1887

Abstract

produces two -amylase-binding proteins, AbpA and AbpB, that have been extensively studied . Little is known, however, about their significance in oral colonization and cariogenicity (virulence). To clarify these issues, weanling specific pathogen-free Osborne-Mendel rats, TAN : SPFOM(OM)BR, were inoculated either with wild-type strains FAS4-S or Challis-S or with strains having isogenic mutations of , , or both, to compare their colonization abilities and persistence on the teeth. Experiments were done with rats fed a sucrose-rich diet containing low amounts of starch or containing only starch. The mutants and wild-types were quantified and carious lesions were scored. In 11 experiments, was a prolific colonizer of the teeth when rats were fed the sucrose (with low starch)-supplemented diet, often dominating the flora. Sucrose-fed rats had several-fold higher recoveries of inoculants than those eating the sucrose-free, starch-supplemented diet, regardless of inoculant type. The strain defective in AbpB could not colonize teeth of starch-only-eating rats, but could colonize rats if sucrose was added to the diet. Strains defective in AbpA surprisingly colonized better than their wild-types. A double mutant deficient in both AbpA and AbpB (/) colonized like its wild-type. Wild-types FAS4-S and Challis-S had no more than marginal cariogenicity. Notably, in the absence of AbpA, cariogenicity was slightly augmented. Both the rescue of colonization by the AbpB mutant and the augmentation of colonization by AbpA mutant in the presence of dietary sucrose suggested additional amylase-binding protein interactions relevant to colonization. Glucosyltransferase activity was greater in mutants defective in and modestly increased in the mutant. It was concluded that AbpB is required for colonization of teeth of starch-eating rats and its deletion is partially masked if rats eat a sucrose-starch diet. AbpA appears to inhibit colonization of the plaque biofilm . This unexpected effect may be associated with interaction of AbpA with glucosyltransferase or with other colonization factors of these cells. These data illustrate that the complex nature of the oral environment may not be adequately modelled by systems.

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2003-09-01
2019-10-17
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References

  1. Bolken, T. C., Franke, C. A., Jones, K. F., Bell, R. H., Swanson, R. M., King, D. S., Fischetti, V. A. & Hruby, D. E. ( 2002; ). Analysis of factors affecting surface expression and immunogenicity of recombinant proteins expressed by gram-positive commensal vectors. Infect Immun 70, 2487–2491.[CrossRef]
    [Google Scholar]
  2. Brown, A. E., Rogers, J. D., Haase, E. M., Zelasko, P. M. & Scannapieco, F. A. ( 1999; ). Prevalence of the amylase binding protein A gene (abpA) in oral streptococci. J Clin Microbiol 37, 4081–4085.
    [Google Scholar]
  3. Chauncey, H. H., Henriques, B. L. & Tanzer, J. M. ( 1963; ). Comparative enzyme activity of saliva from the sheep, hog, dog, rabbit and human. Arch Oral Biol 8, 615–627.[CrossRef]
    [Google Scholar]
  4. Demuth, D. R., Duan, Y., Brooks, W., Holmes, A. R., McNab, R. & Jenkinson, H. F. ( 1996; ). 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 20, 403–413.[CrossRef]
    [Google Scholar]
  5. Douglas, C. W. I. ( 1990; ). Characterization of the α-amylase receptor of Streptococcus gordonii NCTC 7868. J Dent Res 69, 1746–1752.[CrossRef]
    [Google Scholar]
  6. Gwynn, J. P. & Douglas, C. W. I. ( 1994; ). Comparison of amylase-binding proteins in oral streptococci. FEMS Microbiol Lett 124, 373–380.[CrossRef]
    [Google Scholar]
  7. Li, L., Tanzer, J. M. & Scannapieco, F. A. ( 2002; ). Identification and analysis of the amylase-binding protein B (AbpB) and gene (abpB) from Streptococcus gordonii. FEMS Microbiol Lett 212, 151–157.[CrossRef]
    [Google Scholar]
  8. McNab, R., Holmes, A. R., Clarke, J. M., Tannock, G. W. & Jenkinson, H. F. ( 1996; ). Cell surface polypeptide CshA mediates binding of Streptococcus gordonii to other oral bacteria and to immobilized fibronectin. Infect Immun 64, 4204–4210.
