The cellular roles of Ccr4-NOT in model and pathogenic fungi-implications for fungal virulence

Frontiers in Genetics

Volumn 4, Issue DEC, 2013, Pages

  Panepinto, John C ^a   Heinz, Eva ^b   Traven, Ana ^b  

^a UNIVERSITY AT BUFFALO   (United States)

^b MONASH UNIVERSITY   (Australia)

Author keywords

Candida albicans; Ccr4 NOT; Cell wall; Cryptococcus neoformans; Fungal pathogen; Stress adaptation

Indexed keywords

EID: 84892377573     PISSN: None     EISSN: 16648021     Source Type: Journal    
DOI: 10.3389/fgene.2013.00302     Document Type: Article

References (108)

1. Andersen, M. P., Nelson, Z. W., Hetrick, E. D., and Gottschling, D. E. (2008). A genetic screen for increased loss of heterozygosity in Saccharomyces cerevisiae. Genetics 179, 1179-1195. doi: 10.1534/genetics.108.089250.
2. Azzouz, N., Panasenko, O. O., Colau, G., and Collart, M. A. (2009a). The CCR4-NOT complex physically and functionally interacts with TRAMP and the nuclear exosome. PLoS ONE 4:e6760. doi: 10.1371/journal.pone.0006760.
3. Azzouz, N., Panasenko, O. O., Deluen, C., Hsieh, J., Theiler, G., and Collart, M. A. (2009b). Specific roles for the Ccr4-Not complex subunits in expression of the genome. RNA 15, 377-383. doi: 10.1261/rna.1348209.
4. Badarinarayana, V., Chiang, Y. C., and Denis, C. L. (2000). Functional interaction of CCR4-NOT proteins with TATAA-binding protein (TBP) and its associated factors in yeast. Genetics 155, 1045-1054.
5. Bai, Y., Salvadore, C., Chiang, Y. C., Collart, M. A., Liu, H. Y., and Denis, C. L. (1999). The CCR4 and CAF1 proteins of the CCR4-NOT complex are physically and functionally separated from NOT2, NOT4, and NOT5. Mol. Cell. Biol. 19, 6642-6651.
6. Banuelos, M. G., Moreno, D. E., Olson, D. K., Nguyen, Q., Ricarte, F., Aguilera-Sandoval, C. R., et al. (2010). Genomic analysis of severe hypersensitivity to hygromycin B reveals linkage to vacuolar defects and new vacuolar gene functions in Saccharomyces cerevisiae. Curr. Genet. 56, 121-137. doi: 10.1007/s00294-009-0285-3.
7. Basquin, J., Roudko, V. V., Rode, M., Basquin, C., Seraphin, B., and Conti, E. (2012). Architecture of the nuclease module of the yeast Ccr4-not complex: the Not1-Caf1-Ccr4 interaction. Mol. Cell 48, 207-218. doi: 10.1016/j.molcel.2012.08.014.
8. Bawankar, P., Loh, B., Wohlbold, L., Schmidt, S., and Izaurralde, E. (2013). NOT10 and C2orf29/NOT11 form a conserved module of the CCR4-NOT complex that docks onto the NOT1 N-terminal domain. RNA Biol. 10, 228-244. doi: 10.4161/rna.23018.
9. Bennett, C. B., Lewis, L. K., Karthikeyan, G., Lobachev, K. S., Jin, Y. H., Sterling, J. F., et al. (2001). Genes required for ionizing radiation resistance in yeast. Nat. Genet. 29, 426-434. doi: 10.1038/ng778.
10. Betz, J. L., Chang, M., Washburn, T. M., Porter, S. E., Mueller, C. L., and Jaehning, J. A. (2002). Phenotypic analysis of Paf1/RNA polymerase II complex mutations reveals connections to cell cycle regulation, protein synthesis, and lipid and nucleic acid metabolism. Mol. Genet. Genomics 268, 272-285. doi: 10.1007/s00438-002-0752-8.
11. Bloom, A. L., Solomons, J. T., Havel, V. E., and Panepinto, J. C. (2013). Uncoupling of mRNA synthesis and degradation impairs adaptation to host temperature in Cryptococcus neoformans. Mol. Microbiol. 89, 65-83. doi: 10.1111/mmi.12258.
