UvA-DARE (Digital Academic Repository)
Exploring the fungal wall proteome by mass spectrometry
Yin, Q.Y.
Publication date
2008
Link to publication
Citation for published version (APA):
Yin, Q. Y. (2008). Exploring the fungal wall proteome by mass spectrometry. Digital Printing
Partners.
General rights
It is not permitted to download or to forward/distribute the text or part of it without the consent of the author(s) and/or copyright holder(s), other than for strictly personal, individual use, unless the work is under an open content license (like Creative Commons).
Disclaimer/Complaints regulations
If you believe that digital publication of certain material infringes any of your rights or (privacy) interests, please let the Library know, stating your reasons. In case of a legitimate complaint, the Library will make the material inaccessible and/or remove it from the website. Please Ask the Library: https://uba.uva.nl/en/contact, or a letter to: Library of the University of Amsterdam, Secretariat, Singel 425, 1012 WP Amsterdam, The Netherlands. You will be contacted as soon as possible.
BIBLIOGRAPHY
Abramova, N., Sertil, O., Mehta, S., and Lowry, C.V. (2001) Reciprocal regulation of anaerobic and
aerobic cell wall mannoprotein gene expression in Saccharomyces cerevisiae. J. Bacteriol. 183: 2881-2887.
Aebersold, R., and Mann, M. (2003) Mass spectrometry-based proteomics. Nature 422: 198-207. Aguilar-Uscanga, B., and François, J.M. (2003) A study of the yeast cell wall composition and
structure in response to growth conditions and mode of cultivation. Lett. Appl. Microbiol. 37: 268-274.
Albrecht, A., Felk, A., Pichova, I., Naglik, J.R., et al. (2006) Glycosylphosphatidylinositol-anchored
proteases of Candida albicans target proteins necessary for both cellular processes and host-pathogen interactions. J. Biol. Chem. 281: 688-694.
Alvarez, F.J., and Konopka, J.B. (2007) Identification of an N-acetylglucosamine transporter that
mediates hyphal induction in Candida albicans. Mol. Biol. Cell 18: 965-975.
Baba, M., Baba, N., Ohsumi, Y., Kanaya, K., and Osumi, M. (1989) 3-Dimensional analysis of
morphogenesis induced by mating pheromone-alpha factor in Saccharomyces cerevisiae. J. Cell Sci. 94: 207-216.
Baba, M. and Osumi, M. (1987). Transmission and scanning electron microscopic examination of
intracellular organelles in freeze-substituted Kloeckera and Saccharomyces cerevisiae yeast cells. J. Electron Microsc. Techniq. 5, 246-261.
Ballou, C. E., Ballou, L. and Ball, G. (1994). Schizosaccharomyces pombe glycosylation mutant with
altered cell surface properties. Proc. Natl Acad. Sci. USA 91, 9327-9331.
Bernard, M., and Latge, J.P. (2001) Aspergillus fumigatus cell wall: composition and biosynthesis.
Med. Mycol. 39 Suppl 1: 9-17.
Boorsma, A., de Nobel, H., ter Riet, B., Bargmann, B., Brul, S., Hellingwerf, K.J., and Klis, F.M.
(2004) Characterization of the transcriptional response to cell wall stress in Saccharomyces cerevisiae. Yeast 21: 413-427.
Borkovich, K.A., Alex, L.A., Yarden, O., Freitag, M., et al. (2004) Lessons from the genome
sequence of Neurospora crassa: tracing the path from genomic blueprint to multicellular organism. Microbiol. Mol. Biol. Rev. 68: 1-108.
Braun, B.R., and Johnson, A.D. (2000) TUP1, CPH1 and EFG1 make independent contributions to
filamentation in Candida albicans. Genetics 155: 57-67.
Braun, P.C., and Calderone, R.A. (1978) Chitin synthesis in Candida albicans: comparison of yeast
and hyphal forms. J. Bacteriol. 133: 1472-1477.
Brul, S., King, A., van der Vaart, J.M., Chapman, J., Klis, F.M., and Verrips, C.T. (1997) The
incorporation of mannoproteins in the cell wall of S. cerevisiae and filamentous Ascomycetes. Antonie Leeuwenhoek 72: 229-237.
Bruneau, J.M., Magnin, T., Tagat, E., Legrand, R., Bernard, M., Diaquin, M., Fudali, C., and Latge, J.P. (2001) Proteome analysis of Aspergillus fumigatus identifies
glycosylphosphatidylinositol-anchored proteins associated to the cell wall biosynthesis. Electrophoresis 22: 2812-2823.
Brunet, S., Thibault, P., Gagnon, E., Kearney, P., Bergeron, J.J., and Desjardins, M. (2003)
Organelle proteomics: looking at less to see more. Trends Cell Biol. 13: 629-638.
Cabib, E., Blanco, N., Grau, C., Rodriguez-Peña, J.M., and Arroyo, J. (2007) Crh1p and Crh2p are
required for the cross-linking of chitin to β(1-6)glucan in the Saccharomyces cerevisiae cell wall. Mol. Microbiol. 63: 921-935.
Calvo, E., Pucciarelli, M.G., Bierne, H., Cossart, P., Albar, J.P., and Garcia-Del Portillo, F. (2005)
Analysis of the Listeria cell wall proteome by two-dimensional nanoliquid chromatography coupled to mass spectrometry. Proteomics 5: 433-443.
Cappellaro, C., Mrsa, V., and Tanner, W. (1998) New potential cell wall glucanases of
Saccharomyces cerevisiae and their involvement in mating. J. Bacteriol. 180: 5030-5037.
Caro, L.H., Tettelin, H., Vossen, J.H., Ram, A.F.J., van den Ende, H., and Klis, F.M. (1997) In
silicio identification of glycosyl-phosphatidylinositol-anchored plasma-membrane and cell wall proteins of Saccharomyces cerevisiae. Yeast 13: 1477-1489.
