Genetics of Candida albicans, a diploid human fungal pathogen

Annual Review of Genetics

Volumn 41, Issue , 2007, Pages 193-211

  Noble, Suzanne M ^a   Johnson, Alexander D ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Clade; Gene disruption; Human pathogen; Parasexual cycle

Indexed keywords

CANDIDA ALBICANS; DIPLOIDY; FUNGAL GENE; GENETICS; PATHOGENICITY; REVIEW;

CANDIDA ALBICANS; DIPLOIDY; GENES, FUNGAL;

EID: 44449137688     PISSN: 00664197     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.genet.41.042007.170146     Document Type: Review

References (88)

1. Alani E, Cao L, Kleckner N. 1987. A method for gene disruption that allows repeated use of URA3 selection in the construction of multiply disrupted yeast strains. Genetics 116:541-545
2. Anderson JB, Wickens C, Khan M, Cowen LE, Federspiel N, et al. 2001. Infrequent genetic exchange and recombination in the mitochondrial genome of Candida albicans. J. Bacteriol. 183:865-872
3. Backen AC, Broadbent ID, Fetherston RW, Rosamond JD, Schnell NF, Stark MJ. 2000. Evaluation of the CaMAL2 promoter for regulated expression of genes in Candida albicans. Yeast 16:1121-1129
4. Bain JM, Stubberfield C, Gow NA. 2001. Ura-status-dependent adhesion of Candida albicans mutants. FEMS Microbiol. Lett. 204:323-328
5. Barchiesi F, Di Francesco LF, Compagnucci P, Arzeni D, Cirioni O, Scalise G. 1997. Genotypic identification of sequential Candida albicans isolates from AIDS patients by polymerase chain reaction techniques. Eur. J. Clin. Microbiol. Infect. Dis. 16:601-605
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, Johnson AD. 2005. Mating in Candida albicans and the search for a sexual cycle. Annu. Rev. Microbiol. 59:233-255
8. BoekeJD, LaCrouteF, FinkGR. 1984. A positive selection for mutants lacking orotidine-5'-phosphate decarboxylase activity in yeast: 5-fluoro-orotic acid resistance. Mol. Gen. Genet. 197:345-346
9. Bougnoux ME, Aanensen DM, Morand S, Theraud M, Spratt BG, d'Enfert C. 2004. Multilocus sequence typing of Candida albicans: strategies, data exchange and applications. Infect. Genet. Evol. 4:243-252
10. Brand A, MacCallum DM, Brown AJ, Gow NA, Odds FC. 2004. Ectopic expression of URA3 can influence the virulence phenotypes and proteome of Candida albicans but can be overcome by targeted reintegration of URA3 at the RPS10 locus. Eukaryot. Cell 3:900-909
11. Braun BR, Johnson AD. 1997. Control of filament formation in Candida albicans by the transcriptional repressor TUP1. Science 277:105-109
12. Braun BR, van HetHoogM, d'Enfert C, Martchenko M, DunganJ, et al. 2005. Ahuman-curated annotation of the Candida albicans genome. PLOS Genet. 1:36-57
13. Brown DH Jr, Slobodkin IV, Kumamoto CA. 1996. Stable transformation and regulated expression of an inducible reporter construct in Candida albicans using restriction enzyme-mediated integration. Mol. Gen. Genet. 251:75-80
14. Calderone RA. 2002. Candida and Candidiasis. Washington, DC: ASM Press. 451 pp.
15. Care RS, TrevethickJ, Binley KM, Sudbery PE. 1999. The MET3 promoter: a new tool for Candida albicans molecular genetics. Mol. Microbiol. 34:792-798
16. Cheng S, Nguyen MH, Zhang Z, Jia H, Handfield M, Clancy CJ. 2003. Evaluation of the roles of four Candida albicans genes in virulence by using gene disruption strains that express URA3 from the native locus. Infect. Immun. 71:6101-6103
17. Davis DA, Bruno VM, Loza L, Filler SG, Mitchell AP. 2002. Candida albicans Mds3p, a conserved regulator of pH responses and virulence identified through insertional mutagenesis. Genetics 162:1573-1581
18. de Hoogt R, Luyten WH, Contreras R, De Backer MD. 2000. PCR-and ligation-mediated synthesis of split-marker cassettes with long flanking homology regions for gene disruption in Candida albicans. Biotechniques 28:1112-1116
