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Chapter 36 : The Staphylococcal Cell Wall

Author: Alexander Tomasz
Content Type: Reference
Publication Year: 2006

Category: Bacterial Pathogenesis

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Abstract:

The history of interest in the staphylococcal cell wall reflects the history of success and failure of the antibiotic era. Elucidation of the mode of action of several important antibiotics in the 1960s and 1970s has been intimately linked to studies on the biosynthesis of staphylococcal cell walls. In addition to the reemergence of interest in cell walls in the context of modern microbial cell biology, two approaches have been making great impact on discoveries in this field: the introduction of high-resolution analytical techniques (high-pressure liquid chromatography [HPLC] and mass spectrometry) and the increasing application of molecular genetic approaches. This chapter includes a brief reminder of the anatomy of staphylococcal cell walls, and reviews new information under four headings: high-resolution analysis of the peptidoglycan; variations in peptidoglycan composition; genetic determinants and enzymes in cell wall synthesis; and complex functions of cell walls. Unlike in streptococci, in consecutive cell divisions occur in three division planes, each at right angles to one another, and proper orientation of cell wall septa must involve a complex and superbly controlled mechanism. Progress in the high-resolution chemistry of the cell wall came from the introduction of HPLC and mass spectrometric methods for the analysis of the peptidoglycan.

Citation: Tomasz A. 2006. The Staphylococcal Cell Wall, p 443-455. In Fischetti V, Novick R, Ferretti J, Portnoy D, Rood J (ed), Gram-Positive Pathogens, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816513.ch36

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The Staphylococcal Cell Wall
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Citation: Tomasz A. 2006. The Staphylococcal Cell Wall, p 443-455. In Fischetti V, Novick R, Ferretti J, Portnoy D, Rood J (ed), Gram-Positive Pathogens, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816513.ch36
/content/10.1128/9781555816513.chap36.fig36-1
FIGURE 1

Localization of cell wall synthesis in . (A) Van-fluorescence labeling of RN4220 cells. The entire cell wall, including the septum, has been labeled. (B) Van-fluorescence labeling of RN4220 cells after transient incubation with an excess of d-serine. This appears to result in specific labeling of new peptidoglycan. Different stages of septum formation can be observed. Left panel: Cells have two fluorescent spots that presumably correspond to a ring of new peptidoglycan at the division site. Middle panel: Cells have a fluorescent line across the middle, which should correspond to a complete disk of new peptidoglycan—the closed septum. Right panel: A tilted cell allows visualization of an entire ring of new peptidoglycan in an incomplete septum. (C) Wheat germ agglutinin labeling of RN4220 cells, followed by incubation in the absence of the dye. Recently synthesized or uncovered wall material appears as a nonfluorescent region that constitutes the new hemisphere of each daughter cell. (D) Immunofluorescence imaging of PBP2 in RN4220 cells. Scale bars, 1 µm. Phase-contrast microscopy images are shown below each fluorescence image in panels B and C. (Reproduced with permission from reference .)

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10.1128/9781555816513/fig36-1.gif
Image of FIGURE 1
FIGURE 1

Localization of cell wall synthesis in . (A) Van-fluorescence labeling of RN4220 cells. The entire cell wall, including the septum, has been labeled. (B) Van-fluorescence labeling of RN4220 cells after transient incubation with an excess of d-serine. This appears to result in specific labeling of new peptidoglycan. Different stages of septum formation can be observed. Left panel: Cells have two fluorescent spots that presumably correspond to a ring of new peptidoglycan at the division site. Middle panel: Cells have a fluorescent line across the middle, which should correspond to a complete disk of new peptidoglycan—the closed septum. Right panel: A tilted cell allows visualization of an entire ring of new peptidoglycan in an incomplete septum. (C) Wheat germ agglutinin labeling of RN4220 cells, followed by incubation in the absence of the dye. Recently synthesized or uncovered wall material appears as a nonfluorescent region that constitutes the new hemisphere of each daughter cell. (D) Immunofluorescence imaging of PBP2 in RN4220 cells. Scale bars, 1 µm. Phase-contrast microscopy images are shown below each fluorescence image in panels B and C. (Reproduced with permission from reference .)

Citation: Tomasz A. 2006. The Staphylococcal Cell Wall, p 443-455. In Fischetti V, Novick R, Ferretti J, Portnoy D, Rood J (ed), Gram-Positive Pathogens, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816513.ch36
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FIGURE 2

The anatomy of cell walls in normal (left) and vancomycin-resistant (right) . (Reproduced with permission from reference .)

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Image of FIGURE 2
FIGURE 2

The anatomy of cell walls in normal (left) and vancomycin-resistant (right) . (Reproduced with permission from reference .)