Carotti, C., Ragni, E., Palomares, O., Fontaine, T., Tedeschi, G., Rodriguez, R., Latge, J.P., Vai, M., and Popolo, L. (2004) Characterization of recombinant forms of the yeast Gas1 protein and
identification of residues essential for glucanosyltransferase activity and folding. Eur. J. Biochem. 271: 3635-3645.
Castillo, L., Martinez, A.I., Garcera, A., Elorza, M.V., Valentin, E., and Sentandreu, R. (2003)
Functional analysis of the cysteine residues and the repetitive sequence of Saccharomyces cerevisiae Pir4/Cis3: the repetitive sequence is needed for binding to the cell wall beta-1,3-glucan. Yeast 20: 973-983.
Chaffin, W.L., Lopez-Ribot, J.L., Casanova, M., Gozalbo, D., and Martinez, J.P. (1998) Cell wall
and secreted proteins of Candida albicans: identification, function, and expression. Microbiol. Mol. Biol. Rev. 62: 130-180.
Conzelmann, A., Riezman, H., Desponds, C., and Bron, C. (1988) A major 125-kd membrane
glycoprotein of Saccharomyces cerevisiae is attached to the lipid bilayer through an inositol-containing phospholipid. EMBO J. 7: 2233-2240.
Cormack, B.P., Ghori, N., and Falkow, S. (1999) An adhesin of the yeast pathogen Candida glabrata
mediating adherence to human epithelial cells. Science 285: 578-582.
Coutinho, P.M., and Henrissat, B. (1999) Carbohydrate-active enzymes: an integrated database
approach. In Recent advances in carbohydrate bioengineering. Gilbert, H.J., Davies, G., Henrissat, B. and Svensson, B. (eds): The Royal Society of Chemistry, Cambridge, pp. 3-12.
Dallies, N., Francois, J. and Paquet, V. (1998). A new method for quantitative determination of
polysaccharides in the yeast cell wall: Application to the cell wall defective mutants of Saccharomyces cerevisiae. Yeast 14, 1297-1306.
Damveld, R.A., Arentshorst, M., Vankuyk, P.A., Klis, F.M., Van den Hondel, C.A.M.J.J., and Ram, A.F.J. (2005) Characterisation of CwpA, a putative glycosylphosphatidylinositol anchored
cell wall mannoprotein in the filamentous fungus Aspergillus niger. Fungal Genet. Biol. 42: 873-885.
De Bernardis, F., Muhlschlegel, F. A., Cassone, A. & Fonzi, W. A. (1998) The pH of the host niche
controls gene expression in and virulence of Candida albicans, Infect. Immun. 66, 3317-25.
De Groot, P.W.J., Ruiz, C., Vázquez de Aldana C.R. et al.(2001) A genomic approach for the
identification and classification of genes involved in cell wall formation and its regulation in Saccharomyces cerevisiae. Comp. Funct. Genomics 2: 124-142.
De Groot, P.W.J., Hellingwerf, K.J., and Klis, F.M. (2003) Genome-wide identification of fungal
GPI proteins. Yeast 20: 781-796.
De Groot, P.W.J., De Boer, A.D., Cunningham, J., Dekker, H.L., De Jong, L., Hellingwerf, K.J., De Koster, C., and Klis, F.M. (2004) Proteomic analysis of Candida albicans cell walls reveals
covalently bound carbohydrate-active enzymes and adhesins. Eukaryot. Cell 3: 955-965.
De Groot, P.W.J., Ram, A.F.J., and Klis, F.M. (2005) Features and functions of covalently linked
proteins in fungal cell walls. Fungal Genet. Biol. 42: 657-675.
De Groot, P.W.J., Yin, Q.Y., Weig, M., Sosinska, G.J., Klis, F.M., and de Koster, C.G. (2007)
Mass spectrometric identification of covalently bound cell wall proteins from the fission yeast Schizosaccharomyces pombe. Yeast 24: 267-278.
De Nobel, J.G., Klis, F.M., Priem, J., Munnik, T., and van den Ende, H. (1990) The
glucanase-soluble mannoproteins limit cell wall porosity in Saccharomyces cerevisiae. Yeast 6: 491-499.
Douglas, L.J. (2003) Candida biofilms and their role in infection. Trends Microbiol. 11: 30-36. Dranginis, A.M., Rauceo, J.M., Coronado, J.E., and Lipke, P.N. (2007) A biochemical guide to
yeast adhesins: glycoproteins for social and antisocial occasions. Microbiol. Mol. Biol. Rev. 71: 282-294.
Dünkler, A., Walther, A., Specht, C.A., and Wendland, J. (2005) Candida albicans CHT3 encodes
the functional homolog of the Cts1 chitinase of Saccharomyces cerevisiae. Fungal Genet. Biol. 42: 935-947.
Ecker, M., Deutzmann, R., Lehle, L., Mrsa, V., and Tanner, W. (2006) Pir proteins of
Saccharomyces cerevisiae are attached to b-1,3-glucan by a new protein-carbohydrate linkage. J. Biol. Chem. 281: 11523-11529.
Eigenheer, R.A., Jin Lee, Y., Blumwald, E., Phinney, B.S., and Gelli, A. (2007) Extracellular
glycosylphosphatidylinositol-anchored mannoproteins and proteases of Cryptococcus neoformans. FEMS Yeast Res. 7: 499-510.
Eisenhaber, B., Schneider, G., Wildpaner, M. and Eisenhaber, F. (2004). A sensitive predictor for
potential GPI lipid modification sites in fungal protein sequences and its application to genome-wide studies for Aspergillus nidulans, Candida albicans, Neurospora crassa, Saccharomyces cerevisiae and Schizosaccharomyces pombe. J. Mol. Biol. 337, 243-253.
Fasman, G.D. (1976) CRC Handbook of Biochemistry and Molecular Biology: Proteins, I. Boca Raton,
Florida: CRC Press.
