1887

Abstract

The fungal cell wall is essential in maintaining cellular integrity and plays key roles in the interplay between fungal pathogens and their hosts. The and genes encode two short and related glycosylphosphatidylinositol-anchored cell wall proteins and their expression has been previously shown to be strongly upregulated when the human pathogen grows as biofilms. Using GFP fusion proteins, we have shown that Pga59 and Pga62 are cell-wall-located, - and -glycosylated proteins. The characterization of ΔΔ, ΔΔ and ΔΔ ΔΔ mutants suggested a minor role of these two proteins in hyphal morphogenesis and that they are not critical to biofilm formation. Importantly, the sensitivity to different cell-wall-perturbing agents was altered in these mutants. In particular, simultaneous inactivation of and resulted in high sensitivity to Calcofluor white, Congo red and nikkomicin Z and in resistance to caspofungin. Furthermore, cell wall composition and observation by transmission electron microscopy indicated an altered cell wall structure in the mutant strains. Collectively, these data suggest that the cell wall proteins Pga59 and Pga62 contribute to cell wall stability and structure.

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2009-06-01
2024-12-13
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References

  1. Albrecht A., Felk A., Pichova I., Naglik J. R., Schaller M., de Groot P., Maccallum D., Odds F. C., Schafer W. other authors 2006; Glycosylphosphatidylinositol-anchored proteases of Candida albicans target proteins necessary for both cellular processes and host-pathogen interactions. J Biol Chem 281:688–694
    [Google Scholar]
  2. Bates S., de la Rosa J. M., MacCallum D. M., Brown A. J., Gow N. A., Odds F. C. 2007; Candida albicans Iff11, a secreted protein required for cell wall structure and virulence. Infect Immun 75:2922–2928
    [Google Scholar]
  3. Bauer J., Wendland J. 2007; Candida albicans Sfl1 suppresses flocculation and filamentation. Eukaryot Cell 6:1736–1744
    [Google Scholar]
  4. Boraston A. B., Bolam D. N., Gilbert H. J., Davies G. J. 2004; Carbohydrate-binding modules: fine-tuning polysaccharide recognition. Biochem J 382:769–781
    [Google Scholar]
  5. Braun B. R., Head W. S., Wang M. X., Johnson A. D. 2000; Identification and characterization of TUP1-regulated genes in Candida albicans . Genetics 156:31–44
    [Google Scholar]
  6. Braun B. R., van Het Hoog M., d'Enfert C., Martchenko M., Dungan J., Kuo A., Inglis D. O., Uhl M. A., Hogues H. other authors 2005; A human-curated annotation of the Candida albicans genome. PLoS Genet 1:e1
    [Google Scholar]
  7. Cabib E. 1991; Differential inhibition of chitin synthetases 1 and 2 from Saccharomyces cerevisiae by polyoxin D and nikkomycins. Antimicrob Agents Chemother 35:170–173
    [Google Scholar]
  8. Calera J. A., Calderone R. 1999; Flocculation of hyphae is associated with a deletion in the putative CaHK1 two-component histidine kinase gene from Candida albicans . Microbiology 145:1431–1442
    [Google Scholar]
  9. Cantero P. D., Lengsfeld C., Prill S. K., Subanovic M., Roman E., Pla J., Ernst J. F. 2007; Transcriptional and physiological adaptation to defective protein- O -mannosylation in Candida albicans . Mol Microbiol 64:1115–1128
    [Google Scholar]
  10. 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]
  11. Castillo L., Martinez A. I., Garcera A., Garcia-Martinez J., Ruiz-Herrera J., Valentin E., Sentandreu R. 2006; Genomic response programs of Candida albicans following protoplasting and regeneration. Fungal Genet Biol 43:124–134
    [Google Scholar]
