Identification of virulence determinants of the human pathogenic fungi Aspergillus fumigatus and Candida albicans by proteomics

International Journal of Medical Microbiology

Volumn 301, Issue 5, 2011, Pages 368-377

  Kniemeyer, Olaf ^a,b   Schmidt, André D ^a,b   Vödisch, Martin ^a,b   Wartenberg, Dirk ^a,b   Brakhage, Axel A ^a,b  

^a HANS KNÖLL INSTITUTE   (Germany)

^b FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

Author keywords

Aspergillus fumigatus; Candida albicans; Mass spectrometry; Pathogenicity; Proteomics; Two dimensional gel electrophoresis

Indexed keywords

ANTIFUNGAL AGENT; FUNGAL PROTEIN; PROTEOME;

ASPERGILLUS FUMIGATUS; CANDIDA ALBICANS; EARLY DIAGNOSIS; ENTOMOPATHOGENIC FUNGUS; ENVIRONMENTAL CHANGE; FUNGAL VIRULENCE; FUNGUS IDENTIFICATION; GEL ELECTROPHORESIS; GENE SEQUENCE; HUMAN; LIQUID CHROMATOGRAPHY; MOLECULAR INTERACTION; NONHUMAN; OXIDATIVE STRESS; PROTEOMICS; SHORT SURVEY;

ASPERGILLUS FUMIGATUS; CANDIDA ALBICANS; CHROMATOGRAPHY, LIQUID; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; HUMANS; MASS SPECTROMETRY; PROTEOMICS; VIRULENCE; VIRULENCE FACTORS;

EID: 79956372535     PISSN: 14384221     EISSN: 16180607     Source Type: Journal    
DOI: 10.1016/j.ijmm.2011.04.001     Document Type: Short Survey

References (122)

1. Aebersold R., Mann M. Mass spectrometry-based proteomics. Nature 2003, 422:198-207.
2. Albrecht D., Guthke R., Brakhage A.A., Kniemeyer O. Integrative analysis of the heat shock response in Aspergillus fumigatus. BMC Genomics 2010, 11:32.
3. Albrecht D., Kniemeyer O., Brakhage A.A., Guthke R. Missing values in gel-based proteomics. Proteomics 2010, 10:1202-1211.
4. Almeida R.S., Wilson D., Hube B. Candida albicans iron acquisition within the host. FEMS Yeast Res. 2009, 9:1000-1012.
5. Andersen M.R., Nielsen J. Current status of systems biology in Aspergilli. Fungal Genet. Biol. 2009, 46:S180-S190.
6. Angiolella L., Vitali A., Stringaro A., Mignogna G., Maras B., Bonito M., Colone M., Palamara A.T., Cassone A. Localisation of Bgl2p upon antifungal drug treatment in Candida albicans. Int. J. Antimicrob. Agents 2009, 33:143-148.
7. Arnaud M.B., Costanzo M.C., Skrzypek M.S., Binkley G., Lane C., Miyasato S.R., Sherlock G. The Candida Genome Database (CGD), a community resource for Candida albicans gene and protein information. Nucleic Acids Res. 2005, 33:D358-D363.
8. Arnaud M.B., Chibucos M.C., Costanzo M.C., Crabtree J., Inglis D.O., Lotia A., Orvis J., Shah P., Skrzypek M.S., Binkley G., Miyasato S.R., Wortman J.R., Sherlock G. The Aspergillus Genome Database, a curated comparative genomics resource for gene, protein and sequence information for the Aspergillus research community. Nucleic Acids Res. 2010, 38:D420-D427.
9. Asif A.R., Oellerich M., Amstrong V.W., Riemenschneider B., Monod M., Reichard U. Proteome of conidial surface associated proteins of Aspergillus fumigatus reflecting potential vaccine candidates and allergens. J. Proteome Res. 2006, 5:954-962.
10. Asif A.R., Oellerich M., Amstrong V.W., Gross U., Reichard U. Analysis of the cellular Aspergillus fumigatus proteome that reacts with sera from rabbits developing an acquired immunity after experimental aspergillosis. Electrophoresis 2010, 31:1947-1958.
