Why are pathogenic staphylococci so lysozyme resistant? The peptidoglycan O-acetyltransferase OatA is the major determinant for lysozyme resistance of Staphylococcus aureus

Molecular Microbiology

Volumn 55, Issue 3, 2005, Pages 778-787

  Bera, Agnieszka ^a   Herbert, Silvia ^a   Jakob, Andreas ^a   Vollmer, Waldemar ^a   Götz, Friedrich ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACYLTRANSFERASE; LYSOZYME; PEPTIDOGLYCAN; PEPTIDOGLYCAN O ACETYLTRANSFERASE; UNCLASSIFIED DRUG;

ACETYLATION; ARTICLE; BACTERIAL CELL WALL; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; DELETION MUTANT; ELECTROSPRAY MASS SPECTROMETRY; GENE FUNCTION; GENE IDENTIFICATION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; NONHUMAN; OATA GENE; PRIORITY JOURNAL; PROTEIN MODIFICATION; STAPHYLOCOCCUS AUREUS; TANDEM MASS SPECTROMETRY; WILD TYPE;

ACETYLATION; ACETYLTRANSFERASES; ANIMALS; DRUG RESISTANCE, BACTERIAL; GENE DELETION; HUMANS; MURAMIDASE; PEPTIDOGLYCAN; STAPHYLOCOCCUS AUREUS;

ANIMALIA; BACTERIA (MICROORGANISMS); POSIBACTERIA; STAPHYLOCOCCUS; STAPHYLOCOCCUS AUREUS;

EID: 13444282403     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2004.04446.x     Document Type: Article

References (40)