Feiz, L., Irshad, M., Pont-Lezica, R.F., Canut, H., and Jamet, E. (2006) Evaluation of cell wall
preparations for proteomics: a new procedure for purifying cell walls from Arabidopsis hypocotyls. Plant Methods 2: 10.
Firon, A., Lesage, G., and Bussey, H. (2004) Integrative studies put cell wall synthesis on the yeast
functional map. Curr. Opin. Microbiol. 7: 617-623.
proper cross-linking of β-1,3-and b-1,6-glucans. J. Bacteriol. 181, 7070-7079.
Fradin, C., Kretschmar, M., Nichterlein, T., Gaillardin, C., d'Enfert, C., and Hube, B. (2003)
Stage-specific gene expression of Candida albicans in human blood. Mol. Microbiol. 47: 1523–1543.
Fradin, C., De Groot, P., MacCallum, D., Schaller, M., Klis, F., Odds, F.C., and Hube, B. (2005)
Granulocytes govern the transcriptional response, morphology and proliferation of Candida albicans in human blood. Mol. Microbiol. 56: 397-415.
Frieman, M.B., McCaffery, J.M., and Cormack, B.P. (2002) Modular domain structure in the
Candida glabrata adhesin Epa1p, a β-1,6-glucan-cross-linked cell wall protein. Mol. Microbiol. 46: 479-492.
Frieman, M.B., and Cormack, B.P. (2003) The omega-site sequence of
glycosylphosphatidylinositol-anchored proteins in Saccharomyces cerevisiae can determine distribution between the membrane and the cell wall. Mol. Microbiol. 50: 883-896.
Frieman, M.B., and Cormack, B.P. (2004) Multiple sequence signals determine the distribution of
glycosylphosphatidylinositol proteins between the plasma membrane and cell wall in Saccharomyces cerevisiae. Microbiology 150: 3105-3114.
Fu, Y., Rieg, G., Fonzi, W.A., Belanger, P.H., Edwards, J.E., Jr., and Filler, S.G. (1998) Expression
of the Candida albicans gene ALS1 in Saccharomyces cerevisiae induces adherence to endothelial and epithelial cells. Infect. Immun. 66: 1783-1786.
Garcia, R., Bermejo, C., Grau, C., Perez, R., Rodríguez-Peña, J.M., Francois, J., Nombela, C., and Arroyo, J. (2004) The global transcriptional response to transient cell wall damage in
Saccharomyces cerevisiae and its regulation by the cell integrity signaling pathway. J. Biol. Chem. 279: 15183-15195.
Garcia-Sanchez, S., Aubert, S., Iraqui, I., Janbon, G., Ghigo, J.M., and d'Enfert, C. (2004)
Candida albicans biofilms: a developmental state associated with specific and stable gene expression patterns. Eukaryot. Cell 3: 536-545.
Gasch, A.P., Spellman, P.T., Kao, C.M., Carmel-Harel, O., Eisen, M.B., Storz, G., Botstein, D., and Brown, P.O. (2000) Genomic expression programs in the response of yeast cells to
environmental changes. Mol. Biol. Cell 11: 4241-4257.
Ghaemmaghami, S., Huh, W.K., Bower, K., Howson, R.W., Belle, A., Dephoure, N., O'Shea, E.K., and Weissman, J.S. (2003) Global analysis of protein expression in yeast. Nature 425:
737-741.
Gemmill, T.R., and Trimble, R.B. (1999) Overview of N- and O-linked oligosaccharide structures
found in various yeast species. Biochim. Biophys. Acta 1426: 227-237.
Gillum, A.M., Tsay, E.Y., and Kirsch, D.R. (1984) Isolation of the Candida albicans gene for
orotidine-5'-phosphate decarboxylase by complementation of S. cerevisiae ura3 and E. coli pyrF mutations. Mol. Gen. Genet. 198: 179–182.
Grün, C. H., Hochstenbach, F., Humbel, B. M., Verkleij, A. J., Sietsma, J. H., Klis, F. M., Kamerling, J. P. and Vliegenthart, J. F. (2005). The structure of cell wall α-glucan from fission
yeast. Glycobiology 15, 245-257.
Gygi, S.P., Rist, B., Gerber, S.A., Turecek, F., Gelb, M.H., and Aebersold, R. (1999) Quantitative
analysis of complex protein mixtures using isotope-coded affinity tags. Nat. Biotechnol. 17: 994-999.
Hamada, K., Fukuchi, S., Arisawa, M., Baba, M., and Kitada, K. (1998) Screening for
glycosylphosphatidylinositol (GPI)-dependent cell wall proteins in Saccharomyces cerevisiae. Mol. Gen. Genet. 258: 53-59.
Hamada, K., Terashima, H., Arisawa, M., Yabuki, N., and Kitada, K. (1999) Amino acid residues
in the omega-minus region participate in cellular localization of yeast glycosylphosphatidylinositol-attached proteins. J. Bacteriol. 181: 3886-3889.
Hartland, R.P., Vermeulen, C.A., Klis, F.M., Sietsma, J.H., and Wessels, J.G. (1994) The linkage
of (1-3)-β-glucan to chitin during cell wall assembly in Saccharomyces cerevisiae. Yeast 10: 1591-1599.
Hoyer, L.L., Payne, T.L., Bell, M., Myers, A.M., and Scherer, S. (1998) Candida albicans ALS3 and
insights into the nature of the ALS gene family. Curr. Genet. 33: 451-459.
Hoyer, L.L. (2001) The ALS gene family of Candida albicans. Trends Microbiol. 9: 176-180. Huh, W.K., Falvo, J.V., Gerke, L.C., Carroll, A.S., Howson, R.W., Weissman, J.S., and O'Shea,
E.K. (2003) Global analysis of protein localization in budding yeast. Nature 425: 686-691. Humbel, B. M., Konomi, M., Takagi, T., Kamasawa, N., Ishijima, S. A. and Osumi, M. (2001). In
situ localization of β-glucans in the cell wall of Schizosaccharomyces pombe. Yeast 18, 433-444.
