Hypoxic adaptation by Efg1 regulates biofilm formation by Candida albicans

Applied and Environmental Microbiology

Volumn 75, Issue 11, 2009, Pages 3663-3672

  Stichternoth, Catrin ^a   Ernst, Joachim F ^a  

^a HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALBICANS; ANTI-FUNGAL; BIOFILM DEVELOPMENT; BIOFILM FORMATION; BIOFILM GROWTH; BIOFILM SYSTEMS; CANDIDA ALBICANS; DOXYCYCLINE; IN-VITRO; INDUCIBLE PROMOTER; IRON UPTAKE; OXYGEN LEVELS; TRANSCRIPTIONAL CONTROL; TRANSCRIPTOME;

BIOFILMS; CARBON DIOXIDE; CYTOLOGY; GENES; GLOBAL WARMING; GROWTH KINETICS; OXYGEN; SULFUR;

BIOFILTERS;

CARBON DIOXIDE; OXYGEN; POLYSTYRENE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR EFG1; TRANSCRIPTOME; UNCLASSIFIED DRUG;

ANTIOXIDANT; BIOFILM; FUNGAL DISEASE; FUNGUS; HYPOXIA;

ADAPTATION; ARTICLE; BACTERIUM MUTANT; BIOFILM; CANDIDA ALBICANS; FUNGUS GROWTH; GENE EXPRESSION; HYPOXIA; IRON TRANSPORT; NONHUMAN; NUCLEOTIDE SEQUENCE; PROMOTER REGION; REAL TIME POLYMERASE CHAIN REACTION;

ANOXIA; BIOFILMS; CANDIDA ALBICANS; DNA-BINDING PROTEINS; FUNGAL PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, FUNGAL; HUMANS; NUCLEAR PROTEINS; SACCHAROMYCES CEREVISIAE PROTEINS; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS;

CANDIDA ALBICANS;

EID: 66249127199     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00098-09     Document Type: Article

References (47)

