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Transcriptional profiling and Functional studies of Zinc cluster transcription factors in Candida albicans

Title:

Transcriptional profiling and Functional studies of Zinc cluster transcription factors in Candida albicans

Parvizi Omran, Raha (2021) Transcriptional profiling and Functional studies of Zinc cluster transcription factors in Candida albicans. PhD thesis, Concordia University.

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Abstract

The yeast Candida albicans is a commensal member of the gastrointestinal and urogenital tracts of most healthy humans. However, its capacity to function as an opportunistic pathogen allows it to cause systematic infections of immunocompromised individuals. Over the past two decades, the C. albicans zinc cluster transcription factor family (ZCFs) has been a fascinating subject of research – with studies identifying their roles in virulence, morphogenesis, biofilm formation, drug resistance and many other cellular processes. An understanding of these ZCFs may reveal new targets for therapeutic strategies.
My work focused on generating genome-wide transcriptional profiling for a large subset of 35 ZCF gain-of-function mutants (GOF) to elucidate the transcriptional profiles among the ZCFs, and on investigating in depth the function of some specific ZCFs in the fungal pathogen.
Transcriptional profiling revealed the target genes that are activated by the ZCF-GOF mutants and provided insight into the underlying roles of the factors. My study focused on establishing the transcriptional regulatory relationship among the ZCFs and understanding the function of some uncharacterized ZCFs. In chapter 2, I selected a set of 35 mostly uncharacterized ZCF, or little is known about them to explore their function using RNA-based transcriptional profiling in collaboration with professor M. Hallett lab. The network approach often shows a specific ZCF-GOF caused activation of expression of other ZCFs, which highlights the extensive interactions among ZCFs. We suggest that most expression changes can be the result of downstream longer-term adaptive responses that induce the expression of intermediate transcription factors.
In chapter 3, I characterized a new element involved in hyphal development regulation as a previously unstudied Candida-specific ZCF encoded by CaORF19.1604 that I named Rha1 (Regulator of Hyphal Activity). I identified Rha1 through screening a ZCF-GOF library and noting the Rha1-GOF strain was in a filamentous form under yeast growth conditions. I have characterized Rha1 inactivation mutants and GOF alleles, and I explored the Rha1 regulatory network involving Brg1 and Ume6, which are upregulated hyphal activators that appeared in the Rha1-GOF profile to show that Rha1 affects hyphal gene expression and upregulates Brg1/Ume6 and downregulates Nrg1.
In chapter 4, I investigated the role of ZCF4 in cell wall biogenesis, filamentation, biofilm formation, and drug resistance. I explored the ZCF4 function after noting its upregulation in most of the activated ZCF profiles like Rha1-GOF. Zcf4-GOF showed a severe filamentation defect on serum-based medium but exhibited normal filamentation under other cues. I have shown that ZCF4-influenced filamentation is nutrient dependent.
In chapter 5, I showed the robust ability of C. albicans to use proline as a carbon and nitrogen source by describing CaPut3 as a proline catabolism regulator. The functional studies demonstrated Put3 has a conserved role in regulating proline catabolism in C. albicans and Saccharomyces cerevisiae, but CaPut3 initiates the degradation of proline even in the presence of a rich nitrogen source such as ammonium sulphate.
Collectively, this study established a framework of functional study TFs and generated robust transcriptional data from an activated set of 35 ZCFs to help understand the biology of C. albicans, an important human pathogen.

Divisions:Concordia University > Faculty of Arts and Science > Biology
Item Type:Thesis (PhD)
Authors:Parvizi Omran, Raha
Institution:Concordia University
Degree Name:Ph. D.