Citation: Tomasz A. 2006. The Staphylococcal Cell Wall, p 443-455. In Fischetti V, Novick R, Ferretti J, Portnoy D, Rood J (ed), Gram-Positive Pathogens, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816513.ch36
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FIGURE 3

Three-dimensional structure of staphylococcal peptidoglycan. The straight lines of large bowls represent the sugar moieties of the peptidoglycan. Each globe in these lines symbolizes an amino sugar, -acetylglucosamine (black globe), or acetylmuramic acid (white globe). Stempeptides, branching from acetylmuramic acid, are characterized by small dark globes with a white center. The connecting interpeptide bridges (pentaglycines) between the stem-peptides are shown as small black globes. Schematic drawing by Peter Giesbrecht, Thomas Kersten, Heiner Maidhof, and Jorg Wecke, Robert-Koch Institute, Berlin, Germany.

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10.1128/9781555816513/fig36-3.gif
Image of FIGURE 3
FIGURE 3

Three-dimensional structure of staphylococcal peptidoglycan. The straight lines of large bowls represent the sugar moieties of the peptidoglycan. Each globe in these lines symbolizes an amino sugar, -acetylglucosamine (black globe), or acetylmuramic acid (white globe). Stempeptides, branching from acetylmuramic acid, are characterized by small dark globes with a white center. The connecting interpeptide bridges (pentaglycines) between the stem-peptides are shown as small black globes. Schematic drawing by Peter Giesbrecht, Thomas Kersten, Heiner Maidhof, and Jorg Wecke, Robert-Koch Institute, Berlin, Germany.

Citation: Tomasz A. 2006. The Staphylococcal Cell Wall, p 443-455. In Fischetti V, Novick R, Ferretti J, Portnoy D, Rood J (ed), Gram-Positive Pathogens, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816513.ch36
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FIGURE 4

Analysis of the peptidoglycan of a methicillin-resistant strain of (bottom) and its mutant (top). (Reproduced with permission from reference .)

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Image of FIGURE 4
FIGURE 4

Analysis of the peptidoglycan of a methicillin-resistant strain of (bottom) and its mutant (top). (Reproduced with permission from reference .)

Citation: Tomasz A. 2006. The Staphylococcal Cell Wall, p 443-455. In Fischetti V, Novick R, Ferretti J, Portnoy D, Rood J (ed), Gram-Positive Pathogens, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816513.ch36
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FIGURE 5

Distribution of glycan chain length in . (Top) Tracing of the HPLC profile by UV absorbance. (Bottom) Tracing of the same HPLC chromatogram through radioactivity due to the labeling of the glycan with H -acetylglucosamine. (Reproduced with permission from reference .)

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10.1128/9781555816513/fig36-5.gif
Image of FIGURE 5
FIGURE 5

Distribution of glycan chain length in . (Top) Tracing of the HPLC profile by UV absorbance. (Bottom) Tracing of the same HPLC chromatogram through radioactivity due to the labeling of the glycan with H -acetylglucosamine. (Reproduced with permission from reference .)

Citation: Tomasz A. 2006. The Staphylococcal Cell Wall, p 443-455. In Fischetti V, Novick R, Ferretti J, Portnoy D, Rood J (ed), Gram-Positive Pathogens, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816513.ch36
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FIGURE 6

Localization of gene products on the cell surface of during the division cycle as determined by scanning electron microscopy. Panels a to d show the immunogold labeling patterns on cells at different stages of the cell cycle. Scale bar, 100 nm. (Reproduced with permission from Yamada et al. [ ].)

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10.1128/9781555816513/fig36-6.gif
Image of FIGURE 6
FIGURE 6

Localization of gene products on the cell surface of during the division cycle as determined by scanning electron microscopy. Panels a to d show the immunogold labeling patterns on cells at different stages of the cell cycle. Scale bar, 100 nm. (Reproduced with permission from Yamada et al. [ ].)

Citation: Tomasz A. 2006. The Staphylococcal Cell Wall, p 443-455. In Fischetti V, Novick R, Ferretti J, Portnoy D, Rood J (ed), Gram-Positive Pathogens, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816513.ch36
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References

