C-terminal signals regulate targeting of glycosylphosphatidylinositol- anchored proteins to the cell wall or plasma membrane in Candida albicans

Eukaryotic Cell

Volumn 7, Issue 11, 2008, Pages 1906-1915

  Mao, Yuxin ^a,b   Zhang, Zimei ^b   Gast, Charles ^a   Wong, Brian ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b YALE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL PROTEIN; GLYCOSYLPHOSPHATIDYLINOSITOL; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; SIGNAL PEPTIDE;

AMINO ACID SEQUENCE; ARTICLE; CANDIDA ALBICANS; CELL MEMBRANE; CELL WALL; CHEMISTRY; GENETICS; METABOLISM; MOLECULAR GENETICS; PROTEIN MOTIF; PROTEIN TRANSPORT;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; CANDIDA ALBICANS; CELL MEMBRANE; CELL WALL; FUNGAL PROTEINS; GLYCOSYLPHOSPHATIDYLINOSITOLS; GREEN FLUORESCENT PROTEINS; MOLECULAR SEQUENCE DATA; PROTEIN SORTING SIGNALS; PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS;

CANDIDA ALBICANS;

EID: 55749101953     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00148-08     Document Type: Article

References (40)

1. Albrecht, A., A. Felk, I. Pichova, J. R. Naglik, M. Schaller, P. de Groot, D. Maccallum, F. C. Odds, W. Schafer, F. Klis, M. Monod, and B. Hube. 2006. Glycosylphosphatidylinositol-anchored proteases of Candida albicans target proteins necessary for both cellular processes and host-pathogen interactions. J. Biol. Chem. 281:688-694.
2. Benachour, A., G. Sipos, I. Flury, F. Reggiori, E. Canivenc-Gansel, C. Vionnet, A. Conzelmann, and M. Benghezal. 1999. Deletion of GPI7, a yeast gene required for addition of a side chain to the glycosylphosphatidylinositol (GPI) core structure, affects GPI protein transport, remodeling, and cell wall integrity. J. Biol. Chem. 274:15251-15261.
3. Braun, B. R., W. S. Head, M. X. Wang, and A. D. Johnson. 2000. Identification and characterization of TUP1-regulated genes in Candida albicans. Genetics 156:31-44.
4. Caro L.H., H. Tettelin, J. H. Vossen, A. F. Ram, H. van den Ende, and F. M. Klis. 1997. In silico identification of glycosyl-phosphatidylinositol- anchored plasma-membrane and cell wall proteins of Saccharomyces cerevisiae. Yeast 13:1477-1489.
5. Castano, I., A. De Las Penas, and B. P. Cormack. 2006. Function and regulation of adhesion gene families in Saccharomyces cerevisiae, Candida albicans, and Candida glabrata, p. 163-175. In J. Heitman, S. G. Filler, J. E. Edwards, Jr., and A. P. Mitchell (ed.), Molecular principles of fungal pathogenesis. ASM Press, Washington, DC.
6. De Bernardis, F., F. A. Muhlschlegel, A. Cassone, and W. A. Fonzi. 1998. The pH of the host niche controls gene expression in and virulence of Candida albicans. Infect. Immun. 66:3317-3325.
7. de Groot, P. W., K. J. Hellingwerf, and F. M. Klis. 2003. Genome-wide identification of fungal GPI proteins. Yeast 20:781-796.
8. de Groot, P. W., A. D. de Boer, J. Cunningham, H. L. Dekker, L. de Jong, K. J. Hellingwerf, C. de Koster, and F. M. Klis. 2004. Proteomic analysis of Candida albicans cell walls reveals covalently bound carbohydrate-active enzymes and adhesins. Eukaryot. Cell 3:955-965.
9. de Sampaio, G., J. P. Bourdineaud, and G. J. Lauquin. 1999. A constitutive role for GPI anchors in Saccharomyces cerevisiae: cell wall targeting. Mol. Microbiol. 34:247-256.
