Structure of pneumococcal peptidoglycan hydrolase LytB reveals insights into the bacterial cell wall remodeling and pathogenesis

Journal of Biological Chemistry

Volumn 289, Issue 34, 2014, Pages 23403-23416

  Bai, Xiao Hui ^a   Chen, Hui Jie ^a   Jiang, Yong Liang ^a   Wen, Zhensong ^b   Huang, Yubin ^a   Cheng, Wang ^a   Li, Qiong ^a   Qi, Lei ^a   Zhang, Jing Ren ^b   Chen, Yuxing ^a   Zhou, Cong Zhao ^a  

^a UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^b Tsinghua University   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROLIFERATION;

BIOCHEMICAL MECHANISMS; CHOLINE BINDING DOMAIN; HYDROLYTIC ACTIVITIES; MODULAR ORGANIZATIONS; N-ACETYLGLUCOSAMINIDASE; PEPTIDOGLYCAN HYDROLASE; STREPTOCOCCUS PNEUMONIAE; STRUCTURAL COMPARISON;

CELL MEMBRANES;

ASPARTIC ACID; BACTERIAL PROTEIN; LYSINE; LYTB PROTEIN; UNCLASSIFIED DRUG; LYTB PROTEIN, STREPTOCOCCUS; N ACETYLMURAMOYLALANINE AMIDASE; PRIMER DNA;

ARTICLE; BACTERIAL CELL WALL; BACTERIUM ADHERENCE; CELL SEPARATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; EPITHELIUM CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; LUNG ALVEOLUS EPITHELIUM; MOLECULAR PATHOLOGY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN HYDROLYSIS; STREPTOCOCCUS MITIS; STREPTOCOCCUS PNEUMONIAE; STRUCTURE ANALYSIS; CELL WALL; CHEMISTRY; GENETICS; LUNG; METABOLISM; MICROBIOLOGY; PATHOGENICITY; POLYMERASE CHAIN REACTION; PROTEIN CONFORMATION; SITE DIRECTED MUTAGENESIS;

BACTERIAL ADHESION; BASE SEQUENCE; CELL WALL; DNA PRIMERS; LUNG; MUTAGENESIS, SITE-DIRECTED; N-ACETYLMURAMOYL-L-ALANINE AMIDASE; POLYMERASE CHAIN REACTION; PROTEIN CONFORMATION; STREPTOCOCCUS PNEUMONIAE;

EID: 84906546265     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.579714     Document Type: Article

References (64)