12. Brown, G. D., Denning, D. W., Gow, N. A., Levitz, S. M., Netea, M. G., and White, T. C. (2012). Hidden killers: human fungal infections. Sci. Transl. Med. 4, 165rv113. doi: 10.1126/science.1222236.
13. Byrne, K. P., and Wolfe, K. H. (2005). The yeast gene order browser: combining curated homology and syntenic context reveals gene fate in polyploid species. Genome Res. 15, 1456-1461. doi: 10.1101/gr.3672305.
14. Capella-Gutierrez, S., Silla-Martinez, J. M., and Gabaldon, T. (2009). trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25, 1972-1973. doi: 10.1093/bioinformatics/btp348.
15. Chen, J., Chiang, Y. C., and Denis, C. L. (2002). CCR4, a 3'-5' poly(A) RNA and ssDNA exonuclease, is the catalytic component of the cytoplasmic deadenylase. EMBO J. 21, 1414-1426. doi: 10.1093/emboj/21.6.1414.
16. Chen, J., Rappsilber, J., Chiang, Y. C., Russell, P., Mann, M., and Denis, C. L. (2001). Purification and characterization of the 1.0 MDa CCR4-NOT complex identifies two novel components of the complex. J. Mol. Biol. 314, 683-694. doi: 10.1006/jmbi.2001.5162.
17. Cheng, S., Clancy, C. J., Checkley, M. A., Zhang, Z., Wozniak, K. L., Seshan, K. R., et al. (2005). The role of Candida albicans NOT5 in virulence depends upon diverse host factors in vivo. Infect. Immun. 73, 7190-7197. doi: 10.1128/IAI.73.11.7190-7197.2005.
18. Cheng, S., Nguyen, M. H., Zhang, Z., Jia, H., Handfield, M., and Clancy, C. J. (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. doi: 10.1128/IAI.71.10.6101-6103.2003.
19. Clamp, M., Cuff, J., Searle, S. M., and Barton, G. J. (2004). The Jalview Java alignment editor. Bioinformatics 20, 426-427. doi: 10.1093/bioinformatics/btg430.
20. Clark, L. B., Viswanathan, P., Quigley, G., Chiang, Y. C., McMahon, J. S., Yao, G., et al. (2004). Systematic mutagenesis of the leucine-rich repeat (LRR) domain of CCR4 reveals specific sites for binding to CAF1 and a separate critical role for the LRR in CCR4 deadenylase activity. J. Biol. Chem. 279, 13616-13623. doi: 10.1074/jbc.M313202200.
21. Collart, M. A., and Panasenko, O. O. (2012). The Ccr4-not complex. Gene 492, 42-53. doi: 10.1016/j.gene.2011.09.033.
22. Collart, M. A., Panasenko, O. O., and Nikolaev, S. I. (2013). The Not3/5 subunit of the Ccr4-Not complex: a central regulator of gene expression that integrates signals between the cytoplasm and the nucleus in eukaryotic cells. Cell. Signal. 25, 743-751. doi: 10.1016/j.cellsig.2012.12.018.
23. Collart, M. A., and Struhl, K. (1993). CDC39, an essential nuclear protein that negatively regulates transcription and differentially affects the constitutive and inducible HIS3 promoters. EMBO J. 12, 177-186.
24. Collart, M. A., and Struhl, K. (1994). NOT1(CDC39), NOT2(CDC36), NOT3, and NOT4 encode a global-negative regulator of transcription that differentially affects TATA-element utilization. Genes Dev. 8, 525-537. doi: 10.1101/gad.8.5.525.
25. Collart, M. A., and Timmers, H. T. (2004). The eukaryotic Ccr4-not complex: a regulatory platform integrating mRNA metabolism with cellular signaling pathways? Prog. Nucleic Acid Res. Mol. Biol. 77, 289-322. doi: 10.1016/S0079-6603(04)77008-7.
26. Cooney, N. M., and Klein, B. S. (2008). Fungal adaptation to the mammalian host: it is a new world, after all. Curr. Opin. Microbiol. 11, 511-516. doi: 10.1016/j.mib.2008.09.018.
