Characterization of SfPgdA, a Shigella flexneri peptidoglycan deacetylase required for bacterial persistence within polymorphonuclear neutrophils

Microbes and Infection

Volumn 14, Issue 7-8, 2012, Pages 619-627

  Kaoukab Raji, Abdelmoughit ^a   Biskri, Latéfa ^a   Bernardini, Maria Lina ^b   Allaoui, Abdelmounaaïm ^a  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

Lysozyme; Peptidoglycan deacetylase; PMN infection; Shigella

Indexed keywords

ACYLTRANSFERASE; BACTERIAL ENZYME; HISTIDINE; LYSOZYME; MAGNESIUM; MUTANT PROTEIN; PHENYLALANINE; SHIGELLA FLEXNERI PEPTIDOGLYCAN DEACETYLASE; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

AMINO ACID SUBSTITUTION; ARTICLE; BACTERIAL GENOME; BACTERIAL VIRULENCE; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME PURIFICATION; ENZYME REGULATION; IN VITRO STUDY; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SEQUENCE ANALYSIS; SHIGELLA FLEXNERI;

ACETYLESTERASE; AMIDOHYDROLASES; AMINO ACID SEQUENCE; CHILD, PRESCHOOL; CONSERVED SEQUENCE; DYSENTERY, BACILLARY; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; INFANT; MUTATION; NEUTROPHILS; SHIGELLA FLEXNERI; VIRULENCE;

BACTERIA (MICROORGANISMS); POSIBACTERIA; SHIGELLA; SHIGELLA FLEXNERI;

EID: 84862252415     PISSN: 12864579     EISSN: 1769714X     Source Type: Journal    
DOI: 10.1016/j.micinf.2012.01.009     Document Type: Article

References (45)

