1887

Abstract

Adherence of the opportunistic pathogen to basement membrane (BM) proteins is considered a crucial step in the development of candidiasis. In this study the interactions of yeast cells with the three main domains of type IV collagen, a major BM glycoprotein, were analysed. adhered to the three immobilized domains by different mechanisms. Adhesion to the N-terminal cross-linking domain (7S) required the presence of divalent cations, whereas interaction with the central collagenous domain (CC) was cation-independent. Recognition of the C-terminal non-collagenous domain (NC1) was partially cation-dependent. Binding inhibition assays with the corresponding domains in soluble form showed that these interactions were specific. Both Ca and Mg promoted adhesion to the 7S domain and the interaction was completely abolished by EDTA. Treatment of the 7S domain, or its subunits, with -glycosidase F reduced yeast binding by approximately 70%. Moreover, several sugars known to be part of the -linked oligosaccharide chains of collagen IV inhibited adhesion to immobilized 7S; -acetylglucosamine, L-fucose and methylmannoside caused a similar inhibition whereas -acetyllactosamine was a more effective inhibitor. In contrast, glucose, galactose, lactose or heparan sulfate did not affect yeast binding. Combinations of the inhibitory sugars at suboptimal inhibition concentrations did not reduce adhesion more than the individual sugars, pointing to a single lectin as responsible for the interaction. These results taken together show that utilizes several adhesins for interacting with type IV collagen, and that at least one of them is a lectin which recognizes the 7S(IV) oligosaccharide residues as its receptor.

Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-147-7-1971
2001-07-01
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/micro/147/7/1471971a.html?itemId=/content/journal/micro/10.1099/00221287-147-7-1971&mimeType=html&fmt=ahah

References

  1. Adini A., Warburg A. 1999; Interaction of Plasmodium gallinaceum ookinetes and oocysts with extracellular matrix proteins. Parasitology 119:331–336 [CrossRef]
    [Google Scholar]
  2. Aitken A., Learmonth M. 1996; Carboxymethylation of cysteine using iodoacetamide/iodoacetic acid. In The Protein Protocols Handbook pp 339–340 Edited by Walker J. M. Totowa, NJ: Humana Press;
    [Google Scholar]
  3. Bejarano P. A., Noelken M. E., Suzuki K., Hudson B. G., Nagase H. 1988; Degradation of basement membranes by human matrix metalloproteinase 3 (stromelysin). Biochem J 256:413–419
    [Google Scholar]
  4. Bejarano P. A., Langeveld J. P. M., Hudson B. G., Noelken M. E. 1989; Degradation of basement membranes by Pseudomonas aeruginosa elastase. Infect Immun 57:3783–3787
    [Google Scholar]
  5. Bouchara J. P., Oumeziane N. A., Lissitzky J. C., Larcher G., Tronchin G., Chabasse D. 1996; Attachment of spores of the human pathogenic fungus Rhizopus oryzae to extracellular matrix components. Eur J Cell Biol 70:76–83
    [Google Scholar]
  6. Brassart D., Woltz A., Golliard M., Neeser J.-R. 1991; In vitro inhibition of adhesion of Candida albicans clinical isolates to human buccal epithelial cells by Fucα1→2Galβ-bearing complex carbohydrates. Infect Immun 59:1605–1613
    [Google Scholar]
  7. Bromley I. M., Donaldson K. 1996; Binding of Aspergillus fumigatus spores to lung epithelial cells and basement membrane proteins: relevance to asthmatic lung. Thorax 51:1203–1209 [CrossRef]
    [Google Scholar]