Hwang, J. S., Seo, D. H. and Kim, J. Y. (2006). Soluble forms of YlCrh1p and YlCrh2p, cell wall
proteins of Yarrowia lipolytica, have β-1,3-glycosidase activity. Yeast 23, 803-812.
Ibrahim, A.S., Spellberg, B.J., Avenissian, V., Fu, Y., Filler, S.G., and Edwards, J.E., Jr. (2005)
Vaccination with recombinant N-terminal domain of Als1p improves survival during murine disseminated candidiasis by enhancing cell-mediated, not humoral, immunity. Infect. Immun. 73: 999-1005.
Jamet, E., Canut, H., Boudart, G., and Pont-Lezica, R.F. (2006) Cell wall proteins: a new insight
through proteomics. Trends Plant Sci. 11: 33-39.
Jung, U.S., and Levin, D.E. (1999) Genome-wide analysis of gene expression regulated by the yeast
cell wall integrity signalling pathway. Mol. Microbiol. 34: 1049-1057.
Kadosh, D., and Johnson, A.D. (2005) Induction of the Candida albicans filamentous growth
program by relief of transcriptional repression: a genome-wide analysis. Mol. Biol. Cell 16: 2903-2912.
Kapteyn, J. C., Ram, A. F. J., Groos, E. M., Kollar, R., Montijn, R. C., Van den Ende, H., Llobell, A., Cabib, E. and Klis, F. M. (1997). Altered extent of cross-linking of β1,6-glucosylated
mannoproteins to chitin in Saccharomyces cerevisiae mutants with reduced cell wall β1,3-glucan content. J. Bacteriol. 179, 6279-6284.
Kapteyn, J.C., van Egmond, P., Sievi, E., van Den Ende, H., Makarow, M., and Klis, F.M. (1999)
The contribution of the O-glycosylated protein Pir2p/Hsp150 to the construction of the yeast cell wall in wild-type cells and beta 1,6-glucan-deficient mutants. Mol. Microbiol. 31: 1835-1844.
Kapteyn, J.C., Hoyer, L.L., Hecht, J.E., Muller, W.H., Andel, A., Verkleij, A.J., Makarow, M., van Den Ende, H., and Klis, F.M. (2000) The cell wall architecture of Candida albicans wild-type
cells and cell wall-defective mutants. Mol. Microbiol. 35: 601-611.
Kapteyn, J.C., ter Riet, B., Vink, E., Blad, S., De Nobel, H., Van Den Ende, H., and Klis, F.M.
(2001) Low external pH induces HOG1-dependent changes in the organization of the Saccharomyces cerevisiae cell wall. Mol. Microbiol. 39: 469-479.
Candida albicans CaACE2 gene affects morphogenesis, adherence and virulence. Mol. Microbiol. 53: 969-983.
Klis, F.M., de Groot, P.W.J., and Hellingwerf, K. (2001) Molecular organization of the cell wall of
Candida albicans. Med. Mycol. 39 Suppl. 1: 1-8.
Klis, F.M., Mol, P., Hellingwerf, K., and Brul, S. (2002) Dynamics of cell wall structure in
Saccharomyces cerevisiae. FEMS Microbiol. Rev. 26: 239-256.
Klis, F.M., Boorsma, A., and De Groot, P.W.J. (2006) Cell wall construction in Saccharomyces
cerevisiae. Yeast 23: 185-202.
Klis, F.M., de Jong, M., Brul, S., and de Groot, P.W. (2007a) Extraction of cell surface-associated
proteins from living yeast cells. Yeast 24: 253-258.
Klis, F.M., Ram, A.F.J., and de Groot, P.W.J. (2007b) A molecular and genomic view of the fungal
cell wall. In The Mycota VIII. Biology of the Fungal Cell. Howard, R.J. and Gow, N.A. (eds). Heidelberg: Springer-Verlag Berlin Heidelberg, pp. 95-117.
Klotz, S.A., Gaur, N.K., Lake, D.F., Chan, V., Rauceo, J., and Lipke, P.N. (2004) Degenerate
peptide recognition by Candida albicans adhesins Als5p and Als1p. Infect. Immun. 72: 2029-2034.
Klotz, S.A., Gaur, N.K., De Armond, R., Sheppard, D., Khardori, N., Edwards, J.E., Jr., Lipke, P.N., and El-Azizi, M. (2007) Candida albicans Als proteins mediate aggregation with bacteria
and yeasts. Med. Mycol. 45: 363-370.
Kollár, R., Reinhold, B.B., Petrakova, E., Yeh, H.J., Ashwell, G., Drgonova, J., Kapteyn, J.C., Klis, F.M., and Cabib, E. (1997) Architecture of the yeast cell wall. Beta(1-->6)-glucan interconnects
mannoprotein, beta(1-->)3-glucan, and chitin. J. Biol. Chem. 272: 17762-17775.
Kondo, A., and Ueda, M. (2004) Yeast cell-surface display-applications of molecular display. Appl.
Microbiol. Biotechnol. 64: 28-40.
Kopecka, M., Phaff, H.J., and Fleet, G.H. (1974) Demonstration of a fibrillar component in the cell
wall of the yeast Saccharomyces cerevisiae and its chemical nature. J. Cell Biol. 62: 66-76.
Kreger, D. R. (1954) Observations on cell walls of yeasts and some other fungi by X-ray diffraction
and solubility tests. Biochim. Biophy. Acta 13:1.
Kumamoto, C.A. (2002) Candida biofilms. Curr. Opin. Microbiol. 5: 608-611.
Kuranda, M.J., and Robbins, P.W. (1991) Chitinase is required for cell separation during growth of
Saccharomyces cerevisiae. J. Biol. Chem. 266: 19758-19767.
Lagorce, A., Hauser, N.C., Labourdette, D., Rodriguez, C., Martin-Yken, H., Arroyo, J., Hoheisel, J.D., and Francois, J. (2003) Genome-wide analysis of the response to cell wall mutations in the
yeast Saccharomyces cerevisiae. J. Biol. Chem. 278: 20345-20357.
