Epigenetic determinants of phenotypic plasticity in Candida albicans

Fungal Biology Reviews

Volumn 32, Issue 1, 2018, Pages 10-19

  Rai, Laxmi Shanker ^a   Singha, Rima ^a   Brahma, Priya ^a   Sanyal, Kaustuv ^a  

^a JAWAHARLAL NEHRU CENTRE FOR ADVANCED SCIENTIFIC RESEARCH   (India)

Author keywords

Biofilm; Chromatin; Filamentation; Histones; Opaque; Post translational modifications

Indexed keywords

EID: 85027562964     PISSN: 17494613     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.fbr.2017.07.002     Document Type: Review

References (119)

1. Alby, K., Bennett, R.J., Stress-induced phenotypic switching in Candida albicans. Mol. Biol. Cell 20 (2009), 3178–3191.
2. Anderson, J.M., Soll, D.R., Unique phenotype of opaque cells in the white-opaque transition of Candida albicans. J. Bacteriol. 169 (1987), 5579–5588.
3. Baillie, G.S., Douglas, L.J., Role of dimorphism in the development of Candida albicans biofilms. J. Med. Microbiol. 48 (1999), 671–679.
4. Becker, P.B., Horz, W., ATP-dependent nucleosome remodeling. Annu. Rev. Biochem. 71 (2002), 247–273.
5. Berman, J., Sudbery, P.E., Candida albicans: a molecular revolution built on lessons from budding yeast. Nat. Rev. Genet. 3 (2002), 918–930.
6. Bernstein, D.A., Vyas, V.K., Weinberg, D.E., Drinnenberg, I.A., Bartel, D.P., et al. Candida albicans Dicer (CaDcr1) is required for efficient ribosomal and spliceosomal RNA maturation. Proc. Natl. Acad. Sci. U. S. A. 109 (2012), 523–528.
7. Bonisch, C., Nieratschker, S.M., Orfanos, N.K., Hake, S.B., Chromatin proteomics and epigenetic regulatory circuits. Expert Rev. Proteomics 5 (2008), 105–119.
8. Bougdour, A., Maubon, D., Baldacci, P., Ortet, P., Bastien, O., et al. Drug inhibition of HDAC3 and epigenetic control of differentiation in Apicomplexa parasites. J. Exp. Med. 206 (2009), 953–966.
9. Braun, B.R., Johnson, A.D., Control of filament formation in Candida albicans by the transcriptional repressor TUP1. Science 277 (1997), 105–109.
10. Brown, A.J.P., Expression of Growth Form-specific Factors During Morphogenesis in Candida albicans. 2002, ASM Press, 87–94.
11. Brownell, J.E., Zhou, J., Ranalli, T., Kobayashi, R., Edmondson, D.G., et al. Tetrahymena histone acetyltransferase A: a homolog to yeast Gcn5p linking histone acetylation to gene activation. Cell 84 (1996), 843–851.
12. Cao, F., Lane, S., Raniga, P.P., Lu, Y., Zhou, Z., et al. The Flo8 transcription factor is essential for hyphal development and virulence in Candida albicans. Mol. Biol. Cell 17 (2006), 295–307.
13. Carlisle, P.L., Banerjee, M., Lazzell, A., Monteagudo, C., Lopez-Ribot, J.L., et al. Expression levels of a filament-specific transcriptional regulator are sufficient to determine Candida albicans morphology and virulence. Proc. Natl. Acad. Sci. U. S. A. 106 (2009), 599–604.
14. Chandra, J., Kuhn, D.M., Mukherjee, P.K., Hoyer, L.L., McCormick, T., et al. Biofilm formation by the fungal pathogen Candida albicans: development, architecture, and drug resistance. J. Bacteriol. 183 (2001), 5385–5394.
15. Chang, P., Fan, X., Chen, J., Function and subcellular localization of Gcn5, a histone acetyltransferase in Candida albicans. Fungal Genet. Biol. 81 (2015), 132–141.
16. Croken, M.M., Nardelli, S.C., Kim, K., Chromatin modifications, epigenetics, and how protozoan parasites regulate their lives. Trends Parasitol. 28 (2012), 202–213.
17. Davis, D., Wilson, R.B., Mitchell, A.P., RIM101-dependent and-independent pathways govern pH responses in Candida albicans. Mol. Cell Biol. 20 (2000), 971–978.
