Candida albicans: A molecular revolution built on lessons from budding yeast

Nature Reviews Genetics

Volumn 3, Issue 12, 2002, Pages 918-930

  Berman, Judith ^a   Sudbery, Peter E ^b  

^a 6 160 Jackson Hall ^*  (United States)

^b UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIFUNGAL AGENT;

CANDIDA ALBICANS; DEATH; DNA MICROARRAY; EVOLUTION; FUNGAL GENE; FUNGEMIA; GENE SEQUENCE; GENOME; GENOME ANALYSIS; HUMAN; IMMUNE DEFICIENCY; INTESTINE FLORA; MOLECULAR GENETICS; MORPHOGENESIS; MUTAGENESIS; NONHUMAN; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; REVIEW; SACCHAROMYCES CEREVISIAE; VIRULENCE; YEAST;

CANDIDA ALBICANS; GENE DELETION; GENOME, FUNGAL; MORPHOGENESIS; MUTAGENESIS; PHENOTYPE; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC; TRANSFECTION;

CANDIDA; CANDIDA ALBICANS; FUNGI; MYXOGASTRIA; SACCHAROMYCES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCETALES;

EID: 0036895608     PISSN: 14710056     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrg948     Document Type: Review

References (120)

1. Beck-Sague, C. & Jarvis, W. R. Secular trends in the epidemiology of nosocomial fungal infections in the United States, 1980-1990. National Nosccomial Infections Surveillance System. J. Infect. Dis. 167, 1247-1251 (1993).
2. Miller, L. G., Hajjeh, R. A. & Edwards, J. E. Jr. Estimating the cost of nosocomial candidemia in the United States. Clin Infect. Dis. 32, 1110 (2001).
3. Berbee, M. L. & Taylor, J. W. in The Mycota Vol. VIIB (eds McLaughlin, D. J. & McLaughlin, E.) 229-246 (Springer, New York, 2000).
4. Hackman, D. et al, Molecular evidence for the early colonization of land by fungi and plants. Science 293, 1129-1133 (2001).
5. Asleson, C. M. et al. Candida albicans INT1-induced filamentation in Saccharomyces cerevisiae depends on Sla2p. Mol. Cell. Biol. 21, 1272-1284 (2001).
6. Scherer, S. in Candida and Candidiasis (ed. Calderone, R. A.) 259-265 (ASM Press, Washington, DC, 2002).
7. Hull, C. M. & Johnson, A. D. Identification of a mating type-like locus in the asexual pathogenic yeast Candida albicans. Science 285, 1271-1275 (1999). The Stanford University-generated genome sequence was used to isolate regions of chromosome 5 that are heterozygous and contain genes (MTLa1, MTLα1 and MTLα2) that resemble the mating-locus genes in S. cerevisiae,
8. Hull, C. M., Raisner, R. M. & Johnson, A. D. Evidence for mating of the 'asexual' yeast Candida albicans in a mammalian host. Science 289, 307-310 (2000).
9. Magee, B. B. & Magee, P. T. Induction of mating in Candida albicans by construction of MTLa and MTLα strains. Science 289, 310-313 (2000). These two papers showed that C. albicans diploid cells that are homozygous for MTLa can generate apparent tetraploid recombinants when mixed with cells that are homozygous for MTLα. Reference 8 showed that this reaction occurs in mice, whereas reference 9 generated in vitro recombinants at room temperature.
10. Pla, J., Perez-Diaz, R. M., Navarro-Garcia, F., Sanchez, M. & Nombela, C. Cloning of the Candida albicans HIS1 gene by direct complementation of a C. albicans histidine auxotroph using an improved double-ARS shuttle vector. Gene 165, 115-120 (1995).
11. Santos, M. A. & Tuite, M. F. The CUG codon is decoded in vivo as serine and not leucine in Candida albicans. Nucleic Acids Res. 23, 1481-1486 (1995).