11. Barea P.L., Calvo E., Rodriguez J.A., Rementeria A., Calcedo R., Sevilla M.J., Ponton J., Hernando F.L. Characterization of Candida albicans antigenic determinants by two-dimensional polyacrylamide gel electrophoresis and enhanced chemiluminescence. FEMS Immunol. Med. Microbiol. 1999, 23:343-354.
12. Bhabhra R., Askew D.S. Thermotolerance and virulence of Aspergillus fumigatus: role of the fungal nucleolus. Med. Mycol. 2005, 43(Suppl. 1):S87-S93.
13. Brakhage A.A., Andrianopoulos A., Kato M., Steidl S., Davis M.A., Tsukagoshi N., Hynes M.J. HAP-like CCAAT-binding complexes in filamentous fungi: implications for biotechnology. Fungal Genet. Biol. 1999, 27:243-252.
14. Brakhage A.A., Bruns S., Thywissen A., Zipfel P.F., Behnsen J. Interaction of phagocytes with filamentous fungi. Curr. Opin. Microbiol. 2010, 13:409-415.
15. Braun B.R., van Het Hoog M., d'Enfert C., Martchenko M., Dungan J., Kuo A., Inglis D.O., Uhl M.A., Hogues H., Berriman M., Lorenz M., Levitin A., Oberholzer U., Bachewich C., Harcus D., Marcil A., Dignard D., Iouk T., Zito R., Frangeul L., Tekaia F., Rutherford K., Wang E., Munro C.A., Bates S., Gow N.A., Hoyer L.L., Kohler G., Morschhauser J., Newport G., Znaidi S., Raymond M., Turcotte B., Sherlock G., Costanzo M., Ihmels J., Berman J., Sanglard D., Agabian N., Mitchell A.P., Johnson A.D., Whiteway M., Nantel A. A human-curated annotation of the Candida albicans genome. PLoS Genet. 2005, 1:36-57.
16. Bruneau J.M., Magnin T., Tagat E., Legrand R., Bernard M., Diaquin M., Fudali C., Latge J.P. Proteome analysis of Aspergillus fumigatus identifies glycosylphosphatidylinositol-anchored proteins associated to the cell wall biosynthesis. Electrophoresis 2001, 22:2812-2823.
17. Bruns S., Seidler M., Albrecht D., Salvenmoser S., Remme N., Hertweck C., Brakhage A.A., Kniemeyer O., Müller F.-M. Functional genomic profiling of Aspergillus fumigatus biofilm reveals enhanced production of the mycotoxin gliotoxin. Proteomics 2010, 10:3097-3107.
18. Cabezon V., Llama-Palacios A., Nombela C., Monteoliva L., Gil C. Analysis of Candida albicans plasma membrane proteome. Proteomics 2009, 9:4770-4786.
19. Carberry S., Neville C.M., Kavanagh K.A., Doyle S. Analysis of major intracellular proteins of Aspergillus fumigatus by MALDI mass spectrometry: identification and characterisation of an elongation factor 1B protein with glutathione transferase activity. Biochem. Biophys. Res. Commun. 2006, 341:1096-1104.
20. Castillo L., Calvo E., Martinez A.I., Ruiz-Herrera J., Valentin E., Lopez J.A., Sentandreu R. A study of the Candida albicans cell wall proteome. Proteomics 2008, 8:3871-3881.
21. Chaffin W.L. Candida albicans cell wall proteins. Microbiol. Mol. Biol. Rev. 2008, 72:495-544.
22. Chhillar A.K., Yadav V., Kumar A., Kumar M., Parmar V.S., Prasad A., Sharma G.L. Differential expression of Aspergillus fumigatus protein in response to treatment with a novel antifungal compound, diethyl 4-(4-methoxyphenyl)-2,6-dimethyl-1,4-dihydropyridin-3,5-dicarboxylate. Mycoses 2009, 52:223-227.
23. D'Enfert C., Goyard S., Rodriguez-Arnaveilhe S., Frangeul L., Jones L., Tekaia F., Bader O., Albrecht A., Castillo L., Dominguez A., Ernst J.F., Fradin C., Gaillardin C., Garcia-Sanchez S., de Groot P., Hube B., Klis F.M., Krishnamurthy S., Kunze D., Lopez M.C., Mavor A., Martin N., Moszer I., Onesime D., Perez Martin J., Sentandreu R., Valentin E., Brown A.J. CandidaDB: a genome database for Candida albicans pathogenomics. Nucleic Acids Res. 2005, 33:D353-D357.
