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Chapter 8 : Glycopeptide Resistance in Enterococci

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Abstract:

This chapter reviews the mode of action and the mechanism of resistance to glycopeptides, as exemplified by the vancomycin A (VanA)-type mediated by transposon Tn1546, which is widely spread in enterococci. Six types of vancomycin-resistant enterococci have been characterized on phenotypic and genotypic bases; five types possess acquired resistance (VanA, B, D, E, and G) and one type, VanC, is an intrinsic property of , , and . Classification of glycopeptide resistance is now based on the primary sequence of the structural genes for the resistance ligases rather than on the levels of resistance to glycopeptides, since the MIC ranges of vancomycin and teicoplanin against the various types overlap. VanA is the most frequently encountered type of glycopeptide resistance in enterococci. An interesting phenomenon that has developed in some VanA- and VanB-type enterococci is vancomycin dependence. Conjugal transfer of plasmids that have acquired Tn1546-like elements by transposition appears to be responsible for the spread of glycopeptide resistance in enterococci. In enterococci, major advances in the understanding of the mechanism of glycopeptide resistance have been achieved. The emergence and dissemination of high-level resistance to glycopeptides in enterococci in the past two decades has resulted in clinical isolates resistant to all antibiotics of proven efficacy. Although enterococci are not highly pathogenic, the incidence of glycopeptide resistance among clinical isolates is increasing and the enterococci have become important as nosocomial pathogens and as a reservoir of resistance genes.

Citation: Depardieu F, Courvalin P. 2005. Glycopeptide Resistance in Enterococci, p 101-123. In White D, Alekshun M, McDermott P (ed), Frontiers in Antimicrobial Resistance. ASM Press, Washington, DC. doi: 10.1128/9781555817572.ch8

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Figures

Image of Figure 1
Figure 1

Schematic representation of peptidoglycan biosynthesis and mode of action of vancomycin. The formation of complexes between the antibiotic and the C-terminal -alanyl--alanine moiety of peptidoglycan precursors prevents transfer of precursors from the lipid carrier to the peptidoglycan by transglycosylation. The reactions catalyzed by transpeptidases and ,-carboxypeptidases are also inhibited.

Citation: Depardieu F, Courvalin P. 2005. Glycopeptide Resistance in Enterococci, p 101-123. In White D, Alekshun M, McDermott P (ed), Frontiers in Antimicrobial Resistance. ASM Press, Washington, DC. doi: 10.1128/9781555817572.ch8
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Image of Figure 2
Figure 2

Interaction between vancomycin and the C-terminal end of peptidoglycan precursors. Binding of vancomycin to the (A) -ala--ala extremity; (B) -ala--Lac extremity (substitution of the NH group by an oxygen prevents the formation of the central hydrogen bond); (C) -ala--Ser extremity (substitution of a CH group by a CHOH group induces steric hindrance to binding).

Citation: Depardieu F, Courvalin P. 2005. Glycopeptide Resistance in Enterococci, p 101-123. In White D, Alekshun M, McDermott P (ed), Frontiers in Antimicrobial Resistance. ASM Press, Washington, DC. doi: 10.1128/9781555817572.ch8
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Image of Figure 3
Figure 3

VanA-type glycopeptide resistance and map of Tn. (A) Schematic representation of the synthesis of peptidoglycan precursors in the VanA-type BM4147 resistant strain. (B) Organization of the operon. Open arrows represent coding sequences and indicate the direction of transcription. Open and closed arrowheads labeled IR and IR indicate the left and right inverted repeats of the transposon. The regulator and and resistance genes , , , , and are cotranscribed from promoters and , respectively.

Citation: Depardieu F, Courvalin P. 2005. Glycopeptide Resistance in Enterococci, p 101-123. In White D, Alekshun M, McDermott P (ed), Frontiers in Antimicrobial Resistance. ASM Press, Washington, DC. doi: 10.1128/9781555817572.ch8
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Image of Figure 4
Figure 4

VanC-type glycopeptide resistance. (A) Organization of the operon. Open arrows represent coding sequences and indicate the direction of transcription. (B) Schematic representation of the synthesis of peptidoglycan precursors in the VanC-type BM4174 strain. Tri, -ala-γ--Glu--Lys.

