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. 1995 Jun;63(6):2126–2132. doi: 10.1128/iai.63.6.2126-2132.1995

Comparative study of the C3d receptor and 58-kilodalton fibrinogen-binding mannoproteins of Candida albicans.

J L López-Ribot 1, J P Martínez 1, W L Chaffin 1
PMCID: PMC173276  PMID: 7768591

Abstract

Using polyclonal antibodies (PAbs) raised against the Candida albicans C3d receptor (CR2; PAb anti-CR2) and the 58-kDa fibrinogen-binding mannoprotein (mp58; PAb anti-mp58) as well as ligand interactions, we have studied the relationship between these two receptors. In an indirect immunofluorescence assay with germ tubes, greater intensity was observed on the mother blastoconidium when PAb anti-CR2 was used, whereas greater intensity was localized to the hyphal extension when PAb anti-mp58 or binding of soluble fibrinogen was used. No competition or change in the fluorescence pattern was observed in dual-labeling experiments with PAb anti-CR2 and either fibrinogen or PAb anti-mp58. Binding competition also was not observed in an enzyme-linked immunosorbent assay using the components present in a beta-mercaptoethanol extract from the cell wall of germ tubes. In immunoblots, PAb anti-CR2 recognized three different discrete bands with apparent molecular masses of 21, 40, and 66 kDa in the beta-mercaptoethanol extracts from the cell wall, whereas a different, single, broader band with an apparent molecular mass of 58 kDa was detected with PAb anti-mp58. However, when nondenaturing conditions were used to separate the materials present in the cell wall extracts, no reactivity could be detected on Western blots (immunoblots) with PAb anti-mp58. When PAb anti-CR2 was used for analysis, a single band migrating in the area corresponding to approximately 40 kDa was detected. These observations suggest a higher molecular weight for mp58 and one or more of the components detected with PAb anti-CR2 in their native state.

