Skip to main content
Infection and Immunity logoLink to Infection and Immunity
. 1997 Dec;65(12):5042–5051. doi: 10.1128/iai.65.12.5042-5051.1997

A specific cell surface antigen of Streptococcus gordonii is associated with bacterial hemagglutination and adhesion to alpha2-3-linked sialic acid-containing receptors.

Y Takahashi 1, A L Sandberg 1, S Ruhl 1, J Muller 1, J O Cisar 1
PMCID: PMC175727  PMID: 9393794

Abstract

A Ca2+-independent lectin activity for alpha2-3-linked sialic acid-containing receptors is associated with Streptococcus gordonii DL1 (Challis) but not with a spontaneous mutant, strain D102, that specifically lacks hemagglutinating activity. Comparison of crossed-immunoelectrophoresis patterns of parent and mutant sonicated cell extracts identified a unique antigen (Hs antigen) in the parent cell extract that was purified by DEAE Sephacel column chromatography and by a wheat germ agglutinin (WGA) lectin affinity column. The purified antigen formed a single arc in crossed immunoelectrophoresis with anti-DL1 serum and migrated as a diffuse band above the 200-kDa marker in sodium dodecyl sulfate-polyacrylamide gel electrophoresis. Immunoelectron microscopy with specific anti-Hs antibody revealed labeling of structures in the fibrillar layer of strain DL1 and no labeling of fibrillar structures on strain D102. Rabbit anti-DL1 serum and anti-Hs Fab inhibited the hemagglutinating activity of strain DL1, and the inhibition was specifically neutralized by purified Hs antigen. Anti-Hs Fab did not inhibit the hemagglutinating activities of several heterologous S. gordonii strains; however, these bacteria were agglutinated by anti-Hs immunoglobulin G and also by WGA. In contrast, two S. gordonii strains that lacked hemagglutinating activity did not react with anti-Hs antibody or with WGA. These findings associate the sialic acid-binding lectin activity of S. gordonii DL1 with a specific fibrillar antigen, which is composed of protein and WGA reactive carbohydrate, and indicate that cross-reactive antigens occur on other strains of this species that possess hemagglutinating activity.

