Diaminopimelic acid amidation in corynebacteriales new insights into the role of ltsa in peptidoglycan modification

Journal of Biological Chemistry

Volumn 290, Issue 21, 2015, Pages 13079-13094

  Levefaudes, Marjorie ^a   Patin, Delphine ^a   De Sousa D'Auria, Célia ^a   Chami, Mohamed ^b   Blanot, Didier ^a   Hervé, Mireille ^a   Arthur, Michel ^c,d,e   Houssin, Christine ^a,f   Mengin Lecreulx, Dominique ^a,f  

^a INSTITUTE FOR INTEGRATIVE BIOLOGY OF THE CELL I2BC   (France)

^b UNIVERSITY OF BASEL   (Switzerland)

^c CENTRE DE RECHERCHE DES CORDELIERS   (France)

^d SORBONNE UNIVERSITÉ   (France)

^e UNIVERSITÉ PARIS DESCARTES   (France)

^f UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; ANTIBIOTICS; CELLS; CYTOLOGY; ENZYMES; ESCHERICHIA COLI; PROTEINS;

AMIDOTRANSFERASES; CELL SUSCEPTIBILITY; CORYNEBACTERIUM GLUTAMICUM; DIAMINOPIMELIC ACIDS; HETEROLOGOUS EXPRESSION; NITROGEN TRANSFER; NUCLEOTIDE PRECURSORS; TRUNCATED VERSIONS;

SUBSTRATES;

AMPICILLIN; BACTERIAL PROTEIN; BETA LACTAM ANTIBIOTIC; CARBENICILLIN; CEFTAZIDIME; CHLORAMPHENICOL; DIAMINOPIMELIC ACID; IMIPENEM; PROTEIN LTSA; UNCLASSIFIED DRUG; AMIDE; AMINOTRANSFERASE; ANTIINFECTIVE AGENT; GLUTAMINE-PYRUVATE AMINOTRANSFERASE; LYSOZYME; MESSENGER RNA; PEPTIDOGLYCAN;

AMIDATION; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL CELL WALL; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL STRAIN; CONTROLLED STUDY; CORYNEBACTERIUM GLUTAMICUM; CROSS LINKING; CYTOLYSIS; ESCHERICHIA COLI; LTSA GENE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN STRUCTURE; AMINO ACID SEQUENCE; CELL CULTURE; CELL WALL; CHEMISTRY; CORYNEBACTERIUM; ENZYME IMMUNOASSAY; GENETICS; GROWTH, DEVELOPMENT AND AGING; MASS SPECTROMETRY; METABOLISM; MOLECULAR GENETICS; MUTATION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY; TRANSMISSION ELECTRON MICROSCOPY; WESTERN BLOTTING;

CORYNEBACTERIUM; CORYNEBACTERIUM GLUTAMICUM; ESCHERICHIA COLI; RHODOCOCCUS;

AMIDES; AMINO ACID SEQUENCE; ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; BLOTTING, WESTERN; CELL WALL; CELLS, CULTURED; CORYNEBACTERIUM; DIAMINOPIMELIC ACID; IMMUNOENZYME TECHNIQUES; MICROSCOPY, ELECTRON, TRANSMISSION; MOLECULAR SEQUENCE DATA; MURAMIDASE; MUTATION; PEPTIDOGLYCAN; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SEQUENCE HOMOLOGY, AMINO ACID; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; TRANSAMINASES;

EID: 84930008437     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.642843     Document Type: Article

References (57)

