Characterization of a novel family of fibronectin-binding proteins with M23 peptidase domains from Treponema denticola

Molecular Oral Microbiology

Volumn 25, Issue 6, 2010, Pages 369-383

  Bamford, C V ^a   Francescutti, T ^b   Cameron, C E ^b   Jenkinson, H F ^a   Dymock, D ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b UNIVERSITY OF VICTORIA   (Canada)

Author keywords

Fibronectin; LysM; M23 peptidase; Periodontal disease; Treponema

Indexed keywords

CARBOHYDRATE; FIBRONECTIN BINDING PROTEIN; PEPTIDASE; PEPTIDOGLYCAN; RECOMBINANT PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CELL SURFACE; ESCHERICHIA COLI; NONHUMAN; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; TREPONEMA DENTICOLA;

ADHESINS, BACTERIAL; AMINO ACID MOTIFS; BACTERIAL ADHESION; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL PROTEINS; BACTERIOCINS; BLOTTING, WESTERN; CARRIER PROTEINS; CONSENSUS SEQUENCE; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ESCHERICHIA COLI; FIBRONECTINS; GENOME, BACTERIAL; HUMANS; LIPOPROTEINS; MEMBRANE PROTEINS; OLIGOPEPTIDES; OPEN READING FRAMES; PEPTIDE HYDROLASES; PEPTIDOGLYCAN; PLASMIDS; SEQUENCE HOMOLOGY, AMINO ACID; TREPONEMA DENTICOLA; TREPONEMA PALLIDUM;

EID: 78049431143     PISSN: 20411006     EISSN: 20411014     Source Type: Journal    
DOI: 10.1111/j.2041-1014.2010.00584.x     Document Type: Article

References (61)

