Aminoacyl-tRNA recognition by the FemXWv transferase for bacterial cell wall synthesis

Nucleic Acids Research

Volumn 37, Issue 5, 2009, Pages 1589-1601

  Fonvielle, Matthieu ^a,b,c   Chemama, Maryline ^b,d   Villet, Régis ^a,b,c   Lecerf, Maxime ^a,b,c   Bouhss, Ahmed ^e,f   Valéry, Jean Marc ^b,d   Ethève Quelquejeu, Mélanie ^b,d   Arthur, Michel ^a,b,c  

^a CENTRE DE RECHERCHE DES CORDELIERS   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d Centre National de la Recherche Scientifique   (France)

^e CNRS   (France)

^f UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; ALANINE TRANSFER RNA; AMINOACYL TRANSFER RNA; GLYCINE; PROTEIN FEMX; SERINE; TRANSFERASE; UNCLASSIFIED DRUG;

AMINOACYLATION; ARTICLE; BACTERIAL CELL WALL; BASE PAIRING; CONTROLLED STUDY; ENTEROCOCCUS FAECALIS; ENZYME ACTIVE SITE; ENZYME MODIFICATION; MOLECULAR INTERACTION; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; RNA SYNTHESIS; RNA TRANSLATION;

ALANINE; BACTERIA; CELL WALL; GLYCINE; NITROGENOUS GROUP TRANSFERASES; RNA, TRANSFER, ALA; RNA, TRANSFER, AMINO ACYL; SERINE; STEREOISOMERISM; SUBSTRATE SPECIFICITY; URIDINE DIPHOSPHATE N-ACETYLMURAMIC ACID;

BACTERIA (MICROORGANISMS);

EID: 63249135046     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkn1039     Document Type: Article

References (51)

