Cell wall composition and decreased autolytic activity and lysostaphin susceptibility of glycopeptide-intermediate Staphylococcus aureus

Antimicrobial Agents and Chemotherapy

Volumn 48, Issue 10, 2004, Pages 3749-3757

  Koehl, Jennifer L ^a,c   Muthaiyan, Arunachalam ^a   Jayaswal, Radheshyam K ^a   Ehlert, Kerstin ^b   Labischinski, Harald ^b   Wilkinson, Brian J ^a  

^a ILLINOIS STATE UNIVERSITY   (United States)

^b BAYER PHARMA AG   (Germany)

^c SAINT VINCENT COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOLYSIN; GLYCOPEPTIDE; LYSOSTAPHIN; PEPTIDOGLYCAN; PHOSPHORUS; TEICHOIC ACID; VANCOMYCIN;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; AUTOLYSIS; BACTERIAL CELL WALL; BACTERIAL STRAIN; BACTERIUM ISOLATE; CELL FUNCTION; CONTROLLED STUDY; CROSS LINKING; DOWN REGULATION; DRUG TOLERANCE; ENZYME ACTIVITY; GENE EXPRESSION; GENETIC TRANSCRIPTION; NONHUMAN; NORTHERN BLOTTING; PHENOTYPE; PRIORITY JOURNAL; PROTEIN STRUCTURE; PURIFICATION; STAPHYLOCOCCUS AUREUS;

ANTI-BACTERIAL AGENTS; BACTERIOLYSIS; BLOTTING, NORTHERN; CELL WALL; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CYTOPLASM; GLYCOPEPTIDES; LYSOSTAPHIN; PEPTIDOGLYCAN; PHOSPHORUS; STAPHYLOCOCCUS AUREUS; TEICHOIC ACIDS; VANCOMYCIN RESISTANCE;

EID: 4644344349     PISSN: 00664804     EISSN: None     Source Type: Journal    
DOI: 10.1128/AAC.48.10.3749-3757.2004     Document Type: Article

References (54)

