1887

Abstract

The ability of to switch from yeast to hyphal growth is essential for its virulence. The walls and especially the covalently attached wall proteins are involved in the primary host–pathogen interactions. Three hyphal induction methods were compared, based on fetal calf serum, the amino sugar -acetylglucosamine (GlcNAc) and the mammalian cell culture medium Iscove’s modified Dulbecco’s medium (IMDM). GlcNAc and IMDM were preferred, allowing stable hyphal growth over a prolonged period without significant reversion to yeast growth and with high biomass yields. We employed Fourier transform-MS combined with a N-metabolically labelled reference culture as internal standard for relative quantification of changes in the wall proteome upon hyphal induction. A total of 21 wall proteins were quantified. Our induction methods triggered a similar response characterized by (i) a category of wall proteins showing strongly increased incorporation levels (Als3, Hwp2, Hyr1, Plb5 and Sod5), (ii) another category with strongly decreased levels (Rhd3, Sod4 and Ywp1) and (iii) a third one enriched for carbohydrate-active enzymes (including Cht2, Crh11, Mp65, Pga4, Phr1, Phr2 and Utr2) and showing only a limited response. This is, to our knowledge, the first systematic, quantitative analysis of the changes in the wall proteome of upon hyphal induction. Finally, we propose new wall-protein-derived candidates for vaccine development.

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2011-08-01
2019-11-17
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References