  12. Castillo L., Calvo E., Martinez A. I., Ruiz-Herrera J., Valentin E., Lopez J. A., Sentandreu R. 2008; A study of the Candida albicans cell wall proteome. Proteomics 8:3871–3881
    [Google Scholar]
  13. Christie K. R., Weng S., Balakrishnan R., Costanzo M. C., Dolinski K., Dwight S. S., Engel S. R., Feierbach B., Fisk D. G. other authors 2004; Saccharomyces Genome Database (SGD) provides tools to identify and analyze sequences from Saccharomyces cerevisiae and related sequences from other organisms. Nucleic Acids Res 32:Database issueD311–D314
    [Google Scholar]
  14. Copping V. M., Barelle C. J., Hube B., Gow N. A., Brown A. J., Odds F. C. 2005; Exposure of Candida albicans to antifungal agents affects expression of SAP2 and SAP9 secreted proteinase genes. J Antimicrob Chemother 55:645–654
    [Google Scholar]
  15. Dallies N., Francois J., 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
    [Google Scholar]
  16. d'Enfert C., Goyard S., Rodriguez-Arnaveilhe S., Frangeul L., Jones L., Tekaia F., Bader O., Albrecht A., Castillo L. other authors 2005; CandidaDB: a genome database for Candida albicans pathogenomics. Nucleic Acids Res 33:D353–D357
    [Google Scholar]
  17. De Groot P. W. J., De Boer A. D., Cunningham J., Dekker H. L., De Jong L., Hellingwerf K. J., De Koster C., Klis F. M. 2004; Proteomic analysis of Candida albicans cell walls reveals covalently bound carbohydrate-active enzymes and adhesins. Eukaryot Cell 3:955–965
    [Google Scholar]
  18. De Groot P. W. J., Ram A. F., Klis F. M. 2005; Features and functions of covalently linked proteins in fungal cell walls. Fungal Genet Biol 42:657–675
    [Google Scholar]
  19. De Nobel J. G., Klis F. M., Munnik T., Priem J., van den Ende H. 1990a; An assay of relative cell wall porosity in Saccharomyces cerevisiae , Kluyveromyces lactis and Schizosaccharomyces pombe . Yeast 6:483–490
    [Google Scholar]
  20. De Nobel J. G., Klis F. M., Priem J., Munnik T., van den Ende H. 1990b; The glucanase-soluble mannoproteins limit cell wall porosity in Saccharomyces cerevisiae . Yeast 6:491–499
    [Google Scholar]
  21. Douglas L. J. 2003; Candida biofilms and their role in infection. Trends Microbiol 11:30–36
    [Google Scholar]
  22. Dujon B., Sherman D., Fischer G., Durrens P., Casaregola S., Lafontaine I., De Montigny J., Marck C., Neuveglise C. other authors 2004; Genome evolution in yeasts. Nature 430:35–44
    [Google Scholar]
  23. Dunkler A., Walther A., Specht C. A., Wendland J. 2005; Candida albicans CHT3 encodes the functional homolog of the Cts1 chitinase of Saccharomyces cerevisiae . Fungal Genet Biol 42:935–947
    [Google Scholar]
  24. Enloe B., Diamond A., Mitchell A. P. 2000; A single-transformation gene function test in diploid Candida albicans . J Bacteriol 182:5730–5736
    [Google Scholar]
  25. Firon A., Aubert S., Iraqui I., Guadagnini S., Goyard S., Prevost M. C., Janbon G., d'Enfert C. 2007; The SUN41 and SUN42 genes are essential for cell separation in Candida albicans . Mol Microbiol 66:1256–1275
    [Google Scholar]
  26. Fonzi W. A., Irwin M. Y. 1993; Isogenic strain construction and gene mapping in Candida albicans . Genetics 134:717–728
    [Google Scholar]
  27. Frieman M. B., 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
    [Google Scholar]
  28. Frieman M. B., 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
    [Google Scholar]
  29. Garcia-Sanchez S., Aubert S., Iraqui I., Janbon G., Ghigo J. M., d'Enfert C. 2004; Candida albicans biofilms: a developmental state associated with specific and stable gene expression patterns. Eukaryot Cell 3:536–545
