De-O-acetylation of peptidoglycan regulates glycan chain extension and affects in vivo survival of Neisseria meningitidis

Molecular Microbiology

Volumn 87, Issue 5, 2013, Pages 1100-1112

  Veyrier, Frédéric J ^a,b   Williams, Allison H ^a,b   Mesnage, Stéphane ^c,d   Schmitt, Christine ^a   Taha, Muhamed Kheir ^a   Boneca, Ivo G ^a,b  

^a INSTITUT PASTEUR   (France)

^b INSERM   (France)

^c CENTRE DE RECHERCHE DES CORDELIERS   (France)

^d UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

APE1 PROTEIN; BACTERIAL ENZYME; BACTERIAL PROTEIN; ESTERASE; PATA PROTEIN; PATB PROTEIN; PEPTIDOGLYCAN; TRIPEPTIDE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; APE1 GENE; ARTICLE; BACTERIAL CELL; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; CELL SIZE; CONTROLLED STUDY; DEACETYLATION; ENZYME ACTIVITY; ESCHERICHIA COLI; GENE LOCUS; GENE SEQUENCE; HETEROLOGOUS EXPRESSION; HOST PATHOGEN INTERACTION; IN VITRO STUDY; IN VIVO STUDY; MENINGOCOCCEMIA; MOUSE; NEISSERIA MENINGITIDIS; NONHUMAN; OPERON; PATA GENE; PATB GENE; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ACETYLATION; ANIMALS; CELL LINE; HUMANS; MENINGITIS, MENINGOCOCCAL; MICE; MICE, INBRED BALB C; MICROBIAL VIABILITY; NEISSERIA MENINGITIDIS; PEPTIDOGLYCAN; POLYSACCHARIDES; VIRULENCE;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; NEGIBACTERIA; NEISSERIA MENINGITIDIS; POSIBACTERIA;

EID: 84874201976     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12153     Document Type: Article

References (41)

