Insights into pneumococcal fratricide from the crystal structures of the modular killing factor LytC

Nature Structural and Molecular Biology

Volumn 17, Issue 5, 2010, Pages 576-581

  Pérez Dorado, Inmaculada ^a,f   González, Ana ^b,c   Morales, María ^b,c   Sanles, Reyes ^a   Striker, Waldemar ^d,g   Vollmer, Waldemar ^d,h   Mobashery, Shahriar ^e   García, José L ^b   Martínez Ripoll, Martín ^a   García, Pedro ^b,c   Hermoso, Juan A ^a  

^a INSTITUTO DE QUÍMICA FÍSICA ROCASOLANO   (Spain)

^b CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^c INSTITUTO DE SALUD CARLOS III   (Spain)

^d UNIVERSITY OF TÜBINGEN   (Germany)

^e UNIVERSITY OF NOTRE DAME   (United States)

^f MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^g UNIVERSITY OF DUNDEE   (United Kingdom)

^h NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOLYSIN; BINDING PROTEIN; CHOLINE BINDING PROTEIN D; HYDROLASE; LYTC PROTEIN; PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GROWTH; BACTERIAL VIRULENCE; CELL DIVISION; CONFORMATION; CRYSTAL STRUCTURE; ENZYME ACTIVATION; ENZYME ACTIVE SITE; HYDROLYSIS; IN VIVO STUDY; NONHUMAN; PREDATION; PRIORITY JOURNAL; PROTEIN FUNCTION; STREPTOCOCCUS PNEUMONIAE;

CHOLINE; CRYSTALLOGRAPHY, X-RAY; MODELS, MOLECULAR; N-ACETYLMURAMOYL-L-ALANINE AMIDASE; PEPTIDOGLYCAN; PROTEIN BINDING; PROTEIN CONFORMATION; STREPTOCOCCUS PNEUMONIAE; TEICHOIC ACIDS;

BACTERIA (MICROORGANISMS);

EID: 77951978074     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.1817     Document Type: Article

References (37)

1. Höltje, J.V. Growth of the stress-bearing and shape-maintaining murein sacculus of Escherichia coli. Microbiol. Mol. Biol. Rev. 62, 181-203 (1998).
2. Vollmer, W., Joris, B., Charlier, P. & Foster, S. peptidoglycan (murein) hydrolases. FEMS Microbiol. Rev. 32, 259-286 (2008).
3. López, R. & García, E. Recent trends on the molecular biology of pneumococcal capsules, lytic enzymes, and bacteriophage. FEMS Microbiol. Rev. 28, 553-580 (2004).
4. Tomasz, A. Choline in the cell wall of a bacterium: novel type of polymer-linked choline in pneumococcus. Science 157, 694-697 (1967).
5. García, J.L., Sánchez-Beato, A.R., Medrano, F.J. & López, R. Versatility of choline-binding domain. in Streptococcus pneumoniae: Molecular Biology & Mechanisms of Disease (ed. Tomasz, A.) 231-244 (Mary Ann Liebert, Inc., Larchmont, New York, USA, 2000).
6. López, R., García, E., García, P. & García, J.L. The pneumococcal cell wall degrading enzymes: a modular design to create new lysins? Microb. Drug Resist. 3, 199-211 (1997).
7. García, P., González, M.P., García, E., García, J.L. & López, R. The molecular characterization of the frst autolytic lysozyme of Streptococcus pneumoniae reveals evolutionary mobile domains. Mol. Microbiol. 33, 128-138 (1999).
8. Claverys, J.P. & Håvarstein, L.S. Cannibalism and fratricide: mechanisms and raisons d'être. Nat. Rev. Microbiol. 5, 219-229 (2007).
9. Claverys, J.P., Prudhomme, M. & Martin, B. Induction of competence regulons as general stress responses in Gram-positive bacteria. Annu. Rev. Microbiol. 60, 451-475 (2006).
10. Johnsborg, O., Eldholm, V., Bjørnstad, M.L. & Håvarstein, L.S. A predatory mechanism dramatically increases the effciency of lateral gene transfer in Streptococcus pneumoniae and related commensal species. Mol. Microbiol. 69, 245-253 (2008).
11. Eldholm, V., Johnsborg, O., Haugen, K., Ohnstad, H.S. & Håvarstein, L.S. Fratricide in Streptococcus pneumoniae: contributions and role of the cell wall hydrolases CbpD, LytA and LytC. Microbiology 155, 2223-2234 (2009).
12. Johnsborg, O. & Håvarstein, L.S. Regulation of natural genetic transformation and acquisition of transforming DNA in Streptococcus pneumoniae. FEMS Microbiol. Rev. 33, 627-642 (2009).
13. Molina, R. et al. Crystal structure of CbpF, a bifunctional choline-binding protein and autolysis regulator from Streptococcus pneumoniae. EMBO Rep. 10, 246-251 (2009).
14. Gosink, K.K., Mann, E.R., Guglielmo, C., Tuomanen, E.I. & Masure, H.R. Role of novel choline binding proteins in virulence of Streptococcus pneumoniae. Infect. Immun. 68, 5690-5695 (2000).
15. Klein, R.A., Hartman, R., Egge, H., Behr, T. & Fischer, W. The aqueous solution of a lipoteichoic acid from Streptococcus pneumoniae strain R6 containing 2,4-diamino-2,4,6-trideoxy-galactose: evidence for conformational mobility of the galactopyranose ring. Carbohydr. Res. 281, 79-98 (1996).
16. Hermoso, J.A. et al. Insights into pneumococcal pathogenesis from the crystal structure of the modular teichoic acid phosphorylcholine esterase Pce. Nat. Struct. Mol. Biol. 12, 533-538 (2005).
17. Jones, G., Willett, P., Glen, R.C., Leach, A.R. & Taylor, R. Development and validation of a genetic algorithm for fexible docking. J. Mol. Biol. 267, 727-748 (1997).
18. De Las Rivas, B., García, J.L., López, R. & García, P. Purifcation and polar localization of the pneumococcal LytB, a putative endo-β-N-acetylglucosaminidase: the chain-dispersing murein hydrolase. J. Bacteriol. 184, 4988-5000 (2002).
19. Hermoso, J.A. et al. Structural basis for selective recognition of pneumococcal cell wall by modular endolysin from phage Cp-1. Structure 11, 1239-1249 (2003).
20. Pérez-Dorado, I. et al. Elucidation of the molecular recognition of bacterial cell wall by modular pneumococcal phage endolysin CPL-1. J. Biol. Chem. 282, 24990-24999 (2007).
21. Monterroso, B., Sáiz, J.L., García, P., García, J.L. & Menéndez, M. Insights into the structure-function relationships of pneumococcal cell wall lysozymes, LytC and Cpl-1. J. Biol. Chem. 283, 28618-28628 (2008).
22. Meroueh, S.O. et al. Three-dimensional structure of the bacterial cell wall peptidoglycan. Proc. Natl. Acad. Sci. USA 103, 4404-4409 (2006).
23. Hesek, D., Lee, M., Morio, K. & Mobashery, S. Synthesis of a fragment of bacterial cell wall. J. Org. Chem. 69, 2137-2146 (2004).
24. Hesek, D. et al. Synthetic peptidoglycan substrates for penicillin-binding protein 5 of Gram-negative bacteria. J. Org. Chem. 69, 778-784 (2004).
25. Ottolenghi, E. & Hotchkiss, R.D. Appearance of genetic transforming activity in pneumococcal cultures. Science 132, 1257-1258 (1960).
26. Horne, D.S. & Tomasz, A. Possible role of a choline-containing teichoic acid in the maintenance of normal cell shape and physiology in Streptococcus oralis. J. Bacteriol. 175, 1717-1722 (1993).
27. Vollmer, W. Preparation and analysis of pneumococcal murein (peptidoglycan). in Molecular Biology of Streptococci (eds. Hakenbeck, R. & Chhatwal, S.) 531-535 (Horizon Scientifc Press, Norfolk, UK, 2007).
28. Severin, A. & Tomasz, A. Naturally occuring peptidoglycan variants of Streptococcus pneumoniae. J. Bacteriol. 178, 168-174 (1996).
29. Sánchez-Puelles, J.M., Sanz, J.M., García, J.L. & García, E. Cloning and expression of gene fragments encoding the choline-binding domain of pneumococcal murein hydrolases. Gene 89, 69-75 (1990).
30. Mosser, J.L. & Tomasz, A. Choline-containing teichoic acid as a structural component of pneumococcal cell wall and its role in sensitivity to lysis by an autolytic enzyme. J. Biol. Chem. 245, 287-298 (1970).
31. Leslie, A.G.W. Profle ftting. in Proceedings of the CCP4 Study Weekend (eds. Machin, J.R. & Papiz, M.Z.) 39-50 (SERC Daresbury Laboratory, Warrington, UK, 1987)
32. Collaborative Computacional Project 4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50, 760-763 (1994).
33. Molina, R., Stelter, M., Kahn, R. & Hermoso, J.A. Characterization of gadolinium complexes for SAD phasing in macromolecular crystallography: application to CbpF. Acta Crystallogr. D Biol. Crystallogr. 65, 823-831 (2009).
34. Jones, T.A., Zou, J.Y., Cowan, S.W. & Kjelgaard, M. Improved methods for model building in electron density maps and the location of errors in these models. Acta Crystallogr. A 47, 110-119 (1991).
35. Brunger, A.T. et al. Crystallographic and NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54, 905-921 (1998).
36. Laskowski, R.A., MacArthur, M.W., Moss, D.S. & Thorton, J.M. PROCHECK, a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26, 283-291 (1993).
37. DeLano, W.L. The PyMOL Molecular Graphics System. (DeLano Scientifc, San Carlos, California, USA, 2002) http://www.pymol.org.