27. Cui, Y., Ramnarain, D. B., Chiang, Y. C., Ding, L. H., McMahon, J. S., and Denis, C. L. (2008). Genome wide expression analysis of the CCR4-NOT complex indicates that it consists of three modules with the NOT module controlling SAGA-responsive genes. Mol. Genet. Genomics 279, 323-337. doi: 10.1007/s00438-007-0314-1.
28. Dagley, M. J., Gentle, I. E., Beilharz, T. H., Pettolino, F. A., Djordjevic, J. T., Lo, T. L., et al. (2011). Cell wall integrity is linked to mitochondria and phospholipid homeostasis in Candida albicans through the activity of the post-transcriptional regulator Ccr4-Pop2. Mol. Microbiol. 79, 968-989. doi: 10.1111/j.1365-2958.2010.07503.x.
29. Deluen, C., James, N., Maillet, L., Molinete, M., Theiler, G., Lemaire, M., et al. (2002). The Ccr4-not complex and yTAF1 (yTaf(II)130p/yTaf(II)145p) show physical and functional interactions. Mol. Cell. Biol. 22, 6735-6749. doi: 10.1128/MCB.22.19.6735-6749.2002.
30. Denis, C. L., and Chen, J. (2003). The CCR4-NOT complex plays diverse roles in mRNA metabolism. Prog. Nucleic Acid Res. Mol. Biol. 73, 221-250. doi: 10.1016/S0079-6603(03)01007-9.
31. Denis, C. L., Chiang, Y. C., Cui, Y., and Chen, J. (2001). Genetic evidence supports a role for the yeast CCR4-NOT complex in transcriptional elongation. Genetics 158, 627-634.
32. Deshpande, G. P., Hayles, J., Hoe, K. L., Kim, D. U., Park, H. O., and Hartsuiker, E. (2009). Screening a genome-wide S. pombe deletion library identifies novel genes and pathways involved in genome stability maintenance. DNA Repair (Amst) 8, 672-679. doi: 10.1016/j.dnarep.2009.01.016.
33. Dimmer, K. S., Fritz, S., Fuchs, F., Messerschmitt, M., Weinbach, N., Neupert, W., et al. (2002). Genetic basis of mitochondrial function and morphology in Saccharomyces cerevisiae. Mol. Biol. Cell 13, 847-853. doi: 10.1091/mbc.01-12-0588.
34. Douglas, C. M., D'ippolito, J. A., Shei, G. J., Meinz, M., Onishi, J., Marrinan, J. A., et al. (1997). Identification of the FKS1 gene of Candida albicans as the essential target of 1,3-beta-D-glucan synthase inhibitors. Antimicrob. Agents Chemother. 41, 2471-2479.
35. Dudley, A. M., Janse, D. M., Tanay, A., Shamir, R., and Church, G. M. (2005). A global view of pleiotropy and phenotypically derived gene function in yeast. Mol. Syst. Biol. 1, 2005.0001. doi: 10.1038/msb4100004.
36. Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797. doi: 10.1093/nar/gkh340.
37. Epp, E., Walther, A., Lepine, G., Leon, Z., Mullick, A., Raymond, M., et al. (2010). Forward genetics in Candida albicans that reveals the Arp2/3 complex is required for hyphal formation, but not endocytosis. Mol. Microbiol. 75, 1182-1198. doi: 10.1111/j.1365-2958.2009.07038.x.
38. Finkel, J. S., and Mitchell, A. P. (2011). Genetic control of Candida albicans biofilm development. Nat. Rev. Microbiol. 9, 109-118. doi: 10.1038/nrmicro2475.
39. Finkel, J. S., Xu, W., Huang, D., Hill, E. M., Desai, J. V., Woolford, C. A., et al. (2012). Portrait of Candida albicans adherence regulators. PLoS Pathog. 8:e1002525. doi: 10.1371/journal.ppat.1002525.
40. Fisher, M. C., Henk, D. A., Briggs, C. J., Brownstein, J. S., Madoff, L. C., McCraw, S. L., et al. (2012). Emerging fungal threats to animal, plant and ecosystem health. Nature 484, 186-194. doi: 10.1038/nature10947.