1. Altschul, S.F., Gish, W., Miller, W., Myers, E.W. and Lipman, D.J. (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
2. Baba, T. and Schneewind, O. (1996) Target cell specificity of a bacteriocin molecule: a C-terminal signal directs lysostaphin to the cell wall of Staphylococcus aureus. EMBO J 15: 4789-4797.
3. Bamford, C.V., Fenno, J.C., Jenkinson, H.F. and Dymock, D. (2007) The chymotrypsin-like protease complex of Treponema denticola ATCC 35405 mediates fibrinogen adherence and degradation. Infect Immun 75: 4364-4372.
4. Beatson, S.A., Sloan, G.L. and Simmonds, R.S. (1998) Zoocin A immunity factor: a femA-like gene found in group C streptococcus. FEMS Microbiol Lett 163: 73-77.
5. Brinkman, M.B., McGill, M.A., Pettersson, J. et al. (2008) A novel Treponema pallidum antigen, Tp0136, is an outer membrane protein that binds human fibronectin. Infect Immun 76: 1848-1857.
6. Cameron, C.E. (2003) Identification of a Treponema pallidum laminin binding protein. Infect Immun 71: 2525-2533.
7. Cameron, C.E., Brown, E.L., Kuroiwa, J.M., Schnapp, L.M. and Brouwer, N.L. (2004) Treponema pallidum fibronectin-binding proteins. J Bacteriol 186: 7019-7022.
8. Cameron, C.E., Kuroiwa, J.M.Y., Yamada, M., Francescutti, T., Chi, B. and Kuramitsu, H.K. (2008) Heterologous expression of the Treponema pallidum laminin-binding adhesin Tp0751 in the culturable spirochete Treponema phagedenis. J Bacteriol 190: 2565-2571.
9. Carroll, S.A., Hain, T., Technow, U. et al. (2003) Identification and characterisation of a peptidoglycan hydrolase, MurA, of Listeria monocytogenes, a muraminidase needed for cell separation. J Bacteriol 185: 6801-6808.
10. Chan, E.C.S., Siboo, R., Keng, T. et al. (1993) Treponema denticola (ex Brumpt 1925) sp. nov., nom. rev., and identification of new spirochete isolates from periodontal pockets. Int J Sys Bacteriol 43: 196-203.
11. Choi, B.K., Paster, B.J., Dewhirst, F.E. and Gobel, U.B. (1994) Diversity of cultivable and uncultivable oral spirochetes from a patient with severe destructive periodontitis. Infect Immun 62: 1889-1895.
12. Couchman, J.R., Austria, M.R. and Woods, A. (1990) Fibronectin-cell interactions. J Invest Dermatol 94: 7S-14S.
13. Dawson, J.R. and Ellen, R.P. (1990) Tip-oriented adherence of Treponema denticola to fibronectin. Infect Immun 58: 3924-3928.
14. DeHart, H.P., Heath, H.E., Heath, L.S., LeBlanc, P.A. and Sloan, G.L. (1995) The lysostaphin endopeptidase resistance gene (epr) specifies modification of peptidoglycan cross bridges in Staphylococcus simulans and Staphylococcus aureus. Appl Environ Microbiol 61: 1475-1479.
15. Dewhirst, F.E., Tamer, M.A., Ericson, R.E. et al. (2000) The diversity of periodontal spirochetes by 16S rRNA analysis. Oral Microbiol Immunol 15: 196-202.
16. Dziewanowska, K., Patti, J.M., Deobald, C.F., Bayles, K.W., Trumble, W.R. and Bohach, G.A. (1999) Fibronectin binding protein and host cell tyrosine kinase are required for internalisation of Staphylococcus aureus by epithelial cells. Infect Immun 67: 4673-4678.
17. Edwards, A.M., Jenkinson, H.F., Woodward, M.J. and Dymock, D. (2005) Binding properties and adhesion-mediating regions of the major sheath protein of Treponema denticola ATCC 35405. Infect Immun 73: 2891-2898.
18. Ellen, R.P., Song, M. and McCulloch, C.A. (1994) Degradation of endogenous plasma membrane fibronectin concomitant with Treponema denticola 35405 adhesion to gingival fibroblasts. Infect Immun 62: 3033-3037.
19. Fenno, J.C., Muller, K.H. and McBride, B.C. (1996) Sequence analysis, expression, and binding activity of recombinant major outer sheath protein (Msp) of Treponema denticola. J Bacteriol 178: 2489-2497.
20. Fenno, J.C., Wong, G.W., Hannam, P.M. and McBride, B.C. (1998) Mutagenesis of outer membrane virulence determinants of the oral spirochete Treponema denticola. FEMS Microbiol Lett 163: 209-215.
21. Fenno, J.C., Tamura, M., Hannam, P.M., Wong, G.W., Chan, R.A. and McBride, B.C. (2000) Identification of a Treponema denticola OppA homologue that binds host proteins present in the subgingival environment. Infect Immun 68: 1884-1892.
