Characterization of Acp, a peptidoglycan hydrolase of Clostridium perfringens with N-acetylglucosaminidase activity that is implicated in cell separation and stress-induced autolysis

Journal of Bacteriology

Volumn 192, Issue 9, 2010, Pages 2373-2384

  Camiade, Emilie ^a,b   Peltier, Johann ^a   Bourgeois, Ingrid ^a   Couture Tosi, Evelyne ^b   Courtin, Pascal ^c   Antunes, Ana ^b   Chapot Chartier, Marie Pierre ^c   Dupuy, Bruno ^b   Pons, Jean Louis ^a  

^a ROUEN UNIVERSITY HOSPITAL   (France)

^b INSTITUT PASTEUR   (France)

^c UMR1319 MICALIS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLGLUCOSAMINIDASE; HYDROLASE; PEPTIDOGLYCAN;

AMINO TERMINAL SEQUENCE; ARTICLE; AUTOLYSIS; BACILLUS SUBTILIS; BACTERIAL GROWTH; CATALYSIS; CELL DIVISION; CELL SEPARATION; CELL WALL; CLOSTRIDIUM PERFRINGENS; CONTROLLED STUDY; ENZYME ACTIVITY; FRACTIONATION; GENE EXPRESSION; GENE IDENTIFICATION; HYDROLYSIS; IMMUNOFLUORESCENCE; INTRON; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MICROSCOPY; NONHUMAN; PLANT CELL; PRIORITY JOURNAL; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; VEGETATIVE GROWTH;

ACETYLGLUCOSAMINIDASE; ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; BACTERIOLYSIS; BLOTTING, WESTERN; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CLOSTRIDIUM PERFRINGENS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; GENOME, BACTERIAL; MICROBIAL SENSITIVITY TESTS; MOLECULAR SEQUENCE DATA; MUTAGENESIS; N-ACETYLMURAMOYL-L-ALANINE AMIDASE; OCTOXYNOL; PEPTIDOGLYCAN; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); CLOSTRIDIUM PERFRINGENS; POSIBACTERIA;

EID: 77951031857     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.01546-09     Document Type: Article

References (60)