  1. Almeida R. S. , Brunke S. , Albrecht A. , Thewes S. , Laue M. , Edwards J. E. , Filler S. G. , Hube B. . ( 2008; ). The hyphal-associated adhesin and invasin Als3 of Candida albicans mediates iron acquisition from host ferritin. . PLoS Pathog 4:, e1000217. [CrossRef].[PubMed].
    [Google Scholar]
  2. Alsteens D. , Garcia M. C. , Lipke P. N. , Dufrêne Y. F. . ( 2010; ). Force-induced formation and propagation of adhesion nanodomains in living fungal cells. . Proc Natl Acad Sci U S A 107:, 20744–20749. [CrossRef].[PubMed].
    [Google Scholar]
  3. Alvarez F. J. , Konopka J. B. . ( 2007; ). Identification of an N-acetylglucosamine transporter that mediates hyphal induction in Candida albicans . . Mol Biol Cell 18:, 965–975. [CrossRef].[PubMed].
    [Google Scholar]
  4. Argimón S. , Wishart J. A. , Leng R. , Macaskill S. , Mavor A. , Alexandris T. , Nicholls S. , Knight A. W. , Enjalbert B. et al. ( 2007; ). Developmental regulation of an adhesin gene during cellular morphogenesis in the fungal pathogen Candida albicans . . Eukaryot Cell 6:, 682–692. [CrossRef].[PubMed].
    [Google Scholar]
  5. Bailey D. A. , Feldmann P. J. , Bovey M. , Gow N. A. , Brown A. J. . ( 1996; ). The Candida albicans HYR1 gene, which is activated in response to hyphal development, belongs to a gene family encoding yeast cell wall proteins. . J Bacteriol 178:, 5353–5360.[PubMed].
    [Google Scholar]
  6. Biswas S. , Van Dijck P. , Datta A. . ( 2007; ). Environmental sensing and signal transduction pathways regulating morphopathogenic determinants of Candida albicans . . Microbiol Mol Biol Rev 71:, 348–376. [CrossRef].[PubMed].
    [Google Scholar]
  7. Braun B. R. , Johnson A. D. . ( 2000; ). TUP1, CPH1 and EFG1 make independent contributions to filamentation in Candida albicans . . Genetics 155:, 57–67.[PubMed].
    [Google Scholar]
  8. 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.[PubMed].
    [Google Scholar]
  9. Brena S. , Omaetxebarría M. J. , Elguezabal N. , Cabezas J. , Moragues M. D. , Pontón J. . ( 2007; ). Fungicidal monoclonal antibody C7 binds to Candida albicans Als3. . Infect Immun 75:, 3680–3682. [CrossRef].[PubMed].
    [Google Scholar]
  10. Bromuro C. , Torosantucci A. , Gomez M. J. , Urbani F. , Cassone A. . ( 1994; ). Differential release of an immunodominant 65 kDa mannoprotein antigen from yeast and mycelial forms of Candida albicans . . J Med Vet Mycol 32:, 447–459. [CrossRef].[PubMed].
    [Google Scholar]
  11. Cantarel B. L. , Coutinho P. M. , Rancurel C. , Bernard T. , Lombard V. , Henrissat B. . ( 2009; ). The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. . Nucleic Acids Res 37: Database issue D233–D238. [CrossRef].[PubMed].
    [Google Scholar]
  12. Castilla R. , Passeron S. , Cantore M. L. . ( 1998; ). N-acetyl-d-glucosamine induces germination in Candida albicans through a mechanism sensitive to inhibitors of cAMP-dependent protein kinase. . Cell Signal 10:, 713–719. [CrossRef].[PubMed].
    [Google Scholar]
  13. Castillo L. , Calvo E. , Martínez A. I. , Ruiz-Herrera J. , Valentín E. , Lopez J. A. , Sentandreu R. . ( 2008; ). A study of the Candida albicans cell wall proteome. . Proteomics 8:, 3871–3881. [CrossRef].[PubMed].
    [Google Scholar]
  14. Chandra J. , Kuhn D. M. , Mukherjee P. K. , Hoyer L. L. , McCormick T. , Ghannoum M. A. . ( 2001; ). Biofilm formation by the fungal pathogen Candida albicans: development, architecture, and drug resistance. . J Bacteriol 183:, 5385–5394. [CrossRef].[PubMed].
    [Google Scholar]
  15. Coleman D. A. , Oh S. H. , Zhao X. , Hoyer L. L. . ( 2010; ). Heterogeneous distribution of Candida albicans cell-surface antigens demonstrated with an Als1-specific monoclonal antibody. . Microbiology 156:, 3645–3659.[CrossRef]
    [Google Scholar]
  16. De Bernardis F. , Mühlschlegel 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:, 3317–3325.[PubMed].
    [Google Scholar]