1. Hoffmann, C., Leis, A., Niederweis, M., Plitzko, J. M., and Engelhardt, H. (2008) Disclosure of the mycobacterial outer membrane: cryo-electron tomography and vitreous sections reveal the lipid bilayer structure. Proc. Natl. Acad. Sci. U.S.A. 105, 3963-3967
2. Zuber, B., Chami, M., Houssin, C., Dubochet, J., Griffiths, G., and Daffé, M. (2008) Direct visualization of the outer membrane of mycobacteria and corynebacteria in their native state. J. Bacteriol. 190, 5672-5680
3. Crick, D. C., Mahapatra, S., and Brennan, P. J. (2001) Biosynthesis of the arabinogalactan-peptidoglycan complex of Mycobacterium tuberculosis. Glycobiology 11, 107R-118R
4. Puech, V., Chami, M., Lemassu, A., Lanéelle, M. A., Schiffler, B., Gounon, P., Bayan, N., Benz, R., and Daffé, M. (2001) Structure of the cell envelope of corynebacteria: importance of the non-covalently bound lipids in the formation of the cell wall permeability barrier and fracture plane. Microbiology 147, 1365-1382
5. McNeil, M., Daffé, M., and Brennan, P. J. (1990) Evidence for the nature of the link between the arabinogalactan and peptidoglycan of mycobacterial cell walls. J. Biol. Chem. 265, 18200-18206
6. Schleifer, K. H., and Kandler, O. (1972) Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol. Rev. 36, 407-477
7. Petit, J. F., Adam, A., Wietzerbin-Falszpan, J., Lederer, E., and Ghuysen, J. M. (1969) Chemical structure of the cell wall of Mycobacterium smegmatis. I. Isolation and partial characterization of the peptidoglycan. Biochem. Biophys. Res. Commun. 35, 478-485
8. Mahapatra, S., Crick, D. C., McNeil, M. R., and Brennan, P. J. (2008)Unique structural features of the peptidoglycan of Mycobacterium leprae. J. Bacteriol. 190, 655-661
9. Gupta, R., Lavollay, M., Mainardi, J. L., Arthur, M., Bishai, W. R., and Lamichhane, G. (2010) The Mycobacterium tuberculosis protein LdtMt2is a nonclassical transpeptidase required for virulence and resistance to amoxicillin. Nat. Med. 16, 466-469
10. rd (2012) Meropenem inhibits DD-carboxypeptidase activity in Mycobacterium tuberculosis. Mol. Microbiol. 86, 367-381
11. 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
12. Lavollay, M., Arthur, M., Fourgeaud, M., Dubost, L., Marie, A., Riegel, P., Gutmann, L., and Mainardi, J. L. (2009) The -lactam-sensitive D,D-carboxypeptidase activity of Pbp4 controls the L,D- and D,D-transpeptidation pathways in Corynebacterium jeikeium. Mol. Microbiol. 74, 650-661
13. Lavollay, M., Fourgeaud, M., Herrmann, J. L., Dubost, L., Marie, A., Gutmann, L., Arthur, M., and Mainardi, J. L. (2011) The peptidoglycan of Mycobacterium abscessus is predominantly cross-linked by L,D-transpeptidases. J. Bacteriol. 193, 778-782
14. Mahapatra, S., Scherman, H., Brennan, P. J., and Crick, D. C. (2005) N Glycolylation of the nucleotide precursors of peptidoglycan biosynthesis of Mycobacterium spp. is altered by drug treatment. J. Bacteriol. 187, 2341-2347
15. Mahapatra, S., Yagi, T., Belisle, J. T., Espinosa, B. J., Hill, P. J., McNeil, M. R., Brennan, P. J., and Crick, D. C. (2005) Mycobacterial lipid II is composed of a complex mixture of modified muramyl and peptide moieties linked to decaprenyl phosphate. J. Bacteriol. 187, 2747-2757
16. Bernard, E., Rolain, T., Courtin, P., Hols, P., and Chapot-Chartier, M. P. (2011) Identification of the amidotransferase AsnB1 as being responsible for meso-diaminopimelic acid amidation in Lactobacillus plantarum peptidoglycan. J. Bacteriol. 193, 6323-6330
17. Girardin, S. E., Travassos, L. H., Hervé, M., Blanot, D., Boneca, I. G., Philpott, D. J., Sansonetti, P. J., and Mengin-Lecreulx, D. (2003) Peptidoglycan molecular requirements allowing detection by Nod1 and Nod2. J. Biol. Chem. 278, 41702-41708
18. Slamti, L., de Pedro, M. A., Guichet, E., and Picardeau, M. (2011) Deciphering morphological determinants of the helix-shaped Leptospira. J. Bacteriol. 193, 6266-6275
