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. 1997 May;4(3):291–296. doi: 10.1128/cdli.4.3.291-296.1997

Antigenic characterization of fimbria preparations from Streptococcus mutans isolates from caries-free and caries-susceptible subjects.

M Perrone 1, L E Gfell 1, M Fontana 1, R L Gregory 1
PMCID: PMC170521  PMID: 9144366

Abstract

The adhesion of pathogenic bacteria to the host surface is an essential step in the development of numerous infections, including dental caries. Attachment of Streptococcus mutans, the main etiological agent of human dental caries, to the tooth surface may be mediated by glucan synthesized by glucosyltransferase (GTF) and by cell surface proteins, such as P1, which bind to salivary receptors. Fimbriae on the surfaces of many microorganisms are known to function in bacterial adhesion. Previous studies in this laboratory have initially characterized the fibrillar surface of S. mutans. The purpose of this investigation was the comparison of the antigenic properties of fimbria preparations of S. mutans isolates from five caries-resistant (CR) and six caries-susceptible (CS) subjects. Sodium dodecyl sulfate-polyacrylamide gel electrophoresis analysis of S. mutans fimbrial preparations revealed five major protein bands at 200, 175, 157, 86, and 66 kDa in preparations from CR and CS subjects. Immunoblot analysis indicated the presence of the same major bands recognized by anti-S. mutans fimbria antisera. Furthermore, the 175- and 157-kDa bands were recognized by antibodies to P1 and GTF, respectively. Immunoblot analysis with antisera to the fimbria preparation, to P1, or to GTF indicated that the levels of fimbria-reactive components and P1 and GTF antigens were higher in S. mutans fimbria preparations from CS subjects than in those from CR individuals. For example, four of six fimbria preparations from CS patients had demonstrable P1, and all had GTF. In contrast, only two of five CR fimbrial preparations exhibited P1 and GTF. Enzyme-linked immunosorbent assay demonstrated similar results for levels of GTF antigen in the fimbrial preparations from CR and CS subjects. The results suggest that differences between the compositions of S. mutans fimbriae in CR and CS individuals may play an important role in the virulence of this microorganism in dental caries.

