A novel type of peptidoglycan-binding domain highly specific for amidated D-Asp cross-bridge, identified in Lactobacillus casei bacteriophage endolysins

Journal of Biological Chemistry

Volumn 288, Issue 28, 2013, Pages 20416-20426

  Regulski, Krzysztof ^a   Courtin, Pascal ^a   Kulakauskas, Saulius ^a   Chapot Chartier, Marie Pierre ^a  

^a UMR1319 MICALIS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL STRAINS; CATALYTIC DOMAINS; CELL WALL-BINDING DOMAIN; DEGRADATION PRODUCTS; ENTEROCOCCUS FAECIUM; LACTOBACILLUS CASEI; LACTOCOCCUS LACTIS; MODULAR STRUCTURES;

AMINO ACIDS; DEGRADATION; ENZYMES;

BACTERIOPHAGES;

ALANINE; AMPICILLIN; ASPARAGINE; CARBOHYDRATE DERIVATIVE; CHLORAMPHENICOL; DEXTRO ASPARTIC ACID; ENDOLYSIN; ERYTHROMYCIN; HYDROLASE; LYSINE; N ACETYLMURAMOYLALANINE AMIDASE; PEPTIDOGLYCAN; PEPTIDOGLYCAN HYDROLASE; PROTEINASE; SERINE; UNCLASSIFIED DRUG;

AMIDATION; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL CELL; BACTERIAL CELL WALL; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIOPHAGE; BACTERIUM MUTANT; CELL WALL BINDING DOMAIN; CONTROLLED STUDY; CYTOLYSIS; ENTEROCOCCUS FAECIUM; ENZYME ACTIVE SITE; ENZYME STRUCTURE; GRAM POSITIVE BACTERIUM; LACTOBACILLUS CASEI; LACTOBACILLUS DELBRUECKII; NONHUMAN; PEPTIDOGLYCAN BINDING DOMAIN; PRIORITY JOURNAL;

BACTERIA; BACTERIOPHAGE; CELL WALL; CELL WALL-BINDING DOMAIN; ENDOLYSIN; HYDROLASES; LACTOBACILLUS; LYSIS; PEPTIDOGLYCAN; PEPTIDOGLYCAN CROSS-BRIDGE;

AMIDES; AMINO ACID SEQUENCE; ASPARAGINE; ASPARTIC ACID; BACTERIOPHAGES; BINDING SITES; CATALYTIC DOMAIN; CELL WALL; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ENDOPEPTIDASES; GRAM-POSITIVE BACTERIA; LACTOBACILLUS CASEI; MICROSCOPY, FLUORESCENCE; MOLECULAR SEQUENCE DATA; MUTATION; N-ACETYLMURAMOYL-L-ALANINE AMIDASE; PEPTIDOGLYCAN; PROPHAGES; PROTEIN BINDING; SEQUENCE HOMOLOGY, AMINO ACID; SUBSTRATE SPECIFICITY;

EID: 84880070064     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.446344     Document Type: Article

References (49)