1. den Blaauwen,T., de Pedro,M.A., Nguyen-Distèche,M. and Ayala,J.A. (2008) Morphogenesis of rod-shaped sacculi. FEMS Microbiol. Rev., 32, 321-344.
2. Dramsi,S., Magnet,S., Davison,S. and Arthur,M. (2008) Covalent attachment of proteins to peptidoglycan. FEMS Microbiol. Rev., 32, 307-320.
3. Vollmer,W. (2008) Structural variation in the glycan strands of bacterial peptidoglycan. FEMS Microbiol. Rev., 32, 287-306.
4. Kern,T., Hediger,S., Muller,P., Giustini,C., Joris,B., Bougault,C., Vollmer,W. and Simorre,J.P. (2008) Toward the characterization of peptidoglycan structure and protein-peptidoglycan interactions by solid-state NMR spectroscopy. J. Am. Chem. Soc., 130, 5618-5619.
5. Vollmer,W., Blanot,D. and de Pedro,M.A. (2008) Peptidoglycan structure and architecture. FEMS Microbiol. Rev., 32, 149-167.
6. Barreteau,H., Kovac,A., Boniface,A., Sova,M., Gobec,S. and Blanot,D. (2008) Cytoplasmic steps of peptidoglycan biosynthesis. FEMS Microbiol. Rev., 32, 168-207.
7. Schleifer,K.H. and Kandler,O. (1972) Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol. Rev., 36, 407-477.
8. Biarrotte-Sorin,S., Maillard,A.P., Delettre,J., Sougakoff,W., Arthur,M. and Mayer,C. (2004) Crystal structures of Weissella viridescens FemX and its complex with UDP-MurNAcpentapeptide: Insights into FemABX family substrates recognition. Structure, 12, 257-267.
9. Benson,T.E., Prince,D.B., Mutchler,V.T., Curry,K.A., Ho,A.M., Sarver,R.W., Hagadorn,J.C., Choi,G.H. and Garlick,R.L. (2002) Xray crystal structure of Staphylococcus aureus FemA. Structure, 10, 1107-1115.
10. Bellais,S., Arthur,M., Dubost,L., Hugonnet,J.E., Gutmann,L., van Heijenoort,J., Legrand,R., Brouard,J.P., Rice,L. and Mainardi,J.L. (2006) Aslfm, the D-aspartate ligase responsible for the addition of D-aspartic acid onto the peptidoglycan precursor of Enterococcus faecium. J. Biol. Chem., 281, 11586-11594.
11. Sauvage,E., Kerff,F., Terrak,M., Ayala,J.A. and Charlier,P. (2008) The penicillin-binding proteins: Structure and role in peptidoglycan biosynthesis. FEMS Microbiol. Rev., 32, 234-258.
12. Mainardi,J.L., Fourgeaud,M., Hugonnet,J.E., Dubost,L., Brouard,J.P., Ouazzani,J., Rice,L.B., Gutmann,L. and Arthur,M. (2005) A novel peptidoglycan cross-linking enzyme for a betalactam-resistant transpeptidation pathway. J. Biol. Chem., 280, 38146-38152.
13. Lavollay,M., Arthur,M., Fourgeaud,M., Dubost,L., Marie,A., Veziris,N., Blanot,D., Gutmann,L. and Mainardi,J.L. (2008) The peptidoglycan of stationary-phase Mycobacterium tuberculosis predominantly contains cross-links generated by L,D-transpeptidation. J. Bacteriol., 190, 4360-4366.
14. Kopp,U., Roos,M., Wecke,J. and Labischinski,H. (1996) Staphylococcal peptidoglycan interpeptide bridge biosynthesis: A novel antistaphylococcal target? Microb. Drug. Resist., 2, 29-41.
15. Arbeloa,A., Hugonnet,J.E., Sentilhes,A.C., Josseaume,N., Dubost,L., Monsempes,C., Blanot,D., Brouard,J.P. and Arthur,M. (2004) Synthesis of mosaic peptidoglycan cross-bridges by hybrid peptidoglycan assembly pathways in gram-positive bacteria. J. Biol. Chem., 279, 41546-41556.
16. Magnet,S., Arbeloa,A., Mainardi,J.L., Hugonnet,J.E., Fourgeaud,M., Dubost,L., Marie,A., Delfosse,V., Mayer,C., Rice,L.B. et al. (2007) Specificity of L,D-transpeptidases from grampositive bacteria producing different peptidoglycan chemotypes. J. Biol. Chem., 282, 13151-13159.
17. Vollmer,W., Joris,B., Charlier,P. and Foster,S. (2008) Bacterial peptidoglycan (murein) hydrolases. FEMS Microbiol. Rev., 32, 259-286.
18. Ehlert,K., Tschierske,M., Mori,C., Schroder,W. and Berger-Bachi,B. (2000) Site-specific serine incorporation by Lif and Epr into positions 3 and 5 of the Staphylococcal peptidoglycan interpeptide bridge. J. Bacteriol., 182, 2635-2638.