22. Haapasalo, M., Singh, U., McBride, B.C. and Uitto, V.J. (1991) Sulfhydryl-dependent attachment of Treponema denticola to laminin and other proteins. Infect Immun 59: 423-427.
23. Haapasalo, M., Muller, K.H., Uitto, V.J., Leung, W.K. and McBride, B.C. (1992) Characterization, cloning, and binding properties of the major 53-kilodalton Treponema denticola surface antigen. Infect Immun 60: 2058-2065.
24. Heath Farris, M., Heath, L.S., Heath, H.E., LeBlanc, P.A., Simmonds, R.S. and Sloan, G.L. (2003) Expression of the genes for lysostaphin and lysostaphin resistance in streptococci. FEMS Microbiol Lett 288: 115-119.
25. Heath, H.E., Heath, L.S., Nitterauer, J.D., Rose, K.E. and Sloan, G.L. (1989) Plasmid-encoded lysostaphin endopeptidase resistance of Staphylococcus simulans biovar staphylolyticus. Biochem Biophys Res Commum 15: 1106-1109.
26. Heath, L.S., Heath, H.E., LeBlanc, P.A. et al. (2004) The streptococcolytic enzyme ZoocinA is a penicillin-binding protein. FEMS Microbiol Lett 236: 205-211.
27. Heath, L.S., Gargis, S.R., Smithberg, S.R. et al. (2005) Plasmid-specified FemBX-like immunity factor in Staphylococcus sciuri DD4747. FEMS Microbiol Lett 249: 227-231.
28. Heilmann, C., Thumm, G., Chhatwal, G.S., Hartleib, J., Uekotter, A. and Peters, G. (2003) Identification and characterisation of a novel autolysin (Aae) with adhesive properties from Staphylococcus epidermidis. Microbiology 149: 2769-2778.
29. Heilmann, C., Niemann, S., Sinha, B., Herrmann, M., Kehrel, B.E. and Peters, G. (2004) Staphylococcus aureus fibronectin-binding protein (FnBP)-mediated adherence to platelets, and aggregation of platelets induced by FnBPA but not by FnBPB. J Infect Dis 190: 321-329.
30. Heilmann, C., Hartleib, J., Hussain, M.S. and Peters, G. (2005) The multifunctional Staphylococcus aureus autolysin, Aaa, mediates adherence to immobilised fibrinogen and fibronectin. Infect Immun 73: 4793-4802.
31. Izard, J., Hsieh, C.-E., Limberger, R.J., Mannella, C.A. and Marko, M. (2008) Native cellular architecture of Treponema denticola revealed by cryo-electron tomography. J Struct Biol 163: 10-17.
32. Izard, J., Renken, C., Hsieh, C.-E. et al. (2009) Cryo-electron tomography elucidates the molecular architecture of Treponema pallidum, the syphilis spirochete. J Bacteriol 191: 7566-7580.
33. Kigure, T., Saito, A., Seida, K., Yamada, S., Ishihara, K. and Okuda, K. (1995) Distribution of Porphyromonas gingivalis and Treponema denticola in human subgingival plaque at different periodontal pocket depths examined by immunohistochemical methods. J Periodontal Res 30: 332-341.
34. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
35. Lai, A.C., Tran, S. and Simmonds, R.S. (2002) Functional characterisation of domains found within a lytic enzyme produced by Streptococcus equi subsp. zooepidemicus. FEMS Microbiol Lett 215: 133-138.
36. Maidhof, H., Reinicke, B., Blumel, P., Berger-Bachi, B. and Labischinski, H. (1991) femA, which encodes a factor essential for expression of methicillin resistance, affects glycine content of peptidoglycan in methicillin-resistant and methicillin-susceptible Staphylococcus aureus strains. J Bacteriol 173: 3507-3513.
37. Naverre, W.W. and Schneewind, O. (1999) Surface proteins of gram-positive bacteria and mechanisms of their targeting to the cell wall envelope. Microbiol Rev 63: 174-229.
38. Nelson, K. and Selander, R.K. (1994) Analysis of genetic variation by polymerase chain reaction-based nucleotide sequencing. Methods Enzymol 235: 174-183.
39. Nilsen, T., Nes, I.F. and Holo, H. (2003) Enterolysin, a cell wall-degrading bacteriocin from Enterococcus faecalis LMG 2333. App Env Microbiol 69: 2975-2984.
40. Pasula, R., Wisniowski, P. and Martin, W.J., 2nd. (2002) Fibronectin facilitates Mycobacterium tuberculosis attachment to murine alveolar macrophages. Infect Immun 70: 1287-1292.
