Skip to main content
NCBI home page
Infection and Immunity logoLink to Infection and Immunity
. 1994 Feb;62(2):509–519. doi: 10.1128/iai.62.2.509-519.1994

Modulation of cell surface-associated mannoprotein antigen expression in experimental candidal vaginitis.

F De Bernardis 1, A Molinari 1, M Boccanera 1, A Stringaro 1, R Robert 1, J M Senet 1, G Arancia 1, A Cassone 1
PMCID: PMC186136  PMID: 7507895

Abstract

The monoclonal antibody (MAb) AF1 recognizes an oligosaccharide epitope present on highly immunogenic and immunomodulatory mannoproteins (MP) of Candida albicans. The expression of this epitope (AF1-MP) during experimental candidal vaginitis was studied in two strains of C. albicans (3153 and CA-2) which were equally vaginopathic but differed in the mode of hypha formation in the vagina. In both strains, immunofluorescence of vaginal samples, taken 1 h after challenge, revealed an intense, MAb AF1-specific labelling of the yeast cells. This labelling was very scarce in fungal cells taken at 24 h and on subsequent days during the development of filamentous forms. Electron-microscopic gold immunolabelling observations showed that molecules carrying AF1-MP spanned the entire cell wall in the initial yeast cells but were absent on the cell surface and in the outermost, capsular layer of the cell wall of the germ tubes and filamentous forms. In both strains, at any time and for any form of intravaginal growth, AF1-MP was clearly expressed in the cytoplasm and cytoplasmic vesicles, and was fully incorporated into the inner layers of the cell wall. As seen by immunofluorescence, the vaginal fluid from C. albicans-infected rats did not hinder the expression of AF1-MP on the yeast cells surface in vitro. In electron-microscopic gold immunolabelling, a hypha-specific MAb (3D9) labelled the surface of the hyphal but not of the yeast cells of C. albicans harvested from rat vagina. Overall, these data strongly suggest that cell surface expression of MP antigen is modulated during intravaginal growth and morphogenesis of C. albicans.

Full text

PDF
509

Images in this article

511Image
on p.511
512Image
on p.512
513Image
on p.513
514Image
on p.514
516Image
on p.516
517Image
on p.517