Lehninger, A.L., Nelson, D.L., and Cox, M.M. (1993) Principles of Biochemistry. New York: Worth
Publishers.
Lesage, G., and Bussey, H. (2006) Cell wall assembly in Saccharomyces cerevisiae. Microbiol. Mol. Biol.
Rev. 70: 317-343.
Levin, D.E. (2005) Cell wall integrity signaling in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev.
69: 262-291.
Levitz, S.M., Nong, S.H., Mansour, M.K., Huang, C., and Specht, C.A. (2001) Molecular
characterization of a mannoprotein with homology to chitin deacetylases that stimulates T cell responses to Cryptococcus neoformans. Proc. Natl. Acad. Sci. USA 98: 10422-10427.
neoformans mannoproteins. FEMS Yeast Res. 6: 513-524.
Li, F., Svarovsky, M.J., Karlsson, A.J., Wagner, J.P., Marchillo, K., Oshel, P., Andes, D., and Palecek, S.P. (2007) Eap1p, an adhesin that mediates Candida albicans biofilm formation in vitro
and in vivo. Eukaryot. Cell DOI:10.1128/EC.00049-07 (http://ec.asm.org).
Li, J., Steen, H., and Gygi, S.P. (2003) Protein profiling with cleavable isotope-coded affinity tag
(cICAT) reagents: the yeast salinity stress response. Mol. Cell. Proteomics 2: 1198-1204.
Link, A.J., Eng, J., Schieltz, D.M., Carmack, E., Mize, G.J., Morris, D.R., Garvik, B.M., and Yates, J.R., 3rd (1999) Direct analysis of protein complexes using mass spectrometry. Nat. Biotechnol. 17:
676-682.
Lussier, M., White, A.M., Sheraton, J., et al. (1997) Large scale identification of genes involved in
cell surface biosynthesis and architecture in Saccharomyces cerevisiae. Genetics 147: 435-450.
Magnelli, P. E., Cipollo, J. F. and Robbins, P. W. (2005). A glucanase-driven fractionation allows
redefinition of Schizosaccharomyces pombe cell wall composition and structure: assignment of diglucan. Anal. Biochem. 336, 202-212.
Maidan, M.M., Thevelein, J.M., and Van Dijck, P. (2005) Carbon source induced yeast-to-hypha
transition in Candida albicans is dependent on the presence of amino acids and on the G-protein-coupled receptor Gpr1. Biochem. Soc. Trans. 33: 291-293.
Manners, D. J. and Meyer, M. T. (1977). The molecular structures of some glucans from the cell
walls of Schizosaccharomyces pombe. Carbohydrate Res. 57, 189-203.
Marchler-Bauer, A., Anderson, J.B., DeWeese-Scott, C., et al. (2003) CDD: a curated Entrez
database of conserved domain alignments. Nucleic Acids Res. 31: 383-387.
Martchenko, M., Alarco, A.M., Harcus, D., and Whiteway, M. (2004) Superoxide dismutases in
Candida albicans: Transcriptional regulation and functional characterization of the hyphal-induced SOD5 gene. Mol. Biol. Cell 15: 456-467.
Martinez-Lopez, R., Park, H., Myers, C.L., Gil, C., and Filler, S.G. (2006) Candida albicans
Ecm33p is important for normal cell wall architecture and interactions with host cells. Eukaryot. Cell 5: 140-147.
Martinez, A.I., Castillo, L., Garcera, A., Elorza, M.V., Valentin, E., and Sentandreu, R. (2004) Role
of Pir1 in the construction of the Candida albicans cell wall. Microbiology 150: 3151-3161.
McCreath, K.J., Specht, C.A., and Robbins, P.W. (1995) Molecular cloning and characterization of
chitinase genes from Candida albicans. Proc. Natl. Acad. Sci. USA 92: 2544-2548.
McFadden, D.C., and Casadevall, A. (2001) Capsule and melanin synthesis in Cryptococcus
neoformans. Med. Mycol. 39 Suppl 1: 19-30.
Meijer, H.J., van de Vondervoort, P.J., Yin, Q.Y., de Koster, C.G., Klis, F.M., Govers, F., and de Groot, P.W.J. (2006) Identification of cell wall-associated proteins from Phytophthora ramorum.
Mol. Plant Microbe Interact. 19: 1348-1358.
Montijn, R.C., Van Wolven, P., De Hoog, S., and Klis, F.M. (1997) β-Glucosylated proteins in the
cell wall of the black yeast Exophiala (Wangiella) dermatitidis. Microbiology 143: 1673-1680.
Morita, T., Tanaka, N., Hosomi, A., Giga-Hama, Y. and Takegawa, K. (2006). An a-amylase
homologue, aah3, encodes a GPI-anchored membrane protein required for cell wall integrity and morphogenesis in Schizosaccharomyces pombe. Biosci. Biotechnol. Biochem. 70, 1454-1463.
Moukadiri, I., Armero, J., Abad, A., Sentandreu, R., and Zueco, J. (1997) Identification of a
179: 2154-2162.
Mouyna, I., Hartland, R. P., Fontaine, T., Diaquin, M., Simenel, C., Delepierre, M., Henrissat, B. and Latgé, J. P. (1998). A 1,3-β-glucanosyltransferase isolated from the cell wall of Aspergillus
fumigatus is a homologue of the yeast Bgl2p. Microbiology 144, 3171-3180.
Mouyna, I., Fontaine, T., Vai, M., Monod, M., Fonzi, W.A., Diaquin, M., Popolo, L., Hartland, R.P., and Latge, J.P. (2000) Glycosylphosphatidylinositol-anchored glucanosyltransferases play
an active role in the biosynthesis of the fungal cell wall. J. Biol. Chem. 275: 14882-14889.