1. Antignac, A., Rousselle, J.C., Namane, A., Labigne, A., Taha, M.K., and Boneca, I.G. (2003) Detailed structural analysis of the peptidoglycan of the human pathogen Neisseria meningitidis. J Biol Chem 278: 31521-31528.
2. van Asselt, E.J., Dijkstra, A.J., Kalk, K.H., Takacs, B., Keck, W., and Dijkstra, B.W. (1999) Crystal structure of Escherichia coli lytic transglycosylase Slt35 reveals a lysozyme-like catalytic domain with an EF-hand. Structure 7: 1167-1180.
3. Aubry, C., Goulard, C., Nahori, M.A., Cayet, N., Decalf, J., Sachse, M., etal. (2011) OatA, a peptidoglycan O-acetyltransferase involved in Listeria monocytogenes immune escape, is critical for virulence. J Infect Dis 204: 731-740.
4. Bera, A., Herbert, S., Jakob, A., Vollmer, W., and Gotz, F. (2005) Why are pathogenic staphylococci so lysozyme resistant? The peptidoglycan O-acetyltransferase OatA is the major determinant for lysozyme resistance of Staphylococcus aureus. Mol Microbiol 55: 778-787.
5. Bera, A., Biswas, R., Herbert, S., and Gotz, F. (2006) The presence of peptidoglycan O-acetyltransferase in various staphylococcal species correlates with lysozyme resistance and pathogenicity. Infect Immun 74: 4598-4604.
6. Bernard, E., Rolain, T., David, B., Andre, G., Dupres, V., Dufrene, Y.F., etal. (2012) Dual role for the O-acetyltransferase OatA in peptidoglycan modification and control of cell septation in Lactobacillus plantarum. PLoS ONE 7: e47893.
7. Blundell, J.K., and Perkins, H.R. (1985) The peptidoglycan of Neisseria gonorrhoeae, with or without O-acetyl groups, contains anhydro-muramyl residues. J Gen Microbiol 131: 3397-3400.
8. Boneca, I.G. (2005) The role of peptidoglycan in pathogenesis. Curr Opin Microbiol 8: 46-53.
9. Boneca, I.G., Dussurget, O., Cabanes, D., Nahori, M.A., Sousa, S., Lecuit, M., etal. (2007) A critical role for peptidoglycan N-deacetylation in Listeria evasion from the host innate immune system. Proc Natl Acad Sci USA 104: 997-1002.
10. Brumfitt, W., Wardlaw, A.C., and Park, J.T. (1958) Development of lysozyme-resistance in Micrococcus lysodiekticus and its association with an increased O-acetyl content of the cell wall. Nature 181: 1783-1784.
11. Carneiro, L.A., Travassos, L.H., and Philpott, D.J. (2004) Innate immune recognition of microbes through Nod1 and Nod2: implications for disease. Microbes Infect 6: 609-616.
12. Chaput, C., Labigne, A., and Boneca, I.G. (2007) Characterization of Helicobacter pylori lytic transglycosylases Slt and MltD. J Bacteriol 189: 422-429.
13. Cloud-Hansen, K.A., Hackett, K.T., Garcia, D.L., and Dillard, J. (2008) Neisseria gonorrhoeae uses two lytic transglycosylases to produce cytotoxic peptidoglycan monomers. J Bacteriol 190: 5989-5994.
14. Dalia, A.B., and Weiser, J.N. (2011) Minimization of bacterial size allows for complement evasion and is overcome by the agglutinating effect of antibody. Cell Host Microbe 10: 486-496.
15. Dillard, J.P., and Hackett, K.T. (2005) Mutations affecting peptidoglycan acetylation in Neisseria gonorrhoeae and Neisseria meningitidis. Infect Immun 73: 5697-5705.
16. Dupont, C., and Clarke, A.J. (1991) Dependence of lysozyme-catalysed solubilization of Proteus mirabilis peptidoglycan on the extent of O-acetylation. Eur J Biochem 195: 763-769.
17. van Heijenoort, Y., Gomez, M., Derrien, M., Ayala, J., and van Heijenoort, J. (1992) Membrane intermediates in the peptidoglycan metabolism of Escherichia coli: possible roles of PBP 1b and PBP 3. J Bacteriol 174: 3549-3557.
18. Holtje, J.V. (1998) Growth of the stress-bearing and shape-maintaining murein sacculus of Escherichia coli. Microbiol Mol Biol Rev 62: 181-203.
19. Kim, M.S., Byun, M., and Oh, B.H. (2003) Crystal structure of peptidoglycan recognition protein LB from Drosophila melanogaster. Nat Immunol 4: 787-793.
20. Laaberki, M.H., Pfeffer, J., Clarke, A.J., and Dworkin, J. (2011) O-acetylation of peptidoglycan is required for proper cell separation and S-layer anchoring in Bacillus anthracis. J Biol Chem 286: 5278-5288.
21. Lear, A.L., and Perkins, H.R. (1986) O-acetylation of peptidoglycan in Neisseria gonorrhoeae. Investigation of lipid-linked intermediates and glycan chains newly incorporated into the cell wall. J Gen Microbiol 132: 2413-2420.