    [Google Scholar]
  30. Garcia-Sanchez S., Mavor A. L., Russell C. L., Argimon S., Dennison P., Enjalbert B., Brown A. J. 2005; Global roles of Ssn6 in Tup1- and Nrg1-dependent gene regulation in the fungal pathogen, Candida albicans . Mol Biol Cell 16:2913–2925
    [Google Scholar]
  31. Gerami-Nejad M., Berman J., Gale C. A. 2001; Cassettes for PCR-mediated construction of green, yellow, and cyan fluorescent protein fusions in Candida albicans . Yeast 18:859–864
    [Google Scholar]
  32. Gillum A. M., Tsay E. Y., 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
    [Google Scholar]
  33. Goffeau A., Dufour J. P. 1988; Plasma membrane ATPase from the yeast Saccharomyces cerevisiae . Methods Enzymol 157:528–533
    [Google Scholar]
  34. Gola S., Martin R., Walther A., Dunkler A., Wendland J. 2003; New modules for PCR-based gene targeting in Candida albicans : rapid and efficient gene targeting using 100 bp of flanking homology region. Yeast 20:1339–1347
    [Google Scholar]
  35. Goyard S., Knechtle P., Chauvel M., Mallet A., Prevost M. C., Proux C., Coppee J. Y., Schwartz P., Dromer F. other authors 2008; The Yak1 kinase is involved in the initiation and maintenance of hyphal growth in Candida albicans . Mol Biol Cell 19:2251–2266
    [Google Scholar]
  36. Granger B. L., Flenniken M. L., Davis D. A., Mitchell A. P., Cutler J. E. 2005; Yeast wall protein 1 of Candida albicans . Microbiology 151:1631–1644
    [Google Scholar]
  37. Hamada K., Terashima H., Arisawa M., Yabuki N., 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
    [Google Scholar]
  38. Harcus D., Nantel A., Marcil A., Rigby T., Whiteway M. 2004; Transcription profiling of cyclic AMP signaling in Candida albicans . Mol Biol Cell 15:4490–4499
    [Google Scholar]
  39. Herth W. 1980; Calcofluor white and Congo red inhibit chitin microfibril assembly of Poterioochromonas : evidence for a gap between polymerization and microfibril formation. J Cell Biol 87:442–450
    [Google Scholar]
  40. Honraet K., Goetghebeur E., Nelis H. J. 2005; Comparison of three assays for the quantification of Candida biomass in suspension and CDC reactor grown biofilms. J Microbiol Methods 63:287–295
    [Google Scholar]
  41. Imai K., Noda Y., Adachi H., Yoda K. 2005; A novel endoplasmic reticulum membrane protein Rcr1 regulates chitin deposition in the cell wall of Saccharomyces cerevisiae . J Biol Chem 280:8275–8284
    [Google Scholar]
  42. Jeffries T. W., Grigoriev I. V., Grimwood J., Laplaza J. M., Aerts A., Salamov A., Schmutz J., Lindquist E., Dehal P. other authors 2007; Genome sequence of the lignocellulose-bioconverting and xylose-fermenting yeast Pichia stipitis . Nat Biotechnol 25:319–326
    [Google Scholar]
  43. Kapteyn J. C., Montijn R. C., Vink E., de la Cruz J., Llobell A., Douwes J. E., Shimoi H., Lipke P. N., Klis F. M. 1996; Retention of Saccharomyces cerevisiae cell wall proteins through a phosphodiester-linked β -1,3-/ β -1,6-glucan heteropolymer. Glycobiology 6:337–345
    [Google Scholar]
  44. Kapteyn J. C., Hoyer L. L., Hecht J. E., Muller W. H., Andel A., Verkleij A. J., Makarow M., Van Den Ende H., Klis F. M. 2000; The cell wall architecture of Candida albicans wild-type cells and cell wall-defective mutants. Mol Microbiol 35:601–611
    [Google Scholar]
  45. Kapteyn J. C., ter Riet B., Vink E., Blad S., De Nobel H., Van Den Ende H., 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
    [Google Scholar]
  46. Klis F. M., de Groot P., Hellingwerf K. 2001; Molecular organization of the cell wall of Candida albicans . Med Mycol 39:Suppl 11–8
    [Google Scholar]