  17. de Boer A. D. , de Groot P. W. , Weindl G. , Schaller M. , Riedel D. , Diez-Orejas R. , Klis F. M. , de Koster C. G. , Dekker H. L. et al. ( 2010; ). The Candida albicans cell wall protein Rhd3/Pga29 is abundant in the yeast form and contributes to virulence. . Yeast 27:, 611–624. [CrossRef].[PubMed].
    [Google Scholar]
  18. de Groot P. W. , 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. [CrossRef].[PubMed].
    [Google Scholar]
  19. De Groot P. W. , Ram A. F. , Klis F. M. . ( 2005; ). Features and functions of covalently linked proteins in fungal cell walls. . Fungal Genet Biol 42:, 657–675. [CrossRef].[PubMed].
    [Google Scholar]
  20. de Koning L. J. , Kasper P. T. , Back J. W. , Nessen M. A. , Vanrobaeys F. , Van Beeumen J. , Gherardi E. , de Koster C. G. , de Jong L. . ( 2006; ). Computer-assisted mass spectrometric analysis of naturally occurring and artificially introduced cross-links in proteins and protein complexes. . FEBS J 273:, 281–291. [CrossRef].[PubMed].
    [Google Scholar]
  21. Desjardins P. , Hansen J. B. , Allen M. . ( 2009; ). Microvolume spectrophotometric and fluorometric determination of protein concentration. . Curr Protoc Protein Sci Chapter 3:, 3– , 10.[PubMed].
    [Google Scholar]
  22. Ecker M. , Deutzmann R. , Lehle L. , Mrsa V. , Tanner W. . ( 2006; ). Pir proteins of Saccharomyces cerevisiae are attached to β-1,3-glucan by a new protein-carbohydrate linkage. . J Biol Chem 281:, 11523–11529. [CrossRef].[PubMed].
    [Google Scholar]
  23. Eisenhaber B. , Schneider G. , Wildpaner M. , 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. [CrossRef].[PubMed].
    [Google Scholar]
  24. Emanuelsson O. , Brunak S. , von Heijne G. , Nielsen H. . ( 2007; ). Locating proteins in the cell using TargetP, SignalP and related tools. . Nat Protoc 2:, 953–971. [CrossRef].[PubMed].
    [Google Scholar]
  25. Fradin C. , De Groot P. , MacCallum D. , Schaller M. , Klis F. , Odds F. C. , Hube B. . ( 2005; ). Granulocytes govern the transcriptional response, morphology and proliferation of Candida albicans in human blood. . Mol Microbiol 56:, 397–415. [CrossRef].[PubMed].
    [Google Scholar]
  26. Frohner I. E. , Bourgeois C. , Yatsyk K. , Majer O. , Kuchler K. . ( 2009; ). Candida albicans cell surface superoxide dismutases degrade host-derived reactive oxygen species to escape innate immune surveillance. . Mol Microbiol 71:, 240–252. [CrossRef].[PubMed].
    [Google Scholar]
  27. Gil-Navarro I. , Gil M. L. , Casanova M. , O’Connor J. E. , Martínez J. P. , Gozalbo D. . ( 1997; ). The glycolytic enzyme glyceraldehyde-3-phosphate dehydrogenase of Candida albicans is a surface antigen. . J Bacteriol 179:, 4992–4999.[PubMed].
    [Google Scholar]
  28. 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. [CrossRef].[PubMed].
    [Google Scholar]
  29. Gomez M. J. , Torosantucci A. , Arancia S. , Maras B. , Parisi L. , Cassone A. . ( 1996; ). Purification and biochemical characterization of a 65-kilodalton mannoprotein (MP65), a main target of anti-Candida cell-mediated immune responses in humans. . Infect Immun 64:, 2577–2584.[PubMed].
    [Google Scholar]
  30. 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. [CrossRef].[PubMed].
    [Google Scholar]
  31. Green C. B. , Cheng G. , Chandra J. , Mukherjee P. , Ghannoum M. A. , Hoyer L. L. . ( 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. [CrossRef].[PubMed].
    [Google Scholar]
  32. Hayek P. , Dib L. , Yazbeck P. , Beyrouthy B. , Khalaf R. A. . ( 2010; ). Characterization of Hwp2, a Candida albicans putative GPI-anchored cell wall protein necessary for invasive growth. . Microbiol Res 165:, 250–258. [CrossRef].[PubMed].
    [Google Scholar]
  33. Heijnis W. H. , Dekker H. L. , de Koning L. J. , Wierenga P. A. , Westphal A. H. , de Koster C. G. , Gruppen H. , van Berkel W. J. . ( 2011; ). Identification of the peroxidase-generated intermolecular dityrosine cross-link in bovine α-lactalbumin. . J Agric Food Chem 59:, 444–449. [CrossRef].[PubMed].
