Changes in the proteome of Candida albicans in response to azole, polyene, and echinocandin antifungal agents

Antimicrobial Agents and Chemotherapy

Volumn 54, Issue 5, 2010, Pages 1655-1664

  Hoehamer, Christopher F ^a,b   Cummings, Edwin D ^a   Hilliard, George M ^a   Rogers, P David ^a,b  

^a UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^b LE BONHEUR CHILDREN'S MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1,3 BETA GLUCAN SYNTHASE; AMPHOTERICIN B; CASPOFUNGIN; ERGOSTEROL; FUNGAL PROTEIN; KETOCONAZOLE; PROTEIN; PROTEOME; PYRUVIC ACID; RHO1P PROTEIN; UNCLASSIFIED DRUG;

ADAPTIVE BEHAVIOR; AMINO ACID SYNTHESIS; ANTIFUNGAL ACTIVITY; ANTIFUNGAL RESISTANCE; ARTICLE; BIOSYNTHESIS; CANDIDA ALBICANS; CARBOHYDRATE METABOLISM; CELL STRESS; CELL WALL; CITRIC ACID CYCLE; CONTROLLED STUDY; DRUG EXPOSURE; DRUG RESPONSE; ENZYME ACTIVITY; GLUCONEOGENESIS; GLYCOLYSIS; HEAT SHOCK; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NONHUMAN; OSMOTIC STRESS; OXIDATIVE STRESS; PENTOSE PHOSPHATE CYCLE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN SYNTHESIS; STEROL SYNTHESIS; TWO DIMENSIONAL GEL ELECTROPHORESIS;

ADAPTATION, PHYSIOLOGICAL; AMPHOTERICIN B; ANTIFUNGAL AGENTS; CANDIDA ALBICANS; CANDIDIASIS; DRUG RESISTANCE, FUNGAL; ECHINOCANDINS; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; ERGOSTEROL; HUMANS; KETOCONAZOLE; OXIDATIVE STRESS; PROTEOME; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; WATER-ELECTROLYTE BALANCE;

EID: 77951243670     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.00756-09     Document Type: Article

References (53)

