1887

Abstract

(−)-Epicatechin gallate (ECg), a component of green tea, sensitizes meticillin-resistant (MRSA) to -lactam antibiotics, promotes staphylococcal cell aggregation and increases cell-wall thickness. The potentiation of -lactam activity against MRSA by ECg was not due to decreased bacterial penicillin-binding protein (PBP) 2a expression or ECg binding to peptidoglycan. A 5–10 % reduction in peptidoglycan cross-linking was observed. Reduced cross-linking was insufficient to compromise the integrity of the cell wall and no evidence of PBP2a activity was detected in the muropeptide composition of ECg-grown cells. ECg increased the quantity of autolysins associated with the cell wall, even though the cells were less susceptible to Triton X-100-induced autolysis than cells grown in the absence of ECg. ECg promoted increased lysostaphin resistance that was not due to alteration of the pentaglycine cross-bridge configuration or inhibition of lysostaphin activity. Rather, decreased lysostaphin susceptibility was associated with structural changes to wall teichoic acid (WTA), an acid-labile component of peptidoglycan. ECg also promoted lipoteichoic acid (LTA) release from the cytoplasmic membrane. It is proposed that ECg reduces -lactam resistance in MRSA either by binding to PBPs at sites distinct from the penicillin-binding site or by intercalation into the cytoplasmic membrane, displacing LTA from the phospholipid palisade. Thus, ECg-mediated alterations to the physical nature of the bilayer will elicit structural changes to WTA that result in modulation of the cell-surface properties necessary to maintain the -lactam-resistant phenotype.

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2007-07-01
2022-01-23
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References

  1. Appelbaum P. C. 2006; The emergence of vancomycin-intermediate and vancomycin-resistant Staphylococcus aureus. Clin Microbiol Infect 12 :Suppl. 116–23
    [Google Scholar]
  2. Bera A., Herbert S., Jakob A., Vollmer W., Götz F. 2005; Why are pathogenic staphylococci so lysozyme resistant? The peptidoglycan O-acetyltransferase OatA is the major determinant for lysozyme resistance of Staphylococcus aureus. Mol Microbiol 55:778–787
    [Google Scholar]
  3. Blanco A. R., Sudano-Roccaro A., Spoto G. C., Nostro A., Rusciano D. 2005; Epigallocatechin gallate inhibits biofilm formation by ocular staphylococcal isolates. Antimicrob Agents Chemother 49:4339–4343 [CrossRef]
    [Google Scholar]
  4. Boyle-Vavra S., Carey R. B., Daum R. S. 2001; Development of vancomycin and lysostaphin resistance in a methicillin-resistant Staphylococcus aureus isolate. J Antimicrob Chemother 48:617–625 [CrossRef]
    [Google Scholar]
  5. Caturla N., Vera-Samper E., Villalaín J., Mateo C. R., Micol V. 2003; The relationship between the antioxidant and the antibacterial properties of galloylated catechins and the structure of phospholipid model membranes. Free Radic Biol Med 34:648–662 [CrossRef]
    [Google Scholar]
  6. Centers for Disease Control 2002; Staphylococcus aureus resistant to vancomycin – United States, 2002. MMWR Morbid Mortal Wkly Rep 51:565–567
    [Google Scholar]
  7. Crisóstomo M. I., Westh H., Tomasz A., Chung M., Oliveira D. C., de Lencastre H. 2001; The evolution of methicillin resistance in Staphylococcus aureus : similarity of genetic backgrounds in historically early methicillin-susceptible and -resistant isolates and contemporary epidemic clones. Proc Natl Acad Sci U S A 98:9865–9870 [CrossRef]
    [Google Scholar]
  8. de Jonge B. L. M., Tomasz A. 1993; Abnormal peptidoglycan produced in a methicillin-resistant strain of Staphylococcus aureus grown in the presence of methicillin: functional role for penicillin-binding protein 2A in cell wall synthesis. Antimicrob Agents Chemother 37:342–346 [CrossRef]
    [Google Scholar]
  9. de Jonge B. L. M., de Lancastre H., Tomasz T. 1991; Suppression of autolysis and cell wall turnover in heterogeneous Tn551 mutants of a methicillin-resistant Staphylococcus aureus strain. J Bacteriol 173:1105–1110
    [Google Scholar]
