Clostridium difficile surface proteins are anchored to the cell wall using CWB2 motifs that recognise the anionic polymer PSII

Molecular Microbiology

Volumn 96, Issue 3, 2015, Pages 596-608

  Willing, Stephanie E ^a   Candela, Thomas ^b   Shaw, Helen Alexandra ^a   Seager, Zoe ^a   Mesnage, Stéphane ^c   Fagan, Robert P ^c   Fairweather, Neil F ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b University Paris Sud   (France)

^c UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MEMBRANE PROTEIN; POLYMER; PROTEIN CWP2; PROTEIN SLPA; PSII; UNCLASSIFIED DRUG; BACTERIAL POLYSACCHARIDE; MEMBRANE PROTEIN; PROTEIN BINDING;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL CELL WALL; CONTROLLED STUDY; GENE LOCUS; GENE SILENCING; MEMBRANE BINDING; MEMBRANE COMPONENT; MOLECULAR RECOGNITION; NONHUMAN; PEPTOCLOSTRIDIUM DIFFICILE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; TANDEM REPEAT; CELL WALL; METABOLISM;

BACTERIA (MICROORGANISMS); CLOSTRIDIUM DIFFICILE; FIRMICUTES; POSIBACTERIA;

AMINO ACID MOTIFS; CELL WALL; CLOSTRIDIUM DIFFICILE; GENE KNOCKDOWN TECHNIQUES; MEMBRANE PROTEINS; POLYSACCHARIDES, BACTERIAL; PROTEIN BINDING; REPETITIVE SEQUENCES, AMINO ACID;

EID: 84928420147     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12958     Document Type: Article

References (48)

