Sequence analysis, expression, and binding activity of recombinant major outer sheath protein (Msp) of Treponema denticola

Journal of Bacteriology

Volumn 178, Issue 9, 1996, Pages 2489-2497

  Fenno, J Christopher ^a   Müller, Karl Heinz ^a   McBride, Barry C ^a,b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b Faculty of Science   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; BACTERIAL PROTEIN; FIBRONECTIN; HYBRID PROTEIN; LAMININ; OUTER MEMBRANE PROTEIN; RECOMBINANT PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL OUTER MEMBRANE; BINDING AFFINITY; EXTRACELLULAR MATRIX; GENE AMPLIFICATION; GENE EXPRESSION; GENOME; HOST RESISTANCE; NONHUMAN; NORTHERN BLOTTING; OPEN READING FRAME; PERIODONTITIS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SPIROCHETE; TREPONEMA DENTICOLA;

BACTERIA (MICROORGANISMS); BOVINAE; ESCHERICHIA COLI; PROKARYOTA; SPIROCHAETALES; TREPONEMA; TREPONEMA DENTICOLA; TREPONEMA DENTICOLA ATCC 35405;

EID: 0029863955     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/jb.178.9.2489-2497.1996     Document Type: Article

References (75)

1. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990 Basic local alignment search tool. J. Mol. Biol. 215:403-410.
2. Arakawa, S., and H. K. Kuramitsu. 1994. Cloning and sequence analysis of a chymotrypsinlike protease from Treponema denticola. Infect. Immun. 62: 3424-3433.
3. Armitage, G. C., W. R. Dickinson, R. S. Jenderseck, S. M. Levine, and D. W. Chambers. 1982. Relationship between the percentage of subgingival spirochetes and the severity of periodontal disease. J. Periodontol. 53:550-556.
4. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl (ed.). 1995. Current protocols in molecular Biology. Wiley-Interscience, New York.
5. Baehni, P. C., M. Song, C. A. McCulloch, and R. P. Ellen. 1992. Treponema denticola induces actin rearrangement and detachment of human gingival fibroblasts. Infect. Immun. 60:3360-3368.
6. Bellinger-Kawahara, C., and M. A. Horwitz. 1990. Complement component C3 fixes selectively to the major outer membrane protein (MOMP) of Legionella pneumophila and mediates phagocytosis of liposome-MOMP complexes by human monocytes. J. Exp. Med. 172:1201-1210.
7. Blanco, D. R., C. I. Champion, M. M. Exner, H. Erdjument-Bromage, R. E. Hancock, P. Tempst, J. N. Miller, and M. A. Lovett. 1995. Porin activity and sequence analysts of a 31-kilodalton Treponema pallidum subsp. pallidum rare outer membrane protein (Tromp1). J. Bacteriol. 177:3556-3562.
8. Chu, L., and S. C. Holt. 1994. Purification and characterization of a 45 kDa hemolysin from Treponema denticola ATCC 35404. Microb. Pathog. 16:197-212.
9. Cockayne, A., R. Sanger, A. Ivic, R. A. Strugnell, J. H. MacDougall, R. R. Russell, and C. W. Penn. 1989. Antigenic and structural analysis of Treponema denticola J Gen. Microbiol. 135:3209-3218.
10. Dalbey, R. E., and G. Von Heijne. 1992. Signal peptidases in prokaryotes and eukaryotes - a new protease family. Trends Biochem. Sci. 17:474-478.
11. Dawson, J. R., and R. P. Ellen. 1990. Tip-oriented adherence of Treponema denticola to fibronectin. Infect. Immun. 58:3924-3928.
12. Egli, C., W. K. Leung, K. H. Muller, R. E. Hancock, and B. C. McBride. 1993. Pore-forming properties of the major 53-kilodalton surface antigen from the outer sheath of Treponema denticola. Infect. Immun. 61:1694-1699.
13. Eisenberg, D., R. M. Weiss, and T. C. Terwilliger. 1984. The hydrophobic moment detects periodicity in protein hydrophobicity. Proc. Natl. Acad. Sci. USA 81:140-144