  8. Calderone R. A., Braun P. C. 1991; Adherence and receptor relationships of Candida albicans . Microbiol Rev 55:1–20
    [Google Scholar]
  9. Cameron B. J., Douglas L. J. 1996; Blood group glycolipids as epithelial cell receptors for Candida albicans . Infect Immun 64:891–896
    [Google Scholar]
  10. Chaffin W. L., Casanova M., Gozalvo D., Martinez J. P, López-Ribot J. L. 1998; Cell wall and secreted proteins of Candida albicans : identification, function, and expression. Microbiol Mol Biol Rev 62:130–180
    [Google Scholar]
  11. Critchley I. A., Douglas L. J. 1987; Role of glycosides as epithelial cell receptors for Candida albicans . J Gen Microbiol 133:637–643
    [Google Scholar]
  12. Cutler J. E. 1991; Putative virulence factors of Candida albicans . Annu Rev Microbiol 45:187–218 [CrossRef]
    [Google Scholar]
  13. De Blas A. L., Cherwinski H. M. 1983; Detection of antigens on nitrocellulose paper immunoblots with monoclonal antibodies. Anal Biochem 133:214–219 [CrossRef]
    [Google Scholar]
  14. Dickerson S. K., Mathis N. L., Rahman M., Bergelson J. M., Santoro S. A. 1999; Determinants of ligand binding specificity of the α1β1 and α2β1 integrins. J Biol Chem 274:32182–32191 [CrossRef]
    [Google Scholar]
  15. Fukazawa Y., Kagaya K. 1997; Molecular bases of adhesion of Candida albicans . J Med Vet Mycol 35:87–99 [CrossRef]
    [Google Scholar]
  16. Gale G., Finkel D., Meinke M., McClelland M., Olson J., Kendrick K., Hostetter M. 1996; Cloning and expression of a gene encoding an integrin-like protein in Candida albicans . Proc Natl Acad Sci USA 93:357–361 [CrossRef]
    [Google Scholar]
  17. Gil M. L., O’Connor J. E., Martinez J. P, Peñalver M. C., López-Ribot J. L. 1996; Binding of extracellular matrix proteins to Aspergillus fumigatus conidia. Infect Immun 64:5239–5247
    [Google Scholar]
  18. Hudson B. G., Reeders S. T., Tryggvason K. 1993; Type IV collagen: structure, gene organization, and role in human diseases. J Biol Chem 268:26033–26036
    [Google Scholar]
  19. Hudson B. G., Gunwar S., Chung A. E., Burgeson R. E. 1995; Matrix components (types IV and VII collagen, entactin and laminin) found in basement membranes. In Extracellular Matrix: a Practical Approach pp 99–129 Edited by Haralson M. A., Hussell J. R. Oxford: IRL Press;
    [Google Scholar]
  20. Jimenez-Lucho V., Ginsburg V., Krivan H. C. 1990; Cryptococcus neoformans, Candida albicans , and other fungi bind specifically to the glycosphingolipid lactosylceramide (Galβ1-4Glcβ1-1Cer), a possible adhesion receptor for yeasts. Infect Immun 58:2085–2090
    [Google Scholar]
  21. Kefalides N. A., Ohno N. 1987; Heterogeneity in basement membranes. In Renal Basement Membrane in Health and Disease pp 81–97 Edited by Price R. G., Hudson B. G. London: Academic Press;
    [Google Scholar]
  22. Klotz S. A. 1990; Adherence of Candida albicans to components of the subendothelial extracellular matrix. FEMS Microbiol Lett 68:249–254
    [Google Scholar]
  23. Klotz S. A. 1994; Plasma and extracellular matrix proteins mediate in the fate of Candida albicans in the human host. Med Hypotheses 42:328–334 [CrossRef]
    [Google Scholar]
  24. Klotz S. A., Rutten M. J., Smith R. L., Babcock S. R., Cunningham M. D. 1993; Adherence of Candida albicans to immobilized extracellular matrix proteins is mediated by calcium-dependent surface glycoproteins. Microb Pathog 14:133–147 [CrossRef]
    [Google Scholar]
  25. Klotz S. A., Hein R. C., Smith R. L., Rouse J. B. 1994; The fibronectin adhesin of Candida albicans . Infect Immun 62:4679–4681