24. Dabur R., Mandal T.K., Sharma G.L. Post-antifungal effects of the antifungal compound 2-(3,4-dimethyl-2,5-dihydro-1H-pyrrol-2-yl)-1-methylethyl pentanoate on Aspergillus fumigatus. J. Med. Microbiol. 2007, 56:815-818.
25. De Backer M.D., de Hoogt R.A., Froyen G., Odds F.C., Simons F., Contreras R., Luyten W.H. Single allele knock-out of Candida albicans CGT1 leads to unexpected resistance to hygromycin B and elevated temperature. Microbiology 2000, 146:353-365.
26. de Godoy L.M., Olsen J.V., Cox J., Nielsen M.L., Hubner N.C., Fröhlich F., Walther T.C., Mann M. Comprehensive mass-spectrometry-based proteome quantification of haploid versus diploid yeast. Nature 2008, 455:1251-1254.
27. De Groot P.W., Hellingwerf K.J., Klis F.M. Genome-wide identification of fungal GPI proteins. Yeast 2003, 20:781-796.
28. 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. Proteomic analysis of Candida albicans cell walls reveals covalently bound carbohydrate-active enzymes and adhesins. Eukaryot. Cell 2004, 3:955-965.
29. Diez-Orejas R., Fernandez-Arenas E. Candida albicans-macrophage interactions: genomic and proteomic insights. Future Microbiol. 2008, 3:661-681.
30. Do J.H., Yamaguchi R., Miyano S. Exploring temporal transcription regulation structure of Aspergillus fumigatus in heat shock by state space model. BMC Genomics 2009, 10:306.
31. Domon B., Aebersold R. Options and considerations when selecting a quantitative proteomics strategy. Nat. Biotechnol. 2010, 28:710-721.
32. Duncan M.W., Aebersold R., Caprioli R.M. The pros and cons of peptide-centric proteomics. Nat. Biotechnol. 2010, 28:659-664.
33. Ebanks R.O., Chisholm K., McKinnon S., Whiteway M., Pinto D.M. Proteomic analysis of Candida albicans yeast and hyphal cell wall and associated proteins. Proteomics 2006, 6:2147-2156.
34. Elias J.E., Haas W., Faherty B.K., Gygi S.P. Comparative evaluation of mass spectrometry platforms used in large-scale proteomics investigations. Nat. Methods 2005, 2:667-675.
35. Fernandez-Arenas E., Molero G., Nombela C., Diez-Orejas R., Gil C. Contribution of the antibodies response induced by a low virulent Candida albicans strain in protection against systemic candidiasis. Proteomics 2004, 4:1204-1215.
36. Fernandez-Arenas E., Molero G., Nombela C., Diez-Orejas R., Gil C. Low virulent strains of Candida albicans: unravelling the antigens for a future vaccine. Proteomics 2004, 4:3007-3020.
37. Fernandez-Arenas E., Cabezon V., Bermejo C., Arroyo J., Nombela C., Diez-Orejas R., Gil C. Integrated proteomics and genomics strategies bring new insight into Candida albicans response upon macrophage interaction. Mol. Cell Proteomics 2007, 6:460-478.
38. Gastebois A., Clavaud C., Aimanianda V., Latge J.P. Aspergillus fumigatus: cell wall polysaccharides, their biosynthesis and organization. Future Microbiol. 2009, 4:583-595.
39. Gautam P., Sundaram C.S., Madan T., Gade W.N., Shah A., Sirdeshmukh R., Sarma P.U. Identification of novel allergens of Aspergillus fumigatus using immunoproteomics approach. Clin. Exp. Allergy 2007, 37:1239-1249.
40. Gautam P., Shankar J., Madan T., Sirdeshmukh R., Sundaram C.S., Gade W.N., Basir S.F., Sarma P.U. Proteomic and transcriptomic analysis of Aspergillus fumigatus on exposure to amphotericin B. Antimicrob. Agents Chemother. 2008, 52:4220-4227.
41. Glaser A.G., Kirsch A.I., Zeller S., Menz G., Rhyner C., Crameri R. Molecular and immunological characterization of Asp f 34, a novel major cell wall allergen of Aspergillus fumigatus. Allergy 2009, 64:1144-1151.