18. Dixon, S.E., Stilger, K.L., Elias, E.V., Naguleswaran, A., Sullivan, W.J. Jr., A decade of epigenetic research in Toxoplasma gondii. Mol. Biochem. Parasitol. 173 (2010), 1–9.
19. Dongari-Bagtzoglou, A., Kashleva, H., Dwivedi, P., Diaz, P., Vasilakos, J., Characterization of mucosal Candida albicans biofilms. PLoS One, 4, 2009, e7967.
20. Donlan, R.M., Costerton, J.W., Biofilms: survival mechanisms of clinically relevant microorganisms. Clin. Microbiol. Rev. 15 (2002), 167–193.
21. Douglas, L.J., Candida biofilms and their role in infection. Trends Microbiol. 11 (2003), 30–36.
22. Drell, T., Lillsaar, T., Tummeleht, L., Simm, J., Aaspollu, A., et al. Characterization of the vaginal micro- and mycobiome in asymptomatic reproductive-age Estonian women. PLoS One, 8, 2013, e54379.
23. Drinnenberg, I.A., Weinberg, D.E., Xie, K.T., Mower, J.P., Wolfe, K.H., et al. RNAi in budding yeast. Science 326 (2009), 544–550.
24. Edmond, M.B., Wallace, S.E., McClish, D.K., Pfaller, M.A., Jones, R.N., et al. Nosocomial bloodstream infections in United States hospitals: a three-year analysis. Clin. Infect. Dis. 29 (1999), 239–244.
25. Egger, G., Liang, G., Aparicio, A., Jones, P.A., Epigenetics in human disease and prospects for epigenetic therapy. Nature 429 (2004), 457–463.
26. Fanning, S., Mitchell, A.P., Fungal biofilms. PLoS Pathog., 8, 2012, e1002585.
27. Fidel, P.L. Jr., Candida-host interactions in HIV disease: relationships in oropharyngeal candidiasis. Adv. Dent. Res. 19 (2006), 80–84.
28. Filler, S.G., Sheppard, D.C., Fungal invasion of normally non-phagocytic host cells. PLoS Pathog., 2, 2006, e129.
29. Findley, K., Oh, J., Yang, J., Conlan, S., Deming, C., et al. Topographic diversity of fungal and bacterial communities in human skin. Nature 498 (2013), 367–370.
30. Fox, E.P., Nobile, C.J., A sticky situation: untangling the transcriptional network controlling biofilm development in Candida albicans. Transcription 3 (2012), 315–322.
31. Garnaud, C., Champleboux, M., Maubon, D., Cornet, M., Govin, J., Histone deacetylases and their inhibition in Candida species. Front. Microbiol., 7, 2016, 1238.
32. Gelato, K.A., Fischle, W., Role of histone modifications in defining chromatin structure and function. Biol. Chem. 389 (2008), 353–363.
33. Gomez-Diaz, E., Jorda, M., Peinado, M.A., Rivero, A., Epigenetics of host-pathogen interactions: the road ahead and the road behind. PLoS Pathog., 8, 2012, e1003007.
34. Gow, N.A., Brown, A.J., Odds, F.C., Fungal morphogenesis and host invasion. Curr. Opin. Microbiol. 5 (2002), 366–371.
35. Guan, Z., Liu, H., Overlapping functions between SWR1 deletion and H3K56 acetylation in Candida albicans. Eukaryot. Cell 14 (2015), 578–587.
36. Guillemette, B., Drogaris, P., Lin, H.H., Armstrong, H., Hiragami-Hamada, K., et al. H3 lysine 4 is acetylated at active gene promoters and is regulated by H3 lysine 4 methylation. PLoS Genet., 7, 2011, e1001354.
37. Hakimi, M.A., Deitsch, K.W., Epigenetics in Apicomplexa: control of gene expression during cell cycle progression, differentiation and antigenic variation. Curr. Opin. Microbiol. 10 (2007), 357–362.
38. Hall, S.E., Chirn, G.W., Lau, N.C., Sengupta, P., RNAi pathways contribute to developmental history-dependent phenotypic plasticity in C. elegans. RNA 19 (2013), 306–319.
39. Hawser, S.P., Baillie, G.S., Douglas, L.J., Production of extracellular matrix by Candida albicans biofilms. J. Med. Microbiol. 47 (1998), 253–256.