  47. Klis F. M., Boorsma A., De Groot P. W. 2006; Cell wall construction in Saccharomyces cerevisiae . Yeast 23:185–202
    [Google Scholar]
  48. Kollar R., Reinhold B. B., Petrakova E., Yeh H. J., Ashwell G., Drgonova J., Kapteyn J. C., Klis F. M., Cabib E. 1997; Architecture of the yeast cell wall. Beta(1 – >6)-glucan interconnects mannoprotein, β (1→)3-glucan, and chitin. J Biol Chem 272:17762–17775
    [Google Scholar]
  49. Kurtz M. B., Douglas C. M. 1997; Lipopeptide inhibitors of fungal glucan synthase. J Med Vet Mycol 35:79–86
    [Google Scholar]
  50. Lan C. Y., Rodarte G., Murillo L. A., Jones T., Davis R. W., Dungan J., Newport G., Agabian N. 2004; Regulatory networks affected by iron availability in Candida albicans . Mol Microbiol 53:1451–1469
    [Google Scholar]
  51. Latge J. P. 2007; The cell wall: a carbohydrate armour for the fungal cell. Mol Microbiol 66:279–290
    [Google Scholar]
  52. Lee K. L., Buckley H. R., Campbell C. C. 1975; An amino acid liquid synthetic medium for the development of mycelial and yeast forms of Candida albicans . Sabouraudia 13:148–153
    [Google Scholar]
  53. Lesage G., Bussey H. 2006; Cell wall assembly in Saccharomyces cerevisiae . Microbiol Mol Biol Rev 70:317–343
    [Google Scholar]
  54. Li F., Palecek S. P. 2003; EAP1 , a Candida albicans gene involved in binding human epithelial cells. Eukaryot Cell 2:1266–1273
    [Google Scholar]
  55. Li F., Palecek S. P. 2008; Distinct domains of the Candida albicans adhesin Eap1p mediate cell-cell and cell-substrate interactions. Microbiology 154:1193–1203
    [Google Scholar]
  56. Li Y., Su C., Mao X., Cao F., Chen J. 2007; Roles of Candida albicans Sfl1 in hyphal development. Eukaryot Cell 6:2112–2121
    [Google Scholar]
  57. Liu H., Kohler J., Fink G. R. 1994; Suppression of hyphal formation in Candida albicans by mutation of a STE12 homolog. Science 266:1723–1726
    [Google Scholar]
  58. Lo H. J., Köhler J. R., DiDomenico B., Loebenberg D., Cacciapuoti A., Fink G. R. 1997; Nonfilamentous C. albicans mutants are avirulent. Cell 90:939–949
    [Google Scholar]
  59. Mao Y., Zhang Z., Gast C., Wong B. 2008; C-terminal signals regulate targeting of glycosylphosphatidylinositol-anchored proteins to the cell wall or plasma membrane in Candida albicans . Eukaryot Cell 7:1906–1915
    [Google Scholar]
  60. Martín-Cuadrado A. B., Encinar del Dedo J. E., de Medina-Redondo M., Fontaine T., del Rey F., Latgé J. P., Vázquez de Aldana C. R. 2008; The Schizosaccharomyces pombe endo-1,3- β -glucanase Eng1 contains a novel carbohydrate binding module required for septum localization. Mol Microbiol 69:188–200
    [Google Scholar]
  61. McCreath K. J., Specht C. A., Robbins P. W. 1995; Molecular cloning and characterization of chitinase genes from Candida albicans . Proc Natl Acad Sci U S A 92:2544–2548
    [Google Scholar]
  62. Murad A. M., Lee P. R., Broadbent I. D., Barelle C. J., Brown A. J. 2000; CIp10, an efficient and convenient integrating vector for Candida albicans . Yeast 16:325–327
    [Google Scholar]
  63. Netea M. G., Gow N. A., Munro C. A., Bates S., Collins C., Ferwerda G., Hobson R. P., Bertram G., Hughes H. B. other authors 2006; Immune sensing of Candida albicans requires cooperative recognition of mannans and glucans by lectin and Toll-like receptors. J Clin Invest 116:1642–1650
    [Google Scholar]
  64. Niimi K., Harding D. R., Parshot R., King A., Lun D. J., Decottignies A., Niimi M., Lin S., Cannon R. D. other authors 2004; Chemosensitization of fluconazole resistance in Saccharomyces cerevisiae and pathogenic fungi by a d-octapeptide derivative. Antimicrob Agents Chemother 48:1256–1271