19. Eggimann P, Garbino J, Pittet D. 2003. Epidemiology of Candida species infections in critically ill nonimmunosuppressed patients. Lancet Infect. Dis. 3:685-702 (Pubitemid 37345347)
20. Enloe B, Diamond A, Mitchell AP. 2000. A single-transformation gene function test in diploid Candida albicans. J. Bacteriol. 182:5730-5736
21. Fonzi WA, Irwin MY. 1993. Isogenic strain construction and gene mapping in Candida albicans. Genetics 134:717-728
22. Giaever G, Chu AM, Ni L, Connelly C, Riles L, et al. 2002. Functional profiling of the Saccharomyces cerevisiae genome. Nature 418:387-391
23. GraserY,VolovsekM,Arrington J, Schonian G, PresberW,et al. 1996. Molecular markers reveal that population structure of the human pathogen Candida albicans exhibits both clonality and recombination. Proc. Natl. Acad. Sci. USA 93:12473-12477
24. Greenberg JR, Price NP, Oliver RP, Sherman F, Rustchenko E. 2005. Candida albicans SOU1 encodes a sorbose reductase required for L-sorbose utilization. Yeast 22:957-969
25. Gudlaugsson O, Gillespie S, Lee K, Vande Berg J, Hu J, et al. 2003. Attributable mortality of nosocomial candidemia, revisited. Clin. Infect. Dis. 37:1172-1177
26. Hoyer LL. 2001. The ALS gene family of Candida albicans. Trends Microbiol. 9:176-180
27. Hughes TR, Roberts CJ, Dai H, Jones AR, Meyer MR, et al. 2000. Widespread aneuploidy revealed by DNA microarray expression profiling. Nat. Genet. 25:333-337
28. Hull CM, Johnson AD. 1999. Identification of a mating type-like locus in the asexual pathogenic yeast Candida albicans. Science 285:1271-1275
29. Hull CM, Raisner RM, Johnson AD. 2000. Evidence for mating of the "asexual" yeast Candida albicans in a mammalian host. Science 289:307-310
30. 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. USA 95:5150-5155
31. Johnson A. 2003. The biology of mating in Candida albicans. Nat. Rev. Microbiol. 1:106-116
32. Jones T, Federspiel NA, Chibana H, Dungan J, Kalman S, et al. 2004. The diploid genome sequence of Candida albicans. Proc. Natl. Acad. Sci. USA 101:7329-7334
33. Kirsch DR, Whitney RR. 1991. Pathogenicity of Candida albicans auxotrophic mutants in experimental infections. Infect. Immun. 59:3297-3300
34. Kohler GA, White TC, Agabian N. 1997. Overexpression of a cloned IMP dehydrogenase gene of Candida albicans confers resistance to the specific inhibitor mycophenolic acid. J. Bacteriol. 179:2331-2338
35. Kohler JR, Fink GR. 1996. Candida albicans strains heterozygous and homozygous for mutationsinmitogen-activated protein kinase signaling components have defectsinhyphal development. Proc. Natl. Acad. Sci. USA 93:13223-13228
36. Kumamoto CA, Vinces MD. 2005. Contributions of hyphae and hypha-coregulated genes to Candida albicans virulence. Cell Microbiol. 7:1546-1554
37. Lan CY, Newport G, Murillo LA, Jones T, Scherer S, et al. 2002. Metabolic specialization associated with phenotypic switching in Candida albicans. Proc. Natl. Acad. Sci. USA 99:14907-14912
38. Lay J, Henry LK, Clifford J, Koltin Y, Bulawa CE, Becker JM. 1998. Altered expression of selectable marker URA3 in gene-disrupted Candida albicans strains complicates interpretation of virulence studies. Infect. Immun. 66:5301-5306
39. Legrand M, Lephart P, Forche A, Mueller FM, Walsh T, et al. 2004. Homozygosity at the MTL locus in clinical strains of Candida albicans: karyotypic rearrangements and tetraploid formation. Mol. Microbiol. 52:1451-1462
40. Liu H, Kohler J, Fink GR. 1994. Suppression of hyphal formation in Candida albicans by mutation of a STE12 homolog. Science 266:1723-1726
41. Lockhart SR, Pujol C, Daniels KJ, Miller MG, Johnson AD, et al. 2002. In Candida albicans, white-opaque switchers are homozygous for mating type. Genetics 162:737-745
42. 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