41. Peterson, K.M., Baseman, J.B. and Alderete, J.F. (1983) Treponema pallidum receptor binding proteins interact with fibronectin. J Exp Med 157: 1958-1970.
42. Pracht, D., Elm, C., Gerber, J. et al. (2005) PavA of Streptococcus pneumoniae modulates adherence invasion and meningeal inflammation. Infect Immun 73: 2680-2689.
43. Recsei, P.A., Gruss, A.D. and Novick, R.P. (1987) Cloning, sequence and expression of the lysostaphin gene from Staphylococcus simulans. Proc Natl Acad Sci USA 84: 1127-1131.
44. Riviere, G.R. and DeRouen, T.A. (1998) Association of oral spirochetes from periodontally healthy sites with development of gingivitis. J Periodontol 69: 496-501.
45. Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
46. Samen, U., Gottschalk, B., Eikmanns, B.J. and Reinscheid, D.J. (2004) Relevance of peptide uptake systems to the physiology and virulence of Streptococcus agalactiae. J Bacteriol 186: 1398-1408.
47. Schindler, C.A. and Schuhardt, V.T. (1964) Lysostaphin: a new bacteriolytic agent for the staphylococcus. Proc Natl Acad Sci USA 51: 414-421.
48. Schindler, C.A. and Schuhardt, V.T. (1965) Purification and properties of lysostaphin - a lytic agent of Staphylococcus aureus. Biochem Biophys Acta 97: 242-250.
49. Schwarz-Linek, U., Hook, M. and Potts, J.R. (2004) The molecular basis of fibronectin-mediated bacterial adherence to host cells. Mol Microbiol 52: 631-641.
50. Seshadri, R., Myers, G.S., Tettelin, H. et al. (2004) Comparison of the genome of the oral pathogen Treponema denticola with other spirochete genomes. Proc Natl Acad Sci USA 101: 5646-5651.
51. Simmonds, R.S., Pearson, L., Kennedy, R.C. and Tagg, J.R. (1996) Mode of action of a lysostaphin-like bacteriolytic agent produced by Streptococcus zooepidemicus 4881. Appl Environ Microbiol 62: 4536-4541.
52. Simmonds, R.S., Simpson, W.J. and Tagg, J.R. (1997) Cloning and sequence analysis of zooA, a Streptococcus zooepidemicus gene encoding a bacteriocin-like inhibitory substance having a domain structure similar to that of lysostaphin. Gene 189: 255-261.
53. Sinha, B., Francois, P.P., Nusse, O. et al. (1999) Fibronectin-binding protein acts as Staphylococcus aureus invasin via fibronectin bridging to integrin α5β1. Cell Microbiol 1: 101-117.
54. Ter Steeg, P.F. and Van Der Hoeven, J.S. (1990) Growth stimulation of Treponema denticola by periodontal microorganisms. Antonie Van Leeuwenhoek, 57: 63-70.
55. Steen, A., Buist, G., Leenhouts, K.J. et al. (2003) Cell wall attachment of a widely distributed peptidoglycan binding domain is hindered by cell wall constituents. J Biol Chem 278: 23874-23881.
56. Sugai, M., Fujiwara, T., Akiyama, T. et al. (1997a) Purification and molecular characterisation of glycineglycine endopeptidase produced by Staphylococcus capitis EPK1. J Bacteriol 179: 1193-1202.
57. Sugai, M., Fujiwara, T., Ohta, K., Komatsuzawa, H., Ohara, M. and Suginaka, H. (1997b) epr, which encodes glycylglycine endopeptidase resistance, is homologous to femAB and affects serine content of peptidoglycan cross bridges in Staphylococcus capitis and Staphylococcus aureus. J Bacteriol 179: 4311-4318.
58. Thomas, D.D., Baseman, J.B. and Alderete, J.F. (1986) Enhanced levels of attachment of fibronectin-primed Treponema pallidum to extracellular matrix. Infect Immun 52: 736-741.
59. Thumm, G. and Gotz, F. (1997) Studies on prolysostaphin processing and characterization of the lysostaphin immunity factor (Lif) of Staphylococcus simulans biovar staphylolyticus. Mol Microbiol 23: 1251-1265.
60. Turner, M.S., Hafner, L.M., Walsh, T. and Giffard, P.M. (2004) Identification and characterisation of the Novel LysM domain-containing surface protein Sep from Lactobacillus fermentum BR11 and its use as a peptide fusion partner in Lactobacillus and Lactococcus. Appl Environ Microbiol 70: 3673-3680.
61. Umemoto, T., Nakatani, Y., Nakamura, Y. and Namikawa, I. (1993) Fibronectin-binding proteins of a human oral spirochete Treponema denticola. Microbiol Immunol 37: 75-78.