  10. Finan J. E., Archer G. L., Pucci M. J., Climo M. W. 2001; Role of penicillin-binding protein 4 in expression of vancomycin resistance among clinical isolates of oxacillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 45:3070–3075 [CrossRef]
    [Google Scholar]
  11. Fournier B., Hooper D. C. 2000; A new two-component regulatory system involved in adhesion, autolysis, and extracellular proteolytic activity of Staphylococcus aureus. J Bacteriol 182:3955–3964 [CrossRef]
    [Google Scholar]
  12. Hamilton-Miller J. M. T., Shah S. 1999; Disorganization of cell division of methicillin-resistant Staphylococcus aureus by a component of tea ( Camellia sinensis ): a study by electron microscopy. FEMS Microbiol Lett 176:463–469 [CrossRef]
    [Google Scholar]
  13. Hartman B. J., Tomasz A. 1984; Low-affinity penicillin-binding protein associated with beta-lactam resistance in Staphylococcus aureus. J Bacteriol 158:513–516
    [Google Scholar]
  14. Hashimoto T., Kumazawa S., Nanjo F., Hara Y., Nakayama T. 1999; Interaction of tea catechins with lipid bilayers investigated with liposome systems. Biosci Biotechnol Biochem 63:2252–2255 [CrossRef]
    [Google Scholar]
  15. Hiramatsu K., Hanaki H., Ino T., Yabuta K., Oguri T., Tenover F. C. 1997; Methicillin-resistant Staphylococcus aureus clinical strain with reduced vancomycin susceptibility. J Antimicrob Chemother 40:135–136 [CrossRef]
    [Google Scholar]
  16. Kajiya K., Kumazawa S., Nakayama T. 2001; Steric effects on interaction of tea catechins with lipid bilayers. Biosci Biotechnol Biochem 65:2638–2643 [CrossRef]
    [Google Scholar]
  17. Kajiya K., Kumazawa S., Nakayama T. 2002; Effects of external factors on the interaction of tea catechins with lipid bilayers. Biosci Biotechnol Biochem 66:2330–2335 [CrossRef]
    [Google Scholar]
  18. Koehl J. L., Muthaiyan A., Jayaswal R. K., Ehlert K., Labischinski H., Wilkinson B. 2004; Cell wall composition and decreased autolytic activity and lysostaphin susceptibility of glycopeptide-intermediate Staphylococcus aureus. Antimicrob Agents Chemother 48:3749–3757 [CrossRef]
    [Google Scholar]
  19. Leloir L. F., Cardini C. E. 1957; Characterization of phosphorus compound by acid lability. Methods Enzymol 3:840–850
    [Google Scholar]
  20. Łęski T. A., Tomasz A. 2005; Role of penicillin-binding protein 2 (PBP2) in the antibiotic susceptibility and cell wall cross-linking of Staphylococcus aureus : evidence for the cooperative functioning of PBP2, PBP4 and PBP2A. J Bacteriol 187:1815–1824 [CrossRef]
    [Google Scholar]
  21. Miller L. A., Ratnam K., Payne D. J. 2001; Beta-lactamase-inhibitor combinations in the 21st century: current agents and new developments. Curr Opin Pharmacol 1:451–458 [CrossRef]
    [Google Scholar]
  22. Ohta K., Komatsuzawa H., Sugai M., Suginaka H. 2000; Triton X-100-induced lipoteichoic acid release is correlated with the methicillin resistance in Staphylococcus aureus. FEMS Microbiol Lett 182:77–79 [CrossRef]
    [Google Scholar]
  23. Peschel A., Vuong C., Otto M., Götz F. 2000; The d-alanine residues of Staphylococcus aureus teichoic acids alter the susceptibility to vancomycin and the activity of autolytic enzymes. Antimicrob Agents Chemother 44:2845–2847 [CrossRef]
    [Google Scholar]
  24. Pinho M. G., Tomasz A., de Lencastre H. 2000; Cloning, characterization, and inactivation of the gene pbpC , encoding penicillin-binding protein 3 of Staphylococcus aureus. J Bacteriol 182:1074–1079 [CrossRef]
    [Google Scholar]
  25. Raychaudhuri D., Chatterjee A. N. 1985; Use of resistant mutants to study the interaction of Triton X-100 with Staphylococcus aureus. J Bacteriol 164:1337–1349
    [Google Scholar]
  26. Raynor R. H., Scott D. F., Best G. K. 1979; Oxacillin-induced lysis of Staphylococcus aureus. Antimicrob Agents Chemother 16:134–140 [CrossRef]
    [Google Scholar]
  27. Roos M., Pittenauer E., Schmid E., Beyer M., Reinike B., Allmaier G., Labischinski H. 1998; Improved high-performance liquid chromatographic separation of peptidoglycan isolated from various Staphylococcus aureus strains for mass spectrometric characterization. J Chromatogr B Biomed Sci Appl 705:183–192 [CrossRef]
    [Google Scholar]
