The Lysozyme-Induced Peptidoglycan N-Acetylglucosamine Deacetylase pgda (EF1843) Is Required for Enterococcus faecalis Virulence

Journal of Bacteriology

Volumn 194, Issue 22, 2012, Pages 6066-6073

  Benachour, Abdellah ^a   Ladjouzi, Rabia ^a   Le Jeune, André ^a   Hébert, Laurent ^a   Thorpe, Simon ^b   Courtin, Pascal ^c   Chapot Chartier, Marie Pierre ^c   Prajsnar, Tomasz K ^b   Foster, Simon J ^b   Mesnage, Stéphane ^b  

^a UNIVERSITÉ DE CAEN   (France)

^b UNIVERSITY OF SHEFFIELD   (United Kingdom)

^c UMR1319 MICALIS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENZYME; LYSOZYME; PEPTIDOGLYCAN; PEPTIDOGLYCAN N ACETYLGLUCOSAMINE DEACETYLASE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; DEACETYLATION; ENTEROCOCCUS FAECALIS; ENZYME ACTIVITY; ENZYME INHIBITION; GAIN OF FUNCTION MUTATION; GALLERIA MELLONELLA; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION;

AMIDOHYDROLASES; ANIMALS; BACTERIAL PROTEINS; DNA, BACTERIAL; ENTEROCOCCUS FAECALIS; GENE EXPRESSION REGULATION, BACTERIAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; LARVA; MOTHS; MURAMIDASE; MUTATION; PLASMIDS; VIRULENCE;

BACTERIA (MICROORGANISMS); ENTEROCOCCUS FAECALIS; GALLERIA MELLONELLA; MAMMALIA; POSIBACTERIA;

EID: 84869116802     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00981-12     Document Type: Article

References (43)