1. Neidhardt, F. C., Ingraham, J. L., and Schaechter, M. (1990) Physiology of the Bacterial Cell: A Molecular Approach, pp. 507, American Society for Microbiology, Washington, D. C.
2. Typas, A., Banzhaf, M., Gross, C. A., and Vollmer, W. (2012) From the regulation of peptidoglycan synthesis to bacterial growth and morphology. Nat. Rev. Microbiol. 10, 123-136
3. Neuhaus, F. C., and Baddiley, J. (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
4. Vollmer, W., Joris, B., Charlier, P., and Foster, S. (2008) Bacterial peptidoglycan (murein) hydrolases. FEMS Microbiol. Rev. 32, 259-286
5. Musher, D. M. (2010) Streptococcus pneumoniae. In Principles and Practice of Infectious Diseases. 7th Ed., pp. 2623-2641, Elsevier Churchill Livingstone, New York
6. Paton, J. C., and Boslego, J. W. (2008) Protein vaccines. In Pneumococcal Vaccines: The Impact of Conjugate Vaccines. 6th Ed., pp. 421-435, American Society for Microbiology, Washington, D. C.
7. Mosser, J. L., and Tomasz, A. (1970) 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
8. García, P., González, M. P., García, E., López, R., and García, J. L. (1999) LytB, a novel pneumococcal murein hydrolase essential for cell separation. Mol. Microbiol. 31, 1275-1281
9. García, P., Paz González, M., García, E., García, J. L., and López, R. (1999) The molecular characterization of the first autolytic lysozyme of Streptococcus pneumoniae reveals evolutionary mobile domains. Mol. Microbiol. 33, 128-138
10. Eldholm, V., Johnsborg, O., Straume, D., Ohnstad, H. S., Berg, K. H., Hermoso, J. A., and Håvarstein, L. S. (2010) Pneumococcal CbpD is a murein hydrolase that requires a dual cell envelope binding specificity to kill target cells during fratricide. Mol. Microbiol. 76, 905-917
11. López, R., González, M. P., García, E., García, J. L., and García, P. (2000) Biological roles of two new murein hydrolases of Streptococcus pneumoniae representing examples of module shuffling. Res. Microbiol. 151, 437-443
12. Tomasz, A., and Waks, S. (1975) Mechanism of action of penicillin: triggering of the pneumococcal autolytic enzyme by inhibitors of cell wall synthesis. Proc. Natl. Acad. Sci. U.S.A. 72, 4162-4166
13. Sanchez-Puelles, J. M., Ronda, C., Garcia, J. L., Garcia, P., Lopez, R., and Garcia, E. (1986) Searching for autolysin functions. Characterization of a pneumococcal mutant deleted in the lytA gene. Eur. J. Biochem. 158, 289-293
14. Fernández-Tornero, C., López, R., García, E., Giménez-Gallego, G., and Romero, A. (2001) A novel solenoid fold in the cell wall anchoring domain of the pneumococcal virulence factor LytA. Nat. Struct. Biol. 8, 1020-1024
15. Yuan, Z. Q., Lv, Z. Y., Gan, H. Q., Xian, M., Zhang, K. X., Mai, J. Y., Yu, X. B., and Wu, Z. D. (2011) Intranasal immunization with autolysin (LytA) in mice model induced protection against five prevalent Streptococcus pneumoniae serotypes in China. Immunol. Res. 51, 108-115
16. Pérez-Dorado, I., González, A., Morales, M., Sanles, R., Striker, W., Vollmer, W., Mobashery, S., García, J. L., Martínez-Ripoll, M., García, P., and Hermoso, J. A. (2010) Insights into pneumococcal fratricide from the crystal structures of the modular killing factor LytC. Nat. Struct. Mol. Biol. 17, 576-581
17. Claverys, J. P., and Håvarstein, L. S. (2007) Cannibalism and fratricide: mechanisms and raisons d'etre. Nat. Rev. Microbiol. 5, 219-229
18. De Las Rivas, B., García, J. L., López, R., and García, P. (2002) Purification and polar localization of pneumococcal LytB, a putative endo-β-n-Acetylglucosaminidase: the chain-dispersing murein hydrolase. J. Bacteriol. 184, 4988-5000
19. Gosink, K. K., Mann, E. R., Guglielmo, C., Tuomanen, E. I., and Masure, H. R. (2000) Role of novel choline binding proteins in virulence of Streptococcus pneumoniae. Infect. Immun. 68, 5690-5695
20. Ramos-Sevillano, E., Moscoso, M., García, P., García, E., and Yuste, J. (2011) Nasopharyngeal colonization and invasive disease are enhanced by the cell wall hydrolases LytB and LytC of Streptococcus pneumoniae. PLoS ONE 6, e23626
21. Atilano, M. L., Pereira, P. M., Vaz, F., Catalão, M. J., Reed, P., Grilo, I. R., Sobral, R. G., Ligoxygakis, P., Pinho, M. G., and Filipe, S. R. (2014) Bacterial autolysins trim cell surface peptidoglycan to prevent detection by the Drosophila innate immune system. eLife 3, e02277
22. Lu, L., Ma, Y., and Zhang, J. R. (2006) Streptococcus pneumoniae recruits complement factorHthrough the amino terminus of CbpA. J. Biol. Chem. 281, 15464-15474
23. Otwinowski, Z., and Minor, W. (1997) Processing of x-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326
24. Brodersen, D. E., de La Fortelle, E., Vonrhein, C., Bricogne, G., Nyborg, J., and Kjeldgaard, M. (2000) Applications of single-wavelength anomalous dispersion at high and atomic resolution. Acta Crystallogr. D. Biol. Crys-tallogr. 56, 431-441
25. Adams, P. D., Afonine, P. V., Bunkóczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., McCoy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D. Biol. Crystallogr. 66, 213-221
26. Terwilliger, T. C., and Berendzen, J. (1999) Automated MAD and MIR structure solution. Acta Crystallogr. D. Biol. Crystallogr. 55, 849-861
27. Terwilliger, T. C. (2003) Automated main-chain model building by template matching and iterative fragment extension. Acta Crystallogr. D. Biol. Crystallogr. 59, 38-44
28. 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
29. Collaborative Computational Project, Number 4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D. Biol. Crystallogr. 50, 760-763
30. Emsley, P., and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D. Biol. Crystallogr. 60, 2126-2132
31. Davis, I. W., Leaver-Fay, A., Chen, V. B., Block, J. N., Kapral, G. J., Wang, X., Murray, L. W., Arendall, W. B., 3rd, Snoeyink, J., Richardson, J. S., and Richardson, D. C. (2007) MolProbity: all-Atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res. 35, W375-W383
32. Laskowski, R. A., Macarthur, M. W., Moss, D. S., and Thornton, J. M. (1993) Procheck: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26, 283-291
33. Trott, O., and Olson, A. J. (2010) AutoDock Vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. J. Comput. Chem. 31, 455-461
34. Morris, G. M., Huey, R., Lindstrom, W., Sanner, M. F., Belew, R. K., Goodsell, D. S., and Olson, A. J. (2009) AutoDock4 and AutoDockTools4: automated docking with selective receptor flexibility. J. Comput. Chem. 30, 2785-2791
35. Vollmer, W. (2007) Preparation and analysis of pneumococcal murein (peptidoglycan). In Molecular Biology of Streptococci, pp. 531-536, Horizon Bioscience, Norfolk, UK
36. Zhou, R., Chen, S., and Recsei, P. (1988) A dye release assay for determination of lysostaphin activity. Anal. Biochem. 171, 141-144
37. Bricker, A. L., and Camilli, A. (1999) Transformation of a type 4 encapsulated strain of Streptococcus pneumoniae. FEMS Microbiol. Lett. 172, 131-135
38. Sung, C. K., Li, H., Claverys, J. P., and Morrison, D. A. (2001) An rpsLcassette, janus, for gene replacement through negative selection in Streptococcus pneumoniae. Appl. Environ. Microbiol. 67, 5190-5196
39. Heckman, K. L., and Pease, L. R. (2007) Gene splicing and mutagenesis by PCR-driven overlap extension. Nat. Protoc. 2, 924-932
40. Zhang, J. R., Mostov, K. E., Lamm, M. E., Nanno, M., Shimida, S., Ohwaki, M., and Tuomanen, E. (2000) The polymeric immunoglobulin receptor translocates pneumococci across human nasopharyngeal epithelial cells. Cell 102, 827-837
41. 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
42. Bublitz, M., Polle, L., Holland, C., Heinz, D. W., Nimtz, M., and Schubert, W. D. (2009) Structural basis for autoinhibition and activation of Auto, a virulence-Associated peptidoglycan hydrolase of Listeria onocytogenes. Mol. Microbiol. 71, 1509-1522
43. Hashimoto, W., Ochiai, A., Momma, K., Itoh, T., Mikami, B., Maruyama, Y., and Murata, K. (2009) Crystal structure of the glycosidase family 73 peptidoglycan hydrolase FlgJ. Biochem. Biophys. Res. Commun. 381, 16-21
44. Biswas, R., Voggu, L., Simon, U. K., Hentschel, P., Thumm, G., and Götz, F. (2006) Activity of the major staphylococcal autolysin Atl. FEMS Microbiol. Lett. 259, 260-268
45. Holm, L., and Rosenström, P. (2010) Dali server: conservation mapping in 3D. Nucleic Acids Res. 38, W545-W549
46. Xu, Q., Sudek, S., McMullan, D., Miller, M. D., Geierstanger, B., Jones, D. H., Krishna, S. S., Spraggon, G., Bursalay, B., Abdubek, P., Acosta, C., Ambing, E., Astakhova, T., Axelrod, H. L., Carlton, D., Caruthers, J., Chiu, H. J., Clayton, T., Deller, M. C., Duan, L., Elias, Y., Elsliger, M. A., Feuerhelm, J., Grzechnik, S. K., Hale, J., Han, G. W., Haugen, J., Jaroszewski, L., Jin, K. K., Klock, H. E., Knuth, M. W., Kozbial, P., Kumar, A., Marciano, D., Morse, A. T., Nigoghossian, E., Okach, L., Oommachen, S., Paulsen, J., Reyes, R., Rife, C. L., Trout, C. V., van den Bedem, H., Weekes, D., White, A., Wolf, G., Zubieta, C., Hodgson, K. O., Wooley, J., Deacon, A. M., Godzik, A., Lesley, S. A., and Wilson, I. A. (2009) Structural basis of murein peptide specificity of a γ-D-glutamyl-L-diamino acid endopeptidase. Structure 17, 303-313
