Skip to main content
NCBI home page
Infection and Immunity logoLink to Infection and Immunity
. 1995 Apr;63(4):1373–1379. doi: 10.1128/iai.63.4.1373-1379.1995

Expression of surface hydrophobic proteins by Candida albicans in vivo.

P M Glee 1, P Sundstrom 1, K C Hazen 1
PMCID: PMC173161  PMID: 7890397

Abstract

Candida albicans modulates cell surface hydrophobicity during growth and morphogenesis in vitro. To determine if surface hydrophobicity is expressed during pathogenesis, we generated a polyclonal antiserum against yeast hydrophobic proteins. The antiserum was then used for indirect immunofluorescence analysis of tissues from mice colonized and chronically infected with C. albicans. Results demonstrated that yeast hydrophobic proteins are exposed on fungal cells present in host tissues. The polyclonal antiserum distinguished between hydrophobic and hydrophilic cell surfaces in vitro and gave similar staining patterns and intensities for C. albicans cells in vivo. Of the yeast forms present within tissue lesions, approximately half exhibited moderate to intense immunofluorescence with the antiserum. Immunoblot analysis indicated that antigens recognized by the antiserum are predominantly low-molecular-mass hydrophobic proteins that are expressed by different C. albicans isolates and are expressed regardless of growth temperature. Taken together, the immunofluorescence and immunoblot analyses of antigens indicate that C. albicans displays surface hydrophobic proteins during pathogenesis and these proteins are available for hydrophobic interactions with host tissues. The effect of hydrophobic protein exposure on the virulence of C. albicans is discussed.

Full Text

The Full Text of this article is available as a PDF (1.1 MB).