12. Ernst, J. F. & Bockmühl, D. P. in Candida and Candidiasis (ed. Calderone, R. A.) 267-278 (ASM Press, Washington, DC, 2002).
13. De Backer, M. D., Magee, P. T. & Pla, J. Recent developments in molecular genetics of Candida albicans. Annu. Rev. Microbiol. 54, 463-498 (2000).
14. Fonzi, W. A. & Irwin, M. Y. Isogenic strain construction and gene mapping in Candida albicans. Genetics 134,717-728 (1993).
15. Sundstrom, P., Cutler, J. E. & Staab, J. F. Reevaluation of the role of HWP1 in systemic candidiasis by use of Candida albicans strains with selectable marker URA3 targeted to the ENO1 locus. Infect. Immun. 70, 3281-3283 (2002).
16. Lay, J. et al. Altered expression of selectable marker URA3 in gene-disrupted Candida albicans strains complicates interpretation of virulence studies. Infect Immun. 66, 5301-5306 (1998).
17. Bain, J. M., Stubberfield, C. & Gow, N. A. Ura-status-dependent adhesion of Candida albicans mutants. FEMS Microbiol. Lett, 204, 323-328 (2001).
18. Wach, A. PCR-synthesis of marker cassettes with long flanking homology regions for gene disruptions in S. cerevisiae Yeast 12, 259-265 (1996).
19. Wilson, R. B., Davis, D., Enloe, B. M. & Mitchell, A. P. A recyclable Candida albicans URA3 cassette for PCR product-directed gene disruptions. Yeast 16, 65-70 (2000). A key methodology paper that describes an efficient PCR-based method for gene disruption that removed the need to first clone the gene before its disruption. This system has now become a standard way to generate homozygous gene deletions in C. albicans.
20. Wilson, R. B., Davis, D. & Mitchell, A. P. Rapid hypothesis testing with Candida albicans through gene disruption with short homology regions. J. Bacteriol. 181, 1868-1874 (1999).
21. Morschhauser, J., Michel, S. & Staib, P. Sequential gene disruption in Candida albicans by FLP-mediated site-specific recombination. Mol. Microbiol. 32, 547-556 (1999).
22. Biery, M. C., Stewart, F. J., Stellwagen, A. E., Raleigh, E. A. & Craig, N. L. A simple in vitro Tn7-based transposition system with low target site selectivity for genome and gene analysis. Nucleic Acids Res. 28, 1067-1077 (2000).
23. De Backer, M. D. et al. An antisense-based functional genomics approach for identification of genes cirtical for growth of Candida albicans. Nature Bictechnol 19, 235-241 (2001).
24. Cormack, B. P. et al. Yeast-enhanced green fluorescent protein (yEGFP) - A reporter of gene expression in Candida albicans. Microbiology 143, 303-311 (1997).
25. Morschhauser, J., Michel, S. & Hacker, J. Expression of a chromosomally integrated, single-copy GFP gene in Candida albicans, and its use as a reporter of gene regulation. Mol. Gen. Genet. 257, 412-420 (1998).
26. Gerami-Nejad, M., Berman, J. & Gale, C. A. Cassettes for PCR-mediated construction of green, yellow and cyan fluorescent protein fusions in Candida albicans, Yeast 18, 859-864 (2001). An important methodology paper that provided convenient tools to study the localization of proteins in C. albicans cells by generating PCR-mediated fusions to CFP, YFP and GFPs.
27. Devasahayam, G., Chaturvedi, V. & Hanes, S. D. The Ess1 prolyl isomerase is required for growth and morphogenetic switching in Candida albicans. Genetics 160, 37-48 (2002).
28. Whiteway, M., Dignard, D. & Thomas, D. Y. Dominant negative selection of heterologous genes: Isolation of Candida albicans genes that interfere with Saccharomyces cerevisiae mating factor-induced cell cycle arrest. Proc. Natl. Acad. Sci. USA 89, 9410-9414 (1992).
29. Gale, C. et al. Cloning and expression of a gene encoding an integrin-like protein in Candida albicans. Proc. Natl. Acad. Sci. USA 93, 357-361 (1996).