Selected References

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

  1. Baccarini M., Vecchiarelli A., Cassone A., Bistoni F. Killing of yeast, germ-tube and mycelial forms of Candida albicans by murine effectors as measured by a radiolabel release microassay. J Gen Microbiol. 1985 Mar;131(3):505–513. doi: 10.1099/00221287-131-3-505. [DOI] [PubMed] [Google Scholar]
  2. Blanchard D. K., Michelini-Norris M. B., Djeu J. Y. Production of granulocyte-macrophage colony-stimulating factor by large granular lymphocytes stimulated with Candida albicans: role in activation of human neutrophil function. Blood. 1991 May 15;77(10):2259–2265. [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. Brawner D. L., Cutler J. E., Beatty W. L. Caveats in the investigation of form-specific molecules of Candida albicans. Infect Immun. 1990 Feb;58(2):378–383. doi: 10.1128/iai.58.2.378-383.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Brawner D. L., Cutler J. E. Cell surface and intracellular expression of two Candida albicans antigens during in vitro and in vivo growth. Microb Pathog. 1987 Apr;2(4):249–257. doi: 10.1016/0882-4010(87)90123-9. [DOI] [PubMed] [Google Scholar]
  6. Brawner D. L., Cutler J. E. Ultrastructural and biochemical studies of two dynamically expressed cell surface determinants on Candida albicans. Infect Immun. 1986 Jan;51(1):327–336. doi: 10.1128/iai.51.1.327-336.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. 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]
  8. Casanova M., Gil M. L., Cardeñoso L., Martinez J. P., Sentandreu R. Identification of wall-specific antigens synthesized during germ tube formation by Candida albicans. Infect Immun. 1989 Jan;57(1):262–271. doi: 10.1128/iai.57.1.262-271.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Casanova M., Martínez J. P., Chaffin W. L. Fab fragments from a monoclonal antibody against a germ tube mannoprotein block the yeast-to-mycelium transition in Candida albicans. Infect Immun. 1990 Nov;58(11):3810–3812. doi: 10.1128/iai.58.11.3810-3812.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. 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]
  11. Cassone A., De Bernardis F., Mondello F., Ceddia T., Agatensi L. Evidence for a correlation between proteinase secretion and vulvovaginal candidosis. J Infect Dis. 1987 Nov;156(5):777–783. doi: 10.1093/infdis/156.5.777. [DOI] [PubMed] [Google Scholar]
  12. Cassone A., Torosantucci A., Boccanera M., Pellegrini G., Palma C., Malavasi F. Production and characterisation of a monoclonal antibody to a cell-surface, glucomannoprotein constituent of Candida albicans and other pathogenic Candida species. J Med Microbiol. 1988 Dec;27(4):233–238. doi: 10.1099/00222615-27-4-233. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. De Bernardis F., Adriani D., Lorenzini R., Pontieri E., Carruba G., Cassone A. Filamentous growth and elevated vaginopathic potential of a nongerminative variant of Candida albicans expressing low virulence in systemic infection. Infect Immun. 1993 Apr;61(4):1500–1508. doi: 10.1128/iai.61.4.1500-1508.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. De Bernardis F., Agatensi L., Ross I. K., Emerson G. W., Lorenzini R., Sullivan P. A., Cassone A. Evidence for a role for secreted aspartate proteinase of Candida albicans in vulvovaginal candidiasis. J Infect Dis. 1990 Jun;161(6):1276–1283. doi: 10.1093/infdis/161.6.1276. [DOI] [PubMed] [Google Scholar]
  16. Fidel P. L., Jr, Lynch M. E., Sobel J. D. Candida-specific cell-mediated immunity is demonstrable in mice with experimental vaginal candidiasis. Infect Immun. 1993 May;61(5):1990–1995. doi: 10.1128/iai.61.5.1990-1995.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Ghannoum M., Abu Elteen K. Correlative relationship between proteinase production, adherence and pathogenicity of various strains of Candida albicans. J Med Vet Mycol. 1986 Oct;24(5):407–413. doi: 10.1080/02681218680000621. [DOI] [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. 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]
  20. Kanbe T., Han Y., Redgrave B., Riesselman M. H., Cutler J. E. Evidence that mannans of Candida albicans are responsible for adherence of yeast forms to spleen and lymph node tissue. Infect Immun. 1993 Jun;61(6):2578–2584. doi: 10.1128/iai.61.6.2578-2584.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kimura L. H., Pearsall N. N. Relationship between germination of Candida albicans and increased adherence to human buccal epithelial cells. Infect Immun. 1980 May;28(2):464–468. doi: 10.1128/iai.28.2.464-468.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Kwon-Chung K. J., Lehman D., Good C., Magee P. T. Genetic evidence for role of extracellular proteinase in virulence of Candida albicans. Infect Immun. 1985 Sep;49(3):571–575. doi: 10.1128/iai.49.3.571-575.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Marot-Leblond A., Robert R., Aubry J., Ezcurra P., Senet J. M. Identification and immunochemical characterization of a germ tube specific antigen of Candida albicans. FEMS Immunol Med Microbiol. 1993 Aug;7(2):175–186. doi: 10.1111/j.1574-695X.1993.tb00397.x. [DOI] [PubMed] [Google Scholar]