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1. Archibald, A. R., 1972. The chemistry of staphylococcal cell walls, p. 75. In J. O. Cohen (ed.), The Staphylococci. Wiley-Interscience, New York, N.Y.
2. Baba, T.,, and O. Schneewind. 1998. Targeting of muralytic enzymes to the cell division site of gram-positive bacteria: repeat domains direct autolysin to the equatorial surface ring of Staphylococcus aureus. EMBO J. 17: 4639– 4646.
3. Benson, T. E.,, D. B. Prince,, V.T. Mutchler,, K. A. Curry,, A. M. Ho,, R. W. Sarver,, J. C. Hagadorn,, G. H. Choi,, and R. L. Garlick. 2002. X-ray crystal structure of Staphylococcus aureus FemA. Structure 10: 1107– 1115.
4. Berger-Bächi, B. 1983. Insertional inactivation of staphylococcal methicillin resistance by Tn551. J. Bacteriol. 154: 479– 487.
5. Bischoff, M.,, M. Roos,, J. Putnik,, A. Wada,, P. Glanzmann,, P. Giachino,, P. Vaudaux,, and B. Berger-Bachi. 2001. Involvement of multiple genetic loci in Staphylococcus aureus teicoplanin resistance. FEMS Microbiol. Lett. 194: 77– 82.
6. Boneca, I. G.,, N. Xu,, D. A. Gage,, B. L. M. de Jonge,, and A. Tomasz. 1997. Structural characterization of an abnormally cross-linked muropeptide dimer that is accumulated in the peptidoglycan of methicillin- and cefotaxime-resistant mutants of Staphylococcus aureus. J. Biol. Chem. 272: 29053– 29059.
7. Boneca, I. G.,, Z.-H. Huang,, D. A. Gage,, and A. Tomasz. 2000. Characterization of Staphylococcus aureus cell wall glycan strands, evidence for a new endo-β-Nacetylglucosaminidase activity. J. Biol. Chem. 275: 9910– 9918.
8. Boyle-Vavra, S.,, H. Labischinski,, C. C. Ebert,, K. Ehlert,, and R. S. Daum. 2001. A spectrum of changes occurs in peptidoglycan composition of glycopeptide-intermediate clinical Staphylococcus aureus isolates. Antimicrob. Agents Chemother. 45: 280– 287.
9. Boyle-Vavra, S.,, R. B. Carey,, and R. S. Daum. 2001. Development of vancomycin and lysostaphin resistance in a methicillin-resistant Staphylococcus aureus isolate. J. Antimicrob. Chemother. 48: 617– 625.
10. Boyle-Vavra, S.,, S. Yin,, M. Challapalli,, and R. S. Daum. 2003. Transcriptional induction of the penicillin-binding protein 2 gene in Staphylococcus aureus by cell wall-active antibiotics oxacillin and vancomycin. Antimicrob. Agents Chemother. 47: 1028– 1036.
11. Brunskill, E. W.,, and K. W. Bayles. 1996. Identification of LytSR-regulated genes from Staphylococcus aureus. J. Bacteriol. 178: 5810– 5812.
12. Brunskill, E. W.,, B. L. de Jonge,, and K. W. Bayles. 1997. The Staphylococcus aureus scdA gene: a novel locus that affects cell division and morphogenesis. Microbiology 143: 2877– 2882.
13. Cui, L.,, H. Murakami,, K. Kuwahara-Arai,, H. Hanaki,, and K. Hiramatsu. 2000. Contribution of a thickened cell wall and its glutamine nonamidated component to the vancomycin resistance expressed by Staphylococcus aureus Mu50. Antimicrob. Agents Chemother. 44: 2276– 2285.
14. Cui, L.,, X. Ma,, K. Sato,, K. Okuma,, F. C. Tenover,, E. M. Mamizuka,, C. G. Gemmell,, M. N. Kim,, M. C. Ploy,, N. El-Solh,, V. Ferraz,, and K. Hiramatsu. 2003. Cell wall thickening is a common feature of vancomycin resistance in Staphylococcus aureus. J. Clin. Microbiol. 41: 5– 14.
15. Daum, R. S.,, S. Gupta,, R. Sabbagh,, and W. M. Milewski. 1992. Characterization of Staphylococcus aureus isolates with decreased susceptibility to vancomycin and teicoplanin: isolation and purification of a constitutively produced protein associated with decreased susceptibility. J. Infect. Dis. 166: 1066– 1072.
16. De Jonge, B. L. M.,, D. Gage,, and N. Xu. 2002. The carboxyl terminus of peptidoglycan stem peptides is a determinant for methicillin resistance in Staphylococcus aureus. Antimicrob. Agents Chemother. 46: 3151– 3155.
17. De Jonge, B. L. M.,, Y.-S. Chang,, D. Gage,, and A. Tomasz. 1992. Peptidoglycan composition of a highly methicillin-resistant Staphylococcus aureus strain: the role of penicillin binding protein 2A. J. Biol. Chem. 267: 11248– 11254.