1. Andes, D., J. Nett, P. Oschel, R. Albrecht, K. Marchillo, and A. Pitula. 2004. Development and characterization of an in vivo central venous catheter Candida albicans biofilm model. Infect. Immun. 72:6023-6031.
2. Bates, S., H. B. Hughes, C. A. Munro, W. P. Thomas, D. M. MacCallum, G. Bertram, A. Atrih, M. A. Ferguson, J. M. Bain, A. Brand, S. Hamilton, C. Westwater, L. M. Thomson, A. J. Brown, F. C. Odds, and N. A. Gow. 2006. Outer chain N-glycans are required for cell wall integrity and virulence of Candida albicans. J. Biol. Chem. 281:90-98. (Pubitemid 43671166)
3. Biswas, S. K., and W. L. Chaffin. 2005. Anaerobic growth of Candida albicans does not support biofilm formation under similar conditions used for aerobic biofilm. Curr. Microbiol. 51:100-104.
4. Brown, D. H., Jr., A. D. Giusani, X. Chen, and C. A. Kumamoto. 1999. Filamentous growth of Candida albicans in response to physical environmental cues and its regulation by the unique CZF1 gene. Mol. Microbiol. 34:651-662.
5. Calera, J. A., X. J. Zhao, and R. Calderone. 2000. Defective hyphal development and avirulence caused by a deletion of the SSK1 response regulator gene in Candida albicans. Infect. Immun. 68:518-525.
6. Cantero, P. D., C. Lengsfeld, S. K.-H. Prill, M. Subanović, E. Román, J. Pla, and J. F. Ernst. 2007. Transcriptional and physiological adaptation to defective protein-O-mannosylation in Candida albicans. Mol. Microbiol. 64:1115-1128.
7. Cao, F., S. Lane, P. P. Raniga, Y. Lu, Z. Zhou, K. J. Ramon, J. Chen, and H. Liu. 2006. The Flo8 transcription factor is essential for hyphal development and virulence in Candida albicans. Mol. Biol. Cell 17:295-307. (Pubitemid 43049482)
8. Chandra, J., D. M. Kuhn, P. K. Mukherjee, L. L. Hoyer, T. McCormick, and M. A. Ghannoum. 2001. Biofilm formation by the fungal pathogen Candida albicans: development, architecture, and drug resistance. J. Bacteriol. 183:5385-5394.
9. D'Enfert, C. 2006. Biofilms and their role in the resistance of pathogenic Candida to antifungal agents. Curr. Drug Targets 7:465-470.
10. Dirmeier, R., K. M. O'Brien, M. Engle, A. Dodd, E. Spears, and R. O. Poyton. 2002. Exposure of yeast cells to anoxia induces transient oxidative stress. J. Biol. Chem. 277:34773-34784.
11. Doedt, T., S. Krishnamurthy, D. P. Bockmühl, B. Tebarth, C. Stempel, C. L. Russell, A. J. P. Brown, and J. F. Ernst. 2004. APSES proteins regulate morphogenesis and metabolism in Candida albicans. Mol. Biol. Cell 15:3167-3180.
12. Douglas, L. J. 2003. Candida biofilms and their role in infection. Trends Microbiol. 11:30-36.
13. Ernst, J. F., and D. Tielker. 2009. Responses to hypoxia in fungal pathogens. Cell. Microbiol. 11:183-190.
14. Fonzi, W. A., and M. Y. Irwin. 1993. Isogenic strain construction and gene mapping in Candida albicans. Genetics 134:717-728.
15. García-Sánchez, S., S. Aubert, I. Iraqui, G. Jambon, J.-M. Ghigo, and C. D'Enfert. 2004. Candida albicans biofilms: a developmental state associated with specific and stable gene expression patterns. Eukaryot. Cell 3:536-545.
16. Giusani, A. D., M. Vinces, and C. A. Kumamoto. 2002. Invasive filamentous growth of Candida albicans is promoted by Czf1p-dependent relief of Efg1p-mediated repression. Genetics 160:1749-1753.
17. Hameed, S., T. Prasad, D. Banerjee, A. Chandra, C. K. Mukhopadhyay, S. K. Goswami, A. A. Lattif, J. Chandra, P. K. Mukherjee, M. A. Ghannoum, and R. Prasad. 2008. Iron deprivation induces EFG1-mediated hyphal development in Candida albicans without affecting biofilm formation. FEMS Yeast Res. 8:744-755.
18. Kelly, M. T., D. M. MacCallum, S. D. Clancy, F. C. Odds, A. J. Brown, and G. Butler. 2004. The Candida albicans CaAce2 gene affects morphogenesis, adherence and virulence. Mol. Microbiol. 53:969-983.
19. Kojic, E. M., and R. O. Darouiche. 2004. Candida infections of medical devices. Clin. Microbiol. Rev. 17:255-267.
20. Kumamoto, C. 2005. A contact-activated kinase signals Candida albicans invasive growth and biofilm development. Proc. Natl. Acad. Sci. USA 102:5576-5581.
21. Lane, S., C. Birse, S. Zhou, R. Matson, and H. Liu. 2001. DNA array studies demonstrate convergent regulation of virulence factors by Cph1, Cph2, and Efg1 in Candida albicans. J. Biol. Chem. 276:48988-48996. (Pubitemid 37370602)
22. Mukherjee, P. K., S. Mohamed, J. Chandra, D. Kuhn, S. Liu, O. S. Antar, R. Munyon, A. P. Mitchell, D. Andes, M. R. Chance, M. Rouabhia, and M. A. Ghannoum. 2006. Alcohol dehydrogenase restricts the ability of the pathogen Candida albicans to form a biofilm on catheter surfaces through an ethanol-based mechanism. Infect. Immun. 74:3804-3816.
23. Mulhern, S. M., M. E. Logue, and G. Butler. 2006. Candida albicans transcription factor Ace2 regulates metabolism and is required for filamentation in hypoxic conditions. Eukaryot. Cell 5:2001-2013.
