Genetic and phenotypic intra-species variation in Candida albicans

Genome Research

Volumn 25, Issue 3, 2015, Pages 413-425

  Hirakawa, Matthew P ^a   Martinez, Diego A ^b   Sakthikumar, Sharadha ^b   Anderson, Matthew Z ^a,c   Berlin, Aaron ^b   Gujja, Sharvari ^b   Zeng, Qiandong ^b   Zisson, Ethan ^a   Wang, Joshua M ^a   Greenberg, Joshua M ^a   Berman, Judith ^c,d   Bennett, Richard J ^a   Cuomo, Christina A ^b  

^a BROWN UNIVERSITY   (United States)

^b BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^c UNIVERSITY OF MINNESOTA   (United States)

^d TEL AVIV UNIVERSITY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MEMBRANE PROTEIN; GENOMIC DNA;

AMINO ACID SUBSTITUTION; ANEUPLOIDY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIFUNGAL RESISTANCE; ARTICLE; BIOFILM; CANDIDA ALBICANS; CELL ADHESION; CHROMOSOME 4; CHROMOSOME 7; CHROMOSOME INVERSION; CONTROLLED STUDY; COPY NUMBER VARIATION; DIPLOIDY; FUNGAL CELL; FUNGAL GENE; FUNGAL GENETICS; FUNGAL VIRULENCE; FUNGUS GROWTH; GALLERIA MELLONELLA; GENE SEQUENCE; GENETIC POLYMORPHISM; GENETIC VARIABILITY; GENOME ANALYSIS; GROWTH RATE; HETEROZYGOSITY; HETEROZYGOSITY LOSS; MOUSE; NONHUMAN; NONSENSE MUTATION; PHENOTYPIC VARIATION; PHYLOGENY; PRIORITY JOURNAL; CANDIDIASIS; CHROMOSOME; CLASSIFICATION; DNA SEQUENCE; FUNGAL GENOME; GENETIC SELECTION; GENETICS; GENOTYPE; HUMAN; MICROBIOLOGY; MOLECULAR EVOLUTION; PHENOTYPE; SINGLE NUCLEOTIDE POLYMORPHISM;

CANDIDA ALBICANS; FUNGI;

ANEUPLOIDY; CANDIDA ALBICANS; CANDIDIASIS; CHROMOSOMES, FUNGAL; DNA COPY NUMBER VARIATIONS; EVOLUTION, MOLECULAR; GENETIC VARIATION; GENOME, FUNGAL; GENOTYPE; HUMANS; PHENOTYPE; PHYLOGENY; POLYMORPHISM, SINGLE NUCLEOTIDE; SELECTION, GENETIC; SEQUENCE ANALYSIS, DNA;

EID: 84923925533     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.174623.114     Document Type: Article

References (105)