10. Fujii, T., H. Shimoi, and Y. Iimura. 1999. Structure of the glucan-binding sugar chain of Tip1p, a cell wall protein of Saccharomyces cerevisiae. Biochim. Biophys. Acta 1427:133-144.
11. Fonzi, W. A. 1999. PHR1 and PHR2 of Candida albicans encode putative glycosidases required for proper cross-linking of beta-1,3- and beta-1,6-glucans. J. Bacteriol. 181:7070-7079.
12. Frieman, M. B., and B. P. Cormack. 2003. The ω-site sequence of glycosylphosphatidylinositol-anchored proteins in Saccharomyces cerevisiae can determine distribution between the membrane and the cell wall. Mol. Microbiol. 50:883-896.
13. Frieman, M. B., J. M. McCaffery, and B. P. Cormack. 2002. Modular domain structure in the Candida glabrata adhesin Epa1p, a beta1,6 glucan-cross-linked cell wall protein. Mol. Microbiol. 46:479-492.
14. Frieman, M. B., and B. P. Cormack. 2004. Multiple sequence signals determine the distribution of glycosylphosphatidylinositol proteins between the plasma membrane and cell wall in Saccharomyces cerevisiae. Microbiology 150:3105-3114.
15. Fu, Y., A. S. Ibrahim, D. C. Sheppard, Y. C. Chen, S. W. French, J. E. Cutler, S. G. Filler, and J. E. Edwards, Jr. 2002. Candida albicans Als1p: an adhesin that is a downstream effector of the EFG1 filamentation pathway. Mol. Microbiol. 44:61-72.
16. Ghannoum, M. A. 2000. Potential role of phospholipases in virulence and fungal pathogenesis. Clin. Microbiol. Rev. 13:122-143.
17. Green, C. B., G. Cheng, J. Chandra, P. Mukherjee, M. A. Ghannoum, and L. L. Hoyer. 2004. RT-PCR detection of Candida albicans ALS gene expression in the reconstituted human epithelium (RHE) model of oral candidiasis and in model biofilms. Microbiology 150:267-275.
18. Hamada, K., H. Terashima, M. Arisawa, and K. Kitada. 1998. Amino acid sequence requirement for efficient incorporation of glycosylphosphatidylinositol-associated proteins into the cell wall of Saccharomyces cerevisiae. J. Biol. Chem. 273:26946-26953.
19. Hamada, K., H. Terashima, M. Arisawa, N. Yabuki, and K. Kitada. 1999. Amino acid residues in the omega-minus region participate in cellular localization of yeast glycosylphosphatidylinositol-attached proteins. J. Bacteriol. 181:3886-3889.
20. Hoyer, L. L. 2001. The ALS gene family of Candida albicans. Trends Microbiol. 9:176-180.
21. Hoyer, L. L., T. L. Payne, and J. E. Hecht. 1998. Identification of Candida albicans ALS2 and ALS4 and localization of Als proteins to the fungal cell surface. J. Bacteriol. 180:5334-5343.
22. Imhof, I., I. Flury, C. Vionnet, C. Roubaty, D. Egger, and A. Conzelmann. 2004. Glycosylphosphatidylinositol (GPI) proteins of Saccharomyces cerevisiae contain ethanolamine phosphate groups on the 1,4-linked mannose of the GPI anchor. J. Biol. Chem. 279:19614-19627.
23. Kapteyn, J. C., L. L. Hoyer, J. E. Hecht, W. H. Muller, A. Andel, A. J. Verkleij, M. Makarow, H. Van Den Ende, and F. M. Klis. 2000. The cell wall architecture of Candida albicans wild-type cells and cell wall-defective mutants. Mol. Microbiol. 35:601-611.
24. Kapteyn, J. C., R. C. Montijn, G. J. Dijkgraaf, and F. M. Klis. 1994. Identification of beta-1,6-glucosylated cell wall proteins in yeast and hyphal forms of Candida albicans. Eur. J. Cell Biol. 65:402-407.
25. Klis, F. M., A. Boorsma, and P. W. de Groot. 2006. Cell wall construction in Saccharomyces cerevisiae. Yeast 23:185-202.