40. Hemberger, M., Dean, W., Reik, W., Epigenetic dynamics of stem cells and cell lineage commitment: digging Waddington's canal. Nat. Rev. Mol. Cell Biol. 10 (2009), 526–537.
41. Hnisz, D., Bardet, A.F., Nobile, C.J., Petryshyn, A., Glaser, W., et al. A histone deacetylase adjusts transcription kinetics at coding sequences during Candida albicans morphogenesis. PLoS Genet., 8, 2012, e1003118.
42. Hnisz, D., Majer, O., Frohner, I.E., Komnenovic, V., Kuchler, K., The Set3/Hos2 histone deacetylase complex attenuates cAMP/PKA signaling to regulate morphogenesis and virulence of Candida albicans. PLoS Pathog., 6, 2010, e1000889.
43. Hnisz, D., Schwarzmuller, T., Kuchler, K., Transcriptional loops meet chromatin: a dual-layer network controls white-opaque switching in Candida albicans. Mol. Microbiol. 74 (2009), 1–15.
44. Hobson, R.P., The global epidemiology of invasive Candida infections–is the tide turning?. J. Hosp. Infect. 55 (2003), 159–168 quiz 233.
45. Hoffmann, C., Dollive, S., Grunberg, S., Chen, J., Li, H., et al. Archaea and fungi of the human gut microbiome: correlations with diet and bacterial residents. PLoS One, 8, 2013, e66019.
46. Huang, G., Srikantha, T., Sahni, N., Yi, S., Soll, D.R., CO(2) regulates white-to-opaque switching in Candida albicans. Curr. Biol. 19 (2009), 330–334.
47. Huang, G., Wang, H., Chou, S., Nie, X., Chen, J., et al. Bistable expression of WOR1, a master regulator of white-opaque switching in Candida albicans. Proc. Natl. Acad. Sci. U. S. A. 103 (2006), 12813–12818.
48. Huang, G., Yi, S., Sahni, N., Daniels, K.J., Srikantha, T., et al. N-acetylglucosamine induces white to opaque switching, a mating prerequisite in Candida albicans. PLoS Pathog., 6, 2010, e1000806.
49. Hube, B., Candida albicans secreted aspartyl proteinases. Curr. Top. Med. Mycol. 7 (1996), 55–69.
50. Hull, C.M., Raisner, R.M., Johnson, A.D., Evidence for mating of the “asexual” yeast Candida albicans in a mammalian host. Science 289 (2000), 307–310.
51. Jacobsen, I.D., Wilson, D., Wachtler, B., Brunke, S., Naglik, J.R., et al. Candida albicans dimorphism as a therapeutic target. Expert Rev. Anti Infect. Ther. 10 (2012), 85–93.
52. Kadosh, D., Johnson, A.D., Induction of the Candida albicans filamentous growth program by relief of transcriptional repression: a genome-wide analysis. Mol. Biol. Cell 16 (2005), 2903–2912.
53. Kaplan, T., Liu, C.L., Erkmann, J.A., Holik, J., Grunstein, M., et al. Cell cycle- and chaperone-mediated regulation of H3K56ac incorporation in yeast. PLoS Genet., 4, 2008, e1000270.
54. Klar, A.J., Srikantha, T., Soll, D.R., A histone deacetylation inhibitor and mutant promote colony-type switching of the human pathogen Candida albicans. Genetics 158 (2001), 919–924.
55. Klein, R.S., Harris, C.A., Small, C.B., Moll, B., Lesser, M., et al. Oral candidiasis in high-risk patients as the initial manifestation of the acquired immunodeficiency syndrome. N. Engl. J. Med. 311 (1984), 354–358.
56. Kohler, J.R., Fink, G.R., Candida albicans strains heterozygous and homozygous for mutations in mitogen-activated protein kinase signaling components have defects in hyphal development. Proc. Natl. Acad. Sci. U. S. A. 93 (1996), 13223–13228.
57. Kuchler, K., Jenull, S., Shivarathri, R., Chauhan, N., Fungal KATs/KDACs: a new highway to better antifungal drugs?. PLoS Pathog., 12, 2016, e1005938.
58. Kumamoto, C.A., Niche-specific gene expression during C. albicans infection. Curr. Opin. Microbiol. 11 (2008), 325–330.