1. Abbey D, Hickman M, Gresham D, Berman J. 2011. High-resolution SNP/ CGH microarrays reveal the accumulation of loss of heterozygosity in commonly used Candida albicans strains. G3 (Bethesda) 1: 523-530.
2. Alby K, Schaefer D, Bennett RJ. 2009. Homothallic and heterothallic mating in the opportunistic pathogen Candida albicans. Nature 460: 890-893.
3. Anderson MZ, Gerstein AC, Wigen L, Baller JA, Berman J. 2014. Silencing is noisy: population and cell level noise in telomere-adjacent genes is dependent on telomere position and Sir2. PLoS Genet 10: e1004436.
4. Baillie GS, Douglas LJ. 1999. Role of dimorphism in the development of Candida albicans biofilms. J Med Microbiol 48: 671-679.
5. Barton RC, Gull K. 1992. Isolation, characterization, and genetic analysis of monosomic, aneuploid mutants of Candida albicans . Mol Microbiol 6:171-177.
6. Bennett RJ, Johnson AD. 2003. Completion of a parasexual cycle in Candida albicans by induced chromosome loss in tetraploid strains. EMBO J 22: 2505-2515.
7. Bennett RJ, Forche A, Berman J. 2014. Rapid mechanisms for generating genome diversity: whole ploidy shifts, aneuploidy, and loss of heterozygosity. Cold Spring Harb Perspect Med 4: a019604.
8. Berman J, Hadany L. 2012. Does stress induce (para)sex? Implications for Candida albicans evolution. Trends Genet 28: 197-203.
9. Blignaut E, Pujol C, Lockhart S, Joly S, Soll DR. 2002. Ca3 fingerprinting of Candida albicans isolates from human immunodeficiency virus-positive and healthy individuals reveals a new clade in South Africa. J Clin Microbiol 40: 826-836.
10. Bouchonville K, Forche A, Tang KE, Selmecki A, Berman J. 2009. Aneuploid chromosomes are highly unstable during DNA transformation of Candida albicans. Eukaryot Cell 8: 1554-1566.
11. Bougnoux ME, Aanensen DM, Morand S, Th'eraud M, Spratt BG, d'Enfert C. 2004. Multilocus sequence typing of Candida albicans: strategies, data exchange and applications. Infect Genet Evol 4: 243-252.
12. Braun BR, Johnson AD. 2000. TUP1, CPH1 and EFG1 make independent contributions to filamentation in Candida albicans . Genetics 155: 57-67.
13. Butler G, Rasmussen MD, Lin MF, Santos MA, Sakthikumar S, Munro CA, Rheinbay E, Grabherr M, Forche A, Reedy JL, et al. 2009. Evolution of pathogenicity and sexual reproduction in eight Candida genomes. Nature 459: 657-662.
14. Chen X, Magee BB, Dawson D, Magee PT, Kumamoto CA. 2004.
15. Chromosome 1 trisomy compromises the virulence of Candida albicans. Mol Microbiol 51: 551-565.
16. Chen K, Wallis JW, McLellan MD, Larson DE, Kalicki JM, Pohl CS, McGrath SD, Wendl MC, Zhang Q, Locke DP, et al. 2009. BreakDancer: an algorithm for high-resolution mapping of genomic structural variation. Nat Methods 6: 677-681.
17. Chibana H, Beckerman JL, Magee PT. 2000. Fine-resolution physical mapping of genomic diversity in Candida albicans . Genome Res 10: 1865-1877.
18. Coste AT, Turner V, Ischer F, Morschhäuser J, Forche A, Selmecki A, Berman J, Bille J, Sanglard D. 2006. A mutation in Tac1p, a transcription factor regulating CDR1 and CDR2, is coupled with loss of heterozygosity at Chromosome 5 to mediate antifungal resistance in Candida albicans. Genetics 172: 2139-2156.
19. Drosophila 12 Genomes Consortium. 2007. Evolution of genes and genomes on the Drosophila phylogeny. Nature 450: 203-218.
20. Dunkel N, Blass J, Rogers PD, Morschhäuser J. 2008. Mutations in the multidrug resistance regulator MRR1, followed by loss of heterozygosity, are the main cause of MDR1 overexpression in fluconazole-resistant Candida albicans strains. Mol Microbiol 69: 827-840.
21. Finkel JS, Mitchell AP. 2011. Genetic control of Candida albicans biofilm development. Nat Rev Microbiol 9: 109-118.
