1887

Abstract

The adhesion of to host tissues contributes to its virulence, and adhesion to tissues or medical devices is a necessary step in biofilm formation. encodes a glycosylphosphatidylinositol (GPI)-anchored glucan-cross-linked cell wall protein that mediates adhesion of to various materials and cells, and appears to be required for biofilm formation and . In this study, we demonstrated that the Eap1p N-terminal signal peptide and C-terminal GPI-anchor sequences result in similar protein localization in and . To investigate the contribution of different Eap1p domains to adhesion, we expressed Eap1p domain deletion mutants in non-adherent strains. The N-terminal domain mediates yeast cell–cell adhesion and invasive growth. Two Ser/Thr-rich domains containing tandem repeats were required to project the N-terminal region into the extracellular environment and to mediate adhesion to polystyrene. The N-terminal tandem repeat domain mediated adhesion to mammalian epithelial cells and promoted pseudohyphal growth. These results suggest a modular structure of Eap1p in which each domain serves multiple, often distinct, functions.

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2008-04-01
2024-12-01
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References

  1. Ahn S. H., Acurio A., Kron S. J. 1999; Regulation of G2/M progression by the STE mitogen-activated protein kinase pathway in budding yeast filamentous growth. Mol Biol Cell 10:3301–3316
    [Google Scholar]
  2. Al-Fattani M. A., Douglas L. J. 2004; Penetration of Candida biofilms by antifungal agents. Antimicrob Agents Chemother 48:3291–3297
    [Google Scholar]
  3. Boder E. T., Midelfort K. S., Wittrup K. D. 2000; Directed evolution of antibody fragments with monovalent femtomolar antigen-binding affinity. Proc Natl Acad Sci U S A 97:10701–10705
    [Google Scholar]
  4. Calderone R. A., Fonzi W. A. 2001; Virulence factors of Candida albicans. Trends Microbiol 9:327–335
    [Google Scholar]
  5. Caro L. H., Tettelin H., Vossen J. H., Ram A. F., van den Ende H., Klis F. M. 1997; In silicio identification of glycosyl-phosphatidylinositol-anchored plasma-membrane and cell wall proteins of Saccharomyces cerevisiae. Yeast 13:1477–1489
    [Google Scholar]
  6. Cormack B. P., Bertram G., Egerton M., Gow N. A., Falkow S., Brown A. J. 1997; Yeast-enhanced green fluorescent protein (yEGFP): a reporter of gene expression in Candida albicans. Microbiology 143:303–311
    [Google Scholar]
  7. Dranginis A. M., Rauceo J. M., Coronado J. E., Lipke P. N. 2007; A biochemical guide to yeast adhesins: glycoproteins for social and antisocial occasions. Microbiol Mol Biol Rev 71:282–294
    [Google Scholar]
  8. Edmond M. B., Wallace S. E., McClish D. K., Pfaller M. A., Jones R. N., Wenzel R. P. 1999; Nosocomial bloodstream infections in United States hospitals: a three-year analysis. Clin Infect Dis 29:239–244
    [Google Scholar]
  9. Frieman M. B., McCaffery J. M., Cormack B. P. 2002; Modular domain structure in the Candida glabrata adhesin Epa1p, a β1,6-glucan-cross-linked cell wall protein. Mol Microbiol 46:479–492
    [Google Scholar]
  10. Fu Y., Ibrahim A. S., Sheppard D. C., Chen Y. C., French S. W., Cutler J. E., Filler S. G., Edwards J. E. Jr 2002; Candida albicans Als1p: an adhesin that is a downstream effector of the EFG1 filamentation pathway. Mol Microbiol 44:61–72
    [Google Scholar]