19. Hegde,S.S. and Blanchard,J.S. (2003) Kinetic and mechanistic characterization of recombinant Lactobacillus viridescens FemX (UDP-N-acetylmuramoyl pentapeptide-lysine N6-alanyltransferase). J. Biol. Chem., 278, 22861-22867.
20. Hegde,S.S. and Shrader,T.E. (2001) FemABX family members are novel nonribosomal peptidyltransferases and important pathogenspecific drug targets. J. Biol. Chem., 276, 6998-7003.
21. Rohrer,S., Ehlert,K., Tschierske,M., Labischinski,H. and Berger-Bachi,B. (1999) The essential Staphylococcus aureus gene fmhB is involved in the first step of peptidoglycan pentaglycine interpeptide formation. Proc. Natl Acad. Sci. USA, 96, 9351-9356.
22. Filipe,S.R., Severina,E. and Tomasz,A. (2002) The mur MN operon: A functional link between antibiotic resistance and antibiotic tolerance in Streptococcus pneumoniae. Proc. Natl Acad. Sci. USA, 99, 1550-1555.
23. Filipe,S.R., Severina,E. and Tomasz,A. (2001) The role of mur MN operon in penicillin resistance and antibiotic tolerance of Streptococcus pneumoniae. Microb. Drug Resist., 7, 303-316.
24. Berger-Bachi,B., Barberis-Maino,L., Strassle,A. and Kayser,F.H. (1989) FemA, a host-mediated factor essential for methicillin resistance in Staphylococcus aureus: Molecular cloning and characterization. Mol. Gen. Genet., 219, 263-269.
25. Schneider,T., Senn,M.M., Berger-Bachi,B., Tossi,A., Sahl,H.G. and Wiedemann,I. (2004) In vitro assembly of a complete, pentaglycine interpeptide bridge containing cell wall precursor (lipid II-Gly5) of Staphylococcus aureus. Mol. Microbiol., 53, 675-685.
26. Lloyd,A.J., Gilbey,A.M., Blewett,A.M., De Pascale,G., El Zoeiby,A., Levesque,R.C., Catherwood,A.C., Tomasz,A., Bugg,T.D., Roper,D.I. et al. (2008) Characterization of tRNA-dependent peptide bond formation by MurM in the synthesis of Streptococcus pneumoniae peptidoglycan. J. Biol. Chem., 283, 6402-6417.
27. Bouhss,A., Josseaume,N., Allanic,D., Crouvoisier,M., Gutmann,L., Mainardi,J.L., Mengin-Lecreulx,D., van Heijenoort,J. and Arthur,M. (2001) Identification of the UDP-MurNAc-pentapeptide: L-alanine ligase for synthesis of branched pepetidoglycan precursors in Enterococcus faecalis. J. Bacteriol., 183, 5122-5127.
28. Bouhss,A., Josseaume,N., Severin,A., Tabei,K., Hugonnet,J.E., Shlaes,D., Mengin-Lecreulx,D., Van Heijenoort,J. and Arthur,M. (2002) Synthesis of the L-alanyl-L-alanine cross-bridge of Enterococcus faecalis peptidoglycan. J. Biol. Chem., 277, 45935-45941.
29. Maillard,A.P., Biarrotte-Sorin,S., Villet,R., Mesnage,S., Bouhss,A., Sougakoff,W., Mayer,C. and Arthur,M. (2005) Structure-based site-directed mutagenesis of the UDP-MurNAc-pentapeptide-binding cavity of the FemX alanyl transferase from Weissella viridescens. J. Bacteriol., 187, 3833-3838.
30. Villet,R., Fonvielle,M., Busca,P., Chemama,M., Maillard,A.P., Hugonnet,J.E., Dubost,L., Marie,A., Josseaume,N., Mesnage,S. et al. (2007) Idiosyncratic features in tRNAs participating in bacterial cell wall synthesis. Nucleic Acids Res., 35, 6870-6883.
31. Babic,A., Patin,D., Boniface,A., Hervé,M., Mengin-Lecreulx,D., Pecar,S., Gobec,S. and Blanot,D. (2007) Chemoenzymatic synthesis of the nucleotide substrates of the Mur ligases. In Proceedings of the 5th Joint Meeting on Medicinal Chemistry, June 17-21, Portoroz, Slovenia, Medimond Srl, Bologna, Italy, Medimond Srl., Bologna, Italy, pp. 1-4.
32. Bouhss,A., Crouvoisier,M., Blanot,D. and Mengin-Lecreulx,D. (2004) Purification and characterization of the bacterial MraY translocase catalyzing the first membrane step of peptidoglycan biosynthesis. J. Biol. Chem., 279, 29974-29980.