  28. Shiota S., Shimizu M., Mizushima T., Ito H., Hatano T., Yoshida T., Tsuchiya T. 1999; Marked reduction in the minimum inhibitory concentration (MIC) of beta-lactams in methicillin-resistant Staphylococcus aureus produced by epicatechin gallate, an ingredient of green tea ( Camellia sinensis ). Biol Pharm Bull 22:1388–1390 [CrossRef]
    [Google Scholar]
  29. Shirai C., Sugai M., Komatsuzawa H., Ohta K., Yamakido M., Suginaka H. 1998; A triazine dye, cibacron blue F3GA, decreases oxacillin resistance levels in methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 42:1278–1280
    [Google Scholar]
  30. Sieradzki K., Tomasz A. 1996; A highly vancomycin-resistant laboratory mutant of Staphylococcus aureus. FEMS Microbiol Lett 142:161–166 [CrossRef]
    [Google Scholar]
  31. Sieradzki K., Tomasz A. 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 [CrossRef]
    [Google Scholar]
  32. Sieradzki K., Pinho M. G., Tomasz A. 1999; Inactivated pbp4 in highly glycopeptide-resistant laboratory mutants of Staphylococcus aureus. J Biol Chem 274:18942–18946 [CrossRef]
    [Google Scholar]
  33. Stapleton P. D., Taylor P. W. 2002; Methicillin resistance in Staphylococcus aureus : mechanisms and modulation. Sci Prog 85:57–72 [CrossRef]
    [Google Scholar]
  34. Stapleton P. D., Shah S., Anderson J. C., Hara Y., Hamilton-Miller J. M. T., Taylor P. W. 2004; Modulation of beta-lactam resistance in Staphylococcus aureus by catechins and gallates. Int J Antimicrob Agents 23:462–467 [CrossRef]
    [Google Scholar]
  35. Stapleton P. D., Shah S., Hara Y., Taylor P. W. 2006; Potentiation of catechin gallate-mediated sensitization of Staphylococcus aureus to oxacillin by nongalloylated catechins. Antimicrob Agents Chemother 50:752–755 [CrossRef]
    [Google Scholar]
  36. Stranden A. M., Ehlert K., Labischinski H., Berger-Bächi B. 1997; Cell wall monoglycine cross-bridges and methicillin hypersusceptibility in a femAB null mutant of methicillin-resistant Staphylococcus aureus. J Bacteriol 179:9–16
    [Google Scholar]
  37. Sugai M., Akiyama T., Komatsuzawa H., Miyake Y., Suginaka H. 1990; Characterization of sodium dodecyl sulfate-stable Staphylococcus aureus bacteriolytic enzymes by polyacrylamide gel electrophoresis. J Bacteriol 172:6494–6498
    [Google Scholar]
  38. Sugai M., Komatsuzawa H., Akiyama T., Hong Y.-M., Oshida T., Miyake Y., Yamaguchi T., Suginaka H. 1995; Identification of endo- β - N -acetylglucosaminidase and N -acetylmuramyl-l-alanine amidase as cluster-dispersing enzymes in Staphylococcus aureus. J Bacteriol 177:1491–1496
    [Google Scholar]
  39. Suzuki J., Komatsuzawa H., Sugai M., Ohta K., Kozai K., Nagasaka N., Suginaka H. 1997; Effects of various types of triton X on the susceptibilities of methicillin-resistant staphylococci to oxacillin. FEMS Microbiol Lett 153:327–331 [CrossRef]
    [Google Scholar]
  40. Taylor P. W., Stapleton P. D., Paul Luzio J. 2002; New ways to treat bacterial infections. Drug Discov Today 7:1086–1091 [CrossRef]
    [Google Scholar]
  41. van Langevelde P., van Dissel J. T., Ravensbergen E., Applemelk B. J., Schrijver I. A., Groeneveld P. H. P. 1998; Antibiotic-induced release of lipoteichoic acid and peptidoglycan from Staphylococcus aureus : quantitative measurements and biological reactivities. Antimicrob Agents Chemother 42:3073–3078
    [Google Scholar]
  42. Wootton M., Bennett P. M., MacGowan A. P., Walsh T. R. 2005; Reduced expression of the atl autolysin gene and susceptibility to autolysis in clinical heterogeneous glycopeptide-intermediate Staphylococcus aureus (hGISA) and GISA strains. J Antimicrob Chemother 56:944–947 [CrossRef]
    [Google Scholar]
  43. Yam T. S., Hamilton-Miller J. M. T., Shah S. 1998; The effect of a component of tea ( Camellia sinensis ) on methicillin resistance, PBP2′ synthesis, and β -lactamase production in Staphylococcus aureus. J Antimicrob Chemother 42:211–216 [CrossRef]
    [Google Scholar]
  44. Zhao W.-H., Hu Z.-Q., Okubo S., Hara Y., Shimamura T. 2001; Mechanism of synergy between epigallocatechin gallate and beta-lactams against methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 45:1737–1742 [CrossRef]
    [Google Scholar]
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