Full Text

The Full Text of this article is available as a PDF (1.8 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bayer E. A., Ben-Hur H., Wilchek M. Biocytin hydrazide--a selective label for sialic acids, galactose, and other sugars in glycoconjugates using avidin-biotin technology. Anal Biochem. 1988 May 1;170(2):271–281. doi: 10.1016/0003-2697(88)90631-8. [DOI] [PubMed] [Google Scholar]
  2. Cisar J. O., Barsumian E. L., Curl S. H., Vatter A. E., Sandberg A. L., Siraganian R. P. Detection and localization of a lectin on Actinomyces viscosus T14V by monoclonal antibodies. J Immunol. 1981 Oct;127(4):1318–1322. [PubMed] [Google Scholar]
  3. Cisar J. O., Kolenbrander P. E., McIntire F. C. Specificity of coaggregation reactions between human oral streptococci and strains of Actinomyces viscosus or Actinomyces naeslundii. Infect Immun. 1979 Jun;24(3):742–752. doi: 10.1128/iai.24.3.742-752.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Clark W. B., Wheeler T. T., Cisar J. O. Specific inhibition of adsorption of Actinomyces viscosus T14V to saliva-treated hydroxyapatite by antibody against type 1 fimbriae. Infect Immun. 1984 Feb;43(2):497–501. doi: 10.1128/iai.43.2.497-501.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Demuth D. R., Berthold P., Leboy P. S., Golub E. E., Davis C. A., Malamud D. Saliva-mediated aggregation of Enterococcus faecalis transformed with a Streptococcus sanguis gene encoding the SSP-5 surface antigen. Infect Immun. 1989 May;57(5):1470–1475. doi: 10.1128/iai.57.5.1470-1475.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. 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]
  7. 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]
  8. 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]
  9. 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]
  10. Elder B. L., Fives-Taylor P. Characterization of monoclonal antibodies specific for adhesion: isolation of an adhesin of Streptococcus sanguis FW213. Infect Immun. 1986 Nov;54(2):421–427. doi: 10.1128/iai.54.2.421-427.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Fachon-Kalweit S., Elder B. L., Fives-Taylor P. Antibodies that bind to fimbriae block adhesion of Streptococcus sanguis to saliva-coated hydroxyapatite. Infect Immun. 1985 Jun;48(3):617–624. doi: 10.1128/iai.48.3.617-624.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Fairbanks G., Steck T. L., Wallach D. F. Electrophoretic analysis of the major polypeptides of the human erythrocyte membrane. Biochemistry. 1971 Jun 22;10(13):2606–2617. doi: 10.1021/bi00789a030. [DOI] [PubMed] [Google Scholar]
  13. Fives-Taylor P. M., Macrina F. L., Pritchard T. J., Peene S. S. Expression of Streptococcus sanguis antigens in Escherichia coli: cloning of a structural gene for adhesion fimbriae. Infect Immun. 1987 Jan;55(1):123–128. doi: 10.1128/iai.55.1.123-128.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Ganeshkumar N., Arora N., Kolenbrander P. E. Saliva-binding protein (SsaB) from Streptococcus sanguis 12 is a lipoprotein. J Bacteriol. 1993 Jan;175(2):572–574. doi: 10.1128/jb.175.2.572-574.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Ganeshkumar N., Song M., McBride B. C. Cloning of a Streptococcus sanguis adhesin which mediates binding to saliva-coated hydroxyapatite. Infect Immun. 1988 May;56(5):1150–1157. doi: 10.1128/iai.56.5.1150-1157.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Gibbons R. J., Etherden I., Moreno E. C. Association of neuraminidase-sensitive receptors and putative hydrophobic interactions with high-affinity binding sites for Streptococcus sanguis C5 in salivary pellicles. Infect Immun. 1983 Dec;42(3):1006–1012. doi: 10.1128/iai.42.3.1006-1012.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Gibbons R. J., Etherden I., Moreno E. C. Contribution of stereochemical interactions in the adhesion of Streptococcus sanguis C5 to experimental pellicles. J Dent Res. 1985 Feb;64(2):96–101. doi: 10.1177/00220345850640021801. [DOI] [PubMed] [Google Scholar]
  18. Hawkes R. Identification of concanavalin A-binding proteins after sodium dodecyl sulfate--gel electrophoresis and protein blotting. Anal Biochem. 1982 Jun;123(1):143–146. doi: 10.1016/0003-2697(82)90634-0. [DOI] [PubMed] [Google Scholar]
  19. Hogg S. D., Handley P. S., Embery G. Surface fibrils may be responsible for the salivary glycoprotein-mediated aggregation of the oral bacterium Streptococcus sanguis. Arch Oral Biol. 1981;26(11):945–949. doi: 10.1016/0003-9969(81)90156-4. [DOI] [PubMed] [Google Scholar]
  20. 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]