43. Loeb JD, Sepulveda-Becerra M, Hazan I, Liu H. 1999. A G1 cyclin is necessary for maintenance of filamentous growth in Candida albicans. Mol. Cell Biol. 19:4019-4027
44. Madhani HD. 2006. From A to Alpha: Yeast As a Model for Cellular Differentiation. Cold Spring Harbor, NY: Cold Spring Harbor Lab. Press
45. Magee BB, Magee PT. 2000. Induction of mating in Candida albicans by construction of MTLa and MTLalpha strains. Science 289:310-313
46. Magee PT, Magee BB. 2004. Through a glass opaquely: the biological significance of mating in Candida albicans. Curr. Opin. Microbiol. 7:661-665
47. McCullough MJ, Ross BC, Dwyer BD, Reade PC. 1994. Genotype and phenotype of oral Candida albicans from patients infected with the human immunodeficiency virus. Microbiology 140(Part 5):1195-1202
48. Mercure S, Poirier S, Lemay G, Auger P, Montplaisir S, de Repentigny L. 1993. Application of biotyping and DNA typing of Candida albicans to the epidemiology of recurrent vulvovaginal candidiasis. J. Infect. Dis. 168:502-507
49. 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
50. Morschhauser J, Michel S, Staib P. 1999. Sequential gene disruption in Candida albicans by FLP-mediated site-specific recombination. Mol. Microbiol. 32:547-556
51. Murad AM, Lee PR, Broadbent ID, Barelle CJ, Brown AJ. 2000. CIp10, an efficient and convenient integrating vector for Candida albicans. Yeast 16:325-327
52. Nakayama H, Mio T, Nagahashi S, Kokado M, Arisawa M, Aoki Y. 2000. Tetracycline-regulatable system to tightly control gene expression in the pathogenic fungus Candida albicans. Infect. Immun. 68:6712-6719
53. Nobile CJ, Bruno VM, Richard ML, Davis DA, Mitchell AP. 2003. Genetic control of chlamydospore formation in Candida albicans. Microbiology 149:3629-3637
54. Nobile CJ, Mitchell AP. 2005. Regulation of cell-surface genes and biofilm formation by the C. albicans transcription factor Bcr1p. Curr. Biol. 15:1150-1155
55. Noble SM, Johnson AD. 2005. Strains and strategies for large-scale gene deletion studies of the diploid human fungal pathogen Candida albicans. Eukaryot. Cell 4:298-309
56. Odds FC. 1988. Candida and Candidosis. Philadelphia: Saunders
57. Odds FC, Bougnoux M, Shaw DJ, Bain J, Davidson AD, et al. 2007. Molecular phyloge-netics of Candida albicans. Eukaryot. Cell. In press Apr. 6. [Epub ahead of print]
58. Odds FC, Davidson AD, Jacobsen MD, Tavanti A, Whyte JA, et al. 2006. Candida albicans strain maintenance, replacement, and microvariation demonstratedbymultilocus sequence typing. J. Clin. Microbiol. 44:3647-3658
59. Park YN, Morschhauser J. 2005. Tetracycline-inducible gene expression and gene deletion in Candida albicans. Eukaryot. Cell 4:1328-1342
60. Pujol C, Joly S, Lockhart SR, Noel S, Tibayrenc M, Soll DR. 1997. Parity among the randomly amplified polymorphic DNA method, multilocus enzyme electrophoresis, and Southern blot hybridization with the moderately repetitive DNA probe Ca3 for fingerprinting Candida albicans. J. Clin. Microbiol. 35:2348-2358
61. Pujol C, Pfaller MA, Soll DR. 2004. Flucytosine resistance is restricted to a single genetic clade of Candida albicans. Antimicrob. Agents Chemother. 48:262-266
62. Pujol C, Reynes J, Renaud F, Raymond M, Tibayrenc M, et al. 1993. The yeast Candida albicans has a clonal mode of reproduction in a population of infected human immunodeficiency virus-positive patients. Proc. Natl. Acad. Sci. USA 90:9456-9459
63. Reuss O, Vik A, Kolter R, Morschhauser J. 2004. The SAT1 flipper, an optimized tool for gene disruption in Candida albicans. Gene 341:119-127
64. Richard ML, Nobile CJ, Bruno VM, Mitchell AP. 2005. Candida albicans biofilm-defective mutants. Eukaryot. Cell 4:1493-1502
65. Roemer T, Jiang B, Davison J, Ketela T, Veillette K, et al. 2003. Large-scale essential gene identification in Candida albicans and applications to antifungal drug discovery. Mol. Microbiol. 50:167-181