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Selected References

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  1. Ackermans F., Klein J. P., Ogier J., Bazin H., Cormont F., Frank R. M. Purification and characterization of a saliva-interacting cell-wall protein from Streptococcus mutans serotype f by using monoclonal-antibody immunoaffinity chromatography. Biochem J. 1985 May 15;228(1):211–217. doi: 10.1042/bj2280211. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Ayakawa G. Y., Boushell L. W., Crowley P. J., Erdos G. W., McArthur W. P., Bleiweis A. S. Isolation and characterization of monoclonal antibodies specific for antigen P1, a major surface protein of mutans streptococci. Infect Immun. 1987 Nov;55(11):2759–2767. doi: 10.1128/iai.55.11.2759-2767.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bammann L. L., Gibbons R. J. Immunoglobulin A antibodies reactive with Streptococcus mutans in saliva of adults, children, and predentate infants. J Clin Microbiol. 1979 Oct;10(4):538–543. doi: 10.1128/jcm.10.4.538-543.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bleiweis A. S., Oyston P. C., Brady L. J. Molecular, immunological and functional characterization of the major surface adhesin of Streptococcus mutans. Adv Exp Med Biol. 1992;327:229–241. doi: 10.1007/978-1-4615-3410-5_25. [DOI] [PubMed] [Google Scholar]
  5. Brady L. J., Piacentini D. A., Crowley P. J., Oyston P. C., Bleiweis A. S. Differentiation of salivary agglutinin-mediated adherence and aggregation of mutans streptococci by use of monoclonal antibodies against the major surface adhesin P1. Infect Immun. 1992 Mar;60(3):1008–1017. doi: 10.1128/iai.60.3.1008-1017.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Challacombe S. J., Bergmeier L. A., Czerkinsky C., Rees A. S. Natural antibodies in man to Streptococcus mutans: specificity and quantification. Immunology. 1984 May;52(1):143–150. [PMC free article] [PubMed] [Google Scholar]
  7. Crawford P. C., Clark W. B. Fimbria-specific antibodies in serum and saliva of mice immunized with Actinomyces viscosus T14V fimbriae. Infect Immun. 1986 Nov;54(2):507–515. doi: 10.1128/iai.54.2.507-515.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. 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]
  9. Ellen R. P., Walker D. L., Chan K. H. Association of long surface appendages with adherence-related functions of the gram-positive species Actinomyces naeslundii. J Bacteriol. 1978 Jun;134(3):1171–1175. doi: 10.1128/jb.134.3.1171-1175.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Evans R. T., Klausen B., Sojar H. T., Bedi G. S., Sfintescu C., Ramamurthy N. S., Golub L. M., Genco R. J. Immunization with Porphyromonas (Bacteroides) gingivalis fimbriae protects against periodontal destruction. Infect Immun. 1992 Jul;60(7):2926–2935. doi: 10.1128/iai.60.7.2926-2935.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Fontana M., Gfell L. E., Gregory R. L. Characterization of preparations enriched for Streptococcus mutans fimbriae: salivary immunoglobulin A antibodies in caries-free and caries-active subjects. Clin Diagn Lab Immunol. 1995 Nov;2(6):719–725. doi: 10.1128/cdli.2.6.719-725.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Forester H., Hunter N., Knox K. W. Characteristics of a high molecular weight extracellular protein of Streptococcus mutans. J Gen Microbiol. 1983 Sep;129(9):2779–2788. doi: 10.1099/00221287-129-9-2779. [DOI] [PubMed] [Google Scholar]
  13. Gibbons R. J., Fitzgerald R. J. Dextran-induced agglutination of Streptococcus mutans, and its potential role in the formation of microbial dental plaques. J Bacteriol. 1969 May;98(2):341–346. doi: 10.1128/jb.98.2.341-346.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Girardeau J. P., Der Vartanian M., Ollier J. L., Contrepois M. CS31A, a new K88-related fimbrial antigen on bovine enterotoxigenic and septicemic Escherichia coli strains. Infect Immun. 1988 Aug;56(8):2180–2188. doi: 10.1128/iai.56.8.2180-2188.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gregory R. L., Filler S. J. Protective secretory immunoglobulin A antibodies in humans following oral immunization with Streptococcus mutans. Infect Immun. 1987 Oct;55(10):2409–2415. doi: 10.1128/iai.55.10.2409-2415.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Gregory R. L., Kindle J. C., Hobbs L. C., Filler S. J., Malmstrom H. S. Function of anti-Streptococcus mutans antibodies: inhibition of virulence factors and enzyme neutralization. Oral Microbiol Immunol. 1990 Aug;5(4):181–188. doi: 10.1111/j.1399-302x.1990.tb00643.x. [DOI] [PubMed] [Google Scholar]
