Abstract
The vancomycin resistance expressed by several strains of Enterococcus gallinarum was studied. Resistance was expressed constitutively, as demonstrated by analysis of growth and inhibition of peptidoglycan synthesis. E. gallinarum strains were moderately resistant to vancomycin (MIC, 16 micrograms/ml) but were as susceptible as vancomycin-susceptible enterococci to the glycopeptides, teicoplanin, A35512B, A47934, A4103A, and A41030E and the glycopeptide actaplanins A1, B2, and C1. Vancomycin resistance in E. gallinarum was inhibited by beta-lactam antibiotics at concentrations that saturated penicillin-binding protein 6 (PBP 6), as demonstrated by binding competition experiments. Spontaneous mutants (frequency, 10(-8)) were two- to fourfold more resistant to beta-lactam inhibition of vancomycin resistance than the parent strain. PBP binding competition experiments suggested that PBP 6 in the mutants bound less cefotaxime, while binding of penicillin and cefoxitin was unaffected. Both a bioassay method and high-performance liquid chromatography showed that E. gallinarum membranes have enzymatic activity which modifies a model pentapeptide yielding a product that is thought to be a tetrapeptide. This activity could be a D,D-carboxypeptidase. In both the parent E. gallinarum strain and its derivatives that were resistant to the synergistic drug combination, the activity was inhibited by beta-lactams at concentrations which correlated with those that inhibit vancomycin resistance and those that saturate PBP 6. These results suggest the possibility that PBP 6 may be involved in the vancomycin resistance of E. gallinarum and that the putative D,D-carboxypeptidase activity seen in E. gallinarum membranes may be attributable to PBP 6.
MeSH Terms
Anti-Bacterial Agents/pharmacology
Bacterial Proteins
Carboxypeptidases/metabolism
Carrier Proteins/metabolism
Cefotaxime/pharmacology
Cefoxitin/pharmacology
Cell Membrane/drug effects,metabolism
Chromatography, High Pressure Liquid
Drug Resistance, Microbial
Enterococcus/drug effects,metabolism
Hexosyltransferases
Microbial Sensitivity Tests
Muramoylpentapeptide Carboxypeptidase/metabolism
Penicillin-Binding Proteins
Peptidyl Transferases
Phenotype
Vancomycin/pharmacology
Chemicals
Anti-Bacterial Agents
Bacterial Proteins
Carrier Proteins
Penicillin-Binding Proteins
Cefoxitin
Vancomycin
Peptidyl Transferases
Hexosyltransferases
Carboxypeptidases
Muramoylpentapeptide Carboxypeptidase
Cefotaxime
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Vincent S
Research Service, Department of Veterans Affairs Medical Center, Case Western Reserve University, Cleveland, Ohio 44106.
Minkler P
Bincziewski B
Etter L
Shlaes D M
References (28)
28 references, click to expand
-
The penicillin-binding proteins in Streptococcus faecalis ATCC 9790.
Eur J Biochem. 1980 Sep;110(2):445-56
PMID: 6777159
-
Taxonomic studies on some group D streptococci.
J Gen Microbiol. 1983 May;129(5):1423-32
PMID: 6413643
-
Self-transferable plasmids determining the hemolysin and bacteriocin of Streptococcus faecalis var. zymogenes.
J Bacteriol. 1975 Mar;121(3):863-72
PMID: 803965
-
Inducible carboxypeptidase activity in vancomycin-resistant enterococci.
Antimicrob Agents Chemother. 1992 Jan;36(1):77-80
PMID: 1534213
-
Sequence of the vanC gene of Enterococcus gallinarum BM4174 encoding a D-alanine:D-alanine ligase-related protein necessary for vancomycin resistance.
Gene. 1992 Mar 1;112(1):53-8
PMID: 1551598
-
Structural relationship between the vancomycin resistance protein VanH and 2-hydroxycarboxylic acid dehydrogenases.
Gene. 1991 Jul 15;103(1):133-4
PMID: 1908809
-
Vancomycin susceptibility and identification of motile enterococci.
