X-ray structure of a novel endolysin encoded by episomal phage phiSM101 of Clostridium perfringens

Molecular Microbiology

Volumn 92, Issue 2, 2014, Pages 326-337

  Tamai, Eiji ^a,b   Yoshida, Hiromi ^a   Sekiya, Hiroshi ^b   Nariya, Hirofumi ^a   Miyata, Shigeru ^a,c   Okabe, Akinobu ^d   Kuwahara, Tomomi ^a   Maki, Jun ^b   Kamitori, Shigehiro ^a  

^a KAGAWA UNIVERSITY   (Japan)

^b MATSUYAMA UNIVERSITY   (Japan)

^c CHUBU UNIVERSITY   (Japan)

^d Chugoku Gakuen University   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOLYSIN; N ACETYLGLUCOSAMINE; UNCLASSIFIED DRUG; VIRUS ENZYME; PROTEIN BINDING; PROTEINASE;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL CELL WALL; BACTERIAL STRAIN; BACTERIOPHAGE; BACTERIOPHAGE PHISM101; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CLOSTRIDIUM PERFRINGENS; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME STRUCTURE; LIGAND BINDING; NONHUMAN; PRIORITY JOURNAL; SRC HOMOLOGY DOMAIN; STRUCTURE ANALYSIS; TANDEM REPEAT; X RAY CRYSTALLOGRAPHY; CHEMICAL STRUCTURE; CHEMISTRY; ENZYMOLOGY; METABOLISM; PROTEIN CONFORMATION; VIROLOGY;

ACETYLGLUCOSAMINE; BACTERIOPHAGES; CLOSTRIDIUM PERFRINGENS; ENDOPEPTIDASES; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION;

EID: 84897963241     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12559     Document Type: Article

References (57)