47. 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
48. Bateman, A., and Rawlings, N. D. (2003) The CHAP domain: a large family of amidases including GSP amidase and peptidoglycan hydrolases. Trends Biochem. Sci. 28, 234-237
49. Hanawa-Suetsugu, K., Sekine, S., Sakai, H., Hori-Takemoto, C., Terada, T., Unzai, S., Tame, J. R., Kuramitsu, S., Shirouzu, M., and Yokoyama, S. (2004) Crystal structure of elongation factor P from Thermus thermophilus HB8. Proc. Natl. Acad. Sci. U.S.A. 101, 9595-9600
50. van Aalten, D. M., Synstad, B., Brurberg, M. B., Hough, E., Riise, B. W., Eijsink, V. G., and Wierenga, R. K. (2000) Structure of a two-domain chitotriosidase from Serratia marcescens at 1.9 Å resolution. Proc. Natl. Acad. Sci. U.S.A. 97, 5842-5847
51. Schüttelkopf, A. W., and van Aalten, D. M. (2004) PRODRG: a tool for high-throughput crystallography of protein-ligand complexes. Acta Crystallogr. D. Biol. Crystallogr. 60, 1355-1363
52. Bogaert, D., De Groot, R., and Hermans, P. W. (2004) Streptococcus pneumoniaecolonisation: the key to pneumococcal disease. Lancet Infect. Dis. 4, 144-154
53. Punta, M., Coggill, P. C., Eberhardt, R. Y., Mistry, J., Tate, J., Boursnell, C., Pang, N., Forslund, K., Ceric, G., Clements, J., Heger, A., Holm, L., Sonnhammer, E. L., Eddy, S. R., Bateman, A., and Finn, R. D. (2012) The Pfam protein families database. Nucleic Acids Res. 40, D290-D301
54. Cabanes, D., Dussurget, O., Dehoux, P., and Cossart, P. (2004) Auto, a surface associated autolysin of Listeria monocytogenes required for entry into eukaryotic cells and virulence. Mol. Microbiol. 51, 1601-1614
55. Camiade, E., Peltier, J., Bourgeois, I., Couture-Tosi, E., Courtin, P., Antunes, A., Chapot-Chartier, M. P., Dupuy, B., and Pons, J. L. (2010) Characterization of Acp, a peptidoglycan hydrolase of Clostridium perfringens with N-Acetylglucosaminidase activity that is implicated in cell separation and stress-induced autolysis. J. Bacteriol. 192, 2373-2384
56. Jonquières, R., Bierne, H., Fiedler, F., Gounon, P., and Cossart, P. (1999) Interaction between the protein InlB of Listeria monocytogenes and lipoteichoic acid: a novel mechanism of protein association at the surface of gram-positive bacteria. Mol. Microbiol. 34, 902-914
57. Eckert, C., Lecerf, M., Dubost, L., Arthur, M., and Mesnage, S. (2006) Functional analysis of AtlA, the majorN-Acetylglucosaminidase of Enterococcus faecalis. J. Bacteriol. 188, 8513-8519
58. Vos, P. D., Garrity, G. M., Jones, D., Krieg, N. R., Ludwig, W., Rainey, F. A., Schleifer, K.-H., and Whitman, W. B. (2009) The Firmicutes, Springer-Verlag, Dordrecht, The Netherlands
59. Mellroth, P., Sandalova, T., Kikhney, A., Vilaplana, F., Hesek, D., Lee, M., Mobashery, S., Normark, S., Svergun, D., Henriques-Normark, B., and Achour, A. (2014) Structural and functional insights into peptidoglycan access for the lytic amidase LytA of Streptococcus pneumoniae. mBio 5, e01120-01113
60. Varea, J., Saiz, J. L., López-Zumel, C., Monterroso, B., Medrano, F. J., Arrondo, J. L., Iloro, I., Laynez, J., Garcia, J. L., and Menéndez, M. (2000) Do sequence repeats play an equivalent role in the cholinebinding module of pneumococcal LytA amidase? J. Biol. Chem. 275, 26842-26855
61. Molina, R., González, A., Stelter, M., Pérez-Dorado, I., Kahn, R., Morales, M., Moscoso, M., Campuzano, S., Campillo, N. E., Mobashery, S., García, J. L., García, P., and Hermoso, J. A. (2009) Crystal structure of CbpF, a bifunctional choline-binding protein and autolysis regulator from Streptococcus pneumoniae. EMBO Rep. 10, 246-251
62. Romero, P., López, R., and García, E. (2007) Key role of amino acid residues in the dimerization and catalytic activation of the autolysin LytA, an important virulence factor in Streptococcus pneumoniae. J. Biol. Chem. 282, 17729-17737
63. Fernández-Tornero, C., García, E., López, R., Giménez-Gallego, G., and Romero, A. (2002) Two new crystal forms of the choline-binding domain of the major pneumococcal autolysin: insights into the dynamics of the active homodimer. J. Mol. Biol. 321, 163-173
64. Krissinel, E., and Henrick, K. (2007) Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372, 774-797