1. Vollmer, W., Joris, B., Charlier, P., and Foster, S. (2008) Bacterial peptidoglycan (murein) hydrolases. FEMS Microbiol. Rev. 32, 259-286 (Pubitemid 351257818)
2. Chapot-Chartier, M.-P. (2010) in Prokaryotic Cell Wall Compounds (König, H., Claus, H., and Varna, A., eds) pp. 383-406, Springer Verlag Berlin, Heidelberg, Germany
3. Loessner, M. J. (2005) Bacteriophage endolysins-current state of research and applications. Curr. Opin. Microbiol. 8, 480-487
4. Hermoso, J. A., García, J. L., and García, P. (2007) Taking aim on bacterial pathogens: from phage therapy to enzybiotics. Curr. Opin. Microbiol. 10, 461-472 (Pubitemid 350064581)
5. Wang, I. N., Smith, D. L., and Young, R. (2000) Holins: the protein clocks of bacteriophage infections. Annu. Rev. Microbiol. 54, 799-825
6. Fischetti, V. A. (2008) Bacteriophage lysins as effective antibacterials. Curr. Opin. Microbiol. 11, 393-400
7. Loessner, M. J., Kramer, K., Ebel, F., and Scherer, S. (2002) C-terminal domains of Listeria monocytogenes bacteriophage murein hydrolases determine specific recognition and high affinity binding to bacterial cell wall carbohydrates. Mol. Microbiol. 44, 335-349 (Pubitemid 34429740)
8. O'Flaherty, S., Ross, R. P., and Coffey, A. (2009) Bacteriophage and their lysins for elimination of infectious bacteria. FEMS Microbiol. Rev. 33, 801-819
9. Schmelcher, M., Shabarova, T., Eugster, M. R., Eichenseher, F., Tchang, V. S., Banz, M., and Loessner, M. J. (2010) Rapid multiplex detection and differentiation of Listeria cells by use of fluorescent phage endolysin cell wall binding domains. Appl. Environ. Microbiol. 76, 5745-5756
10. Lee, S. Y., Choi, J. H., and Xu, Z. (2003) Microbial cell-surface display. Trends Biotechnol. 21, 45-52 (Pubitemid 35441293)
11. Bermúdez-Humarán, L. G., Kharrat, P., Chatel, J. M., and Langella, P. (2011) Lactococci and lactobacilli as mucosal delivery vectors for therapeutic proteins and DNA vaccines. Microb. Cell Fact. 10, S4
12. Leenhouts, K., Buist, G., and Kok, J. (1999) Anchoring of proteins to lactic acid bacteria. Antonie Van Leeuwenhoek 76, 367-376 (Pubitemid 29440740)
13. Ribelles, P., Rodríguez, I., and Suárez, J. E. (2012) LysA2, the Lactobacillus casei bacteriophage A2 lysin is an endopeptidase active on a wide spectrum of lactic acid bacteria. Appl. Microbiol. Biotechnol. 94, 101-110
14. Regulski, K., Courtin, P., Meyrand, M., Claes, I. J., Lebeer, S., Vanderleyden, J., Hols, P., Guillot, A., and Chapot-Chartier, M. P. (2012) Analysis of the peptidoglycan hydrolase complement of Lactobacillus casei and characterization of the major γ-D-glutamyl-L-lysyl endopeptidase. PLoS One 7, e32301
15. Finn, R. D., Mistry, J., Tate, J., Coggill, P., Heger, A., Pollington, J. E., Gavin, O. L., Gunasekaran, P., Ceric, G., Forslund, K., Holm, L., Sonnhammer, E. L., Eddy, S. R., and Bateman, A. (2010) The Pfam protein families database. Nucleic Acids Res. 38, D211-D222
16. Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2nd Ed., Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
17. Dower, W. J., Miller, J. F., and Ragsdale, C. W. (1988) High efficiency transformation of E. coli by high voltage electroporation. Nucleic Acids Res. 16, 6127-6145
18. Huard, C., Miranda, G., Wessner, F., Bolotin, A., Hansen, J., Foster, S. J., and Chapot-Chartier, M. P. (2003) Characterization of AcmB, an N-acetylglucosaminidase autolysin from Lactococcus lactis. Microbiology 149, 695-705 (Pubitemid 36395104)