22. Moynihan, P.J., and Clarke, A.J. (2010) O-acetylation of peptidoglycan in Gram-negative bacteria: identification and characterization of peptidoglycan O-acetyltransferase in Neisseria gonorrhoeae. J Biol Chem 285: 13264-13273.
23. Pfeffer, J.M., and Clarke, A.J. (2012) Identification of the first known inhibitors of O-acetylpeptidoglycan esterase: a potential new antibacterial target. Chembiochem 13: 722-731.
24. Rae, C.S., Geissler, A., Adamson, P.C., and Portnoy, D.A. (2011) Mutations of the Listeria monocytogenes peptidoglycan N-deacetylase and O-acetylase result in enhanced lysozyme sensitivity, bacteriolysis, and hyperinduction of innate immune pathways. Infect Immun 79: 3596-3606.
25. Rosenthal, R.S., Blundell, J.K., and Perkins, H.R. (1982) Strain-related differences in lysozyme sensitivity and extent of O-acetylation of gonococcal peptidoglycan. Infect Immun 37: 826-829.
26. Russell, A.B., Hood, R.D., Bui, N.K., LeRoux, M., Vollmer, W., and Mougous, J.D. (2011) Type VI secretion delivers bacteriolytic effectors to target cells. Nature 475: 343-347.
27. Saunders, N.J., Jeffries, A.C., Peden, J.F., Hood, D.W., Tettelin, H., Rappuoli, R., and Moxon, E.R. (2000) Repeat-associated phase variable genes in the complete genome sequence of Neisseria meningitidis strain MC58. Mol Microbiol 37: 207-215.
28. Shimada, T., Park, B.G., Wolf, A.J., Brikos, C., Goodridge, H.S., Becker, C.A., etal. (2010) Staphylococcus aureus evades lysozyme-based peptidoglycan digestion that links phagocytosis, inflammasome activation, and IL-1beta secretion. Cell Host Microbe 7: 38-49.
29. Sinha, R.K., and Rosenthal, R.S. (1980) Release of soluble peptidoglycan from growing conococci: demonstration of anhydro-muramyl-containing fragments. Infect Immun 29: 914-925.
30. Snyder, L.A., Butcher, S.A., and Saunders, N.J. (2001) Comparative whole-genome analyses reveal over 100 putative phase-variable genes in the pathogenic Neisseria spp. Microbiology 147: 2321-2332.
31. Sobral, R.G., Ludovice, A.M., de Lencastre, H., and Tomasz, A. (2006) Role of murF in cell wall biosynthesis: isolation and characterization of a murF conditional mutant of Staphylococcus aureus. J Bacteriol 188: 2543-2553.
32. Swim, S.C., Gfell, M.A., Wilde, C.E., and Rosenthal, R.S. (1983) Strain distribution in extents of lysozyme resistance and O-acetylation of gonococcal peptidoglycan determined by high-performance liquid chromatography. Infect Immun 42: 446-452.
33. Szatanik, M., Hong, E., Ruckly, C., Ledroit, M., Giorgini, D., Jopek, K., etal. (2011) Experimental meningococcal sepsis in congenic transgenic mice expressing human transferrin. PLoS ONE 6: e22210.
34. Tettelin, H., Saunders, N.J., Heidelberg, J., Jeffries, A.C., Nelson, K.E., Eisen, J.A., etal. (2000) Complete genome sequence of Neisseria meningitidis serogroup B strain MC58. Science 287: 1809-1815.
35. Veyrier, F.J., Boneca, I.G., Cellier, M.F., and Taha, M.K. (2011) A novel metal transporter mediating manganese export (MntX) regulates the Mn to Fe intracellular ratio and Neisseria meningitidis virulence. PLoS Pathog 7: e1002261.
36. Vollmer, W. (2008) Structural variation in the glycan strands of bacterial peptidoglycan. FEMS Microbiol Rev 32: 287-306.
37. Vollmer, W., Joris, B., Charlier, P., and Foster, S. (2008) Bacterial peptidoglycan (murein) hydrolases. FEMS Microbiol Rev 32: 259-286.
38. Weadge, J.T., and Clarke, A.J. (2006) Identification and characterization of O-acetylpeptidoglycan esterase: a novel enzyme discovered in Neisseria gonorrhoeae. Biochemistry 45: 839-851.
39. Weadge, J.T., and Clarke, A.J. (2007) Neisseria gonorrheae O-acetylpeptidoglycan esterase, a serine esterase with a Ser-His-Asp catalytic triad. Biochemistry 46: 4932-4941.
40. Weadge, J.T., Pfeffer, J.M., and Clarke, A.J. (2005) Identification of a new family of enzymes with potential O-acetylpeptidoglycan esterase activity in both Gram-positive and Gram-negative bacteria. BMC Microbiol 5: 49.
41. Zarantonelli, M.L., Szatanik, M., Giorgini, D., Hong, E., Huerre, M., Guillou, F., etal. (2007) Transgenic mice expressing human transferrin as a model for meningococcal infection. Infect Immun 75: 5609-5614.