Program:Biology
Date:4 November 2021
Thesis Supervisor(s):Whiteway, Malcolm
Keywords:Transcription factors, Transcriptional regulators, Candida albicans, Zinc cluster factors (ZCFs)
ID Code:990139
Deposited By: Raha Parvizi Omran
Deposited On:16 Jun 2022 14:25
Last Modified:16 Jun 2022 14:25

References:

Akache B., and B. Turcotte, 2002 New Regulators of Drug Sensitivity in the Family of Yeast Zinc Cluster Proteins*. J. Biol. Chem. 277: 21254–21260. https://doi.org/10.1074/jbc.M202566200
Amorim-Vaz S., E. Delarze, F. Ischer, D. Sanglard, and A. T. Coste, 2015 Examining the virulence of Candida albicans transcription factor mutants using Galleria mellonella and mouse infection models. Front. Microbiol. 6: 367. https://doi.org/10.3389/fmicb.2015.00367
Askew C., A. Sellam, E. Epp, H. Hogues, A. Mullick, et al., 2009 Transcriptional regulation of carbohydrate metabolism in the human pathogen Candida albicans. PLoS Pathog. 5: e1000612. https://doi.org/10.1371/journal.ppat.1000612
Azadmanesh J., A. M. Gowen, P. E. Creger, N. D. Schafer, and J. R. Blankenship, 2017 Filamentation Involves Two Overlapping, but Distinct, Programs of Filamentation in the Pathogenic Fungus Candida albicans. G3 Bethesda Md 7: 3797–3808. https://doi.org/10.1534/g3.117.300224
Banerjee M. T., 2008 UME6, a Novel Filament-specific Regulator of Candida albicans Hyphal Extension and Virulence. MBoC 19: 1059–1524.
Banerjee M., D. S. Thompson, A. Lazzell, P. L. Carlisle, C. Pierce, et al., 2008 UME6 , a Novel Filament-specific Regulator of Candida albicans Hyphal Extension and Virulence, (H. Riezman, Ed.). Mol. Biol. Cell 19: 1354–1365. https://doi.org/10.1091/mbc.e07-11-1110
Barelle C. J., C. L. Priest, D. M. Maccallum, N. A. R. Gow, F. C. Odds, et al., 2006 Niche-specific regulation of central metabolic pathways in a fungal pathogen. Cell. Microbiol. 8: 961–971. https://doi.org/10.1111/j.1462-5822.2005.00676.x
Bartel P. L., 1991 Current Protocols in Molecular Biology. Frederick M. Ausubel , Roger Brent , Robert E. Kingston , David D. Moore , J. G. Seidman , John A. Smith , Kevin Struhl Short Protocols in Molecular Biology. A Compendium of Methods from Current Protocols in Molecular Biology. Frederick M. Ausubel , Roger Brent , Robert E. Kingston , David D. Moore , J. G. Seidman , John A. Smith , Kevin Struhl. Q. Rev. Biol. 66: 199–200. https://doi.org/10.1086/417163
Basso V., C. d’Enfert, S. Znaidi, and S. Bachellier-Bassi, 2019 From Genes to Networks: The Regulatory Circuitry Controlling Candida albicans Morphogenesis, pp. 61–99 in Fungal Physiology and Immunopathogenesis, Current Topics in Microbiology and Immunology. edited by Rodrigues M. L. Springer International Publishing, Cham.
Basso Jr L. R., A. Bartiss, Y. Mao, C. E. Gast, P. S. Coelho, et al., 2010 Transformation of Candida albicans with a synthetic hygromycin B resistance gene. Yeast 27: 1039–1048.
Benjamini Y., and Y. Hochberg, 1995 Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. J. R. Stat. Soc. Ser. B Methodol. 57: 289–300. https://doi.org/10.1111/j.2517-6161.1995.tb02031
Biswas K., and J. Morschhäuser, 2005 The Mep2p ammonium permease controls nitrogen starvation-induced filamentous growth in Candida albicans. Mol. Microbiol. 56: 649–669. https://doi.org/10.1111/j.1365-2958.2005.04576.x
Biswas S., P. Van Dijck, and A. Datta, 2007 Environmental sensing and signal transduction pathways regulating morphopathogenic determinants of Candida albicans. Microbiol. Mol. Biol. Rev. MMBR 71: 348–376.