1. Allignet, J., P. England, I. Old, and N. El Solh. 2002. Several regions of the repeat domain of the Staphylococcus caprae autolysin, AtlC, are involved in fibronectin binding. FEMS Microbiol. Lett. 213:193-197.
2. Atrih, A., G. Bacher, G. Allmaier, M. P. Williamson, and S. J. Foster. 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.
3. Bateman, A., and M. Bycroft. 2000. The structure of a LysM domain from E. coli membrane-bound lytic murein transglycosylase D (MltD). J. Mol. Biol. 299:1113-1119.
4. Berry, A. M., R. A. Lock, D. Hansman, and J. C. Paton. 1989. Contribution of autolysin to virulence of Streptococcus pneumoniae. Infect. Immun. 57: 2324-2330.
5. Bourgeois, I., E. Camiade, R. Biswas, P. Courtin, L. Gibert, F. Gotz, M. P. Chapot-Chartier, J. L. Pons, and M. Pestel-Caron. 2009. Characterization of AtlL, a bifunctional autolysin of Staphylococcus lugdunensis with N-acetylglucosaminidase and N-acetylmuramoyl-l-alanine amidase activities. FEMS Microbiol. Lett. 290:105-113.
6. Bourgeois, I., M. Pestel-Caron, J. F. Lemeland, J. L. Pons, and F. Caron. 2007. Tolerance to the glycopeptides vancomycin and teicoplanin in coagulase-negative staphylococci. Antimicrob. Agents Chemother. 51:740-743.
7. Bravetti, A. L., S. Mesnage, A. Lefort, F. Chau, C. Eckert, L. Garry, M. Arthur, and B. Fantin. 2009. Contribution of the autolysin AtlA to the bactericidal activity of amoxicillin against Enterococcus faecalis JH2-2. Antimicrob. Agents Chemother. 53:1667-1669.
8. Candela, T., and A. Fouet. 2005. Bacillus anthracis CapD, belonging to the gamma-glutamyltranspeptidase family, is required for the covalent anchoring of capsule to peptidoglycan. Mol. Microbiol. 57:717-726.
9. Chen, Y., S. Miyata, S. Makino, and R. Moriyama. 1997. Molecular characterization of a germination-specific muramidase from Clostridium perfringens S40 spores and nucleotide sequence of the corresponding gene. J. Bacteriol. 179:3181-3187.
10. Cleveland, R. F., A. J. Wicken, L. Daneo-Moore, and G. D. Shockman. 1976. Inhibition of wall autolysis in Streptococcus faecalis by lipoteichoic acid and lipids. J. Bacteriol. 126:192-197.
11. Courtin, P., G. Miranda, A. Guillot, F. Wessner, C. Mezange, E. Domakova, S. Kulakauskas, and M. P. Chapot-Chartier. 2006. Peptidoglycan structure analysis of Lactococcus lactis reveals the presence of an L, D-carboxypeptidase involved in peptidoglycan maturation. J. Bacteriol. 188:5293-5298.
12. De Las Rivas, B., J. L. Garcia, R. Lopez, and P. Garcia. 2002. Purification and polar localization of pneumococcal LytB, a putative endo-beta-N-acetylglucosaminidase: the chain-dispersing murein hydrolase. J. Bacteriol. 184: 4988-5000.
13. Dhalluin, A., I. Bourgeois, M. Pestel-Caron, E. Camiade, G. Raux, P. Courtin, M. P. Chapot-Chartier, and J. L. Pons. 2005. Acd, a peptidoglycan hydrolase of Clostridium difficile with N-acetylglucosaminidase activity. Microbiology 151:2343-2351.
14. Foster, S. J. 1991. Cloning, expression, sequence analysis and biochemical characterization of an autolytic amidase of Bacillus subtilis 168 trpC2. J. Gen. Microbiol. 137:1987-1998.
15. Gazzola, S., and P. S. Cocconcelli. 2008. Vancomycin heteroresistance and biofilm formation in Staphylococcus epidermidis from food. Microbiology 154:3224-3231.
16. Ghuysen, J. M., D. J. Tipper, and J. L. Strominger. 1966. Enzymes that degrade bacterial cell walls. Methods Enzymol. 8:685-699.
17. Ginsburg, I. 2002. Role of lipoteichoic acid in infection and inflammation. Lancet Infect. Dis. 2:171-179.
18. Goda, H. M., K. Ushigusa, H. Ito, N. Okino, H. Narimatsu, and M. Ito. 2008. Molecular cloning, expression, and characterization of a novel endo-alpha-N-acetylgalactosaminidase from Enterococcus faecalis. Biochem. Biophys. Res. Commun. 375:441-446.
19. Gupta, P., and Y. Chen. 2008. Chromosomal engineering of Clostridium perfringens using group II introns. Methods Mol. Biol. 435:217-228.
20. Heilmann, C., M. Hussain, G. Peters, and F. Gotz. 1997. Evidence for autolysin-mediated primary attachment of Staphylococcus epidermidis to a polystyrene surface. Mol. Microbiol. 24:1013-1024.