1. van Aalten, D.M., Komander, D., Synstad, B., Gåseidnes, S., Peter, M.G., and Eijsink, V.G. (2001) Structural insights into the catalytic mechanism of a family 18 exo-chitinase. Proc Natl Acad Sci USA 98: 8979-8984.
2. Adak, G.K., Long, S.M., and O'Brien, S.J. (2000) Trends in indigenous foodborne disease and deaths, England and Wales: 1992 to 2000. Gut 51: 832-841.
3. Beeby, M., Gumbart, J.C., Roux, B., and Jensen, G.J. (2013) Architecture and assembly of the Gram-positive cell wall. Mol Microbiol 88: 664-672.
4. Brünger, A.T. (1993) X-PLOR 3.1: A System for X-ray Crystallography and NMR. New Haven and London: Yale University Press.
5. Bryant, A.E., Bayer, C.R., Aldape, M.J., Wallace, R.J., Titball, R.W., and Stevens, D.L. (2006) Clostridium perfringens phospholipase C-induced platelet/leukocyte interactions impede neutrophil diapedesis. J Med Microbiol 55: 495-504.
6. Cantarel, B.L., Coutinho, P.M., Rancurel, C., Bernard, T., Lombard, V., and Henrissat, B. (2009) The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Res 37: D233-D238.
7. Collaborative Computational Project 4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50: 760-763.
8. Courchesne, N.M., Parisien, A., and Lan, C.Q. (2009) Production and application of bacteriophage and bacteriophage-encoded lysins. Recent Pat Biotechnol 3: 37-45.
9. Croux, C., Ronda, C., López, R., and García, J.L. (1993) Interchange of functional domains switches enzyme specificity: construction of a chimeric pneumococcal-clostridial cell wall lytic enzyme. Mol Microbiol 9: 1019-1025.
10. DeLano, W.L. (2002) The PyMOL Molecular Graphics System. San Carlos, CA, USA: DeLano Scientific [WWW document]. URL http://www.pymol.org/
11. Dhalluin, A., Bourgeois, I., Pestel-Caron, M., Camiade, E., Raux, G., Courtin, P., etal. (2005) Acd, a peptidoglycan hydrolase of Clostridium difficile with N-acetylglucosaminidase activity. Microbiology 151: 2343-2351.
12. Dmitriev, B.A., Toukach, F.V., Schaper, K.J., Holst, O., Rietschel, E.T., and Ehlers, S. (2003) Tertiary structure of bacterial murein: the scaffold model. J Bacteriol 185: 3458-3468.
13. Emsley, P., and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132.
14. 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.
15. Fischetti, V.A. (2008) Bacteriophage lysins as effective antibacterials. Curr Opin Microbiol 11: 393-400.
16. Gerova, M., Halgasova, N., Ugorcakova, J., and Bukovska, G. (2011) Endolysin of bacteriophage BFK20: evidence of a catalytic and a cell wall binding domain. FEMS Microbiol Lett 321: 83-91.
17. Ghuysen, J.M. (1968) Structure of the meso-diaminopimelic acid containing peptidoglycans in Escherichia coli B and Bacillus megaterium KM. Bacteriol Rev 32: 425-464.
18. Hayhurst, E.J., Kailas, L., Hobbs, J.K., and Foster, S.J. (2008) Cell wall peptidoglycan architecture in Bacillus subtilis. Proc Natl Acad Sci USA 105: 14603-14608.
19. Hermoso, J.A., Monterroso, B., Albert, A., Galán, B., Ahrazem, O., García, P., etal. (2003) Structural basis for selective recognition of pneumococcal cell wall by modular endolysin from phage Cp-1. Structure 11: 1239-1249.
20. Ho, S.N., Hunt, H.D., Horton, R.M., Pullen, J.K., and Pease, L.R. (1989) Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77: 51-59.
21. Holm, L., and Rosenström, P. (2010) Dali server: conservation mapping in 3D. Nucleic Acids Res 38: W545-W549.
22. Korczynska, J.E., Danielsen, S., Schagerlöf, U., Turkenburg, J.P., Davies, G.J., Wilson, K.S., and Taylor, E.J. (2010) The structure of a family GH25 lysozyme from Aspergillus fumigatus. Acta Crystallograph Sect F Struct Biol Cryst Commun 66: 973-977.
23. Laskowski, R.A., MacArthur, M.W., Moss, D.S., and Thornton, J.M. (1992) PROCHECK v.2: Programs to Check the Stereochemical Quality of Protein Structures. Oxford, England: Oxford Molecular.
24. Layec, S., Decaris, B., and Leblond-Bourget, N. (2008) Diversity of Firmicutes peptidoglycan hydrolases and specificities of those involved in daughter cell separation. Res Microbiol 159: 507-515.
25. Leyh-Bouille, M., Bonaly, R., Ghuysen, J.M., Tinelli, R., and Tipper, D. (1970) LL-diaminopimelic acid containing peptidoglycans in walls of Streptomyces sp. and of Clostridium perfringens (type A). Biochemistry 9: 2944-2952.
26. Loeffler, J.M., and Fischetti, V.A. (2003) Synergistic lethal effect of a combination of phage lytic enzymes with different activities on penicillin-sensitive and -resistant Streptococcus pneumoniae strains. Antimicrob Agents Chemother 47: 375-377.
27. Low, L.Y., Yang, C., Perego, M., Osterman, A., and Liddington, R.C. (2005) Structure and lytic activity of a Bacillus anthracis prophage endolysin. J Biol Chem 280: 35433-35439.
28. 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.
29. Lynch, M., Painter, J., Woodruff, R., and Braden, C. (2006) Surveillance for foodborne-disease outbreaks - United States, 1998-2002. MMWR Surveill Summ 55: 1-42.