Selected References

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

  1. Antley P. P., Hazen K. C. Role of yeast cell growth temperature on Candida albicans virulence in mice. Infect Immun. 1988 Nov;56(11):2884–2890. doi: 10.1128/iai.56.11.2884-2890.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bendel C. M., Hostetter M. K. Distinct mechanisms of epithelial adhesion for Candida albicans and Candida tropicalis. Identification of the participating ligands and development of inhibitory peptides. J Clin Invest. 1993 Oct;92(4):1840–1849. doi: 10.1172/JCI116775. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bouchara J. P., Tronchin G., Annaix V., Robert R., Senet J. M. Laminin receptors on Candida albicans germ tubes. Infect Immun. 1990 Jan;58(1):48–54. doi: 10.1128/iai.58.1.48-54.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1016/0003-2697(76)90527-3. [DOI] [PubMed] [Google Scholar]
  5. Braun P. C. Surface hydrophobicity enhances corticosterone incorporation in Candida albicans. Infect Immun. 1994 Sep;62(9):4087–4090. doi: 10.1128/iai.62.9.4087-4090.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. 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]
  7. Cantorna M. T., Balish E. Mucosal and systemic candidiasis in congenitally immunodeficient mice. Infect Immun. 1990 Apr;58(4):1093–1100. doi: 10.1128/iai.58.4.1093-1100.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cassone A. Cell wall of Candida albicans: its functions and its impact on the host. Curr Top Med Mycol. 1989;3:248–314. doi: 10.1007/978-1-4612-3624-5_10. [DOI] [PubMed] [Google Scholar]
  9. Cutler J. E. Putative virulence factors of Candida albicans. Annu Rev Microbiol. 1991;45:187–218. doi: 10.1146/annurev.mi.45.100191.001155. [DOI] [PubMed] [Google Scholar]
  10. Domer J. E. Candida cell wall mannan: a polysaccharide with diverse immunologic properties. Crit Rev Microbiol. 1989;17(1):33–51. doi: 10.3109/10408418909105721. [DOI] [PubMed] [Google Scholar]
  11. Elorza M. V., Marcilla A., Sentandreu R. Wall mannoproteins of the yeast and mycelial cells of Candida albicans: nature of the glycosidic bonds and polydispersity of their mannan moieties. J Gen Microbiol. 1988 Aug;134(8):2393–2403. doi: 10.1099/00221287-134-8-2393. [DOI] [PubMed] [Google Scholar]
  12. Elorza M. V., Murgui A., Sentandreu R. Dimorphism in Candida albicans: contribution of mannoproteins to the architecture of yeast and mycelial cell walls. J Gen Microbiol. 1985 Sep;131(9):2209–2216. doi: 10.1099/00221287-131-9-2209. [DOI] [PubMed] [Google Scholar]
  13. Ener B., Douglas L. J. Correlation between cell-surface hydrophobicity of Candida albicans and adhesion to buccal epithelial cells. FEMS Microbiol Lett. 1992 Nov 15;78(1):37–42. doi: 10.1016/0378-1097(92)90284-u. [DOI] [PubMed] [Google Scholar]
  14. Gil M. L., Casanova M., Martínez J. P., Sentandreu R. Antigenic cell wall mannoproteins in Candida albicans isolates and in other Candida species. J Gen Microbiol. 1991 May;137(5):1053–1061. doi: 10.1099/00221287-137-5-1053. [DOI] [PubMed] [Google Scholar]
  15. Hartland R. P., Emerson G. W., Sullivan P. A. A secreted beta-glucan-branching enzyme from Candida albicans. Proc Biol Sci. 1991 Nov 22;246(1316):155–160. doi: 10.1098/rspb.1991.0138. [DOI] [PubMed] [Google Scholar]
  16. Hazen B. W., Hazen K. C. Dynamic expression of cell surface hydrophobicity during initial yeast cell growth and before germ tube formation of Candida albicans. Infect Immun. 1988 Sep;56(9):2521–2525. doi: 10.1128/iai.56.9.2521-2525.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hazen K. C., Brawner D. L., Riesselman M. H., Jutila M. A., Cutler J. E. Differential adherence of hydrophobic and hydrophilic Candida albicans yeast cells to mouse tissues. Infect Immun. 1991 Mar;59(3):907–912. doi: 10.1128/iai.59.3.907-912.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hazen K. C., Hazen B. W. Hydrophobic surface protein masking by the opportunistic fungal pathogen Candida albicans. Infect Immun. 1992 Apr;60(4):1499–1508. doi: 10.1128/iai.60.4.1499-1508.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hazen K. C., Hazen B. W. Surface hydrophobic and hydrophilic protein alterations in Candida albicans. FEMS Microbiol Lett. 1993 Feb 15;107(1):83–87. doi: 10.1111/j.1574-6968.1993.tb06008.x. [DOI] [PubMed] [Google Scholar]
  20. Hazen K. C., Hazen B. W. Temperature-modulated physiological characteristics of Candida albicans. Microbiol Immunol. 1987;31(6):497–508. doi: 10.1111/j.1348-0421.1987.tb03112.x. [DOI] [PubMed] [Google Scholar]