    [Google Scholar]
  34. Hoyer L. L. , Payne T. L. , Bell M. , Myers A. M. , Scherer S. . ( 1998; ). Candida albicans ALS3 and insights into the nature of the ALS gene family. . Curr Genet 33:, 451–459. [CrossRef].[PubMed].
    [Google Scholar]
  35. Ibrahim A. S. , Mirbod F. , Filler S. G. , Banno Y. , Cole G. T. , Kitajima Y. , Edwards J. E. Jr , Nozawa Y. , Ghannoum M. A. . ( 1995; ). Evidence implicating phospholipase as a virulence factor of Candida albicans . . Infect Immun 63:, 1993–1998.[PubMed].
    [Google Scholar]
  36. Kadosh D. , 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. [CrossRef].[PubMed].
    [Google Scholar]
  37. Kasper P. T. , Back J. W. , Vitale M. , Hartog A. F. , Roseboom W. , de Koning L. J. , van Maarseveen J. H. , Muijsers A. O. , de Koster C. G. , de Jong L. . ( 2007; ). An aptly positioned azido group in the spacer of a protein cross-linker for facile mapping of lysines in close proximity. . ChemBioChem 8:, 1281–1292. [CrossRef].[PubMed].
    [Google Scholar]
  38. Klis F. M. , Sosinska G. J. , de Groot P. W. , Brul S. . ( 2009; ). Covalently linked cell wall proteins of Candida albicans and their role in fitness and virulence. . FEMS Yeast Res 9:, 1013–1028. [CrossRef].[PubMed].
    [Google Scholar]
  39. Klis F. M. , Brul S. , De Groot P. W. . ( 2010; ). Covalently linked wall proteins in ascomycetous fungi. . Yeast 27:, 489–493. [CrossRef].[PubMed].
    [Google Scholar]
  40. Kulkarni R. D. , Kelkar H. S. , Dean R. A. . ( 2003; ). An eight-cysteine-containing CFEM domain unique to a group of fungal membrane proteins. . Trends Biochem Sci 28:, 118–121. [CrossRef].[PubMed].
    [Google Scholar]
  41. Lehmann E. L. , D’Abrera H. J. M. . ( 1975; ). Nonparametrics: Statistical Methods Based on Ranks. San Francisco:: McGraw-Hill International Book Co;.
    [Google Scholar]
  42. 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. [CrossRef].[PubMed].
    [Google Scholar]
  43. Lorenz M. C. , Bender J. A. , Fink G. R. . ( 2004; ). Transcriptional response of Candida albicans upon internalization by macrophages. . Eukaryot Cell 3:, 1076–1087. [CrossRef].[PubMed].
    [Google Scholar]
  44. Luo G. , Ibrahim A. S. , Spellberg B. , Nobile C. J. , Mitchell A. P. , Fu Y. . ( 2010; ). Candida albicans Hyr1p confers resistance to neutrophil killing and is a potential vaccine target. . J Infect Dis 201:, 1718–1728. [CrossRef].[PubMed].
    [Google Scholar]
  45. Maidan M. M. , Thevelein J. M. , 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. [CrossRef].[PubMed].
    [Google Scholar]
  46. Martchenko M. , Alarco A. M. , Harcus D. , 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. [CrossRef].[PubMed].
    [Google Scholar]
  47. Martínez A. I. , Castillo L. , Garcerá A. , Elorza M. V. , Valentín E. , Sentandreu R. . ( 2004; ). Role of Pir1 in the construction of the Candida albicans cell wall. . Microbiology 150:, 3151–3161. [CrossRef].[PubMed].
    [Google Scholar]
  48. Monteoliva L. , Martinez-Lopez R. , Pitarch A. , Hernaez M. L. , Serna A. , Nombela C. , Albar J. P. , Gil C. . ( 2011; ). Quantitative proteome and acidic subproteome profiling of Candida albicans yeast-to-hypha transition. . J Proteome Res 10:, 502–517. [CrossRef].[PubMed].
    [Google Scholar]
  49. Müller M. Q. , de Koning L. J. , Schmidt A. , Ihling C. , Syha Y. , Rau O. , Mechtler K. , Schubert-Zsilavecz M. , Sinz A. . ( 2009; ). An innovative method to study target protein–drug interactions by mass spectrometry. . J Med Chem 52:, 2875–2879. [CrossRef].[PubMed].
    [Google Scholar]
  50. Naglik J. , Albrecht A. , Bader O. , Hube B. . ( 2004; ). Candida albicans proteinases and host/pathogen interactions. . Cell Microbiol 6:, 915–926. [CrossRef].[PubMed].
    [Google Scholar]