19. Meyrand, M., Boughammoura, A., Courtin, P., Mézange, C., Guillot, A., and Chapot-Chartier, M.-P. (2007) Peptidoglycan N-acetylglucosamine deacetylation decreases autolysis in Lactococcus lactis. Microbiology 153, 3275-3285 (Pubitemid 47629533)
20. Courtin, P., Miranda, G., Guillot, A., Wessner, F., Mézange, C., Domakova, E., Kulakauskas, S., and Chapot-Chartier, M. P. (2006) Peptidoglycan structure analysis of Lactococcus lactis reveals the presence of an LD-carboxypeptidase involved in peptidoglycan maturation. J. Bacteriol. 188, 5293-5298 (Pubitemid 44051497)
21. Kashige, N., Nakashima, Y., Miake, F., and Watanabe, K. (2000) Cloning, sequence analysis, and expression of Lactobacillus casei phage PL-1 lysis genes. Arch. Virol. 145, 1521-1534
22. 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 cross-bridge. J. Bacteriol. 191, 3752-3757
23. Veiga, P., Piquet, S., Maisons, A., Furlan, S., Courtin, P., Chapot-Chartier, M. P., and Kulakauskas, S. (2006) Identification of an essential gene responsible for D-Asp incorporation in the Lactococcus lactis peptidoglycan cross-bridge. Mol. Microbiol. 62, 1713-1724 (Pubitemid 44813815)
24. Mainardi, J. L., Legrand, R., Arthur, M., Schoot, B., van Heijenoort, J., and Gutmann, L. (2000) Novel mechanism of β-lactam resistance due to bypass of DD-transpeptidation in Enterococcus faecium. J. Biol. Chem. 275, 16490-16496 (Pubitemid 30398871)
25. Chapot-Chartier, M. P., Vinogradov, E., Sadovskaya, I., Andre, G., Mistou, M. Y., Trieu-Cuot, P., Furlan, S., Bidnenko, E., Courtin, P., Péchoux, C., Hols, P., Dufrêne, Y. F., and Kulakauskas, S. (2010) The cell surface of Lactococcus lactis is covered by a protective polysaccharide pellicle. J. Biol. Chem. 285, 10464-10471
26. Bosma, T., Kanninga, R., Neef, J., Audouy, S. A., van Roosmalen, M. L., Steen, A., Buist, G., Kok, J., Kuipers, O. P., Robillard, G., and Leenhouts, K. (2006) Novel surface display system for proteins on nongenetically modified Gram-positive bacteria. Appl. Environ. Microbiol. 72, 880-889
27. García, E., García, J. L., García, P., Arrarás, A., Sánchez-Puelles, J. M., and López, R. (1988) Molecular evolution of lytic enzymes of Streptococcus pneumoniae and its bacteriophages. Proc. Natl. Acad. Sci. U.S.A. 85, 914-918
28. Eugster, M. R., Haug, M. C., Huwiler, S. G., and Loessner, M. J. (2011) The cell wall binding domain of Listeria bacteriophage endolysin PlyP35 recognizes terminal GlcNAc residues in cell wall teichoic acid. Mol. Microbiol. 81, 1419-1432
29. Mo, K. F., Li, X., Li, H., Low, L. Y., Quinn, C. P., and Boons, G. J. (2012) Endolysins of Bacillus anthracis bacteriophages recognize unique carbohydrate epitopes of vegetative cell wall polysaccharides with high affinity and selectivity. J. Am. Chem. Soc. 134, 15556-15562
30. Bustamante, N., Campillo, N. E., García, E., Gallego, C., Pera, B., Diakun, G. P., Sáiz, J. L., García, P., Díaz, J. F., and Menéndez, M. (2010) Cpl-7, a lysozyme encoded by a pneumococcal bacteriophage with a novel cell wall-binding motif. J. Biol. Chem. 285, 33184-33196
31. Bustamante, N., Rico-Lastres, P., García, E., García, P., and Menéndez, M. (2012) Thermal Stability of Cpl-7 Endolysin from the Streptococcus pneumoniae bacteriophage Cp-7; cell wall targeting of its CW-7 motifs. PLoS One 7, e46654
32. Eugster, M. R., and Loessner, M. J. (2012) Wall teichoic acids restrict access of bacteriophage endolysin Ply118, Ply511, and PlyP40 cell wall binding domains to the Listeria monocytogenes peptidoglycan. J. Bacteriol. 194, 6498-6506
33. Hu, S., Kong, J., Kong, W., Guo, T., and Ji, M. (2010) Characterization of a novel LysM domain from Lactobacillus fermentum bacteriophage endolysin and its use as an anchor to display heterologous proteins on the surfaces of lactic acid bacteria. Appl. Environ. Microbiol. 76, 2410-2418