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Selected References

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  1. Alaei S., Larcher C., Ebenbichler C., Prodinger W. M., Janatova J., Dierich M. P. Isolation and biochemical characterization of the iC3b receptor of Candida albicans. Infect Immun. 1993 Apr;61(4):1395–1399. doi: 10.1128/iai.61.4.1395-1399.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bouali A., Robert R., Tronchin G., Senet J. M. Characterization of binding of human fibrinogen to the surface of germ-tubes and mycelium of candida albicans. J Gen Microbiol. 1987 Mar;133(3):545–551. doi: 10.1099/00221287-133-3-545. [DOI] [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. 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]
  5. Burnette W. N. "Western blotting": electrophoretic transfer of proteins from sodium dodecyl sulfate--polyacrylamide gels to unmodified nitrocellulose and radiographic detection with antibody and radioiodinated protein A. Anal Biochem. 1981 Apr;112(2):195–203. doi: 10.1016/0003-2697(81)90281-5. [DOI] [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. Calderone R. A., Linehan L., Wadsworth E., Sandberg A. L. Identification of C3d receptors on Candida albicans. Infect Immun. 1988 Jan;56(1):252–258. doi: 10.1128/iai.56.1.252-258.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Calderone R. A. Recognition between Candida albicans and host cells. Trends Microbiol. 1993 May;1(2):55–58. doi: 10.1016/0966-842x(93)90033-n. [DOI] [PubMed] [Google Scholar]
  9. Casanova M., Chaffin W. L. Cell wall glycoproteins of Candida albicans as released by different methods. J Gen Microbiol. 1991 May;137(5):1045–1051. doi: 10.1099/00221287-137-5-1045. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. Casanova M., Lopez-Ribot J. L., Martinez J. P., Sentandreu R. Characterization of cell wall proteins from yeast and mycelial cells of Candida albicans by labelling with biotin: comparison with other techniques. Infect Immun. 1992 Nov;60(11):4898–4906. doi: 10.1128/iai.60.11.4898-4906.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Casanova M., Lopez-Ribot J. L., Monteagudo C., Llombart-Bosch A., Sentandreu R., Martinez J. P. Identification of a 58-kilodalton cell surface fibrinogen-binding mannoprotein from Candida albicans. Infect Immun. 1992 Oct;60(10):4221–4229. doi: 10.1128/iai.60.10.4221-4229.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Chaffin W. L., Collins B., Marx J. N., Cole G. T., Morrow K. J., Jr Characterization of mutant strains of Candida albicans deficient in expression of a surface determinant. Infect Immun. 1993 Aug;61(8):3449–3458. doi: 10.1128/iai.61.8.3449-3458.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Chaffin W. L., Stocco D. M. Cell wall proteins of Candida albicans. Can J Microbiol. 1983 Oct;29(10):1438–1444. doi: 10.1139/m83-220. [DOI] [PubMed] [Google Scholar]
  15. 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]
  16. 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]
  17. Gilmore B. J., Retsinas E. M., Lorenz J. S., Hostetter M. K. An iC3b receptor on Candida albicans: structure, function, and correlates for pathogenicity. J Infect Dis. 1988 Jan;157(1):38–46. doi: 10.1093/infdis/157.1.38. [DOI] [PubMed] [Google Scholar]
  18. Gustafson K. S., Vercellotti G. M., Bendel C. M., Hostetter M. K. Molecular mimicry in Candida albicans. Role of an integrin analogue in adhesion of the yeast to human endothelium. J Clin Invest. 1991 Jun;87(6):1896–1902. doi: 10.1172/JCI115214. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Han Y., van Rooijen N., Cutler J. E. Binding of Candida albicans yeast cells to mouse popliteal lymph node tissue is mediated by macrophages. Infect Immun. 1993 Aug;61(8):3244–3249. doi: 10.1128/iai.61.8.3244-3249.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Hawkes R. Identification of concanavalin A-binding proteins after sodium dodecyl sulfate--gel electrophoresis and protein blotting. Anal Biochem. 1982 Jun;123(1):143–146. doi: 10.1016/0003-2697(82)90634-0. [DOI] [PubMed] [Google Scholar]
  21. 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]
  22. 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]
  23. Hynes R. O. Integrins: versatility, modulation, and signaling in cell adhesion. Cell. 1992 Apr 3;69(1):11–25. doi: 10.1016/0092-8674(92)90115-s. [DOI] [PubMed] [Google Scholar]
  24. Kalo A., Segal E., Sahar E., Dayan D. Interaction of Candida albicans with genital mucosal surfaces: involvement of fibronectin in adherence. J Infect Dis. 1988 Jun;157(6):1253–1256. doi: 10.1093/infdis/157.6.1253. [DOI] [PubMed] [Google Scholar]
  25. 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]
  26. Kanbe T., Jutila M. A., Cutler J. E. Evidence that Candida albicans binds via a unique adhesion system on phagocytic cells in the marginal zone of the mouse spleen. Infect Immun. 1992 May;60(5):1972–1978. doi: 10.1128/iai.60.5.1972-1978.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Kanbe T., Li R. K., Wadsworth E., Calderone R. A., Cutler J. E. Evidence for expression of the C3d receptor of Candida albicans in vitro and in vivo obtained by immunofluorescence and immunoelectron microscopy. Infect Immun. 1991 May;59(5):1832–1838. doi: 10.1128/iai.59.5.1832-1838.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Klotz S. A. Adherence of Candida albicans to components of the subendothelial extracellular matrix. FEMS Microbiol Lett. 1990 Mar 15;56(3):249–254. doi: 10.1016/s0378-1097(05)80049-7. [DOI] [PubMed] [Google Scholar]
