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Vancomycin Resistance in Enterococci cm7509.qxd 05/03/2000 09:02 Page R109 Review R109 Vancomycin resistance in enterococci: reprogramming of the D-Ala–D-Ala ligases in bacterial peptidoglycan biosynthesis Vicki L Healy1, Ivan AD Lessard2, David I Roper3, James R Knox4 and Christopher T Walsh1 Vancomycin binds to bacterial cell-wall intermediates to achieve Introduction its antibiotic effect. Infections of vancomycin-resistant Vancomycin belongs to the glycopeptide class of anti- enterococci are, however, becoming an increasing problem; the biotics, which are effective against gram-positive organ- bacteria are resistant because they synthesize different cell-wall isms. In contrast, gram-negative bacteria are intrinsically intermediates. The enzymes involved in cell-wall biosynthesis, resistant to glycopeptides because of their impermeable therefore, are potential targets for combating this resistance. outer membrane. Glycopeptides are composed of a hepta- Recent biochemical and crystallographic results are providing peptide backbone that is substituted with five to seven mechanistic and structural details about some of these targets. aromatic rings and different sugars. Vancomycin contains two hexoses and five aromatic rings; chloroeremomycin has Addresses: 1Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, 240 Longwood Avenue, an additional sugar molecule (Figure 1a,b). A second gly- Boston, MA 02115, USA. 2Boehringer Ingelheim (Canada) Ltée, copeptide antibiotic approved for human use, teicoplanin, Bio-Méga division recherche, 2100 rue Cunard, Laval, Québec, H7S contains three sugars and seven aromatic rings (Figure 1c). 2G5, Canada. 3Department of Chemistry, The University of York, 4 Heslington, York, YO10 5DD, UK. Department of Molecular and Cell In contrast to penicillin, which directly binds to and Biology, University of Connecticut, Storrs, CT 06269, USA. inhibits the bifunctional transglycosylases/transpeptidases Correspondence: Christopher T Walsh involved in cell-wall biosynthesis, vancomycin binds to E-mail: [email protected] the substrate of these enzymes, the D-alanyl–D-alanine Chemistry & Biology 2000, 7:R109–R119 (D-Ala–D-Ala) terminus of the lipid-PP-disaccharide-pen- tapeptide (Figure 2a). Binding of vancomycin to this 1074-5521/00/$ – see front matter target is thought to sterically prevent the subsequent © 2000 Elsevier Science Ltd. All rights reserved. action of both activities of the transglycosylase/transpepti- View metadata, citation and similar papers at core.ac.uk dase: adding disaccharyl pentapeptide units to the brought to you by CORE growing peptidoglycan (PG) strand and then cross-linking provided by Elsevier - Publisher Connector peptides within and between PG strands on the external face of the cytoplasmic membrane (Figure 2b). This failure to form cross-links between peptidoglycan inter- mediates lowers the rigidity of the cell wall and renders these bacteria susceptible to osmotic lysis [1–5]. During the past decade, vancomycin has become the front-line therapy for treating problematic infections caused by methicillin-resistant Staphylococcus aureus (MRSA), and by enterococci in patients after surgery. The specter of vancomycin-resistant MRSA looms [6–9], whereas vancomycin-resistant enterococci (VRE), which cause high mortality rates, have become a distressingly common reality in hospital settings [10,11]. Three VRE phenotypes have been designated VanA, VanB and VanC on the basis of the minimal inhibitory concentration (MIC) in VRE and susceptibility to teicoplanin (Table 1) [3,11]. The VanA and VanB phenotypes differ in that VanA is resistant to teicoplanin, whereas VanB is not resis- tant because the VanB resistance pathway is not activated by teicoplanin (MIC ≤ 0.5 µg/ml) [3]. Both phenotypes are the result of the incorporation into cell-wall intermediates of a D-alanyl–D-lactate (D-Ala–D-Lac) depsipeptide syn- thesized by the VanA or VanB ligase in place of the usual D-Ala–D-Ala dipeptide. Vancomycin binds with a three orders of magnitude lower affinity to D-Ala–D-Lac termini cm7509.qxd 05/03/2000 09:02 Page R110 R110 Chemistry & Biology 2000, Vol 7 No 5 Figure 1 Structure of glycopeptide antibiotics. (a) (b) (a) (b) H N OH H N OH Vancomycin. Chloroeremomycin. HO 2 OH HO 2 OH O O (c) Teicoplanin. H3C O CH2OH H3C O CH2OH O HO O CH3 CH3 O Cl O Cl O O H2N O O O HO H O H H Cl H Cl H N O OH H N O OH H H O H H H O H