30. Gale, C. A. et al. Candida albicans Int1p interacts with the septin ring in yeast and hyphal cells. Mol. Biol. Cell 12, 3538-3549 (2001).
31. Gale, C. et al. Linkage of adhesion, filamentous growth, and virulence in Candida albicans to a single gene, INT1. Science 279, 1355-1358 (1998). References 30 and 31 describe the isolation and characterization of INT1 - A gene that is important for virulence, adhesion and hyphal formation, under some conditions.
32. Fu, Y. et al. Expression of the Candida albicans gene ALS1 in Saccharomyces cerevisiae induces adherence to endothelial and epithelial cells. Infect. Immun. 66, 1783-1786 (1998).
33. Gaur, N. K. & Klotz, S. A. Expression, cloning, and characterization of a Candida albicans gene, ALA1, that confers adherence properties upon Saccharomyces cerevisiae for extracellular matrix proteins. Infect. Immun. 65, 5289-5294 (1997).
34. Fu, Y. et al. Cloning and characterization of CAD1/AAF1, a gene from Candida albicans that induces adherence to endothelial cells after expression in Saccharomyces cerevisiae. Infect. Immun. 66, 2078-2084 (1998).
35. Liu, H., Köhler, J. & Fink, G R. Suppression of hyphal formation in Candida albicans by mutation of a STE12 homolog. Science 266, 1723-1726 (1994).
36. Romani, L. in Candida and Candidiasis (ed. Calderone, R. A.) 223-241 (ASM Press, Washington, DC, 2002).
37. Lo, H. J. et al. Nonfilamentous C. albicans mutants are avirulent. Cell 90, 939-949 (1997).
38. Lorenz, M. C. & Fink, G. R. The glyoxylate cycle is required for fungal virulence. Nature 412, 83-86 (2001).
39. De Backer, M. D. et al. Genomic profiling of the response of Candida albicans to itraconazole treatment using a DNA microarray. Antimicrob. Agents Chemother. 45, 1660-1670 (2001).
40. Cowen, L. E. et al. Population genomics of drug resistance in experimental populations of Candida albicans Proc. Natl. Acad. Sci. USA 99, 9284-9289 (2002). Transcription profiling using whole-genome arrays to monitor the changes in gene expression in four replicate C. albicans populations during long-term exposure to a fungicide, fluconazole.
41. Nantel, A. et al. Transcription profiling of C. albicans cells undergoing the yeast to hyphal transition. Mol. Biol. Cell 13, 3452-3465 (2002). This paper describes the first whole-genome array study of the yeast-to-hyphal transition.
42. Magee, B. B. & Magee, P. T. Electrophoretic karyotypes and chromosome numbers in Candida species. J. Gen. Microbiol. 133, 425-430 (1987).
43. McEachern, M. J. & Hicks, J. B. Unusually large telomeric repeats in the yeast Candida albicans. Mol. Cell. Biol. 13, 551-560 (1993).
44. Metz, A. M., Love, R. A., Strobel, G. A. & Long, D. M. Two telomerase reverse transcriptases (TERTs) expressed in Candice albicans. Biotechnol. Appl. Biochem. 34, 47-54 (2001).
45. Singh, S. M., Steinberg-Neifach, O., Mian, I. S & Lue, N. F. Analysis of telomerase in Candida albicans: A potential role in telomere end protection. Eukaryotic Cell 1 (in the press).
46. Merz, W. G., Connelly, C. & Hieter, P. Variation of electrophoretic karyotypes among clinical isolates of Candida albicans. J. Clin. Microbiol. 26, 842-845 (1988).
47. Magee, P. T., Bowdin, L. & Staudinger, J. Comparison of molecular typing methods for Candida albicans. J. Clin. Microbiol. 30, 2674-2679 (1992).
48. Rustchenko, E. P. & Sherman, F. Physical constitution of ribosomal genes in common strains of Saccharomyces cerevisiae. Yeast 10, 1157-1171 (1994).