34. Steen, A., Buist, G., Leenhouts, K. J., El Khattabi, M., Grijpstra, F., Zomer, A. L., Venema, G., Kuipers, O. P., and Kok, J. (2003) Cell wall attachment of a widely distributed peptidoglycan binding domain is hindered by cell wall constituents. J. Biol. Chem. 278, 23874-23881 (Pubitemid 36830214)
35. Frankel, M. B., and Schneewind, O. (2012) Determinants of murein hydrolase targeting to cross-wall of Staphylococcus aureus peptidoglycan. J. Biol. Chem. 287, 10460-10471
36. Pritchard, D. G., Dong, S., Kirk, M. C., Cartee, R. T., and Baker, J. R. (2007) LambdaSa1 and LambdaSa2 prophage lysins of Streptococcus agalactiae. Appl. Environ. Microbiol. 73, 7150-7154 (Pubitemid 350196661)
37. Gründling, A., and Schneewind, O. (2006) Cross-linked peptidoglycan mediates lysostaphin binding to the cell wall envelope of Staphylococcus aureus. J. Bacteriol. 188, 2463-2472
38. Lu, J. Z., Fujiwara, T., Komatsuzawa, H., Sugai, M., and Sakon, J. (2006) Cell wall-targeting domain of glycylglycine endopeptidase distinguishes among peptidoglycan cross-bridges. J. Biol. Chem. 281, 549-558 (Pubitemid 43671218)
39. Ribelles, P., Benbouziane, B., Langella, P., Suärez, J. E., and Bermüdez-Humarán, L. G. (2013) Protection against human papillomavirus type 16-induced tumors in mice using nongenetically modified lactic acid bacteria displaying E7 antigen at its surface. Appl. Microbiol. Biotechnol. 97, 1231-1239
40. Garneau, J. E., and Moineau, S. (2011) Bacteriophages of lactic acid bacteria and their impact on milk fermentations. Microb. Cell Fact. 10, S20
41. Lortal, S., and Chapot-Chartier, M. P. (2005) Role, mechanisms and control of lactic acid bacteria lysis in cheese. Int. Dairy J. 15, 857-871 (Pubitemid 40743083)
42. Gasson, M. J. (1996) Lytic systems in lactic acid bacteria and their bacteriophages. Antonie Van Leeuwenhoek 70, 147-159
43. Nilsen, T., Nes, I. F., and Holo, H. (2003) Enterolysin A, a cell wall-degrading bacteriocin from Enterococcus faecalis LMG 2333. Appl. Environ. Microbiol. 69, 2975-2984 (Pubitemid 36560382)
44. Acedo-Félix, E., and Pérez-Martínez, G. (2003) Significant differences between Lactobacillus casei subsp. casei ATCC 393T and a commonly used plasmid-cured derivative revealed by a polyphasic study. Int. J. Syst. Evol. Microbiol. 53, 67-75
45. Gasson, M. J. (1983) Plasmid complements of Streptococcus lactis NCDO 712 and other lactic streptococci after protoplast-induced curing. J. Bacteriol. 154, 1-9
46. Kuipers, O. P., de Ruyter P. G., Kleerebezem M., and de Vos, W. M. (1998) Quorum sensing-controlled gene expression in lactic acid bacteria. J. Biotechnol. 64, 15-21 (Pubitemid 29027781)
47. Veiga, P., Bulbarela-Sampieri, C., Furlan, S., Maisons, A., Chapot-Chartier, M.-P., Erkelenz, M., Mervelet, P., Noirot, P., Frees, D., Kuipers, O. P., Kok, J., Gruss, A., Buist, G., and Kulakauskas, S. (2007) SpxB regu-lates O-acetylation-dependent resistance of Lactococcus lactis peptidoglycan to hydrolysis. J. Biol. Chem. 282, 19342-19354 (Pubitemid 47100109)
48. Roces, C., Courtin, P., Kulakauskas, S., Rodríguez, A., Chapot-Chartier, M. P., and Martínez, B. (2012) Isolation of Lactococcus lactis mutants simultaneously resistant to the cell wall-active bacteriocin Lcn972, lysozyme, nisin, and bacteriophage c2. Appl. Environ. Microbiol. 78, 4157-4163
49. Schleifer, K. H., and Kandler, O. (1972) Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol. Rev. 36, 407-477