    [Google Scholar]
  26. Knight C. G., Morton L. F., Peachey A. R., Tuckwell D. S., Farndale R. W., Barnes M. J. 2000; The collagen-binding A-domains of integrins α1β1 and α2β1 recognize the same specific amino acid sequence, GFOGER, in native (triple-helical) collagens. J Biol Chem 275:35–40 [CrossRef]
    [Google Scholar]
  27. Laemmli U. K. 1970; Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685 [CrossRef]
    [Google Scholar]
  28. Langeveld J. P. M., Wieslander J., Timoneda J., McKinney P., Butkowski R. J., Wisdom B. J., Hudson B. G. 1988; Structural heterogeneity of the noncollagenous domain of basement membrane collagen. J Biol Chem 263:10481–10488
    [Google Scholar]
  29. Langeveld J. P. M., Noelken M. E., Hard K., Todd P., Vliegenthart J. F. G., Rouse J., Hudson B. G. 1991; Bovine glomerular basement membrane. Location and structure of the asparagine-linked oligosaccharide units and their potential role in the assembly of the 7S collagen IV tetramer. J Biol Chem 266:2622–2631
    [Google Scholar]
  30. Lee K. L., Buckley H. R., Campbell C. C. 1975; An amino acid liquid synthetic medium for development of mycelial and yeast forms of Candida albicans . Sabouradia 13:148–153 [CrossRef]
    [Google Scholar]
  31. Linblom A., Paulsson M. 1996; Basement membranes. In Extracellular Matrix: Tissue Function pp 132–174 Edited by Comper W. D. Amsterdam: Hardwood Academic Publishers;
    [Google Scholar]
  32. López-Ribot J. L., Casanova M., Monteagudo C., Martinez J. P, Sepúlveda P. 1994; Evidence for the presence of a high-affinity laminin receptor-like molecule on the surface of Candida albicans yeast cells. Infect Immun 62:742–746
    [Google Scholar]
  33. Lowrance J. H., Hasty D. L., Simpson W. A. 1988; Adherence of Streptococcus sanguis to conformationally specific determinants in fibronectin. Infect Immun 56:2279–2285
    [Google Scholar]
  34. Martin G. R., Timple R. 1987; Laminin and other basement membrane components. Annu Rev Cell Biol 3:57–85 [CrossRef]
    [Google Scholar]
  35. Nayak B. R., Spiro R. G. 1991; Localization and structure of the asparagine-linked oligosaccharides of type IV collagen from glomerular basement membrane and lens capsule. J Biol Chem 266:13978–13987
    [Google Scholar]
  36. Nègre E. Vogel T., Levanon A., Guy R., Walsh T. J., Roberts D. D. 1994; The collagen binding domain of fibronectin contains a high affinity binding site for Candida albicans . J Biol Chem 269:22039–22045
    [Google Scholar]
  37. Ogata R. 1998; Type IV collagen and laminin enhance the motility, adhesion, and proliferation of hepatoma cells. Kurume Med J 45:11–20 [CrossRef]
    [Google Scholar]
  38. Ollert M. W., Korting H. C., Ollert U, Söhnchen R., Bräutigam S., Bräutigam W. 1993; Mechanisms of adherence of Candida albicans to cultured human epidermal keratinocytes. Infect Immun 61:4560–4568
    [Google Scholar]
  39. Peczon B. D., McCarthy C. A., Merritt R. B. 1982; Probing the subunit structure of cow anterior lens capsule with the detergent, sodium dodecyl sulfate. Exp Eye Res 35:643–651 [CrossRef]
    [Google Scholar]
  40. Peñalver M. C. O’Connor J. E., Martinez J. P., Gil M. L. 1996; Binding of human fibronectin to Aspergillus fumigatus conidia. Infect Immun 64:1146–1153
    [Google Scholar]
  41. Penefsky H. S. 1977; Reversible binding of Pi by beef heart mitochondrial adenosine triphosphatase. J Biol Chem 252:2891–2899
    [Google Scholar]
