Bacterial cell wall composition and the influence of antibiotics by cell-wall and whole-cell NMR

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 370, Issue 1679, 2015, Pages

  Romaniuk, Joseph A H ^a   Cegelski, Lynette ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

Antibiotics; Bacterial cell wall; Peptidoglycan; S. aureus; Solid state NMR; Whole cell NMR

Indexed keywords

ANTIBIOTICS; BACTERIUM; CELLS AND CELL COMPONENTS; INHIBITOR; NUCLEAR MAGNETIC RESONANCE;

BACTERIA (MICROORGANISMS); STAPHYLOCOCCUS AUREUS;

ALANINE; ANTIINFECTIVE AGENT; GLYCOPEPTIDE; LYSINE; ORITAVANCIN; PEPTIDOGLYCAN; VANCOMYCIN;

CELL WALL; CHEMICAL STRUCTURE; CHEMISTRY; DRUG EFFECTS; MOLECULAR MODEL; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROCEDURES; STAPHYLOCOCCUS AUREUS; ULTRASTRUCTURE;

ALANINE; ANTI-BACTERIAL AGENTS; CELL WALL; GLYCOPEPTIDES; LYSINE; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; MOLECULAR STRUCTURE; PEPTIDOGLYCAN; STAPHYLOCOCCUS AUREUS; VANCOMYCIN;

EID: 84941712152     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2015.0024     Document Type: Review

References (96)