1. Akins, R. A. 2005. An update on antifungal targets and mechanisms of resistance in Candida albicans. Med. Mycol. 43:285-318.
2. Arning, M., K. O. Kliche, A. H. Heer-Sonderhoff, and A. Wehmeier. 1995. Infusion-related toxicity of three different amphotericin B formulations and its relation to cytokine plasma levels. Mycoses 38:459-465.
3. Bates, D. W., L. Su, D. T. Yu, G. M. Chertow, D. L. Seger, D. R. Gomes, and R. Platt. 2001. Correlates of acute renal failure in patients receiving parenteral amphotericin B. Kidney Int. 60:1452-1459.
4. Braun, B. R., M. van Het Hoog, C. d'Enfert, M. Martchenko, J. Dungan, A. Kuo, D. O. Inglis, M. A. Uhl, H. Hogues, M. Berriman, M. Lorenz, A. Levitin, U. Oberholzer, C. Bachewich, D. Harcus, A. Marcil, D. Dignard, T. Iouk, R. Zito, L. Frangeul, F. Tekaia, K. Rutherford, E. Wang, C. A. Munro, S. Bates, N. A. Gow, L. L. Hoyer, G. Kohler, J. Morschhauser, G. Newport, S. Znaidi, M. Raymond, B. Turcotte, G. Sherlock, M. Costanzo, J. Ihmels, J. Berman, D. Sanglard, N. Agabian, A. P. Mitchell, A. D. Johnson, M. Whiteway, and A. Nantel. 2005. A human-curated annotation of the Candida albicans genome. PLoS Genet. 1:36-57.
5. Bruneau, J. M., I. Maillet, E. Tagat, R. Legrand, F. Supatto, C. Fudali, J. P. Caer, V. Labas, D. Lecaque, and J. Hodgson. 2003. Drug induced proteome changes in Candida albicans: comparison of the effect of beta (1,3) glucan synthase inhibitors and two triazoles, fluconazole and itraconazole. Proteomics 3:325-336.
6. Choi, W., Y. J. Yoo, M. Kim, D. Shin, and H. B. Jeon. 2003. Identification of proteins highly expressed in the hyphae of Candida albicans by two-dimensional electrophoresis. Yeast 20:1053-1060.
7. Cummings, E. D., J. M. Brown, S. T. Sarva, R. H. Waldo, and G. M. Hilliard. 2007. High-throughput proteomics processing of proteins in polyacrylamide in a multiwell format. J. Proteome Res. 6:1603-1608.
8. De Backer, M. D., T. Ilyind, X.-J. Ma, S. Vandoninck, W. H. M. L. Luyten, and H. Vanden Bossche. 2001. Genetic profiling of the response of Candida albicans to itraconazole treatment using a DNA microarray. Antimicrob. Agents Chemother. 45:1660-1670.
9. de Groot, P. W., C. Ruiz, C. R. Vazquez de Aldana, E. Duenas, V. J. Cid, F. Del Rey, J. M. Rodriquez-Pena, P. Perez, A. Andel, J. Caubin, J. Arroyo, J. C. Garcia, C. Gil, M. Molina, L. J. Garcia, C. Nombela, and F. M. Klis. 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.
10. Demasi, A. P., G. A. Pereira, and L. E. Netto. 2001. Cytosolic thioredoxin peroxidase I is essential for the antioxidant defense of yeast with dysfunctional mitochondria. FEBS Lett. 509:430-434.
11. Edmond, M. B., S. E. Wallace, D. K. McClish, M. A. Pfaller, R. N. Jones, and R. P. Wenzel. 1999. Nosocomial bloodstream infections in United States hospitals: a three-year analysis. Clin. Infect. Dis. 29:239-244.
12. Fernandez-Arenas, E., V. Cabezon, C. Bermejo, J. Arroyo, C. Nombela, R. Diez-Orejas, and C. Gil. 2007. Integrated proteomics and genomics strategies bring new insight into Candida albicans response upon macrophage interaction. Mol. Cell. Proteomics 6:460-478.
13. Harcus, D., A. Nantel, A. Marcil, T. Rigby, and M. Whiteway. 2004. Transcription profiling of cyclic AMP signaling in Candida albicans. Mol. Biol. Cell 15:4490-4499.
14. Hashimoto, H., A. Sakakibara, M. Yamasaki, and K. Yoda. 1997. Saccharomyces cerevisiae VIG9 encodes GDP-mannose pyrophosphorylase, which is essential for protein glycosylation. J. Biol. Chem. 272:16308-16314.
15. Hoehamer, C. F., E. D. Cummings, G. M. Hilliard, J. Morschhauser, and P. D. Rogers. 2009. Upc2p-associated differential protein expression in Candida albicans. Proteomics 9:4726-4730.
16. Hooshdaran, M. Z., K. S. Barker, G. M. Hilliard, H. Kusch, J. Morschhauser, and P. D. Rogers. 2004. Proteomic analysis of azole resistance in Candida albicans clinical isolates. Antimicrob. Agents Chemother. 48:2733-2735.
17. Jang, H. H., K. O. Lee, Y. H. Chi, B. G. Jung, S. K. Park, J. H. Park, J. R. Lee, S. S. Lee, J. C. Moon, J. W. Yun, Y. O. Choi, W. Y. Kim, J. S. Kang, G. W. Cheong, D. J. Yun, S. G. Rhee, M. J. Cho, and S. Y. Lee. 2004. Two enzymes in one; two yeast peroxiredoxins display oxidative stress-dependent switching from a peroxidase to a molecular chaperone function. Cell 117: 625-635.
