Stress-induced phenotypic switching in Candida albicans

Molecular Biology of the Cell

Volumn 20, Issue 14, 2009, Pages 3178-3191

  Alby, Kevin ^a   Bennett, Richard J ^a  

^a BROWN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; GREEN FLUORESCENT PROTEIN; HYDROGEN PEROXIDE; INTRINSIC FACTOR; RAD51 PROTEIN; RAD52 PROTEIN; RNA;

ARTICLE; BIOFILM; CANDIDA ALBICANS; CANDIDIASIS; CELL CYCLE; CELL GROWTH; COMMENSAL; CONTROLLED STUDY; CULTURE MEDIUM; DNA REPAIR; FUNGAL VIRULENCE; GENE MUTATION; GENOTOXICITY; GENOTYPE; GROWTH INHIBITION; GROWTH RATE; MATING; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PHENOTYPE; PHENOTYPIC SWITCHING; PLASMID; PRIORITY JOURNAL; STRESS;

CANDIDA ALBICANS; DNA DAMAGE; GENE DELETION; GENE DOSAGE; GENE EXPRESSION REGULATION, FUNGAL; GENES, FUNGAL; GENES, SWITCH; HYDROXYUREA; METHYL METHANESULFONATE; OXIDATIVE STRESS; PHENOTYPE; S PHASE; STRESS, PHYSIOLOGICAL;

CANDIDA ALBICANS;

EID: 67749113256     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E09-01-0040     Document Type: Article

References (50)

