Proteomic analysis of cytoplasmic and surface proteins from yeast cells, hyphae, and biofilms of Candida albicans

Proteomics

Volumn 9, Issue 8, 2009, Pages 2230-2252

  Montserrat Martinez Gomariz ^a   Perumal, Palani ^b,d   Mekala, Satish ^b,e   Nombela, César ^a   Chaffin, W LaJean ^b   Gil, Concha ^a,c  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^b TEXAS TECH UNIVERSITY   (United States)

^c Faculty of Pharmacy   (Spain)

^d UNIVERSITY OF MADRAS   (India)

^e Guindy Campus ^*  (United States)

Author keywords

Biofilm; Candida albicans; Cell surface; Cytoplasm; DIGE

Indexed keywords

CELL SURFACE PROTEIN; CYTOPLASM PROTEIN; FOLIC ACID; GLUCOSE; PENTOSE; POLY(METHYL METHACRYLATE);

ARTICLE; BIOFILM; CANDIDA ALBICANS; CONTROLLED STUDY; FUNGUS HYPHAE; GLUCOSE METABOLISM; NONHUMAN; OXIDATIVE STRESS; PLANKTON; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEOMICS; YEAST CELL;

BIOFILMS; CANDIDA ALBICANS; CELL MEMBRANE; CYTOPLASM; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; FUNGAL PROTEINS; HYPHAE; MEMBRANE PROTEINS; METABOLIC NETWORKS AND PATHWAYS; OXIDATIVE STRESS; PROTEOME; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

CANDIDA ALBICANS;

EID: 65349134093     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.200700594     Document Type: Article

References (61)