33. Robertson,S.A., Noren,C.J., Anthony-Cahill,S.J., Griffith,M.C. and Schultz,P.G. (1989) The use of 5′-phospho-2 deoxyribocytidylylri-boadenosine as a facile route to chemical aminoacylation of tRNA. Nucleic Acids Res., 17, 9649-9660.
34. Lodder,M., Golovine,S., Laikhter,A.L., Karginov,V.A. and Hecht,S.M. (1998) Misacylated Transfer RNAs Having a Chemically Removable Protecting Group. J. Org. Chem., 63, 794-803.
35. Lodder,M., Wang,B. and Hecht,S.M. (2005) The N-pentenoyl protecting group for aminoacyl-tRNAs. Methods, 36, 245-251.
36. Chung,H.H., Benson,D.R., Cornish,V.W. and Schultz,P.G. (1993) Probing the role of loop 2 in Ras function with unnatural amino acids. Proc. Natl Acad Sci. USA, 90, 10145-10149.
37. Chemama,M., Fonvielle,M., Villet,R., Arthur,M., Valery,J.M. and Etheve-Quelquejeu,M. (2007) Stable analogues of aminoacyl-tRNA for inhibition of an essential step of bacterial cell-wall synthesis. J. Am. Chem. Soc., 129, 12642-12643.
38. Ibba,M. and Soll,D. (2004) Aminoacyl-tRNAs: Setting the limits of the genetic code. Genes Dev., 18, 731-738.
39. Sheppard,K., Yuan,J., Hohn,M.J., Jester,B., Devine,K.M. and Soll,D. (2008) From one amino acid to another: TRNA-dependent amino acid biosynthesis. Nucleic Acids Res., 36, 1813-1825.
40. Bailly,M., Blaise,M., Roy,H., Deniziak,M., Lorber,B., Birck,C., Becker,H.D. and Kern,D. (2008) tRNA-dependent asparagine formation in prokaryotes: Characterization, isolation and structural and functional analysis of a ribonucleoprotein particle generating Asn-tRNA(Asn). Methods, 44, 146-163.
41. RajBhandary,U.L. and Soll,D. (2008) Aminoacyl-tRNAs, the bacterial cell envelope, and antibiotics. Proc. Natl Acad. Sci. USA, 105, 5285-5286.
42. Mainardi,J.L., Villet,R., Bugg,T.D., Mayer,C. and Arthur,M. (2008) Evolution of peptidoglycan biosynthesis under the selective pressure of antibiotics in Gram-positive bacteria. FEMS Microbiol. Rev., 32 386-408.
43. Randau,L., Schauer,S., Ambrogelly,A., Salazar,J.C., Moser,J., Sekine,S., Yokoyama,S., Soll,D. and Jahn,D. (2004) tRNA recognition by glutamyl-tRNA reductase. J. Biol. Chem., 279, 34931-34937.
44. Roy,H. and Ibba,M. (2008) RNA-dependent lipid remodeling by bacterial multiple peptide resistance factors. Proc. Natl Acad. Sci. USA, 105, 4667-4672.
45. Watanabe,K., Toh,Y., Suto,K., Shimizu,Y., Oka,N., Wada,T. and Tomita,K. (2007) Protein-based peptide-bond formation by aminoacyl-tRNA protein transferase. Nature, 449, 867-871.
46. Levican,G., Katz,A., Valenzuela,P., Soll,D. and Orellana,O. (2005) A tRNA(Glu) that uncouples protein and tetrapyrrole biosynthesis. FEBS Lett., 579, 6383-6387.
47. Roberts,R.J. (1974) Staphylococcal transfer ribonucleic acids. II. Sequence analysis of isoaccepting glycine transfer ribonucleic acids IA and IB from Staphylococcus epidermidis Texas 26. J. Biol. Chem. 249, 4787-4796.
48. Abramochkin,G. and Shrader,T.E. (1996) Aminoacyl-tRNA recognition by the leucyl/phenylalanyl-tRNA-protein transferase. J. Biol. Chem., 271, 22901-22907.
49. LaRiviere,FJ., Wolfson,AD. and Uhlenbeck,OC. (2001) Uniform binding of aminoacyl-tRNAs to elongation factor Tu by thermodynamic compensation. Science, 294, 165-168.
50. Dong,X., Kato-Murayama,M., Muramatsu,T., Mori,H., Shirouzu,M., Bessho,Y. and Yokoyama,S. (2007) The crystal structure of leucyl/ phenylalanyl-tRNA-protein transferase from Escherichia coli. Protein Sci., 16, 528-534.
51. Suto,K., Shimizu,Y., Watanabe,K., Ueda,T., Fukai,S., Nureki,O. and Tomita,K. (2006) Crystal structures of leucyl/phenylalanyl-tRNA-protein transferase and its complex with an aminoacyl-tRNA analog. EMBO J. 25, 5942-5950