24. Murillo, L. A., G. Newport, C.-Y. Lan, S. Habelitz, J. Dungan, and N. M. Agabian. 2005. Genome-wide transcription profiling of the early phase of biofilm formation by Candida albicans. Eukaryot. Cell 4:1562-1573. (Pubitemid 41339111)
25. Nailis, H., R. Vandenbroucke, K. Tilleman, D. Deforce, H. Nelis, and T. Coenye. 2009. Monitoring ALS1 and ALS3 gene expression during in vitro Candida albicans biofilm formation under continuous flow conditions. Mycopathologia 167:9-17.
26. 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.
27. Navarro-Garcia, F., M. Sanchez, J. Pla, and C. Nombela. 1995. Functional characterization of the MKC1 gene of Candida albicans, which encodes a mitogen-activated protein kinase homolog related to cell integrity. Mol. Cell. Biol. 15:2197-2206.
28. Nobile, C. J., and A. P. Mitchell. 2006. Genetics and genomics of Candida albicans biofilm formation. Cell. Microbiol. 8:1382-1391.
29. Nobile, C. J., and A. P. Mitchell. 2005. Regulation of cell-surface genes and biofilm formation by the C. albicans transcription factor Bcr1p. Curr. Biol. 15:1150-1155.
30. Nobile, C. J., D. R. Andes, J. E. Nett, F. J. Smith, Jr., F. Yue, Q.-T. Phan, J. E. Edwards, S. G. Filler, and A. P. Mitchell. 2006. Critical role of Bcr1-dependent adhesins in C. albicans biofilm formation in vitro and in vivo. PLoS Pathog. 2:e63.
31. Park, H., C. L. Myers, D. C. Sheppard, Q. T. Phan, A. A. Sanchez, J. Edwards, and S. G. Filler. 2005. Role of the fungal Ras-protein kinase A pathway in governing epithelial cell interactions during oropharyngeal candidiasis. Cell. Microbiol. 7:499-510.
32. Park, Y.-N., and J. Morschhäuser. 2005. Tetracycline-inducible gene expression and gene deletion in Candida albicans. Eukaryot. Cell 4:1328-1342.
33. Peltroche-Llacsahuanga, H., S. Goyard, C. D'Enfert, S. K. Prill, and J. F. Ernst. 2006. Protein O-mannosyltransferase isoforms regulate biofilm formation in Candida albicans. Antimicrob. Agents Chemother. 50:3488-3492. (Pubitemid 44527534)
34. Pérez, A., B. Pedrós, A. Murgui, M. Casanova, J. L. López-Ribot, and J. P. Martínez. 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.
35. Ramage, G., K. VandeWalle, B. L. Wickes, and J. López-Ribot. 2001. Standardized method for in vitro antifungal susceptibility testing of Candida albicans biofilms. Antimicrob. Agents Chemother. 45:2475-2479.
36. Ramage, G., K. VandeWalle, J. L. López-Ribot, and B. L. Wickes. 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. (Pubitemid 35245528)
37. Ramage, G., S. P. Saville, D. P. Thomas, and J. L. López-Ribot. 2005. Candida biofilms: an update. Eukaryot. Cell 4:633-638.
38. Rossignol, T., C. Ding, A. Guida, C. d'Enfert, D. G. Higgins, and G. Butler. 2009. Correlation between biofilm formation and the hypoxic response in Candida parapsilosis. Eukaryot. Cell 8:550-559.
39. Schweizer, A., S. Rupp, B. N. Taylor, M. Röllinghoff, and K. Schröppel. 2000. The TEA/ATTS transcription factor CaTec1p regulates hyphal development and virulence in Candida albicans. Mol. Microbiol. 38:435-445.
40. Sellam, A., T. Al-Niemi, K. McInnerney, S. Brumfield, A. Nantel, and P. A. Suci. 2009. A Candida albicans early stage biofilm detachment event in rich medium. BMC Microbiol. 9:25.
41. Seneviratne, C. J., Y. Wang, L. Jin, Y. Abiko, and L. P. Samaranayake. 2008. Candida albicans biofilm formation is associated with increased anti-oxidative capacities. Proteomics 8:2936-2947.
42. Setiadi, E. R., T. Doedt, F. Cottier, C. Noffz, and J. F. Ernst. 2006. Transcriptional response of Candida albicans to hypoxia: linkage of oxygen-sensing- and Efg1p-regulatory networks. J. Mol. Biol. 361:399-411.
43. Stoldt, V. R., A. Sonneborn, C. E. Leuker, and J. F. Ernst. 1997. Efg1p, an essential regulator of morphogenesis of the human fungal pathogen Candida albicans, is a member of a conserved class of bHLH proteins regulating morphogenetic processes in fungi. EMBO J. 16:1982-1991.
44. Thein, Z. M., Y. H. Samaranayake, and L. P. Samaranayake. 2007. In vitro biofilm formation of Candida albicans and non-albicans Candida species under dynamic and anaerobic conditions. Arch. Oral Biol. 52:761-767.
45. Thomas, D. P., S. P. Bachmann, and J. L. Lopez-Ribot. 2006. Proteomics for the analysis of the Candida albicans biofilm lifestyle. Proteomics 6:5795-5804.
46. Yeater, K. M., J. Chandra, G. Cheng, P. K. Mukherjee, X. Zhao, S. L. Rodriguez-Zas, K. E. Kwast, M. A. Ghannoum, and L. L. Hoyer. 2007. Temporal analysis of Candida albicans gene expression during biofilm development. Microbiology 153:2373-2385.
47. Zhao, X., K. J. Daniels, S.-H. Oh, C. B. Green, K. Yeater, D. R. Soll, and L. L. Hoyer. 2006. Candida albicans Als3p is required for wild-type biofilm formation on silicone elastomer surfaces. Microbiology 152:2287-2299.