30. McGowan, S., Buckle, A.M., Mitchell, M.S., Hoopes, J.T., Gallagher, D.T., Heselpoth, R.D., etal. (2012) X-ray crystal structure of the streptococcal specific phage lysin PlyC. Proc Natl Acad Sci USA 109: 12752-12757.
31. McRee, D.E. (1999) XtalView/Xfit: a versatile program for manipulating atomic coordinate and electron density. J Struct Biol 125: 156-165.
32. Martinez-Fleites, C., Korczynska, J.E., Davies, G.J., Cope, M.J., Turkenburg, J.P., and Taylor, E.J. (2009) The crystal structure of a family GH25 lysozyme from Bacillus anthracis implies a neighboring-group catalytic mechanism with retention of anomeric configuration. Carbohydr Res 344: 1753-1757.
33. Meroueh, S.O., Bencze, K.Z., Hesek, D., Lee, M., Fisher, J.F., Stemmler, T.L., and Mobashery, S. (2006) Three-dimensional structure of the bacterial cell wall peptidoglycan. Proc Natl Acad Sci USA 103: 4404-4409.
34. Murshudov, G.N., Vagin, A.A., and Dodson, E.J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53: 240-255.
35. Myers, G.S., Rasko, D.A., Cheung, J.K., Ravel, J., Seshadri, R., DeBoy, R.T., etal. (2006) Skewed genomic variability in strains of the toxigenic bacterial pathogen, Clostridium perfringens. Genome Res 16: 1031-1040.
36. Nariya, H., Miyata, S., Tamai, E., Sekiya, H., Maki, J., and Okabe, A. (2011) Identification and characterization of a putative endolysin encoded by episomal phage phiSM101 of Clostridium perfringens. Appl Microbiol Biotechnol 90: 1973-1979.
37. 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.
38. Otwinowski, Z., and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 276 (Macromolecular Crystallography, part A): 307-326.
39. Pérez-Dorado, I., Campillo, N.E., Monterroso, B., Hesek, D., Lee, M., Páez, J.A., etal. (2007) Elucidation of the molecular recognition of bacterial cell wall by modular pneumococcal phage endolysin CPL-1. J Biol Chem 282: 24990-24999.
40. Pérez-Dorado, I., González, A., Morales, M., Sanles, R., Striker, W., Vollmer, W., etal. (2010) Insights into pneumococcal fratricide from the crystal structures of the modular killing factor LytC. Nat Struct Mol Biol 17: 576-581.
41. Popham, D.L. (2013) Visualizing the production and arrangement of peptidoglycan in Gram-positive cells. Mol Microbiol 88: 645-649.
42. Porter, C.J., Schuch, R., Pelzek, A.J., Buckle, A.M., McGowan, S., Wilce, M.C., etal. (2006) The 1.6Å crystal structure of the catalytic domain of PlyB, a bacteriophage lysin active against Bacillus anthracis. J Mol Biol 366: 540-550.
43. Present, D.A., Meislin, R., and Shaffer, B. (1990) Gas gangrene. A review. Orthop Rev 19: 333-341.
44. Ramachandran, G.N., and Sasisekharan, V. (1968) Conformation of polypeptides and protein. Adv Protein Chem 23: 283-437.
45. Rau, A., Hogg, T., Marquardt, R., and Hilgenfeld, R. (2001) A new lysozyme fold. Crystal structure of the muramidase from Streptomyces coelicolor at 1.65Å resolution. J Biol Chem 276: 31994-31999.
46. Reid, C.W., Vinogradov, E., Li, J., Jarrell, H.C., Logan, S.M., and Brisson, J.R. (2012) Structural characterization of surface glycans from Clostridium difficile. Carbohydr Res 354: 65-73.
47. Saksela, K., and Permi, P. (2012) SH3 domain ligand binding: what's the consensus and where's the specificity? FEBS Lett 586: 2609-2614.
48. Schuch, R., Pelzek, A.J., Raz, A., Euler, C.W., Ryan, P.A., Winer, B.Y., etal. (2013) Use of a bacteriophage lysin to identify a novel target for antimicrobial development. PLoS ONE 8: e60754.
49. Tišáková, L., Vidová, B., Farkašovská, J., and Godány, A. (2014) Bacteriophage endolysin Lyt μ1/6: characterization of the C-terminal binding domain. FEMS Microbiol Lett 350: 199-208.
50. Touhami, A., Jericho, M.H., and Beveridge, T.J. (2004) Atomic force microscopy of cell growth and division in Staphylococcus aureus. J Bacteriol 186: 3286-3295.
51. Vagin, A., and Teplyakov, A. (1997) MOLREP: an automated program for molecular replacement. J Appl Crystallogr 30: 1022-1025.
52. Vollmer, W., Blanot, D., and de Pedro, M.A. (2008) Peptidoglycan structure and architecture. FEMS Microbiol Rev 32: 149-167.
53. Wang, I.N., Smith, D.L., and Young, R. (2000) Holins: the protein clocks of bacteriophage infections. Annu Rev Microbiol 54: 799-825.
54. Whisstock, J.C., and Lesk, A.M. (1999) SH3 domains in prokaryotes. Trends Biochem Sci 24: 132-133.
55. Wu, X., Knudsen, B., Feller, S.M., Zheng, J., Sali, A., Cowburn, D., etal. (1995) Structural basis for the specific interaction of lysine-containing proline-rich peptides with the N-terminal SH3 domain of c-Crk. Structure 3: 215-226.
56. Young, R. (1992) Bacteriophage lysis: mechanism and regulation. Microbiol Rev 56: 430-481.
57. Zimmer, M., Vukov, N., Scherer, S., and Loessner, M.J. (2002) The murein hydrolase of the bacteriophage phi3626 dual lysis system is active against all tested Clostridium perfringens strains. Appl Environ Microbiol 68: 5311-5317.