O H O H N NH O H N NH O H N N N N NH H O H O NH H O H O H H HO H H3CN HO H H3CN NH2 H H CH3 NH2 H H CH3 O O O O H CH3 H CH3 HO OHOH HO OHOH (c) OHOH O CH2OH N O O Cl H NHCOCH O O HO 3 HO O O HO H Cl H N O H O O H H O H N HN NH H O HN NH H O - H H + O N H3 O HO HO O HO O OH O OH OH HO CH OH 2 Chemistry & Biology than to D-Ala–D-Ala termini (Figure 2a), and thus is less family. The D-Ala–D-Ala and D-Ala–D-Ser ligase (VanC) able to sterically block the transpeptidation and trans- families also have similar sequences for the projected glycosylation steps necessary for the formation of the pep- omega loop that closes over the active site of DdlB and the tidoglycan cell wall [12]. loop contains Lys215 and Tyr216 (DdlB numbering), which are important for catalysis (discussed further in the In contrast to the VanA and VanB phenotypes, VanC resis- next section) [17,18,20]. Of the two D-Ala–D-Lac ligase tance in Enterococcus gallinarum and E. casseliflavus is chro- families, the one represented by the Leuconostoc mesen- mosomal, and has only been detected in a few clinical teroides ligase (LmDdl2) has a comparable omega loop, isolates [11,13]. VanC resistance has a VanC D-alanyl– whereas the second, represented by the VanA and VanB D-serine (D-Ala–D-Ser) ligase in place of the D-Ala–D-Lac ligases and the DdlM from the glycopeptide antibiotic pro- ligases (VanA and VanB). The hydroxymethyl sidechain of ducer Streptomyces toyocaensis, has a strikingly different D-serine is thought to disrupt sterically the optimal geom- sequence of residues for the putative omega loop. The gain etry for vancomycin binding to the usual D-Ala–D-Ala of function to make the D-Ala–D-Lac depsipeptide is the termini, resulting in about a sixfold decrease in affinity for key molecular switch that reprograms the VanA and VanB vancomycin [14] and a corresponding eightfold increase in type VRE to produce a vancomycin-resistant cell wall. the MIC for vancomycin (Table 1) [11]. VanD [15] and VanE [16] clinical phenotypes have been described E. coli DdlB as D-Ala–D-Ala ligase prototype recently, but are not yet completely characterized. Until recently, the only available X-ray structure of a D-Ala–D-X ligase superfamily member has been that of D-Ala–D-X ligase superfamily the D-Ala–D-Ala ligase from E. coli (DdlB) with bound Homology analysis of the D-Ala–D-X (where X = alanine, ADP and a phosphorylated D-Ala–D-Ala phosphinate serine or lactate) superfamily of bacterial ligases revealed transition-state inhibitor (Figure 4a,b) [19]. DdlB belongs five constituent families: two that are D-Ala–D-Ala ligases to the ATP-grasp superfamily of enzymes that have an physiologically, two that are D-Ala–D-Lac ligases and one unusual nucleotide-binding fold [21–24]. All of these D-Ala–D-Ser ligase family (Figure 3) [17]. Many of the ATP-grasp enzymes hydrolyze ATP to ADP and inor- residues shown by site-directed mutagenesis [18] and ganic phosphate and ligate one substrate with a carboxy- structural studies [19] to be important for substrate binding late to a second substrate with a primary amine, secondary and catalysis by the Escherichia coli D-Ala-D-Ala ligase amine, hydroxyl or thiol [25]. The catalytic mechanism of (DdlB) are highly conserved among the entire Ddl super- these enzymes is also thought to include formation of an cm7509.qxd 05/03/2000 09:02 Page R111 Review Vancomycin resistance in enterococci Healy et al. R111 Figure 2 Mode of action of vancomycin. (a) Binding of (a) OH OH vancomycin to D-Ala–D-Ala and D-Ala–D-Lac Me Me O O peptidoglycan termini. (b) Inhibition of NH2 NH2 HO O Me HO O Me transglycosylation and transpeptidation steps O O HOCH2 HOCH2 in cell-wall biosynthesis by vancomycin. HO O HO O Cl Cl O O O O Cl Cl HO OH HO OH H O H O H O H O N H O N H O N H Me N H Me O H N O H N H N H N H H N + H H N + H NH O H NH2 H NH O H NH2 – – O 2C H O O 2C H O O O HO NH2 HO NH2 OH OH HO HO O– O– O H O N O O O N N H H R O R O N-acyl-D-Ala–D-Ala N-acyl-D-Ala–D-Lac (b) D-Ala D-Ala HO Transpeptidase L-Lys •• D-Glu O L-Ala • • NH2 NH NH O Ac HO NH O Ac HO NH Transglycosylase O O O HO HO O PO2 O PO2 O Cell membrane 11 Precursors lipid II disaccharide-pentapeptide Chemistry & Biology activated acyl phosphate intermediate that is nucleophili- enzymes (Figure 4b) [19]. The first loop connects two cally attacked by the second substrate [26–29] (Figure 5). β strands and contains Glu148–Gly–Ser–Ser–Val–Gly.
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