22. Fisher S, Barry A, Abreu J, Minie B, Nolan J, Delorey TM, Young G, Fennell TJ, Allen A, Ambrogio L, et al. 2011. A scalable, fully automated process for construction of sequence-ready human exome targeted capture libraries. Genome Biol 12: R1.
23. Forche A, Alby K, Schaefer D, Johnson AD, Berman J, Bennett RJ. 2008. The parasexual cycle in Candida albicans provides an alternative pathway to meiosis for the formation of recombinant strains. PLoS Biol 6: e110.
24. Forche A, Abbey D, Pisithkul T, Weinzierl MA, Ringstrom T, Bruck D, Petersen K, Berman J. 2011. Stress alters rates and types of loss of heterozygosity in Candida albicans . MBio 2: e00129-11.
25. Fuchs BB, Eby J, Nobile CJ, El Khoury JB, Mitchell AP, Mylonakis E. 2010a. Role of filamentation in Galleria mellonella killing by Candida albicans. Microbes Infect 12: 488-496.
26. Fuchs BB, O'Brien E, Khoury JB, Mylonakis E. 2010b. Methods for using Galleria mellonella as a model host to study fungal pathogenesis. Virulence 1: 475-482.
27. Gnerre S, Maccallum I, Przybylski D, Ribeiro FJ, Burton JN, Walker BJ, Sharpe T, Hall G, Shea TP, Sykes S, et al. 2011. High-quality draft assemblies of mammalian genomes from massively parallel sequence data. Proc Natl Acad Sci 108: 1513-1518.
28. Goodwin TJ, Ormandy JE, Poulter RT. 2001. L1-like non-LTR retrotransposons in the yeast Candida albicans . Curr Genet 39: 83-91.
29. Grad YH, Lipsitch M, FeldgardenM, Arachchi HM, Cerqueira GC, Fitzgerald M, Godfrey P, Haas BJ, Murphy CI, Russ C, et al. 2012. Genomic epidemiology of the Escherichia coli O104:H4 outbreaks in Europe, 2011. Proc Natl Acad Sci 109: 3065-3070.
30. Gudlaugsson O, Gillespie S, Lee K, Vande Berg J, Hu J, Messer S, Herwaldt L, Pfaller M, Diekema D. 2003. Attributable mortality of nosocomial candidemia, revisited. Clin Infect Dis 37: 1172-1177.
31. Guthrie C, Fink GR. 1991. Guide to yeast genetics and molecular biology. Academic Press, San Diego, CA.
32. Harrison BD, Hashemi J, Bibi M, Pulver R, Bavli D, Nahmias Y, Wellington M, Sapiro G, Berman J. 2014. A tetraploid intermediate precedes aneuploid formation in yeasts exposed to fluconazole. PLoS Biol 12: e1001815.
33. Hickman MA, Zeng G, Forche A, Hirakawa MP, Abbey D, Harrison BD, Wang YM, Su CH, Bennett RJ, Wang Y, et al. 2013. The 'obligate diploid' Candida albicans forms mating-competent haploids. Nature 494: 55-59.
34. Holton NJ, Goodwin TJ, Butler MI, Poulter RT. 2001. An active retrotransposon in Candida albicans. Nucleic Acids Res 29: 4014-4024.
35. Hsueh YP, Idnurm A, Heitman J. 2006. Recombination hotspots flank the Cryptococcus mating-type locus: implications for the evolution of a fungal sex chromosome. PLoS Genet 2: e184.
36. Hull CM, Johnson AD. 1999. Identification of a mating type-like locus in the asexual pathogenic yeast Candida albicans. Science 285: 1271-1275.
37. Hull CM, Raisner RM, Johnson AD. 2000. Evidence for mating of the "asexual" yeast Candida albicans in amammalian host. Science 289: 307-310.
38. Jacobsen ID. 2014. Galleria mellonella as a model host to study virulence of Candida. Virulence 5: 237-239.
39. Janbon G, Sherman F, Rustchenko E. 1998. Monosomy of a specific chromosome determines L-sorbose utilization: a novel regulatory mechanism in Candida albicans. Proc Natl Acad Sci 95: 5150-5155.
40. Jones T, Federspiel NA, Chibana H, Dungan J, Kalman S, Magee BB, Newport G, Thorstenson YR, Agabian N, Magee PT, et al. 2004. The diploid genome sequence of Candida albicans. Proc Natl Acad Sci 101: 7329-7334.
41. Kleinegger CL, Lockhart SR, Vargas K, Soll DR. 1996. Frequency, intensity, species, and strains of oral Candida vary as a function of host age. J Clin Microbiol 34: 2246-2254.