Blankenship J. R., and A. P. Mitchell, 2006 How to build a biofilm: a fungal perspective. Curr. Opin. Microbiol. 9: 588–594. https://doi.org/10.1016/j.mib.2006.10.003
Boc A., A. B. Diallo, and V. Makarenkov, 2012 T-REX: a web server for inferring, validating and visualizing phylogenetic trees and networks. Nucleic Acids Res. 40: W573-579. https://doi.org/10.1093/nar/gks485
Bockmühl D. P., and J. F. Ernst, 2001 A Potential Phosphorylation Site for an A-Type Kinase in the Efg1 Regulator Protein Contributes to Hyphal Morphogenesis of Candida albicans. Genetics 157: 1523–1530.
Böhm L., S. Torsin, S. H. Tint, M. T. Eckstein, T. Ludwig, et al., 2017 The yeast form of the fungus Candida albicans promotes persistence in the gut of gnotobiotic mice. PLoS Pathog. 13: e1006699.
Boija A., I. A. Klein, B. R. Sabari, A. Dall’Agnese, E. L. Coffey, et al., 2018 Transcription Factors Activate Genes through the Phase-Separation Capacity of Their Activation Domains. Cell 175: 1842-1855.e16. https://doi.org/10.1016/j.cell.2018.10.042
Boonyasiri A., J. Jearanaisilavong, and S. Assanasen, 2013 Candidemia in Siriraj Hospital: epidemiology and factors associated with mortality. J Med Assoc Thai 96: S91-97.
Böttcher B., C. Pöllath, P. Staib, B. Hube, and S. Brunke, 2016 Candida species Rewired Hyphae Developmental Programs for Chlamydospore Formation. Front. Microbiol. 7: 1697. https://doi.org/10.3389/fmicb.2016.01697
Brandriss M. C., and B. Magasanik, 1979 Genetics and physiology of proline utilization in Saccharomyces cerevisiae: enzyme induction by proline. J. Bacteriol. 140: 498–503. https://doi.org/10.1128/jb.140.2.498-503.1979
Braun B. R., and A. D. Johnson, 1997 Control of Filament Formation in Candida albicans by the Transcriptional Repressor TUP1. Science 277: 105–109. https://doi.org/10.1126/science.277.5322.105
Braun B. R., and A. D. Johnson, 2000 TUP1, CPH1 and EFG1 make independent contributions to filamentation in Candida albicans. Genetics 155: 57–67.
Braun B. R., D. Kadosh, and A. D. Johnson, 2001 NRG1, a repressor of filamentous growth in Candida. albicans, is down‐regulated during filament induction. EMBO J. 20: 4753–4761.
Brown G. D., D. W. Denning, N. A. R. Gow, S. M. Levitz, M. G. Netea, et al., 2012 Hidden Killers: Human Fungal Infections. Sci. Transl. Med. 4: 165rv13-165rv13. https://doi.org/10.1126/scitranslmed.3004404
Brown A. J. P., S. Budge, D. Kaloriti, A. Tillmann, M. D. Jacobsen, et al., 2014 Stress adaptation in a pathogenic fungus. J. Exp. Biol. 217: 144–155. https://doi.org/10.1242/jeb.088930
Buffo J., M. A. Herman, and D. R. Soll, 1984 A characterization of pH-regulated dimorphism in Candida albicans. Mycopathologia 85: 21–30. https://doi.org/10.1007/BF00436698
Calderone R. A., and C. J. Clancy, 2011 Candida and Candidiasis. American Society for Microbiology Press.
Carlisle P. L., and D. Kadosh, 2013 A genome-wide transcriptional analysis of morphology determination in Candida albicans. Mol. Biol. Cell 24: 246–260. https://doi.org/10.1091/mbc.e12-01-0065
Cassola A., M. Parrot, S. Silberstein, B. B. Magee, S. Passeron, et al., 2004 Candida albicans Lacking the Gene Encoding the Regulatory Subunit of Protein Kinase A Displays a Defect in Hyphal Formation and an Altered Localization of the Catalytic Subunit. Eukaryot. Cell 3: 190–199. https://doi.org/10.1128/EC.3.1.190-199.2004
CDC, 2013 Antibiotic resistance threats in the United States.