1. Abramoff, M. D., Magelhaes, P. J., and Ram, S. J. (2004). Image processing with ImageJ. Biophotonics Int. 11, 36-42.
2. Acar, M., Mettetal, J. T., and van Oudenaarden, A. (2008). Stochastic switching as a survival strategy in fluctuating environments. Nat. Genet. 40, 471-475.
3. Barelle, C. J., Manson, C. L., MacCallum, D. M., Odds, F. C., Gow, N. A., and Brown, A. J. (2004). GFP as a quantitative reporter of gene regulation in Candida albicans. Yeast 21, 333-340.
4. Bennett, R. J., and Johnson, A. D. (2003). Completion of a parasexual cycle in Candida albicans by induced chromosome loss in tetraploid strains. EMBO J. 22, 2505-2515.
5. Bennett, R. J., and Johnson, A. D. (2005). Mating in Candida albicans and the search for a sexual cycle. Annu. Rev. Microbiol. 59, 233-255.
6. Bennett, R. J., Miller, M. G., Chua, P. R., Maxon, M. E., and Johnson, A. D. (2005). Nuclear fusion occurs during mating in Candida albicans and is dependent on the KAR3 gene. Mol. Microbiol. 55, 1046-1059.
7. Bensen, E. S., Clemente-Blanco, A., Finley, K. R., Correa-Bordes, J., and Berman, J. (2005). The mitotic cyclins Clb2p and Clb4p affect morphogenesis in Candida albicans. Mol. Biol. Cell 16, 3387-3400.
8. Care, R. S., Trevethick, J., Binley, K. M., and Sudbery, P. E. (1999). The MET3 promoter: a new tool for Candida albicans molecular genetics. Mol. Microbiol. 34, 792-798.
9. Ciudad, T., Andaluz, E., Steinberg-Neifach, O., Lue, N. F., Gow, N. A., Calderone, R. A., and Larriba, G. (2004). Homologous recombination in Candida albicans: role of CaRad52p in DNA repair, integration of linear DNA fragments and telomere length. Mol. Microbiol. 53, 1177-1194.
10. Daniels, K. J., Srikantha, T., Lockhart, S. R., Pujol, C., and Soll, D. R. (2006). Opaque cells signal white cells to form biofilms in Candida albicans. EMBO J. 25, 2240-2252.
11. Dubnau, D., and Losick, R. (2006). Bistability in bacteria. Mol. Microbiol. 61, 564-572.
12. Forche, A., Alby, K., Schaefer, D., Johnson, A. D., Berman, J., and Bennett, R. J. (2008). The parasexual cycle in Candida albicans provides an alternative pathway to meiosis for the formation of recombinant strains. PLoS Biol. 6, e110.
13. Geiger, J., Wessels, D., Lockhart, S. R., and Soll, D. R. (2004). Release of a potent polymorphonuclear leukocyte chemoattractant is regulated by whiteopaque switching in Candida albicans. Infect. Immun. 72, 667-677.
14. Gerami-Nejad, M., Berman, J., and Gale, C. A. (2001). Cassettes for PCRmediated construction of green, yellow, and cyan fluorescent protein fusions in Candida albicans. Yeast 18, 859-864.
15. Grummt, I., and Ladurner, A. G. (2008). A metabolic throttle regulates the epigenetic state of rDNA. Cell 133, 577-580.
16. Guthrie, C., and Fink, G. R. (1991). Guide to Yeast Genetics and Molecular Biology, San Diego, CA: Academic Press.
17. Huang, G., Wang, H., Chou, S., Nie, X., Chen, J., and Liu, H. (2006). Bistable expression of WOR1, a master regulator of white-opaque switching in Candida albicans. Proc. Natl. Acad. Sci. USA 103, 12813-12818.
18. Hull, C. M., Raisner, R. M., and Johnson, A. D. (2000). Evidence for mating of the "asexual" yeast Candida albicans in a mammalian host. Science 289, 307-310.
19. Jakubovics, N. S., Gill, S. R., Vickerman, M. M., and Kolenbrander, P. E. (2008). Role of hydrogen peroxide in competition and cooperation between Streptococcus gordonii and Actinomyces naeslundii. FEMS Microbiol. Ecol. 66, 637-644.
20. Janbon, G., Sherman, F., and Rustchenko, E. (1998). Monosomy of a specific chromosome determines L-sorbose utilization: a novel regulatory mechanism in Candida albicans. Proc. Natl. Acad. Sci. USA 95, 5150-5155.
21. Kolotila, M. P., and Diamond, R. D. (1990). Effects of neutrophils and in vitro oxidants on survival and phenotypic switching of Candida albicans WO-1. Infect. Immun. 58, 1174-1179.
22. Krogh, B. O., and Symington, L. S. (2004). Recombination proteins in yeast. Annu. Rev. Genet. 38, 233-271.
23. Kvaal, C., Lachke, S. A., Srikantha, T., Daniels, K., McCoy, J., and Soll, D. R. (1999). Misexpression of the opaque-phase-specific gene PEP1 (SAP1) in the white phase of Candida albicans confers increased virulence in a mouse model of cutaneous infection. Infect. Immun. 67, 6652-6662.
24. Kvaal, C. A., Srikantha, T., and Soll, D. R. (1997). Misexpression of the white-phase-specific gene WH11 in the opaque phase of Candida albicans affects switching and virulence. Infect. Immun. 65, 4468-4475.
25. Lan, C. Y., Newport, G., Murillo, L. A., Jones, T., Scherer, S., Davis, R. W., and Agabian, N. (2002). Metabolic specialization associated with phenotypic switching in Candida albicans. Proc. Natl. Acad. Sci. USA 99, 14907-14912.