  17. Gregory R. L., Michalek S. M., Filler S. J., Mestecky J., McGhee J. R. Prevention of Streptococcus mutans colonization by salivary IgA antibodies. J Clin Immunol. 1985 Jan;5(1):55–62. doi: 10.1007/BF00915169. [DOI] [PubMed] [Google Scholar]
  18. Hajishengallis G., Koga T., Russell M. W. Affinity and specificity of the interactions between Streptococcus mutans antigen I/II and salivary components. J Dent Res. 1994 Sep;73(9):1493–1502. doi: 10.1177/00220345940730090301. [DOI] [PubMed] [Google Scholar]
  19. Hamada S., Slade H. D. Biology, immunology, and cariogenicity of Streptococcus mutans. Microbiol Rev. 1980 Jun;44(2):331–384. doi: 10.1128/mr.44.2.331-384.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Iwaki M., Okahashi N., Takahashi I., Kanamoto T., Sugita-Konishi Y., Aibara K., Koga T. Oral immunization with recombinant Streptococcus lactis carrying the Streptococcus mutans surface protein antigen gene. Infect Immun. 1990 Sep;58(9):2929–2934. doi: 10.1128/iai.58.9.2929-2934.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Jones C. H., Jacob-Dubuisson F., Dodson K., Kuehn M., Slonim L., Striker R., Hultgren S. J. Adhesin presentation in bacteria requires molecular chaperones and ushers. Infect Immun. 1992 Nov;60(11):4445–4451. doi: 10.1128/iai.60.11.4445-4451.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Kawata Y., Hanazawa S., Amano S., Murakami Y., Matsumoto T., Nishida K., Kitano S. Porphyromonas gingivalis fimbriae stimulate bone resorption in vitro. Infect Immun. 1994 Jul;62(7):3012–3016. doi: 10.1128/iai.62.7.3012-3016.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Klemm P. Fimbrial adhesions of Escherichia coli. Rev Infect Dis. 1985 May-Jun;7(3):321–340. doi: 10.1093/clinids/7.3.321. [DOI] [PubMed] [Google Scholar]
  24. Koga T., Asakawa H., Okahashi N., Hamada S. Sucrose-dependent cell adherence and cariogenicity of serotype c Streptococcus mutans. J Gen Microbiol. 1986 Oct;132(10):2873–2883. doi: 10.1099/00221287-132-10-2873. [DOI] [PubMed] [Google Scholar]
  25. Koga T., Asakawa H., Okahashi N., Takahashi I. Effect of subculturing on expression of a cell-surface protein antigen by Streptococcus mutans. J Gen Microbiol. 1989 Dec;135(12):3199–3207. doi: 10.1099/00221287-135-12-3199. [DOI] [PubMed] [Google Scholar]
  26. Krogfelt K. A. Bacterial adhesion: genetics, biogenesis, and role in pathogenesis of fimbrial adhesins of Escherichia coli. Rev Infect Dis. 1991 Jul-Aug;13(4):721–735. doi: 10.1093/clinids/13.4.721. [DOI] [PubMed] [Google Scholar]
  27. 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]
  28. Lee S. F. Identification and characterization of a surface protein-releasing activity in Streptococcus mutans and other pathogenic streptococci. Infect Immun. 1992 Oct;60(10):4032–4039. doi: 10.1128/iai.60.10.4032-4039.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Lee S. F., Progulske-Fox A., Bleiweis A. S. Molecular cloning and expression of a Streptococcus mutans major surface protein antigen, P1 (I/II), in Escherichia coli. Infect Immun. 1988 Aug;56(8):2114–2119. doi: 10.1128/iai.56.8.2114-2119.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Lehner T., Caldwell J., Smith R. Local passive immunization by monoclonal antibodies against streptococcal antigen I/II in the prevention of dental caries. Infect Immun. 1985 Dec;50(3):796–799. doi: 10.1128/iai.50.3.796-799.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Lehner T., Russell M. W., Caldwell J., Smith R. Immunization with purified protein antigens from Streptococcus mutans against dental caries in rhesus monkeys. Infect Immun. 1981 Nov;34(2):407–415. doi: 10.1128/iai.34.2.407-415.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Loesche W. J., Straffon L. H. Longitudinal investigation of the role of Streptococcus mutans in human fissure decay. Infect Immun. 1979 Nov;26(2):498–507. doi: 10.1128/iai.26.2.498-507.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Lowe M. A., Holt S. C., Eisenstein B. I. Immunoelectron microscopic analysis of elongation of type 1 fimbriae in Escherichia coli. J Bacteriol. 1987 Jan;169(1):157–163. doi: 10.1128/jb.169.1.157-163.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Ma J. K., Hunjan M., Smith R., Kelly C., Lehner T. An investigation into the mechanism of protection by local passive immunization with monoclonal antibodies against Streptococcus mutans. Infect Immun. 