    [Google Scholar]
  9. Oggioni, M. R., Medaglini, D., Romano, L. & 8 other authors ( 1999; ). Antigenicity and immunogenicity of the V3 domain of HIV type 1 glycoprotein 120 expressed on the surface of Streptococcus gordonii. AIDS Res Hum Retroviruses 15, 451–459.[CrossRef]
    [Google Scholar]
  10. Pozzi, G., Contorni, M., Oggioni, M. R., Manganelli, R., Tommasino, M., Cavalieri, F. & Fischetti, V. A. ( 1992; ). Delivery and expression of a heterologous antigen on the surface of streptococci. Infect Immun 60, 1902–1907.
    [Google Scholar]
  11. Pozzi, G., Oggioni, M. R., Manganelli, R., Medaglini, D., Fischetti, V. A., Fenoglio, D., Valle, M. T., Kunkl, A. & Manca, F. ( 1994; ). Human T-helper cell recognition of an immunodominant epitope of HIV-1 gp120 expressed on the surface of Streptococcus gordonii. Vaccine 12, 1071–1077.[CrossRef]
    [Google Scholar]
  12. Rinehimer, L. A. & Tanzer, J. M. ( 1980; ). Statistical relationship of morsal to bucco-lingual, approximal and sulcal caries in rats. J Dent Res 59, 745–748.[CrossRef]
    [Google Scholar]
  13. Rogers, J. D., Haase, E. M., Brown, A. E., Douglas, C. W. I., Gwynn, J. P. & Scannapieco, F. A. ( 1998; ). Identification and analysis of a gene (abpA) encoding a major amylase-binding protein in Streptococcus gordonii. Microbiology 144, 1223–1233.[CrossRef]
    [Google Scholar]
  14. Rogers, J. D., Palmer, R. J., Jr, Kolenbrander, P. E. & Scannapieco, F. A. ( 2001; ). Role of Streptococcus gordonii amylase-binding protein A in adhesion to hydroxyapatite, starch metabolism, and biofilm formation. Infect Immun 69, 7046–7056.[CrossRef]
    [Google Scholar]
  15. Scannapieco, F. A., Bhandary, K., Ramasubbu, N. & Levine, M. J. ( 1990; ). Structural relationship between the enzymatic and streptococcal binding sites of human salivary α-amylase. Biochem Biophys Res Commun 173, 1109–1115.[CrossRef]
    [Google Scholar]
  16. Scannapieco, F. A., Haraszthy, G. G., Cho, M. I. & Levine, M. J. ( 1992; ). Characterization of an amylase-binding component from Streptococcus gordonii G9B. Infect Immun 60, 4726–4733.
    [Google Scholar]
  17. Scannapieco, F. A., Torres, G. & Levine, M. J. ( 1993; ). Salivary alpha-amylase: role in dental plaque and caries formation. Crit Rev Oral Biol Med 4, 301–307.
    [Google Scholar]
  18. Scannapieco, F. A., Solomon, L. & Wadenya, R. O. ( 1994; ). Emergence in human dental plaque and host distribution of amylase-binding streptococci. J Dental Res 73, 1627–1635.
    [Google Scholar]
  19. Scannapieco, F. A., Torres, G. I. & Levine, M. J. ( 1995; ). Salivary amylase promotes adhesion of oral streptococci to hydroxyapatite. J Dent Res 74, 1360–1366.[CrossRef]
    [Google Scholar]
  20. Sharma, A., Honma, K., Sojar, H. T., Hruby, D. E., Kuramitsu, H. K. & Genco, R. J. ( 1999; ). Expression of saliva-binding epitopes of the Porphyromonas gingivalis FimA protein on the surface of Streptococcus gordonii. Biochem Biophys Res Commun 258, 222–226.[CrossRef]
    [Google Scholar]
  21. Snedecor, G. & Cochran, W. ( 1967; ). Statistical Methods, 5th edn, p. 251. Ames, IA: Iowa State University Press.
  22. Sulavik, M. C., Tardif, G. & Clewell, D. B. ( 1992; ). Identification of a gene, rgg, which regulates expression of glucosyltransferase and influences the Spp phenotype of Streptococcus gordonii Challis. J Bacteriol 174, 3577–3586.