Chaillot J., M. A. Cook, J. Corbeil, and A. Sellam, 2017 Genome-Wide Screen for Haploinsufficient Cell Size Genes in the Opportunistic Yeast Candida albicans. G3 Bethesda Md 7: 355–360. https://doi.org/10.1534/g3.116.037986
Chamilos G., C. J. Nobile, V. M. Bruno, R. E. Lewis, A. P. Mitchell, et al., 2009 Candida albicans Cas5, a regulator of cell wall integrity, is required for virulence in murine and toll mutant fly models. J. Infect. Dis. 200: 152–157. https://doi.org/10.1086/599363
Chandra J., D. M. Kuhn, P. K. Mukherjee, L. L. Hoyer, T. McCormick, et al., 2001 Biofilm Formation by the Fungal PathogenCandida albicans: Development, Architecture, and Drug Resistance. J. Bacteriol. 183: 5385–5394. https://doi.org/10.1128/JB.183.18.5385-5394.2001
Chen C., K. Pande, S. D. French, B. B. Tuch, and S. M. Noble, 2011 An Iron Homeostasis Regulatory Circuit with Reciprocal Roles in Candida albicans Commensalism and Pathogenesis. Cell Host Microbe 10: 118–135. https://doi.org/10.1016/j.chom.2011.07.005
Cherry J. M., E. L. Hong, C. Amundsen, R. Balakrishnan, G. Binkley, et al., 2012 Saccharomyces Genome Database: the genomics resource of budding yeast. Nucleic Acids Res. 40: D700-705. https://doi.org/10.1093/nar/gkr1029
Clarke M., A. J. Lohan, B. Liu, I. Lagkouvardos, S. Roy, et al., 2013 Genome of Acanthamoeba castellanii highlights extensive lateral gene transfer and early evolution of tyrosine kinase signaling. Genome Biol. 14: R11.
Cleary I. A., A. L. Lazzell, C. Monteagudo, D. P. Thomas, and S. P. Saville, 2012 BRG1 and NRG1 form a novel feedback circuit regulating Candida albicans hypha formation and virulence. Mol. Microbiol. 85: 557–573. https://doi.org/10.1111/j.1365-2958.2012.08127
Cooper T. G., C. Lam, and V. Turoscy, 1980 Structural Analysis of the dur Loci in S. CEREVISIAE: Two Domains of a Single Multifunctional Gene. Genetics 94: 555–580.
Cornu T. I., S. Thibodeau-Beganny, E. Guhl, S. Alwin, M. Eichtinger, et al., 2008 DNA-binding Specificity Is a Major Determinant of the Activity and Toxicity of Zinc-finger Nucleases. Mol. Ther. 16: 352–358. https://doi.org/10.1038/sj.mt.6300357
Costa A. C. B. P., R. P. Omran, T. O. Correia-Mesquita, V. Dumeaux, and M. Whiteway, 2019 Screening of Candida albicans GRACE library revealed a unique pattern of biofilm formation under repression of the essential gene ILS1. Sci. Rep. 9: 1–12.