  51. Nantel A. , Dignard D. , Bachewich C. , Harcus D. , Marcil A. , Bouin A. P. , Sensen C. W. , Hogues H. , van het Hoog M. et al. ( 2002; ). Transcription profiling of Candida albicans cells undergoing the yeast-to-hyphal transition. . Mol Biol Cell 13:, 3452–3465. [CrossRef].[PubMed].
    [Google Scholar]
  52. Nobile C. J. , Mitchell A. P. . ( 2005; ). Regulation of cell-surface genes and biofilm formation by the C. albicans transcription factor Bcr1p. . Curr Biol 15:, 1150–1155. [CrossRef].[PubMed].
    [Google Scholar]
  53. Nobile C. J. , Andes D. R. , Nett J. E. , Smith F. J. , Yue F. , Phan Q. T. , Edwards J. E. , Filler S. G. , Mitchell A. P. . ( 2006; ). Critical role of Bcr1-dependent adhesins in C. albicans biofilm formation in vitro and in vivo. . PLoS Pathog 2:, e63. [CrossRef].[PubMed].
    [Google Scholar]
  54. Oda Y. , Huang K. , Cross F. R. , Cowburn D. , Chait B. T. . ( 1999; ). Accurate quantitation of protein expression and site-specific phosphorylation. . Proc Natl Acad Sci U S A 96:, 6591–6596. [CrossRef].[PubMed].
    [Google Scholar]
  55. Otoo H. N. , Lee K. G. , Qiu W. , Lipke P. N. . ( 2008; ). Candida albicans Als adhesins have conserved amyloid-forming sequences. . Eukaryot Cell 7:, 776–782. [CrossRef].[PubMed].
    [Google Scholar]
  56. Pérez A. , Pedrós B. , Murgui A. , Casanova M. , López-Ribot J. L. , Martínez J. P. . ( 2006; ). Biofilm formation by Candida albicans mutants for genes coding fungal proteins exhibiting the eight-cysteine-containing CFEM domain. . FEMS Yeast Res 6:, 1074–1084. [CrossRef].[PubMed].
    [Google Scholar]
  57. 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. [CrossRef].[PubMed].
    [Google Scholar]
  58. 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. [CrossRef].[PubMed].
    [Google Scholar]
  59. Ramsook C. B. , Tan C. , Garcia M. C. , Fung R. , Soybelman G. , Henry R. , Litewka A. , O’Meally S. , Otoo H. N. et al. ( 2010; ). Yeast cell adhesion molecules have functional amyloid-forming sequences. . Eukaryot Cell 9:, 393–404. [CrossRef].[PubMed].
    [Google Scholar]
  60. Richard M. L. , Plaine A. . ( 2007; ). Comprehensive analysis of glycosylphosphatidylinositol-anchored proteins in Candida albicans . . Eukaryot Cell 6:, 119–133. [CrossRef].[PubMed].
    [Google Scholar]
  61. Schaller M. , Borelli C. , Korting H. C. , Hube B. . ( 2005; ). Hydrolytic enzymes as virulence factors of Candida albicans . . Mycoses 48:, 365–377. [CrossRef].[PubMed].
    [Google Scholar]
  62. Silverman R. J. , Nobbs A. H. , Vickerman M. M. , Barbour M. E. , Jenkinson H. F. . ( 2010; ). Interaction of Candida albicans cell wall Als3 protein with Streptococcus gordonii SspB adhesin promotes development of mixed-species communities. . Infect Immun 78:, 4644–4652. [CrossRef].[PubMed].
    [Google Scholar]
  63. Simonetti N. , Strippoli V. , Cassone A. . ( 1974; ). Yeast–mycelial conversion induced by N-acetyl-d-glucosamine in Candida albicans . . Nature 250:, 344–346. [CrossRef].[PubMed].
    [Google Scholar]
  64. Skrzypek M. S. , Arnaud M. B. , Costanzo M. C. , Inglis D. O. , Shah P. , Binkley G. , Miyasato S. R. , Sherlock G. . ( 2010; ). New tools at the Candida Genome Database: biochemical pathways and full-text literature search. . Nucleic Acids Res 38: Database issue D428–D432. [CrossRef].[PubMed].
    [Google Scholar]
  65. 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. [CrossRef].[PubMed].
    [Google Scholar]
  66. Sorgo A. G. , Heilmann C. J. , Dekker H. L. , Brul S. , de Koster C. G. , Klis F. M. . ( 2010; ). Mass spectrometric analysis of the secretome of Candida albicans . . Yeast 27:, 661–672. [CrossRef].[PubMed].
    [Google Scholar]
  67. Sorgo A. G. , Heilmann C. J. , Dekker H. L. , Bekker M. , Brul S. , de Koster C. G. , de Koning C. J. , Klis F. M. . ( 2011; ). The effects of fluconazole on the secretome, the wall proteome and wall integrity of the clinical fungus Candida albicans. Eukaryot Cell . doi:10.1128/EC.05011-11 (in press).