21. Hell, W., H. G. Meyer, and S. G. Gatermann. 1998. Cloning of aas, a gene encoding a Staphylococcus saprophyticus surface protein with adhesive and autolytic properties. Mol. Microbiol. 29:871-881.
22. Hirst, R. A., B. Gosai, A. Rutman, C. J. Guerin, P. Nicotera, P. W. Andrew, and C. O'Callaghan. 2008. Streptococcus pneumoniae deficient in pneumolysin or autolysin has reduced virulence in meningitis. J. Infect. Dis. 197: 744-751.
23. Hofmann, A. F. 1994. Bile acids, p. 677-718. In I. M. Arias, J. L. Boyer, N. Fausto, W. B. Jackoby, D. A. Schachter, and D. A. Shafritz (ed.), The liver: biology and pathobiology. Raven Press, New York, NY.
24. Horsburgh, G. J., A. Atrih, M. P. Williamson, and S. J. Foster. 2003. LytG of Bacillus subtilis is a novel peptidoglycan hydrolase: the major active glucosaminidase. Biochemistry 42:257-264.
25. Huard, C., G. Miranda, F. Wessner, A. Bolotin, J. Hansen, S. J. Foster, and M. P. Chapot-Chartier. 2003. Characterization of AcmB, an N-acetylglucosaminidase autolysin from Lactococcus lactis. Microbiology 149:695-705.
26. Humann, J., R. Bjordahl, K. Andreasen, and L. L. Lenz. 2007. Expression of the p60 autolysin enhances NK cell activation and is required for Listeria monocytogenes expansion in IFN-gamma-responsive mice. J. Immunol. 178: 2407-2414.
27. Humann, J., and L. L. Lenz. 2009. Bacterial peptidoglycan degrading enzymes and their impact on host muropeptide detection. J. Innate Immun. 1:88-97.
28. Jirásková, A., L. Vitek, J. Fevery, T. Ruml, and P. Branny. 2005. Rapid protocol for electroporation of Clostridium perfringens. J. Microbiol. Methods 62:125-127.
29. Johnsborg, O., and L. S. Havarstein. 2009. Pneumococcal LytR, a protein from the LytR-CpsA-Psr family, is essential for normal septum formation in Streptococcus pneumoniae. J. Bacteriol. 191:5859-5864.
30. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
31. Leclerc, D., and A. Asselin. 1989. Detection of bacterial cell wall hydrolases after denaturing polyacrylamide gel electrophoresis. Can. J. Microbiol. 35: 749-753.
32. Lenz, L. L., S. Mohammadi, A. Geissler, and D. A. Portnoy. 2003. SecA2-dependent secretion of autolytic enzymes promotes Listeria monocytogenes pathogenesis. Proc. Natl. Acad. Sci. U. S. A. 100:12432-12437.
33. T Method. Methods 25:402-408.
34. Margot, P., M. Pagni, and D. Karamata. 1999. Bacillus subtilis 168 gene lytF encodes a gamma-D-glutamate-meso-diaminopimelate muropeptidase expressed by the alternative vegetative sigma factor, sigmaD. Microbiology 145:57-65.
35. Mesnage, S., F. Chau, L. Dubost, and M. Arthur. 2008. Role of N-acetylglucosaminidase and N-acetylmuramidase activities in Enterococcus faecalis peptidoglycan metabolism. J. Biol. Chem. 283:19845-19853.
36. Meyrand, M., A. Boughammoura, P. Courtin, C. Mezange, A. Guillot, and M. P. Chapot-Chartier. 2007. Peptidoglycan N-acetylglucosamine deacetylation decreases autolysis in Lactococcus lactis. Microbiology 153:3275-3285.
37. Miyata, S., S. Kozuka, Y. Yasuda, Y. Chen, R. Moriyama, K. Tochikubo, and S. Makino. 1997. Localization of germination-specific spore-lytic enzymes in Clostridium perfringens S40 spores detected by immunoelectron microscopy. FEMS Microbiol. Lett. 152:243-247.
38. Miyata, S., R. Moriyama, N. Miyahara, and S. Makino. 1995. A gene (sleC) encoding a spore-cortex-lytic enzyme from Clostridium perfringens S40 spores; cloning, sequence analysis and molecular characterization. Microbiology 141:2643-2650.
39. Moreillon, P., Z. Markiewicz, S. Nachman, and A. Tomasz. 1990. Two bactericidal targets for penicillin in pneumococci: autolysis-dependent and autolysis-independent killing mechanisms. Antimicrob. Agents Chemother. 34:33-39.
40. Myhre, A. E., J. F. Stuestol, M. K. Dahle, G. Overland, C. Thiemermann, S. J. Foster, P. Lilleaasen, A. O. Aasen, and J. E. Wang. 2004. Organ injury and cytokine release caused by peptidoglycan are dependent on the structural integrity of the glycan chain. Infect. Immun. 72:1311-1317.