1. Vollmer W, Blanot D, de Pedro MA. 2008 Peptidoglycan structure and architecture. FEMS Microbiol. Rev. 32, 149–167. (doi:10.1111/j.15746976.2007.00094.x)
2. Lowy FD. 1998 Staphylococcus aureus infections. N. Engl. J. Med. 339, 520–532. (doi:10.1056/NEJM199808203390806)
3. Klevens RM et al. 2007 Invasive methicillin-resistant Staphylococcus aureus infections in the United States. JAMA 298, 1763–1771. (doi:10.1001/jama.298.15.1763)
4. Boucher HW, Talbot GH, Bradley JS, Edwards JE, Gilbert D, Rice LB, Scheld M, Spellberg B, Bartlett J. 2009 Bad bugs, no drugs: no ESKAPE! An update from the Infectious Diseases Society of America. Clin. Infect. Dis. 48, 1–12. (doi:10.1086/595011)
5. Wright GD. 2012 Antibiotics: a new hope. Chem. Biol. 19, 3–10. (doi:10.1016/j.chembiol. 2011.10.019)
6. Bush K et al. 2011 Tackling antibiotic resistance. Nat. Rev. Microbiol. 9, 894–896. (doi:10.1038/nrmicro2693)
7. Walsh CT, Wencewicz TA. 2014 Prospects for new antibiotics: a molecule-centered perspective. J. Antibiot. (Tokyo) 67, 7–22. (doi:10.1038/ja.2013.49)
8. Lovering AL, Safadi SS, Strynadka NC. 2012 Structural perspective of peptidoglycan biosynthesis and assembly. Annu. Rev. Biochem. 81, 451–478. (doi:10.1146/annurev-biochem-061809-112742)
9. Kahan FM, Kahan JS, Cassidy PJ, Kropp H. 1974 Mechanism of action of fosfomycin (phosphonomycin). Ann. NY Acad. Sci. 235, 364–386. (doi:10.1111/j.1749-6632.1974.tb43277.x)
10. Tipper DJ, Strominger JL. 1965 Mechanism of action of penicillins: a proposal based on their structural similarity to acyl-D-alanyl-D-alanine. Proc. Natl Acad. Sci. USA 54, 1133–1141. (doi:10.1073/pnas.54.4.1133)
11. Yocum RR, Rasmussen JR, Strominger JL. 1980 The mechanism of action of penicillin: penicillin acylates the active-site of Bacillus stearothermophilus D-alanine carboxypeptidase. J. Biol. Chem. 255, 3977–3986.
12. Brown S, Santa Maria JP, Walker S. 2013 Wall teichoic acids of Gram-positive bacteria. Annu. Rev. Microbiol. 67, 313–336. (doi:10.1146/annurevmicro-092412-155620)
13. Navarre WW, Schneewind O. 1999 Surface proteins of Gram-positive bacteria and mechanisms of their targeting to the cell wall envelope. Microbiol. Mol. Biol. Rev. 63, 174.
14. Bumsted RM et al. 1968 Biosynthesis of the peptidoglycan of bacterial cell walls. X. Further study of the glycyl transfer ribonucleic acids active in peptidoglycan synthesis in Staphylococcus aureus. J. Biol. Chem. 243, 779–782.
15. Siewert G, Strominger JL. 1968 Biosynthesis of the peptidoglycan of bacterial cell walls. XI. Formation of the isoglutamine amide group in the cell walls of Staphylococcus aureus. J. Biol. Chem. 243, 783–790.
16. Tipper DJ, Strominger JL. 1968 Biosynthesis of the peptidoglycan of bacterial cell walls. XII. Inhibition of cross-linking by penicillins and cephalosporins: studies in Staphylococcus aureus in vivo. J. Biol. Chem. 243, 3169–3179.
17. Glauner B. 1988 Separation and quantification of muropeptides with high-performance liquid chromatography. Anal. Biochem. 172, 451–464. (doi:10.1016/0003-2697(88)90468-X)
18. Patti GJ, Chen J, Gross ML. 2009 Method revealing bacterial cell-wall architecture by time-dependent isotope labeling and quantitative liquid chromatography/mass spectrometry. Anal. Chem. 81, 2437–2445. (doi:10.1021/ac802587r)
19. de Jonge BL et al. 1992 Peptidoglycan composition of a highly methicillin-resistant Staphylococcus aureus strain. The role of penicillin binding protein 2A. J. Biol. Chem. 267, 11 248–11 254.
20. Boneca IG et al. 2000 Characterization of Staphylococcus aureus cell wall glycan strands, evidence for a new beta-N-acetylglucosaminidase activity. J. Biol. Chem. 275, 9910–9918. (doi:10.1074/jbc.275.14.9910)