  11. Gaur N. K., Klotz S. A. 1997; Expression, cloning, and characterization of a Candida albicans gene, ALA1, that confers adherence properties upon Saccharomyces cerevisiae for extracellular matrix proteins. Infect Immun 65:5289–5294
    [Google Scholar]
  12. Gietz D., St Jean A., Woods R. A., Schiestl R. H. 1992; Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Res 20:1425
    [Google Scholar]
  13. Guo B., Styles C. A., Feng Q., Fink G. R. 2000; A Saccharomyces gene family involved in invasive growth, cell-cell adhesion, and mating. Proc Natl Acad Sci U S A 97:12158–12163
    [Google Scholar]
  14. Hawser S. P., Douglas L. J. 1995; Resistance of Candida albicans biofilms to antifungal agents in vitro. Antimicrob Agents Chemother 39:2128–2131
    [Google Scholar]
  15. Hoyer L. L. 2001; The ALS gene family of Candida albicans. Trends Microbiol 9:176–180
    [Google Scholar]
  16. Jarvis W. R. 1995; Epidemiology of nosocomial fungal infections, with emphasis on Candida species. Clin Infect Dis 20:1526–1530
    [Google Scholar]
  17. King L., Butler G. 1998; Ace2p, a regulator of CTS1 (chitinase) expression, affects pseudohyphal production in Saccharomyces cerevisiae. Curr Genet 34:183–191
    [Google Scholar]
  18. Kron S. J., Styles C. A., Fink G. R. 1994; Symmetric cell division in pseudohyphae of the yeast Saccharomyces cerevisiae. Mol Biol Cell 5:1003–1022
    [Google Scholar]
  19. Lambrechts M. G., Bauer F. F., Marmur J., Pretorius I. S. 1996; Muc1, a mucin-like protein that is regulated by Mss10, is critical for pseudohyphal differentiation in yeast. Proc Natl Acad Sci U S A 93:8419–8424
    [Google Scholar]
  20. Li F., Palecek S. P. 2003; EAP1, a Candida albicans gene involved in binding human epithelial cells. Eukaryot Cell 2:1266–1273
    [Google Scholar]
  21. Li F., Palecek S. P. 2005; Identification of Candida albicans genes that induce Saccharomyces cerevisiae cell adhesion and morphogenesis. Biotechnol Prog 21:1601–1609
    [Google Scholar]
  22. Li F., Svarovsky M. J., Karlsson A. J., Wagner J. P., Marchillo K., Oshel P., Andes D., Palecek S. P. 2007; Eap1p, an adhesin that mediates Candida albicans biofilm formation in vitro and in vivo. Eukaryot Cell 6:931–939
    [Google Scholar]
  23. Liu H., Styles C. A., Fink G. R. 1996; Saccharomyces cerevisiae S288C has a mutation in FLO8, a gene required for filamentous growth. Genetics 144:967–978
    [Google Scholar]
  24. Lo W. S., Dranginis A. M. 1998; The cell surface flocculin Flo11 is required for pseudohyphae formation and invasion by Saccharomyces cerevisiae. Mol Biol Cell 9:161–171
    [Google Scholar]
  25. Lopez-Ribot J. L. 2005; Candida albicans biofilms: more than filamentation. Curr Biol 15:R453–R455
    [Google Scholar]
  26. Loza L., Fu Y., Ibrahim A. S., Sheppard D. C., Filler S. G., Edwards J. E. Jr 2004; Functional analysis of the Candida albicans ALS1 gene product. Yeast 21:473–482
    [Google Scholar]
  27. Mao Y., Zhang Z., Wong B. 2003; Use of green fluorescent protein fusions to analyse the N- and C-terminal signal peptides of GPI-anchored cell wall proteins in Candida albicans. Mol Microbiol 50:1617–1628
    [Google Scholar]
  28. Palecek S. P., Parikh A. S., Kron S. J. 2000; Genetic analysis reveals that FLO11 upregulation and cell polarization independently regulate invasive growth in Saccharomyces cerevisiae. Genetics 156:1005–1023
    [Google Scholar]
  29. Pan X., Heitman J. 2000; Sok2 regulates yeast pseudohyphal differentiation via a transcription factor cascade that regulates cell-cell adhesion. Mol Cell Biol 20:8364–8372
