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. 1995 Jun;63(6):2173–2179. doi: 10.1128/iai.63.6.2173-2179.1995

Evidence for the presence of collagenous domains in Candida albicans cell surface proteins.

P Sepúlveda 1, A Murgui 1, J L López-Ribot 1, M Casanova 1, J Timoneda 1, J P Martínez 1
PMCID: PMC173282  PMID: 7768595

Abstract

Rabbit polyclonal antibodies (PAbs) directed towards the amino-terminal cysteine-rich 7S domain (PAb anti-7S), the major internal collagenous domain (PAb anti-type IV), and the C-terminal noncollagenous region (PAb anti-NC1) of the type IV collagen molecule were probed by indirect immunofluorescence against Candida albicans blastoconidia and germinated blastoconidia. Most nongerminating cells and mother blastoconidia from which germ tubes originated showed strong fluorescence when PAb anti-7S was used, whereas with PAb anti-type IV, fluorescence was found almost exclusively on the surface of filamentous forms. A patched fluorescent pattern rather than a homogenous confluent fluorescence was observed in all cases. No fluorescent cells were observed with PAb anti-NC1. By Western immunoblotting, PAb anti-type IV cross-reacted primarily with a polypeptide of 37 kDa present in wall extracts obtained from intact cells of both growth forms by treatment with beta-mercaptoethanol, whereas PAb anti-7S recognized a major 58-kDa antigen also present in both extracts, along with some other high-molecular-mass (> 106-kDa) polydisperse species present only in the material released from blastoconidia with beta-mercaptoethanol. No reactive bands were observed when PAb anti-NC1 was used as a probe in Western immunoblotting experiments. The sensitivities or resistances to collagenase digestion of the different polypeptides that cross-reacted with PAbs anti-type IV and anti-7S suggest the existence of cell wall components in C. albicans that contain epitopes that mimic the collagenous domains of the type IV collagen molecule.

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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. Bejarano P. A., Langeveld J. P., Hudson B. G., Noelken M. E. Degradation of basement membranes by Pseudomonas aeruginosa elastase. Infect Immun. 1989 Dec;57(12):3783–3787. doi: 10.1128/iai.57.12.3783-3787.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bouali A., Robert R., Tronchin G., Senet J. M. Binding of human fibrinogen to Candida albicans in vitro: a preliminary study. J Med Vet Mycol. 1986 Aug;24(4):345–348. doi: 10.1080/02681218680000511. [DOI] [PubMed] [Google Scholar]
  4. 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]
  5. 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]
  6. Bozzini S., Visai L., Pignatti P., Petersen T. E., Speziale P. Multiple binding sites in fibronectin and the staphylococcal fibronectin receptor. Eur J Biochem. 1992 Jul 1;207(1):327–333. doi: 10.1111/j.1432-1033.1992.tb17054.x. [DOI] [PubMed] [Google Scholar]
  7. 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]
  8. Brinker J. M., Pegg M. T., Howard P. S., Kefalides N. A. Immunochemical characterization of type IV procollagen from anterior lens capsule. Coll Relat Res. 1985 Jun;5(3):233–244. doi: 10.1016/s0174-173x(85)80013-3. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. 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]
  11. 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]
  12. 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]
  13. 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]
  14. 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]
  15. 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]
  16. 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]
  17. 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]
  18. Douglas L. J. Adhesion of Candida species to epithelial surfaces. Crit Rev Microbiol. 1987;15(1):27–43. doi: 10.3109/10408418709104446. [DOI] [PubMed] [Google Scholar]
  19. 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]
  20. Fox J. W., Mayer U., Nischt R., Aumailley M., Reinhardt D., Wiedemann H., Mann K., Timpl R., Krieg T., Engel J. Recombinant nidogen consists of three globular domains and mediates binding of laminin to collagen type IV. EMBO J. 1991 Nov;10(11):3137–3146. doi: 10.1002/j.1460-2075.1991.tb04875.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. 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]
  22. 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]
  23. 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]
  24. Hostetter M. K., Lorenz J. S., Preus L., Kendrick K. E. The iC3b receptor on Candida albicans: subcellular localization and modulation of receptor expression by glucose. J Infect Dis. 1990 Apr;161(4):761–768. doi: 10.1093/infdis/161.4.761. [DOI] [PubMed] [Google Scholar]
  25. Jensenius J. C., Laursen S. B., Zheng Y., Holmskov U. Conglutinin and CL-43, two collagenous C-type lectins (collectins) in bovine serum. Biochem Soc Trans. 1994 Feb;22(1):95–100. doi: 10.1042/bst0220095. [DOI] [PubMed] [Google Scholar]
  26. 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]
  27. 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]
  28. Krieger M. Molecular flypaper and atherosclerosis: structure of the macrophage scavenger receptor. Trends Biochem Sci. 1992 Apr;17(4):141–146. doi: 10.1016/0968-0004(92)90322-z. [DOI] [PubMed] [Google Scholar]
  29. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  30. 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]
  31. Langeveld J. P., Wieslander J., Timoneda J., McKinney P., Butkowski R. J., Wisdom B. J., Jr, Hudson B. G. Structural heterogeneity of the noncollagenous domain of basement membrane collagen. J Biol Chem. 1988 Jul 25;263(21):10481–10488. [PubMed] [Google Scholar]
  32. 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]
  33. 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]
  34. 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]
  35. 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]
  36. Malhotra R., Haurum J., Thiel S., Sim R. B. Interaction of C1q receptor with lung surfactant protein A. Eur J Immunol. 1992 Jun;22(6):1437–1445. doi: 10.1002/eji.1830220616. [DOI] [PubMed] [Google Scholar]
  37. 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]
  38. 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]
  39. 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]
  40. 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]
  41. Reid K. B. Isolation, by partial pepsin digestion, of the three collagen-like regions present in subcomponent Clq of the first component of human complement. Biochem J. 1976 Apr 1;155(1):5–17. doi: 10.1042/bj1550005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. 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]
  43. 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]
  44. Tronchin G., Robert R., Bouali A., Senet J. M. Immunocytochemical localization of in vitro binding of human fibrinogen to Candida albicans germ tube and mycelium. Ann Inst Pasteur Microbiol. 1987 Mar-Apr;138(2):177–187. doi: 10.1016/0769-2609(87)90194-3. [DOI] [PubMed] [Google Scholar]
  45. Turner M. W. Mannose binding protein. Biochem Soc Trans. 1994 Feb;22(1):88–94. doi: 10.1042/bst0220088. [DOI] [PubMed] [Google Scholar]
  46. Yu L., Lee K. K., Ens K., Doig P. C., Carpenter M. R., Staddon W., Hodges R. S., Paranchych W., Irvin R. T. Partial characterization of a Candida albicans fimbrial adhesin. Infect Immun. 1994 Jul;62(7):2834–2842. doi: 10.1128/iai.62.7.2834-2842.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Yu L., Lee K. K., Sheth H. B., Lane-Bell P., Srivastava G., Hindsgaul O., Paranchych W., Hodges R. S., Irvin R. T. Fimbria-mediated adherence of Candida albicans to glycosphingolipid receptors on human buccal epithelial cells. Infect Immun. 1994 Jul;62(7):2843–2848. doi: 10.1128/iai.62.7.2843-2848.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]

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