19. Hirasawa, T., Wachi, M., and Nagai, K. (2000) A mutation in the Corynebacterium glutamicum ltsA gene causes susceptibility to lysozyme, tem-perature- sensitive growth, and L-glutamate production. J. Bacteriol. 182, 2696-2701
20. Mitani, Y., Meng, X., Kamagata, Y., and Tamura, T. (2005) Characterization of LtsA from Rhodococcus erythropolis, an enzyme with glutamineamidotransferase activity. J. Bacteriol. 187, 2582-2591
21. Larsen, T. M., Boehlein, S. K., Schuster, S. M., Richards, N. G., Thoden, J. B., Holden, H. M., and Rayment, I. (1999) Three-dimensional structure of Escherichia coli asparagine synthetase B: a short journey from substrate to product. Biochemistry 38, 16146-16157
22. Boehlein, S. K., Richards, N. G., and Schuster, S. M. (1994) Glutamine-dependent nitrogen transfer in Escherichia coli asparagine synthetase B. Searching for the catalytic triad. J. Biol. Chem. 269, 7450-7457
23. Ren, H., and Liu, J. (2006) AsnB is involved in natural resistance of Mycobacterium smegmatis to multiple drugs. Antimicrob. Agents Chemother. 50, 250-255
24. Dusch, N., Pühler, A., and Kalinowski, J. (1999) Expression of the Corynebacterium glutamicum panD gene encoding L-aspartate-decarboxylase leads to pantothenate overproduction in Escherichia coli. Appl. Environ. Microbiol. 65, 1530-1539
25. Miller, J. H. (1972) Experiments in Molecular Genetics, pp. 431-435, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
26. nd Ed., Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
27. Dagert, M., and Ehrlich, S. D. (1979) Prolonged incubation in calcium chloride improves the competence of Escherichia coli cells. Gene 6, 23-28
28. Bonamy, C., Guyonvarch, A., Reyes, O., David, F., and Leblon, G. (1990)Interspecies electro-transformation in Corynebacteria. FEMS Microbiol. Lett. 54, 263-269
29. Portevin, D., De Sousa-D'Auria, C., Houssin, C., Grimaldi, C., Chami, M., Daffé, M., and Guilhot, C. (2004) A polyketide synthase catalyzes the last condensation step of mycolic acid biosynthesis in mycobacteria and related organisms. Proc. Natl. Acad. Sci. U.S.A. 101, 314-319
30. Barreteau, H., Bouhss, A., Fourgeaud, M., Mainardi, J. L., Touzé, T., Gérard, F., Blanot, D., Arthur, M., and Mengin-Lecreulx, D. (2009) Humanand plant-pathogenic Pseudomonas species produce bacteriocins exhibiting colicin M-like hydrolase activity towards peptidoglycan precursors. J. Bacteriol. 191, 3657-3664
31. Mengin-Lecreulx, D., Flouret, B., and van Heijenoort, J. (1982) Cytoplasmic steps of peptidoglycan synthesis in Escherichia coli. J. Bacteriol. 151, 1109-1117
32. Mengin-Lecreulx, D., and van Heijenoort, J. (1985) Effect of growth conditions on peptidoglycan content and cytoplasmic steps of its biosynthesis in Escherichia coli. J. Bacteriol. 163, 208-212
33. Jayatissa, P. M., and Rose, A. H. (1976) Role of wall phosphomannan in flocculation of Saccharomyces cerevisiae. J. Gen. Microbiol. 96, 165-174
34. Glauner, B. (1988) Separation and quantification of muropeptides with high-performance liquid chromatography. Anal. Biochem. 172, 451-464
35. Mengin-Lecreulx, D., Flouret, B., and van Heijenoort, J. (1983) Pool levels of UDP N-acetylglucosamine and UDP N-acetylglucosamine-enolpyruvate in Escherichia coli and correlation with peptidoglycan synthesis. J. Bacteriol. 154, 1284-1290
36. 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
37. Laemmli, U. K., and Favre, M. (1973) Maturation of the head of bacteriophage T4. I. DNA packaging events. J. Mol. Biol. 80, 575-599
38. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254
39. Mengin-Lecreulx, D., Texier, L., Rousseau, M., and van Heijenoort, J. (1991) The murG gene of Escherichia coli codes for the UDP-N-acetylglucosamine: N-acetylmuramyl-(pentapeptide) pyrophosphoryl-undecaprenol N-acetylglucosamine transferase involved in the membrane steps of peptidoglycan synthesis. J. Bacteriol. 173, 4625-4636