1. Avison, M. B., P. M. Bennett, R. A. Howe, and T. R. Walsh. 2002. Preliminary analysis of the genetic basis for vancomycin resistance in Staphylococcus aureus strain Mu50. J. Antimicrob. Chemother. 49:255-260.
2. Bayles, K. W. 2003. Are the molecular strategies that control apoptosis conserved in bacteria? Trends Microbiol. 11:306-311.
3. 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.
4. Boyle-Vavra, S., M. Challapalli, and R. S. Daum. 2003. Resistance to autolysis in vancomycin-selected Staphylococcus aureus isolates precedes vancomycin-intermediate resistance. Antimicrob. Agents Chemother. 47: 2036-2039.
5. Boyle-Vavra, S., H. Labischinski, C. C. Ebert, K. Ehlert, and R. S. Daum. 2001. A spectrum of changes in peptidoglycan composition of glycopeptide-intermediate clinical Staphylococcus aureus isolates. Antimicrob. Agents Chemother. 45:280-287.
6. Brunskill, E. W., B. L. de Jonge, and K. W. Bayles. 1997. Staphylococcus aureus scdA gene: a novel locus that affects cell division and morphogenesis. Microbiology 143:2877-2882.
7. Chatterjee, A. N. 1969. Use of bacteriophage-resistant mutants to study the nature of the bacteriophage receptor site of Staphylococcus aureus. J. Bacteriol. 98:519-527.
8. Climo, M. W., K. Ehlert, and G. L. Archer. 2001. Mechanism and suppression of lysostaphin resistance in oxacillin-resistant Staphylococcus aureus. Antimicrob. Agents Chemother. 45:1431-1437.
9. Cui, L., X. Ma, K. Sato, K. Okuma, F. C. Tenover, E. M. Mamizuka, C. G. Gemmell, M. N. Kim, M. C. Ploy, N. E. 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.
10. 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 expression by Staphylococcus aureus Mu50. Antimicrob. Agents Chemother. 44:2276-2285.
11. Daum, R. S., S. Gupta, R. Sabbath, 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.
12. Ehlert, K., M. Tschierske, C. Mon, W. Schröder, and B. Berger-Bächi. 2000. Site-specific serine incorporation by Lif and Epr into positions 3 and 5 of the staphylococcal interpeptide bridge. J. Bacteriol. 182:2635-2638.
13. Foster, S. J. 1995. Molecular characterization and functional analysis of the major autolysin of Staphylococcus aureus 8325-4. J. Bacteriol. 177:5723-5725.
14. Fournier, B., and D. C. Hooper. 2000. A new two-component regulatory system involved in adhesion, autolysis, and extracellular proteolytic activity of Staphylococcus aureus. J. Bacteriol. 182:3955-3964.
15. 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.
16. Gustafson, J., B. Berger-Bächi, A. Strassle, and B. J. Wilkinson. 1992. Autolysis of methicillin-resistant and -susceptible Staphylococcus aureus. Antimicrob. Agents Chemother. 36:566-572.
17. Gustafson, J. E., F. G. O'Brien, G. W. Coombs, M. J. Malkowski, W. B. Grubb, R. F. Pfeltz, and B. J. Wilkinson. 2003. Alterations in phage-typing patterns in vancomycin-intermediate Staphylococcus aureus. J. Med. Microbiol. 52:1-4.
18. Groicher, K. H., B. A. Firek, D. F. Fujimoto, and K. W. Bayles. 2000. The Staphylococcus aureus lrgAB operon modulates murein hydrolase activity and penicillin tolerance. J. Bacteriol. 182:1794-1801.
19. Hanaki, H., K. Kuwahara-Arai, S. Boyle-Vavra, R. S. Daum, H. Labischinski, and K. Hiramatsu. 1998. Activated cell-wall synthesis is associated with vancomycin resistance in methicillin-resistant Staphylococcus aureus clinical strains Mu3 and Mu50. J. Antimicrob. Chemother. 42:199-209.
20. Hanaki, H., H. Labischinski, V. 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.
21. Hiramatsu, K. 1998. Vancomycin resistance in staphylococci. Drug Resist. Updates 1:135-150.
22. Hiramatsu, K. 2001. Vancomycin-resistant Staphylococcus aureus: a new model of antibiotic resistance. Lancet Infect. Dis. 1:147-155.
23. Hiramatsu, K., H. Hanaki, T. Ino, K. Yabuta, T. Oguri, and F. C. Tenover. 1997. Methicillin-resistant Staphylococcus aureus clinical strain with reduced vancomycin susceptibility. J. Antimicrob. Chemother. 40:135-136.
24. Huff, E., C. S. Silverman, N. J. Adams, and W. S. Awkard. 1970. Extracellular cell wall lytic enzyme from Staphylococcus aureus: purification and partial characterization. J. Bacteriol. 103:761-769.
25. Ingavale, S. S., W. Van Wauel, and A. L. Cheung. 2003. Characterization of RAT, an autolysis regulator in Staphylococcus aureus. Mol. Microbiol. 48: 1451-1456.
26. Jenni, R., and B. Berger-Bächi. 1998. Teichoic acid content in different lineages of Staphylococcus aureus NCTC8325. Arch. Microbiol. 170:171-178.
