Abstract
Porphyromonas gingivalis, a primary pathogen in adult periodontitis, may establish itself in the oral cavity by adhering to early plaque bacteria such as Streptococcus gordonii. Our previous studies (R. J. Lamont et al., Microbiology 140:867-872, 1994) suggested that this interaction is mediated by the SspB polypeptide, a member of the antigen I/II family of streptococcal surface proteins. S. gordonii was recently shown to express a second Ssp polypeptide (SspA) that resembles SspB and the structurally homologous antigen I/II polypeptide (Pac) of Streptococcus mutans. To determine if all of these related antigen I/II proteins interacted with P. gingivalis, SspA, SspB, and Pac were tested for adhesion to P. gingivalis cells. Both of the S. gordonii Ssp proteins bound labeled target cells, whereas the S. mutans Pac polypeptide did not, suggesting that antigen I/II-mediated binding of P. gingivalis by streptococci may be species specific. To investigate the molecular basis for this functional difference, the P. gingivalis binding domain of SspB was mapped. The binding properties of a family of truncated SspB polypeptides lacking C-terminal sequences were determined. In addition, the lack of binding activity exhibited by the Pac protein was exploited to construct and analyze chimeric SspB-Pac polypeptides. Both approaches revealed that the region defined by residues 1167 to 1250 of SspB was essential for P. gingivalis binding. This region of SspA and SspB is entirely conserved, consistent with the binding properties determined for these proteins. However, the corresponding region of Pac differs in both the primary sequence and predicted secondary structure, suggesting that the overall structure of this domain may define its functional activity.
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Selected References
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- Cutler C. W., Kalmar J. R., Genco C. A. Pathogenic strategies of the oral anaerobe, Porphyromonas gingivalis. Trends Microbiol. 1995 Feb;3(2):45–51. doi: 10.1016/s0966-842x(00)88874-5. [DOI] [PubMed] [Google Scholar]
- Demuth D. R., Davis C. A., Corner A. M., Lamont R. J., Leboy P. S., Malamud D. Cloning and expression of a Streptococcus sanguis surface antigen that interacts with a human salivary agglutinin. Infect Immun. 1988 Sep;56(9):2484–2490. doi: 10.1128/iai.56.9.2484-2490.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Demuth D. R., Duan Y., Brooks W., Holmes A. R., McNab R., Jenkinson H. F. Tandem genes encode cell-surface polypeptides SspA and SspB which mediate adhesion of the oral bacterium Streptococcus gordonii to human and bacterial receptors. Mol Microbiol. 1996 Apr;20(2):403–413. doi: 10.1111/j.1365-2958.1996.tb02627.x. [DOI] [PubMed] [Google Scholar]
- Demuth D. R., Golub E. E., Malamud D. Streptococcal-host interactions. Structural and functional analysis of a Streptococcus sanguis receptor for a human salivary glycoprotein. J Biol Chem. 1990 May 5;265(13):7120–7126. [PubMed] [Google Scholar]
- Demuth D. R., Lammey M. S., Huck M., Lally E. T., Malamud D. Comparison of Streptococcus mutans and Streptococcus sanguis receptors for human salivary agglutinin. Microb Pathog. 1990 Sep;9(3):199–211. doi: 10.1016/0882-4010(90)90022-i. [DOI] [PubMed] [Google Scholar]
- Duan Y., Fisher E., Malamud D., Golub E., Demuth D. R. Calcium-binding properties of SSP-5, the Streptococcus gordonii M5 receptor for salivary agglutinin. Infect Immun. 1994 Dec;62(12):5220–5226. doi: 10.1128/iai.62.12.5220-5226.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Goulbourne P. A., Ellen R. P. Evidence that Porphyromonas (Bacteroides) gingivalis fimbriae function in adhesion to Actinomyces viscosus. J Bacteriol. 1991 Sep;173(17):5266–5274. doi: 10.1128/jb.173.17.5266-5274.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hanahan D. Studies on transformation of Escherichia coli with plasmids. J Mol Biol. 1983 Jun 5;166(4):557–580. doi: 10.1016/s0022-2836(83)80284-8. [DOI] [PubMed] [Google Scholar]