1. Kojic, E. M., Darouiche, R. O., Candida infections of medical devices. Clin. Microbiol. Rev. 2004, 17, 255-267.
2. Budtz-Jorgensen, E., Ecology of Candida-associated denture stomatitis. Microbial Ecol. Health Dis. 2000, 12, 170-185.
3. Webb, B. C., Thomas, C. J., Willcox, M. D., Harty, D. W., Knox, K. W., Candida-associated denture stomatitis. Aetiology and management: a review. Part 2. Oral diseases caused by Candida species. Aust. Dent. J. 1998, 43, 160-166.
4. Wilson, J., The aetiology, diagnosis and management of denture stomatitis. Br. Dent. J. 1998, 185, 380-384.
5. Pfaller, M. A., Jones, R. N., Messer, S. A., Edmond, M. B., Wenzel, R. P., National surveillance of nosocomial blood stream infection due to Candida albicans: frequency of occurrence and antifungal susceptibility in the SCOPE Program. Diagn. Microbiol. Infect. Dis. 1998, 31, 327-332.
6. Crump, J. A., Collignon, P. J., Intravascular catheter-associated infections. Eur. J. Clin. Microbiol. Infect. Dis. 2000, 19, 1-8.
7. Wisplinghoff, H., Bischoff, T., Tallent, S. M., Seifert, H. et al., Nosocomial bloodstream infections in US hospitals: analysis of 24,179 cases from a prospective nationwide surveillance study. Clin. Infect. Dis. 2004, 39, 309-317.
8. Garcia-Sanchez, S., Aubert, S., Iraqui, I., Janbon, G. et al., Candida albicans biofilms: a developmental state associated with specific and stable gene expression patterns. Eukaryot. Cell 2004, 3, 536-545.
9. Murillo, L. A., Newport, G., Lan, C. Y., Habelitz, S. et al., Genome-wide transcription profiling of the early phase of biofilm formation by Candida albicans. Eukaryot. Cell 2005, 4, 1562-1573.
10. Nantel, A., Dignard, D., Bachewich, C., Harcus, D. et al., Transcription profiling of Candida albicans cells undergoing the yeast-to-hyphal transition. Mol. Biol. Cell 2002, 13, 3452- 3465.
11. Yeater, K. M., Chandra, J., Cheng, G., Mukherjee, P. K. et al., Temporal analysis of Candida albicans gene expression during biofilm development. Microbiology 2007, 153, 2373- 2385.
12. Hernandez, R., Nombela, C., Diez-Orejas, R., Gil, C., Twodimensional reference map of Candida albicans hyphal forms. Proteomics 2004, 4, 374-382.
13. Fernandez-Arenas, E., Cabezon, V., Bermejo, C., Arroyo, J. et al., Integrated proteomics and genomics strategies bring new insight into Candida albicans response upon macrophage interaction. Mol. Cell. Proteomics 2007, 6, 460-478.
14. Kusch, H., Engelmann, S., Bode, R., Albrecht, D. et al., A proteomic view of Candida albicans yeast cell metabolism in exponential and stationary growth phases. Int. J. Med. Microbiol. 2007.
15. 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.
16. Chaffin, W. L., Lopez-Ribot, J. L., Casanova, M., Gozalbo, D., Martinez, J. P., Cell wall and secreted proteins of Candida albicans: identification, function, and expression. Microbiol Mol. Biol. Rev. 1998, 62, 130-180.
17. Chaffin, W. L., Candida albicans cell wall proteins. Microbiol. Mol. Biol. Rev. 2008, 72, 495-544.
18. Klis, F. M., de Groot, P., Hellingwerf, K., Molecular organization of the cell wall of Candida albicans. Med. Mycol. 2001, 39 Suppl 1, 1-8.
19. Smits, G. J., van den Ende, H., Klis, F. M., Differential regulation of cell wall biogenesis during growth and development in yeast. Microbiology (Reading, England) 2001, 147, 781-794.
20. Nombela, C., Gil, C., Chaffin, W. L., Non-conventional protein secretion in yeast. Trends Microbiol. 2006, 14, 15-21.
21. Pitarch, A., Abian, J., Carrascal, M., Sanchez, M. et al., Proteomics-based identification of novel Candida albicans antigens for diagnosis of systemic candidiasis in patients with underlying hematological malignancies. Proteomics 2004, 4, 3084-3106.
22. Pitarch, A., Jimenez, A., Nombela, C., Gil, C., Decoding serological response to Candida cell wall immunome into novel diagnostic, prognostic, and therapeutic candidates for systemic candidiasis by proteomic and bioinformatic analyses. Mol. Cell. Proteomics 2006, 5, 79-96.
23. de Groot, P. W., de Boer, A. D., Cunningham, J., Dekker, H. L. et al., Proteomic analysis of Candida albicans cell walls reveals covalently bound carbohydrate-active enzymes and adhesins. Eukaryot. Cell 2004, 3, 955-965.
24. Saville, S. P., Thomas, D. P., Lopez Ribot, , J. L., A role for Efg1p in Candida albicans interactions with extracellular matrices. FEMS Microbiol. Lett. 2006, 256, 151-158.
25. Urban, C., Sohn, K., Lottspeich, F., Brunner, H., Rupp, S., Identification of cell surface determinants in Candida albicans reveals Tsa1p, a protein differentially localized in the cell. FEBS Lett. 2003, 544, 228-235.
26. 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.
27. Mukherjee, P. K., Mohamed, S., Chandra, J., Kuhn, D. et al., 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.
28. 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.
29. 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.
30. Thomas, D. P., Viudes, A., Monteagudo, C., Lazzell, A. L. et al., A proteomic-based approach for the identification of Candida albicans protein components present in a subunit vaccine that protects against disseminated candidiasis. Proteomics 2006, 6, 6033-6041.
31. Vediyappan, G., Chaffin, W. L., Non-glucan attached proteins of Candida albicans biofilm formed on various surfaces. Mycopathologia 2006, 161, 3-10.
32. Uppuluri, P., Perumal, P., Chaffin, W. L., Analysis of RNA species of various sizes from stationary-phase planktonic yeast cells of Candida albicans. FEMS Yeast Res. 2007, 7, 110-117.