42. Görg A., Drews O., Luck C., Weiland F., Weiss W. 2-DE with IPGs. Electrophoresis 2009, 30(Suppl. 1):S122-S132.
43. Grosse C., Heinekamp T., Kniemeyer O., Gehrke A., Brakhage A.A. Protein kinase A regulates growth, sporulation, and pigment formation in Aspergillus fumigatus. Appl. Environ. Microbiol. 2008, 74:4923-4933.
44. Gstaiger M., Aebersold R. Applying mass spectrometry-based proteomics to genetics, genomics and network biology. Nat. Rev. Genet. 2009, 10:617-627.
45. Hernaez M.L., Ximenez-Embun P., Martinez-Gomariz M., Gutierrez-Blazquez M.D., Nombela C., Gil C. Identification of Candida albicans exposed surface proteins in vivo by a rapid proteomic approach. J. Proteomics 2010, 73:1404-1409.
46. Hernando F.L., Calvo E., Abad A., Ramirez A., Rementeria A., Sevilla M.J., Ponton J. Identification of protein and mannoprotein antigens of Candida albicans of relevance for the serodiagnosis of invasive candidiasis. Int. Microbiol. 2007, 10:103-108.
47. Hortschansky P., Eisendle M., Al-Abdallah Q., Schmidt A.D., Bergmann S., Thön M., Kniemeyer O., Abt B., Seeber B., Werner E.R., Kato M., Brakhage A.A., Haas H. Interaction of HapX with the CCAAT-binding complex-a novel mechanism of gene regulation by iron. EMBO J. 2007, 26:3157-3168.
48. Jones T., Federspiel N.A., Chibana H., Dungan J., Kalman S., Magee B.B., Newport G., Thorstenson Y.R., Agabian N., Magee P.T., Davis R.W., Scherer S. The diploid genome sequence of Candida albicans. Proc. Natl. Acad. Sci. USA 2004, 101:7329-7334.
49. Kim K.H., Brown K.M., Harris P.V., Langston J.A., Cherry J.R. A proteomics strategy to discover beta-glucosidases from Aspergillus fumigatus with two-dimensional page in-gel activity assay and tandem mass spectrometry. J. Proteome Res. 2007, 6:4749-4757.
50. Kim Y., Nandakumar M.P., Marten M.R. The state of proteome profiling in the fungal genus Aspergillus. Brief. Funct. Genomic Proteomic 2008, 7:87-94.
51. Klose J. Protein mapping by combined isoelectric focusing and electrophoresis of mouse tissues. A novel approach to testing for induced point mutations in mammals. Humangenetik 1975, 26:231-243.
52. Kniemeyer O., Lessing F., Scheibner O., Hertweck C., Brakhage A.A. Optimisation of a 2-D gel electrophoresis protocol for the human-pathogenic fungus Aspergillus fumigatus. Curr. Genet. 2006, 49:178-189.
53. Kniemeyer O., Brakhage A.A. Proteomics and its application to the human-pathogenic fungi. Human and Animal Relationships: The Mycota VI 2008, vol. VI:154-186. Springer, Berlin.
54. Kniemeyer O., Lessing F., Brakhage A.A. Proteome analysis for pathogenicity and new diagnostic markers for Aspergillus fumigatus. Med. Mycol. 2009, 47(Suppl. 1):S248-S254.
55. Kusch H., Biswas K., Schwanfelder S., Engelmann S., Rogers P.D., Hecker M., Morschhauser J. A proteomic approach to understanding the development of multidrug-resistant Candida albicans strains. Mol. Genet. Genomics 2004, 271:554-565.
56. Kusch H., Engelmann S., Albrecht D., Morschhäuser J., Hecker M. Proteomic analysis of the oxidative stress response in Candida albicans. Proteomics 2007, 7:686-697.
57. Kusch H., Engelmann S., Bode R., Albrecht D., Morschhäuser J., Hecker M. A proteomic view of Candida albicans yeast cell metabolism in exponential and stationary growth phases. Int. J. Med. Microbiol. 2008, 298:291-318.
58. Lass-Flörl C., Perkhofer S., Mayr A. In vitro susceptibility testing in fungi: a global perspective on a variety of methods. Mycoses 2010, 53:1-11.
59. Latge J.P., Mouyna I., Tekaia F., Beauvais A., Debeaupuis J.P., Nierman W. Specific molecular features in the organization and biosynthesis of the cell wall of Aspergillus fumigatus. Med. Mycol. 2005, 43(Suppl. 1):S15-S22.
