1887

Microbiology Society logo

Volume 146, Issue 1

Adhesion of to oral streptococci is promoted by selective adsorption of salivary proteins to the streptococcal cell surface Free

Abstract

Adhesion of to saliva-coated surfaces is an important early step in the colonization of the oral cavity. cells also adhere to several species of oral streptococci including , and in what are believed to be multi-modal interactions. It is now demonstrated that incubation of streptococcal cells of these species with human parotid saliva further promotes the adhesion of cells by up to 23-fold. Various species of streptococci were shown to adsorb different protein components of parotid saliva to their cell surfaces. The basic proline-rich proteins (bPRPs), to which cells bind on nitrocellulose blot overlay, were strongly adsorbed to the surface of cells but not to cells. Parotid saliva that was pre-adsorbed with cells and then applied to hydroxylapatite beads was <50% effective at supporting adhesion of compared with control (non-adsorbed) saliva, demonstrating that bPRPs are major pellicle receptors. cells did not adsorb bPRPs from fluid-phase parotid saliva. Following size-exclusion chromatography of parotid saliva samples, pooled fractions enriched in bPRPs promoted maximal adhesion of to cells. The results demonstrate that cells recognize only surface-bound forms of bPRPs and suggest that these proteins adsorbed to enamel or to streptococcal surfaces promote adhesion and oral colonization.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
Keyword(s): aPRPs, acidic proline-rich proteins , bPRPs, basic proline-rich proteins , Candida albicans , co-adhesion , HA, hydroxylapatite , proline-rich proteins , PRPs, proline-rich proteins and streptococci
© Microbiology Society
Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-146-1-41
2000-01-01
2024-04-24
Loading full text...

Full text loading...

/deliver/fulltext/micro/146/1/1460041a.html?itemId=/content/journal/micro/10.1099/00221287-146-1-41&mimeType=html&fmt=ahah