Mrsa, V., Klebl, F. and Tanner, W. (1993). Purification and characterization of the Saccharomyces
cerevisiae BGL2 gene product, a cell wall endo-β-1,3-glucanase. J. Bacteriol. 175, 2102-2106.
Mrsa, V., Seidl, T., Gentzsch, M., and Tanner, W. (1997) Specific labelling of cell wall proteins by
biotinylation. Identification of four covalently linked O-mannosylated proteins of Saccharomyces cerevisiae. Yeast 13: 1145-1154.
Mrsa, V., and Tanner, W. (1999) Role of NaOH-extractable cell wall proteins Ccw5p, Ccw6p,
Ccw7p and Ccw8p (members of the Pir protein family) in stability of the Saccharomyces cerevisiae cell wall. Yeast 15: 813-820.
Mühlschlegel, F.A., and Fonzi, W.A. (1997) PHR2 of Candida albicans encodes a functional
homolog of the pH-regulated gene PHR1 with an inverted pattern of pH-dependent expression. Mol. Cell Biol. 17: 5960-5967.
Nantel, A., Dignard, D., Bachewich, C., Harcus, D., et al. (2002) Transcription profiling of
Candida albicans cells undergoing the yeast-to-hyphal transition. Mol. Biol. Cell 13: 3452-3465.
Nobile, C.J., Nett, J.E., Andes, D.R., and Mitchell, A.P. (2006) Function of Candida albicans
adhesin Hwp1 in biofilm formation. Eukaryot. Cell 5: 1604-1610.
Nombela, C., Gil, C., and Chaffin, W.L. (2006) Non-conventional protein secretion in yeast. Trends
Microbiol. 14: 15-21.
Oda, Y., Huang, K., Cross, F.R., Cowburn, D., and Chait, B.T. (1999) Accurate quantitation of
protein expression and site-specific phosphorylation. Proc. Natl. Acad. Sci. USA 96: 6591-6596.
Oda, Y., Owa, T., Sato, T., Boucher, B., Daniels, S., Yamanaka, H., Shinohara, Y., Yokoi, A., Kuromitsu, J., and Nagasu, T. (2003) Quantitative chemical proteomics for identifying
candidate drug targets. Anal. Chem. 75: 2159-2165.
Ohishi, K., Inoue, N., Maeda, Y., Takeda, J., Riezman, H., and Kinoshita, T. (2000) Gaa1p and
gpi8p are components of a glycosylphosphatidylinositol (GPI) transamidase that mediates attachment of GPI to proteins. Mol. Biol. Cell 11: 1523-1533.
Omi, K., Sonoda, H., Nagata, K. and Sugita, K. (1999). Cloning and characterization of psu1+ , a new essential fission yeast gene involved in cell wall synthesis. Biochem. Biophys. Res. Commun. 262, 368-374.
Ong, S.E., Blagoev, B., Kratchmarova, I., Kristensen, D.B., Steen, H., Pandey, A., and Mann, M.
(2002) Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol. Cell. Proteomics 1: 376-386.
Ong, S.E., and Mann, M. (2005) Mass spectrometry-based proteomics turns quantitative. Nat. Chem.
Biol. 1: 252-262.
Orlean, P. (1997) Biogenesis of yeast wall and surface components. In Molecular and cellular biology
of the yeast Saccharomyces. Vol. 3. Pringle, J.R., Broach, J. and Jones, E. (eds). Cold Spring Harbor: Cold Spring Harbor Laboratory Press, pp. 229-362.
Osumi, M. (1998) The ultrastructure of yeast: cell wall structure and formation. Micron 29: 207-233. Page, R. D. (1996). TreeView: an application to display phylogenetic trees on personal computers.
Comput. Appl. Biosci. 12, 357-358.
Pardini, G., De Groot, P.W., Coste, A.T., Karababa, M., Klis, F.M., de Koster, C.G., and Sanglard, D. (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.
Pardo, M., Monteoliva, L., Vazquez, P., Martinez, R., Molero, G., Nombela, C., and Gil, C. (2004)
PST1 and ECM33 encode two yeast cell surface GPI proteins important for cell wall integrity. Microbiology 150: 4157-4170.
Pérez, P. and Ribas, J. C. (2004). Cell wall analysis. Methods 33, 245-251.
Peschen, D., Li, H.P., Fischer, R., Kreuzaler, F., and Liao, Y.C. (2004) Fusion proteins comprising
a Fusarium-specific antibody linked to antifungal peptides protect plants against a fungal pathogen. Nat. Biotechnol. 22: 732-738.
Phan, Q.T., Myers, C.L., Fu, Y., Sheppard, D.C., Yeaman, M.R., Welch, W.H., Ibrahim, A.S., Edwards, J.E., and Filler, S.G. (2007) Als3 is a Candida albicans invasin that binds to cadherins
and induces endocytosis by host cells. PLoS Biol. 5: 543-557.
Popolo, L. and Vai, M. (1999). The Gas1 glycoprotein, a putative wall polymer cross-linker. Biochim.
Biophys. Acta 1426, 385-400.
Protchenko, O., Ferea, T., Rashford, J., Tiedeman, J., Brown, P.O., Botstein, D., and Philpott, C.C. (2001) Three cell wall mannoproteins facilitate the uptake of iron in Saccharomyces cerevisiae.
J. Biol. Chem. 276: 49244-49250.
Ragni, E., Fontaine, T., Gissi, C., Latge, J.P., and Popolo, L. (2007a) The Gas family of proteins of
Saccharomyces cerevisiae: characterization and evolutionary analysis. Yeast 24: 297-308.
Ragni, E., Sipiczki, M., and Strahl, S. (2007b) Characterization of Ccw12p, a major key player in
cell wall stability of Saccharomyces cerevisiae. Yeast 24: 309-319.