  29. Klotz S. A., Hein R. C., Smith R. L., Rouse J. B. The fibronectin adhesin of Candida albicans. Infect Immun. 1994 Oct;62(10):4679–4681. doi: 10.1128/iai.62.10.4679-4681.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Klotz S. A., Maca R. D. Endothelial cell contraction increases Candida adherence to exposed extracellular matrix. Infect Immun. 1988 Sep;56(9):2495–2498. doi: 10.1128/iai.56.9.2495-2498.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Klotz S. A., Rutten M. J., Smith R. L., Babcock S. R., Cunningham M. D. Adherence of Candida albicans to immobilized extracellular matrix proteins is mediated by calcium-dependent surface glycoproteins. Microb Pathog. 1993 Feb;14(2):133–147. doi: 10.1006/mpat.1993.1014. [DOI] [PubMed] [Google Scholar]
  32. 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]
  33. Klotz S. A., Smith R. L., Stewart B. W. Effect of an arginine-glycine-aspartic acid-containing peptide on hematogenous candidal infections in rabbits. Antimicrob Agents Chemother. 1992 Jan;36(1):132–136. doi: 10.1128/aac.36.1.132. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. 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]
  35. Lee K. L., Buckley H. R., Campbell C. C. An amino acid liquid synthetic medium for the development of mycelial and yeast forms of Candida Albicans. Sabouraudia. 1975 Jul;13(2):148–153. doi: 10.1080/00362177585190271. [DOI] [PubMed] [Google Scholar]
  36. Li R. K., Cutler J. E. Chemical definition of an epitope/adhesin molecule on Candida albicans. J Biol Chem. 1993 Aug 25;268(24):18293–18299. [PubMed] [Google Scholar]
  37. Linehan L., Wadsworth E., Calderone R. Candida albicans C3d receptor, isolated by using a monoclonal antibody. Infect Immun. 1988 Aug;56(8):1981–1986. doi: 10.1128/iai.56.8.1981-1986.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. 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]
  39. López-Ribot J. L., Casanova M., Monteagudo C., Sepúlveda P., Martínez J. P. Evidence for the presence of a high-affinity laminin receptor-like molecule on the surface of Candida albicans yeast cells. Infect Immun. 1994 Feb;62(2):742–746. doi: 10.1128/iai.62.2.742-746.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. López-Ribot J. L., Chaffin W. L. Binding of the extracellular matrix component entactin to Candida albicans. Infect Immun. 1994 Oct;62(10):4564–4571. doi: 10.1128/iai.62.10.4564-4571.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Marcantonio E. E., Hynes R. O. Antibodies to the conserved cytoplasmic domain of the integrin beta 1 subunit react with proteins in vertebrates, invertebrates, and fungi. J Cell Biol. 1988 May;106(5):1765–1772. doi: 10.1083/jcb.106.5.1765. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Martinez J. P., Gil M. L., Casanova M., Lopez-Ribot J. L., Garcia De Lomas J., Sentandreu R. Wall mannoproteins in cells from colonial phenotypic variants of Candida albicans. J Gen Microbiol. 1990 Dec;136(12):2421–2432. doi: 10.1099/00221287-136-12-2421. [DOI] [PubMed] [Google Scholar]
  43. 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]
  44. Millette C. F., Scott B. K. Identification of spermatogenic cell plasma membrane glycoproteins by two-dimensional electrophoresis and lectin blotting. J Cell Sci. 1984 Jan;65:233–248. doi: 10.1242/jcs.65.1.233. [DOI] [PubMed] [Google Scholar]
  45. Miyakawa Y., Kuribayashi T., Kagaya K., Suzuki M., Nakase T., Fukazawa Y. Role of specific determinants in mannan of Candida albicans serotype A in adherence to human buccal epithelial cells. Infect Immun. 1992 Jun;60(6):2493–2499. doi: 10.1128/iai.60.6.2493-2499.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Nègre E., Vogel T., Levanon A., Guy R., Walsh T. J., Roberts D. D. The collagen binding domain of fibronectin contains a high affinity binding site for Candida albicans. J Biol Chem. 1994 Sep 2;269(35):22039–22045. [PubMed] [Google Scholar]
  47. Page S., Odds F. C. Binding of plasma proteins to Candida species in vitro. J Gen Microbiol. 1988 Oct;134(10):2693–2702. doi: 10.1099/00221287-134-10-2693. [DOI] [PubMed] [Google Scholar]
  48. Ponton J., Jones J. M. Analysis of cell wall extracts of Candida albicans by sodium dodecyl sulfate-polyacrylamide gel electrophoresis and Western blot techniques. Infect Immun. 1986 Sep;53(3):565–572. doi: 10.1128/iai.53.3.565-572.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. 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]
  50. Skerl K. G., Calderone R. A., Segal E., Sreevalsan T., Scheld W. M. In vitro binding of Candida albicans yeast cells to human fibronectin. Can J Microbiol. 1984 Feb;30(2):221–227. doi: 10.1139/m84-033. [DOI] [PubMed] [Google Scholar]
  51. Soll D. R. High-frequency switching in Candida albicans. Clin Microbiol Rev. 1992 Apr;5(2):183–203. doi: 10.1128/cmr.5.2.183. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Tosh F. D., Douglas L. J. Characterization of a fucoside-binding adhesin of Candida albicans. Infect Immun. 1992 Nov;60(11):4734–4739. doi: 10.1128/iai.60.11.4734-4739.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. 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]
  54. 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]
  55. 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]
  56. Wadsworth E., Prasad S. C., Calderone R. Analysis of mannoproteins from blastoconidia and hyphae of Candida albicans with a common epitope recognized by anti-complement receptor type 2 antibodies. Infect Immun. 1993 Nov;61(11):4675–4681. doi: 10.1128/iai.61.11.4675-4681.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]

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