1. Kotloff K.L., Winickoff J.P., Ivanoff B., Clemens J.D., Swerdlow D.L., Sansonetti P.J., Adak G.K., Levine M.M. Global burden of Shigella infections: implications for vaccine development and implementation of control strategies. Bull. World Health Organ. 1999, 77:651-666.
2. Parsot C. Shigella type III secretion effectors: how, where, when, for what purposes?. Curr. Opin. Microbiol. 2009, 12:110-116.
3. Humann J., Lenz L.L. Bacterial peptidoglycan degrading enzymes and their impact on host muropeptide detection. J.Innate. Immun. 2009, 1:88-97.
4. Prager E.M., Jolles P. Animal lysozymes c and g: an overview. EXS 1996, 75:9-31.
5. Jolles P., Jolles J. What's new in lysozyme research? Always a model system, today as yesterday. Mol. Cell. Biochem. 1984, 63:165-189.
6. Girardin S.E., Tournebize R., Mavris M., Page A.L., Li X., Stark G.R., Bertin J., DiStefano P.S., Yaniv M., Sansonetti P.J., Philpott D.J. CARD4/Nod1 mediates NF-kappaB and JNK activation by invasive Shigella flexneri. EMBO Rep. 2001, 2:736-742.
7. Philpott D.J., Girardin S.E. The role of Toll-like receptors and Nod proteins in bacterial infection. Mol. Immunol. 2004, 41:1099-1108.
8. Lowell G.H., MacDermott R.P., Summers P.L., Reeder A.A., Bertovich M.J., Formal S.B. Antibody-dependent cell-mediated antibacterial activity: K lymphocytes, monocytes, and granulocytes are effective against Shigella. J. Immunol. 1980, 125:2778-2784.
9. Weinrauch Y., Drujan D., Shapiro S.D., Weiss J., Zychlinsky A. Neutrophil elastase targets virulence factors of enterobacteria. Nature 2002, 417:91-94.
10. Bellamy W., Takase M., Wakabayashi H., Kawase K., Tomita M. Antibacterial spectrum of lactoferricin B, a potent bactericidal peptide derived from the N-terminal region of bovine lactoferrin. J. Appl. Bacteriol. 1992, 73:472-479.
11. Bellamy W.R., Wakabayashi H., Takase M., Kawase K., Shimamura S., Tomita M. Role of cell-binding in the antibacterial mechanism of lactoferricin B. J. Appl. Bacteriol. 1993, 75:478-484.
12. Callewaert L., Vanoirbeek K.G., Lurquin I., Michiels C.W., Aertsen A. The Rcs two-component system regulates expression of lysozyme inhibitors and is induced by exposure to lysozyme. J. Bacteriol. 2009, 191:1979-1981.
13. Yum S., Kim M.J., Xu Y., Jin X.L., Yoo H.Y., Park J.W., Gong J.H., Choe K.M., Lee B.L., Ha N.C. Structural basis for the recognition of lysozyme by MliC, a periplasmic lysozyme inhibitor in Gram-negative bacteria. Biochem. Biophys. Res. Commun. 2009, 378:244-248.
14. Boneca I.G., Dussurget O., Cabanes D., Nahori M.A., Sousa S., Lecuit M., Psylinakis E., Bouriotis V., Hugot J.P., Giovannini M., Coyle A., Bertin J., Namane A., Rousselle J.C., Cayet N., Prevost M.C., Balloy V., Chignard M., Philpott D.J., Cossart P., Girardin S.E. A critical role for peptidoglycan N-deacetylation in Listeria evasion from the host innate immune system. Proc. Natl. Acad. Sci. U S A 2007, 104:997-1002.
15. Wang G., Olczak A., Forsberg L.S., Maier R.J. Oxidative stress-induced peptidoglycan deacetylase in Helicobacter pylori. J. Biol. Chem. 2009, 284:6790-6800.
16. Wang G., Maier S.E., Lo L.F., Maier G., Dosi S., Maier R.J. Peptidoglycan deacetylation in Helicobacter pylori contributes to bacterial survival by mitigating host immune responses. Infect. Immun. 2010, 78:4660-4666.
17. Blair D.E., Schuttelkopf A.W., MacRae J.I., van Aalten D.M. Structure and metal-dependent mechanism of peptidoglycan deacetylase, a streptococcal virulence factor. Proc. Natl. Acad. Sci. U S A 2005, 102:15429-15434.
18. Davis K.M., Akinbi H.T., Standish A.J., Weiser J.N. Resistance to mucosal lysozyme compensates for the fitness deficit of peptidoglycan modifications by Streptococcus pneumoniae. PLoS Pathog. 2008, 4:e1000241.
19. Blair D.E., van Aalten D.M. Structures of Bacillus subtilis PdaA, a family 4 carbohydrate esterase, and a complex with N-acetyl-glucosamine. FEBS Lett. 2004, 570:13-19.
20. Goldman S.R., Tu Y., Goldberg M.B. Differential regulation by magnesium of the two MsbB paralogs of Shigella flexneri. J. Bacteriol. 2008, 190:3526-3537.
21. Allaoui A., Sansonetti P.J., Parsot C. MxiJ, a lipoprotein involved in secretion of Shigella Ipa invasins, is homologous to YscJ, a secretion factor of the Yersinia Yop proteins. J. Bacteriol. 1992, 174:7661-7669.
22. Demarre G., Guerout A.M., Matsumoto-Mashimo C., Rowe-Magnus D.A., Marliere P., Mazel D. A new family of mobilizable suicide plasmids based on broad host range R388 plasmid (IncW) and RP4 plasmid (IncPalpha) conjugative machineries and their cognate Escherichia coli host strains. Res. Microbiol. 2005, 156:245-255.