Ram, A.F.J., Kapteyn, J.C., Montijn, R.C., Caro, L.H., Douwes, J.E., Baginsky, W., Mazur, P., van den Ende, H., and Klis, F.M. (1998) Loss of the plasma membrane-bound protein Gas1p in
Saccharomyces cerevisiae results in the release of beta1,3-glucan into the medium and induces a compensation mechanism to ensure cell wall integrity. J. Bacteriol. 180: 1418-1424.
Reynolds, T.B., and Fink, G.R. (2001) Bakers' yeast, a model for fungal biofilm formation. Science
291: 878-881.
Rodriguez-Ortega, M.J., Norais, N., Bensi, G., Liberatori, S., et al. (2006) Characterization and
identification of vaccine candidate proteins through analysis of the group A Streptococcus surface proteome. Nat. Biotechnol. 24: 191-197.
Rodríguez-Peña, J.M., Cid, V.J., Arroyo, J., and Nombela, C. (2000) A novel family of cell
wall-related proteins regulated differently during the yeast life cycle. Mol. Cell. Biol. 20: 3245-3255.
Rodriguez-Pena, J.M., Rodriguez, C., Alvarez, A., Nombela, C., and Arroyo, J. (2002) Mechanisms
for targeting of the Saccharomyces cerevisiae GPI-anchored cell wall protein Crh2p to polarised growth sites. J. Cell Sci. 115: 2549-2558.
Ross, P.L., Huang, Y.N., Marchese, J.N., Williamson, B., et al. (2004) Multiplexed protein
Proteomics 3: 1154-1169.
Ruiz-Herrera, J., Leon, C.G., Carabez-Trejo, A., and Reyes-Salinas, E. (1996) Structure and
chemical composition of the cell walls from the haploid yeast and mycelial forms of Ustilago maydis. Fungal Genet. Biol. 20: 133-142.
Russo, P., Kalkkinen, N., Sareneva, H., Paakkola, J., and Makarow, M. (1992) A heat shock gene
from Saccharomyces cerevisiae encoding a secretory glycoprotein. Proc. Natl. Acad. Sci. USA 89: 3671-3675.
Sadygov, R.G., Cociorva, D., and Yates, J.R., 3rd (2004) Large-scale database searching using
tandem mass spectra: looking up the answer in the back of the book. Nat. Methods 1: 195-202.
Sanglard D. and Odds F.C. (2002) Resistance of Candida species to antifungal agents: molecular
mechanisms and clinical consequences. Lancet Infect. Dis. 2:73-85.
Schoffelmeer, E.A.M., Kapteyn, J.C., Montijn, R.C., Cornelissen, B.C., and Klis, F.M. (1996)
Glucosylation of fungal cell wall proteins as a potential target for novel antifungal agents. In Modern fungicides and antifungal compounds. Lyr, H., Russel, P.E. and Sisler, H.D. (eds). Andover: Intercept, pp. 157-162.
Schoffelmeer, E.A.M., Vossen, J.H., Van Doorn, A.A., Cornelissen, B.J., and Haring, M.A. (2001)
FEM1, a Fusarium oxysporum glycoprotein that is covalently linked to the cell wall matrix and is conserved in filamentous fungi. Mol. Genet. Genomics 265: 143-152.
Schuldiner, M., Collins, S.R., Thompson, N.J., Denic, V., et al. (2005) Exploration of the function
and organization of the yeast early secretory pathway through an epistatic miniarray profile. Cell 123: 507-519.
Setiadi, E.R., Doedt, T., Cottier, F., Noffz, C., and Ernst, J.F. (2006) Transcriptional response
Candida albicans to hypoxia: Linkage of oxygen sensing and Efg1p-regulatory networks. J. Mol. Biol. 361: 399-411.
Severin, A., Nickbarg, E., Wooters, J., Quazi, S.A., Matsuka, Y.V., Murphy, E., Moutsatsos, I.K., Zagursky, R.J., and Olmsted, S.B. (2007) Proteomic analysis and identification of Streptococcus
pyogenes surface-associated proteins. J. Bacteriol. 189: 1514-1522.
Shepherd, M.G., Poulter, R.T.M., and Sullivan, P.A. (1985) Candida albicans: biology, genetics,
and pathogenicity. Ann. Rev. Microbiol. 39:579-614
Shevchenko, A., Wilm, M., Vorm, O., and Mann, M. (1996) Mass spectrometric sequencing of
proteins silver-stained polyacrylamide gels. Anal. Chem. 68: 850-858.
Shimoi, H., Kitagaki, H., Ohmori, H., Iimura, Y., and Ito, K. (1998) Sed1p is a major cell wall
protein of Saccharomyces cerevisiae in the stationary phase and is involved in lytic enzyme resistance. J. Bacteriol. 180: 3381-3387.
Simonetti, N., Strippoli, V., and Cassone, A. (1974) Yeast-mycelial conversion induced by
N-acetyl-D-glucosamine in Candida albicans. Nature 250: 344-346.
Singh P., Ghosh S., Datta A. (2001) Attenuation of virulence and changes in morphology in
Candida albicans by disruption of the N-acetylglucosamine catabolic pathway. Infect. Immun. 69:7898–7903.
Skory, C. D. and Freer, S. N. (1995). Cloning and characterization of a gene encoding a cell-bound,
extracellular b-glucosidase in the yeast Candida wickerhamii. Appl. Environ. Microbiol. 61, 518-525.
during growth and development in yeast. Microbiology 147: 781-794.
Smits, G.J., Schenkman, L.R., Brul, S., Pringle, J.R., and Klis, F.M. (2006) Role of cell
cycle-regulated expression in the localized incorporation of cell wall proteins in yeast. Mol. Biol. Cell 17: 3267-3280.
Staab, J.F., Bahn, Y.S., Tai, C.H., Cook, P.F., and Sundstrom, P. (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.
Staab J.F., Bradway, S.D., Fidel, P.L., and Sundstrom, P. (1999) Adhesive and mammalian
transglutaminase substrate properties of Candida albicans Hwp1. Science 283:1535-1538
Sudbery, P., Gow, N., and Berman, J. (2004) The distinct morphogenic states of Candida albicans.