14. Feavers, I. M., J. Suker, A. J. McKenna, A. B. Heath, and M. C. Maiden. 1992. Molecular analysis of the serotyping antigens of Neisseria meningitidis Infect. Immun. 60:3620-3629.
15. Feinberg, A. P., and B. Vogelstein. 1983. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal. Biochem. 132:6-13.
16. Gopalsami, C., W. Yotis, K. Corrigan, S. Schade, J. Keene, and L. Simonson. 1993. Effect of outer membrane of Treponema denticola on bone resorption. Oral Microbiol. Immunol. 8:121-124.
17. Gotschlich, E. C., M. E. Seiff, M. S. Blake, and M. Koomey. 1987. Porin protein of Neisseria gonorrhoeae: cloning and gene structure. Proc. Natl. Acad. Sci. USA 84:8135-8139.
18. Grenier, D. 1991. Characteristics of hemolytic and hemagglutinating activities of Treponema denticola. Oral Microbiol. Immunol. 6:246-249.
19. Grenier, D. 1992. Demonstration of a bimodal coaggregation reaction between Porphyromonas gingivalis and Treponema denticola Oral Microbiol. Immunol. 7:280-284
20. Grenier, D., and V. J. Uitto. 1993. Cytotoxic effect of peptidoglycan from Treponema denticola. Microb. Pathog. 15:389-397.
21. Grenier, D., V. J. Uitto, and B. C. McBride. 1990. Cellular location of a Treponema denticola chymotrypsinlike protease and importance of the protease in migration through the basement membrane. Infect. Immun. 58:347-351.
22. Haapasalo, M., K. H. Muller, V. J. Uitto, W. K. Leung, and B. C. McBride. 1992. Characterization, cloning, and binding properties of the major 53-kilodalton Treponema denticola surface antigen. Infect Immun. 60:2058-2065.
23. Haapasalo, M., U. Singh, B. C. McBride, and V.-J. Uitto. 1991. Sulfhydryl dependent attachment of Treponema denticola to laminin and other proteins. Infect. Immun. 59:4230-4237.
24. Hansen, E. J., F. R. Gonzales, N. R. Chamberlain, M. V. Norgard, E. E. Miller, L. D. Cope, S. E. Pelzel, B. Gaddy, and A. Clausell. 1988. Cloning of the gene encoding the major outer membrane protein of Haemophilus influenzae type b. Infect. Immun. 56:2709-2716.
25. Harlow, E., and D. Lane. 1988. Antibodies, a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
26. Heinzerling, H. F., J. E. Penders, and R. A. Burne. 1995. Identification of a fliG homologue in Treponema denticola. Gene 161:69-73.
27. Ishihara, K., M. Ishihara, I. Takazoe, and K. Okuda. 1992. Cloning and expression of the aspartate carbamoyltransferase gene from Treponema denticola. Appl. Environ Microbiol. 58:3399-3403.
28. Ishihara, K., and H. K. Kuramitsu. 1995. Cloning and expression of a neutral phosphatase gene from Treponema denticola. Infect. Immun. 63: 1147-1152.
29. Jeanteur, D., J. H. Lakey, and F. Pattus. 1991. The bacterial porin superfamily: sequence alignment and structure prediction. Mol. Microbiol. 5:2153-2164.
30. Karunakaran, T., and S. C. Holt. 1994. Cloning and expression of hemolysin genes from Treponema denticola strains ATCC 35404 (TD-4) and human clinical isolate GM-1 in Escherichia coli. Microb Pathog. 16:337-348
31. Keulers, R. A., J. C. Maltha, F. H. Mikx, and J. M. Wolters-Lutgerhorst. 1993. Attachment of Treponema denticola strains to monolayers of epithelial cells of different origin. Oral Microbiol. Immunol. 8:84-88.
32. Kolenbrander, P. E., and J. London. 1993. Adhere today, here tomorrow: oral bacterial adherence. J. Bacteriol. 175:3247-3252.
33. Kyte, J., and R. F. Doolittle. 1982. A simple method for displaying the hydropathic character of a protein. J Mol. Biol. 157:105-132.
34. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (London) 277:680-685.
35. Lin, H. C., S. P. Lei, and G. Wilcox. 1985 An improved DNA sequencing strategy. Anal. Biochem. 147:114-119.