    [Google Scholar]
  30. Pfaller M. A., Diekema D. J. 2007; Epidemiology of invasive candidiasis: a persistent public health problem. Clin Microbiol Rev 20:133–163
    [Google Scholar]
  31. Pfaller M. A., Jones R. N., Messer S. A., Edmond M. B., Wenzel R. P. 1998; National surveillance of nosocomial blood stream infection due to Candida albicans: frequency of occurrence and antifungal susceptibility in the SCOPE Program. Diagn Microbiol Infect Dis 31:327–332
    [Google Scholar]
  32. Phan Q. T., Myers C. L., Fu Y., Sheppard D. C., Yeaman M. R., Welch W. H., Ibrahim A. S., Edwards J. E. Jr, Filler S. G. 2007; Als3 is a Candida albicans invasin that binds to cadherins and induces endocytosis by host cells. PLoS Biol 5:e64
    [Google Scholar]
  33. Ramage G., Vande Walle K., Wickes B. L., Lopez-Ribot J. L. 2001; Standardized method for in vitro antifungal susceptibility testing of Candida albicans biofilms. Antimicrob Agents Chemother 45:2475–2479
    [Google Scholar]
  34. Rauceo J. M., De Armond R., Otoo H., Kahn P. C., Klotz S. A., Gaur N. K., Lipke P. N. 2006; Threonine-rich repeats increase fibronectin binding in the Candida albicans adhesin Als5p. Eukaryot Cell 5:1664–1673
    [Google Scholar]
  35. Richard M. L., Plaine A. 2007; Comprehensive analysis of glycosylphosphatidylinositol-anchored proteins in Candida albicans. Eukaryot Cell 6:119–133
    [Google Scholar]
  36. Sambrook J., Fritsch E. F., Maniatis T. 1989 Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
  37. Sheppard D. C., Yeaman M. R., Welch W. H., Phan Q. T., Fu Y., Ibrahim A. S., Filler S. G., Zhang M., Waring A. J., Edwards J. E. Jr 2004; Functional and structural diversity in the Als protein family of Candida albicans. J Biol Chem 279:30480–30489
    [Google Scholar]
  38. Staab J. F., Sundstrom P. 1998; Genetic organization and sequence analysis of the hypha-specific cell wall protein gene HWP1 of Candida albicans. Yeast 14:681–686
    [Google Scholar]
  39. Staab J. F., Bradway S. D., Fidel P. L., Sundstrom P. 1999; Adhesive and mammalian transglutaminase substrate properties of Candida albicans Hwp1. Science 283:1535–1538
    [Google Scholar]
  40. Svarovsky M. J., Palecek S. P. 2005; Disruption of LRG1 inhibits mother-daughter separation in Saccharomyces cerevisiae. Yeast 22:1117–1132
    [Google Scholar]
  41. Verstrepen K. J., Jansen A., Lewitter F., Fink G. R. 2005; Intragenic tandem repeats generate functional variability. Nat Genet 37:986–990
    [Google Scholar]
  42. Vyas V. K., Kuchin S., Berkey C. D., Carlson M. 2003; Snf1 kinases with different beta-subunit isoforms play distinct roles in regulating haploid invasive growth. Mol Cell Biol 23:1341–1348
    [Google Scholar]
  43. Wojciechowicz D., Lu C. F., Kurjan J., Lipke P. N. 1993; Cell surface anchorage and ligand-binding domains of the Saccharomyces cerevisiae cell adhesion protein α-agglutinin, a member of the immunoglobulin superfamily. Mol Cell Biol 13:2554–2563
    [Google Scholar]
  44. Zhao X., Oh S. H., Yeater K. M., Hoyer L. L. 2005; Analysis of the Candida albicans Als2p and Als4p adhesins suggests the potential for compensatory function within the Als family. Microbiology 151:1619–1630
    [Google Scholar]
  45. Zhao X., Oh S. H., Hoyer L. L. 2007; Unequal contribution of ALS9 alleles to adhesion between Candida albicans and human vascular endothelial cells. Microbiology 153:2342–2350
    [Google Scholar]
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