    [Google Scholar]
  65. Plaine A., Walker L., Da Costa G., Mora-Montes H. M., McKinnon A., Gow N. A., Gaillardin C., Munro C. A., Richard M. L. 2008; Functional analysis of Candida albicans GPI-anchored proteins: roles in cell wall integrity and caspofungin sensitivity. Fungal Genet Biol 45:1404–1414
    [Google Scholar]
  66. Popolo L., Gualtieri T., Ragni E. 2001; The yeast cell-wall salvage pathway. Med Mycol 39:Suppl 1111–121
    [Google Scholar]
  67. Popolo L., Ragni E., Carotti C., Palomares O., Aardema R., Back J. W., Dekker H. L., de Koning L. J., de Jong L., de Koster C. G. 2008; Disulfide bond structure and domain organization of yeast β (1,3)-glucanosyltransferases involved in cell wall biogenesis. J Biol Chem 283:18553–18565
    [Google Scholar]
  68. Ragni E., Sipiczki M., Strahl S. 2007; Characterization of Ccw12p, a major key player in cell wall stability of Saccharomyces cerevisiae . Yeast 24:309–319
    [Google Scholar]
  69. Ramage G., VandeWalle K., Lopez-Ribot J. L., Wickes B. L. 2002; The filamentation pathway controlled by the Efg1 regulator protein is required for normal biofilm formation and development in Candida albicans . FEMS Microbiol Lett 214:95–100
    [Google Scholar]
  70. Reuss O., Vik A., Kolter R., Morschhauser J. 2004; The SAT1 flipper, an optimized tool for gene disruption in Candida albicans . Gene 341:119–127
    [Google Scholar]
  71. Richard M. L., Plaine A. 2007; Comprehensive analysis of glycosylphosphatidylinositol-anchored proteins in Candida albicans . Eukaryot Cell 6:119–133
    [Google Scholar]
  72. Richard M., De Groot P., Courtin O., Poulain D., Klis F., Gaillardin C. 2002a; GPI7 affects cell-wall protein anchorage in Saccharomyces cerevisiae and Candida albicans . Microbiology 148:2125–2133
    [Google Scholar]
  73. Richard M., Ibata-Ombetta S., Dromer F., Bordon-Pallier F., Jouault T., Gaillardin C. 2002b; Complete glycosylphosphatidylinositol anchors are required in Candida albicans for full morphogenesis, virulence and resistance to macrophages. Mol Microbiol 44:841–853
    [Google Scholar]
  74. Richard M. L., Nobile C. J., Bruno V. M., Mitchell A. P. 2005; Candida albicans biofilm-defective mutants. Eukaryot Cell 4:1493–1502
    [Google Scholar]
  75. Rossignol T., Lechat P., Cuomo C., Zeng Q., Moszer I., d'Enfert C. 2008; CandidaDB: a multi-genome database for Candida species and related Saccharomycotina. Nucleic Acids Res 36:D557–D561
    [Google Scholar]
  76. Ruiz-Herrera J., Elorza M. V., Valentin E., Sentandreu R. 2006; Molecular organization of the cell wall of Candida albicans and its relation to pathogenicity. FEMS Yeast Res 6:14–29
    [Google Scholar]
  77. Saville S. P., Lazzell A. L., Monteagudo C., Lopez-Ribot J. L. 2003; Engineered control of cell morphology in vivo reveals distinct roles for yeast and filamentous forms of Candida albicans during infection. Eukaryot Cell 2:1053–1060
    [Google Scholar]
  78. Sharp P. M., Li W. H. 1987; The codon Adaptation Index – a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res 15:1281–1295
    [Google Scholar]
  79. Shen J., Guo W., Köhler J. R. 2005; CaNAT1 , a heterologous dominant selectable marker for transformation of Candida albicans and other pathogenic Candida species. Infect Immun 73:1239–1242
    [Google Scholar]
  80. Sohn K., Urban C., Brunner H., Rupp S. 2003; EFG1 is a major regulator of cell wall dynamics in Candida albicans as revealed by DNA microarrays. Mol Microbiol 47:89–102
    [Google Scholar]