27. 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 vancomycin-resistant Staphylococcus aureus mutant. Antimicrob. Agents Chemother. 46: 75-81.
28. 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.
29. Leloir, L. T., and C. E. Gardini. 1957. Characterization of phosphorus compounds by acid lability. Methods Enzymol. 3:840-850.
30. Lewis, K. 2000. Programmed death in bacteria. Microbiol. Mol. Biol. Rev. 64:503-514.
31. Mani, N., P. Tobin, and R. K. Jayaswal. 1993. Isolation and characterization of autolysis-defective mutants of Staphylococcus aureus created by Tn917-lacZ mutagenesis. J. Bacteriol. 185:1493-1499.
32. Mongodin, E., J. Finan, M. W. Climo, A. Rosato, S. Gill, and G. L. Archer. 2003. Microarray transcription analysis of clinical Staphylococcus aureus isolates resistant to vancomycin. J. Bacteriol. 185:4638-4643.
33. Moreira, B., S. Boyle-Vavra, B. L. M. de Jonge, and R. S. Daum. 1997. Increased production of penicillin-binding protein 2, increased detection of other penicillin-binding proteins, and decreased coagulase activity associated with glycopeptide resistance in Staphylococcus aureus. Antimicrob. Agents Chemother. 41:1788-1793.
34. Muthaiyan, A., R. K. Jayaswal, and B. J. Wilkinson. 2004. Intact mutS gene in laboratory-derived and clinical glycopeptide-intermediate Staphylococcus aureus strains. Antimicrob. Agents Chemother. 48:623-625.
35. O'Neill, A. J., and I. Chopra. 2002. Insertional inactivation of mutS in Staphylococcus aureus reveals potential for elevated mutation frequencies, although the prevalence of mutation in clinical isolates is low. J. Antimicrob. Chemother. 50:161-169.
36. 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.
37. Peschel, A., C. Vuong, M. Otto, and F. Götz. 2003. 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.
38. 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.
39. Qoronfleh, M. W., J. E. Gustafson, and B. J. Wilkinson. 1998. Conditions that induce Staphylococcus aureus heat shock proteins also inhibit autolysis. FEMS Microbiol. Lett. 166:103-107.
40. Qoronfleh, M. W., and B. J. Wilkinson. 1986. Effects of growth of methicillin-resistant and -susceptible Staphylococcus aureus in the presence of β-lactams on peptidoglycan structure and susceptibility to lytic enzymes. Antimicrob. Agents Chemother. 29:250-257.
41. Ramadurai, L., and R. K. Jayaswal. 1997. Molecular cloning, sequencing, and expression of lytM, a unique autolytic gene of Staphylococcus aureus. J. Bacteriol. 179:3625-3631.
42. Rice, K. C., B. A. Firek, J. B. Nelson, S. J. Jang, T. G. Patton, and K. W. Bayles. 2003. The Staphylococcus aureus cidAB operon: evaluation of its role in regulation of murein hydrolase activity and penicillin tolerance. J. Bacteriol. 185:2635-2643.
43. Rice, K., R. Peralta, D. Bast, J. de Azavedo, and M. J. McGavin. 2001. Description of Staphylococcus serine protease (ssp) operon in Staphylococcus aureus and nonpolar inactivation of sspA-encoded serine protease. Infect. Immun. 69:159-169.
44. Roos, M., E. Pittenauer, E. Schmid, M. Beyer, B. Reinike, G. Allmaier, and H. Labischinski. 1998. Improved high-performance liquid chromatographic separation of peptidoglycan isolated from various Staphylococcus aureus strains for mass spectrometric characterization. J. Chromatogr. B 705:183-192.
45. Schaaff, F., A. Reipert, and G. Bierbaum. 2002. An elevated mutation frequency favors development of vancomycin resistance in Staphylococcus aureus. Antimicrob. Agents Chemother. 46:3540-3548.
46. 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.
47. 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.
48. 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.
49. 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.
50. Stranden, 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.
51. Sugai, M., T. Fujiwara, H. Komatsuzawa, and H. Suginaka. 1998. Identification and molecular characterization of a gene homologous to epr (endopeptidase resistance gene) in Staphylococcus aureus. J. Bacteriol. 97:837-847.
52. Tomasz, A., A. Albino, and E. Zanati. 1970. Multiple antibiotic resistance in a bacterium with suppressed autolytic system. Nature 227:138-140.
53. Tschierske, M., K. Ehlert, A. M. Stranden, and B. Berger-Bächi. 1997. Lif, the lysostaphin immunity factor, complements FemB in staphylococcal peptidoglycan interpeptide bridge formation. FEMS Microbiol. Lett. 153:261-264.
54. 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.