1. Abrams, A. (1958) O-acetyl groups in the cell wall of Streptococcus faecalis. J Biol Chem 230: 949-959.
2. Antignac, A., Rousselle, U.C., Namane, A., Labigne, A., Taha, M.K., and Boneca, I.G. (2003) Detailed structural analysis of the peptidoglycan of the human pathogen Neisseria meningitidis. J Biol Chem 278: 31521-31528.
3. Araki, Y., Nakatani, T., Nakayama, K., and Ito, E. (1972) Occurrence of N-nonsubstituted glucosamine residues in peptidoglycan of lysozyme-resistant cell walls from Bacillus cereus. J Biol Chem 247: 6312-6322.
4. Augustin, J., and Gotz, F. (1990) Transformation of Staphylococcus epidermidis and other staphylococcal species with plasmid DNA by electroporation. FEMS Microbiol Lett 54: 203-207.
5. Blake, C.C., Koenig, D.F., Mair, G.A., North, A.C., Phillips, D.C., and Sarma, V.R. (1965) Structure of hen egg-white lysozyme. A three-dimensional Fourier synthesis at 2 Angstrom resolution. Nature 206: 757-761.
6. Blake, C.C., Johnson, L.N., Mair, G.A., North, A.C., Phillips, D.C., and Sarma, V.R. (1967) Crystallographic studies of the activity of hen egg-white lysozyme. Proc R Soc Lond B Biol Sci 167: 378-388.
7. Blundell, J.K., and Perkins, H.R. (1985) The peptidoglycan of Neisseria gonorrhoeae, with or without O-acetyl groups, contains anhydro-muramyl residues. J General Microbiol 131: 3397-3400.
8. Bruckner, R. (1997) Gene replacement in Staphylococcus carnosus and Staphylococcus xylosus. FEMS Microbiol Lett 151: 1-8.
9. Brumfitt, W. (1959) The mechanism of development of resistance to lysozyme by some gram-positive bacteria and its results. Br J Exp Pathol 40: 441-451.
10. Brumfitt, W., Wardlaw, A.C., and Park, J.T. (1958) Development of lysozyme-resistance in Micrococcus lysodiekticus and its association with an increased O-acetyl content of the cell wall. Nature 181: 1783-1784.
11. Clarke, A.J. (1993) Extent of peptidoglycan O-acetylation in the tribe Proteeae. J Bacteriol 175: 4550-4553.
12. Clarke, A.J., and Dupont, C. (1991) O-acetylated peptidoglycan: its occurrence, pathobiological significance, and biosynthesis. Can J Microbiol 38: 85-91.
13. Cramton, S.E., Gerke, C., and Götz, F. (2001) In vitro methods to study staphylococcal biofilm formation. Methods Enzymol 336: 239-255.
14. Dupont, C., and Clarke, A.J. (1991) Evidence for N-O acetyl migration as the mechanism for O-acetylation of peptidoglycan in Proteus mirabilis. J Bacteriol 173: 4318-4324.
15. von Eiff, C., Becker, K., Machka, K., Stammer, H., and Peters, G. (2001) Nasal carriage as a source of Staphylococcus aureus bacteremia. Study Group. N Engl J Med 344:11-16.
16. Fahlgren, A., Hammarstrom, S., Danielsson, A., and Hammarstrom, M.L. (2003) Increased expression of antimicrobial peptides and lysozyme in colonie epithelial cells of patients with ulcerative colitis. Clin Exp Immunol 131: 90-101.
17. Feng, W.Y., Chan, K.K., and Covey, J.M. (2002) Electrospray LC-MS/MS quantitation, stability, and preliminary pharmacokinetics of bradykinin antagonist polypeptide B201 (NSC 710295) in the mouse. J Pharm Biomed Anal 28: 601-612.
18. Ghuysen, J.M., and Strominger, J.L. (1963) Structure of the cell wall of Staphylococcus aureus, strain Copenhagen. Ii. Separation and structure of disaccharides. Biochemistry 338: 1119-1125.
19. Glauner, B. (1988) Separation and quantification of muropeptides with high-performance liquid chromatography. Anal Biochem 172: 451-464.
20. Götz, F., and Schumacher, B. (1987) Improvements of protoplast transformation in Staphylococcus carnosus. FEMS Microbiol Lett 40: 285-288.
21. Hash, J.H., and Rothlauf, M.V. (1967) The N,O-diacetylmuramidase of Chalaropsis species. I. Purification and crystallization. J Biol Chem 242: 5586-5590.
22. Hayashi, K. (1975) A rapid determination of sodium dodecyl sulfate with methylene blue. Anal Biochem 67: 503-506.
23. lordanescu, S., and Surdeanu, M. (1976) Two restriction and modification systems in Staphylococcus aureus NCTC8325. J Gen Microbiol 96: 277-281.
24. de Jonge, B.L., Chang, Y.S., Gage, D., and Tomasz, A. (1992) Peptidoglycan composition in heterogeneous Tn55i mutants of a methicillin-resistant Staphylococcus aureus strain. J Biol Chem 267: 11255-11259.
25. Keshav, S., Chung, P., Milon, G., and Gordon, S. (1991) Lysozyme is an inducible marker of macrophage activation in murine tissues as demonstrated by in situ hybridization. J Exp Med 174: 1049-1058.
26. Krause, R.M., and McCarty, M. (1961) Studies on the chemical structure of the streptococcal cell wall. I. The identification of a mucopeptide in the cell walls of groups A and A-variant streptococci. J Exp Med 114: 127-140.
27. Kristian, S.A., Lauth, X., Nizet, V., Götz, F., Neumeister, B., Peschel, A., and Landmann, R. (2003) Alanylation of teichoic acids protects Staphylococcus aureus against Toll-like receptor 2-dependent host defense in a mouse tissue cage infection model. J Infect Dis 188: 414-423.
28. Kuroda, M., Ohta, T., Uchiyama, I., Baba, T., Yuzawa, H., Kobayashi, I., et al. (2001) Whole genome sequencing of methicillin-resistant Staphylococcus aureus. Lancet 357: 1225-1240.
29. Liu, Z.Q., Deng, G.M., Foster, S., and Tarkowski, A. (2001) Staphylococcal peptidoglycans induce arthritis. Arthritis Res 3: 375-380.
30. Martin, H.H., and Gmeiner, J. (1979) Modification of peptidoglycan structure by penicillin action in cell walls of Proteus mirabilis. Eur J Biochem 35: 487-495.
31. Peschel, A., Otto, M., Jack, R.W., Kaibacher, H., Jung, G., and Götz, F. (1999) Inactivation of the dlt operon in Staphylococcus aureus confers sensitivity to defensins, protegrins, and other antimicrobial peptides. J Biol Chem 274: 8405-8410.
32. Roxstrom-Lindquist, K., Terenius, O., and Faye, I. (2004) Parasite-specific immune response in adult Drosophila melanogaster: a genomic study. EMBO Rep 5: 207-212.
33. Sandman, K., Losick, R., and Youngman, P. (1987) Genetic analysis of Bacillus subtilis spo mutations generated by Tn917-mediated insertional mutagenesis. Genetics 117: 603-617.
34. Schleifer, K.H. (1975) Chemical structure of the peptidoglycan, its modifiability and relation to the biological activity. Z Immunitatsforsch Exp Klin Immunol 149: 104-117.
35. Staubitz, P., Neumann, H., Schneider, T., Wiedemann, I., and Peschel, A. (2004) MprF-mediated biosynthesis of lysylphosphatidylglycerol, an important determinant in staphylococcal defensin resistance. FEMS Microbiol Lett 231: 67-71.
36. Strominger, J.L., and Ghuysen, J.M. (1967) Mechanisms of enzymatic bacteriolysis. Cell walls of bacteria are solubilized by action of either specific carbohydrases or specific peptidases. Science 156: 213-221.
37. Vocadlo, D.J., Davies, G.J., Laine, R., and Withers, S.G. (2001) Catalysis by hen egg-white lysozyme proceeds via a covalent intermediate. Nature 412: 835-838.
38. Vollmer, W., and Tomasz, A. (2000) The pgdA gene encodes for a peptidoglycan N-acetylglucosamine deacetylase in Streptococcus pneumoniae. J Biol Chem 275: 20496-20501.
39. Weidenmaier, C., Kokal-Kun, J.F., Kristian, S.A., Chanturiya, T., Kalbacher, H., Gross, M., et al. (2004) Role of teichoic acids in Staphylococcus aureus nasal colonization, a major risk factor in nosocomial infections. Nat Med 10: 243-245.
40. Wilm, M., and Mann, M. (1996) Analytical properties of the nanoelectrospray ion source. Anal Chem 68: 1-8.