60. Latge J.P. The cell wall: a carbohydrate armour for the fungal cell. Mol. Microbiol. 2007, 66:279-290.
61. Lenardon M.D., Milne S.A., Mora-Montes H.M., Kaffarnik F.A., Peck S.C., Brown A.J., Munro C.A., Gow N.A. Phosphorylation regulates polarisation of chitin synthesis in Candida albicans. J. Cell. Sci. 2010, 123:2199-2206.
62. Lessing F., Kniemeyer O., Wozniok I., Loeffler J., Kurzai O., Haertl A., Brakhage A.A. The Aspergillus fumigatus transcriptional regulator AfYap1 represents the major regulator for defense against reactive oxygen intermediates but is dispensable for pathogenicity in an intranasal mouse infection model. Eukaryot. Cell 2007, 6:2290-2302.
63. Leventakos K., Lewis R.E., Kontoyiannis D.P. Fungal infections in leukemia patients: how do we prevent and treat them?. Clin. Infect. Dis. 2010, 50:405-415.
64. Lis M., Bobek L.A. Proteomic and metabolic characterization of a Candida albicans mutant resistant to the antimicrobial peptide MUC7 12-mer. FEMS Immunol. Med. Microbiol. 2008, 54:80-91.
65. Luo S., Poltermann S., Kunert A., Rupp S., Zipfel P.F. Immune evasion of the human pathogenic yeast Candida albicans: Pra1 is a factor H, FHL-1 and plasminogen binding surface protein. Mol. Immunol. 2009, 47:541-550.
66. Mabey J.E., Anderson M.J., Giles P.F., Miller C.J., Attwood T.K., Paton N.W., Bornberg-Bauer E., Robson G.D., Oliver S.G., Denning D.W. CADRE: the Central Aspergillus Data REpository. Nucleic Acids Res. 2004, 32:D401-D405.
67. Maddi A., Bowman S.M., Free S.J. Trifluoromethanesulfonic acid-based proteomic analysis of cell wall and secreted proteins of the ascomycetous fungi Neurospora crassa and Candida albicans. Fungal Genet. Biol. 2009, 46:768-781.
68. Mann M., Kelleher N.L. Precision proteomics: the case for high resolution and high mass accuracy. Proc. Natl. Acad. Sci. USA 2008, 105:18132-18138.
69. Manning M., Mitchell T.G. Analysis of cytoplasmic antigens of the yeast and mycelial phases of Candida albicans by two-dimensional electrophoresis. Infect. Immun. 1980, 30:484-495.
70. Marinach C., Alanio A., Palous M., Kwasek S., Fekkar A., Brossas J.Y., Brun S., Snounou G., Hennequin C., Sanglard D., Datry A., Golmard J.L., Mazier D. MALDI-TOF MS-based drug susceptibility testing of pathogens: the example of Candida albicans and fluconazole. Proteomics 2009, 9:4627-4631.
71. Martinez-Gomariz M., Perumal P., Mekala S., Nombela C., Chaffin W.L., Gil C. Proteomic analysis of cytoplasmic and surface proteins from yeast cells, hyphae, and biofilms of Candida albicans. Proteomics 2009, 9:2230-2252.
72. Martinez-Lopez R., Nombela C., Diez-Orejas R., Monteoliva L., Gil C. Immunoproteomic analysis of the protective response obtained from vaccination with Candida albicans ecm33 cell wall mutant in mice. Proteomics 2008, 8:2651-2664.
73. Martinez-Solano L., Nombela C., Molero G., Gil C. Differential protein expression of murine macrophages upon interaction with Candida albicans. Proteomics 2006, 6(Suppl. 1):S133-S144.
74. Martinez-Solano L., Reales-Calderon J.A., Nombela C., Molero G., Gil C. Proteomics of RAW 264.7 macrophages upon interaction with heat-inactivated Candida albicans cells unravel an anti-inflammatory response. Proteomics 2009, 9:2995-3010.
75. Miethke M., Marahiel M.A. Siderophore-based iron acquisition and pathogen control. Microbiol. Mol. Biol. Rev. 2007, 71:413-451.
76. Minden J.S., Dowd S.R., Meyer H.E., Stuhler K. Difference gel electrophoresis. Electrophoresis 2009, 30(Suppl. 1):S156-S161.