    [Google Scholar]
  68. Sosinska G. J. , de Koning L. J. , de Groot P. W. , Manders E. M. , Dekker H. L. , Hellingwerf K. J. , de Koster C. G. , Klis F. M. . ( 2011; ). Mass spectrometric quantification of the adaptations in the wall proteome of Candida albicans in response to ambient pH. . Microbiology 157:, 136–146. [CrossRef].[PubMed].
    [Google Scholar]
  69. Spellberg B. J. , Ibrahim A. S. , Avanesian V. , Fu Y. , Myers C. , Phan Q. T. , Filler S. G. , Yeaman M. R. , Edwards J. E. Jr . ( 2006; ). Efficacy of the anti-Candida rAls3p-N or rAls1p-N vaccines against disseminated and mucosal candidiasis. . J Infect Dis 194:, 256–260. [CrossRef].[PubMed].
    [Google Scholar]
  70. 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. [CrossRef].[PubMed].
    [Google Scholar]
  71. Theiss S. , Ishdorj G. , Brenot A. , Kretschmar M. , Lan C. Y. , Nichterlein T. , Hacker J. , Nigam S. , Agabian N. , Köhler G. A. . ( 2006; ). Inactivation of the phospholipase B gene PLB5 in wild-type Candida albicans reduces cell-associated phospholipase A2 activity and attenuates virulence. . Int J Med Microbiol 296:, 405–420. [CrossRef].[PubMed].
    [Google Scholar]
  72. Urban C. , Sohn K. , Lottspeich F. , Brunner H. , Rupp S. . ( 2003; ). Identification of cell surface determinants in Candida albicans reveals Tsa1p, a protein differentially localized in the cell. . FEBS Lett 544:, 228–235. [CrossRef].[PubMed].
    [Google Scholar]
  73. Weissman Z. , Kornitzer D. . ( 2004; ). A family of Candida cell surface haem-binding proteins involved in haemin and haemoglobin-iron utilization. . Mol Microbiol 53:, 1209–1220. [CrossRef].[PubMed].
    [Google Scholar]
  74. Weissman Z. , Shemer R. , Conibear E. , Kornitzer D. . ( 2008; ). An endocytic mechanism for haemoglobin–iron acquisition in Candida albicans . . Mol Microbiol 69:, 201–217. [CrossRef].[PubMed].
    [Google Scholar]
  75. Wheeler R. T. , Fink G. R. . ( 2006; ). A drug-sensitive genetic network masks fungi from the immune system. . PLoS Pathog 2:, e35. [CrossRef].[PubMed].
    [Google Scholar]
  76. Wheeler R. T. , Kombe D. , Agarwala S. D. , Fink G. R. . ( 2008; ). Dynamic, morphotype-specific Candida albicans β-glucan exposure during infection and drug treatment. . PLoS Pathog 4:, e1000227. [CrossRef].[PubMed].
    [Google Scholar]
  77. Wisplinghoff H. , Bischoff T. , Tallent S. M. , Seifert H. , Wenzel R. P. , Edmond M. B. . ( 2004; ). Nosocomial bloodstream in US hospitals: analysis of 24,179 cases from a prospective nationwide surveillance study. . Clin Infect Dis 39:, 309–317. [CrossRef].[PubMed].
    [Google Scholar]
  78. Xu X. L. , Lee R. T. , Fang H. M. , Wang Y. M. , Li R. , Zou H. , Zhu Y. , Wang Y. . ( 2008; ). Bacterial peptidoglycan triggers Candida albicans hyphal growth by directly activating the adenylyl cyclase Cyr1p. . Cell Host Microbe 4:, 28–39. [CrossRef].[PubMed].
    [Google Scholar]
  79. 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. [CrossRef].[PubMed].
    [Google Scholar]
  80. 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. [CrossRef].[PubMed].
    [Google Scholar]
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vol. , part 8, pp. 2297 - 2307

Peptides used for SP-protein quantification for IMDM grown cells at 37°C for 18h.

All identified peptide pairs.

MS-MS identified peptides in N reference culture.

Peptides used for FT-MS mass calibration.

Peptide pairs used for relative protein quantification for YNB-S grown cells at 30°C for 18h.

Peptide pairs used for relative protein quantification for YNB-S grown cells at 37°C for 18h.

Peptide pairs used for relative protein quantification for YNB-S+10% FCS grown cells at 37°C for 18h.

Peptide pairs used for relative protein quantification for YNB-S+5mM GlcNAc grown cells at 37°C for 18h.

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