Abstract
The muropeptide compositions of isogenic vancomycin-resistant and -susceptible Enterococcus faecalis strains were analyzed by reverse-phase high-performance liquid chromatography combined with amino acid analysis and fast atom bombardment mass spectrometry. Peptidoglycan of the susceptible strain contained pentapeptides as stem peptides, whereas peptidoglycan of the isogenic resistant strain was composed of muropeptides with tetrapeptide stem peptides. Despite the synthesis of lactate-terminating peptidoglycan precursors, no lactate-containing muropeptides were detected in peptidoglycan of the resistant strain. These findings indicate that either lactate-terminating precursors are not incorporated into peptidoglycan of the resistant strain or that the lactate residues are removed from peptidoglycan during synthesis.
Full Text
The Full Text of this article is available as a PDF (214.0 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Adam M., Damblon C., Plaitin B., Christiaens L., Frère J. M. Chromogenic depsipeptide substrates for beta-lactamases and penicillin-sensitive DD-peptidases. Biochem J. 1990 Sep 1;270(2):525–529. doi: 10.1042/bj2700525. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Allen N. E., Hobbs J. N., Jr, Richardson J. M., Riggin R. M. Biosynthesis of modified peptidoglycan precursors by vancomycin-resistant Enterococcus faecium. FEMS Microbiol Lett. 1992 Nov 1;77(1-3):109–115. doi: 10.1016/0378-1097(92)90140-j. [DOI] [PubMed] [Google Scholar]
- Arthur M., Courvalin P. Genetics and mechanisms of glycopeptide resistance in enterococci. Antimicrob Agents Chemother. 1993 Aug;37(8):1563–1571. doi: 10.1128/aac.37.8.1563. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Arthur M., Depardieu F., Snaith H. A., Reynolds P. E., Courvalin P. Contribution of VanY D,D-carboxypeptidase to glycopeptide resistance in Enterococcus faecalis by hydrolysis of peptidoglycan precursors. Antimicrob Agents Chemother. 1994 Sep;38(9):1899–1903. doi: 10.1128/aac.38.9.1899. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Arthur M., Molinas C., Courvalin P. Sequence of the vanY gene required for production of a vancomycin-inducible D,D-carboxypeptidase in Enterococcus faecium BM4147. Gene. 1992 Oct 12;120(1):111–114. doi: 10.1016/0378-1119(92)90017-j. [DOI] [PubMed] [Google Scholar]
- Arthur M., Molinas C., Courvalin P. The VanS-VanR two-component regulatory system controls synthesis of depsipeptide peptidoglycan precursors in Enterococcus faecium BM4147. J Bacteriol. 1992 Apr;174(8):2582–2591. doi: 10.1128/jb.174.8.2582-2591.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Arthur M., Molinas C., Depardieu F., Courvalin P. Characterization of Tn1546, a Tn3-related transposon conferring glycopeptide resistance by synthesis of depsipeptide peptidoglycan precursors in Enterococcus faecium BM4147. J Bacteriol. 1993 Jan;175(1):117–127. doi: 10.1128/jb.175.1.117-127.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bugg T. D., Wright G. D., Dutka-Malen S., Arthur M., Courvalin P., Walsh C. T. Molecular basis for vancomycin resistance in Enterococcus faecium BM4147: biosynthesis of a depsipeptide peptidoglycan precursor by vancomycin resistance proteins VanH and VanA. Biochemistry. 1991 Oct 29;30(43):10408–10415. doi: 10.1021/bi00107a007. [DOI] [PubMed] [Google Scholar]
