Aminoacyl-tRNA Recognition by the FemXWv Transferase for Bacterial Cell Wall Synthesis

Overview

Journal Nucleic Acids Res

Publisher Oxford University Press

Specialty Biochemistry

Date 2009 Jan 20

PMID 19151092

Citations 23

Authors

Matthieu Fonvielle

Maryline Chemama

Regis Villet

Maxime Lecerf

Ahmed Bouhss

Jean-Marc Valery

Melanie Etheve-Quelquejeu

Michel Arthur

Affiliations

Soon will be listed here.

Abstract

Transferases of the Fem family catalyse peptide-bond formation by using aminoacyl-tRNAs and peptidoglycan precursors as donor and acceptor substrates, respectively. The specificity of Fem transferases is essential since mis-incorporated amino acids could act as chain terminators thereby preventing formation of a functional stress-bearing peptidoglycan network. Here we have developed chemical acylation of RNA helices with natural and non-proteinogenic amino acids to gain insight into the specificity of the model transferase FemX(Wv). Combining modifications in the RNA and aminoacyl moieties of the donor substrate revealed that unfavourable interactions of FemX(Wv) with the acceptor arm of tRNA(Gly) and with L-Ser or larger residues quantitatively accounts for the preferential transfer of L-Ala observed with complete aminoacyl-tRNAs. The main FemX(Wv) identity determinant was identified as the penultimate base pair (G(2)-C(71)) of the acceptor arm instead of G(3)*U(70) for the alanyl-tRNA synthetase. FemX(Wv) tolerated a configuration inversion of the Calpha of L-Ala but not the introduction of a second methyl on this atom. These results indicate that aminoacyl-tRNA recognition by FemX(Wv) is distinct from other components of the translation machinery and relies on the exclusion of bulky amino acids and of the sequence of tRNA(Gly) from the active site.

Citing Articles

Traceless Staudinger Ligation to Access Stable Aminoacyl- or Peptidyl-Dinucleotide.

Kitoun C, Saidjalolov S, Bouquet D, Djago F, Remaury Q, Sargueil B ACS Omega. 2023; 8(4):3850-3860.

PMID: 36743074 PMC: 9893454. DOI: 10.1021/acsomega.2c06135.

Amino-acyl tXNA as inhibitors or amino acid donors in peptide synthesis.

Rietmeyer L, Li de la Sierra-Gallay I, Schepers G, Dorchene D, Iannazzo L, Patin D Nucleic Acids Res. 2022; 50(20):11415-11425.

PMID: 36350642 PMC: 9723616. DOI: 10.1093/nar/gkac1023.

Proteome of Biofilm Changes Significantly with Aging.

Rahman M, Amirkhani A, Chowdhury D, Mempin M, Molloy M, Deva A Int J Mol Sci. 2022; 23(12).

PMID: 35742863 PMC: 9223533. DOI: 10.3390/ijms23126415.

Unique anticodon loop conformation with the flipped-out wobble nucleotide in the crystal structure of unbound tRNA.

Jeong H, Kim J RNA. 2021; 27(11):1330-1338.

PMID: 34315814 PMC: 8522699. DOI: 10.1261/rna.078863.121.

Flexizyme-aminoacylated shortened tRNAs demonstrate that only the aminoacylated acceptor arms of the two tRNA substrates are required for cyclodipeptide synthase activity.

Canu N, Tellier C, Babin M, Thai R, Ajel I, Seguin J Nucleic Acids Res. 2020; 48(20):11615-11625.

PMID: 33095883 PMC: 7672478. DOI: 10.1093/nar/gkaa903.

References

Bouhss A, Crouvoisier M, Blanot D, Mengin-Lecreulx D . Purification and characterization of the bacterial MraY translocase catalyzing the first membrane step of peptidoglycan biosynthesis. J Biol Chem. 2004; 279(29):29974-80. DOI: 10.1074/jbc.M314165200. View

Lavollay M, Arthur M, Fourgeaud M, Dubost L, Marie A, Veziris N . The peptidoglycan of stationary-phase Mycobacterium tuberculosis predominantly contains cross-links generated by L,D-transpeptidation. J Bacteriol. 2008; 190(12):4360-6. PMC: 2446752. DOI: 10.1128/JB.00239-08. View

Bailly M, Blaise M, Roy H, Deniziak M, Lorber B, Birck C . tRNA-dependent asparagine formation in prokaryotes: characterization, isolation and structural and functional analysis of a ribonucleoprotein particle generating Asn-tRNA(Asn). Methods. 2008; 44(2):146-63. DOI: 10.1016/j.ymeth.2007.11.012. View