Citation: Depardieu F, Courvalin P. 2005. Glycopeptide Resistance in Enterococci, p 101-123. In White D, Alekshun M, McDermott P (ed), Frontiers in Antimicrobial Resistance. ASM Press, Washington, DC. doi: 10.1128/9781555817572.ch8
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Figure 5

Comparison of the gene clusters. Open arrows represent coding sequences and indicate the direction of transcription. The guanosine plus cytosine content (% GC) is indicated in the arrows. The percentage of amino acid (aa) identity between the deduced proteins of reference strains BM4147 (VanA) (15), V583 (VanB) (53), BM4339 (VanD) (32), BM4174 (VanC) (4), BM4405 (VanE) (1), and BM4518 (VanG) (42) is indicated under the arrows. Transposon Tn (10851 bp) carries the operon and is delineated by 38-bp imperfect inverted repeats represented by arrowheads (IR and IR). Transposon Tn (65 kb) carries the gene cluster and is delineated by insertion sequences IS-like and IS in direct orientation (represented by boxes). The vertical bar in indicates the frameshift mutation leading to a predicted truncated protein.

Citation: Depardieu F, Courvalin P. 2005. Glycopeptide Resistance in Enterococci, p 101-123. In White D, Alekshun M, McDermott P (ed), Frontiers in Antimicrobial Resistance. ASM Press, Washington, DC. doi: 10.1128/9781555817572.ch8
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Figure 6

VanD-type glycopeptide resistance. (A) Schematic representation of the synthesis of peptidoglycan precursors in a VanD-type resistant strain. (B) Organization of the operon. Open arrows represent coding sequences and indicate the direction of transcription. Regulatory and and resistance genes , , , and are cotranscribed from promoters and , respectively. •, N-acetylmuramic acid; ○, N-acetylglucosamine; tri, -ala-g--Glu--Lys; |, undecaprenylpyrophosphate (lipid carrier).

Citation: Depardieu F, Courvalin P. 2005. Glycopeptide Resistance in Enterococci, p 101-123. In White D, Alekshun M, McDermott P (ed), Frontiers in Antimicrobial Resistance. ASM Press, Washington, DC. doi: 10.1128/9781555817572.ch8
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Figure 7

Schematic representation of the synthesis of peptidoglycan precursors in a vancomycin-dependent strain. Due to inactivation of the indigenous -ala:-ala ligase (Ddl), vancomycin is required in the culture medium to induce expression of the resistance pathway, thus allowing bacterial growth.

Citation: Depardieu F, Courvalin P. 2005. Glycopeptide Resistance in Enterococci, p 101-123. In White D, Alekshun M, McDermott P (ed), Frontiers in Antimicrobial Resistance. ASM Press, Washington, DC. doi: 10.1128/9781555817572.ch8
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Image of Figure 8
Figure 8

Schematic representation of, and regulation by, the VanRS two-component regulatory system. (A) Structure of VanR and VanS proteins. Asp, aspartate; His, histidine; P, phosphate. (B) Model for positive (phosphorylation) and negative (dephosphorylation) control of VanR by VanS.

Citation: Depardieu F, Courvalin P. 2005. Glycopeptide Resistance in Enterococci, p 101-123. In White D, Alekshun M, McDermott P (ed), Frontiers in Antimicrobial Resistance. ASM Press, Washington, DC. doi: 10.1128/9781555817572.ch8
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Image of Figure 9
Figure 9

Schematic representation of the VanS sensor and location of the amino acid substitutions in teicoplanin-resistant mutants. H, N, Gl, F, and G2 refer to the motifs conserved in histidine protein kinases. The putative membrane-associated sensor domain (dotted black) containing transmembrane segments (black) and the putative cytoplasmic kinase domain (white) are indicated. Het, heterogeneously resistant; R, resistant; Vm, vancomycin; Te, teicoplanin.

Citation: Depardieu F, Courvalin P. 2005. Glycopeptide Resistance in Enterococci, p 101-123. In White D, Alekshun M, McDermott P (ed), Frontiers in Antimicrobial Resistance. ASM Press, Washington, DC. doi: 10.1128/9781555817572.ch8
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Figure 10

Phylogenetic tree derived from the alignment of -ala:-ala ligases and related enzymes.

Citation: Depardieu F, Courvalin P. 2005. Glycopeptide Resistance in Enterococci, p 101-123. In White D, Alekshun M, McDermott P (ed), Frontiers in Antimicrobial Resistance. ASM Press, Washington, DC. doi: 10.1128/9781555817572.ch8
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Tables

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Table 1

Glycopeptide resistance in enterococci

Citation: Depardieu F, Courvalin P. 2005. Glycopeptide Resistance in Enterococci, p 101-123. In White D, Alekshun M, McDermott P (ed), Frontiers in Antimicrobial Resistance. ASM Press, Washington, DC. doi: 10.1128/9781555817572.ch8

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