detection of weak heteronuclear dipolar coupling by rotational-echo double-resonance nuclear magnetic resonance. Adv. Magn. Reson. 13 (1989) 57-83
21. Kim S.J., and Schaefer J. 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
22. Kim S.J., Matsuoka S., Patti G.J., and Schaefer J. 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
23. Kim S.J., Cegelski L., Stueber D., Singh M., Dietrich E., Tanaka K.S., et al. Oritavancin exhibits dual mode of action to inhibit cell-wall biosynthesis in Staphylococcus aureus. J. Mol. Biol. 377 (2008) 281-293
24. Cui L., Murakami H., Kuwahara-Arai K., Hanaki H., and Hiramatsu K. 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
25. 15N REDOR NMR. Biochemistry 36 (1997) 9859-9866
26. Huang H., Wooley K.L., and Schaefer J. REDOR determination of the composition of shell cross-linked amphiphilic core-shell nanoparticles and the partitioning of sequestered fluorinated guests. Macromolecules 34 (2001) 547-551
27. Cegelski L., Rice C.V., O'Connor R.D., Caruano A.L., Tochtrop G.P., Cai Z.Y., et al. Mapping the locations of estradiol and potent neuroprotective analogues in phospholipid bilayers by REDOR. Drug Dev. Res. 66 (2006) 93-102
28. Pasciak M., Holst O., Lindner B., Mordarska H., and Gamian A. Novel bacterial polar lipids containing ether-linked alkyl chains, the structures and biological properties of the four major glycolipids from Propionibacterium propionicum PCM 2431 (ATCC 14157T). J. Biol. Chem. 278 (2003) 3948-3956
29. Perkins H.R., and Nieto M. The preparation of iodinated vancomycin and its distribution in bacteria treated with the antibiotic. Biochem. J. 116 (1970) 83-92
30. Allison S.D., Manning M.C., Randolph T.W., Middleton K., Davis A., and Carpenter J.F. Optimization of storage stability of lyophilized actin using combinations of disaccharides and dextran. J. Pharm. Sci. 89 (2000) 199-214
31. Holtje J.V. Growth of the stress-bearing and shape-maintaining murein sacculus of Escherichia coli. Microbiol. Mol. Biol. Rev. 62 (1998) 181-203
32. Dmitriev B.A., Toukach F.V., Schaper K.J., Holst O., Rietschel E.T., and Ehlers S. Tertiary structure of bacterial murein: the scaffold model. J. Bacteriol. 185 (2003) 3458-3468
33. Gan L., Chen S., and Jensen G.J. Molecular organization of Gram-negative peptidoglycan. Proc. Natl Acad. Sci. USA 105 (2008) 18953-18957
34. Geisel R., Schmitz F.J., Fluit A.C., and Labischinski H. Emergence, mechanism, and clinical implications of reduced glycopeptide susceptibility in Staphylococcus aureus. Eur. J. Clin. Microbiol. Infect. Dis. 20 (2001) 685-697
35. Ghuysen J.M. Use of bacteriolytic enzymes in determination of wall structure and their role in cell metabolism. Bacteriol. Rev. 32 (1968) 425-464
36. Gullion T., and Schaefer J. Rotational-echo double-resonance NMR. J. Magn. Reson. 81 (1989) 196-200
37. Bennett A.E., Reienstra C.M., Auger M., Lakshmi K.V., and Griffin R.G. Heteronuclear decoupling in rotating solids. J. Chem. Phys. 103 (1995) 6951-6958
38. Gullion T., Baker D.B., and Conradi M.S. New, compensated Carr-Purcell sequences. J. Magn. Reson. 89 (1990) 479-484
39. 19F} rotational-echo double-resonance NMR. J. Polym. Sci., Part B: Polym. Phys. 44 (2006) 2760-2775
40. Mueller K.T., Jarvie T.P., Aurentz D.J., and Roberts B.W. The REDOR transform: direct calculation of internuclear couplings from dipolar-dephasing NMR data. Chem. Phys. Lett. 242 (1995) 535-542
41. de la Caillerie J.-B.d.E., and Fretigny C. Analysis of the REDOR signal and inversion. J. Magn. Reson. 133 (1998) 273-280