Coste A. T., M. Karababa, F. Ischer, J. Bille, and D. Sanglard, 2004 TAC1, transcriptional activator of CDR genes, is a new transcription factor involved in the regulation of Candida albicans ABC transporters CDR1 and CDR2. Eukaryot. Cell 3: 1639–1652. https://doi.org/10.1128/EC.3.6.1639-1652.2004
Coste A. T., M. Ramsdale, F. Ischer, and D. Sanglard, 2008 Divergent functions of three Candida albicans zinc-cluster transcription factors (CTA4, ASG1 and CTF1) complementing pleiotropic drug resistance in Saccharomyces cerevisiae. Microbiology 154: 1491–1501. https://doi.org/10.1099/mic.0.2007/016063-0
Crawford A. C., L. E. Lehtovirta-Morley, O. Alamir, M. J. Niemiec, B. Alawfi, et al., 2018 Biphasic zinc compartmentalisation in a human fungal pathogen. PLoS Pathog. 14: e1007013. https://doi.org/10.1371/journal.ppat.1007013
Dabas N., and J. Morschhäuser, 2007 Control of ammonium permease expression and filamentous growth by the GATA transcription factors GLN3 and GAT1 in Candida albicans. Eukaryot. Cell 6: 875–888. https://doi.org/10.1128/EC.00307-06
Dalal C. K., I. A. Zuleta, K. F. Mitchell, D. R. Andes, H. El-Samad, et al., 2016 Transcriptional rewiring over evolutionary timescales changes quantitative and qualitative properties of gene expression, (N. Barkai, Ed.). eLife 5: e18981. https://doi.org/10.7554/eLife.18981
Dalal C. K., and A. D. Johnson, 2017 How transcription circuits explore alternative architectures while maintaining overall circuit output. Genes Dev. 31: 1397–1405. https://doi.org/10.1101/gad.303362.117
Daniels K. J., Y. N. Park, T. Srikantha, C. Pujol, and D. R. Soll, 2013 Impact of environmental conditions on the form and function of Candida albicans biofilms. Eukaryot. Cell 12: 1389–1402. https://doi.org/10.1128/EC.00127-13
Des Etages S. A., D. Saxena, H. L. Huang, D. A. Falvey, D. Barber, et al., 2001 Conformational changes play a role in regulating the activity of the proline utilization pathway-specific regulator in Saccharomyces cerevisiae. Mol. Microbiol. 40: 890–899. https://doi.org/10.1046/j.1365-2958.2001.02432.x
Devaux F., P. Marc, C. Bouchoux, T. Delaveau, I. Hikkel, et al., 2001 An artificial transcription activator mimics the genome-wide properties of the yeast Pdr1 transcription factor. EMBO Rep. 2: 493–498. https://doi.org/10.1093/embo-reports/kve114
Doedt T., S. Krishnamurthy, D. P. Bockmuhl, B. Tebarth, C. Stempel, et al., 2004 APSES proteins regulate morphogenesis and metabolism in Candida albicans. Mol. Biol. Cell 15: 3167–3180. https://doi.org/10.1091/mbc.e03-11-0782
Dowell R. D., 2010 Transcription factor binding variation in the evolution of gene regulation. Trends Genet. 26: 468–475. https://doi.org/10.1016/j.tig.2010.08.005
Du H., G. Guan, J. Xie, Y. Sun, Y. Tong, et al., 2012 Roles of Candida albicans Gat2, a GATA-type zinc finger transcription factor, in biofilm formation, filamentous growth and virulence. PloS One 7: e29707. https://doi.org/10.1371/journal.pone.0029707
Dunkel N., J. Blass, P. D. Rogers, and J. Morschhäuser, 2008 Mutations in the multi-drug 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. https://doi.org/10.1111/j.1365-2958.2008.06309.x
Duret L., E. Gasteiger, and G. Perrière, 1996 LALNVIEW: a graphical viewer for pairwise sequence alignments. Comput. Appl. Biosci. CABIOS 12: 507–510. https://doi.org/10.1093/bioinformatics/12.6.507
Edgar R., M. Domrachev, and A. E. Lash, 2002 Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 30: 207–210.