26. Kollár, R., B. B. Reinhold, E. Petráková, H. J. Yeh, G. Ashwell, J. Drgonová, J. C. Kapteyn, F. M. Klis, and E. Cabib. 1997. Architecture of the yeast cell wall. Beta(136)-glucan interconnects mannoprotein, beta(13)3-glucan, and chitin. J. Biol. Chem. 272:17762-17775.
27. Lee, S. A., S. Wormsley, S. Kamoun, K. Joiner, and B. Wong. 2003. An analysis of the Candida albicans genome database for soluble secreted proteins using computer-based prediction algorithms. Yeast 20:595-610.
28. Lu, C. F., J. Kurjan, and P. N. Lipke. 1994. A pathway for cell wall anchorage of Saccharomyces cerevisiae alpha-agglutinin. Mol. Cell. Biol. 14: 4825-4833.
29. Mao, Y., Z. Zhang, and B. Wong. 2003. Use of green fluorescent protein fusions to analyze the N- and C-terminal signal peptides of GPI-anchored cell wall proteins in Candida albicans. Mol. Microbiol. 50:1617-1628.
30. Martinez, J. P., M. L. Gil, J. L. Lopez-Ribot, and W. L. Chaffin. 1998. Serologic response to cell wall mannoproteins and proteins of Candida albicans. Clin. Microbiol. Rev. 11:121-141.
31. Martinez-Lopez, R., L. Monteoliva, R. Diez-Orejas, C. Nombela, and C. Gil. 2004. The GPI-anchored protein CaEcm33p is required for cell wall integrity, morphogenesis and virulence in Candida albicans. Microbiology 150: 3341-3354.
32. Mayor, S., and H. Riezman. 2004. Sorting GPI-anchored proteins. Nat. Rev. Mol. Cell Biol. 5:110-120.
33. Pardini, G., P. W. de Groot, A. T. Coste, M. Karababa, F. M. Klis, C. G. de Koster, and D. Sanglard. 2006. The CRH family coding for cell wall glycosylphosphatidylinositol proteins with a predicted transglycosidase domain affects cell wall organization and virulence of Candida albicans. J. Biol. Chem. 281:40399-40411.
34. Staab, J. F., S. D. Bradway, P. L. Fidel, and P. Sundstrom. 1999. Adhesive and mammalian transglutaminase substrate properties of Candida albicans Hwp1. Science 283:1535-1538.
35. Staab, J. F., Y. S. Bahn, C. H. Tai, P. F. Cook, and P. Sundstrom. 2004. Expression of transglutaminase substrate activity on Candida albicans germ tubes through a coiled, disulfide-bonded N-terminal domain of Hwp1 requires C-terminal glycosylphosphatidylinositol modification. J. Biol. Chem. 279:40737-40747.
36. Terashima, H., K. Hamada, and K. Kitada. 2003. The localization change of Ybr078w/Ecm33, a yeast GPI-associated protein, from the plasma membrane to the cell wall, affecting the cellular function. FEMS Microbiol. Lett. 218:175-180.
37. Tiede, A., I. Bastisch, J. Schubert, P. Orlean, and R. E. Schmidt. 1999. Biosynthesis of glycosyl-phosphatidylinositols in mammals and unicellular microbes. Biol. Chem. 380:503-523.
38. Udenfriend, S., and K. Kodukula. 1995. Prediction of omega site in nascent precursor of glycosylphosphatidylinositol protein. Methods Enzymol. 250: 571-582.
39. Vossen, J. H., W. H. Muller, P. N. Lipke, and F. M. Klis. 1997. Restrictive glycosylphosphatidylinositol anchor synthesis in cwh6/gpi3 yeast cells causes aberrant biogenesis of cell wall proteins. J. Bacteriol. 179:2202-2209.
40. Yin, Q. Y., P. W. de Groot, L. de Jong, F. M. Klis, and C. G. De Koster. 2007. Mass spectrometric quantitation of covalently bound cell wall proteins in Saccharomyces cerevisiae. FEMS Yeast Res. 7:887-896.