- Dougherty T. J. Analysis of Neisseria gonorrhoeae peptidoglycan by reverse-phase, high-pressure liquid chromatography. J Bacteriol. 1985 Jul;163(1):69–74. doi: 10.1128/jb.163.1.69-74.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Driehuis F., Wouters J. T. Effect of growth rate and cell shape on the peptidoglycan composition in Escherichia coli. J Bacteriol. 1987 Jan;169(1):97–101. doi: 10.1128/jb.169.1.97-101.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Driehuis F., de Jonge B., Nanninga N. Cross-linkage and cross-linking of peptidoglycan in Escherichia coli: definition, determination, and implications. J Bacteriol. 1992 Mar;174(6):2028–2031. doi: 10.1128/jb.174.6.2028-2031.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fontana R., Cerini R., Longoni P., Grossato A., Canepari P. Identification of a streptococcal penicillin-binding protein that reacts very slowly with penicillin. J Bacteriol. 1983 Sep;155(3):1343–1350. doi: 10.1128/jb.155.3.1343-1350.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Garcia-Bustos J. F., Chait B. T., Tomasz A. Structure of the peptide network of pneumococcal peptidoglycan. J Biol Chem. 1987 Nov 15;262(32):15400–15405. [PubMed] [Google Scholar]
- Glauner B., Höltje J. V., Schwarz U. The composition of the murein of Escherichia coli. J Biol Chem. 1988 Jul 25;263(21):10088–10095. [PubMed] [Google Scholar]
- Gutmann L., Billot-Klein D., al-Obeid S., Klare I., Francoual S., Collatz E., van Heijenoort J. Inducible carboxypeptidase activity in vancomycin-resistant enterococci. Antimicrob Agents Chemother. 1992 Jan;36(1):77–80. doi: 10.1128/aac.36.1.77. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hammes W. P., Kandler O. Biosynthesis of peptidoglycan in Gaffkya homari. The incorporation of peptidoglycan into the cell wall and the direction of transpeptidation. Eur J Biochem. 1976 Nov 1;70(1):97–106. doi: 10.1111/j.1432-1033.1976.tb10960.x. [DOI] [PubMed] [Google Scholar]
- Handwerger S. Alterations in peptidoglycan precursors and vancomycin susceptibility in Tn917 insertion mutants of Enterococcus faecalis 221. Antimicrob Agents Chemother. 1994 Mar;38(3):473–475. doi: 10.1128/aac.38.3.473. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Handwerger S., Pucci M. J., Volk K. J., Liu J., Lee M. S. The cytoplasmic peptidoglycan precursor of vancomycin-resistant Enterococcus faecalis terminates in lactate. J Bacteriol. 1992 Sep;174(18):5982–5984. doi: 10.1128/jb.174.18.5982-5984.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Handwerger S., Skoble J., Discotto L. F., Pucci M. J. Heterogeneity of the vanA gene cluster in clinical isolates of enterococci from the northeastern United States. Antimicrob Agents Chemother. 1995 Feb;39(2):362–368. doi: 10.1128/aac.39.2.362. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Handwerger S., Tomasz A. Alterations in kinetic properties of penicillin-binding proteins of penicillin-resistant Streptococcus pneumoniae. Antimicrob Agents Chemother. 1986 Jul;30(1):57–63. doi: 10.1128/aac.30.1.57. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Johnson A. P., Uttley A. H., Woodford N., George R. C. Resistance to vancomycin and teicoplanin: an emerging clinical problem. Clin Microbiol Rev. 1990 Jul;3(3):280–291. doi: 10.1128/cmr.3.3.280. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kandler O., Schleifer K. H., Dandl R. Differentiation of Streptococcus faecalis Andrewes and Horder and Streptococcus faecium Orla-Jensen based on the amino acid composition of their murein. J Bacteriol. 1968 Dec;96(6):1935–1939. doi: 10.1128/jb.96.6.1935-1939.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Leclercq R., Dutka-Malen S., Brisson-Noël A., Molinas C., Derlot E., Arthur M., Duval J., Courvalin P. Resistance of enterococci to aminoglycosides and glycopeptides. Clin Infect Dis. 1992 Sep;15(3):495–501. doi: 10.1093/clind/15.3.495. [DOI] [PubMed] [Google Scholar]
- Messer J., Reynolds P. E. Modified peptidoglycan precursors produced by glycopeptide-resistant enterococci. FEMS Microbiol Lett. 1992 Jul 1;73(1-2):195–200. doi: 10.1016/0378-1097(92)90608-q. [DOI] [PubMed] [Google Scholar]