1. Abergel C, et al. 2007. Structure and evolution of the Ivy protein family, unexpected lysozyme inhibitors in Gram-negative bacteria. Proc. Natl. Acad. Sci. U. S. A. 104:6394-6399.
2. Aubry C, et al. 2011. OatA, a peptidoglycan O-acetyltransferase involved in Listeria monocytogenes immune escape, is critical for virulence. J. Infect. Dis. 204:731-740.
3. Benachour A, et al. 2005. The Enterococcus faecalis SigV protein is an extracytoplasmic function sigma factor contributing to survival following heat, acid, and ethanol treatments. J. Bacteriol. 187:1022-1035.
4. Bera A, Herbert S, Jakob A, Vollmer W, 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.
5. Binks MJ, Fernie-King BA, Seilly DJ, Lachmann PJ, Sriprakash KS. 2005. Attribution of the various inhibitory actions of the streptococcal inhibitor of complement (SIC) to regions within the molecule. J. Biol. Chem. 280:20120-20125.
6. Boneca IG, et al. 2007. A critical role for peptidoglycanN-deacetylation in Listeria evasion from the host innate immune system. Proc. Natl. Acad. Sci. U. S. A. 104:997-1002.
7. Brouwer J, van Leeuwen-Herberts T, Otting-van de Ruit M. 1984. Determination of lysozyme in serum, urine, cerebrospinal fluid and feces by enzyme immunoassay. Clin. Chim. Acta 142:21-30.
8. Callewaert L, et al. 2008. A new family of lysozyme inhibitors contributing to lysozyme tolerance in gram-negative bacteria. PLoS Pathog. 4:e1000019. doi:10.1371/journal.ppat.1000019.
9. Callewaert L, Michiels CW. 2010. Lysozymes in the animal kingdom. J. Biosci. 35:127-160.
10. Crisóstomo MI, et al. 2006. Attenuation of penicillin resistance in a peptidoglycan O-acetyl transferase mutant of Streptococcus pneumoniae. Mol. Microbiol. 61:1497-1509.
11. Cruz-Rodz AL, Gilmore MS. 1990. High efficiency introduction of plasmid DNA into glycine treated Enterococcus faecalis by electroporation. Mol. Gen. Genet. 224:152-154.
12. Davis KM, Akinbi HT, Standish AJ, Weiser JN. 2008. Resistance to mucosal lysozyme compensates for the fitness deficit of peptidoglycan modifications by Streptococcus pneumoniae. PLoS Pathog. 4:e1000241. doi:10.1371/journal.ppal.1000241.
13. Dommett R, Zilbauer M, George JT, Bajaj-Elliott M. 2005. Innate immune defence in the human gastrointestinal tract. Mol. Immunol. 42: 903-912.
14. Eckert C, Lecerf M, Dubost L, Arthur M, Mesnage S. 2006. Functional analysis of AtlA, the majorN-acetylglucosaminidase of Enterococcus faecalis. J. Bacteriol. 188:8513-8519.
15. Emirian A, et al. 2009. Impact of peptidoglycan O-acetylation on autolytic activities of the Enterococcus faecalis N-acetylglucosaminidase AtlA and N-acetylmuramidase AtlB. FEBS Lett. 583:3033-3038.
16. Ernst CM, Peschel A. 2011. Broad-spectrum antimicrobial peptide resistance by MprF-mediated aminoacylation and flipping of phospholipids. Mol. Microbiol. 80:290-299.
17. Faurschou M, Borregaard N. 2003. Neutrophil granules and secretory vesicles in inflammation. Microbes Infect. 5:1317-1327.
18. Fittipaldi N, et al. 2008. Significant contribution of the pgdA gene to the virulence of Streptococcus suis. Mol. Microbiol. 70:1120-1135.
19. Flahaut S, et al. 1996. Relationship between stress response toward bile salts, acid and heat treatment in Enterococcus faecalis. FEMS Microbiol. Lett. 138:49-54.
20. Gaspar F, et al. 2009. Virulence of Enterococcus faecalis dairy strains in an insect model: the role of fsrB and gelE. Microbiology 155:3564-3571.
21. Ge Y, et al. 1999. In vitro antibacterial properties of pexiganan, an analog of magainin. Antimicrob. Agents Chemother. 43:782-788.
22. Guariglia-Oropeza V, Helmann JD. 2011. Bacillus subtilis sigma(V) confers lysozyme resistance by activation of two cell wall modification pathways, peptidoglycan O-acetylation and D-alanylation of teichoic acids. J. Bacteriol. 193:6223-6232.
23. Hancock LE, Gilmore MS. 2006. Pathogenicity of enterococci, p 299-311. In Fischetti VA, Novick RP, Ferretti JJ, Portnoy DA, Rood JI (ed), Gram-positive pathogens. ASM Press, Washington, DC.
24. Hébert L, et al. 2007. Enterococcus faecalis constitutes an unusual bacterial model in lysozyme resistance. Infect. Immun. 75:5390-5398.
25. Herbert S, et al. 2007. Molecular basis of resistance to muramidase and cationic antimicrobial peptide activity of lysozyme in staphylococci. PLoS Pathog. 3:e102. doi:10.1371/journal.ppat.0030102.
26. Ho TD, Hastie JL, Intile PJ, Ellermeier CD. 2011. The Bacillus subtilis extracytoplasmic function sigma factor sigma(V) is induced by lysozyme and provides resistance to lysozyme. J. Bacteriol. 193:6215-6222.
27. Ibrahim HR, Aoki T, Pellegrini A. 2002. Strategies for new antimicrobial proteins and peptides: lysozyme and aprotinin as model molecules. Curr. Pharm. Des. 8:671-693.
28. Kavanagh K, Reeves EP. 2004. Exploiting the potential of insects for in vivo pathogenicity testing of microbial pathogens. FEMS Microbiol. Rev. 28:101-112.
29. Keshav S, Chung P, Milon G, Gordon S. 1991. Lysozyme is an inducible marker of macrophage activation in murine tissues as demonstrated by in situ hybridization. J. Exp. Med. 174:1049-1058.
30. Le Jeune A, et al. 2010. The extracytoplasmic function sigma factor SigV plays a key role in the original model of lysozyme resistance and virulence of Enterococcus faecalis. PLoS One 5:e9658. doi:10.1371/journal.pone.0009658.
31. Mason KL, et al. 2011. From commensal to pathogen: translocation of Enterococcus faecalis from the midgut to the hemocoel of Manduca sexta. mBio 2:e00065-11. doi:10.1128/mBio.00065-11.
32. Olsen RJ, Watkins ME, Cantu CC, Beres SB, Musser JM. 2011. Virulence of serotype M3 group A Streptococcus strains in wax worms (Galleria mellonella larvae). Virulence 2:111-119.
33. Paulsen IT, et al. 2003. Role of mobile DNA in the evolution of vancomycin- resistant Enterococcus faecalis. Science 299:2071-2074.
34. Peschel A, et al. 1999. Inactivation of the dlt operon in Staphylococcus aureus confers sensitivity to defensins, protegrins, and other antimicrobial peptides. J. Biol. Chem. 274:8405-8410.
35. Rae CS, Geissler A, Adamson PC, Portnoy DA. 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.
36. Sambrook J, Fritsch EF, Maniatis T (ed). 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
37. Solheim M, Aakra A, Vebo H, Snipen L, Nes IF. 2007. Transcriptional responses of Enterococcus faecalis V583 to bovine bile and sodium dodecyl sulfate. Appl. Environ. Microbiol. 73:5767-5774.
38. Terzaghi BE, Sandine WE. 1975. Improved medium for lactic streptococci and their bacteriophages. Appl. Microbiol. 29:807-813.
39. Vanderkelen L, et al. 2011. Identification of a bacterial inhibitor against g-type lysozyme. Cell. Mol. Life Sci. 68:1053-1064.
40. Van Herreweghe JM, et al. 2010. Lysozyme inhibitor conferring bacterial tolerance to invertebrate type lysozyme. Cell. Mol. Life Sci. 67:1177-1188.
41. Veiga P, et al. 2007. SpxB regulatesO-acetylation-dependent resistance of Lactococcus lactis peptidoglycan to hydrolysis. J. Biol. Chem. 282:19342-19354.
42. Veiga P, et al. 2009. Identification of the asparagine synthase responsible for D-Asp amidation in the Lactococcus lactis peptidoglycan interpeptide crossbridge. J. Bacteriol. 191:3752-3757.
43. Vollmer W, Tomasz A. 2000. The pgdA gene encodes for a peptidoglycan N-acetylglucosamine deacetylase in Streptococcus pneumoniae. J. Biol. Chem. 275:20496-20501.