  24. Mattia E., Carruba G., Angiolella L., Cassone A. Induction of germ tube formation by N-acetyl-D-glucosamine in Candida albicans: uptake of inducer and germinative response. J Bacteriol. 1982 Nov;152(2):555–562. doi: 10.1128/jb.152.2.555-562.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. McCourtie J., Douglas L. J. Relationship between cell surface composition, adherence, and virulence of Candida albicans. Infect Immun. 1984 Jul;45(1):6–12. doi: 10.1128/iai.45.1.6-12.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Molinari A., Gomez M. J., Crateri P., Torosantucci A., Cassone A., Arancia G. Differential cell surface expression of mannoprotein epitopes in yeast and mycelial forms of Candida albicans. Eur J Cell Biol. 1993 Feb;60(1):146–153. [PubMed] [Google Scholar]
  27. Odds F. C. Candida infections: an overview. Crit Rev Microbiol. 1987;15(1):1–5. doi: 10.3109/10408418709104444. [DOI] [PubMed] [Google Scholar]
  28. Palma C., Serbousek D., Torosantucci A., Cassone A., Djeu J. Y. Identification of a mannoprotein fraction from Candida albicans that enhances human polymorphonuclear leukocyte (PMNL) functions and stimulates lactoferrin in PMNL inhibition of candidal growth. J Infect Dis. 1992 Nov;166(5):1103–1112. doi: 10.1093/infdis/166.5.1103. [DOI] [PubMed] [Google Scholar]
  29. Ponton J., Jones J. M. Identification of two germ-tube-specific cell wall antigens of Candida albicans. Infect Immun. 1986 Dec;54(3):864–868. doi: 10.1128/iai.54.3.864-868.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Poulain D., Faille C., Delaunoy C., Jacquinot P. M., Trinel P. A., Camus D. Probable presence of beta(1-2)-linked oligomannosides that act as human immunoglobulin G3 epitopes and are distributed over a Candida albicans 14- to 18-kilodalton antigen. Infect Immun. 1993 Mar;61(3):1164–1166. doi: 10.1128/iai.61.3.1164-1166.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. 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]
  32. Rüchel R. Cleavage of immunoglobulins by pathogenic yeasts of the genus Candida. Microbiol Sci. 1986 Oct;3(10):316–319. [PubMed] [Google Scholar]
  33. Saxena A., Calderone R. Purification and characterization of the extracellular C3d-binding protein of Candida albicans. Infect Immun. 1990 Feb;58(2):309–314. doi: 10.1128/iai.58.2.309-314.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Shepherd M. G. Cell envelope of Candida albicans. Crit Rev Microbiol. 1987;15(1):7–25. doi: 10.3109/10408418709104445. [DOI] [PubMed] [Google Scholar]
  35. Sobel J. D. Epidemiology and pathogenesis of recurrent vulvovaginal candidiasis. Am J Obstet Gynecol. 1985 Aug 1;152(7 Pt 2):924–935. doi: 10.1016/s0002-9378(85)80003-x. [DOI] [PubMed] [Google Scholar]
  36. Sobel J. D., Muller G., Buckley H. R. Critical role of germ tube formation in the pathogenesis of candidal vaginitis. Infect Immun. 1984 Jun;44(3):576–580. doi: 10.1128/iai.44.3.576-580.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Sobel J. D., Muller G., McCormick J. F. Experimental chronic vaginal candidosis in rats. Sabouraudia. 1985 Jun;23(3):199–206. doi: 10.1080/00362178585380301. [DOI] [PubMed] [Google Scholar]
  38. Sobel J. D. Pathogenesis of Candida vulvovaginitis. Curr Top Med Mycol. 1989;3:86–108. doi: 10.1007/978-1-4612-3624-5_5. [DOI] [PubMed] [Google Scholar]
  39. Sundstrom P. M., Kenny G. E. Enzymatic release of germ tube-specific antigens from cell walls of Candida albicans. Infect Immun. 1985 Sep;49(3):609–614. doi: 10.1128/iai.49.3.609-614.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Torosantucci A., Boccanera M., Casalinuovo I., Pellegrini G., Cassone A. Differences in the antigenic expression of immunomodulatory mannoprotein constituents on yeast and mycelial forms of Candida albicans. J Gen Microbiol. 1990 Jul;136(7):1421–1428. doi: 10.1099/00221287-136-7-1421. [DOI] [PubMed] [Google Scholar]
  41. Torosantucci A., Bromuro C., Gomez M. J., Ausiello C. M., Urbani F., Cassone A. Identification of a 65-kDa mannoprotein as a main target of human cell-mediated immune response to Candida albicans. J Infect Dis. 1993 Aug;168(2):427–435. doi: 10.1093/infdis/168.2.427. [DOI] [PubMed] [Google Scholar]
  42. Torosantucci A., Gomez M. J., Bromuro C., Casalinuovo I., Cassone A. Biochemical and antigenic characterization of mannoprotein constituents released from yeast and mycelial forms of Candida albicans. J Med Vet Mycol. 1991;29(6):361–372. doi: 10.1080/02681219180000591. [DOI] [PubMed] [Google Scholar]
  43. Torosantucci A., Palma C., Boccanera M., Ausiello C. M., Spagnoli G. C., Cassone A. Lymphoproliferative and cytotoxic responses of human peripheral blood mononuclear cells to mannoprotein constituents of Candida albicans. J Gen Microbiol. 1990 Nov;136(11):2155–2163. doi: 10.1099/00221287-136-11-2155. [DOI] [PubMed] [Google Scholar]
  44. Trinel P. A., Borg-von-Zepelin M., Lepage G., Jouault T., Mackenzie D., Poulain D. Isolation and preliminary characterization of the 14- to 18-kilodalton Candida albicans antigen as a phospholipomannan containing beta-1,2-linked oligomannosides. Infect Immun. 1993 Oct;61(10):4398–4405. doi: 10.1128/iai.61.10.4398-4405.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Tronchin G., Bouchara J. P., Robert R. Dynamic changes of the cell wall surface of Candida albicans associated with germination and adherence. Eur J Cell Biol. 1989 Dec;50(2):285–290. [PubMed] [Google Scholar]
  46. Tronchin G., Poulain D., Herbaut J., Biguet J. Cytochemical and ultrastructural studies of Candida albicans. II. Evidence for a cell wall coat using concanavalin A. J Ultrastruct Res. 1981 Apr;75(1):50–59. doi: 10.1016/s0022-5320(81)80099-8. [DOI] [PubMed] [Google Scholar]

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

RESOURCES