49. Wickes, B, et al. Physical and genetic mapping of Candida albicans: Several genes previously assigned to chromosome 1 map to chromosome R, the rDNA-containing linkage group. Infect. Immun. 59, 2480-2484 (1991).
50. Rustchenko, E. P., Curran, T. M. & Sherman, F. Variations in the number of ribosomal DNA units in morphological mutants and normal strains of Candida albicans and in normal strains of Saccharomyces cerevisiae. J. Bacteriol. 175, 7189-7199 (1993).
51. Thrash-Bingham, C. & Gorman, J. A. DNA translocations contribute to chromosome length polymorphisms in Candida albicans. Curr. Genet. 22, 93-100 (1992).
52. Chu, W. S., Megee, B. B. & Megee, P. T. Construction of an Sfil macrorestriction map of the Candida albicans genome. J. Bacteriol. 175, 6637-6651 (1993).
53. Chibana, H., Beckerman, J. L. & Magee, P. T. Fine-resolution physical mapping of genomic diversity in Candida albicans. Genome Res. 10, 1865-1877 (2000).
54. Chindampom, A. et al. Repetitive sequences (RPSs) in the chromosomes of Candida albicans are sandwiched between two novel stretches, HOK and RB2, common to each chromosome. Microbiology 144, 849-857 (1998).
55. Hughes, T. R. et al. Widespread aneuploidy revealed by DNA microarray expression profiling. Nature Genet. 25, 333-837 (2000).
56. Janbon, G., Sherman, F. & Rustchenko, E. Monosomy of a specific chromosome determines L-sorbose utilization: A novel regulatory mechanism in Candida albicans. Proc. Natl. Acad. Sci. USA 95, 5150-5155 (1998). The authors discovered that forcing cells to grow on sorbose leads to a high level of chromosome 5 loss. When cells are returned to a medium that contains glucose, the remaining chromosome 5 is duplicated, showing plasticity of the C. albicans genome and that loss of a chromosome can confer benefits under some stress conditions.
57. Perepnikhatka, V. et al. Specific chromosome alterations in fluconazole-resistant mutants of Candida albicans. J. Bacteriol. 181, 4041-4049 (1999).
58. Tzung, K. W. et al. Genomic evidence for a complete sexual cycle in Candida albicans. Proc. Natl. Acad. Sci. USA 98, 3249-3253 (2001).
59. Wolfe, K. H. & Shields, D. C. Molecular evidence for an ancient duplication of the entire yeast genome. Nature 387, 708-713 (1997).
60. Seoighe, C. et al. Prevalence of small inversions in yeast gene order evolution. Proc. Natl. Acad. Sci. USA 97, 14433-14437 (2000).
61. Laprade, L., Boyartchuk, V. L., Dietrich, W. F. & Winston, F. Spt3 plays opposite roles in filamentous growth in Saccharomyces cerevisiae and Candida albicans and is required for C. albicans virulence. Genetics 161, 509-519 (2002).
62. Feng, Q., Summers, E., Guo, B. & Fink, G. Ras signaling is required for serum-induced hyphal differentiation in Candida albicans. J. Bacteriol. 181, 6339-6346 (1999).
63. Gow, N. A. R. in Candida and Candidiasis (ed. Calderone, R. A.) 145-158 (ASM Press, Washington, DC, 2002).
64. Odds, F. C. Candida and Candidosis 2nd Edn. (Baillière Tindall, London, 1988).
65. Merson-Davies, L. A. & Odds, F. C. A morphology index for characterization of cell shape in Candida albicans. J. Gen. Microbiol. 135, 3143-3152 (1989).
66. Sudbery, P. E. The germ tubes of Candida albicans hyphae and pseudohyphae show different patterns of septin ring localization. Mol. Microbiol. 41, 19-31 (2001). This paper shows that there are fundamental differences in cell-cycle organization between the switch from unbudded yeast cells to hyphae and to pseudohyphae.