  81. Sosinska G. J., de Groot P. W., Teixeira de Mattos M. J., Dekker H. L., de Koster C. G., Hellingwerf K. J., Klis F. M. 2008; Hypoxic conditions and iron restriction affect the cell-wall proteome of Candida albicans grown under vagina-simulative conditions. Microbiology 154:510–520
    [Google Scholar]
  82. 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]
  83. Stevens D. A., Espiritu M., Parmar R. 2004; Paradoxical effect of caspofungin: reduced activity against Candida albicans at high drug concentrations. Antimicrob Agents Chemother 48:3407–3411
    [Google Scholar]
  84. Stevens D. A., Ichinomiya M., Koshi Y., Horiuchi H. 2006; Escape of Candida from caspofungin inhibition at concentrations above the MIC (paradoxical effect) accomplished by increased cell wall chitin; evidence for β -1,6-glucan synthesis inhibition by caspofungin. Antimicrob Agents Chemother 50:3160–3161
    [Google Scholar]
  85. Stoldt V. R., Sonneborn A., Leuker C. E., Ernst J. F. 1997; Efg1p, an essential regulator of morphogenesis of the human pathogen Candida albicans , is a member of a conserved class of bHLH proteins regulating morphogenetic processes in fungi. EMBO J 16:1982–1991
    [Google Scholar]
  86. St Onge R. P., Mani R., Oh J., Proctor M., Fung E., Davis R. W., Nislow C., Roth F. P., Giaever G. 2007; Systematic pathway analysis using high-resolution fitness profiling of combinatorial gene deletions. Nat Genet 39:199–206
    [Google Scholar]
  87. Sundstrom P. 2002; Adhesion in Candida spp. Cell Microbiol 4:461–469
    [Google Scholar]
  88. Thomas J. R., Dwek R. A., Rademacher T. W. 1990; Structure, biosynthesis, and function of glycosylphosphatidylinositols. Biochemistry 29:5413–5422
    [Google Scholar]
  89. Tiede A., Bastisch I., Schubert J., Orlean P., Schmidt R. E. 1999; Biosynthesis of glycosylphosphatidylinositols in mammals and unicellular microbes. Biol Chem 380:503–523
    [Google Scholar]
  90. van der Vaart J. M., van Schagen F. S., Mooren A. T., Chapman J. W., Klis F. M., Verrips C. T. 1996; The retention mechanism of cell wall proteins in Saccharomyces cerevisiae . Wall-bound Cwp2p is β -1,6-glucosylated. Biochim Biophys Acta 1291:206–214
    [Google Scholar]
  91. Walker L. A., Munro C. A., de Bruijn I., Lenardon M. D., McKinnon A., Gow N. A. 2008; Stimulation of chitin synthesis rescues Candida albicans from echinocandins. PLoS Pathog 4:e1000040
    [Google Scholar]
  92. Walther A., Wendland J. 2003; An improved transformation protocol for the human fungal pathogen Candida albicans . Curr Genet 42:339–343
    [Google Scholar]
  93. Wang Q., Zhou S., Chen J. Y. 1999; Functions of CRK1 gene of Candida albicans as studied by gene knock-out. Sheng Wu Hua Xue Yu Sheng Wu Wu Li Xue Bao (Shanghai 31:545–552
    [Google Scholar]
  94. Wiederhold N. P., Kontoyiannis D. P., Prince R. A., Lewis R. E. 2005; Attenuation of the activity of caspofungin at high concentrations against Candida albicans : possible role of cell wall integrity and calcineurin pathways. Antimicrob Agents Chemother 49:5146–5148
    [Google Scholar]
  95. Wilson R. B., Davis D., Mitchell A. P. 1999; Rapid hypothesis testing with Candida albicans through gene disruption with short homology regions. J Bacteriol 181:1868–1874
    [Google Scholar]
  96. Wu G., Culley D. E., Zhang W. 2005; Predicted highly expressed genes in the genomes of Streptomyces coelicolor and Streptomyces avermitilis and the implications for their metabolism. Microbiology 151:2175–2187
    [Google Scholar]
  97. Yin Q. Y., de Groot P. W., Dekker H. L., de Jong L., Klis F. M., 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
    [Google Scholar]
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