42. Korting HC, Hube B, Oberbauer S, Januschke E, Hamm G, Albrecht A, Borelli C, Schaller M. 2003. Reduced expression of the hyphal-independent Candida albicans proteinase genes SAP1 and SAP3 in the efg1 mutant is associated with attenuated virulence during infection of oral epithelium. J Med Microbiol 52: 623-632.
43. Kumamoto CA, Vinces MD. 2005. Alternative Candida albicans lifestyles: growth on surfaces. Annu Rev Microbiol 59: 113-133.
44. Legrand M, Lephart P, Forche A, Mueller FM, Walsh T, Magee PT, Magee BB. 2004. Homozygosity at the MTL locus in clinical strains of Candida albicans: karyotypic rearrangements and tetraploid formation. Mol Microbiol 52: 1451-1462.
45. Li H, Durbin R. 2010. Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 26: 589-595.
46. Li X, Yan Z, Xu J. 2003. Quantitative variation of biofilms among strains in natural populations of Candida albicans. Microbiology 149: 353-362.
47. Lo HJ, Köhler JR, DiDomenico B, Loebenberg D, Cacciapuoti A, FinkGR. 1997. Nonfilamentous C. albicans mutants are avirulent. Cell 90: 939-949.
48. Lockhart SR, Reed BD, Pierson CL, Soll DR. 1996. Most frequent scenario for recurrent Candida vaginitis is strain maintenance with "substrain shuffling": demonstration by sequential DNA fingerprinting with probes Ca3, C1, and CARE2. J Clin Microbiol 34: 767-777.
49. Lockhart SR, Pujol C, Daniels KJ, Miller MG, Johnson AD, Pfaller MA, Soll DR. 2002. In Candida albicans, white-opaque switchers are homozygous for mating type. Genetics 162: 737-745.
50. Lohse MB, Johnson AD. 2009. White-opaque switching in Candida albicans. Curr Opin Microbiol 12: 650-654.
51. Luo H, Hughes AL. 2012. dN/dS does not show positive selection drives separation of polar-tropical SAR11 populations. Mol Syst Biol 8: 625.
52. MacCallum DM, Castillo L, Nather K, Munro CA, Brown AJ, Gow NA, Odds FC. 2009. Property differences among the four major Candida albicans strain clades. Eukaryot Cell 8: 373-387.
53. Magee BB, Magee PT. 2000. Induction of mating in Candida albicans by construction of MTLa and MTLa strains. Science 289: 310-313.
54. McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M, et al. 2010. The Genome Analysis Toolkit: aMapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20: 1297-1303.
55. Miller MG, Johnson AD. 2002. White-opaque switching in Candida albicans is controlled by mating-type locus homeodomain proteins and allows efficient mating. Cell 110: 293-302.
56. Muzzey D, Schwartz K, Weissman JS, Sherlock G. 2013. Assembly of a phased diploid Candida albicans genome facilitates allele-specific measurements and provides a simple model for repeat and indel structure. Genome Biol 14: R97.
57. Nobile CJ, Mitchell AP. 2006. Genetics and genomics of Candida albicans biofilm formation. Cell Microbiol 8: 1382-1391.
58. Nobile CJ, Fox EP, Nett JE, Sorrells TR, Mitrovich QM, Hernday AD, Tuch BB, Andes DR, Johnson AD. 2012. A recently evolved transcriptional network controls biofilm development in Candida albicans. Cell 148: 126-138.
59. Noble SM, French S, Kohn LA, Chen V, Johnson AD. 2010. Systematic screens of a Candida albicans homozygous deletion library decouple morphogenetic switching and pathogenicity. Nat Genet 42: 590-598.
60. Noffz CS, Liedschulte V, Lengeler K, Ernst JF. 2008. Functional mapping of the Candida albicans Efg1 regulator. Eukaryot Cell 7: 881-893.
61. Odds FC, Bougnoux ME, Shaw DJ, Bain JM, Davidson AD, Diogo D, Jacobsen MD, Lecomte M, Li SY, Tavanti A, et al. 2007. Molecular phylogenetics of Candida albicans. Eukaryot Cell 6: 1041-1052.
62. Pande K, Chen C, Noble SM. 2013. Passage through the mammalian gut triggers a phenotypic switch that promotes Candida albicans commensalism. Nat Genet 45: 1088-1091.