67. Braun, B. R., Head, W. S., Wang, M. X. & Johnson, A. D. Identification and characterization of TUP1-regulated genes in Candida albicans. Genetics 156, 31-44 (2000).
68. Gow, N., Brown, A. & Odds, F. Fungal morphogenesis and host invasion. Curr. Opin. Microbiol. 5, 366 (2002).
69. Brown, A. J. P. in Candida and Candidiasis (ed. Calderone, R. A.) 87-93 (ASM Press, Washington, DC, 2002).
70. Liu, H. Transcriptional control of dimorphism in Candida albicans. Curr. Opin. Microbiol. 4, 728-735 (2001).
71. 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. USA 93, 13223-13228 (1996).
72. Leberel, E. et al. Signal transduction through homologs of the Ste20p and Ste7p protein kinases can trigger hyphal formation in the pathogenic fungus Candida albicans. Proc. Natl. Acad. Sci. USA 93, 13217-13222 (1996).
73. Riggle, P. J., Andrutis, K. A., Chen, X., Tzipon, S. R. & Kumamoto, C. A. Invasive lesions containing filamentous forms produced by a Candida albicans mutant that is defective in filamentous growth in culture. Infect. Immun. 67, 3649-3652 (1999).
74. Davis, D., Edwards, J. E. Jr, Mitchell, A. P. & Ibrahim, A. S. Candida albicans RIM101 pH response pathway is required for host-pathogen interactions. Infect. Immun. 68, 5953-5959 (2000).
75. El Barkani, A. et al. Dominant active alleles of RIM101 (PRF2) bypass the pH restriction on filamentation of Candida albicans. Mol. Cell. Biol. 20, 4635-4647 (2000). References 74 and 75 describe the identification of the Rim101 protein as the regulator of hyphal development in response to alkaline pH. At alkaline pH, the carboxyl terminus of Rim101 is removed by proteolytik; cleavage. The truncated protein acts a dominant inducer of alkaline-specific genes and a repressor of acid-induced genes.
76. Brown, D. H., Giusani, A. D., Chen, X. & Kumamoto, C. A. Filamentous growth of Candida albicans in response to physical environmental cues and its regulation by the unique CZF1 gene. Mol. Microbiol. 34, 651-662 (1999).
77. Braun, B. R. & Johnson, A. D. Control of filament formation in Candida albicans by the transcriptional repressor TUP1. Science 277, 105-109 (1997).
78. Braun, B. R., Kadosh, D. & Johnson, A. D. NPG1, a repressor of filamentous growth in C. albicans, is down-regulated during filament induction. EMBO J. 20, 4753-4761 (2001).
79. Murad, A. M. et al. NRG1 represses yeast-hypha morphogenesis and hypha-specific gene expression in Candida albicans. EMBO J. 20, 4742-4752 (2001)
80. Kadosh, D. & Johnson, A. D. Rfg1, a protein related to the Saccharomyces cerevisiae hypoxic regulator Rox1, controls filamentous growth and virulence in Candida albicans. Mol. Cell. Biol. 21, 2496-2505 (2001).
81. Braun, B. R. & Johnson, A. D. TUP1, CPH1 and EFG1 make independent contributions to filamentation in Candida albicans. Genetics 155, 57-67 (2000).
82. Staab, J. F., Bradway, S. D., Fidel, P. L. & Sundstrom, P. Adhesive and mammalian transglutaminese substrate properties of Candida albicans Hwp1, Science 283, 1535-1538 (1999).
83. Murad, A. M. et al. Transcript profiling in Candida albicans reveals new cellular functions for the transcriptional repressors CaTup1, CaMig1 and CaNrg1. Mol. Microbiol. 42, 981-993 (2001) References 79 and 83 describe transcription profiling of more than 2,000 genes in tup1, nrg1 and mig1 mutants. The results broadly confirmed the model that Nrg1 and Mig1 target the repressing activity of Tup1 to different subsets of genes.