41. Neuhaus, F. C., and J. Baddiley. 2003. A continuum of anionic charge: structures and functions of D-alanyl-teichoic acids in gram-positive bacteria. Microbiol. Mol. Biol. Rev. 67:686-723.
42. Obregón, V., P. Garcia, E. Garcia, A. Fenoll, R. Lopez, and J. L. Garcia. 2002. Molecular peculiarities of the lytA gene isolated from clinical pneumococcal strains that are bile insoluble. J. Clin. Microbiol. 40:2545-2554.
43. Oshida, T., M. Sugai, H. Komatsuzawa, Y. M. Hong, H. Suginaka, and A. Tomasz. 1995. A Staphylococcus aureus autolysin that has an N-acetylmuramoyl-L- alanine amidase domain and an endo-beta-N-acetylglucosaminidase domain: cloning, sequence analysis, and characterization. Proc. Natl. Acad. Sci. U. S. A. 92:285-289.
44. Oshida, T., and A. Tomasz. 1992. Isolation and characterization of a Tn551-autolysis mutant of Staphylococcus aureus. J. Bacteriol. 174:4952-4959.
45. Paredes-Sabja, D., P. Setlow, and M. R. Sarker. 2009. SleC is essential for cortex peptidoglycan hydrolysis during germination of spores of the pathogenic bacterium Clostridium perfringens. J. Bacteriol. 191:2711-2720.
46. Qin, X., K. V. Singh, Y. Xu, G. M. Weinstock, and B. E. Murray. 1998. Effect of disruption of a gene encoding an autolysin of Enterococcus faecalis OG1RF. Antimicrob. Agents Chemother. 42:2883-2888.
47. Qin, Z., Y. Ou, L. Yang, Y. Zhu, T. Tolker-Nielsen, S. Molin, and D. Qu. 2007. Role of autolysin-mediated DNA release in biofilm formation of Staphylococcus epidermidis. Microbiology 153:2083-2092.
48. Rashid, M. H., M. Mori, and J. Sekiguchi. 1995. Glucosaminidase of Bacillus subtilis: cloning, regulation, primary structure and biochemical characterization. Microbiology 141:2391-2404.
49. Raychaudhuri, D., and A. N. Chatterjee. 1985. Use of resistant mutants to study the interaction of triton X-100 with Staphylococcus aureus. J. Bacteriol. 164:1337-1349.
50. Shibata, Y., M. Kawada, Y. Nakano, K. Toyoshima, and Y. Yamashita. 2005. Identification and characterization of an autolysin-encoding gene of Streptococcus mutans. Infect. Immun. 73:3512-3520.
51. Shimamoto, S., R. Moriyama, K. Sugimoto, S. Miyata, and S. Makino. 2001. Partial characterization of an enzyme fraction with protease activity which converts the spore peptidoglycan hydrolase (SleC) precursor to an active enzyme during germination of Clostridium perfringens S40 spores and analysis of a gene cluster involved in the activity. J. Bacteriol. 183:3742-3751.
52. Shimizu, T., S. Ohshima, K. Ohtani, T. Shimizu, and H. Hayashi. 2001. Genomic map of Clostridium perfringens strain 13. Microbiol. Immunol. 45:179-189.
53. Shockman, G. D., and J.-V. Höltje. 1994. Microbial peptidoglycan (murein) hydrolases, p. 131-166. Elsevier Science B. V., Amsterdam, Netherlands.
54. Smith, T. J., S. A. Blackman, and S. J. Foster. 2000. Autolysins of Bacillus subtilis: multiple enzymes with multiple functions. Microbiology 146:249-262.
55. Thomasz, A. 2000. The staphylococcal cell wall, p. 351-360. In V. A. Fischetti (ed.), Gram-positive pathogens. American Society for Microbiology, Washington, DC.
56. Tjalsma, H., H. Antelmann, J. D. Jongbloed, P. G. Braun, E. Darmon, R. Dorenbos, J. Y. Dubois, H. Westers, G. Zanen, W. J. Quax, O. P. Kuipers, S. Bron, M. Hecker, and J. M. van Dijl. 2004. Proteomics of protein secretion by Bacillus subtilis: separating the "secrets" of the secretome. Microbiol. Mol. Biol. Rev. 68:207-233.
57. Tomasz, A., P. Moreillon, and G. Pozzi. 1988. Insertional inactivation of the major autolysin gene of Streptococcus pneumoniae. J. Bacteriol. 170:5931-5934.
58. Vollmer, W., B. Joris, P. Charlier, and S. Foster. 2008. Bacterial peptidoglycan (murein) hydrolases. FEMS Microbiol. Rev. 32:259-286.
59. Wang, L., and M. Lin. 2008. A novel cell wall-anchored peptidoglycan hydrolase (autolysin), IspC, essential for Listeria monocytogenes virulence: genetic and proteomic analysis. Microbiology 154:1900-1913.
60. Ward, J. B., and R. Williamson. 1984. Bacterial autolysins: specificity and function, p. 159-166. In C. Nombela (ed.), Microbial cell wall synthesis and autolysis. Elsevier Science Publishers, Amsterdam, Netherlands.