63. Pavelka N, Rancati G, Zhu J, Bradford WD, Saraf A, Florens L, Sanderson BW, Hattem GL, Li R. 2010. Aneuploidy confers quantitative proteome changes and phenotypic variation in budding yeast. Nature 468: 321-325.
64. Perepnikhatka V, Fischer FJ, Niimi M, Baker RA, Cannon RD, Wang YK, Sherman F, Rustchenko E. 1999. Specific chromosome alterations in fluconazole-resistant mutants of Candida albicans. J Bacteriol 181: 4041-4049.
65. Pfaller MA, Diekema DJ. 2007. Epidemiology of invasive candidiasis: a persistent public health problem. Clin Microbiol Rev 20: 133-163.
66. Phan QT, Myers CL, Fu Y, Sheppard DC, Yeaman MR, Welch WH, Ibrahim AS, Edwards JE Jr, Filler SG. 2007. Als3 is a Candida albicans invasin that binds to cadherins and induces endocytosis by host cells. PLoS Biol 5: e64.
67. Pierce JV, Kumamoto CA. 2012. Variation in Candida albicans EFG1 expression enables host-dependent changes in colonizing fungal populations. MBio 3: e00117-12.
68. Pierce JV, Dignard D, Whiteway M, Kumamoto CA. 2013. Normal adaptation of Candida albicans to the murine gastrointestinal tract requires Efg1p-dependent regulation of metabolic and host defense genes. Eukaryot Cell 12: 37-49.
69. Pryszcz LP, Németh T, Gácser A, Gabaldón T. 2013. Unexpected genomic variability in clinical and environmental strains of the pathogenic yeast Candida parapsilosis . Genome Biol Evol 5: 2382-2392.
70. Pujol C, Pfaller M, Soll DR. 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.
71. Ram AF, Klis FM. 2006. Identification of fungal cell wall mutants using susceptibility assays based on Calcofluor white and Congo red. Nat Protoc 1: 2253-2256.
72. Richard ML, Plaine A. 2007. Comprehensive analysis of glycosylphosphatidylinositol-anchored proteins in Candida albicans. Eukaryot Cell 6: 119-133.
73. Rustchenko E. 2007. Chromosome instability in Candida albicans. FEMS Yeast Res 7: 2-11.
74. Rustchenko EP, Howard DH, Sherman F. 1997. Variation in assimilating functions occurs in spontaneous Candida albicans mutants having chromosomal alterations. Microbiology 143: 1765-1778.
75. Rustchenko-Bulgac EP. 1991. Variations of Candida albicans electrophoretic karyotypes. J Bacteriol 173: 6586-6596.
76. Rustchenko-Bulgac EP, Sherman F, Hicks JB. 1990. Chromosomal rearrangements associated withmorphological mutants provide ameans for genetic variation of Candida albicans. J Bacteriol 172: 1276-1283.
77. Sampaio P, Santos M, Correia A, Amaral FE, Chav'ez-Galarza J, Costa-de- Oliveira S, Castro AG, Pedrosa J, Pais C. 2010. Virulence attenuation of Candida albicans genetic variants isolated from a patientwith a recurrent bloodstream infection. PLoS ONE 5: e10155.
78. Selmecki A, Forche A, Berman J. 2006. Aneuploidy and isochromosome formation in drug-resistant Candida albicans. Science 313: 367-370.
79. Selmecki A, Gerami-Nejad M, Paulson C, Forche A, Berman J. 2008. An isochromosome confers drug resistance in vivo by amplification of two genes, ERG11 and TAC1. Mol Microbiol 68: 624-641.
80. Selmecki A, Forche A, Berman J. 2010. Genomic plasticity of the human fungal pathogen Candida albicans . Eukaryot Cell 9: 991-1008.
81. Siegel JJ, Amon A. 2012. New insights into the troubles of aneuploidy. Annu Rev Cell Dev Biol 28: 189-214.
82. Slutsky B, Buffo J, Soll DR. 1985. High-frequency switching of colony morphology in Candida albicans . Science 230: 666-669.
83. Slutsky B, Staebell M, Anderson J, Risen L, Pfaller M, Soll DR. 1987. "White-opaque transition": a second high-frequency switching system in Candida albicans. J Bacteriol 169: 189-197.
84. Soll DR. 1993. High frequency phenotypic switching in Candida albicans. Trends Genet 9: 61-65.
85. Sonneborn A, Tebarth B, Ernst JF. 1999. Control of white-opaque phenotypic switching in Candida albicans by the Efg1p morphogenetic regulator. Infect Immun 67: 4655-4660.