References

  1. Arendorf T. M., Walker D. M. 1979; Oral candidal populations in health and disease. Br Dent J 147:267–272 [CrossRef]
     [Google Scholar]
  2. Arendorf T. M., Walker D. M. 1980; The prevalence and intra-oral distribution of Candida albicans in man. Arch Oral Biol 25:1–10 [CrossRef]
     [Google Scholar]
  3. Branting C., Sund M. L., Linder L. E. 1989; The influence of Streptococcus mutans on adhesion of Candida albicans to acrylic surfaces in vitro. Arch Oral Biol 34:347–353 [CrossRef]
     [Google Scholar]
  4. Cannon R. D., Chaffin W. L. 1999; Oral colonization by Candida albicans. Crit Rev Oral Biol Med 10:359–383 [CrossRef]
     [Google Scholar]
  5. Cannon R. D., Holmes A. R., Mason A. B., Monk B. C. 1995a; Oral Candida: clearance, colonization, or candidiasis?. J Dent Res 74:1152–1161 [CrossRef]
     [Google Scholar]
  6. Cannon R. D., Nand A. K., Jenkinson H. F. 1995b; Adherence of Candida albicans to human salivary components adsorbed to hydroxylapatite. Microbiology 141:213–219 [CrossRef]
     [Google Scholar]
  7. Douglas C. W., Russell R. R. 1984; The adsorption of human salivary components to strains of the bacterium Streptococcus mutans. Arch Oral Biol 29:751–757 [CrossRef]
     [Google Scholar]
  8. Douglas C. W. I., Pease A. A., Whiley R. A. 1990; Amylase-binding as a discriminator among oral streptococci. FEMS Microbiol Lett 66:193–198 [CrossRef]
     [Google Scholar]
  9. Edgerton M., Scannapieco F. A., Reddy M. S., Levine M. J. 1993; Human submandibular-sublingual saliva promotes adhesion of Candida albicans to polymethylmethacrylate. Infect Immun 61:2644–2652
     [Google Scholar]
  10. Gibbons R. J., Hay D. I. 1988; Human salivary acidic proline-rich proteins and statherin promote the attachment of Actinomyces naeslundii LY7 to apatitic surfaces. Infect Immun 56:439–445
     [Google Scholar]
  11. Gibbons R. J., Hay D. I., Childs W. C. 3rd, Davis G. 1990; Role of cryptic receptors (cryptitopes) in bacterial adhesion to oral surfaces. Arch Oral Biol 35:107S–114S [CrossRef]
     [Google Scholar]
  12. Gibbons R. J., Hay D. I., Schlesinger D. H. 1991; Delineation of a segment of adsorbed salivary acidic proline-rich proteins which promotes adhesion of Streptococcus gordonii to apatitic surfaces. Infect Immun 59:2948–2954
     [Google Scholar]
  13. Grimaudo N. J., Nesbitt W. E., Clark W. B. 1996; Coaggregation of Candida albicans with oral Actinomyces species. Oral Microbiol Immunol 11:59–61 [CrossRef]
     [Google Scholar]
  14. Hodson J. J., Craig G. T. 1972; The incidence of Candida albicans in the plaques of teeth of children. Dent Pract Dent Rec 22:296–301
     [Google Scholar]
  15. Holmes A. R., Shepherd M. G. 1988; Nutritional factors determine germ tube formation in Candida albicans. J Med Vet Mycol 26:127–131 [CrossRef]
     [Google Scholar]
  16. Holmes A. R., Cannon R. D., Jenkinson H. F. 1995a; Interactions of Candida albicans with bacteria and salivary molecules in oral biofilms. J Ind Microbiol 15:208–213 [CrossRef]
     [Google Scholar]
  17. Holmes A. R., Gopal P. K., Jenkinson H. F. 1995b; Adherence of Candida albicans to a cell surface polysaccharide receptor on Streptococcus gordonii. Infect Immun 63:1827–1834
     [Google Scholar]
  18. Holmes A. R., McNab R., Jenkinson H. F. 1996; Candida albicans binding to the oral bacterium Streptococcus gordonii involves multiple adhesin-receptor interactions. Infect Immun 64:4680–4685
     [Google Scholar]
  19. Iontcheva I., Oppenheim F. G., Troxler R. F. 1997; Human salivary mucin MG1 selectively forms heterotypic complexes with amylase, proline-rich proteins, statherin, and histatins. J Dent Res 76:734–743 [CrossRef]
     [Google Scholar]
  20. Jenkinson H. F., Demuth D. R. 1997; Structure, function, and immunogenicity of streptococcal antigen I/II polypeptides. Mol Microbiol 23:183–190 [CrossRef]
     [Google Scholar]
  21. Jenkinson H. F., Lamont R. J. 1997; Streptococcal adhesion and colonization. Crit Rev Oral Biol Med 8:175–200 [CrossRef]
     [Google Scholar]
  22. Jenkinson H. F., Lala H. C., Shepherd M. G. 1990; Coaggregation of Streptococcus sanguis and other streptococci with Candida albicans. Infect Immun 58:1429–1436
     [Google Scholar]
  23. Kimura L. H., Pearsall N. N. 1978; Adherence of Candida albicans to human buccal epithelial cells. Infect Immun 21:64–68
     [Google Scholar]
  24. Kolenbrander P. E., London J. 1993; Adhere today, here tomorrow: oral bacterial adherence. J Bacteriol 175:3247–3252
     [Google Scholar]
  25. Laemmli U. K. 1970; Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685 [CrossRef]
     [Google Scholar]
  26. Lamont R. J., Rosan B. 1990; Adherence of mutans streptococci to other oral bacteria. Infect Immun 58:1738–1743
     [Google Scholar]
  27. Lynch D. P., Tenn M. 1994; Oral candidiasis. History, classification, and clinical presentation. Oral Surg Oral Med Oral Pathol 78:189–193 [CrossRef]
     [Google Scholar]
  28. McNab R., Jenkinson H. F., Loach D. M., Tannock G. W. 1994; Cell-surface-associated polypeptides CshA and CshB of high molecular mass are colonization determinants in the oral bacterium Streptococcus gordonii. Mol Microbiol 14:743–754 [CrossRef]
     [Google Scholar]
  29. Moreno E. C., Kresak M., Hay D. I. 1984; Adsorption of molecules of biological interest onto hydroxyapatite. Calcif Tissue Int 36:48–59 [CrossRef]
     [Google Scholar]
  30. Newman F., Beeley J. A., MacFarlane T. W., Gailbraith J., Buchanan L. 1993; Salivary protein interactions with oral bacteria: an electrophoretic study. Electrophoresis 14:1322–1327 [CrossRef]
     [Google Scholar]
  31. Newman F., Beeley J. A., MacFarlane T. W. 1996; Adherence of oral micro-organisms to human parotid salivary proteins. Electrophoresis 17:266–270 [CrossRef]
     [Google Scholar]
  32. Nikawa H., Hamada T. 1990; Binding of salivary or serum proteins to Candida albicans in vitro. Arch Oral Biol 35:571–573 [CrossRef]
     [Google Scholar]
  33. Nikawa H., Hayashi S., Nikawa Y., Hamada T., Samaranayake L. P. 1993; Interactions between denture lining material, protein pellicles and Candida albicans. Arch Oral Biol 38:631–634 [CrossRef]
     [Google Scholar]
  34. Odds F. C. 1988 Candida and Candidosis: a Review and Bibliography London: Baillière Tindall;
     [Google Scholar]
  35. O’Sullivan J. M., Cannon R. D., Sullivan P. A., Jenkinson H. F. 1997; Identification of salivary basic proline-rich proteins as receptors for Candida albicans adhesion. Microbiology 143:341–348 [CrossRef]
     [Google Scholar]
  36. Pakula R., Walczak W. 1963; On the nature of competence of transformable streptococci. J Gen Microbiol 31:125–133 [CrossRef]
     [Google Scholar]
  37. Rams T. E., Slots J. 1991; Candida biotypes in human adult periodontitis. Oral Microbiol Immunol 6:191–192 [CrossRef]
     [Google Scholar]
  38. Rogers J. D., Haase E. M., Brown A. E., Douglas C. W., 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]
  39. Rudney J. D., Ji Z., Larson C. J., Liljemark W. F., Hickey K. L. 1995; Saliva protein binding to layers of oral streptococci in vitro and in vivo. J Dent Res 74:1280–1288 [CrossRef]
     [Google Scholar]
  40. Samaranayake L. P. 1992; Oral mycoses in HIV infection. Oral Surg Oral Med Oral Pathol 73:171–180 [CrossRef]
     [Google Scholar]
  41. Samaranayake L. P., MacFarlane T. W. 1982; Factors affecting the in vitro adherence of the fungal oral pathogen Candida albicans to epithelial cells of human origin. Arch Oral Biol 27:869–873 [CrossRef]
     [Google Scholar]
  42. Scannapieco F. A., Bergey E. J., Reddy M. S., Levine M. J. 1989; Characterization of salivary α-amylase binding to Streptococcus sanguis. Infect Immun 57:2853–2863
     [Google Scholar]
  43. Shannon I. L., Prigmore J. R., Chauncey H. H. 1962; Modified Carlson–Crittenden device for the collection of parotid fluid. J Dent Res 41:778–783 [CrossRef]
     [Google Scholar]
  44. Slots J., Rams T. E., Listgarten M. A. 1988; Yeasts, enteric rods and pseudomonads in the subgingival flora of severe adult periodontitis. Oral Microbiol Immunol 3:47–52 [CrossRef]
     [Google Scholar]
  45. Stinson M. W., Haraszthy G. G., Zhang X. L., Levine M. J. 1992; Inhibition of Porphyromonas gingivalis adhesion to Streptococcus gordonii by human submandibular-sublingual saliva. Infect Immun 60:2598–2604
     [Google Scholar]
  46. Towbin H., Staehelin T., Gordon J. 1979; Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 76:4350–4354 [CrossRef]
     [Google Scholar]
  47. Vasilas A., Molina L., Hoffman M., Haidaris C. G. 1992; The influence of morphological variation on Candida albicans adhesion to denture acrylic in vitro. Arch Oral Biol 37:613–622 [CrossRef]
     [Google Scholar]
  48. Verran J., Motteram K. L. 1987; The effect of adherent oral streptococci on the subsequent adherence of Candida albicans to acrylic in vitro. J Dent 15:73–76 [CrossRef]
     [Google Scholar]
  49. Whittaker C. J., Klier C. M., Kolenbrander P. E. 1996; Mechanisms of adhesion by oral bacteria. Annu Rev Microbiol 50:513–552 [CrossRef]
     [Google Scholar]
  50. Wright P. S., Clark P., Hardie J. M. 1985; The prevalence and significance of yeasts in persons wearing complete dentures with soft-lining materials. J Dent Res 64:122–125 [CrossRef]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-146-1-41
Loading
Adhesion of Candida albicans to oral streptococci is promoted by selective adsorption of salivary proteins to the streptococcal cell surface
Microbiology 146, 41 (2000); https://doi.org/10.1099/00221287-146-1-41
/content/journal/micro/10.1099/00221287-146-1-41
/content/journal/micro/10.1099/00221287-146-1-41
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error