1. Bertolo, L., Boncheff, A.G., Ma, Z., Chen, Y.H., Wakeford, T., Friendship, R.M., etal. (2012) Clostridium difficile carbohydrates: glucan in spores, PSII common antigen in cells, immunogenicity of PSII in swine and synthesis of a dual C.difficile-ETEC conjugate vaccine. Carbohydr Res 354: 79-86.
2. Brown, S., Santa Maria, J.P., Jr, and Walker, S. (2013) Wall teichoic acids of Gram-positive bacteria. Annu Rev Microbiol 67: 313-336.
3. Cairns, M.D., Stabler, R.A., Shetty, N., and Wren, B.W. (2012) The continually evolving Clostridium difficile species. Future Microbiol 7: 945-957.
4. Calabi, E., Ward, S., Wren, B., Paxton, T., Panico, M., Morris, H., etal. (2001) Molecular characterization of the surface layer proteins from Clostridium difficile. Mol Microbiol 40: 1187-1199.
5. Calabi, E., Calabi, F., Phillips, A.D., and Fairweather, N. (2002) Binding of Clostridium difficile surface layer proteins to gastrointestinal tissues. Infect Immun 70: 5770-5778.
6. Campbell, J., Singh, A.K., Santa Maria, J.P., Jr, Kim, Y., Brown, S., Swoboda, J.G., etal. (2011) Synthetic lethal compound combinations reveal a fundamental connection between wall teichoic acid and peptidoglycan biosyntheses in Staphylococcus aureus. ACS Chem Biol 6: 106-116.
7. Candela, T., Maes, E., Garenaux, E., Rombouts, Y., Krzewinski, F., Gohar, M., and Guerardel, Y. (2011) Environmental and biofilm-dependent changes in a Bacillus cereus secondary cell wall polysaccharide. J Biol Chem 286: 31250-31262.
8. Cox, A.D., St. Michael, F., Aubry, A., Cairns, C.M., Strong, P.C.R., Hayes, A.C., and Logan, S.M. (2013) Investigating the candidacy of a lipoteichoic acid-based glycoconjugate as a vaccine to combat Clostridium difficile infection. Glycoconj J 30: 843-855.
9. Deakin, L.J., Clare, S., Fagan, R.P., Dawson, L.F., Pickard, D.J., West, M.R., etal. (2012) The Clostridium difficile spo0A gene is a persistence and transmission factor. Infect Immun 80: 2704-2711.
10. Denapaite, D., Bruckner, R., Hakenbeck, R., and Vollmer, W. (2012) Biosynthesis of teichoic acids in Streptococcus pneumoniae and closely related species: lessons from genomes. Microb Drug Resist 18: 344-358.
11. D'Elia, M.A., Millar, K.E., Beveridge, T.J., and Brown, E.D. (2006) Wall teichoic acid polymers are dispensable for cell viability in Bacillus subtilis. J Bacteriol 188: 8313-8316.
12. Emerson, J., Reynolds, C.B., Fagan, R.P., Shaw, H.A., Goulding, D., and Fairweather, N.F. (2009) A novel genetic switch controls phase variable expression of CwpV, a Clostridium difficile cell wall protein. Mol Microbiol 74: 541-556.
13. Fagan, R., and Fairweather, N. (2010) Dissecting the cell surface. Methods Mol Biol 646: 117-134.
14. Fagan, R.P., and Fairweather, N.F. (2011) Clostridium difficile has two parallel and essential Sec secretion systems. J Biol Chem 286: 27483-27493.
15. Fagan, R.P., and Fairweather, N.F. (2014) Biogenesis and functions of bacterial S-layers. Nat Rev Microbiol 12: 211-222.
16. Fagan, R.P., Albesa-Jove, D., Qazi, O., Svergun, D.I., Brown, K.A., and Fairweather, N.F. (2009) Structural insights into the molecular organization of the S-layer from Clostridium difficile. Mol Microbiol 71: 1308-1322.
17. Fagan, R.P., Janoir, C., Collignon, A., Mastrantonio, P., Poxton, I.R., and Fairweather, N.F. (2011) A proposed nomenclature for cell wall proteins of Clostridium difficile. J Med Microbiol 60: 1225-1228.
18. Faulds-Pain, A., Twine, S.M., Vinogradov, E., Strong, P.C., Dell, A., Buckley, A.M., etal. (2014) The post-translational modification of the Clostridium difficile flagellin affects motility, cell surface properties and virulence. Mol Microbiol 94: 272-289.
19. Fernandez-Tornero, C., Lopez, R., Garcia, E., Gimenez-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.
20. Ganeshapillai, J., Vinogradov, E., Rousseau, J., Weese, J.S., and Monteiro, M.A. (2008) Clostridium difficile cell-surface polysaccharides composed of pentaglycosyl and hexaglycosyl phosphate repeating units. Carbohydr Res 343: 703-710.
21. Heap, J.T., Kuehne, S.A., Ehsaan, M., Cartman, S.T., Cooksley, C.M., Scott, J.C., and Minton, N.P. (2010) The ClosTron: mutagenesis in Clostridium refined and streamlined. J Microbiol Meth 80: 49-55.
22. Hussain, H.A., Roberts, A.P., and Mullany, P. (2005) Generation of an erythromycin-sensitive derivative of Clostridium difficile strain 630 (630Δerm) and demonstration that the conjugative transposon Tn916E enters the genome of this strain at multiple sites. J Med Microbiol 54: 137-141.
23. Jonquieres, 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.