41. Gaillard, H., Tous, C., Botet, J., Gonzalez-Aguilera, C., Quintero, M. J., Viladevall, L., et al. (2009). Genome-wide analysis of factors affecting transcription elongation and DNA repair: a new role for PAF and Ccr4-not in transcription-coupled repair. PLoS Genet. 5:e1000364. doi: 10.1371/journal.pgen.1000364.
42. Goldstrohm, A. C., Hook, B. A., Seay, D. J., and Wickens, M. (2006). PUF proteins bind Pop2p to regulate messenger RNAs. Nat. Struct. Mol. Biol. 13, 533-539. doi: 10.1038/nsmb1100.
43. Goldstrohm, A. C., and Wickens, M. (2008). Multifunctional deadenylase complexes diversify mRNA control. Nat. Rev. Mol. Cell Biol. 9, 337-344. doi: 10.1038/nrm2370.
44. Goler-Baron, V., Selitrennik, M., Barkai, O., Haimovich, G., Lotan, R., and Choder, M. (2008). Transcription in the nucleus and mRNA decay in the cytoplasm are coupled processes. Genes Dev. 22, 2022-2027. doi: 10.1101/gad.473608.
45. Gow, N. A., and Hube, B. (2012). Importance of the Candida albicans cell wall during commensalism and infection. Curr. Opin. Microbiol. 15, 406-412. doi: 10.1016/j.mib.2012.04.005.
46. Grahl, N., Shepardson, K. M., Chung, D., and Cramer, R. A. (2012). Hypoxia and fungal pathogenesis: to air or not to air? Eukaryotic Cell 11, 560-570. doi: 10.1128/EC.00031-12.
47. Grigull, J., Mnaimneh, S., Pootoolal, J., Robinson, M. D., and Hughes, T. R. (2004). Genome-wide analysis of mRNA stability using transcription inhibitors and microarrays reveals posttranscriptional control of ribosome biogenesis factors. Mol. Cell. Biol. 24, 5534-5547. doi: 10.1128/MCB.24.12.5534-5547.2004.
48. Hanway, D., Chin, J. K., Xia, G., Oshiro, G., Winzeler, E. A., and Romesberg, F. E. (2002). Previously uncharacterized genes in the UV-and MMS-induced DNA damage response in yeast. Proc. Natl. Acad. Sci. U.S.A. 99, 10605-10610. doi: 10.1073/pnas.152264899.
49. Hanzawa, H., De Ruwe, M. J., Albert, T. K., Van Der Vliet, P.C., Timmers, H. T., and Boelens, R. (2001). The structure of the C4C4 ring finger of human NOT4 reveals features distinct from those of C3HC4 RING fingers. J. Biol. Chem. 276, 10185-10190. doi: 10.1074/jbc.M009298200.
50. Harel-Sharvit, L., Eldad, N., Haimovich, G., Barkai, O., Duek, L., and Choder, M. (2010). RNA polymerase II subunits link transcription and mRNA decay to translation. Cell 143, 552-563. doi: 10.1016/j.cell.2010.10.033.
51. Hartman, J. L. T., and Tippery, N. P. (2004). Systematic quantification of gene interactions by phenotypic array analysis. Genome Biol. 5, R49. doi: 10.1186/gb-2004-5-7-r49.
52. Havel, V. E., Wool, N. K., Ayad, D., Downey, K. M., Wilson, C. F., Larsen, P., et al. (2011). Ccr4 promotes resolution of the endoplasmic reticulum stress response during host temperature adaptation in Cryptococcus neoformans. Eukaryotic Cell 10, 895-901. doi: 10.1128/EC.00006-11.
53. Herrero, A. B., Magnelli, P., Mansour, M. K., Levitz, S. M., Bussey, H., and Abeijon, C. (2004). KRE5 gene null mutant strains of Candida albicans are avirulent and have altered cell wall composition and hypha formation properties. Eukaryotic Cell 3, 1423-1432. doi: 10.1128/EC.3.6.1423-1432.2004.