77. Morio F., Loge C., Besse B., Hennequin C., Le Pape P. Screening for amino acid substitutions in the Candida albicans Erg11 protein of azole-susceptible and azole-resistant clinical isolates: new substitutions and a review of the literature. Diagn. Microbiol. Infect. Dis. 2010, 66:373-384.
78. Mouyna I., Kniemeyer O., Jank T., Loussert C., Mellado E., Aimanianda V., Beauvais A., Wartenberg D., Sarfati J., Bayry J., Prevost M.C., Brakhage A.A., Strahl S., Huerre M., Latge J.P. Members of protein O-mannosyltransferase family in Aspergillus fumigatus differentially affect growth, morphogenesis and viability. Mol. Microbiol. 2010, 76:1205-1221.
79. Mukherjee P.K., Mohamed S., Chandra J., Kuhn D., Liu S., Antar O.S., Munyon R., Mitchell A.P., Andes D., Chance M.R., Rouabhia M., Ghannoum M.A. Alcohol dehydrogenase restricts the ability of the pathogen Candida albicans to form a biofilm on catheter surfaces through an ethanol-based mechanism. Infect. Immun. 2006, 74:3804-3816.
80. Netea M.G., Brown G.D., Kullberg B.J., Gow N.A. An integrated model of the recognition of Candida albicans by the innate immune system. Nat. Rev. Microbiol. 2008, 6:67-78.
81. Nicholls S., Leach M.D., Priest C.L., Brown A.J. Role of the heat shock transcription factor, Hsf1, in a major fungal pathogen that is obligately associated with warm-blooded animals. Mol. Microbiol. 2009, 74:844-861.
82. Nierman W.C., Pain A., Anderson M.J., Wortman J.R., Kim H.S., Arroyo J., Berriman M., Abe K., Archer D.B., Bermejo C., Bennett J., Bowyer P., Chen D., Collins M., Coulsen R., Davies R., Dyer P.S., Farman M., Fedorova N., Feldblyum T.V., Fischer R., Fosker N., Fraser A., García J.L., García M.J., Goble A., Goldman G.H., Gomi K., Griffith-Jones S., Gwilliam R., Haas B., Haas H., Harris D., Horiuchi H., Huang J., Humphray S., Jiménez J., Keller N., Khouri H., Kitamoto K., Kobayashi T., Konzack S., Kulkarni R., Kumagai T., Lafon A., Latgé J.P., Li W., Lord A., Lu C., Majoros W.H., May G.S., Miller B.L., Mohamoud Y., Molina M., Monod M., Mouyna I., Mulligan S., Murphy L., O'Neil S., Paulsen I., Peñalva M.A., Pertea M., Price C., Pritchard B.L., Quail M.A., Rabbinowitsch E., Rawlins N., Rajandream M.A., Reichard U., Renauld H., Robson G.D., Rodríguez de Cordoba S., Rodríguez-Peña J.M., Ronning C.M., Rutter S., Salzberg S.L., Sanchez M., Sánchez-Ferrero J.C., Saunders D., Seeger K., Squares R., Squares S., Takeuchi M., Tekaia F., Turner G., Vazquez de Aldana C.R., Weidman J., White O., Woodward J., Yu J.H., Fraser C., Galagan J.E., Asai K., Machida M., Hall N., Barrell B., Denning D.W. Genomic sequence of the pathogenic and allergenic filamentous fungus Aspergillus fumigatus. Nature 2005, 438:1151-1156.
83. Nobile C.J., Nett J.E., Hernday A.D., Homann O.R., Deneault J.S., Nantel A., Andes D.R., Johnson A.D., Mitchell A.P. Biofilm matrix regulation by Candida albicans Zap1. PLoS Biol. 2009, 7:e1000133.
84. O'Farrell P.H. High resolution two-dimensional electrophoresis of proteins. J. Biol. Chem. 1975, 250:4007-4021.
85. Ouyang H., Luo Y., Zhang L., Li Y., Jin C. Proteome analysis of Aspergillus fumigatus total membrane proteins identifies proteins associated with the glycoconjugates and cell wall biosynthesis using 2D LC-MS/MS. Mol. Biotechnol. 2010, 44:177-189.