24. Kern, J., Ryan, C., Faull, K., and Schneewind, O. (2010) Bacillus anthracis surface-layer proteins assemble by binding to the secondary cell wall polysaccharide in a manner that requires csaB and tagO. J Mol Biol 401: 757-775.
25. Kern, J., Wilton, R., Zhang, R., Binkowski, T.A., Joachimiak, A., and Schneewind, O. (2011) Structure of the SLH domains from Bacillus anthracis surface array protein. J Biol Chem 286: 26042-26049.
26. Kirby, J.M., Ahern, H., Roberts, A.K., Kumar, V., Freeman, Z., Acharya, K.R., and Shone, C.C. (2009) Cwp84, a surface-associated cysteine protease, plays a role in the maturation of the surface layer of Clostridium difficile. J Biol Chem 284: 34666-34673.
27. Lawley, T.D., Clare, S., Deakin, L.J., Goulding, D., Yen, J.L., Raisen, C., etal. (2010) Use of purified Clostridium difficile spores to facilitate evaluation of health care disinfection regimens. Appl Environ Microbiol 76: 6895-6900.
28. Mazmanian, S.K., Liu, G., Ton-That, H., and Schneewind, O. (1999) Staphylococcus aureus sortase, an enzyme that anchors surface proteins to the cell wall. Science 285: 760-763.
29. Merrigan, M.M., Venugopal, A., Roxas, J.L., Anwar, F., Mallozzi, M.J., Roxas, B.A., etal. (2013) Surface-layer protein A (SlpA) is a major contributor to host-cell adherence of Clostridium difficile. PLoS ONE 8: e78404.
30. Mesnage, S., Fontaine, T., Mignot, T., Delepierre, M., Mock, M., and Fouet, A. (2000) Bacterial SLH domain proteins are non-covalently anchored to the cell surface via a conserved mechanism involving wall polysaccharide pyruvylation. EMBO J 19: 4473-4484.
31. Mesnage, S., Dellarole, M., Baxter, N.J., Rouget, J.-B., Dimitrov, J.D., Wang, N., etal. (2014) Molecular basis for bacterial peptidoglycan recognition by LysM domains. Nat Comm 5: 4269.
32. Percy, M.G., and Gründling, A. (2014) Lipoteichoic acid synthesis and function in gram-positive bacteria. Annu Rev Microbiol 68: 81-100.
33. Pizarro-Cerda, J., and Cossart, P. (2006) Bacterial adhesion and entry into host cells. Cell 124: 715-727.
34. 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.
35. Reynolds, C.B., Emerson, J.E., de la Riva, L., Fagan, R.P., and Fairweather, N.F. (2011) The Clostridium difficile cell wall protein CwpV is antigenically variable between strains, but exhibits conserved aggregation-promoting function. PLoS Pathog 7: e1002024.
36. de la Riva, L., Willing, S.E., Tate, E.W., and Fairweather, N.F. (2011) Roles of cysteine proteases Cwp84 and Cwp13 in biogenesis of the cell wall of Clostridium difficile. J Bacteriol 193: 3276-3285.
37. Rupnik, M., Widmer, A., Zimmermann, O., Eckert, C., and Barbut, F. (2008) Clostridium difficile toxinotype V, ribotype 078, in animals and humans. J Clin Microbiol 46: 2146.
38. Rupnik, M., Wilcox, M.H., and Gerding, D.N. (2009) Clostridium difficile infection: new developments in epidemiology and pathogenesis. Nat Rev Microbiol 7: 526-536.
39. Schneewind, O., and Missiakas, D.M. (2012) Protein secretion and surface display in Gram-positive bacteria. Philos Trans R Soc Lond B Biol Sci 367: 1123-1139.
40. Sebaihia, M., Wren, B.W., Mullany, P., Fairweather, N.F., Minton, N., Stabler, R., etal. (2006) The multidrug-resistant human pathogen Clostridium difficile has a highly mobile, mosaic genome. Nat Genet 38: 779-786.
41. Seekatz, A.M., and Young, V.B. (2014) Clostridium difficile and the microbiota. J Clin Invest 124: 4182-4189.
42. Sham, L.T., Butler, E.K., Lebar, M.D., Kahne, D., Bernhardt, T.G., and Ruiz, N. (2014) Bacterial cell wall. MurJ is the flippase of lipid-linked precursors for peptidoglycan biogenesis. Science 345: 220-222.
43. Spigaglia, P., Barketi-Klai, A., Collignon, A., Mastrantonio, P., Barbanti, F., Rupnik, M., etal. (2013) Surface-layer (S-layer) of human and animal Clostridium difficile strains and their behaviour in adherence to epithelial cells and intestinal colonization. J Med Microbiol 62: 1386-1393.
44. Swoboda, J.G., Campbell, J., Meredith, T.C., and Walker, S. (2010) Wall teichoic acid function, biosynthesis, and inhibition. Chembiochem 11: 35-45.
45. Voth, D.E., and Ballard, J.D. (2005) Clostridium difficile toxins: mechanism of action and role in disease. Clin Microbiol Rev 18: 247-263.
46. Waligora, A.J., Hennequin, C., Mullany, P., Bourlioux, P., Collignon, A., and Karjalainen, T. (2001) Characterization of a cell surface protein of Clostridium difficile with adhesive properties. Infect Immun 69: 2144-2153.
47. Weidenmaier, C., and Peschel, A. (2008) Teichoic acids and related cell-wall glycopolymers in Gram-positive physiology and host interactions. Nat Rev Microbiol 6: 276-287.
48. Whitfield, C. (2006) Biosynthesis and assembly of capsular polysaccharides in Escherichia coli. Annu Rev Biochem 75: 39-68.