59. Lan, C.Y., Newport, G., Murillo, L.A., Jones, T., Scherer, S., et al. Metabolic specialization associated with phenotypic switching in Candida albicans. Proc. Natl. Acad. Sci. U. S. A. 99 (2002), 14907–14912.
60. Lassak, T., Schneider, E., Bussmann, M., Kurtz, D., Manak, J.R., et al. Target specificity of the Candida albicans Efg1 regulator. Mol. Microbiol. 82 (2011), 602–618.
61. Liu, H., Transcriptional control of dimorphism in Candida albicans. Curr. Opin. Microbiol. 4 (2001), 728–735.
62. Lo, H.J., Kohler, J.R., DiDomenico, B., Loebenberg, D., Cacciapuoti, A., et al. Nonfilamentous C. albicans mutants are avirulent. Cell 90 (1997), 939–949.
63. Lohse, M.B., Hernday, A.D., Fordyce, P.M., Noiman, L., Sorrells, T.R., et al. Identification and characterization of a previously undescribed family of sequence-specific DNA-binding domains. Proc. Natl. Acad. Sci. U. S. A. 110 (2013), 7660–7665.
64. Lopes da Rosa, J., Boyartchuk, V.L., Zhu, L.J., Kaufman, P.D., Histone acetyltransferase Rtt109 is required for Candida albicans pathogenesis. Proc. Natl. Acad. Sci. U. S. A. 107 (2010), 1594–1599.
65. Lu, Y., Su, C., Wang, A., Liu, H., Hyphal development in Candida albicans requires two temporally linked changes in promoter chromatin for initiation and maintenance. PLoS Biol., 9, 2011, e1001105.
66. Magee, B.B., Magee, P.T., Induction of mating in Candida albicans by construction of MTLa and MTLalpha strains. Science 289 (2000), 310–313.
67. Mao, X., Cao, F., Nie, X., Liu, H., Chen, J., The Swi/Snf chromatin remodeling complex is essential for hyphal development in Candida albicans. FEBS Lett. 580 (2006), 2615–2622.
68. Martinez-Gomariz, M., Perumal, P., Mekala, S., Nombela, C., Chaffin, W.L., et al. Proteomic analysis of cytoplasmic and surface proteins from yeast cells, hyphae, and biofilms of Candida albicans. Proteomics 9 (2009), 2230–2252.
69. Mayer, F.L., Wilson, D., Hube, B., Candida albicans pathogenicity mechanisms. Virulence 4 (2013), 119–128.
70. Miller, M.G., Johnson, A.D., White-opaque switching in Candida albicans is controlled by mating-type locus homeodomain proteins and allows efficient mating. Cell 110 (2002), 293–302.
71. Morrow, B., Anderson, J., Wilson, J., Soll, D.R., Bidirectional stimulation of the white-opaque transition of Candida albicans by ultraviolet irradiation. J. Gen. Microbiol. 135 (1989), 1201–1208.
72. Murad, A.M., Leng, P., Straffon, M., Wishart, J., Macaskill, S., et al. NRG1 represses yeast-hypha morphogenesis and hypha-specific gene expression in Candida albicans. EMBO J. 20 (2001), 4742–4752.
73. Nantel, A., Dignard, D., Bachewich, C., Harcus, D., Marcil, A., et al. Transcription profiling of Candida albicans cells undergoing the yeast-to-hyphal transition. Mol. Biol. Cell 13 (2002), 3452–3465.
74. Nicholls, S., MacCallum, D.M., Kaffarnik, F.A., Selway, L., Peck, S.C., et al. Activation of the heat shock transcription factor Hsf1 is essential for the full virulence of the fungal pathogen Candida albicans. Fungal Genet. Biol. 48 (2011), 297–305.
75. Nobile, C.J., Fox, E.P., Hartooni, N., Mitchell, K.F., Hnisz, D., et al. A histone deacetylase complex mediates biofilm dispersal and drug resistance in Candida albicans. MBio 5 (2014), e01201–01214.
76. Nobile, C.J., Fox, E.P., Nett, J.E., Sorrells, T.R., Mitrovich, Q.M., et al. A recently evolved transcriptional network controls biofilm development in Candida albicans. Cell 148 (2012), 126–138.
77. Nobile, C.J., Johnson, A.D., Candida albicans biofilms and human disease. Annu. Rev. Microbiol. 69 (2015), 71–92.
78. Nobile, C.J., Mitchell, A.P., Regulation of cell-surface genes and biofilm formation by the C. albicans transcription factor Bcr1p. Curr. Biol. 15 (2005), 1150–1155.