- Nieto M., Perkins H. R. Modifications of the acyl-D-alanyl-D-alanine terminus affecting complex-formation with vancomycin. Biochem J. 1971 Aug;123(5):789–803. doi: 10.1042/bj1230789. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ornelas-Soares A., de Lencastre H., de Jonge B., Gage D., Chang Y. S., Tomasz A. The peptidoglycan composition of a Staphylococcus aureus mutant selected for reduced methicillin resistance. J Biol Chem. 1993 Dec 15;268(35):26268–26272. [PubMed] [Google Scholar]
- Pisabarro A. G., de Pedro M. A., Vázquez D. Structural modifications in the peptidoglycan of Escherichia coli associated with changes in the state of growth of the culture. J Bacteriol. 1985 Jan;161(1):238–242. doi: 10.1128/jb.161.1.238-242.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rasmussen J. R., Strominger J. L. Utilization of a depsipeptide substrate for trapping acyl-enzyme intermediates of penicillin-sensitive D-alanine carboxypeptidases. Proc Natl Acad Sci U S A. 1978 Jan;75(1):84–88. doi: 10.1073/pnas.75.1.84. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Reynolds P. E., Depardieu F., Dutka-Malen S., Arthur M., Courvalin P. Glycopeptide resistance mediated by enterococcal transposon Tn1546 requires production of VanX for hydrolysis of D-alanyl-D-alanine. Mol Microbiol. 1994 Sep;13(6):1065–1070. doi: 10.1111/j.1365-2958.1994.tb00497.x. [DOI] [PubMed] [Google Scholar]
- Schleifer K. H., Kandler O. Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol Rev. 1972 Dec;36(4):407–477. doi: 10.1128/br.36.4.407-477.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sheldrick G. M., Jones P. G., Kennard O., Williams D. H., Smith G. A. Structure of vancomycin and its complex with acetyl-D-alanyl-D-alanine. Nature. 1978 Jan 19;271(5642):223–225. doi: 10.1038/271223a0. [DOI] [PubMed] [Google Scholar]
- Tipper D. J., Strominger J. L. 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. 1968 Jun 10;243(11):3169–3179. [PubMed] [Google Scholar]
- Vincent S., Minkler P., Bincziewski B., Etter L., Shlaes D. M. Vancomycin resistance in Enterococcus gallinarum. Antimicrob Agents Chemother. 1992 Jul;36(7):1392–1399. doi: 10.1128/aac.36.7.1392. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Williamson R., Al-Obeid S., Shlaes J. H., Goldstein F. W., Shlaes D. M. Inducible resistance to vancomycin in Enterococcus faecium D366. J Infect Dis. 1989 Jun;159(6):1095–1104. doi: 10.1093/infdis/159.6.1095. [DOI] [PubMed] [Google Scholar]
- Wright G. D., Molinas C., Arthur M., Courvalin P., Walsh C. T. Characterization of vanY, a DD-carboxypeptidase from vancomycin-resistant Enterococcus faecium BM4147. Antimicrob Agents Chemother. 1992 Jul;36(7):1514–1518. doi: 10.1128/aac.36.7.1514. [DOI] [PMC free article] [PubMed] [Google Scholar]
- de Jonge B. L., Chang Y. S., Gage D., Tomasz A. Peptidoglycan composition in heterogeneous Tn551 mutants of a methicillin-resistant Staphylococcus aureus strain. J Biol Chem. 1992 Jun 5;267(16):11255–11259. [PubMed] [Google Scholar]
- de Jonge B. L., Chang Y. S., Gage D., Tomasz A. Peptidoglycan composition of a highly methicillin-resistant Staphylococcus aureus strain. The role of penicillin binding protein 2A. J Biol Chem. 1992 Jun 5;267(16):11248–11254. [PubMed] [Google Scholar]
- de Jonge B. L., Sidow T., Chang Y. S., Labischinski H., Berger-Bachi B., Gage D. A., Tomasz A. Altered muropeptide composition in Staphylococcus aureus strains with an inactivated femA locus. J Bacteriol. 1993 May;175(9):2779–2782. doi: 10.1128/jb.175.9.2779-2782.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]