18. De Jonge, B. L. M.,, Y.-S. Chang,, D. Gage,, and A. Tomasz. 1992. Peptidoglycan composition in heterogeneous Tn 551 mutants of a methicillin-resistant Staphylococcus aureus strain. J. Biol. Chem. 267: 11255– 11259.
19. De Jonge, B. L. M.,, Y.-S. Chang,, N. Xu,, and D. Gage. 1996. Effect of exogenous glycine on peptidoglycan composition and resistance in a methicillin-resistant Staphylococcus aureus strain. Antimicrob. Agents Chemother. 40: 1498– 1503.
20. De Lencastre, H.,, B. L. M., de Jonge,, P. R. Matthews,, and A. Tomasz. 1994. Molecular aspects of methicillin resistance in Staphylococcus aureus. J. Antimicrob. Chemother. 33: 7– 24.
21. De Lencastre, H.,, and A. Tomasz. 1994. Reassessment of the number of auxiliary genes essential for expression of high-level methicillin resistance in Staphylococcus aureus. Antimicrob. Agents Chemother. 38: 2590– 2598.
22. De Lencastre, H.,, S. W. Wu,, M. G. Pinho,, A. M. Ludovice,, S. R. Filipe,, S. Gardete,, R. Sobral,, S. Gill,, M. Chung,, and A. Tomasz. 1999. Antibiotic resistance as a stress response: complete sequence of a large number of chromosomal loci in Staphylococcus aureus strain COL that impact on the expression of resistance to methicillin. Microb. Drug Resist. 5: 163– 175.
23. Dijkstra, A. J.,, and W. Keck. 1996. Peptidoglycan as a barrier to transenvelope transport. J. Bacteriol. 178: 5555– 5562.
24. Domanski, T. L.,, and K. W. Bayles. 1995. Analysis of Staphylococcus aureus genes encoding penicillin-binding protein 4 and an ABC-type transporter. Gene 167: 111– 113.
25. Domanski, T. L.,, B. L. M., de Jonge,, and K. W. Bayles. 1997. Transcription analysis of the Staphylococcus aureus gene encoding penicillin-binding protein 4. J. Bacteriol. 179: 2651– 2657.
26. Fujimoto, D. F.,, and K. W. Bayles. 1998. Opposing roles of the Staphylococcus aureus virulence regulators, Agr and Sar, in Triton X-100- and penicillin-induced autolysis. J. Bacteriol. 180: 3724– 3726.
27. Fujimura, T.,, and K. Murakami. 1997. Increase of methicillin resistance in Staphylococcus aureus caused by deletion of a gene whose product is homologous to lytic enzymes. J. Bacteriol. 179: 6294– 6301.
28. Georgopapadakou, N. H.,, B. A. Dix,, and Y. R. Mauriz. 1986. Possible physiological functions of penicillin-binding proteins in Staphylococcus aureus. Antimicrob. Agents Chemother. 29: 333– 336.
29. Ghuysen, J.-M.,, and R. Hakenbeck (ed.). 1994. Bacterial Cell Wall. Elsevier Science B.V., Amsterdam, The Netherlands.
30. Giesbrecht, P.,, T. Kersten,, H. Maidhof,, and J. Weeke. 1998. The staphylococcal cell wall: morphogenesis and fatal variations in the presence of penicillin. Microbiol. Mol. Biol. Rev. 62: 1371– 1414.
31. Gustafson, J.,, A. Strässle,, H. Hächler,, F. H. Kayser,, and B. Berger-Bächi. 1994. The femC locus of Staphylococcus aureus required for methicillin resistance includes the glutamine synthetase operon. J. Bacteriol. 176: 1460– 1467.
32. Hackbarth, C. J.,, T. Kocagoz,, S. Kocagoz,, and H. F. Chambers. 1995. Point mutations in Staphylococcus aureus PBP2 gene affect penicillin-binding kinetics and are associated with resistance. Antimicrob. Agents Chemother. 39: 103– 106.
33. Hakenbeck, R.,, J.-V. Höltje,, and H. Labischinski (ed.). 1983. The Target of Penicillin. Walter de Gruyter, Berlin, Germany.
34. Hanaki, H.,, H. Labischinski,, Y. Inaba,, N. Kondo,, H. Murakami,, and K. Hiramatsu. 1998. Increase in glutamine-non-amidated muropeptides in the peptidoglycan of vancomycin-resistant Staphylococcus aureus strain Mu50. J. Antimicrob. Chemother. 42: 315– 320.
35. Henze, U. U.,, and B. Berger-Bächi. 1995. Staphylococcus aureus penicillin-binding protein 4 and intrinsic β-lactam resistance. Antimicrob. Agents Chemother. 39: 2415– 2422.
36. Henze, U. U.,, and B. Berger-Bächi. 1996. Penicillin-binding protein 4 overproduction increases β-lactam resistance in Staphylococcus aureus. Antimicrob. Agents Chemother. 40: 2121– 2125.
37. Jacobs, C.,, J.-M. Frère,, and S. Normark. 1997. Cytosolic intermediates for cell wall biosynthesis and degradation control inducible β-lactam resistance in gram-negative bacteria. Cell 88: 823– 832.