79. Noble, S.M., Gianetti, B.A., Witchley, J.N., Candida albicans cell-type switching and functional plasticity in the mammalian host. Nat. Rev. Microbiol. 15 (2016), 96–108.
80. Odds, F.C., Pathogenesis of Candida infections. J. Am. Acad. Dermatol. 31 (1994), S2–S5.
81. Pande, K., Chen, C., Noble, S.M., Passage through the mammalian gut triggers a phenotypic switch that promotes Candida albicans commensalism. Nat. Genet. 45 (2013), 1088–1091.
82. Perez-Martin, J., Uria, J.A., Johnson, A.D., Phenotypic switching in Candida albicans is controlled by a SIR2 gene. EMBO J. 18 (1999), 2580–2592.
83. Perlroth, J., Choi, B., Spellberg, B., Nosocomial fungal infections: epidemiology, diagnosis, and treatment. Med. Mycol. 45 (2007), 321–346.
84. Probst, A.V., Dunleavy, E., Almouzni, G., Epigenetic inheritance during the cell cycle. Nat. Rev. Mol. Cell Biol. 10 (2009), 192–206.
85. Pukkila-Worley, R., Peleg, A.Y., Tampakakis, E., Mylonakis, E., Candida albicans hyphal formation and virulence assessed using a Caenorhabditis elegans infection model. Eukaryot. Cell 8 (2009), 1750–1758.
86. Rai, M.N., Balusu, S., Gorityala, N., Dandu, L., Kaur, R., Functional genomic analysis of Candida glabrata-macrophage interaction: role of chromatin remodeling in virulence. PLoS Pathog., 8, 2012, e1002863.
87. Raman, S.B., Nguyen, M.H., Zhang, Z., Cheng, S., Jia, H.Y., et al. Candida albicans SET1 encodes a histone 3 lysine 4 methyltransferase that contributes to the pathogenesis of invasive candidiasis. Mol Microbiol 60 (2006), 697–709.
88. Richmond, T.J., Davey, C.A., The structure of DNA in the nucleosome core. Nature 423 (2003), 145–150.
89. Rojas-Rios, P., Gonzalez-Reyes, A., Concise review: the plasticity of stem cell niches: a general property behind tissue homeostasis and repair. Stem Cells 32 (2014), 852–859.
90. Russell, C., Lay, K.M., Natural history of Candida species and yeasts in the oral cavities of infants. Arch. Oral Biol. 18 (1973), 957–962.
91. Saha, A., Wittmeyer, J., Cairns, B.R., Chromatin remodelling: the industrial revolution of DNA around histones. Nat. Rev. Mol. Cell Biol. 7 (2006), 437–447.
92. Santoro, S.W., Dulac, C., Histone variants and cellular plasticity. Trends Genet. 31 (2015), 516–527.
93. Sasse, C., Hasenberg, M., Weyler, M., Gunzer, M., Morschhauser, J., White-opaque switching of Candida albicans allows immune evasion in an environment-dependent fashion. Eukaryot. Cell 12 (2013), 50–58.
94. Saville, S.P., Lazzell, A.L., Monteagudo, C., Lopez-Ribot, J.L., Engineered control of cell morphology in vivo reveals distinct roles for yeast and filamentous forms of Candida albicans during infection. Eukaryot. Cell 2 (2003), 1053–1060.
95. Schrode, N., Xenopoulos, P., Piliszek, A., Frankenberg, S., Plusa, B., et al. Anatomy of a blastocyst: cell behaviors driving cell fate choice and morphogenesis in the early mouse embryo. Genesis 51 (2013), 219–233.
96. Sellam, A., Askew, C., Epp, E., Lavoie, H., Whiteway, M., et al. Genome-wide mapping of the coactivator Ada2p yields insight into the functional roles of SAGA/ADA complex in Candida albicans. Mol. Biol. Cell 20 (2009), 2389–2400.
97. Slutsky, B., Staebell, M., Anderson, J., Risen, L., Pfaller, M., et al. “White-opaque transition”: a second high-frequency switching system in Candida albicans. J. Bacteriol. 169 (1987), 189–197.
98. Soll, D.R., Candida commensalism and virulence: the evolution of phenotypic plasticity. Acta Trop. 81 (2002), 101–110.