40. 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
41. El Ghachi, M., Bouhss, A., Barreteau, H., Touzé, T., Auger, G., Blanot, D., and Mengin-Lecreulx, D. (2006) Colicin M exerts its bacteriolytic effect via enzymatic degradation of undecaprenyl phosphate-linked peptidoglycan precursors. J. Biol. Chem. 281, 22761-22772
42. Ammam, F., Meziane-Cherif, D., Mengin-Lecreulx, D., Blanot, D., Patin, D., Boneca, I. G., Courvalin, P., Lambert, T., and Candela, T. (2013) The functional vanGCd cluster of Clostridium difficile does not confer vancomycin resistance. Mol. Microbiol. 89, 612-625
43. Marchand, C. H., Salmeron, C., Bou Raad, R., Méniche, X., Chami, M., Masi, M., Blanot, D., Daffé, M., Tropis, M., Huc, E., Le Maréchal, P., Decottignies, P., and Bayan, N. (2012) Biochemical disclosure of the mycolate outer membrane of Corynebacterium glutamicum . J. Bacteriol. 194, 587-597
44. Geis, A., and Plapp, R. (1978) Phospho-N-acetylmuramoyl pentapeptidetransferase of Escherichia coli K12. Properties of the membrane-bound and the extracted and partially purified enzyme. Biochim. Biophys. Acta 527, 414-424
45. Atrih, A., Bacher, G., Allmaier, G., Williamson, M. P., and Foster, S. J. (1999) Analysis of peptidoglycan structure from vegetative cells of Bacillus subtilis 168 and role of PBP 5 in peptidoglycan maturation. J. Bacteriol. 181, 3956-3966
46. Atrih, A., Zöllner, P., Allmaier, G., Williamson, M. P., and Foster, S. J. (1998) Peptidoglycan structural dynamics during germination of Bacillus subtilis 168 endospores. J. Bacteriol. 180, 4603-4612
47. Münch, D., Roemer, T., Lee, S. H., Engeser, M., Sahl, H. G., and Schneider, T. (2012) Identification and in vitro analysis of the GatD/MurT enzymecomplex catalyzing lipid II amidation in Staphylococcus aureus. PLoS Pathog. 8, e1002509
48. Figueiredo, T. A., Sobral, R. G., Ludovice, A. M., Almeida, J. M., Bui, N. K., Vollmer, W., de Lencastre, H., and Tomasz, A. (2012) Identification of genetic determinants and enzymes involved with the amidation of glutamic acid residues in the peptidoglycan of Staphylococcus aureus. PLoS Pathog. 8, e1002508
49. Veiga, P., Erkelenz, M., Bernard, E., Courtin, P., Kulakauskas, S., and Chapot-Chartier, M. P. (2009) Identification of the asparagine synthase responsible for D-Asp amidation in the Lactococcus lactis peptidoglycan interpeptide crossbridge. J. Bacteriol. 191, 3752-3757
50. Desmarais, S. M., De Pedro, M. A., Cava, F., and Huang, K. C. (2013)Peptidoglycan at its peaks: how chromatographic analyses can reveal bacterial cell wall structure and assembly. Mol. Microbiol. 89, 1-13
51. Bera, A., Herbert, S., Jakob, A., Vollmer, W., and Götz, F. (2005) Why are pathogenic staphylococci so lysozyme resistant? The peptidoglycan Oacetyltransferase OatA is the major determinant for lysozyme resistance of Staphylococcus aureus. Mol. Microbiol. 55, 778-787
52. Vollmer, W. (2008) Structural variation in the glycan strands of bacterial peptidoglycan. FEMS Microbiol Rev. 32, 287-306
53. Zipperle, G. F., Jr., Ezzell, J. W., Jr., and Doyle, R. J. (1984) Glucosamine substitution and muramidase susceptibility in Bacillus anthracis. Can. J. Microbiol. 30, 553-559
54. Bera, A., Biswas, R., Herbert, S., Kulauzovic, E., Weidenmaier, C., Peschel, A., and Götz, F. (2007) Influence of wall teichoic acid on lysozyme resistance in Staphylococcus aureus. J. Bacteriol. 189, 280-283
55. Mauck, J., and Glaser, L. (1972) On the mode of in vivo assembly of the cell wall of Bacillus subtilis. J. Biol. Chem. 247, 1180-1187
56. Humbert, R., and Simoni, R. D. (1980) Genetic and biomedical studies demonstrating a second gene coding for asparagine synthetase in Escherichia coli. J. Bacteriol. 142, 212-220
57. Vollmer, W., Blanot, D., and de Pedro, M. A. (2008) Peptidoglycan structure and architecture. FEMS Microbiol. Rev. 32, 149-167