86. Srikantha T, Tsai LK, Daniels K, Soll DR. 2000. EFG1 null mutants of Candida albicans switch but cannot express the complete phenotype of whitephase budding cells. J Bacteriol 182: 1580-1591.
87. Stoldt VR, Sonneborn A, Leuker CE, Ernst JF. 1997. Efg1p, an essential regulator of morphogenesis of the human pathogen Candida albicans, is a member of a conserved class of bHLH proteins regulating morphogenetic processes in fungi. EMBO J 16: 1982-1991.
88. Sudbery PE. 2011. Growth of Candida albicans hyphae. Nat Rev Microbiol 9: 737-748.
89. Suzuki T, Nishibayashi S, Kuroiwa T, Kanbe T, Tanaka K. 1982. Variance of ploidy in Candida albicans. J Bacteriol 152: 893-896.
90. Tao L, Du H, Guan G, Dai Y, Nobile CJ, Liang W, Cao C, Zhang Q, Zhong J, Huang G. 2014. Discovery of a "white-gray-opaque" tristable phenotypic switching system in Candida albicans: roles of non-genetic diversity in host adaptation. PLoS Biol 12: e1001830.
91. Tavanti A, Davidson AD, Fordyce MJ, Gow NA, Maiden MC, Odds FC. 2005. Population structure and properties of Candida albicans, as determined by multilocus sequence typing. J Clin Microbiol 43: 5601-5613.
92. Tibayrenc M. 1997. Are Candida albicans natural populations subdivided?Trends Microbiol 5: 253-254.
93. Torres EM, Sokolsky T, Tucker CM, Chan LY, Boselli M, Dunham MJ, Amon A. 2007. Effects of aneuploidy on cellular physiology and cell division in haploid yeast. Science 317: 916-924.
94. van het Hoog M, Rast TJ, Martchenko M, Grindle S, Dignard D, Hogues H, Cuomo C, Berriman M, Scherer S, Magee BB, et al. 2007. Assembly of the Candida albicans genome into sixteen supercontigs aligned on the eight chromosomes. Genome Biol 8: R52.
95. Viaud MC, Balhadère PV, Talbot NJ. 2002. A Magnaporthe grisea cyclophilin acts as a virulence determinant during plant infection. Plant Cell 14: 917-930.
96. Wang P, Cardenas ME, Cox GM, Perfect JR, Heitman J. 2001. Two cyclophilin A homologs with shared and distinct functions important for growth and virulence of Cryptococcus neoformans. EMBO Rep 2: 511-518.
97. Wey SB, Mori M, Pfaller MA, Woolson RF, Wenzel RP. 1988. Hospitalacquired candidemia. The attributable mortality and excess length of stay. Arch Intern Med 148: 2642-2645.
98. White TC. 1997. The presence of an R467K amino acid substitution and loss of allelic variation correlate with an azole-resistant lanosterol 14a demethylase in Candida albicans. Antimicrob Agents Chemother 41: 1488-1494.
99. Wolf JB, Künstner A, Nam K, Jakobsson M, Ellegren H. 2009. Nonlinear dynamics of nonsynonymous (d N) and synonymous (dS) substitution rates affects inference of selection. Genome Biol Evol 1: 308-319.
100. Wu W, Pujol C, Lockhart SR, Soll DR. 2005. Chromosome loss followed by duplication is the major mechanism of spontaneous mating-type locus homozygosis in Candida albicans. Genetics 169: 1311-1327.
101. Wu W, Lockhart SR, Pujol C, Srikantha T, Soll DR. 2007. Heterozygosity of genes on the sex chromosome regulates Candida albicans virulence. Mol Microbiol 64: 1587-1604.
102. Yang F, Yan TH, Rustchenko E, Gao PH, Wang Y, Yan L, Cao YY, Wang QJ, Ji H, Cao YB, et al. 2011. High-frequency genetic contents variations in clinical Candida albicans isolates. Biol Pharm Bull 34: 624-631.
103. Zhang A, Petrov KO, Hyun ER, Liu Z, Gerber SA, Myers LC. 2012. The Tlo proteins are stoichiometric components of Candida albicans mediator anchored via the Med3 subunit. Eukaryot Cell 11: 874-884.
104. ZhuW, Filler SG. 2009. Interactions of Candida albicans with epithelial cells. Cell Microbiol 12: 273-282.
105. Zordan RE, Miller MG, Galgoczy DJ, Tuch BB, Johnson AD. 2007. Interlocking transcriptional feedback loops control white-opaque switching in Candida albicans. PLoS Biol 5: e256.