Fan Y., H. He, Y. Dong, and H. Pan, 2013 Hyphae-Specific Genes HGC1, ALS3, HWP1, and ECE1 and Relevant Signaling Pathways in Candida albicans. Mycopathologia 176: 329–335. https://doi.org/10.1007/s11046-013-9684-6
Fanning S., and A. P. Mitchell, 2012 Fungal Biofilms. PLOS Pathog. 8: e1002585. https://doi.org/10.1371/journal.ppat.1002585
Feller A., E. Dubois, F. Ramos, and A. Piérard, 1994 Repression of the genes for lysine biosynthesis in Saccharomyces cerevisiae is caused by limitation of Lys14-dependent transcriptional activation. Mol. Cell. Biol. 14: 6411–6418. https://doi.org/10.1128/mcb.14.10.6411-6418.1994
Feng Q., E. Summers, B. Guo, and G. Fink, 1999 Ras signaling is required for serum-induced hyphal differentiation in Candida albicans. J. Bacteriol. 181: 6339–6346. https://doi.org/10.1128/JB.181.20.6339-6346.1999
Feng J., S. Yao, Y. Dong, J. Hu, M. Whiteway, et al., 2020 Nucleotide Excision Repair Protein Rad23 Regulates Cell Virulence Independent of Rad4 in Candida albicans. mSphere 5. https://doi.org/10.1128/mSphere.00062-20
Fernández E., F. Moreno, and R. Rodicio, 1992 The ICL1 gene from Saccharomyces cerevisiae. Eur. J. Biochem. 204: 983–990. https://doi.org/10.1111/j.1432-1033.1992.tb16720.x
Finkel J. S., W. Xu, D. Huang, E. M. Hill, J. V. Desai, et al., 2012 Portrait of Candida albicans Adherence Regulators. PLoS Pathog. 8. https://doi.org/10.1371/journal.ppat.1002525
Friden P., and P. Schimmel, 1988 LEU3 of Saccharomyces cerevisiae activates multiple genes for branched-chain amino acid biosynthesis by binding to a common decanucleotide core sequence. Mol. Cell. Biol. 8: 2690–2697. https://doi.org/10.1128/mcb.8.7.2690-2697.1988
Ghosh S., B. W. Kebaara, A. L. Atkin, and K. W. Nickerson, 2008 Regulation of aromatic alcohol production in Candida albicans. Appl. Environ. Microbiol. 74: 7211–7218. https://doi.org/10.1128/AEM.01614-08
Ghosh S., D. H. M. L. P. Navarathna, D. D. Roberts, J. T. Cooper, A. L. Atkin, et al., 2009 Arginine-Induced Germ Tube Formation in Candida albicans Is Essential for Escape from Murine Macrophage Line RAW 264.7. Infect. Immun. 77: 1596–1605. https://doi.org/10.1128/IAI.01452-08
Giaever G., A. M. Chu, L. Ni, C. Connelly, L. Riles, et al., 2002 Functional profiling of the Saccharomyces cerevisiae genome. Nature 418: 387–391. https://doi.org/10.1038/nature00935
Gietz R. D., R. H. Schiestl, A. R. Willems, and R. A. Woods, 1995 Studies on the transformation of intact yeast cells by the LiAc/SS-DNA/PEG procedure. Yeast Chichester Engl. 11: 355–360.
Gillum A. M., E. Y. Tsay, and D. R. Kirsch, 1984 Isolation of the Candida albicans gene for orotidine-5′-phosphate decarboxylase by complementation of S. cerevisiae ura3 and E. coli pyrF mutations. Mol. Gen. Genet. MGG 198: 179–182.