1990 Oct;58(10):3407–3414. doi: 10.1128/iai.58.10.3407-3414.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Ma J. K., Smith R., Lehner T. Use of monoclonal antibodies in local passive immunization to prevent colonization of human teeth by Streptococcus mutans. Infect Immun. 1987 May;55(5):1274–1278. doi: 10.1128/iai.55.5.1274-1278.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Madison B., Ofek I., Clegg S., Abraham S. N. Type 1 fimbrial shafts of Escherichia coli and Klebsiella pneumoniae influence sugar-binding specificities of their FimH adhesins. Infect Immun. 1994 Mar;62(3):843–848. doi: 10.1128/iai.62.3.843-848.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. McGhee J. R., Michalek S. M. Immunobiology of dental caries: microbial aspects and local immunity. Annu Rev Microbiol. 1981;35:595–638. doi: 10.1146/annurev.mi.35.100181.003115. [DOI] [PubMed] [Google Scholar]
  38. Moro I., Russell M. W. Ultrastructural localization of protein antigens I/II and III in Streptococcus mutans. Infect Immun. 1983 Jul;41(1):410–413. doi: 10.1128/iai.41.1.410-413.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. 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]
  40. Okahashi N., Sasakawa C., Yoshikawa M., Hamada S., Koga T. Cloning of a surface protein antigen gene from serotype c Streptococcus mutans. Mol Microbiol. 1989 Feb;3(2):221–228. doi: 10.1111/j.1365-2958.1989.tb01811.x. [DOI] [PubMed] [Google Scholar]
  41. Okahashi N., Sasakawa C., Yoshikawa M., Hamada S., Koga T. Cloning of a surface protein antigen gene from serotype c Streptococcus mutans. Mol Microbiol. 1989 Feb;3(2):221–228. doi: 10.1111/j.1365-2958.1989.tb01811.x. [DOI] [PubMed] [Google Scholar]
  42. Oligino L., Fives-Taylor P. Overexpression and purification of a fimbria-associated adhesin of Streptococcus parasanguis. Infect Immun. 1993 Mar;61(3):1016–1022. doi: 10.1128/iai.61.3.1016-1022.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Qureshi J. V., Goldner M., Riche W. H., Hargreaves J. A. Streptococcus mutans serotypes in young schoolchildren. Caries Res. 1977;11(3):141–152. doi: 10.1159/000260260. [DOI] [PubMed] [Google Scholar]
  44. 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]
  45. Russell R. R. Wall-associated protein antigens of Streptococcus mutans. J Gen Microbiol. 1979 Sep;114(1):109–115. doi: 10.1099/00221287-114-1-109. [DOI] [PubMed] [Google Scholar]
  46. Schilling K. M., Bowen W. H. Glucans synthesized in situ in experimental salivary pellicle function as specific binding sites for Streptococcus mutans. Infect Immun. 1992 Jan;60(1):284–295. doi: 10.1128/iai.60.1.284-295.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Smith D. J., Akita H., King W. F., Taubman M. A. Purification and antigenicity of a novel glucan-binding protein of Streptococcus mutans. Infect Immun. 1994 Jun;62(6):2545–2552. doi: 10.1128/iai.62.6.2545-2552.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Smith R., Lehner T., Beverley P. C. Characterization of monoclonal antibodies to Streptococcus mutans antigenic determinants I/II, I, II, and III and their serotype specificities. Infect Immun. 1984 Oct;46(1):168–175. doi: 10.1128/iai.46.1.168-175.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Smith R., Lehner T. Characterisation of monoclonal antibodies to common protein epitopes on the cell surface of Streptococcus mutans and Streptococcus sobrinus. Oral Microbiol Immunol. 1989 Sep;4(3):153–158. doi: 10.1111/j.1399-302x.1989.tb00243.x. [DOI] [PubMed] [Google Scholar]
  50. Steven A. C., Bisher M. E., Trus B. L., Thomas D., Zhang J. M., Cowell J. L. Helical structure of Bordetella pertussis fimbriae. J Bacteriol. 1986 Sep;167(3):968–974. doi: 10.1128/jb.167.3.968-974.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. 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]
  52. Uhlin B. E., Båga M., Göransson M., Lindberg F. P., Lund B., Norgren M., Normark S. Genes determining adhesin formation in uropathogenic Escherichia coli. Curr Top Microbiol Immunol. 1985;118:163–178. doi: 10.1007/978-3-642-70586-1_9. [DOI] [PubMed] [Google Scholar]
  53. van Houte J., Burgess R. C., Onose H. Oral implantation of human strains of Streptococcus mutans in rats fed sucrose or glucose diets. Arch Oral Biol. 1976;21(9):561–564. doi: 10.1016/0003-9969(76)90023-6. [DOI] [PubMed] [Google Scholar]

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