Presence of UDP-N-acetylmuramyl-hexapeptides and -heptapeptides in Enterococci and Staphylococci After Treatment with Ramoplanin, Tunicamycin, or Vancomycin

Overview

Journal J Bacteriol

Publisher American Society for Microbiology

Specialty Microbiology

Date 1997 Aug 1

PMID 9244253

Citations 10

Authors

D Billot-Klein

D Shlaes

D Bryant

D Bell

R Legrand

L Gutmann

J van Heijenoort

Affiliations

Soon will be listed here.

Abstract

Analyses of the peptidoglycan nucleotide precursor contents of enterococci and staphylococci treated with ramoplanin, tunicamycin, or vancomycin were carried out by high-pressure liquid chromatography coupled with mass spectrometry (MS). In all cases, a sharp increase in the UDP-N-actetylmuramoyl-pentapeptide or -pentadepsipeptide pool was observed. Concomitantly, new peptidoglycan nucleotide peptides of higher molecular masses with hexa- or heptapeptide moieties were identified: UDP-MurNAc-pentapeptide-Asp or pentadepsipeptide-Asp in enterococci and UDP-MurNAc-pentapeptide-Gly or -Ala and UDP-MurNAc-pentapeptide-Gly-Gly or -Ala-Gly in staphylococci. These new compounds are derivatives of normal UDP-MurNAc-pentapeptide or -pentadepsipeptide precursors with the extra amino acid(s) linked to the lysine epsilon-amino group as established by various analytical procedures (MS, MS-MS fragmentation, chemical analysis, and digestion with R39 D,D carboxypeptidase). Except for tunicamycin-treated cells, it was not possible to ascertain whether these unusual nucleotides were formed by direct addition of the amino acids to UDP-MurNAc-pentapeptide (or -pentadepsipeptide) or whether they arose by reverse reactions from lipid I intermediates to which the amino acids had been added.

Citing Articles

Effect of Vancomycin on Cytoplasmic Peptidoglycan Intermediates and Operon mRNA Levels in VanA-Type Vancomycin-Resistant Enterococcus faecium.

Gargvanshi S, Vemula H, Gutheil W J Bacteriol. 2021; 203(16):e0023021.

PMID: 34060906 PMC: 8297532. DOI: 10.1128/JB.00230-21.

Synthesis, 68Ga-radiolabeling, and preliminary in vivo assessment of a depsipeptide-derived compound as a potential PET/CT infection imaging agent.

Mokaleng B, Ebenhan T, Ramesh S, Govender T, Kruger H, Parboosing R Biomed Res Int. 2015; 2015:284354.

PMID: 25699267 PMC: 4324493. DOI: 10.1155/2015/284354.

Lipid intermediates in the biosynthesis of bacterial peptidoglycan.

van Heijenoort J Microbiol Mol Biol Rev. 2007; 71(4):620-35.

PMID: 18063720 PMC: 2168651. DOI: 10.1128/MMBR.00016-07.

Idiosyncratic features in tRNAs participating in bacterial cell wall synthesis.

Villet R, Fonvielle M, Busca P, Chemama M, Maillard A, Hugonnet J Nucleic Acids Res. 2007; 35(20):6870-83.

PMID: 17932062 PMC: 2175331. DOI: 10.1093/nar/gkm778.

Mycobacterial lipid II is composed of a complex mixture of modified muramyl and peptide moieties linked to decaprenyl phosphate.

Mahapatra S, Yagi T, Belisle J, Espinosa B, Hill P, McNeil M J Bacteriol. 2005; 187(8):2747-57.

PMID: 15805521 PMC: 1070386. DOI: 10.1128/JB.187.8.2747-2757.2005.

References

Matsuhashi M, Dietrich C, Strominger J . Incorporation of glycine into the cell wall glycopeptide in Staphylococcus aureus: role of sRNA and lipid intermediates. Proc Natl Acad Sci U S A. 1965; 54(2):587-94. PMC: 219708. DOI: 10.1073/pnas.54.2.587. View

Billot-Klein D, Gutmann L, Sable S, Guittet E, van Heijenoort J . Modification of peptidoglycan precursors is a common feature of the low-level vancomycin-resistant VANB-type Enterococcus D366 and of the naturally glycopeptide-resistant species Lactobacillus casei, Pediococcus pentosaceus, Leuconostoc.... J Bacteriol. 1994; 176(8):2398-405. PMC: 205365. DOI: 10.1128/jb.176.8.2398-2405.1994. View

Staudenbauer W, Strominger J . Activation of D-aspartic acid for incorporation into peptidoglycan. J Biol Chem. 1972; 247(16):5095-102. View