38. Jayaswal, R. K.,, Y. I. Lee,, and B. J. Wilkinson. 1990. Cloning and expression of a Staphylococcus aureus gene encoding a peptidoglycan hydrolase activity. J. Bacteriol. 172: 5783– 5788.
39. Jolly, L.,, S. Wu,, J. van Heijenoort,, H. de Lencastre,, D. Mengin-Lecreulx,, and A. Tomasz. 1997. The femR315 gene from Staphylococcus aureus, the interruption of which results in reduced methicillin resistance, encodes a phosphoglucosamine mutase. J. Bacteriol. 179: 5321– 5325.
40. Kojima, N.,, Y. Araki,, and E. Ito. 1985. Structure of the linkage units between ribitol teichoic acids and peptidoglycan. J. Bacteriol. 161: 299– 306.
41. Komatsuzawa, H.,, G. H. Choi,, T. Fujiwara,, Y. Huang,, K. Ohta,, M. Sugai,, and H. Suginaka. 2000. Identification of a fmtA-like gene that has similarity to other PBPs and beta-lactamases in Staphylococcus aureus. FEMS Microbiol. Lett. 188: 35– 39.
42. Komatsuzawa, H.,, K. Ohta,, M. Sugai,, T. Fujiwara,, P. Glanzmann,, B. Berger-Bachi,, and H. Suginaka. 2000. Tn551-mediated insertional inactivation of the fmtB gene encoding a cell wall-associated protein abolishes methicillin resistance in Staphylococcus aureus. J. Antimicrob. Chemother. 45: 421– 431.
43. Komatsuzawa, H.,, T. Fujiwara,, H. Nishi,, S. Yamada,, M. Ohara,, N. McCallum,, B. Berger-Bachi,, and M. Sugai. 2004. The gate controlling cell wall synthesis in Staphylococcus aureus. Mol. Microbiol. 53: 1221– 1231.
44. Komatsuzawa, H.,, K. Ohta,, H. Labischinski,, M. Sugai,, and H. Suginaka. 1999. Characterization of fmtA, a gene that modulates the expression of methicillin resistance in Staphylococcus aureus. Antimicrob. Agents Chemother. 43: 2121– 2125.
45. Komatsuzawa, H.,, K. Ohta,, S. Yamada,, K. Ehlert,, H. Labischinski,, J. Kajimura,, T. Fujiwara,, and M. Sugai. 2002. Increased glycan chain length distribution and decreased susceptibility to moenomycin in a vancomycinresistant Staphylococcus aureus mutant. Antimicrob. Agents Chemother. 46: 75– 81.
46. Komatsuzawa, H.,, K. Ohta,, T. Fujiwara,, G. H. Choi,, H. Labischinski,, and M. Sugai. 2001. Cloning and sequencing of the gene, fmtC, which affects oxacillin resistance in methicillin-resistant Staphylococcus aureus. FEMS Microbiol. Lett. 203: 49– 54.
47. Komatsuzawa, H.,, M. Sugai,, K. Ohta,, T. Fujiwara,, S. Nakashima,, J. Suzuki,, C. Y. Lee,, and H. Suginaka. 1997. Cloning and characterization of the fmt gene which affects the methicillin resistance level and autolysis in the presence of Triton X-100 in methicillin-resistant Staphylococcus aureus. Antimicrob. Agents Chemother. 41: 2355– 2361.
48. Kornblum, J.,, B. J. Hartman,, R. P. Novick,, and A. Tomasz. 1986. Conversion of a homogeneously methicillin resistant strain of Staphylococcus aureus to heterogeneous resistance by Tn 551-mediated insertional inactivation. Eur. J. Clin. Microbiol. 5: 714– 718.
49. Kruger, R. G.,, B. Otvos,, B. A. Frankel,, M. Bentley,, P. Dostal,, and D. G. McCafferty. 2004. Analysis of the substrate specificity of the Staphylococcus aureus sortase transpeptidase SrtA. Biochemistry 43: 1541– 1551.
50. Kuroda, M.,, H. Kuroda,, T. Oshima,, F. Takeuchi,, H. Mori,, and K. Hiramatsu. 2003. Two-component system VraSR positively modulates the regulation of cell-wall biosynthesis pathway in Staphylococcus aureus. Mol. Microbiol. 49: 807– 821.
51. Lim, D.,, and N. C. J. Strynadka. 2002. Structural basis for the β-lactam resistance of PBP2a from methicillin-resistant Staphylococcus aureus. Nat. Struct. Biol. 9: 789– 885.
52. Ludovice, A. M.,, S. Wu,, and H. de Lencastre. 1998. Molecular cloning and DNA sequencing of the Staphylococcus aureus UDP-N-acetylmuramyl tripeptide synthetase ( murE) gene, essential for the optimal expression of methicillin resistance. Microb. Drug Resist. 4: 85– 90.
53. Luker, F. I.,, D. Mitchell,, and H. P. Laburn. 2000. Fever and motor activity in rats following day and night injections of Staphylococcus aureus cell walls. Am. J. Physiol. Regul. Integr. Comp. Physiol. 279: R610– R616.