99. Srikantha, T., Borneman, A.R., Daniels, K.J., Pujol, C., Wu, W., et al. TOS9 regulates white-opaque switching in Candida albicans. Eukaryot. Cell 5 (2006), 1674–1687.
100. Srikantha, T., Tsai, L., Daniels, K., Klar, A.J., Soll, D.R., The histone deacetylase genes HDA1 and RPD3 play distinct roles in regulation of high-frequency phenotypic switching in Candida albicans. J. Bacteriol. 183 (2001), 4614–4625.
101. Stevenson, J.S., Liu, H., Regulation of white and opaque cell-type formation in Candida albicans by Rtt109 and Hst3. Mol. Microbiol. 81 (2011), 1078–1091.
102. Stevenson, J.S., Liu, H., Nucleosome assembly factors CAF-1 and HIR modulate epigenetic switching frequencies in an H3K56 acetylation-associated manner in Candida albicans. Eukaryot Cell 12 (2013), 591–603.
103. Sudbery, P., Gow, N., Berman, J., The distinct morphogenic states of Candida albicans. Trends Microbiol. 12 (2004), 317–324.
104. Tao, L., Du, H., Guan, G., Dai, Y., Nobile, C.J., et al. Discovery of a “white-gray-opaque” tristable phenotypic switching system in Candida albicans: roles of non-genetic diversity in host adaptation. PLoS Biol., 12, 2014, e1001830.
105. Thomas, D.P., Bachmann, S.P., Lopez-Ribot, J.L., Proteomics for the analysis of the Candida albicans biofilm lifestyle. Proteomics 6 (2006), 5795–5804.
106. Thompson, D.S., Carlisle, P.L., Kadosh, D., Coevolution of morphology and virulence in Candida species. Eukaryot. Cell 10 (2011), 1173–1182.
107. Tost, J., DNA methylation: an introduction to the biology and the disease-associated changes of a promising biomarker. Methods Mol. Biol. 507 (2009), 3–20.
108. Tscherner, M., Stappler, E., Hnisz, D., Kuchler, K., The histone acetyltransferase Hat1 facilitates DNA damage repair and morphogenesis in Candida albicans. Mol. Microbiol. 86 (2012), 1197–1214.
109. Turner, B.M., Cellular memory and the histone code. Cell 111 (2002), 285–291.
110. van Holde, K.E., Chromatin. 1988.
111. van Wolfswinkel, J.C., Ketting, R.F., The role of small non-coding RNAs in genome stability and chromatin organization. J. Cell Sci. 123 (2010), 1825–1839.
112. Wang, X., Chang, P., Ding, J., Chen, J., Distinct and redundant roles of the two MYST histone acetyltransferases Esa1 and Sas2 in cell growth and morphogenesis of Candida albicans. Eukaryot. Cell 12 (2013), 438–449.
113. Watanabe, S., Radman-Livaja, M., Rando, O.J., Peterson, C.L., A histone acetylation switch regulates H2A.Z deposition by the SWR-C remodeling enzyme. Science 340 (2013), 195–199.
114. Weig, M., Gross, U., Muhlschlegel, F., Clinical aspects and pathogenesis of Candida infection. Trends Microbiol. 6 (1998), 468–470.
115. Wu, J.I., Lessard, J., Crabtree, G.R., Understanding the words of chromatin regulation. Cell 136 (2009), 200–206.
116. Wurtele, H., Tsao, S., Lepine, G., Mullick, A., Tremblay, J., et al. Modulation of histone H3 lysine 56 acetylation as an antifungal therapeutic strategy. Nat. Med. 16 (2010), 774–780.
117. Zarnowski, R., Westler, W.M., Lacmbouh, G.A., Marita, J.M., Bothe, J.R., et al. Novel entries in a fungal biofilm matrix encyclopedia. mBio, 5, 2014 e01333–14.
118. Zordan, R.E., Galgoczy, D.J., Johnson, A.D., Epigenetic properties of white-opaque switching in Candida albicans are based on a self-sustaining transcriptional feedback loop. Proc. Natl. Acad. Sci. U. S. A. 103 (2006), 12807–12812.
119. Zordan, R.E., Miller, M.G., Galgoczy, D.J., Tuch, B.B., Johnson, A.D., Interlocking transcriptional feedback loops control white-opaque switching in Candida albicans. PLoS Biol., 5, 2007, e256.