    [Google Scholar]
  23. Takahashi, Y., Konishi, K., Cisar, J. O. & Yoshikawa, M. ( 2002; ). Identification and characterization of hsa, the gene encoding the sialic acid-binding adhesin of Streptococcus gordonii DL1. Infect Immun 70, 1209–1218.[CrossRef]
    [Google Scholar]
  24. Tanzer, J. M. ( 1979; ). Essential dependence of smooth surface caries on, and augmentation of fissure caries by, sucrose and Streptococcus mutans infection. Infect Immun 25, 526–531.
    [Google Scholar]
  25. Tanzer, J. M., Freedman, M. L., Fitzgerald, R. J. & Larson, R. H. ( 1974; ). Altered virulence of mutants of Streptococcus mutans defective in polysaccharide synthesis. Infect Immun 10, 197–203.
    [Google Scholar]
  26. Tanzer, J. M., Kurasz, A. B. & Clive, J. ( 1985a; ). Competitive displacement of mutans streptococci and inhibition of tooth decay by Streptococcus salivarius TOVE-R. Infect Immun 48, 44–50.
    [Google Scholar]
  27. Tanzer, J. M., Kurasz, A. B. & Clive, J. ( 1985b; ). Inhibition of ecological emergence of mutans streptococci naturally transmitted between rats and consequent caries inhibition by Streptococcus salivarius TOVE-R infection. Infect Immun 49, 76–83.
    [Google Scholar]
  28. Tanzer, J. M., Baranowski, L. K., Rogers, J. D., Haase, E. M. & Scannapieco, F. A. ( 2001a; ). Oral colonization and cariogenicity of Streptococcus gordonii in specific pathogen-free TAN : SPFOM(OM)BR rats consuming starch or sucrose diets. Arch Oral Biol 46, 323–333.[CrossRef]
    [Google Scholar]
  29. Tanzer, J. M., Livingston, J. & Thompson, A. ( 2001b; ). The microbiology of primary dental caries. In The Diagnosis and Management of Dental Caries Throughout Life. National Institute of Dental and Craniofacial Research and Office of Medical Applications of Research, NIH: http://www.nidcr.nih.gov/news/consensus.asp.
  30. Tanzer, J. M., Grant, L., Thompson, A., Li, L., Rogers, J. D. & Scannapieco, F. A. ( 2002a; ). Differential effects of amylase-binding protein A (AbpA) and B (AbpB) in colonization of teeth by S. gordonii. J Dent Res 81, Abstract 0090, p. A40.
    [Google Scholar]
  31. Tanzer, J. M., Grant, L., Thompson, A. L., Rogers, J. D. & Scannapieco, F. ( 2002b; ). Amylase-binding protein A knockout of S. gordonii colonizes teeth better than its wild type. Caries Res 36, Abstract 60, p. 193.
    [Google Scholar]
  32. Terleckyj, B., Willet, N. P. & Schockman, G. D. ( 1975; ). Growth of several cariogenic strains of oral streptococci in a chemically defined medium. Infect Immun 11, 649–655.
    [Google Scholar]
  33. Tseng, C. C., Scannapieco, F. A. & Levine, M. J. ( 1992; ). Use of a replica plate assay for the rapid assessment of salivary protein–bacteria interactions. Oral Microbiol Immunol 7, 53–56.[CrossRef]
    [Google Scholar]
  34. Vickerman, M. M. & Jones, G. W. ( 1995; ). Sucrose-dependent accumulation of oral streptococci and their adhesion-defective mutants on saliva-coated hydroxyapatite. Oral Microbiol Immunol 10, 175–182.[CrossRef]
    [Google Scholar]
  35. Vickerman, M. M. & Minick, P. E. ( 2002; ). Genetic analysis of the rgg-gtfG junctional region and its role in Streptococcus gordonii glucosyltransferase activity. Infect Immun 70, 1703–1714.[CrossRef]
    [Google Scholar]
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