54. Horiuchi, M., Takeuchi, K., Noda, N., Muroya, N., Suzuki, T., Nakamura, T., et al. (2009). Structural basis for the antiproliferative activity of the Tob-hCaf1 complex. J. Biol. Chem. 284, 13244-13255. doi: 10.1074/jbc.M809250200.
55. Ito, W., Li, X., Irie, K., and Mizuno, T. (2011). RNA-binding protein Khd1 and Ccr4 deadenylase play overlapping roles in the cell wall integrity pathway in Saccharomyces cerevisiae. Eukaryotic Cell 10, 1340-1347. doi: 10.1128/EC.05181-11.
56. Jin, R., Dobry, C. J., McCown, P. J., and Kumar, A. (2008). Large-scale analysis of yeast filamentous growth by systematic gene disruption and overexpression. Mol. Biol. Cell 19, 284-296. doi: 10.1091/mbc.E07-05-0519.
57. Jonstrup, A. T., Andersen, K. R., Van, L. B., and Brodersen, D. E. (2007). The 1.4-A crystal structure of the S. pombe Pop2p deadenylase subunit unveils the configuration of an active enzyme. Nucleic Acids Res. 35, 3153-3164. doi: 10.1093/nar/gkm178.
58. Kaeberlein, M., and Guarente, L. (2002). Saccharomyces cerevisiae MPT5 and SSD1 function in parallel pathways to promote cell wall integrity. Genetics 160, 83-95.
59. Kapitzky, L., Beltrao, P., Berens, T. J., Gassner, N., Zhou, C., Wuster, A., et al. (2010). Cross-species chemogenomic profiling reveals evolutionarily conserved drug mode of action. Mol. Syst. Biol. 6, 451. doi: 10.1038/msb.2010.107.
60. Kerr, S. C., Azzouz, N., Fuchs, S. M., Collart, M. A., Strahl, B. D., Corbett, A. H., et al. (2011). The Ccr4-Not complex interacts with the mRNA export machinery. PLoS ONE 6:e18302. doi: 10.1371/journal.pone.0018302.
61. Kruk, J. A., Dutta, A., Fu, J., Gilmour, D. S., and Reese, J. C. (2011). The multifunctional Ccr4-Not complex directly promotes transcription elongation. Genes Dev. 25, 581-593. doi: 10.1101/gad.2020911.
62. Kupferschmidt, K. (2012). Mycology. Attack of the clones.Science 337, 636-638. doi: 10.1126/science.337.6095.636.
63. Lavoie, H., Hogues, H., and Whiteway, M. (2009). Rearrangements of the transcriptional regulatory networks of metabolic pathways in fungi. Curr. Opin. Microbiol. 12, 655-663. doi: 10.1016/j.mib.2009.09.015.
64. Lenssen, E., Azzouz, N., Michel, A., Landrieux, E., and Collart, M. A. (2007). The Ccr4-not complex regulates Skn7 through Srb10 kinase. Eukaryotic Cell 6, 2251-2259. doi: 10.1128/EC.00327-06.
65. Lenssen, E., James, N., Pedruzzi, I., Dubouloz, F., Cameroni, E., Bisig, R., et al. (2005). The Ccr4-Not complex independently controls both Msn2-dependent transcriptional activation-via a newly identified Glc7/Bud14 type I protein phosphatase module-and TFIID promoter distribution. Mol. Cell. Biol. 25, 488-498. doi: 10.1128/MCB.25.1.488-498.2005.
66. Lenssen, E., Oberholzer, U., Labarre, J., De Virgilio, C., and Collart, M. A. (2002). Saccharomyces cerevisiae Ccr4-not complex contributes to the control of Msn2p-dependent transcription by the Ras/cAMP pathway. Mol. Microbiol. 43, 1023-1037. doi: 10.1046/j.1365-2958.2002.02799.x.
67. Levin, D. E. (2011). Regulation of cell wall biogenesis in Saccharomyces cerevisiae: the cell wall integrity signaling pathway. Genetics 189, 1145-1175. doi: 10.1534/genetics.111.128264.
68. Liu, H. Y., Badarinarayana, V., Audino, D. C., Rappsilber, J., Mann, M., and Denis, C. L. (1998). The NOT proteins are part of the CCR4 transcriptional complex and affect gene expression both positively and negatively. EMBO J. 17, 1096-1106. doi: 10.1093/emboj/17.4.1096.