Trends Microbiol. 12:317-324
Sundstrom, P. (2002) Adhesion in Candida spp. Cell Microbiol. 4: 461-469.
Tarcha, E.J., Basrur, V., Hung, C.Y., Gardner, M.J., and Cole, G.T. (2006) Multivalent
recombinant protein vaccine against coccidioidomycosis. Infect. Immun. 74: 5802-5813.
Teparic, R., Stuparevic, I., and Mrsa, V. (2007) Binding assay for incorporation of alkali-extractable
proteins in the Saccharomyces cerevisiae cell wall. Yeast 24: 259-266.
Travassos, L.R. (1985) Sporothrix schenchii. In Fungal dimorphism: with emphasis on fungi
pathogenic for humans. Szaniszlo, P.J. (ed). New York: Plenum, pp. 121-163.
Terashima, H., Fukuchi, S., Nakai, K., Arisawa, M., Hamada, K., Yabuki, N., and Kitada, K.
(2002) Sequence-based approach for identification of cell wall proteins in Saccharomyces cerevisiae. Curr. Genet. 40: 311-316.
Terashima, H., Hamada, K., and Kitada, K. (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.
Tokunaga, M., Kusamichi, M., and Koike, H. (1986) Ultrastructure of outermost layer of cell wall
in Candida albicans observed by rapid-freezing technique. J. Electron Microsc. (Tokyo) 35: 237-246.
Tomishige, N., Noda, Y., Adachi, H., Shimoi, H., and Yoda, K. (2005) SKG1, a suppressor gene of
synthetic lethality of kex2Δgas1Δ mutations, encodes a novel membrane protein that affects cell wall composition. Yeast 22: 141-155.
Urban, C., Xiong, X., Sohn, K., Schroppel, K., Brunner, H., and Rupp, S. (2005) The
moonlighting protein Tsa1p is implicated in oxidative stress response and in cell wall biogenesis in Candida albicans. Mol. Microbiol. 57: 1318-1341.
Van der Vaart, J., Caro, L., Chapman, J., Klis, F., and Verrips, C. (1995) Identification of three
mannoproteins in the cell wall of Saccharomyces cerevisiae. J. Bacteriol. 177: 3104-3110.
Verstrepen, K.J., and Klis, F.M. (2006) Flocculation, adhesion and biofilm formation in yeasts. Mol.
Microbiol. 60: 5-15.
Vossen, J.H., Muller, W.H., Lipke, P.N., and Klis, F.M. (1997) Restrictive
glycosylphosphatidylinositol anchor synthesis in cwh6/gpi3 yeast cells causes aberrant biogenesis of cell wall proteins. J. Bacteriol. 179: 2202-2209.
Waffenschmidt, S., Kusch, T., and Woessner, J.P. (1999) A transglutaminase immunologically
reinhardtii. Plant Physiol. 121: 1003-1015.
Washburn, M.P., Wolters, D., and Yates, J.R., 3rd (2001) Large-scale analysis of the yeast proteome
by multidimensional protein identification technology. Nat. Biotechnol. 19: 242-247.
Weig, M., Gross, U., and Muhlschlegel, F. (1998) Clinical aspects and pathogenesis of Candida
infection. Trends Microbiol. 6: 468-470.
Weig, M., Haynes, K., Rogers, T. R., Kurzai, O., Frosch, M. and Muhlschlegel, F. A. (2001). A
GAS-like gene family in the pathogenic fungus Candida glabrata. Microbiology 147, 2007-2019.
Weig, M., Jansch, L., Gross, U., De Koster, C.G., Klis, F.M., and De Groot, P.W. (2004)
Systematic identification in silico of covalently bound cell wall proteins and analysis of protein-polysaccharide linkages of the human pathogen Candida glabrata. Microbiology 150: 3129-3144.
Weissman, Z., and Kornitzer, D. (2004) A family of Candida cell surface haem-binding proteins
involved in haemin and haemoglobin-iron utilization. Mol. Microbiol. 53: 1209-1220.
Williams, K.; Hochstrasser, D. (1997) Proteome Research: New Frontiers in Functional Genomics.
Edited by Wilkins M, Williams K, Appel R, Hochstrasser D. Berlin: Springer Press. pp. 1–12.
Wu, C.C., MacCoss, M.J., Howell, K.E., Matthews, D.E., and Yates, J.R., 3rd (2004) Metabolic
labeling of mammalian organisms with stable isotopes for quantitative proteomic analysis. Anal. Chem. 76: 4951-4959.
Yin, Q.Y., de Groot, P.W.J., Dekker, H.L., de Jong, L., Klis, F.M., and de Koster, C.G. (2005)
Comprehensive proteomic analysis of Saccharomyces cerevisiae cell walls: identification of proteins covalently attached via glycosylphosphatidylinositol remnants or mild alkali-sensitive linkages. J. Biol. Chem. 280: 20894-20901.
Yin, Q.Y., de Groot, P.W.J., de Jong, L., Klis, F.M., and de Koster, C.G. (2007) Mass
spectrometric quantitation of covalently bound cell wall proteins in Saccharomyces cerevisiae. FEMS Yeast Res. DOI:10.1111/j.1567-1364.2007.00272.x.
Zeng, C., and Biemann, K. (1999) Determination of N-linked glycosylation of yeast external
invertase by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. J. Mass Spectrom. 34: 311-329.
Zhao, X., Daniels, K.J., Oh, S.H., Green, C.B., Yeater, K.M., Soll, D.R., and Hoyer, L.L. (2006)
Candida albicans Als3p is required for wild-type biofilm formation on silicone elastomer surfaces. Microbiology 152: 2287-2299.
Zhu, K., Chi, Z., Li, J., Zhang, F., Li, M., Yasoda, H.N., and Wu, L. (2006) The surface display of
haemolysin from Vibrio harveyi on yeast cells and their potential applications as live vaccine in marine fish. Vaccine 24: 6046-6052.