54. Maki, H.,, T. Yamaguchi,, and K. Murakami. 1994. Cloning and characterization of a gene affecting the methicillin resistance level and the autolysis rate in Staphylococcus aureus. J. Bacteriol. 176: 4993– 5000.
55. Mani, N.,, P. Tobin,, and R. K. Jayaswal. 1993. Isolation and characterization of autolysis-defective mutants of Staphylococcus aureus created by Tn 917- lacZ mutagenesis. J. Bacteriol. 175: 1493– 1499.
56. Matsui, K.,, R. Motohashi,, and A. Nishikawa. 2000. Cell wall components of Staphylococcus aureus induce interleukin-5 production in patients with atopic dermatitis. J. Interferon Cytokine Res. 20: 321– 324.
57. May Wang, Q.,, R. B Perry,, R. B. Johnson,, W. E. Alborn,, W.-K. Yeh,, and P. L. Skatrud. 2001. Identification and characterization of a monofunctional glycosyltransferase from Staphylococcus aureus. J. Bacteriol. 183: 4779– 4785.
58. Moreau, M.,, J. C. Richards,, J. M. Fournier,, R. A. Byrd,, W. W. Karakawa,, and W. F. Vann. 1990. Structure of the type-5 capsular polysaccharide of Staphylococcus aureus. Carbohydr. Res. 201: 285– 297.
59. Murakami, K.,, and A. Tomasz. 1989. Involvement of multiple genetic determinants in high-level methicillin-resistance in Staphylococcus aureus. J. Bacteriol. 171: 874– 879.
60. Murakami, K.,, T. Fujimura,, and M. Doi. 1994. Nucleotide sequence of the structural gene for the penicillin-binding protein 2 of Staphylococcus aureus and the presence of a homologous gene in other staphylococci. FEMS Microbiol. Lett. 117: 131– 136.
61. Ornelas-Soares, A.,, H. de Lencastre,, B. de Jonge,, D. Gage,, Y.-S. Chang,, and A. Tomasz. 1993. The peptidoglycan composition of a Staphylococcus aureus mutant selected for reduced methicillin resistance. J. Biol. Chem. 268: 26268– 26272.
62. Ornelas-Soares, A.,, H. de Lencastre,, B. L. M. de Jonge,, and A. Tomasz. 1994. Reduced methicillin resistance in a new Staphylococcus aureus transposon mutant that incorporates muramyl dipeptides into the cell wall peptidoglycan. J. Biol. Chem. 269: 27246– 27250.
63. Oshida, T.,, and A. Tomasz. 1992. Isolation and characterization of a Tn 551-autolysis mutant of Staphylococcus aureus. J. Bacteriol. 174: 4952– 4959.
64. Oshida, T.,, M. Sugai,, H. Komatsuzawa,, Y.-M. Hong,, H. Suginaka,, and A. Tomasz. 1995. A Staphylococcus aureus autolysin that has an N-acetylmuramoyl-L-alanine amidase domain and an endo-β-N-acetylglucosaminidase domain: cloning, sequence analysis and characterization. Proc. Natl. Acad. Sci. USA 92: 285– 289.
65. Pfeltz, R. F.,, V. K. Singh,, J. L. Schmidt,, M. A. Batten,, C. S. Baranyk,, M. J. Nadakavukaren,, R. K. Jayaswal,, and B. J. Wilkinson. 2000. Characterization of passage-selected vancomycin-resistant Staphylococcus aureus strains of diverse parental backgrounds. Antimicrob. Agents Chemother. 44: 294– 303.
66. Pinho, M. G.,, and J. Errington. 2003. Dispersed mode of Staphylococcus aureus cell wall synthesis in the absence of the division machinery. Mol. Microbiol. 50: 871– 881.
67. Pinho, M. G.,, H. de Lencastre,, and A. Tomasz. 2000. Cloning, characterization, and inactivation of the gene pbpC, encoding penicillin-binding protein 3 of Staphylococcus aureus. J. Bacteriol. 182: 1074– 1079.
68. Pinho, M. G.,, H. de Lencastre,, and A. Tomasz. 2001. An acquired and a native penicillin-binding protein cooperate in building the cell wall of drug-resistant staphylococci. Proc. Natl. Acad. Sci. USA 98: 10886– 10891.
69. Pinho, M. G.,, S. Filipe,, H. de Lencastre,, and A. Tomasz. 2001. Complementation of the essential peptidoglycan transpeptidase function of penicillin-binding protein (PBP) 2 by the drug resistance protein PBP2A in Staphylococcus aureus. J. Bacteriol. 183: 6525– 6531.
70. Pucci, M. J.,, J. A. Thanassi,, L. F. Discotto,, R. E. Kessler,, and T. J. Dougherty. 1998. Identification and characterization of cell wall-cell division gene clusters in pathogenic gram-positive cocci. J. Bacteriol. 179: 5632– 5635.