21. Laws DD, Bitter HM, Jerschow A. 2002 Solid-state NMR spectroscopic methods in chemistry. Angew. Chem. Int. Ed. Engl. 41, 3096–3129. (doi:10.1002/1521-3773(20020902)41:17,3096::AID-ANIE30 96.3.0.CO;2-X)
22. Reichhardt C, Cegelski L. 2014 Solid-state NMR for bacterial biofilms. Mol. Phys. 112, 887–894. (doi:10.1080/00268976.2013.837983)
23. McDermott A. 2009 Structure and dynamics of membrane proteins by magic angle spinning solidstate NMR. Annu. Rev. Biophys. 38, 385–403. (doi:10.1146/annurev.biophys.050708.133719)
24. Renault M, Tommassen-van Boxtel R, Bos MP, Post JA, Tommassen J, Baldus M. 2012 Cellular solidstate nuclear magnetic resonance spectroscopy. Proc. Natl Acad. Sci. USA 109, 4863–4868. (doi:10. 1073/pnas.1116478109)
25. Durr UHN, Gildenberg M, Ramamoorthy A. 2012 The magic of bicelles lights up membrane protein structure. Chem. Rev. 112, 6054–6074. (doi:10.1021/cr300061w)
26. Yamamoto K, Caporini MA, Im S-C, Waskell L, Ramamoorthy A. 2015 Cellular solid-state NMR investigation of a membrane protein using dynamic nuclear polarization. Biochim. Et Biophys. ActaBiomembr. 1848, 342–349. (doi:10.1016/j.bbamem.2014.07.008)
27. Vogel EP, Weliky DP. 2013 Quantitation of recombinant protein in whole cells and cell extracts via solid-state NMR spectroscopy. Biochemistry 52, 4285–4287. (doi:10.1021/bi4007034)
28. Kim SJ, Chang J, Singh M. 2015 Peptidoglycan architecture of Gram-positive bacteria by solid-state NMR. Biochim. Biophys. Acta 1848, 350–362. (doi:10.1016/j.bbamem.2014.05.031)
29. Kern T et al. 2010 Dynamics characterization of fully hydrated bacterial cell walls by solid-state NMR: evidence for cooperative binding of metal ions. J. Am. Chem. Soc. 132, 10 911–10 919. (doi:10.1021/ja104533w)
30. Ramamoorthy A. 2009 Beyond NMR spectra of antimicrobial peptides: dynamical images at atomic resolution and functional insights. Solid State Nucl. Magn. Reson. 35, 201–207. (doi:10.1016/j.ssnmr.2009.03.003)
31. Bechinger B, Salnikov ES. 2012 The membrane interactions of antimicrobial peptides revealed by solid-state NMR spectroscopy. Chem. Phys. Lipids 165, 282–301. (doi:10.1016/j.chemphyslip.2012.01.009)
32. Hong M, Su YC. 2011 Structure and dynamics of cationic membrane peptides and proteins: insights from solid-state NMR. Protein Sci. 20, 641–655. (doi:10.1002/pro.600)
33. Toke O, Cegelski L, Schaefer J. 2006 Peptide antibiotics in action: investigation of polypeptide chains in insoluble environments by rotational-echo double resonance. Biochim. Biophys. ActaBiomembr. 1758, 1314–1329. (doi:10.1016/j.bbamem.2006.02.031)
34. Schaefer J, Stejskal EO. 1976 Carbon-13 nuclear magnetic resonance of polymers spinning at the magic angle. J. Am. Chem. Soc. 98, 1031–1032. (doi:10.1021/ja00420a036)
35. Yannoni CS. 1982 High-resolution NMR in solids: the CPMAS experiment. Acc. Chem. Res. 15, 201–208. (doi:10.1021/ar00079a003)
36. McCrate OA, Zhou X, Reichhardt C, Cegelski L. 2013 Sum of the parts: composition and architecture of the bacterial extracellular matrix. J. Mol. Biol. 425, 4286–4294. (doi:10.1016/j.jmb.2013.06.022)
37. Reichhardt C, Fong JCN, Yildiz F, Cegelski L. 2015 Characterization of the Vibrio cholerae extracellular matrix: a top-down solid-state NMR approach. Biochim. Biophys. Acta 1848, 378–383. (doi:10.1016/j.bbamem.2014.05.030)
38. De Paëpe G. 2012 Dipolar recoupling in magic angle spinning solid-state nuclear magnetic resonance. Annu. Rev. Phys. Chem. 63, 661–684. (doi:10.1146/ annurev-physchem-032511-143726)
39. Cegelski L. 2013 REDOR NMR for drug discovery. Bioorg. Med. Chem. Lett. 23, 5767–5775. (doi:10.1016/j.bmcl.2013.08.064)