86. Paramonova E., Krom B.P., van der Mei H.C., Busscher H.J., Sharma P.K. Hyphal content determines the compression strength of Candida albicans biofilms. Microbiology 2009, 155:1997-2003.
87. Pardo M., Ward M., Pitarch A., Sanchez M., Nombela C., Blackstock W., Gil C. Cross-species identification of novel Candida albicans immunogenic proteins by combination of two-dimensional polyacrylamide gel electrophoresis and mass spectrometry. Electrophoresis 2000, 21:2651-2659.
88. Picotti P., Bodenmiller B., Mueller L.N., Domon B., Aebersold R. Full dynamic range proteome analysis of S. cerevisiae by targeted proteomics. Cell 2009, 138:795-806.
89. Pitarch A., Pardo M., Jimenez A., Pla J., Gil C., Sanchez M., Nombela C. Two-dimensional gel electrophoresis as analytical tool for identifying Candida albicans immunogenic proteins. Electrophoresis 1999, 20:1001-1010.
90. Pitarch A., Sanchez M., Nombela C., Gil C. Sequential fractionation and two-dimensional gel analysis unravels the complexity of the dimorphic fungus Candida albicans cell wall proteome. Mol. Cell. Proteomics 2002, 1:967-982.
91. Rabilloud T. Membrane proteins and proteomics: love is possible, but so difficult. Electrophoresis 2009, 30(Suppl. 1):S174-S180.
92. Rabilloud T., Vaezzadeh A.R., Potier N., Lelong C., Leize-Wagner E., Chevallet M. Power and limitations of electrophoretic separations in proteomics strategies. Mass Spectrom. Rev. 2009, 28:816-843.
93. Ramage G., VandeWalle K., Lopez-Ribot J.L., Wickes B.L. The filamentation pathway controlled by the Efg1 regulator protein is required for normal biofilm formation and development in Candida albicans. FEMS Microbiol. Lett. 2002, 214:95-100.
94. Ramage G., Mowat E., Jones B., Williams C., Lopez-Ribot J. Our current understanding of fungal biofilms. Crit. Rev. Microbiol. 2009, 35:340-355.
95. Righetti P.G., Castagna A., Antonioli P., Boschetti E. Prefractionation techniques in proteome analysis: the mining tools of the third millennium. Electrophoresis 2005, 26:297-319.
96. Rupp S. Proteomics on its way to study host-pathogen interaction in Candida albicans. Curr. Opin. Microbiol. 2004, 7:330-335.
97. Rupp S. Transcriptomics and proteomics to identify virulence mechanisms in Candida albicans and screening for new antifungals. Mycoses 2008, 51:397.
98. Schmaler-Ripcke J., Sugareva V., Gebhardt P., Winkler R., Kniemeyer O., Heinekamp T., Brakhage A.A. Production of pyomelanin, a second type of melanin, via the tyrosine degradation pathway in Aspergillus fumigatus. Appl. Environ. Microbiol. 2009, 75:493-503.
99. Schmidt A., Claassen M., Aebersold R. Directed mass spectrometry: towards hypothesis-driven proteomics. Curr. Opin. Chem. Biol. 2009, 13:510-517.
100. Schrettl M., Bignell E., Kragl C., Joechl C., Rogers T., Arst H.N., Haynes K., Haas H. Siderophore biosynthesis but not reductive iron assimilation is essential for Aspergillus fumigatus virulence. J. Exp. Med. 2004, 200:1213-1219.
101. Schrettl M., Bignell E., Kragl C., Sabiha Y., Loss O., Eisendle M., Wallner A., Arst H.N., Haynes K., Haas H. Distinct roles for intra- and extracellular siderophores during Aspergillus fumigatus infection. PLoS Pathog. 2007, 3:1195-1207.
102. Segal A.W. How neutrophils kill microbes. Annu. Rev. Immunol. 2005, 23:197-223.
103. Seneviratne C.J., Wang Y., Jin L., Abiko Y., Samaranayake L.P. Candida albicans biofilm formation is associated with increased anti-oxidative capacities. Proteomics 2008, 8:2936-2947.
104. Shapiro R.S., Uppuluri P., Zaas A.K., Collins C., Senn H., Perfect J.R., Heitman J., Cowen L.E. Hsp90 orchestrates temperature-dependent Candida albicans morphogenesis via Ras1-PKA signaling. Curr. Biol. 2009, 19:621-629.