26. Lockhart, S. R., Pujol, C., Daniels, K. J., Miller, M. G., Johnson, A. D., Pfaller, M. A., and Soll, D. R. (2002). In Candida albicans, white-opaque switchers are homozygous for mating type. Genetics 162, 737-745.
27. Lohse, M. B., and Johnson, A. D. (2008). Differential phagocytosis of white versus opaque Candida albicans by Drosophila and mouse phagocytes. PLoS ONE 3, e1473.
28. Miller, M. G., and Johnson, A. D. (2002). White-opaque switching in Candida albicans is controlled by mating-type locus homeodomain proteins and allows efficient mating. Cell 110, 293-302.
29. Morrow, B., Anderson, J., Wilson, J., and Soll, D. R. (1989). Bidirectional stimulation of the white-opaque transition of Candida albicans by ultraviolet irradiation. J. Gen. Microbiol. 135, 1201-1208.
30. Nathan, C. (2006). Neutrophils and immunity: challenges and opportunities. Nat. Rev. 6, 173-182.
31. Noble, S. M., and Johnson, A. D. (2005). Strains and strategies for large-scale gene deletion studies of the diploid human fungal pathogen Candida albicans. Eukaryot. Cell 4, 298-309.
32. Odds, F. C., et al. (2007). Molecular phylogenetics of Candida albicans. Eukaryot. Cell 6, 1041-1052.
33. Park, Y. N., and Morschhauser, J. (2005). Tetracycline-inducible gene expression and gene deletion in Candida albicans. Eukaryot. Cell 4, 1328-1342.
34. Pujol, C., Pfaller, M., and Soll, D. R. (2002). Ca3 fingerprinting of Candida albicans bloodstream isolates from the United States, Canada, South America, and Europe reveals a European clade. J. Clin. Microbiol. 40, 2729-2740.
35. Ramirez-Zavala, B., Reuss, O., Park, Y. N., Ohlsen, K., and Morschhauser, J. (2008). Environmental induction of white-opaque switching in Candida albicans. PLoS Pathog. 4, e1000089.
36. Reuss, O., Vik, A., Kolter, R., and Morschhauser, J. (2004). The SAT1 flipper, an optimized tool for gene disruption in Candida albicans. Gene 341, 119-127.
37. Rikkerink, E. H., Magee, B. B., and Magee, P. T. (1988). Opaque-white phenotype transition: a programmed morphological transition in Candida albicans. J. Bacteriol. 170, 895-899.
38. Sakano, K., Oikawa, S., Hasegawa, K., and Kawanishi, S. (2001). Hydroxyurea induces site-specific DNA damage via formation of hydrogen peroxide and nitric oxide. Jpn. J. Cancer Res. 92, 1166-1174.
39. Sherwood, R. K., and Bennett, R. J. (2008). The microtubule motor protein Kar3 is required for normal mitotic division and morphogenesis in Candida albicans. Eukaryot. Cell 7, 1460-1474.
40. Shi, Q. M., Wang, Y. M., Zheng, X. D., Lee, R. T., and Wang, Y. (2007). Critical role of DNA checkpoints in mediating genotoxic-stress-induced filamentous growth in Candida albicans. Mol. Biol. Cell 18, 815-826.
41. Slutsky, B., Staebell, M., Anderson, J., Risen, L., Pfaller, M., and Soll, D. R. (1987). "White-opaque transition": a second high-frequency switching system in Candida albicans. J. Bacteriol. 169, 189-197.
42. Sonneborn, A., Tebarth, B., and Ernst, J. F. (1999). Control of white-opaque phenotypic switching in Candida albicans by the Efg1p morphogenetic regulator. Infect. Immun. 67, 4655-4660.
43. Srikantha, T., Borneman, A. R., Daniels, K. J., Pujol, C., Wu, W., Seringhaus, M. R., Gerstein, M., Yi, S., Snyder, M., and Soll, D. R. (2006). TOS9 regulates white-opaque switching in Candida albicans. Eukaryot. Cell 5, 1674-1687.
44. Srikantha, T., Tsai, L. K., Daniels, K., and Soll, D. R. (2000). EFG1 null mutants of Candida albicans switch but cannot express the complete phenotype of white-phase budding cells. J. Bacteriol. 182, 1580-1591.
45. Tsong, A. E., Miller, M. G., Raisner, R. M., and Johnson, A. D. (2003). Evolution of a combinatorial transcriptional circuit: a case study in yeasts. Cell 115, 389-399.
46. Vinces, M. D., and Kumamoto, C. A. (2007). The morphogenetic regulator Czf1p is a DNA-binding protein that regulates white opaque switching in Candida albicans. Microbiology 153, 2877-2884.
47. Yi, S., Sahni, N., Daniels, K. J., Pujol, C., Srikantha, T., and Soll, D. R. (2008). The same receptor, G protein, and mitogen-activated protein kinase pathway activate different downstream regulators in the alternative white and opaque pheromone responses of Candida albicans. Mol. Biol. Cell 19, 957-970.
48. Zhao, X., Muller, E. G., and Rothstein, R. (1998). A suppressor of two essential checkpoint genes identifies a novel protein that negatively affects dNTP pools. Mol. Cell 2, 329-340.
49. Zordan, R. E., Galgoczy, D. J., and Johnson, A. D. (2006). Epigenetic properties of white-opaque switching in Candida albicans are based on a self-sustaining transcriptional feedback loop. Proc. Natl. Acad. Sci. USA103, 12807-12812.
50. Zordan, R. E., Miller, M. G., Galgoczy, D. J., Tuch, B. B., and Johnson, A. D. (2007). Interlocking transcriptional feedback loops control white-opaque switching in Candida albicans. PLoS Biol. 5, e256.