66. Rustchenko EP, Howard DH, Sherman F. 1994. Chromosomal alterations of Candida albicans are associated with the gain and lossof assimilating functions. J. Bacteriol. 176:3231-3241
67. Rustchenko-Bulgac EP, Sherman F, Hicks JB. 1990. Chromosomal rearrangements associated with morphological mutants provide a means for genetic variation of Candida albicans. J. Bacteriol. 172:1276-1283
68. Sangeorzan JA, Bradley SF, He X, Zarins LT, Ridenour GL, et al. 1994. Epidemiology of oral candidiasis in HIV-infected patients: colonization, infection, treatment, and emergence of fluconazole resistance. Am. J. Med. 97:339-346
69. Selmecki A, Forche A, Berman J. 2006. Aneuploidy and isochromosome formation in drug-resistant Candida albicans. Science 313:367-370
70. Sharkey LL, Liao WL, Ghosh AK, Fonzi WA. 2005. Flanking direct repeats of hisG alter URA3 marker expression at the HWP1 locus of Candida albicans. Microbiology 151:1061-1071
71. Shen J, Guo W, Kohler JR. 2005. CaNAT1, a heterologous dominant selectable marker for transformation of Candida albicans and other pathogenic Candida species. Infect. Immun. 73:1239-1242
72. 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 (Pubitemid 17228707)
73. Soll DR, Pujol C. 2003. Candida albicans clades. FEMS Immunol. Med. Microbiol. 39:1-7
74. Staib P, Kretschmar M, Nichterlein T, Kohler G, Michel S, et al. 1999. Host-induced, stage-specific virulence gene activation in Candida albicans during infection. Mol. Microbiol. 32:533-546
75. Sundstrom P, Cutler JE, Staab JF. 2002. 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
76. 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
77. Tsong AE, Miller MG, Raisner RM, Johnson AD. 2003. Evolution of a combinatorial transcriptional circuit: a case study in yeasts. Cell 115:389-399
78. Uhl MA, Biery M, Craig N, Johnson AD. 2003. Haploinsufficiency-based large-scale forward genetic analysis of filamentous growth in the diploid human fungal pathogen C. albicans. EMBO J. 22:2668-2678
79. Vazquez JA, Sobel JD, Demitriou R, Vaishampayan J, Lynch M, Zervos MJ. 1994. Kary-otyping of Candida albicans isolates obtained longitudinally in women with recurrent vul-vovaginal candidiasis. J. Infect. Dis. 170:1566-1569
80. Wellington M, Kabir MA, Rustchenko E. 2006. 5-fluoro-orotic acid induces chromosome alterations in genetically manipulated strains of Candida albicans. Mycologia 98:393-398
81. Wey SB, Mori M, Pfaller MA, Woolson RF, Wenzel RP. 1988. Hospital-acquired can-didemia. The attributable mortality and excess length of stay. Arch. Intern. Med. 148:2642-2645
82. Whelan WL, Magee PT. 1981. Natural heterozygosity in Candida albicans. J. Bacteriol. 145:896-903
83. Wilson RB, Davis D, Enloe BM, Mitchell AP. 2000. A recyclable Candida albicans URA3 cassette for PCR product-directed gene disruptions. Yeast 16:65-70
84. Wilson RB, Davis D, Mitchell AP. 1999. Rapid hypothesis testing with Candida albicans through gene disruption with short homology regions. J. Bacteriol. 181:1868-1874
85. Winzeler EA, Shoemaker DD, Astromoff A, Liang H, Anderson K, et al. 1999. Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285:901-906
86. Wirsching S, Michel S,Morschhauser J.2000. Targeted gene disruption in Candida albicans wild-type strains: the role of the MDR1 gene in fluconazole resistance of clinical Candida albicans isolates. Mol. Microbiol. 36:856-865 (Pubitemid 30326531)
87. Xu J, Mitchell TG, Vilgalys R. 1999. PCR-restriction fragment length polymorphism (RFLP) analyses reveal both extensive clonality and local genetic differences in Candida albicans. Mol. Ecol. 8:59-73
88. Yesland K, Fonzi WA. 2000. Allele-specific gene targeting in Candida albicans results from heterology between alleles. Microbiology 146(Part 9):2097-2104