105. Shin Y.K., Kim K.Y., Paik Y.K. Alterations of protein expression in macrophages in response to Candida albicans infection. Mol. Cells 2005, 20:271-279.
106. 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. Hypoxic conditions and iron restriction affect the cell-wall proteome of Candida albicans grown under vagina-simulative conditions. Microbiology 2008, 154:510-520.
107. Speers A.E., Wu C.C. Proteomics of integral membrane proteins-theory and application. Chem. Rev. 2007, 107:3687-3714.
108. Sugiyama K., Izawa S., Inoue Y. The Yap1p-dependent induction of glutathione synthesis in heat shock response of Saccharomyces cerevisiae. J. Biol. Chem. 2000, 275:15535-15540.
109. Teutschbein J., Albrecht D., Potsch M., Guthke R., Aimanianda V., Clavaud C., Latgé J.P., Brakhage A.A., Kniemeyer O. Proteome profiling and functional classification of intracellular proteins from conidia of the human-pathogenic mold Aspergillus fumigatus. J. Proteome Res. 2010, 9:3724-3742.
110. Thomas D.P., Bachmann S.P., Lopez-Ribot J.L. Proteomics for the analysis of the Candida albicans biofilm lifestyle. Proteomics 2006, 6:5795-5804.
111. Thön M., Al Abdallah Q., Hortschansky P., Scharf D.H., Eisendle M., Haas H., Brakhage A.A. The CCAAT-binding complex coordinates the oxidative stress response in eukaryotes. Nucleic Acids Res. 2010, 38:1098-1113.
112. Verweij P.E., Howard S.J., Melchers W.J., Denning D.W. Azole-resistance in Aspergillus: proposed nomenclature and breakpoints. Drug Resist. Updat. 2009, 12:141-147.
113. Vialas V., Nogales-Cadenas R., Nombela C., Pascual-Montano A., Gil C. Proteopathogen, a protein database for studying Candida albicans-host interaction. Proteomics 2009, 9:4664-4668.
114. Vödisch M., Albrecht D., Lessing F., Schmidt A.D., Winkler R., Guthke R., Brakhage A.A., Kniemeyer O. Two-dimensional proteome reference maps for the human pathogenic filamentous fungus Aspergillus fumigatus. Proteomics 2009, 9:1407-1415.
115. Wilkins M.R., Sanchez J.C., Gooley A.A., Appel R.D., Humphery-Smith I., Hochstrasser D.F., Williams K.L. Progress with proteome projects: why all proteins expressed by a genome should be identified and how to do it. Biotechnol. Genet. Eng. Rev. 1996, 13:19-50.
116. Xu Y., Wang Y., Yan L., Liang R.M., Dai B.D., Tang R.J., Gao P.H., Jiang Y.Y. Proteomic analysis reveals a synergistic mechanism of fluconazole and berberine against fluconazole-resistant Candida albicans: endogenous ROS augmentation. J. Proteome Res. 2009, 8:5296-5304.
117. Yan L., Zhang J.D., Cao Y.B., Gao P.H., Jiang Y.Y. Proteomic analysis reveals a metabolism shift in a laboratory fluconazole-resistant Candida albicans strain. J. Proteome Res. 2007, 6:2248-2256.
118. Yates J.R., Carmack E., Hays L., Link A.J., Eng J.K. Automated protein identification using microcolumn liquid chromatography-tandem mass spectrometry. Methods Mol. Biol. 1999, 112:553-569.
119. Yates J.R. Proteomics power to the people. The Scientist 2005, 19:30.
120. Yin Z., Stead D., Walker J., Selway L., Smith D.A., Brown A.J., Quinn J. A proteomic analysis of the salt, cadmium and peroxide stress responses in Candida albicans and the role of the Hog1 stress-activated MAPK in regulating the stress-induced proteome. Proteomics 2009, 9:4686-4703.
121. Zeuthen M.L., Howard D.H. Thermotolerance and the heat-shock response in Candida albicans. J. Gen. Microbiol. 1989, 135:2509-2518.
122. Zhang L., Feng D., Fang W., Ouyang H., Luo Y., Du T., Jin C. Comparative proteomic analysis of an Aspergillus fumigatus mutant deficient in glucosidase I (AfCwh41). Microbiology 2009, 155:2157-2167.