  21. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  22. Levine M. J., Herzberg M. C., Levine M. S., Ellison S. A., Stinson M. W., Li H. C., van Dyke T. Specificity of salivary-bacterial interactions: role of terminal sialic acid residues in the interaction of salivary glycoproteins with Streptococcus sanguis and Streptococcus mutans. Infect Immun. 1978 Jan;19(1):107–115. doi: 10.1128/iai.19.1.107-115.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Lotan R., Sharon N., Mirelman D. Interaction of wheat-germ agglutinin with bacterial cells and cell-wall polymers. Eur J Biochem. 1975 Jun 16;55(1):257–262. doi: 10.1111/j.1432-1033.1975.tb02158.x. [DOI] [PubMed] [Google Scholar]
  24. Maryanski J. H., Wittenberger C. L. Mannitol transport in Streptococcus mutans. J Bacteriol. 1975 Dec;124(3):1475–1481. doi: 10.1128/jb.124.3.1475-1481.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. McBride B. C., Gisslow M. T. Role of sialic acid in saliva-induced aggregation of Streptococcus sanguis. Infect Immun. 1977 Oct;18(1):35–40. doi: 10.1128/iai.18.1.35-40.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. McIntire F. C., Crosby L. K., Vatter A. E. Inhibitors of coaggregation between Actinomyces viscosus T14V and Streptococcus sanguis 34: beta-galactosides, related sugars, and anionic amphipathic compounds. Infect Immun. 1982 Apr;36(1):371–378. doi: 10.1128/iai.36.1.371-378.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. McIntire F. C., Vatter A. E., Baros J., Arnold J. Mechanism of coaggregation between Actinomyces viscosus T14V and Streptococcus sanguis 34. Infect Immun. 1978 Sep;21(3):978–988. doi: 10.1128/iai.21.3.978-988.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Misevic G. N., Burger M. M. Reconstitution of high cell binding affinity of a marine sponge aggregation factor by cross-linking of small low affinity fragments into a large polyvalent polymer. J Biol Chem. 1986 Feb 25;261(6):2853–2859. [PubMed] [Google Scholar]
  29. Morris E. J., Ganeshkumar N., Song M., McBride B. C. Identification and preliminary characterization of a Streptococcus sanguis fibrillar glycoprotein. J Bacteriol. 1987 Jan;169(1):164–171. doi: 10.1128/jb.169.1.164-171.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Morris E. J., McBride B. C. Adherence of Streptococcus sanguis to saliva-coated hydroxyapatite: evidence for two binding sites. Infect Immun. 1984 Feb;43(2):656–663. doi: 10.1128/iai.43.2.656-663.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Murray P. A., Levine M. J., Reddy M. S., Tabak L. A., Bergey E. J. Preparation of a sialic acid-binding protein from Streptococcus mitis KS32AR. Infect Immun. 1986 Aug;53(2):359–365. doi: 10.1128/iai.53.2.359-365.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Murray P. A., Levine M. J., Tabak L. A., Reddy M. S. Specificity of salivary-bacterial interactions: II. Evidence for a lectin on Streptococcus sanguis with specificity for a NeuAc alpha 2, 3Ga1 beta 1, 3Ga1NAc sequence. Biochem Biophys Res Commun. 1982 May 31;106(2):390–396. doi: 10.1016/0006-291x(82)91122-6. [DOI] [PubMed] [Google Scholar]
  33. Osterland C. K., Miller E. J., Karakawa W. W., Krause R. M. Characteristics of streptococcal group-specific antibody isolated from hyperimmune rabbits. J Exp Med. 1966 Apr 1;123(4):599–614. doi: 10.1084/jem.123.4.599. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. PORTER R. R. The hydrolysis of rabbit y-globulin and antibodies with crystalline papain. Biochem J. 1959 Sep;73:119–126. doi: 10.1042/bj0730119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Rosan B., Malamud D., Appelbaum B., Golub E. Characteristic differences between saliva-dependent aggregation and adhesion of streptococci. Infect Immun. 1982 Jan;35(1):86–90. doi: 10.1128/iai.35.1.86-90.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Ruhl S., Sandberg A. L., Cole M. F., Cisar J. O. Recognition of immunoglobulin A1 by oral actinomyces and streptococcal lectins. Infect Immun. 1996 Dec;64(12):5421–5424. doi: 10.1128/iai.64.12.5421-5424.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Schneewind O., Fowler A., Faull K. F. Structure of the cell wall anchor of surface proteins in Staphylococcus aureus. Science. 1995 Apr 7;268(5207):103–106. doi: 10.1126/science.7701329. [DOI] [PubMed] [Google Scholar]
  38. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350–4354. doi: 10.1073/pnas.76.9.4350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Weeke B. A manual of quantitative immunoelectrophoresis. Methods and applications. 1. General remarks on principles, equipment, reagents and procedures. Scand J Immunol Suppl. 1973;1:15–35. doi: 10.1111/j.1365-3083.1973.tb03776.x. [DOI] [PubMed] [Google Scholar]

Articles from Infection and Immunity are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES