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. 1993 Jun;61(6):2644–2652. doi: 10.1128/iai.61.6.2644-2652.1993

Human submandibular-sublingual saliva promotes adhesion of Candida albicans to polymethylmethacrylate.

M Edgerton 1, F A Scannapieco 1, M S Reddy 1, M J Levine 1
PMCID: PMC280896  PMID: 8500903

Abstract

The purpose of this study was to identify components of saliva that interact with Candida albicans in solution and that may modulate adhesion to dental acrylic (polymethylmethacrylate [PMMA]) surfaces. Saliva-derived pellicles extracted from C. albicans blastoconidia and hyphal-form cells mixed with fresh human submandibular-sublingual saliva (HSMSL) contained predominantly high- and low-molecular-weight mucins (MG1 and MG2, respectively). In contrast, few components from fresh human parotid saliva were adsorbed to yeast cells. Coating PMMA beads with HSMSL significantly enhanced (10-fold) adhesion of both growth forms of C. albicans compared with human parotid saliva (2-fold), suggesting a role for mucins in adhesion. HSMSL-enhanced adhesion was completely abolished by preadsorbing HSMSL with either blastoconidia or hyphal-form cells prior to coating PMMA. However, coating PMMA with purified salivary mucins or the addition of mucin to preadsorbed saliva did not enhance or restore adhesion to levels found with fresh HSMSL. Adhesion assays employing guanidine-treated fresh HSMSL showed a complete lack of Candida binding, suggesting that subjecting HSMSL to dissociating conditions may alter a property of salivary mucins crucial for C. albicans adhesion. Protease and glycosidase treatment of yeast cells significantly reduced adhesion to HSMSL-coated PMMA. In addition, preincubation of C. albicans with mannose and galactose inhibited adhesion to HSMSL-coated PMMA. These results suggest that mucins may play a role in C. albicans adhesion to saliva-coated PMMA and that a glycoprotein on the yeast surface may be involved in these events.

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Selected References

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

  1. Aguirre A., Testa-Weintraub L. A., Banderas J. A., Dunford R., Levine M. J. Levels of salivary cystatins in periodontally healthy and diseased older adults. Arch Oral Biol. 1992;37(5):355–361. doi: 10.1016/0003-9969(92)90018-4. [DOI] [PubMed] [Google Scholar]
  2. Biesbrock A. R., Reddy M. S., Levine M. J. Interaction of a salivary mucin-secretory immunoglobulin A complex with mucosal pathogens. Infect Immun. 1991 Oct;59(10):3492–3497. doi: 10.1128/iai.59.10.3492-3497.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Brassart D., Woltz A., Golliard M., Neeser J. R. In vitro inhibition of adhesion of Candida albicans clinical isolates to human buccal epithelial cells by Fuc alpha 1----2Gal beta-bearing complex carbohydrates. Infect Immun. 1991 May;59(5):1605–1613. doi: 10.1128/iai.59.5.1605-1613.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Budtz-Jorgensen E., Bertram U. Denture stomatitis. II. The effect of antifungal and prosthetic treatment. Acta Odontol Scand. 1970 Jun;28(3):283–304. doi: 10.3109/00016357009032036. [DOI] [PubMed] [Google Scholar]
  5. Budtz-Jörgensen E., Löe H. Chlorhexidine as a denture disinfectant in the treatment of denture stomatitis. Scand J Dent Res. 1972;80(6):457–464. doi: 10.1111/j.1600-0722.1972.tb00314.x. [DOI] [PubMed] [Google Scholar]
  6. Budtz-Jörgensen E., Theilade E. Regional variations in viable bacterial and yeast counts of 1-week-old denture plaque in denture-induced stomatitis. Scand J Dent Res. 1983 Aug;91(4):288–295. doi: 10.1111/j.1600-0722.1983.tb00818.x. [DOI] [PubMed] [Google Scholar]
  7. Budtz-Jörgensen E., Theilade E., Theilade J. Quantitative relationship between yeast and bacteria in denture-induced stomatitis. Scand J Dent Res. 1983 Apr;91(2):134–142. doi: 10.1111/j.1600-0722.1983.tb00790.x. [DOI] [PubMed] [Google Scholar]
  8. Budtz-Jørgensen E. Oral mucosal lesions associated with the wearing of removable dentures. J Oral Pathol. 1981 Apr;10(2):65–80. doi: 10.1111/j.1600-0714.1981.tb01251.x. [DOI] [PubMed] [Google Scholar]
  9. Butrus S. I., Klotz S. A. Blocking Candida adherence to contact lenses. Curr Eye Res. 1986 Oct;5(10):745–750. doi: 10.3109/02713688609000015. [DOI] [PubMed] [Google Scholar]
  10. CURBY W. A. Device for collection of human parotid saliva. J Lab Clin Med. 1953 Mar;41(3):493–496. [PubMed] [Google Scholar]
  11. Calderone R. A., Braun P. C. Adherence and receptor relationships of Candida albicans. Microbiol Rev. 1991 Mar;55(1):1–20. doi: 10.1128/mr.55.1.1-20.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Cohen R. E., Aguirre A., Neiders M. E., Levine M. J., Jones P. C., Reddy M. S., Haar J. G. Immunochemistry and immunogenicity of low molecular weight human salivary mucin. Arch Oral Biol. 1991;36(5):347–356. doi: 10.1016/0003-9969(91)90004-E. [DOI] [PubMed] [Google Scholar]
  13. Cohen R. E., Aguirre A., Neiders M. E., Levine M. J., Jones P. C., Reddy M. S., Haar J. G. Immunochemistry of high molecular-weight human salivary mucin. Arch Oral Biol. 1990;35(2):127–136. doi: 10.1016/0003-9969(90)90174-9. [DOI] [PubMed] [Google Scholar]
  14. Critchley I. A., Douglas L. J. Isolation and partial characterization of an adhesin from Candida albicans. J Gen Microbiol. 1987 Mar;133(3):629–636. doi: 10.1099/00221287-133-3-629. [DOI] [PubMed] [Google Scholar]
  15. Edgerton M., Levine M. J. Characterization of acquired denture pellicle from healthy and stomatitis patients. J Prosthet Dent. 1992 Oct;68(4):683–691. doi: 10.1016/0022-3913(92)90387-p. [DOI] [PubMed] [Google Scholar]
  16. Fukayama M., Calderone R. A. Adherence of cell surface mutants of Candida albicans to buccal epithelial cells and analyses of the cell surface proteins of the mutants. Infect Immun. 1991 Apr;59(4):1341–1345. doi: 10.1128/iai.59.4.1341-1345.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. GREENWOOD F. C., HUNTER W. M., GLOVER J. S. THE PREPARATION OF I-131-LABELLED HUMAN GROWTH HORMONE OF HIGH SPECIFIC RADIOACTIVITY. Biochem J. 1963 Oct;89:114–123. doi: 10.1042/bj0890114. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Guentzel M. N., Cole G. T., Pope L. M. Animal models for candidiasis. Curr Top Med Mycol. 1985;1:57–116. doi: 10.1007/978-1-4613-9547-8_3. [DOI] [PubMed] [Google Scholar]
  19. Kennedy M. J., Rogers A. L., Yancey R. J., Jr Environmental alteration and phenotypic regulation of Candida albicans adhesion to plastic. Infect Immun. 1989 Dec;57(12):3876–3881. doi: 10.1128/iai.57.12.3876-3881.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kennedy M. J., Volz P. A., Edwards C. A., Yancey R. J. Mechanisms of association of Candida albicans with intestinal mucosa. J Med Microbiol. 1987 Dec;24(4):333–341. doi: 10.1099/00222615-24-4-333. [DOI] [PubMed] [Google Scholar]
  21. Klein A., Carnoy C., Wieruszeski J. M., Strecker G., Strang A. M., van Halbeek H., Roussel P., Lamblin G. The broad diversity of neutral and sialylated oligosaccharides derived from human salivary mucins. Biochemistry. 1992 Jul 7;31(26):6152–6165. doi: 10.1021/bi00141a028. [DOI] [PubMed] [Google Scholar]
  22. Klotz S. A., Drutz D. J., Zajic J. E. Factors governing adherence of Candida species to plastic surfaces. Infect Immun. 1985 Oct;50(1):97–101. doi: 10.1128/iai.50.1.97-101.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. 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]
  24. Lamey P. J., Darwazeh A. M., Muirhead J., Rennie J. S., Samaranayake L. P., MacFarlane T. W. Chronic hyperplastic candidosis and secretor status. J Oral Pathol Med. 1991 Feb;20(2):64–67. doi: 10.1111/j.1600-0714.1991.tb00891.x. [DOI] [PubMed] [Google Scholar]
  25. Levine M. J., Reddy M. S., Tabak L. A., Loomis R. E., Bergey E. J., Jones P. C., Cohen R. E., Stinson M. W., Al-Hashimi I. Structural aspects of salivary glycoproteins. J Dent Res. 1987 Feb;66(2):436–441. doi: 10.1177/00220345870660020901. [DOI] [PubMed] [Google Scholar]
  26. McCourtie J., Douglas L. J. Extracellular polymer of Candida albicans: isolation, analysis and role in adhesion. J Gen Microbiol. 1985 Mar;131(3):495–503. doi: 10.1099/00221287-131-3-495. [DOI] [PubMed] [Google Scholar]
  27. McCourtie J., Douglas L. J. Relationship between cell surface composition of Candida albicans and adherence to acrylic after growth on different carbon sources. Infect Immun. 1981 Jun;32(3):1234–1241. doi: 10.1128/iai.32.3.1234-1241.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. McCourtie J., MacFarlane T. W., Samaranayake L. P. Effect of saliva and serum on the adherence of Candida species to chlorhexidine-treated denture acrylic. J Med Microbiol. 1986 May;21(3):209–213. doi: 10.1099/00222615-21-3-209. [DOI] [PubMed] [Google Scholar]
  29. Meitner S. W., Bowen W. H., Haidaris C. G. Oral and esophageal Candida albicans infection in hyposalivatory rats. Infect Immun. 1990 Jul;58(7):2228–2236. doi: 10.1128/iai.58.7.2228-2236.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Miller M. J., Wilson L. A., Ahearn D. G. Effects of protein, mucin, and human tears on adherence of Pseudomonas aeruginosa to hydrophilic contact lenses. J Clin Microbiol. 1988 Mar;26(3):513–517. doi: 10.1128/jcm.26.3.513-517.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Milne R. W., Dawes C. The relative contributions of different salivary glands to the blood group activity of whole saliva in humans. Vox Sang. 1973 Oct;25(4):298–307. doi: 10.1111/j.1423-0410.1973.tb04377.x. [DOI] [PubMed] [Google Scholar]
  32. Minagi S., Miyake Y., Inagaki K., Tsuru H., Suginaka H. Hydrophobic interaction in Candida albicans and Candida tropicalis adherence to various denture base resin materials. Infect Immun. 1985 Jan;47(1):11–14. doi: 10.1128/iai.47.1.11-14.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Nairn R. I. Nystatin and amphotericin B in the treatment of denture-related candidiasis. Oral Surg Oral Med Oral Pathol. 1975 Jul;40(1):68–75. doi: 10.1016/0030-4220(75)90348-5. [DOI] [PubMed] [Google Scholar]
  34. Nikawa H., Hamada T. Binding of salivary or serum proteins to Candida albicans in vitro. Arch Oral Biol. 1990;35(7):571–573. doi: 10.1016/0003-9969(90)90090-w. [DOI] [PubMed] [Google Scholar]
  35. Olsen I., Haanaes H. R. Experimental palatal candidosis and saliva flow in monkeys. Scand J Dent Res. 1977 Jan-Feb;85(2):135–141. doi: 10.1111/j.1600-0722.1977.tb00544.x. [DOI] [PubMed] [Google Scholar]
  36. Pratt-Terpstra I. H., Weerkamp A. H., Busscher H. J. The effects of pellicle formation on streptococcal adhesion to human enamel and artificial substrata with various surface free-energies. J Dent Res. 1989 Mar;68(3):463–467. doi: 10.1177/00220345890680030501. [DOI] [PubMed] [Google Scholar]
  37. Raj P. A., Edgerton M., Levine M. J. Salivary histatin 5: dependence of sequence, chain length, and helical conformation for candidacidal activity. J Biol Chem. 1990 Mar 5;265(7):3898–3905. [PubMed] [Google Scholar]
  38. Ramasubbu N., Reddy M. S., Bergey E. J., Haraszthy G. G., Soni S. D., Levine M. J. Large-scale purification and characterization of the major phosphoproteins and mucins of human submandibular-sublingual saliva. Biochem J. 1991 Dec 1;280(Pt 2):341–352. doi: 10.1042/bj2800341. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Rotrosen D., Calderone R. A., Edwards J. E., Jr Adherence of Candida species to host tissues and plastic surfaces. Rev Infect Dis. 1986 Jan-Feb;8(1):73–85. doi: 10.1093/clinids/8.1.73. [DOI] [PubMed] [Google Scholar]
  40. Samaranayake L. P., MacFarlane T. W. Factors affecting the in-vitro adherence of the fungal oral pathogen Candida albicans to epithelial cells of human origin. Arch Oral Biol. 1982;27(10):869–873. doi: 10.1016/0003-9969(82)90043-7. [DOI] [PubMed] [Google Scholar]
  41. Samaranayake L. P., McCourtie J., MacFarlane T. W. Factors affecting th in-vitro adherence of Candida albicans to acrylic surfaces. Arch Oral Biol. 1980;25(8-9):611–615. doi: 10.1016/0003-9969(80)90076-x. [DOI] [PubMed] [Google Scholar]
  42. Stinson M. W., Levine M. J., Cavese J. M., Prakobphol A., Murray P. A., Tabak L. A., Reddy M. S. Adherence of Streptococcus sanguis to salivary mucin bound to glass. J Dent Res. 1982 Dec;61(12):1390–1393. doi: 10.1177/00220345820610120101. [DOI] [PubMed] [Google Scholar]
  43. Sundstrom P. M., Nichols E. J., Kenny G. E. Antigenic differences between mannoproteins of germ tubes and blastospores of Candida albicans. Infect Immun. 1987 Mar;55(3):616–620. doi: 10.1128/iai.55.3.616-620.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Tabak L. A., Levine M. J., Mandel I. D., Ellison S. A. Role of salivary mucins in the protection of the oral cavity. J Oral Pathol. 1982 Feb;11(1):1–17. doi: 10.1111/j.1600-0714.1982.tb00138.x. [DOI] [PubMed] [Google Scholar]
  45. Tapper-Jones L., Aldred M., Walker D. M. Prevalence and intraoral distribution of Candida albicans in Sjögren's syndrome. J Clin Pathol. 1980 Mar;33(3):282–287. doi: 10.1136/jcp.33.3.282. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Thom S. M., Blackwell C. C., MacCallum C. J., Weir D. M., Brettle R. P., Kinane D. F., Wray D. Non-secretion of blood group antigens and susceptibility to infection by Candida species. FEMS Microbiol Immunol. 1989 Jun;1(6-7):401–405. doi: 10.1111/j.1574-6968.1989.tb02428.x. [DOI] [PubMed] [Google Scholar]
  47. 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]
  48. Tronchin G., Bouchara J. P., Robert R., Senet J. M. Adherence of Candida albicans germ tubes to plastic: ultrastructural and molecular studies of fibrillar adhesins. Infect Immun. 1988 Aug;56(8):1987–1993. doi: 10.1128/iai.56.8.1987-1993.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Vasilas A., Molina L., Hoffman M., Haidaris C. G. The influence of morphological variation on Candida albicans adhesion to denture acrylic in vitro. Arch Oral Biol. 1992 Aug;37(8):613–622. doi: 10.1016/0003-9969(92)90123-p. [DOI] [PubMed] [Google Scholar]
  50. Wagh P. V., Bahl O. P. Sugar residues on proteins. CRC Crit Rev Biochem. 1981;10(4):307–377. doi: 10.3109/10409238109113602. [DOI] [PubMed] [Google Scholar]

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