18. Johnson, M. D., and J. R. Perfect. 2003. Caspofungin: first approved agent in a new class of antifungals. Expert Opin. Pharmacother. 4:807-823.
19. Kelly, S. L., D. C. Lamb, D. E. Kelly, N. J. Manning, J. Loeffler, H. Hebart, U. Schumacher, and H. Einsele. 1997. Resistance to fluconazole and crossresistance to amphotericin B in Candida albicans from AIDS patients caused by defective sterol delta 5,6-desaturation. FEBS Lett. 400:80-82.
20. Kuge, S., and N. Jones. 1994. YAP1 dependent activation of TRX2 is essential for the response of Saccharomyces cerevisiae to oxidative stress by hydroperoxides. EMBO J. 13:655-664.
21. Kusch, H., K. Biswas, S. Schwanfelder, S. Engelmann, P. D. Rogers, M. Hecker, and J. Morschhauser. 2004. A proteomic approach to understanding the development of multidrug-resistant Candida albicans strains. Mol. Genet. Genomics 271:554-565.
22. Kusch, H., S. Engelmann, D. Albrecht, J. Morschhauser, and M. Hecker. 2007. Proteomic analysis of the oxidative stress response in Candida albicans. Proteomics 7:686-697.
23. Lee, J., C. Godon, G. Lagniel, D. Spector, J. Garin, J. Labarre, and M. B. Toledano. 1999. Yap1 and Skn7 control two specialized oxidative stress response regulons in yeast. J. Biol. Chem. 274:16040-16046.
24. Liu, L., M. Zeng, A. Hausladen, J. Heitman, and J. S. Stamler. 2000. Protection from nitrosative stress by yeast flavohemoglobin. Proc. Natl. Acad. Sci. U. S. A. 97:4672-4676.
25. Liu, T. T., R. E. Lee, K. S. Barker, L. Wei, R. Homayouni, and P. D. Rogers. 2005. Genome-wide expression profiling of the response to azole, polyene, echinocandin, and pyrimidine antifungal agents in Candida albicans. Antimicrob. Agents Chemother. 49:2226-2236.
26. Lorenz, M. C., J. A. Bender, and G. R. Fink. 2004. Transcriptional response of Candida albicans upon internalization by macrophages. Eukaryot. Cell 3:1076-1087.
27. Maesaki, S., M. A. Hossain, Y. Miyazaki, K. Tomono, T. Tashiro, and S. Kohno. 2000. Efficacy of FK463, a (1,3)-beta-D-glucan synthase inhibitor, in disseminated azole-resistant Candida albicans infection in mice. Antimicrob. Agents Chemother. 44:1728-1730.
28. Martinez-Solano, L., C. Nombela, G. Molero, and C. Gil. 2006. Differential protein expression of murine macrophages upon interaction with Candida albicans. Proteomics 6(Suppl. 1):S133-S144.
29. Moore, C. B., K. L. Oakley, and D. W. Denning. 2001. In vitro activity of a new echinocandin, LY303366, and comparison with fluconazole, flucytosine and amphotericin B against Candida species. Clin. Microbiol. Infect. 7:11-16.
30. Morgan, B. A., G. R. Banks, W. M. Toone, D. Raitt, S. Kuge, and L. H. Johnston. 1997. The Skn7 response regulator controls gene expression in the oxidative stress response of the budding yeast Saccharomyces cerevisiae. EMBO J. 16:1035-1044.
31. Morschhauser, J., K. S. Barker, T. T. Liu, B. W. J. Bla, R. Homayouni, and P. D. Rogers. 2007. The transcription factor Mrr1p controls expression of the MDR1 efflux pump and mediates multidrug resistance in Candida albicans. PLoS Pathog. 3:e164.
32. Nantel, A., D. Dignard, C. Bachewich, D. Harcus, A. Marcil, A. P. Bouin, C. W. Sensen, H. Hogues, M. van het Hoog, P. Gordon, T. Rigby, F. Benoit, D. C. Tessier, D. Y. Thomas, and M. Whiteway. 2002. Transcription profiling of Candida albicans cells undergoing the yeast-to-hyphal transition. Mol. Biol. Cell 13:3452-3465.
33. Pahlman, A. K., K. Granath, R. Ansell, S. Hohmann, and L. Adler. 2001. The yeast glycerol 3-phosphatases Gpp1p and Gpp2p are required for glycerol biosynthesis and differentially involved in the cellular responses to osmotic, anaerobic, and oxidative stress. J. Biol. Chem. 276:3555-3563.
34. Pfaller, M. A., R. N. Jones, S. A. Messer, M. B. Edmond, and R. P. Wenzel. 1998. 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. 31:327-332.