  21. Hazen K. C., Lay J. G., Hazen B. W., Fu R. C., Murthy S. Partial biochemical characterization of cell surface hydrophobicity and hydrophilicity of Candida albicans. Infect Immun. 1990 Nov;58(11):3469–3476. doi: 10.1128/iai.58.11.3469-3476.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Hazen K. C., LeMelle W. G. Improved assay for surface hydrophobic avidity of Candida albicans cells. Appl Environ Microbiol. 1990 Jun;56(6):1974–1976. doi: 10.1128/aem.56.6.1974-1976.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Hazen K. C. Participation of yeast cell surface hydrophobicity in adherence of Candida albicans to human epithelial cells. Infect Immun. 1989 Jul;57(7):1894–1900. doi: 10.1128/iai.57.7.1894-1900.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Hostetter M. K. Adhesins and ligands involved in the interaction of Candida spp. with epithelial and endothelial surfaces. Clin Microbiol Rev. 1994 Jan;7(1):29–42. doi: 10.1128/cmr.7.1.29. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Kato Y., Kitamura T., Hashimoto T. New support for hydrophobic interaction chromatography of proteins. J Chromatogr. 1984 Jun 1;292(2):418–426. doi: 10.1016/s0021-9673(01)83622-0. [DOI] [PubMed] [Google Scholar]
  26. 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]
  27. Klotz S. A., Smith R. L. A fibronectin receptor on Candida albicans mediates adherence of the fungus to extracellular matrix. J Infect Dis. 1991 Mar;163(3):604–610. doi: 10.1093/infdis/163.3.604. [DOI] [PubMed] [Google Scholar]
  28. Kurtz M. B., Cortelyou M. W., Kirsch D. R. Integrative transformation of Candida albicans, using a cloned Candida ADE2 gene. Mol Cell Biol. 1986 Jan;6(1):142–149. doi: 10.1128/mcb.6.1.142. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Lopez-Ribot J. L., Casanova M., Martinez J. P., Sentandreu R. Characterization of cell wall proteins of yeast and hydrophobic mycelial cells of Candida albicans. Infect Immun. 1991 Jul;59(7):2324–2332. doi: 10.1128/iai.59.7.2324-2332.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Luna-Arias J. P., Andaluz E., Ridruejo J. C., Olivero I., Larriba G. The major exoglucanase from Candida albicans: a non-glycosylated secretory monomer related to its counterpart from Saccharomyces cerevisiae. Yeast. 1991 Nov;7(8):833–841. doi: 10.1002/yea.320070808. [DOI] [PubMed] [Google Scholar]
  31. Martínez J. P., López-Ribot J. L., Chaffin W. L. Heterogeneous surface distribution of the fibrinogen-binding protein on Candida albicans. Infect Immun. 1994 Feb;62(2):709–712. doi: 10.1128/iai.62.2.709-712.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Ponton J., Marot-Leblond A., Ezkurra P. A., Barturen B., Robert R., Senet J. M. Characterization of Candida albicans cell wall antigens with monoclonal antibodies. Infect Immun. 1993 Nov;61(11):4842–4847. doi: 10.1128/iai.61.11.4842-4847.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Poulain D., Hopwood V., Vernes A. Antigenic variability of Candida albicans. Crit Rev Microbiol. 1985;12(3):223–270. doi: 10.3109/10408418509104430. [DOI] [PubMed] [Google Scholar]
  34. 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]
  35. Shen H. D., Choo K. B., Lee H. H., Hsieh J. C., Lin W. L., Lee W. R., Han S. H. The 40-kilodalton allergen of Candida albicans is an alcohol dehydrogenase: molecular cloning and immunological analysis using monoclonal antibodies. Clin Exp Allergy. 1991 Nov;21(6):675–681. doi: 10.1111/j.1365-2222.1991.tb03195.x. [DOI] [PubMed] [Google Scholar]
  36. Shepherd M. G. Cell envelope of Candida albicans. Crit Rev Microbiol. 1987;15(1):7–25. doi: 10.3109/10408418709104445. [DOI] [PubMed] [Google Scholar]
  37. Sundstrom P. M., Kenny G. E. Characterization of antigens specific to the surface of germ tubes of Candida albicans by immunofluorescence. Infect Immun. 1984 Mar;43(3):850–855. doi: 10.1128/iai.43.3.850-855.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Takahashi M., Banno Y., Nozawa Y. Secreted Candida albicans phospholipases: purification and characterization of two forms of lysophospholipase-transacylase. J Med Vet Mycol. 1991;29(3):193–204. [PubMed] [Google Scholar]
  39. 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]
  40. White T. C., Miyasaki S. H., Agabian N. Three distinct secreted aspartyl proteinases in Candida albicans. J Bacteriol. 1993 Oct;175(19):6126–6133. doi: 10.1128/jb.175.19.6126-6133.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Wu S. L., Figueroa A., Karger B. L. Protein conformational effects in hydrophobic interaction chromatography. Retention characterization and the role of mobile phase additives and stationary phase hydrophobicity. J Chromatogr. 1986 Dec 26;371:3–27. doi: 10.1016/s0021-9673(01)94689-8. [DOI] [PubMed] [Google Scholar]

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

RESOURCES