J Clin Microbiol. 1991 Oct;29(10):2335-7
PMID: 1939593
-
Identification of vancomycin resistance protein VanA as a D-alanine:D-alanine ligase of altered substrate specificity.
Biochemistry. 1991 Feb 26;30(8):2017-21
PMID: 1998664
-
Synergistic killing of vancomycin-resistant enterococci of classes A, B, and C by combinations of vancomycin, penicillin, and gentamicin.
Antimicrob Agents Chemother. 1991 Apr;35(4):776-9
PMID: 2069388
-
Comparison of vancomycin-inducible proteins from four strains of Enterococci.
FEMS Microbiol Lett. 1990 Jun 15;58(1):101-5
PMID: 2118867
-
Mechanism of resistance to vancomycin in Enterococcus faecium D366 and Enterococcus faecalis A256.
Antimicrob Agents Chemother. 1990 Feb;34(2):252-6
PMID: 2139314
-
The VANA glycopeptide resistance protein is related to D-alanyl-D-alanine ligase cell wall biosynthesis enzymes.
Mol Gen Genet. 1990 Dec;224(3):364-72
PMID: 2266943
-
Different modes of vancomycin and D-alanyl-D-alanine peptidase binding to cell wall peptide and a possible role for the vancomycin resistance protein.
Antimicrob Agents Chemother. 1990 Jul;34(7):1342-7
PMID: 2386365
-
Inducible, transferable resistance to vancomycin in Enterococcus faecalis A256.
Antimicrob Agents Chemother. 1989 Feb;33(2):198-203
PMID: 2497704
-
Inducible, transferable resistance to vancomycin in Enterococcus faecium, D399.
J Antimicrob Chemother. 1989 Apr;23(4):503-8
PMID: 2501270
-
Transferable vancomycin and teicoplanin resistance in Enterococcus faecium.
Antimicrob Agents Chemother. 1989 Jan;33(1):10-5
PMID: 2523687
-
Inducible resistance to vancomycin in Enterococcus faecium D366.
J Infect Dis. 1989 Jun;159(6):1095-104
PMID: 2723455
-
Problems with the disk diffusion test for detection of vancomycin resistance in enterococci.
J Clin Microbiol. 1989 Sep;27(9):2140-2
PMID: 2778080
-
Vancomycin-resistant enterococci.
Lancet. 1988 Jan 2-9;1(8575-6):57-8
PMID: 2891921
-
Plasmid-mediated resistance to vancomycin and teicoplanin in Enterococcus faecium.
N Engl J Med. 1988 Jul 21;319(3):157-61
PMID: 2968517
-
Use of penicillin-binding proteins for the identification of enterococci.
J Gen Microbiol. 1986 Jul;132(7):1929-37
PMID: 3098903
-
Recovery of resistant enterococci during vancomycin prophylaxis.
J Clin Microbiol. 1988 Jun;26(6):1216-8
PMID: 3384933
-
Penicillin-sensitive enzymes in peptidoglycan biosynthesis.
Crit Rev Microbiol. 1985;11(4):299-396
PMID: 3888533
-
Reversal by a specific peptide (diacetyl-alpha gamma-L-diaminobutyryl-D-alanyl-D-alanine) of vancomycin inhibition in intact bacteria and cell-free preparations.
Biochem J. 1972 Jan;126(1):139-49
PMID: 4627581
-
Modifications of the acyl-D-alanyl-D-alanine terminus affecting complex-formation with vancomycin.
Biochem J. 1971 Aug;123(5):789-803
PMID: 5124386
-
Specificity of combination between mucopeptide precursors and vancomycin or ristocetin.
Biochem J. 1969 Jan;111(2):195-205
PMID: 5763787
-
The structure and mode of action of glycopeptide antibiotics of the vancomycin group.
Annu Rev Microbiol. 1984;38:339-57
PMID: 6388496
-
Mutational evidence for identity of penicillin-binding protein 5 in Escherichia coli with the major D-alanine carboxypeptidase IA activity.
J Bacteriol. 1979 Jan;137(1):644-7
PMID: 368033