84. Lane, S., Birse, C., Zhou, S., Matson, R. & Liu, H. DNA array studies demonstrate convergent regulation of virulence factors by Cph1, Cph2, and Efg1 in Candida albicans. J. Biol. Chem. 276, 48968-48996 (2001). Transcription profiling experiments that compared the expression of 700 genes in single cph1, cph2 and efg1 mutants showed that each gene transduced signals from different environmental inputs but targeted the induction of a common set of hyphal-specific genes.
85. Lew, D. J. & Reed, S. I. Cell cycle control of morphogenesis in budding yeast. Curr. Opin. Genet. Dev. 5, 17-23 (1995).
86. Rua, D., Tobe, B. T. & Kron, S. J. Cell cycle control of yeast filamentous growth. Curr. Opin. Microbiol. 4, 726-727 (2001).
87. Loeb, J. D., Sepulveda-Becerra, M., Hazan, I., & Liu, H. A G1 cyclin is necessary for maintenance of filamentous growth in Candida albicanus. Mol. Cell. Biol. 19, 4019-4027 (1999).
88. Bensen, E. S., Filler, S. G. & Berman, J. A forkhead transcription factor is important for true hyphal as well as yeast morphogenesis in Candida albicans. Eukaryotic Cell 1, 787-798 (2002).
89. Hazan, I., Sepulveda-Becerra, M. & Liu, H. Hyphal elongation is regulated independently of cell cycle in Candida albicans. Mol. Biol. Cell 13, 134-145 (2002).
90. Bai, C., Ramanan, N., Wang, Y. M. & Wang, Y. Spindle assembly checkpoint component CaMad2p is indispensable for Candida albicans survival and virulence in mice. Mol. Microbiol. 45, 31-44 (2002).
91. Slutsky, B., Buffo, J. & Soll, D. R. High-frequency switching of colony morphology in Candida albicans. Science 230, 666-669 (1985).
92. Pomes, R., Gil, C. & Nombela, C. Genetic analysis of Candida albicans morphological mutants. J. Gen Microbiol. 131, 2107-2113 (1985).
93. Soll, D. R. High-frequency switching in Candida albicans. Clin. Microbiol. Rev. 5, 183-203 (1992).
94. Sonneborn, A., Tebarth, B. & Ernst, J. F. Control of white-opaque phenotypic switching in Candida albicans by the Efg1p morphogenetic regulator. Infect. Immun. 67, 4655-4660 (1999).
95. Zhao, R., Lockhart, S. R., Daniels, K. & Soll, D. R. Roles of TUP1 in switching, phase maintenance, and phase-specific gene expression in Candida albicans. Eukaryotic Cell 1, 353-365 (2002).
96. Lockhart, S. R., Nguyen, M., Srikantha, T. & Soll, D. R. A MADS box protein consensus binding site is necessary and sufficient for activation of the opaque-phase-specific gene OP4 of Candida albicans. J. Bacteriol. 180, 6607-6616 (1998).
97. Srikantha, T., Tsai, L., Daniels, K., Klar, A. J. S. & 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, 4614-4625 (2001).
98. 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, 919-924 (2001).
99. Taylor, J. W., Geiser, D. M., Burt, A. & Koufopanou, V. The evolutionary biology and population genetics underlying fungal strain typing. Clin. Microbiol. Rev. 12, 126-146 (1999).
100. Rustad, T. R., Stevens, D. A., Pfaller, M. A. & White, T. C. Homozygosity at the Candida albicans MTL locus associated with azole resistance. Microbiology 148, 1061-1072 (2002).
101. 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, 293-302 (2002). The authors revealed an intriguing relationship between white - opaque phenotypic switching and the ability to mate. Cells that have only one MTL locus switch more frequently to the opaque state, and cells that are opaque mate with higher efficiency.
102. Scherer, S. & Magee, P. T. Genetics of Candida albicans. Microbiol. Rev. 64, 226-241 (1990).
103. Kirsch, D. R. & Whitney, R. R. Pathogenicity of Candida albicans auxotrophic mutants in experimental infections. Infect. Immun. 59, 3297-3300 (1991).