  42. Petitclerc E., Boutaud A., Prestayko A., Xu J., Sado Y., Ninomiya Y., Hudson B. G., Brooks P. C, Sarras M. P.Jr. 2000; New functions for non-collagenous domains of human collagen type IV. Novel integrin ligands inhibiting angiogenesis and tumour growth in vivo . J Biol Chem 275:8051–8061 [CrossRef]
    [Google Scholar]
  43. Setty S., Kim Y., Fields G. B., Clegg D. O., Wayner E. A., Tsilibary E. C. 1998; Interactions of type IV collagen and its domains with human mesangial cells. J Biol Chem 273:12244–12249 [CrossRef]
    [Google Scholar]
  44. Shahan T. A., Ziaie Z., Pasco S., Fawzi A., Bellon G., Monboisse J. C., Kefalides N. A. 1999; Identification of CD47/integrin-associated protein and αvβ3 a two receptors for the alpha3(IV) chain of type IV collagen on tumour cells. Cancer Res 59:4584–4590
    [Google Scholar]
  45. Smith P. K., Krohn R. I., Hermanson G. T. 7 other authors 1985; Measurement of protein using bicinchoninic acid. Anal Biochem 150:76–85 [CrossRef]
    [Google Scholar]
  46. Spiro R. J., Fukushi S. 1969; The lens capsule. Studies on the carbohydrate units. J Biol Chem 244:2049–2058
    [Google Scholar]
  47. Spreghini E., Gismondi A., Piccoli M., Santoni G. 1999; Evidence for αvβ3 and αvβ5 integrin-like vitronectin (VN) receptors in Candida albicans and their involvement in yeast cell adhesion to VN. J Infect Dis 180:156–166 [CrossRef]
    [Google Scholar]
  48. Sundstrom P. 1999; Adhesins in Candida albicans . Curr Opin Microbiol 2:353–357 [CrossRef]
    [Google Scholar]
  49. Toda S., Matsumara S., Yonemitsu N., Fujitani N., Terayama K., Funatsumaru S., Sugihara H. 1995; Effects of various types of extracellular matrices on adhesion, proliferation, differentiation, and c-fos protein expression of porcine thyroid follicle cells. Cell Struct Funct 20:345–354 [CrossRef]
    [Google Scholar]
  50. Tosh F. D., Douglas L. J. 1992; Characterization of a fucoside-binding adhesin of Candida albicans . Infect Immun 60:4734–4739
    [Google Scholar]
  51. Towbin H., Staehelin T., Gordon J. 1979; Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 76:4350–4354 [CrossRef]
    [Google Scholar]
  52. Trust T. J., Doig P., Emody L., Kienle Z., Wadstrom T., O’Toole P. 1991; High-affinity binding of the basement membrane proteins collagen type IV and laminin to the gastric pathogen Helicobacter pylori. Infect Immun 59:4398–4404
    [Google Scholar]
  53. Vázquez-Torres A. Balish E. 1997; Macrophages in resistance to candidiasis. Microbiol Mol Biol Rev 61:170–192
    [Google Scholar]
  54. Westerlund B., Van Die I., Kramer C. 8 other authors 1991; Multifunctional nature of P fimbriae of uropathogenic Escherichia coli : mutations in fsoE and fsoF influence fimbrial binding to renal tubuli and immobilized fibronectin. Mol Microbiol 5:2965–2975 [CrossRef]
    [Google Scholar]
  55. Yan S., Rodrigues R. G., Cahn-Hidalgo D., Walsh T. J., Roberts D. D. 1998; Hemoglobin induces binding of several extracellular matrix proteins to Candida albicans . Identification of a common receptor for fibronectin, fibrinogen and laminin. J Biol Chem 273:5638–5644 [CrossRef]
    [Google Scholar]
  56. Yu L., Lee K. K., Sheth H. B., Lane-Bell P., Srivastava G., Hindsgaul O., Paranchych W., Hodges R. S., Irvin R. T. 1994; Fimbria-mediated adherence of Candida albicans to glycosphingolipid receptors on human buccal epithelial cells. Infect Immun 62:2843–2848
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-147-7-1971
Loading
/content/journal/micro/10.1099/00221287-147-7-1971
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error