71. Rohrer, S.,, and B. Berger-Bachi. 2003. Application of a bacterial two-hybrid system for the analysis of protein-protein interactions between FemABX family proteins. Microbiology 149: 2733– 2738.
72. Rohrer, S.,, H. Maki,, and B. Berger-Bachi. 2003. What makes resistance to methicillin heterogeneous? J. Med. Microbiol. 52: 605.
73. Rohrer, S.,, and B. Berger-Bachi. 2003. FemABX peptidyl transferases: a link between branched-chain cell wall peptide formation and beta-lactam resistance in gram-positive cocci. Antimicrob. Agents Chemother. 47: 837– 846.
74. Rohrer, S.,, K. Ehlert,, M. Tschierske,, H. Labischinski,, and B. Berger-Bachi. 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.
75. Sau, S.,, N. Bhasin,, E. R. Wann,, J. C. Lee,, T. J. Foster,, and C. Y. Lee. 1997. The Staphylococcus aureus allelic genetic loci for serotype 5 and 8 capsule expression contain the type-specific genes flanked by common genes. Microbiology 143: 2395– 2405.
76. Schneider, T.,, M. M. Senn,, B. Berger-Bachi,, A. Tossi,, H. G. Sahl,, and I. Wiedemann. 2004. In vitro assembly of a complete, pentaglycine interpeptide bridge containing cell wall precursor (lipid II-Gly5) of Staphylococcus aureus. Mol. Microbiol. 53: 675– 685.
77. Severin, A.,, K. Tabei,, F. Tenover,, M. Chung,, N. Clarke,, and A. Tomasz. 2004. High level oxacillin and van comycin resistance and altered cell wall composition in Staphylococcus aureus carrying both the staphylococcal mecA gene and the enterococcal vanA gene complex . J. Biol. Chem. 279: 3398– 3407.
78. Severin, A.,, S. W. Wu,, K. Tabei,, and A. Tomasz. 2004. Penicillin-binding protein 2 is essential for the expression of high level vancomycin resistance and cell wall synthesis in vancomycin-resistant S. aureus carrying the enterococcal vanA gene complex. Antimicrob. Agents Chemother. 48: 4566– 4573.
79. Sieradzki, K.,, and A. Tomasz. 1997. Inhibition of cell wall turnover and autolysis by vancomycin in a highly vancomycin-resistant mutant of Staphylococcus aureus. J. Bacteriol. 179: 2557– 2566.
80. Sieradzki, K.,, and A. Tomasz. 1998. Suppression of glycopeptide resistance in a highly teicoplanin resistant mutant of Staphylococcus aureus by transposon inactivation of genes involved in cell wall synthesis. Microb. Drug Resist. 4: 159– 168.
81. Sieradzki, K.,, and A. Tomasz. 1999. Gradual alterations in cell wall structure and metabolism in vancomycin-resistant mutants of Staphylococcus aureus. J. Bacteriol. 181: 7566– 7570.
82. Sieradzki, K.,, and A. Tomasz. 2003. Alterations of cell wall structure and metabolism accompany reduced susceptibility to vancomycin in an isogenic series of clinical isolates of Staphylococcus aureus. J. Bacteriol. 185: 7103– 7110.
83. Sieradzki, K.,, L. Borio,, J. Dick,, and A. Tomasz. 2003. Evolution of VISA strain in vivo: multiple genetic changes in a single lineage of MRSA under the impact of antibiotics administered for chemotherapy. J. Clin. Microbiol. 41: 1687– 1693.
84. Sieradzki, K.,, M. G. Pinho,, and A. Tomasz. 1999. Inactivated pbp4 in highly glycopeptide-resistant laboratory mutants of Staphylococcus aureus. J. Biol. Chem. 274: 18942– 18946.
85. Snowden, M. A.,, and H. R. Perkins. 1990. Peptidoglycan cross-linking in Staphylococcus aureus: an apparent random polymerisation process. Eur. J. Biochem. 191: 373– 377.
86. Sobral, R. G.,, A. M. Ludovice,, S. Gardete,, K. Tabei,, H. de Lencastre,, and A. Tomasz. 2003. Normally functioning murF is essential for the optimal expression of methicillin resistance in Staphylococcus aureus. Microb. Drug Resist. 9: 231– 241.
87. Strandén, A. M.,, K. Ehlert,, H. Labischinski,, and B. Berger-Bächi. 1997. Cell wall monoglycine cross-bridges and methicillin hypersusceptibility in a femAB null mutant of methicillin-resistant Staphylococcus aureus. J. Bacteriol. 179: 9– 16.
88. Timmerman, C. P.,, E. Mattson,, L. Martinez-Martinez,, L. de Graaf,, J. A. G. van Strijp,, V. H. Verbrugh,, J. Verhoef,, and A. Fleer. 1993. Induction of release of tumor necrosis factor from human monocytes by staphylococci and staphylococcal peptidoglycans. Infect. Immun. 61: 4167– 4172.