- Jenkinson H. F., Demuth D. R. Structure, function and immunogenicity of streptococcal antigen I/II polypeptides. Mol Microbiol. 1997 Jan;23(2):183–190. doi: 10.1046/j.1365-2958.1997.2021577.x. [DOI] [PubMed] [Google Scholar]
- Kinane D. F., Jenkins W. M., Adonogianaki E., Murray G. D. Cross-sectional assessment of caries and periodontitis risk within the same subject. Community Dent Oral Epidemiol. 1991 Apr;19(2):78–81. doi: 10.1111/j.1600-0528.1991.tb00115.x. [DOI] [PubMed] [Google Scholar]
- Lamont R. J., Bevan C. A., Gil S., Persson R. E., Rosan B. Involvement of Porphyromonas gingivalis fimbriae in adherence to Streptococcus gordonii. Oral Microbiol Immunol. 1993 Oct;8(5):272–276. doi: 10.1111/j.1399-302x.1993.tb00573.x. [DOI] [PubMed] [Google Scholar]
- Lamont R. J., Gil S., Demuth D. R., Malamud D., Rosan B. Molecules of Streptococcus gordonii that bind to Porphyromonas gingivalis. Microbiology. 1994 Apr;140(Pt 4):867–872. doi: 10.1099/00221287-140-4-867. [DOI] [PubMed] [Google Scholar]
- Lamont R. J., Hersey S. G., Rosan B. Characterization of the adherence of Porphyromonas gingivalis to oral streptococci. Oral Microbiol Immunol. 1992 Aug;7(4):193–197. doi: 10.1111/j.1399-302x.1992.tb00024.x. [DOI] [PubMed] [Google Scholar]
- Lamont R. J., Hsiao G. W., Gil S. Identification of a molecule of Porphyromonas gingivalis that binds to Streptococcus gordonii. Microb Pathog. 1994 Nov;17(5):355–360. doi: 10.1006/mpat.1994.1081. [DOI] [PubMed] [Google Scholar]
- Li J., Ellen R. P., Hoover C. I., Felton J. R. Association of proteases of Porphyromonas (Bacteroides) gingivalis with its adhesion to Actinomyces viscosus. J Dent Res. 1991 Feb;70(2):82–86. doi: 10.1177/00220345910700021501. [DOI] [PubMed] [Google Scholar]
- Loesche W. J. Bacterial mediators in periodontal disease. Clin Infect Dis. 1993 Jun;16 (Suppl 4):S203–S210. doi: 10.1093/clinids/16.supplement_4.s203. [DOI] [PubMed] [Google Scholar]
- Ma J. K., Kelly C. G., Munro G., Whiley R. A., Lehner T. Conservation of the gene encoding streptococcal antigen I/II in oral streptococci. Infect Immun. 1991 Aug;59(8):2686–2694. doi: 10.1128/iai.59.8.2686-2694.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mayrand D., Holt S. C. Biology of asaccharolytic black-pigmented Bacteroides species. Microbiol Rev. 1988 Mar;52(1):134–152. doi: 10.1128/mr.52.1.134-152.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nyvad B., Kilian M. Microbiology of the early colonization of human enamel and root surfaces in vivo. Scand J Dent Res. 1987 Oct;95(5):369–380. doi: 10.1111/j.1600-0722.1987.tb01627.x. [DOI] [PubMed] [Google Scholar]
- Okahashi N., Sasakawa C., Yoshikawa M., Hamada S., Koga T. Molecular characterization of a surface protein antigen gene from serotype c Streptococcus mutans, implicated in dental caries. Mol Microbiol. 1989 May;3(5):673–678. doi: 10.1111/j.1365-2958.1989.tb00215.x. [DOI] [PubMed] [Google Scholar]
- Potempa J., Pavloff N., Travis J. Porphyromonas gingivalis: a proteinase/gene accounting audit. Trends Microbiol. 1995 Nov;3(11):430–434. doi: 10.1016/s0966-842x(00)88996-9. [DOI] [PubMed] [Google Scholar]
- Ross A. M., Golub E. E. A computer graphics program system for protein structure representation. Nucleic Acids Res. 1988 Mar 11;16(5):1801–1812. doi: 10.1093/nar/16.5.1801. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Russell M. W., Bergmeier L. A., Zanders E. D., Lehner T. Protein antigens of Streptococcus mutans: purification and properties of a double antigen and its protease-resistant component. Infect Immun. 1980 May;28(2):486–493. doi: 10.1128/iai.28.2.486-493.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Slots J., Gibbons R. J. Attachment of Bacteroides melaninogenicus subsp. asaccharolyticus to oral surfaces and its possible role in colonization of the mouth and of periodontal pockets. Infect Immun. 1978 Jan;19(1):254–264. doi: 10.1128/iai.19.1.254-264.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Socransky S. S., Haffajee A. D. The bacterial etiology of destructive periodontal disease: current concepts. J Periodontol. 1992 Apr;63(4 Suppl):322–331. doi: 10.1902/jop.1992.63.4s.322. [DOI] [PubMed] [Google Scholar]