69. Lo, T. L., Qu, Y., Uwamahoro, N., Quenault, T., Beilharz, T. H., and Traven, A. (2012). The mRNA decay pathway regulates the expression of the Flo11 adhesin and biofilm formation in Saccharomyces cerevisiae. Genetics 191, 1387-1391. doi: 10.1534/genetics.112.141432.
70. Lussier, M., Sdicu, A. M., Shahinian, S., and Bussey, H. (1998). The Candida albicans KRE9 gene is required for cell wall beta-1, 6-glucan synthesis and is essential for growth on glucose. Proc. Natl. Acad. Sci. U.S.A. 95, 9825-9830. doi: 10.1073/pnas.95.17.9825.
71. Maguire, S. L., Oheigeartaigh, S. S., Byrne, K. P., Schroder, M. S., O'gaora, P., Wolfe, K. H., et al. (2013). Comparative genome analysis and gene finding in Candida species using CGOB. Mol. Biol. Evol. 30, 1281-1291. doi: 10.1093/molbev/mst042.
72. Markovich, S., Yekutiel, A., Shalit, I., Shadkchan, Y., and Osherov, N. (2004). Genomic approach to identification of mutations affecting caspofungin susceptibility in Saccharomyces cerevisiae. Antimicrob. Agents Chemother. 48, 3871-3876. doi: 10.1128/AAC.48.10.3871-3876.2004.
73. Miller, J. E., and Reese, J. C. (2012). Ccr4-Not complex: the control freak of eukaryotic cells. Crit. Rev. Biochem. Mol. Biol. 47, 315-333. doi: 10.3109/10409238.2012.667214.
74. Moriya, H., and Isono, K. (1999). Analysis of genetic interactions between DHH1, SSD1 and ELM1 indicates their involvement in cellular morphology determination in Saccharomyces cerevisiae. Yeast 15, 481-496.
75. Morrow, C. A., and Fraser, J. A. (2013). Ploidy variation as an adaptive mechanism in human pathogenic fungi. Semin. Cell Dev. Biol. 24, 339-346. doi: 10.1016/j.semcdb.2013.01.008.
76. Mulder, K. W., Winkler, G. S., and Timmers, H. T. (2005). DNA damage and replication stress induced transcription of RNR genes is dependent on the Ccr4-Not complex. Nucleic Acids Res. 33, 6384-6392. doi: 10.1093/nar/gki938.
77. Nasertorabi, F., Batisse, C., Diepholz, M., Suck, D., and Bottcher, B. (2011). Insights into the structure of the CCR4-NOT complex by electron microscopy. FEBS Lett. 585, 2182-2186. doi: 10.1016/j.febslet.2011.05.071.
78. O'Meara, T. R., and Alspaugh, J. A. (2012). The Cryptococcus neoformans capsule: a sword and a shield. Clin. Microbiol. Rev. 25, 387-408. doi: 10.1128/CMR.00001-12.
79. Pan, X., Ye, P., Yuan, D. S., Wang, X., Bader, J. S., and Boeke, J. D. (2006). A DNA integrity network in the yeast Saccharomyces cerevisiae. Cell 124, 1069-1081. doi: 10.1016/j.cell.2005.12.036.
80. Panasenko, O., Landrieux, E., Feuermann, M., Finka, A., Paquet, N., and Collart, M. A. (2006). The yeast Ccr4-Not complex controls ubiquitination of the nascent-associated polypeptide (NAC-EGD) complex. J. Biol. Chem. 281, 31389-31398. doi: 10.1074/jbc.M604986200.
81. Panepinto, J. C., Komperda, K. W., Hacham, M., Shin, S., Liu, X., and Williamson, P. R. (2007). Binding of serum mannan binding lectin to a cell integrity-defective Cryptococcus neoformans ccr4Delta mutant. Infect. Immun. 75, 4769-4779. doi: 10.1128/IAI.00536-07.