89. Tomasz, A.,, H. B. Drugeon,, H. M. de Lencastre,, D. Jabes,, L. McDougall,, and J. Bille. 1989. New mechanism for methicillin resistance in Staphylococcus aureus: clinical isolates that lack the PBP 2a gene and contain normal penicillin-binding proteins with modified penicillin-binding capacity. Antimicrob. Agents Chemother. 33: 1869-– 1874.
90. Toney, J. H.,, G. G. Hammond,, B. Leiting,, K.-A. D. Pryor,, J. K. Wu,, G. C. Cuca,, and D. L. Pompliano. 1998. Soluble penicillin-binding protein 2a: β-lactam binding and inhibition of non-β-lactams using a 96-well format. Anal. Biochem. 255: 113– 119.
91. Utaida, S.,, P. M. Dunman,, D. Macapagal,, E. Murphy,, S. J. Projan,, V. K. Singh,, R. K. Jayaswal,, and B. J. Wilkinson. 2003. Genome-wide transcriptional profiling of the response of Staphylococcus aureus to cell-wall-active antibiotics reveals a cell-wall-stress stimulon. Microbiology 149: 2719– 2732.
92. VanNieuwenhze, M. S.,, S. C. Mauldin,, M. Zia-Ebrahimi,, B. E. Winger,, W. J. Hornback,, S. L. Saha,, J. A. Aikins,, and L. C. Blaszczak. 2002. The first total synthesis of lipid II: the final monomeric intermediate in bacterial cell wall biosynthesis. J. Am. Chem. Soc. 124: 3656– 3660.
93. Wada, A.,, and H. Watanabe. 1998. Penicillin-binding protein 1 of Staphylococcus aureus is essential for growth. J. Bacteriol. 180: 2759– 2765.
94. Wray, G. M.,, S. J. Foster,, C. J. Hinds,, and C. Thiemermann. 2001. A cell wall component from pathogenic and non-pathogenic gram-positive bacteria (peptidoglycan) synergises with endotoxin to cause the release of tumour necrosis factor-alpha, nitric oxide production, shock, and multiple organ injury/dysfunction in the rat. Shock 5: 135– 142.
95. Wu, S.,, H. de Lencastre,, A. Sali,, and A. Tomasz. 1996. A phosphoglucomutase-like gene essential for the optimal expression of methicillin resistance in Staphylococcus aureus: molecular cloning and DNA sequencing. Microb. Drug Resist. 2: 277– 286.
96. Wu, S.,, H. de Lencastre,, and A. Tomasz. 1996. Sigma-B, a putative operon encoding alternate sigma factor of Staphylococcus aureus RNA polymerase: molecular cloning and DNA sequencing. J. Bacteriol. 178: 6036– 6042.
97. Xu, N.,, Z.-H. Huang,, B. L. M. de Jonge,, and D. A. Gage. 1997. Structural characterization of peptidoglycan muro-peptides by matrix-assisted laser desorption ionization mass spectrometry and postsource decay analysis. Anal. Biochem. 248: 7– 14.
98. Yamada, S.,, M. Sugai,, H. Komatsuzawa,, S. Nakashima,, T. Oshida,, A. Matsumoto,, and H. Suginaka. 1996. An autolysin ring associated with cell separation of Staphylococcus aureus. J. Bacteriol. 178: 1565– 1571.
99. Zong, Y.,, S. K. Mazmanian,, O. Schneewind,, and S. V. Narayana. 2004. The structure of sortase B, a cysteine transpeptidase that tethers surface protein to the S. aureus cell wall. Structure 12: 105– 112.

Tables

The Staphylococcal Cell Wall
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Citation: Tomasz A. 2006. The Staphylococcal Cell Wall, p 443-455. In Fischetti V, Novick R, Ferretti J, Portnoy D, Rood J (ed), Gram-Positive Pathogens, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816513.ch36
/content/10.1128/9781555816513.chap36.tab36-1
TABLE 1

Structure of muropeptide components in the methicillin-resistant parental strain and its mutant 208

Reproduced with permission from reference .

ND, not determined.

10.1128/9781555816513/tab36-1_thmb.gif
10.1128/9781555816513/tab36-1.gif
Generic image for table
TABLE 1

Structure of muropeptide components in the methicillin-resistant parental strain and its mutant 208

Reproduced with permission from reference .

ND, not determined.

Citation: Tomasz A. 2006. The Staphylococcal Cell Wall, p 443-455. In Fischetti V, Novick R, Ferretti J, Portnoy D, Rood J (ed), Gram-Positive Pathogens, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816513.ch36

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