40. Cegelski L. 2015 Bottom-up and top-down solidstate NMR approaches for bacterial biofilm matrix composition. J. Magn Reson. 253, 91–97. (doi:10. 1016/j.jmr.2015.01.014)
41. Schanda P, Triboulet S, Laguri C, Bougault CM, Ayala I, Callon M, Arthur M, Simorre J-P. 2014 Atomic model of a cell-wall cross-linking enzyme in complex with an intact bacterial peptidoglycan. J. Am. Chem. Soc. 136, 17 852–17 860. (doi:10.1021/ja5105987)
42. 31Pg REDOR NMR studies of the binding of phosphonate reaction intermediate analogues to Saccharomyces cerevisiae lumazine synthase. Biochemistry 47, 13 942–13 951. (doi:10.1021/bi8015789)
43. McDowell LM, Studelska DR, Poliks B, O’Connor RD, Schaefer J. 2004 Characterization of the complex of a trifluoromethyl-substituted shikimate-based bisubstrate inhibitor and 5-enolpyruvylshikimate-3phosphate synthase by REDOR NMR. Biochemistry 43, 6606–6611. (doi:10.1021/bi049685w)
44. McDowell LM et al. 2003 Human factor Xa bound amidine inhibitor conformation by double rotationalecho double resonance nuclear magnetic resonance and molecular dynamics simulations. J. Med. Chem. 46, 359–363. (doi:10.1021/jm0202324)
45. Jiang YL et al. 2004 Recognition of an unnatural difluorophenyl nucleotide by uracil DNA glycosylase. Biochemistry 43, 15 429–15 438. (doi:10.1021/bi0483864)
46. 19 Fg rotational-echo double resonance. Biochemistry 45, 5235–5250. (doi:10.1021/bi052660s)
47. 15N labeling. J. Mol. Biol. 357, 1253–1262. (doi:10.1016/j.jmb.2006.01.040)
48. 3 is essential for the transglycosylase inhibition of peptidoglycan biosynthesis. Biochemistry 52, 1973–1979. (doi:10.1021/bi4000222)
49. Garbow JR, Jacob GS, Stejskal EO, Schaefer J. 1989 Protein dynamics from chemical shift and dipolar rotational spin-echo nitrogen-NMR. Biochemistry 28, 1362–1367. (doi:10.1021/bi00429a063)
50. 15 N REDOR NMR. Biochemistry 36, 9859–9866. (doi:10.1021/bi970495d)
51. Kern T et al. 2008 Toward the characterization of peptidoglycan structure and protein-peptidoglycan interactions by solid-state NMR spectroscopy. J. Am. Chem. Soc. 130, 5618–5619. (doi:10.1021/ja7108135)
52. Zhou X, Cegelski L. 2012 Nutrient-dependent structural changes in S. aureus peptidoglycan revealed by solid-state NMR spectroscopy. Biochemistry 51, 8143–8153. (doi:10.1021/bi3012115)
53. Nygaard R, Romaniuk JAH, Rice DM, Cegelski L. 2015 Spectral snapshots of bacterial cell-wall composition and the influence of antibiotics by whole-cell NMR. Biophys. J. 108, 1380–1389. (doi:10.1016/j.bpj.2015.01.037)
54. Meredith TC, Swoboda JG, Walker S. 2008 Latestage polyribitol phosphate wall teichoic acid biosynthesis in Staphylococcus aureus. J. Bacteriol. 190, 3046–3056. (doi:10.1128/JB.01880-07)
55. Mirelman D, Beck BD, Shaw DR. 1970 The location of the D-alanyl ester in the ribitol teichoic acid of Staphylococcus aureus. Biochem. Biophys. Res. Commun. 39, 712–717. (doi:10.1016/0006-291X(70)90263-9)
56. Coles NW, Gross R. 1973 Preparation of metabolically active Staphylococcus aureus protoplasts by use of the Aeromonas hydrophila lytic enzyme. J. Bacteriol. 115, 746–751.
57. Kim SJ, Singh M, Schaefer J. 2009 Oritavancin binds to isolated protoplast membranes but not intact protoplasts of Staphylococcus aureus. J. Mol. Biol. 391, 414–425. (doi:10.1016/j.jmb.2009.06.033)
58. Morath S, von Aulock S, Hartung T. 2005 Structure/ function relationships of lipoteichoic acids. J. Endotoxin Res 11, 348–356. (doi:10.1177/09680519050110061001)
59. Grif K et al. 2001 In vitro activity of fosfomycin in combination with various antistaphylococcal substances. J. Antimicrob. Chemother. 48, 209–217. (doi:10.1093/jac/48.2.209)