82. Panepinto, J., Liu, L., Ramos, J., Zhu, X., Valyi-Nagy, T., Eksi, S., et al. (2005). The DEAD-box RNA helicase Vad1 regulates multiple virulence-associated genes in Cryptococcus neoformans. J. Clin. Invest. 115, 632-641. doi: 10.1172/JCI200523048.
83. Park, Y. U., Hur, H., Ka, M., and Kim, J. (2006). Identification of translational regulation target genes during filamentous growth in Saccharomyces cerevisiae: regulatory role of Caf20 and Dhh1. Eukaryotic Cell 5, 2120-2127. doi: 10.1128/EC.00121-06.
84. Parker, J. E., Merkamm, M., Manning, N. J., Pompon, D., Kelly, S. L., and Kelly, D. E. (2008). Differential azole antifungal efficacies contrasted using a Saccharomyces cerevisiae strain humanized for sterol 14 alpha-demethylase at the homologous locus. Antimicrob. Agents Chemother. 52, 3597-3603. doi: 10.1128/AAC.00517-08.
85. Parsons, A. B., Brost, R. L., Ding, H., Li, Z., Zhang, C., Sheikh, B., et al. (2004). Integration of chemical-genetic and genetic interaction data links bioactive compounds to cellular target pathways. Nat. Biotechnol. 22, 62-69. doi: 10.1038/nbt919.
86. Perrone, G. G., Grant, C. M., and Dawes, I. W. (2005). Genetic and environmental factors influencing glutathione homeostasis in Saccharomyces cerevisiae. Mol. Biol. Cell 16, 218-230. doi: 10.1091/mbc.E04-07-0560.
87. Petit, A. P., Wohlbold, L., Bawankar, P., Huntzinger, E., Schmidt, S., Izaurralde, E., et al. (2012). The structural basis for the interaction between the CAF1 nuclease and the NOT1 scaffold of the human CCR4-NOT deadenylase complex. Nucleic Acids Res. 40, 11058-11072. doi: 10.1093/nar/gks883.
88. Pfaller, M. A., and Diekema, D. J. (2010). Epidemiology of invasive mycoses in North America. Crit. Rev. Microbiol. 36, 1-53. doi: 10.3109/10408410903241444.
89. Qiu, H., Hu, C., Yoon, S., Natarajan, K., Swanson, M. J., and Hinnebusch, A. G. (2004). An array of coactivators is required for optimal recruitment of TATA binding protein and RNA polymerase II by promoter-bound Gcn4p. Mol. Cell Biol. 24, 4104-4117.
90. Qu, Y., Jelicic, B., Pettolino, F., Perry, A., Lo, T. L., Hewitt, V. L., et al. (2012). Mitochondrial sorting and assembly machinery subunit Sam37 in Candida albicans: insight into the roles of mitochondria in fitness, cell wall integrity, and virulence. Eukaryotic Cell 11, 532-544. doi: 10.1128/EC.05292-11.
91. Ronquist, F., and Huelsenbeck, J. P. (2003). MrBayes 3: bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572-1574. doi: 10.1093/bioinformatics/btg180.
92. Ryan, O., Shapiro, R. S., Kurat, C. F., Mayhew, D., Baryshnikova, A., Chin, B., et al. (2012). Global gene deletion analysis exploring yeast filamentous growth. Science 337, 1353-1356. doi: 10.1126/science.1224339.
93. Selmecki, A., Forche, A., and Berman, J. (2010). Genomic plasticity of the human fungal pathogen Candida albicans. Eukaryotic Cell 9, 991-1008. doi: 10.1128/EC.00060-10.
94. Stewart, M. S., Krause, S. A., McGhie, J., and Gray, J. V. (2007). Mpt5p, a stress tolerance-and lifespan-promoting PUF protein in Saccharomyces cerevisiae, acts upstream of the cell wall integrity pathway. Eukaryotic Cell 6, 262-270. doi: 10.1128/EC.00188-06.
95. Sudbery, P. E. (2011). Growth of Candida albicans hyphae. Nat. Rev. Microbiol. 9, 737-748. doi: 10.1038/nrmicro2636.
96. Swanson, M. J., Qiu, H., Sumibcay, L., Krueger, A., Kim, S. J., Natarajan, K., et al. (2003). A multiplicity of coactivators is required by Gcn4p at individual promoters in vivo. Mol. Cell Biol. 23, 2800-2820.