36. Lisser, S., and H. Margalit. 1993. Compilation of E. coli mRNA promoter sequences. Nucleic Acids Res. 21:1507-1516.
37. Listgarten, M. A. 1987. Nature of periodontal diseases: pathogenic mechanisms. J. Periodontal Res. 22:172-178.
38. Listgarten, M. A., and S. Levin. 1981. Positive correlation between the proportions of subgingival spirochetes and motile bacteria and susceptibility of human subjects to periodontal deterioration. J. Clin. Periodontol. 8:122-138.
39. Loesche, W. J. 1993. Bacterial mediators in periodontal disease. Clin. Infect. Dis. 16:S203-S210.
40. Loesche, W. J., and B. E. Laughon. 1982. Role of spirochetes in periodontal disease, p. 62-75. In R. J. Genco and S. E. Mergenhagen (ed.), Host-parasite interactions in periodontal diseases. American Society for Microbiology, Washington, D.C.
41. Loesche, W. J., S. A. Syed, E. Schmidt, and E. C. Morrison. 1985. Bacterial profiles of subgingival plaques in periodontitis. J. Periodontol. 56:447-456.
42. MacDougall, J., D. Margarita, and I. Saint Girons. 1992. Homology of a plasmid from the spirochete Treponema denticola with the single-stranded DNA plasmids. J. Bacteriol. 174:2724-2728.
43. Messner, P., and U. B. Sleytr. 1991. Bacterial surface layer glycoproteins Glycobiology 1:545-551.
44. Messner, P., and U. B. Sleytr. 1992. Crystalline bacterial cell-surface layers. Adv. Microb. Physiol. 33:213-275.
45. Miyamoto, M., S. Noji, S. Kokeguchi, K. Kato, H. Kurihara, Y. Murayama, and S. Taniguchi. 1991. Molecular cloning and sequence analysis of antigen gene tdpA of Treponema denticola. Infect. Immun. 59:1941-1947.
46. Moore, W. E. 1987. Microbiology of periodontal disease. J. Periodontal Res. 22:335-341.
47. Nakamura, Y., T. Umenrato, Y. Nakatani, I. Namikawa, and A. Wadood. 1993. Common and specific antigens of several treponemes detected by polyclonal antisera against major cellular proteins. Oral Microbiol. Immunol. 8:288-294.
48. Olsen, I. 1984. Attachment of Treponema denticola to cultured human epithelial cells. Scand. J. Dent Res. 92:55-63.
49. Paster, B. J., F. E. Dewhirst, W. G. Weisburg, L. A. Tordoff, G. J. Fraser, R. B. Hespell, T. B. Stanton, L. Zablen, L. Mandelco, and C. R. Woese. 1991. Phylogenetic analysts of the spirochetes. J. Bacteriol. 173:6101-6109.
50. Pugsley, A. P. 1993. The complete general secretory pathway in gram-negative bacteria. Microbiol. Rev. 57:50-108.
51. Qi, H. L., J. Y. Tai, and M. S. Blake. 1994. Expression of large amounts of neisserial porin proteins in Escherichia coli and refolding of the proteins into native trimers Infect. Immun. 62:2432-2439.
52. Reijntjens, F. M., F. H. Mikx, J. M. Wolters-Lutgerhorst, and J. C. Maltha. 1986. Adherence of oral treponemes and their effect on morphological damage and detachment of epithelial cells in vitro. Infect. Immun. 51:642-647.
53. Ringquist, S., S. Shinedling, D. Barrick, L. Green, J. Binkley, G. D. Stormo, and L. Gold. 1992. Translation initiation in Escherichia coli: sequences within the ribosome-binding site. Mol. Microbiol. 6:1219-1229
54. Saglie, R., F. A. Carranza, Jr., M. G. Newman, A. L. Cheng, and K. J. Lewin. 1982. Identification of tissue-invading bacteria in human periodontal disease. J. Periodontal Res. 17:452-455.
55. Saglie, R., M. G. Newman, F. A. Carranza, Jr., and G. L. Pattison. 1982. Bacterial invasion of gingiva in advanced periodontitis in humans. J. Periodontol. 53:217-222.
56. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
57. Sela, M. N., A. Weinberg, R. Borinsky, S. C. Holt, and T. Dishon. 1988. Inhibition of superoxide production in human polymorphonuclear leukocytes by oral treponemal factors. Infect. Immun. 56:589-594