23. Menard R., Sansonetti P.J., Parsot C. Nonpolar mutagenesis of the ipa genes defines IpaB, IpaC, and IpaD as effectors of Shigella flexneri entry into epithelial cells. J. Bacteriol. 1993, 175:5899-5906.
24. Popowska M., Kusio M., Szymanska P., Markiewicz Z. Inactivation of the wall-associated de-N-acetylase (PgdA) of Listeria monocytogenes results in greater susceptibility of the cells to induced autolysis. J. Microbiol. Biotechnol. 2009, 19:932-945.
25. Pycock J.F., Allen W.E., Morris T.H. Rapid, single-step isolation of equine neutrophils on a discontinuous Percoll density gradient. Res. Vet. Sci. 1987, 42:411-412.
26. Rosenthal R.S., Dziarski R. Isolation of peptidoglycan and soluble peptidoglycan fragments. Methods Enzymol. 1994, 235:253-285.
27. Buchrieser C., Glaser P., Rusniok C., Nedjari H., D'Hauteville H., Kunst F., Sansonetti P., Parsot C. The virulence plasmid pWR100 and the repertoire of proteins secreted by the type III secretion apparatus of Shigella flexneri. Mol. Microbiol. 2000, 38:760-771.
28. Caufrier F., Martinou A., Dupont C., Bouriotis V. Carbohydrate esterase family 4 enzymes: substrate specificity. Carbohydr. Res. 2003, 338:687-692.
29. Bui N.K., Turk S., Buckenmaier S., Stevenson-Jones F., Zeuch B., Gobec S., Vollmer W. Development of screening assays and discovery of initial inhibitors of pneumococcal peptidoglycan deacetylase PgdA. Biochem. Pharmacol. 2011, 82:43-52.
30. Masschalck B., Van Houdt R., Michiels C.W. High pressure increases bactericidal activity and spectrum of lactoferrin, lactoferricin and nisin. Int. J. Food Microbiol. 2001, 64:325-332.
31. Masschalck B., Van Houdt R., Van Haver E.G., Michiels C.W. Inactivation of gram-negative bacteria by lysozyme, denatured lysozyme, and lysozyme-derived peptides under high hydrostatic pressure. Appl. Environ. Microbiol. 2001, 67:339-344.
32. Roy S.C., Singh V.K., More T. Electrophoretic detection of myeloperoxidase, protease, lactoferrin and lysozyme in buffalo polymorphonuclear granular acid extracts. Vet. Res. Commun. 1997, 21:325-334.
33. Moss J.E., Fisher P.E., Vick B., Groisman E.A., Zychlinsky A. The regulatory protein PhoP controls susceptibility to the host inflammatory response in Shigella flexneri. Cell. Microbiol. 2000, 2:443-452.
34. Phalipon A., Sansonetti P.J. Shigella's ways of manipulating the host intestinal innate and adaptive immune system: a tool box for survival?. Immunol. Cell. Biol. 2007, 85:119-129.
35. Czuprynski C.J., Campbell P.A., Henson P.M. Killing of Listeria monocytogenes by human neutrophils and monocytes, but not by monocyte-derived macrophages. J. Reticuloendothel. Soc. 1983, 34:29-44.
36. Czuprynski C.J., Henson P.M., Campbell P.A. Killing of Listeria monocytogenes by inflammatory neutrophils and mononuclear phagocytes from immune and nonimmune mice. J. Leukoc. Biol. 1984, 35:193-208.
37. Mandic-Mulec I., Weiss J., Zychlinsky A. Shigella flexneri is trapped in polymorphonuclear leukocyte vacuoles and efficiently killed. Infect. Immun. 1997, 65:110-115.
38. Bera A., Herbert S., Jakob A., Vollmer W., Gotz F. Why are pathogenic staphylococci so lysozyme resistant? The peptidoglycan O-acetyltransferase OatA is the major determinant for lysozyme resistance of Staphylococcus aureus. Mol. Microbiol. 2005, 55:778-787.
39. Hebert L., Courtin P., Torelli R., Sanguinetti M., Chapot-Chartier M.P., Auffray Y., Benachour A. Enterococcus faecalis constitutes an unusual bacterial model in lysozyme resistance. Infect. Immun. 2007, 75:5390-5398.
40. Vollmer W., Tomasz A. The pgdA gene encodes for a peptidoglycan N-acetylglucosamine deacetylase in Streptococcus pneumoniae. J. Biol. Chem. 2000, 275:20496-20501.
41. Psylinakis E., Boneca I.G., Mavromatis K., Deli A., Hayhurst E., Foster S.J., Varum K.M., Bouriotis V. Peptidoglycan N-acetylglucosamine deacetylases from Bacillus cereus, highly conserved proteins in Bacillus anthracis. J. Biol. Chem. 2005, 280:30856-30863.
42. Meyrand M., Boughammoura A., Courtin P., Mezange C., Guillot A., Chapot-Chartier M.P. Peptidoglycan N-acetylglucosamine deacetylation decreases autolysis in Lactococcus lactis. Microbiology 2007, 153:3275-3285.
43. Dillard J.P., Hackett K.T. Mutations affecting peptidoglycan acetylation in Neisseria gonorrhoeae and Neisseria meningitidis. Infect. Immun. 2005, 73:5697-5705.
44. Vollmer W., Tomasz A. Peptidoglycan N-acetylglucosamine deacetylase, a putative virulence factor in Streptococcus pneumoniae. Infect. Immun. 2002, 70:7176-7178.
45. Nigro G., Fazio L.L., Martino M.C., Rossi G., Tattoli I., Liparoti V., De Castro C., Molinaro A., Philpott D.J., Bernardini M.L. Muramylpeptide shedding modulates cell sensing of Shigella flexneri. Cell. Microbiol. 2008, 10:682-695.