97. Takahashi, S., Kontani, K., Araki, Y., and Katada, T. (2007). Caf1 regulates translocation of ribonucleotide reductase by releasing nucleoplasmic Spd1-Suc22 assembly. Nucleic Acids Res. 35, 1187-1197. doi: 10.1093/nar/gkm015.
98. Tange, Y., Kurabayashi, A., Goto, B., Hoe, K. L., Kim, D. U., Park, H. O., et al. (2012). The CCR4-NOT complex is implicated in the viability of aneuploid yeasts. PLoS Genet. 8:e1002776. doi: 10.1371/journal.pgen.1002776.
99. Traven, A., Hammet, A., Tenis, N., Denis, C. L., and Heierhorst, J. (2005). Ccr4-not complex mRNA deadenylase activity contributes to DNA damage responses in Saccharomyces cerevisiae. Genetics 169, 65-75. doi: 10.1534/genetics.104.030940.
100. Traven, A., Lo, T. L., Lithgow, T., and Heierhorst, J. (2010). The yeast PUF protein Puf5 has Pop2-independent roles in response to DNA replication stress. PLoS ONE 5:e10651. doi: 10.1371/journal.pone.0010651.
101. Tucker, M., Staples, R. R., Valencia-Sanchez, M. A., Muhlrad, D., and Parker, R. (2002). Ccr4p is the catalytic subunit of a Ccr4p/Pop2p/Notp mRNA deadenylase complex in Saccharomyces cerevisiae. EMBO J. 21, 1427-1436. doi: 10.1093/emboj/21.6.1427.
102. Tucker, M., Valencia-Sanchez, M. A., Staples, R. R., Chen, J., Denis, C. L., and Parker, R. (2001). The transcription factor associated Ccr4 and Caf1 proteins are components of the major cytoplasmic mRNA deadenylase in Saccharomyces cerevisiae. Cell 104, 377-386. doi: 10.1016/S0092-8674(01)00225-2.
103. Umeyama, T., Kaneko, A., Watanabe, H., Hirai, A., Uehara, Y., Niimi, M., et al. (2006). Deletion of the CaBIG1 gene reduces beta-1,6-glucan synthesis, filamentation, adhesion, and virulence in Candida albicans. Infect. Immun. 74, 2373-2381. doi: 10.1128/IAI.74.4.2373-2381.2006.
104. Van De Veerdonk, F.L., Kullberg, B. J., Van Der Meer, J.W., Gow, N. A., and Netea, M. G. (2008). Host-microbe interactions: innate pattern recognition of fungal pathogens. Curr. Opin. Microbiol. 11, 305-312. doi: 10.1016/j.mib.2008.06.002.
105. Warrilow, A. G., Parker, J. E., Kelly, D. E., and Kelly, S. L. (2013). Azole affinity of sterol 14alpha-demethylase (CYP51) enzymes from Candida albicans and Homo sapiens. Antimicrob. Agents Chemother. 57, 1352-1360. doi: 10.1128/AAC.02067-12.
106. Westmoreland, T. J., Marks, J. R., Olson, J. A. Jr., Thompson, E. M., Resnick, M. A., and Bennett, C. B. (2004). Cell cycle progression in G1 and S phases is CCR4 dependent following ionizing radiation or replication stress in Saccharomyces cerevisiae. Eukaryotic Cell 3, 430-446. doi: 10.1128/EC.3.2.430-446.2004.
107. Woolstencroft, R. N., Beilharz, T. H., Cook, M. A., Preiss, T., Durocher, D., and Tyers, M. (2006). Ccr4 contributes to tolerance of replication stress through control of CRT1 mRNA poly(A) tail length. J. Cell Sci. 119, 5178-5192. doi: 10.1242/jcs.03221.
108. Zulkifli, M. N., Kaur, J. N., and Panepinto, J. C. (2012). Hydroxyurea enhances post-fusion hyphal extension during sexual development in C. neoformans var. grubii. Mycopathologia 173, 113-119. doi: 10.1007/s11046-011-9474-y.