Schleifer K, Kandler O . Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol Rev. 1972; 36(4):407-77. PMC: 408328. DOI: 10.1128/br.36.4.407-477.1972. View

Swenson J, Neuhaus F . Biosynthesis of peptidoglycan in Staphylococcus aureus: incorporation of the Nepsilon-Ala-Lys moiety into the peptide subunit of nascent peptidoglycan. J Bacteriol. 1976; 125(2):626-34. PMC: 236124. DOI: 10.1128/jb.125.2.626-634.1976. View

Flouret B, van Heijenoort J . Cytoplasmic steps of peptidoglycan synthesis in Escherichia coli. J Bacteriol. 1982; 151(3):1109-17. PMC: 220385. DOI: 10.1128/jb.151.3.1109-1117.1982. View

Flouret B, van Heijenoort J . Pool levels of UDP N-acetylglucosamine and UDP N-acetylglucosamine-enolpyruvate in Escherichia coli and correlation with peptidoglycan synthesis. J Bacteriol. 1983; 154(3):1284-90. PMC: 217602. DOI: 10.1128/jb.154.3.1284-1290.1983. View

PALLANZA R, Berti M, Scotti R, Randisi E, Arioli V . A-16686, a new antibiotic from Actinoplanes. II. Biological properties. J Antibiot (Tokyo). 1984; 37(4):318-24. DOI: 10.7164/antibiotics.37.318. View

Ciabatti R, Kettenring J, WINTERS G, Tuan G, Zerilli L, CAVALLERI B . Ramoplanin (A-16686), a new glycolipodepsipeptide antibiotic. III. Structure elucidation. J Antibiot (Tokyo). 1989; 42(2):254-67. DOI: 10.7164/antibiotics.42.254. View

10.

Reynolds P . Structure, biochemistry and mechanism of action of glycopeptide antibiotics. Eur J Clin Microbiol Infect Dis. 1989; 8(11):943-50. DOI: 10.1007/BF01967563. View

11.

Somner E, Reynolds P . Inhibition of peptidoglycan biosynthesis by ramoplanin. Antimicrob Agents Chemother. 1990; 34(3):413-9. PMC: 171607. DOI: 10.1128/AAC.34.3.413. View

12.

Kaatz G, Seo S, Dorman N, Lerner S . Emergence of teicoplanin resistance during therapy of Staphylococcus aureus endocarditis. J Infect Dis. 1990; 162(1):103-8. DOI: 10.1093/infdis/162.1.103. View

13.

Al-Obeid S, Gutmann L, Shlaes D, Williamson R, Collatz E . Comparison of vancomycin-inducible proteins from four strains of Enterococci. FEMS Microbiol Lett. 1990; 58(1):101-5. DOI: 10.1016/0378-1097(90)90110-c. View

14.

Herwaldt L, Boyken L, Pfaller M . In vitro selection of resistance to vancomycin in bloodstream isolates of Staphylococcus haemolyticus and Staphylococcus epidermidis. Eur J Clin Microbiol Infect Dis. 1991; 10(12):1007-12. DOI: 10.1007/BF01984921. View

15.

Gutmann L, Billot-Klein D, Al-Obeid S, Klare I, Francoual S, Collatz E . Inducible carboxypeptidase activity in vancomycin-resistant enterococci. Antimicrob Agents Chemother. 1992; 36(1):77-80. PMC: 189230. DOI: 10.1128/AAC.36.1.77. View

16.

de Jonge B, Chang Y, 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; 267(16):11248-54. View

17.

Billot-Klein D, Gutmann L, Collatz E, van Heijenoort J . Analysis of peptidoglycan precursors in vancomycin-resistant enterococci. Antimicrob Agents Chemother. 1992; 36(7):1487-90. PMC: 191609. DOI: 10.1128/AAC.36.7.1487. View

18.

Messer J, Reynolds P . Modified peptidoglycan precursors produced by glycopeptide-resistant enterococci. FEMS Microbiol Lett. 1992; 73(1-2):195-200. DOI: 10.1016/0378-1097(92)90608-q. View

19.

Handwerger S, Pucci M, Volk K, Liu J, Lee M . The cytoplasmic peptidoglycan precursor of vancomycin-resistant Enterococcus faecalis terminates in lactate. J Bacteriol. 1992; 174(18):5982-4. PMC: 207137. DOI: 10.1128/jb.174.18.5982-5984.1992. View

20.

Allen N, Hobbs Jr J, Richardson J, Riggin R . Biosynthesis of modified peptidoglycan precursors by vancomycin-resistant Enterococcus faecium. FEMS Microbiol Lett. 1992; 77(1-3):109-15. DOI: 10.1016/0378-1097(92)90140-j. View