33. Casanova, M., Chaffin, W. L., Cell wall glycoproteins of Candida albicans as released by different methods. J. Gen. Microbiol. 1991, 137, 1045-1051.
34. Bland, J. M., Altman, D. G., Multiple significance tests: the Bonferroni method. Bmj 1995, 310, 170.
35. Havlis, J., Thomas, H., Sebela, M., Shevchenko, A., Fast-response proteomics by accelerated in-gel digestion of proteins. Anal. Chem. 2003, 75, 1300-1306.
36. d'Enfert, C., Goyard, S., Rodriguez-Arnaveilhe, S., Frangeul, L. et al., CandidaDB: a genome database for Candida albicans pathogenomics. Nucleic Acids Res. 2005, 33, D353-357.
37. Arnaud, M. B., Costanzo, M. C., Skrzypek, M. S., Binkley, G. et al., The Candida Genome Database (CGD), a community resource for Candida albicans gene and protein information. Nucleic Acids Res. 2005, 33, D358-363.
38. Boyle, E. I., Weng, S., Gollub, J., Jin, H. et al., GO::TermFinder-open source software for accessing Gene Ontology information and finding significantly enriched Gene Ontology terms associated with a list of genes. Bioinformatics 2004, 20, 3710-3715.
39. Arnaud, M. B., Costanzo, M. C., Skrzypek, M. S., Shah, P. et al., Sequence resources at the Candida Genome Database. Nucleic Acids Res. 2007, 35, D452-456.
40. Uppuluri, P., Sarmah, B., Chaffin, W. L., Candida albicans SNO1 and SNZ1 expressed in stationary-phase planktonic yeast cells and base of biofilm. Microbiology (Reading, England) 2006, 152, 2031-2038.
41. Pitarch, A., Diez-Orejas, R., Molero, G., Pardo, M. et al., Analysis of the serologic response to systemic Candida albicans infection in a murine model. Proteomics 2001, 1, 550-559.
42. Ihmels, J., Bergmann, S., Gerami-Nejad, M., Yanai, I. et al., Rewiring of the yeast transcriptional network through the evolution of motif usage. Science 2005, 309, 938-940.
43. Uppuluri, P., Chaffin, W. L., Defining Candida albicans stationary phase by cellular and DNA replication, gene expression and regulation. Mol. Microbiol. 2007, 64, 1572-1586.
44. Lorenz, M. C., Bender, J. A., Fink, G. R., Transcriptional response of Candida albicans upon internalization by macrophages. Eukaryot. Cell 2004, 3, 1076-1087.
45. Lorenz, M. C., Fink, G. R., The glyoxylate cycle is required for fungal virulence. Nature 2001, 412, 83-86.
46. Carman, A. J., Vylkova, S., Lorenz, M. C., Role of acetyl coenzyme a synthesis and breakdown in alternative carbon source utilization in Candida albicans. Eukaryot. Cell 2008, 7, 1733-1741.
47. Alloush, H. M., Lopez-Ribot, J. L., Masten, B. J., Chaffin, W. L., 3-phosphoglycerate kinase: a glycolytic enzyme protein present in the cell wall of Candida albicans. Microbiology (Reading, England) 1997, 143 (Pt 2), 321-330.
48. Edwards, S. R., Braley, R., Chaffin, W. L., Enolase is present in the cell wall of Saccharomyces cerevisiae. FEMS Microbiol. Lett. 1999, 177, 211-216.
49. Lopez-Ribot, J. L., Alloush, H. M., Masten, B. J., Chaffin, W. L., Evidence for presence in the cell wall of Candida albicans of a protein related to the hsp70 family. Infect. Immun. 1996, 64, 3333-3340.
50. Lopez-Ribot, J. L., Chaffin, W. L., Members of the Hsp70 family of proteins in the cell wall of Saccharomyces cerevisiae. J. Bacteriol. 1996, 178, 4724-4726.
51. Pardo, M., Monteoliva, L., Pla, J., Sanchez, M. et al., Twodimensional analysis of proteins secreted by Saccharomyces cerevisiae regenerating protoplasts: a novel approach to study the cell wall. Yeast 1999, 15, 459-472.
52. Lopez-Villar, E., Monteoliva, L., Larsen, M. R., Sachon, E. et al., Genetic and proteomic evidences support the localization of yeast enolase in the cell surface. Proteomics 2006, 6 Suppl 1, S107-118.
53. Delgado, M. L., Gil, M. L., Gozalbo, D., Candida albicans TDH3 gene promotes secretion of internal invertase when expressed in Saccharomyces cerevisiae as a glyceraldehyde-3-phosphate dehydrogenase-invertase fusion protein. Yeast 2003, 20, 713-722.
54. Crowe, J. D., Sievwright, I. K., Auld, G. C., Moore, N. R. et al., Candida albicans binds human plasminogen: identification of eight plasminogen-binding proteins. Mol. Microbiol. 2003, 47, 1637-1651.
55. Poltermann, S., Kunert, A., von der Heide, M., Eck, R. et al., Gpm1p is a factor H-, FHL-1-, and plasminogen-binding surface protein of Candida albicans. J. Biol. Chem. 2007, 282, 37537-37544.
56. Li, X. S., Reddy, M. S., Baev, D., Edgerton, M., Candida albicans Ssa1/2p is the cell envelope binding protein for human salivary histatin 5. J. Biol. Chem. 2003, 278, 28553-28561.
57. Vylkova, S., Li, X. S., Berner, J. C., Edgerton, M., Distinct antifungal mechanisms: beta-defensins require Distinct antifungal mechanisms: beta-Candida albicans Ssa1 protein, while Trk1p mediates activity of cysteine-free cationic peptides. Antimicrob. Agents Chemother. 2006, 50, 324- 331.
58. Donlan, R. M., Costerton, J. W., Biofilms: survival mechanisms of clinically relevant microorganisms. Clin. Microbiol. Rev. 2002, 15, 167-193.
59. Chandra, J., McCormick, T. S., Imamura, Y., Mukherjee, P. K., Ghannoum, M. A., Interaction of Candida albicans with adherent human peripheral blood mononuclear cells increases C. albicans biofilm formation and results in differential expression of pro- and anti-inflammatory cytokines. Infect. Immun. 2007, 75, 2612-2620.
60. Klis, F. M., Mol, P., Hellingwerf, K., Brul, S., Dynamics of cell wall structure in Saccharomyces cerevisiae. FEMS Microbiol. Rev. 2002, 26, 239-256.
61. Cossins, E. A., Chen, L., Folates and one-carbon metabolism in plants and fungi. Phytochemistry 1997, 45, 437-452.