60. Gisin J, Schneider A, Nägele B, Borisova M, Mayer C. 2013 A cell wall recycling shortcut that bypasses peptidoglycan de novo biosynthesis. Nat. Chem. Biol. 9, 491–493. (doi:10.1038/nchembio.1289)
61. Contreras A, Barbacid M, Vazquez D. 1974 Binding to ribosomes and mode of action of chloramphenicol analogues. Biochim. Biophys. Acta 349, 376–388. (doi:10.1016/00052787(74)90124-5)
62. Takahashi H, Ayala I, Bardet M, De Paëpe G, Simorre J-P, Hediger S. 2013 Solid-state NMR on bacterial cells: selective cell wall signal enhancement and resolution improvement using dynamic nuclear polarization. J. Am. Chem. Soc. 135, 5105–5110. (doi:10.1021/ja312501d)
63. Wang T, Park YB, Caporini MA, Rosay M, Zhong L, Cosgrove DJ, Hong M. 2013 Sensitivity-enhanced solid-state NMR detection of expansin’s target in plant cell walls. Proc. Natl Acad. Sci. USA 110, 16 444–16 449. (doi:10.1073/pnas.1316290110)
64. Ni QZ et al. 2013 High frequency dynamic nuclear polarization. Acc. Chem. Res. 46, 1933–1941. (doi:10.1021/ar300348n)
65. Bui NK, Eberhardt A, Vollmer D, Kern T, Bougault C, Tomasz A, Simorre J-P, Vollmer W. 2012 Isolation and analysis of cell wall components from Streptococcus pneumoniae. Anal. Biochem. 421, 657–666. (doi:10.1016/j.ab.2011.11.026)
66. Breukink E, de Kruijff B. 2006 Lipid II as a target for antibiotics. Nat. Rev. Drug Discov. 5, 321–332. (doi:10.1038/nrd2004)
67. Cegelski L, Kim SJ, Hing AW, Studelska DR, O’Connor RD, Mehta AK, Schaefer J. 2002 Rotational-echo double resonance characterization of the effects of vancomycin on cell wall synthesis in Staphylococcus aureus. Biochemistry 41, 13 053–13 058. (doi:10. 1021/bi0202326)
68. 15 N NMR. J. Biol. Chem. 268, 18 692–18 695.
69. 15 N nuclear magnetic resonance. J. Biol. Chem. 258, 10 824–10 826.
70. Hing A, Vega S, Schaefer J. 1993 Measurement of heteronuclear dipolar coupling by transferred-echo double-resonance NMR. J. Magn. Reson. 103, 151–162. (doi:10.1006/jmra.1993.1146)
71. Patti GJ, Kim SJ, Schaefer J. 2008 Characterization of the peptidoglycan of vancomycin-susceptible Enterococcus faecium. Biochemistry 47, 8378–8385. (doi:10.1021/bi8008032)
72. 15 N NMR studies of the effects of penicillin on cellwall metabolism of Aerococcus viridans (Gaffkya homari). Biochem. Biophys. Res. Commun. 126, 1006–1012. (doi:10.1016/0006-291X(85)90285-2)
73. Siewert G, Strominger JL. 1967 Bacitracin: an inhibitor of the dephosphorylation of lipid pyrophosphate, an intermediate in the biosynthesis of the peptidoglycan of bacterial cell walls. Proc. Natl Acad. Sci. USA 57, 767–773. (doi:10.1073/pnas.57.3.767)
74. Strominger JL. 1957 Microbial uridine-5 pyrophosphate N-acetylamino sugar compounds. I. Biology of the penicillin-induced accumulation. J. Biol. Chem. 224, 509–523.
75. Turner RD, Ratcliffe EC, Wheeler R, Golestanian R, Hobbs JK, Foster SJ. 2010 Peptidoglycan architecture can specify division planes in Staphylococcus aureus. Nat. Commun. 1, 26. (doi:10.1038/ncomms1025)
76. Williams I et al. 1999 Flow cytometry and other techniques show that Staphylococcus aureus undergoes significant physiological changes in the early stages of surface-attached culture. Microbiology 145, 1325–1333. (doi:10.1099/13500872-145-6-1325)
77. Rohrer S, Ehlert K, Tschierske M, Labischinski H, 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. USA 96, 9351–9356. (doi:10. 1073/pnas.96.16.9351)
78. Kim SJ et al. 2008 Oritavancin exhibits dual mode of action to inhibit cell-wall biosynthesis in Staphylococcus aureus. J. Mol. Biol. 377, 281–293. (doi:10.1016/j.jmb.2008.01.031)