58. Shea, C. M., and M. A. McIntosh. 1991. Nucleotide sequence and genetic organization of the ferric enterobactin transport system: homology to other periplasmic binding protein-dependent systems in Escherichia coli. Mol. Microbiol. 5:1415-1428.
59. Silhavy, T. J., M. J. Herman, and L. W. Enquist. 1984. Experiments with gene fusions. Cold Spring Harbor Laboratory, Cold Spring Harbor, N Y
60. Simonson, L. G., C. H. Goodman, J. J. Bial, and H. E. Morton. 1988. Quantitative relationship of Treponema denticola to severity of periodontal disease. Infect. Immun. 56:726-728.
61. Simonson, L. G., R. F. Rouse, and S. W. Bockowski. 1988. Monoclonal antibodies that recognize a specific surface antigen of Treponema denticola. Infect. Immun. 56:60-63.
62. Sorsa, T., T. Ingman, K. Suomalainen, M. Haapasalo, Y. T. Konttinen, O. Lindy, H. Saari, and V. J. Uitto. 1992. Identification of proteases from periodontopathogenic bacteria as activators of latent human neutrophil and fibroblast-type interstitial collagenases. Infect. Immun. 60:4491-4495.
63. Su, H., N. G. Watkins, Y. X. Zhang, and H. D. Caldwell. 1990. Chlamydia trachomatis-host cell interactions: role of the chlamydial major outer membrane protein as an adhesin. Infect. Immun 58:1017-1025.
64. Towbin, H., T. Staehelin, and J. Gordon. 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedures and some applications. Proc. Natl. Acad. Sci. USA 76:4350-4354.
65. Ditto, V.-J., D. Grenier, E. C. Chan, and B. C. McBride. 1988. Isolation of a chymotrypsinlike enzyme from Treponema denticola. Infect. Immun. 56:2717-2722.
66. Uitto, V.-J., Y. M. Pan, W. K. Leung, H. Larjava, R. P. Ellen, B. B. Finlay, and B. C. McBride. 1995. Cytopathic effects of Treponema denticola chymotrypsin-like proteinase on migrating and stratified epithelial cells. Infect. Immun. 63:3401-3410.
67. Umemoto, T., Y. Nakatani, Y. Nakamura, and I. Namikawa. 1993. Fibronectin-binding proteins of a human oral spirochete Treponema denticola. Microbiol. Immunol. 37:75-78.
68. Umemoto, T., and I. Namikawa. 1994. Binding of host-associated treponeme proteins to collagens and laminin: a possible mechanism of spirochetal adherence to host tissues. Microbiol. Immunol 38:655-663
69. Umemoto, T., I. Namikawa, H. Suido, and S. Asai. 1989 A major antigen on the outer envelope of a human oral spirochete, Treponema denticola Infect. Immun. 57:2470-2474
70. Umemoto, T., J. J. Zambon, R. J. Genco, and I. Namikawa. 1988. Major antigens of human oral spirochetes associated with periodontal disease. Adv. Dent. Res. 2:292-296.
71. Vidgrén, G., I. Palva, R. Pakkanen, K. Lounatmaa, and A. Palva. 1992 S-layer protein gene of Lactobacillus brevis: cloning by polymerase chain reaction and determination of the nucleotide sequence. J. Bacteriol. 174: 7419-7427.
72. Weinberg, A., and S. C. Holt. 1990. Interaction of Treponema denticola TD-4. GM-1, and MS25 with human gingival fibroblasts Infect. Immun. 58:1720-1729.
73. Weinberg, A., and S. C. Holt. 1991. Chemical and biological activities of a 64-kilodalton outer sheath protein from Treponema denticola strains. J. Bacteriol. 173:6935-6947.
74. Westerlund, B., and T. K. Korhonen. 1993. Bacterial proteins binding to the mammalian extracellular matrix Mol. Microbiol. 9:687-694.
75. Yotis, W. W., V. K. Sharma, C. Gopalsami, S. Chegini, J. McNulty, K. Hoerman, J. Keene, Jr., and L. G. Simonson. 1991. Biochemical properties of the outer membrane of Treponema denticola. J. Clin. Microbiol. 29:1397-1406.