Bouhss A, Josseaume N, Allanic D, Crouvoisier M, Gutmann L, Mainardi J . Identification of the UDP-MurNAc-pentapeptide:L-alanine ligase for synthesis of branched peptidoglycan precursors in Enterococcus faecalis. J Bacteriol. 2001; 183(17):5122-7. PMC: 95388. DOI: 10.1128/JB.183.17.5122-5127.2001. View

Lodder M, Golovine S, Laikhter A, Karginov V, Hecht S . Misacylated Transfer RNAs Having a Chemically Removable Protecting Group. J Org Chem. 2001; 63(3):794-803. DOI: 10.1021/jo971692l. View

Rohrer S, Ehlert K, Tschierske M, Labischinski H, Berger-Bachi B . The essential Staphylococcus aureus gene fmhB is involved in the first step of peptidoglycan pentaglycine interpeptide formation. Proc Natl Acad Sci U S A. 1999; 96(16):9351-6. PMC: 17786. DOI: 10.1073/pnas.96.16.9351. View

Benson T, Prince D, Mutchler V, Curry K, Ho A, Sarver R . X-ray crystal structure of Staphylococcus aureus FemA. Structure. 2002; 10(8):1107-15. DOI: 10.1016/s0969-2126(02)00807-9. View

Abramochkin G, Shrader T . Aminoacyl-tRNA recognition by the leucyl/phenylalanyl-tRNA-protein transferase. J Biol Chem. 1996; 271(37):22901-7. DOI: 10.1074/jbc.271.37.22901. View

Vollmer W . Structural variation in the glycan strands of bacterial peptidoglycan. FEMS Microbiol Rev. 2007; 32(2):287-306. DOI: 10.1111/j.1574-6976.2007.00088.x. View

10.

Randau L, Schauer S, Ambrogelly A, Salazar J, Moser J, Sekine S . tRNA recognition by glutamyl-tRNA reductase. J Biol Chem. 2004; 279(33):34931-7. DOI: 10.1074/jbc.M401529200. View

11.

Roberts R . Staphylococcal transfer ribonucleic acids. II. Sequence analysis of isoaccepting glycine transfer ribonucleic acids IA and IB from Staphylococcus epidermidis Texas 26. J Biol Chem. 1974; 249(15):4787-96. View

12.

Magnet S, Arbeloa A, Mainardi J, Hugonnet J, Fourgeaud M, Dubost L . Specificity of L,D-transpeptidases from gram-positive bacteria producing different peptidoglycan chemotypes. J Biol Chem. 2007; 282(18):13151-9. DOI: 10.1074/jbc.M610911200. View

13.

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

14.

Barreteau H, Kovac A, Boniface A, Sova M, Gobec S, Blanot D . Cytoplasmic steps of peptidoglycan biosynthesis. FEMS Microbiol Rev. 2008; 32(2):168-207. DOI: 10.1111/j.1574-6976.2008.00104.x. View

15.

Schneider T, Senn M, Berger-Bachi B, Tossi A, Sahl H, Wiedemann I . In vitro assembly of a complete, pentaglycine interpeptide bridge containing cell wall precursor (lipid II-Gly5) of Staphylococcus aureus. Mol Microbiol. 2004; 53(2):675-85. DOI: 10.1111/j.1365-2958.2004.04149.x. View

16.

Hegde S, Blanchard J . Kinetic and mechanistic characterization of recombinant Lactobacillus viridescens FemX (UDP-N-acetylmuramoyl pentapeptide-lysine N6-alanyltransferase). J Biol Chem. 2003; 278(25):22861-7. DOI: 10.1074/jbc.M301565200. View

17.

Bouhss A, Josseaume N, Severin A, Tabei K, Hugonnet J, Shlaes D . Synthesis of the L-alanyl-L-alanine cross-bridge of Enterococcus faecalis peptidoglycan. J Biol Chem. 2002; 277(48):45935-41. DOI: 10.1074/jbc.M207449200. View

18.

Biarrotte-Sorin S, Maillard A, Delettre J, Sougakoff W, Arthur M, Mayer C . Crystal structures of Weissella viridescens FemX and its complex with UDP-MurNAc-pentapeptide: insights into FemABX family substrates recognition. Structure. 2004; 12(2):257-67. DOI: 10.1016/j.str.2004.01.006. View

19.

Kern T, Hediger S, Muller P, Giustini C, Joris B, Bougault C . Toward the characterization of peptidoglycan structure and protein-peptidoglycan interactions by solid-state NMR spectroscopy. J Am Chem Soc. 2008; 130(17):5618-9. DOI: 10.1021/ja7108135. View

20.

Chemama M, Fonvielle M, Villet R, Arthur M, Valery J, Etheve-Quelquejeu M . Stable analogues of aminoacyl-tRNA for inhibition of an essential step of bacterial cell-wall synthesis. J Am Chem Soc. 2007; 129(42):12642-3. DOI: 10.1021/ja0749946. View