35. Rex, J. H., T. J. Walsh, M. Nettleman, E. J. Anaissie, J. E. Bennett, E. J. Bow, A. J. Carillo-Munoz, P. Chavanet, G. A. Cloud, D. W. Denning, B. E. de Pauw, J. E. Edwards, Jr., J. W. Hiemenz, C. A. Kauffman, G. Lopez-Berestein, P. Martino, J. D. Sobel, D. A. Stevens, R. Sylvester, J. Tollemar, C. Viscoli, M. A. Viviani, and T. Wu. 2001. Need for alternative trial designs and evaluation strategies for therapeutic studies of invasive mycoses. Clin. Infect. Dis. 33:95-106.
36. Richard, P., M. H. Toivari, and M. Penttila. 1999. Evidence that the gene YLR070c of Saccharomyces cerevisiae encodes a xylitol dehydrogenase. FEBS Lett. 457:135-138.
37. Rybowicz, J., and C. Gurk-Turner. 2002. Caspofungin: the first agent available in the echinocandin class of antifungals. Proc. (Bayl. Univ. Med. Cent.) 15:97-99.
38. Singh, V., S. V. Satheesh, M. L. Raghavendra, and P. P. Sadhale. 2007. The key enzyme in galactose metabolism, UDP-galactose-4-epimerase, affects cell-wall integrity and morphology in Candida albicans even in the absence of galactose. Fungal Genet. Biol. 44:563-574.
39. Singleton, D. R., and K. C. Hazen. 2004. Differential surface localization and temperature-dependent expression of the Candida albicans CSH1 protein. Microbiology 150:285-292.
40. Singleton, D. R., J. Masuoka, and K. C. Hazen. 2001. Cloning and analysis of a Candida albicans gene that affects cell surface hydrophobicity. J. Bacteriol. 183:3582-3588.
41. Skoneczna, A., A. Micialkiewicz, and M. Skoneczny. 2007. Saccharomyces cerevisiae Hsp31p, a stress response protein conferring protection against reactive oxygen species. Free Radic. Biol. Med. 42:1409-1420.
42. Smith, P. K., R. I. Krohn, G. T. Hermanson, A. K. Mallia, F. H. Gartner, M. D. Provenzano, E. K. Fujimoto, N. M. Goeke, B. J. Olson, and D. C. Klenk. 1985. Measurement of protein using bicinchoninic acid. Anal. Biochem. 150:76-85.
43. Sokol-Anderson, M., J. E. Sligh, Jr., S. Elberg, J. Brajtburg, G. S. Kobayashi, and G. Medoff. 1988. Role of cell defense against oxidative damage in the resistance of Candida albicans to the killing effect of amphotericin B. Antimicrob. Agents Chemother. 32:702-705.
44. Sokol-Anderson, M. L., J. Brajtburg, and G. Medoff. 1986. Amphotericin B-induced oxidative damage and killing of Candida albicans. J. Infect. Dis. 154:76-83.
45. Ullmann, B. D., H. Myers, W. Chiranand, A. L. Lazzell, Q. Zhao, L. A. Vega, J. L. Lopez-Ribot, P. R. Gardner, and M. C. Gustin. 2004. Inducible defense mechanism against nitric oxide in Candida albicans. Eukaryot. Cell 3:715-723.
46. Wang, Y., Y. Y. Cao, X. M. Jia, Y. B. Cao, P. H. Gao, X. P. Fu, K. Ying, W. S. Chen, and Y. Y. Jiang. 2006. Cap1p is involved in multiple pathways of oxidative stress response in Candida albicans. Free Radic. Biol. Med. 40: 1201-1209.
47. White, T. C., K. A. Marr, and R. A. Bowden. 1998. Clinical, cellular, and molecular factors that contribute to antifungal drug resistance. Clin. Microbiol. Rev. 11:382-402.
48. Wingard, J. R., P. Kubilis, L. Lee, G. Yee, M. White, L. Walshe, R. Bowden, E. Anaissie, J. Hiemenz, and J. Lister. 1999. Clinical significance of nephrotoxicity in patients treated with amphotericin B for suspected or proven aspergillosis. Clin. Infect. Dis. 29:1402-1407.
49. Yamochi, W., K. Tanaka, H. Nonaka, A. Maeda, T. Musha, and Y. Takai. 1994. Growth site localization of Rho1 small GTP-binding protein and its involvement in bud formation in Saccharomyces cerevisiae. J. Cell Biol. 125: 1077-1093.
50. Yan, L., J. D. Zhang, Y. B. Cao, P. H. Gao, and Y. Y. Jiang. 2007. Proteomic analysis reveals a metabolism shift in a laboratory fluconazole-resistant Candida albicans strain. J. Proteome Res. 6:2248-2256.
51. Yin, Z., D. Stead, J. Walker, L. Selway, D. A. Smith, A. J. Brown, and J. Quinn. 2009. 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 9:4686-4703.
52. Yu, D. T., J. F. Peterson, D. L. Seger, W. C. Gerth, and D. W. Bates. 2005. Frequency of potential azole drug-drug interactions and consequences of potential fluconazole drug interactions. Pharmacoepidemiol. Drug Saf. 14: 755-767.
53. Znaidi, S., K. S. Barker, S. Weber, A. M. Alarco, T. T. Liu, G. Boucher, P. D. Rogers, and M. Raymond. 2009. Identification of the Candida albicans Cap1p regulon. Eukaryot. Cell 8:806-820.