79. Kim SJ, Cegelski L, Studelska DR, O’Connor RD, Mehta AK, Schaefer J. 2002 Rotational-echo double resonance characterization of vancomycin binding sites in Staphylococcus aureus. Biochemistry 41, 6967–6977. (doi:10.1021/bi0121407)
80. Kim SJ, Singh M, Sharif S, Schaefer J. 2014 Crosslink formation and peptidoglycan lattice assembly in the FemA mutant of Staphylococcus aureus. Biochemistry 53, 1420–1427. (doi:10.1021/bi4016742)
81. Singh M, Kim SJ, Sharif S, Preobrazhenskaya M, Schaefer J. 2015 REDOR constraints on the peptidoglycan lattice architecture of Staphylococcus aureus and its FemA mutant. Biochim. Biophys. Acta 1848, 363–368. (doi:10.1016/j.bbamem.2014.05.025)
82. Strominger JL, Willoughby E, Kamiryo T, Blumberg PM, Yocum RR. 1974 Penicillin-sensitive enzymes and penicillin-binding components in bacterial cells. Ann. NY Acad. Sci. 235, 210–224. (doi:10.1111/j.1749-6632.1974.tb43267.x)
83. Cho H, Uehara T, Bernhardt TG. 2014 Beta-lactam antibiotics induce a lethal malfunctioning of the bacterial cell wall synthesis machinery. Cell 159, 1300–1311. (doi:10.1016/j.cell.2014.11.017)
84. 13C NMR. Magn. Reson. Chem. 24, 835–852. (doi:10.1002/mrc.1260241002)
85. Meroueh SO, Bencze KZ, Hesek D, Lee M, Fisher JF, Stemmler TL, Mobashery S. 2006 Three-dimensional structure of the bacterial cell wall peptidoglycan. Proc. Natl Acad. Sci. USA 103, 4404–4409. (doi:10.1073/pnas.0510182103)
86. Sharif S, Kim SJ, Labischinski H, Schaefer J. 2009 Characterization of peptidoglycan in fem-deletion mutants of methicillin-resistant Staphylococcus aureus by solid-state NMR. Biochemistry 48, 3100–3108. (doi:10.1021/bi801750u)
87. Sharif S, Kim SJ, Labischinski H, Chen J, Schaefer J. 2013 Uniformity of glycyl bridge lengths in the mature cell walls of FEM mutants of methicillinresistant Staphylococcus aureus. J. Bacteriol. 195, 1421–1427. (doi:10.1128/JB.01471-12)
88. Sharif S, Singh M, Kim SJ, Schaefer J. 2009 Staphylococcus aureus peptidoglycan tertiary structure from carbon-13 spin diffusion. J. Am. Chem. Soc. 131, 7023–7030. (doi:10.1021/ja808971c)
89. Allen NE, LeTourneau DL, Hobbs JN Jr. 1997 Molecular interactions of a semisynthetic glycopeptide antibiotic with D-alanyl-D-alanine and D-alanyl-D-lactate residues. Antimicrob. Agents Chemother. 41, 66–71.
90. Williams DH et al. 1998 An analysis of the origins of a cooperative binding energy of dimerization. Science 280, 711–714. (doi:10.1126/science.280.5364.711)
91. Sharman GJ et al. 1997 The roles of dimerization and membrane anchoring in activity of glycopeptide antibiotics against vancomycin-resistant bacteria. J. Am. Chem. Soc. 119, 12 041–12 047. (doi:10.1021/ja964477f)
92. Kim SJ, 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, 10 155–10 161. (doi:10.1021/bi800838c)
93. Kim SJ, Tanaka KSE, Dietrich E, Rafai Far A, Schaefer J. 2013 Locations of the hydrophobic side chains of lipoglycopeptides bound to the peptidoglycanof Staphylococcus aureus. Biochemistry 52, 3405–3414. (doi:10.1021/bi400054p)
94. Good VM, Gwynn MN, Knowles DJ. 1990 MM 45289, a potent glycopeptide antibiotic which interacts weakly with diacetyl-L-lysyl-D-alanyl-Dalanine. J. Antibiot. (Tokyo) 43, 550- 555. (doi:10.7164/antibiotics.43.550)
95. Allen NEL, Hobbs DL. 1997 The role of hydrophobic side chains as determinants of antibacterial activity of semisynthetic glycopeptide antibiotics. J. Antibiot. (Tokyo) 50, 677–684. (doi:10.7164/antibiotics.50.677)
96. Patti GJ, Kim SJ, Yu T-Y, Dietrich E, Tanaka KSE, Parr TR, Far AR, Schaefer J. 2009 Vancomycin and oritavancin have different modes of action in Enterococcus faecium. J. Mol. Biol. 392, 1178–1191. (doi:10.1016/j.jmb.2009.06.064)