104. Kohler, G. A., White, T. C. & Agabian, N, Overexpression of a cloned IMP dehydrogenase gene of Candida albicans confers resistance to the specific inhibitor mycophenolic acid. J. Bacteriol. 179, 2331-2338 (1997).
105. Staib, P. et al. Host-induced, stage-specific virulence gene activation in Candida albicans during infection. Mol. Microbiol. 32, 533-546 (1999).
106. Beckerman, J., Chibana, H., Turner, J. & Magee, P. T. Single-copy IMH3 allele is sufficient to confer resistance to mycophenolic acid in Candida albicans and to mediate transformation of clinical Candida species. Infect. Immun. 69, 108-114 (2001).
107. Enloe, B., Diamond, A. & Mitchell, A. P. A single-transformation gene function test in diploid Candida albicans. J. Bacteriol. 182, 5730-5736 (2000).
108. Bailey, D. A., Feldmann, P. J., Bovey, M., Gow, N. A. & Brown, A. J. The Candida albicans HYR1 gene, which is activated in response to hyphal development, belongs to a gene family encoding yeast cell wall proteins. J. Bacteriol. 178, 5353-5360 (1996).
109. Bertram, G., Swoboda, R. K., Gooday, G. W., Gow, N. A. & Brown, A. J. Structure and regulation of the Candida albicans ADH1 gene encoding an immunogenic alcohol dehydrogenase. Yeast 12, 115-127 (1996).
110. Delbruck, S. & Ernst, J. F. Morphogenesis-independent regulation of actin transcript levels in the pathogenic yeast Candida albicans. Mol. Microbiol. 10, 859-866 (1993).
111. Rademacher, F., Kehren, V., Stoldt, V. R. & Ernst, J. F. A Candida albicans chaperonin subunit (CaCct8p) as a suppressor of morphogenesis and Ras phenotypes in C. albicans and Saccharomyces cerevisiae. Microbiology 144, 2951-2960 (1998).
112. Gorman, J. A., Chan, W. & Gorman, J. W. Repeated use of GAL1 for gene disruption in Candida albicans. Genetics 129, 19-24 (1991)
113. Leuker, C. E., Sonneborn, A., Delbruck, S. & Ernst, J. F. Sequence and promoter regulation of the PCK1 gene encoding phosphoanolpyruvate carboxykinase of the fungal pathogen Candida albicans. Gene 192, 235-240 (1997).
114. Geber, A., Williamson, P. R., Rex, J. H., Sweeney, E. C. & Bennett, J. E. Cloning and characterization of a maltase gene involved in sucrose utilization. J. Bacteriol. 174, 6992-6996 (1992).
115. Brown, D. H. Jr, Slobodkin, I. V. & Kumamoto, C. A. Stable transformation and regulated expression of an inducible reporter construct in Candida albicans using restriction enzyme-mediated integration. Mol. Gen. Genet. 251, 75-80 (1996).
116. Care, R. S., Trevethick, J., Binley, K. M. & Sudbery, P. E. The MET3 promoter: A new tool for Candida albicans molecular genetics. Mol. Microbiol. 34, 792-798 (1999).
117. Nakayama, H. et al. Tetracycline-regulatable system to tightly control gene expression in the pathogenic fungus Candida albicans. Infect. Immun. 68, 6712-6719 (2000).
118. Leuker, C. E., Hahn, A. M. & Emst, J. F. β-galactosidase of Kluyveromyces lactis (Lac4p) as reporter of gene expression in Candida albicans and C. tropicalis. Mot. Gen. Genet. 235, 231-241 (1992).
119. Uhl, M. A. & Johnson, A. D. Development of Streptococcus thermophilus lacZ as a reporter gene for Candida albicans. Microbiology 147, 1189-1195 (2001).
120. Srikantha, T. et al. The sea pansy Renilla reniformis luciferase serves as a sensitive bioluminescent reporter for differential gene expression in Candida albicans. J. Bacteriol. 178, 121-129 (1996).