Gola S., R. Martin, A. Walther, A. Dünkler, and J. Wendland, 2003 New modules for PCR-based gene targeting in Candida albicans: rapid and efficient gene targeting using 100 bp of flanking homology region. Yeast Chichester Engl. 20: 1339–1347. https://doi.org/10.1002/yea.1044
Grant C. E., T. L. Bailey, and W. S. Noble, 2011 FIMO: scanning for occurrences of a given motif. Bioinforma. Oxf. Engl. 27: 1017–1018. https://doi.org/10.1093/bioinformatics/btr064
Gray W. M., and J. S. Fassler, 1996 Isolation and analysis of the yeast TEA1 gene, which encodes a zinc cluster Ty enhancer-binding protein. Mol. Cell. Biol. 16: 347–358. https://doi.org/10.1128/MCB.16.1.347
Gray K. C., D. S. Palacios, I. Dailey, M. M. Endo, B. E. Uno, et al., 2012 Amphotericin primarily kills yeast by simply binding ergosterol. Proc. Natl. Acad. Sci. 109: 2234–2239. https://doi.org/10.1073/pnas.1117280109
Greenblatt H. K., and D. J. Greenblatt, 2014 Liver injury associated with ketoconazole: Review of the published evidence. J. Clin. Pharmacol. 54: 1321–1329. https://doi.org/10.1002/jcph.400
Grove C. A., and A. J. M. Walhout, 2008 Transcription factor functionality and transcription regulatory networks. Mol. Biosyst. 4: 309–314. https://doi.org/10.1039/b715909a
Gu Z., R. Eils, and M. Schlesner, 2016 Complex heatmaps reveal patterns and correlations in multidimensional genomic data. Bioinforma. Oxf. Engl. 32: 2847–2849. https://doi.org/10.1093/bioinformatics/btw313
Gulati M., and C. J. Nobile, 2016 Candida albicans biofilms: development, regulation, and molecular mechanisms. Microbes Infect. Inst. Pasteur 18: 310–321. https://doi.org/10.1016/j.micinf.2016.01.002
Gustavsen J. A., S. Pai, R. Isserlin, B. Demchak, and A. R. Pico, 2019 RCy3: Network biology using Cytoscape from within R. F1000Research 8: 1774. https://doi.org/10.12688/f1000research.20887.3
Han T.-L., R. D. Cannon, S. M. Gallo, and S. G. Villas-Bôas, 2019 A metabolomic study of the effect of Candida albicans glutamate dehydrogenase deletion on growth and morphogenesis. Npj Biofilms Microbiomes 5: 1–14. https://doi.org/10.1038/s41522-019-0086-5
Harbison C. T., D. B. Gordon, T. I. Lee, N. J. Rinaldi, K. D. Macisaac, et al., 2004 Transcriptional regulatory code of a eukaryotic genome. Nature 431: 99–104. https://doi.org/10.1038/nature02800
He K., G. Gkioxari, P. Dollár, and R. Girshick, 2017 Mask r-cnn, pp. 2961–2969 in.
Hernández-Cervantes A., S. Znaidi, L. van Wijlick, I. Denega, V. Basso, et al., 2020 A conserved regulator controls asexual sporulation in the fungal pathogen Candida albicans. Nat. Commun. 11: 6224. https://doi.org/10.1038/s41467-020-20010-9
Hikkel I., A. Lucau-Danila, T. Delaveau, P. Marc, F. Devaux, et al., 2003 A General Strategy to Uncover Transcription Factor Properties Identifies a New Regulator of Drug Resistance in Yeast *. J. Biol. Chem. 278: 11427–11432. https://doi.org/10.1074/jbc.M208549200
Ho S.-W., G. Jona, C. T. L. Chen, M. Johnston, and M. Snyder, 2006 Linking DNA-binding proteins to their recognition sequences by using protein microarrays. Proc. Natl. Acad. Sci. U. S. A. 103: 9940–9945. https://doi.org/10.1073/pnas.0509185103
Hogues H., H. Lavoie, A. Sellam, M. Mangos, T. Roemer, et al., 2008 Transcription Factor Substitution during the Evolution of Fungal Ribosome Regulation. Mol. Cell 29: 552–562. https://doi.org/10.1016/j.molcel.2008.02.006
Homann O. R., J. Dea, S. M. Noble, and A. D. Johnson, 2009 A phenotypic profile of the Candida albicans regulatory network. PLoS Genet. 5: e1000783. https://doi.org/10.1371/journal.pgen.1000783
Huang X., and W. Miller, 1991 A time-efficient, linear-space local similarity algorithm. Adv. Appl. Math. 12: 337–357. https://doi.org/10.1016/0196-8858(91)90017-D
Huang H. L., and M. C. Brandriss, 2000 The Regulator of the Yeast Proline Utilization Pathway Is Differentially Phosphorylated in Response to the Quality of the Nitrogen Source. Mol. Cell. Biol. 20: 892–899. https://doi.org/10.1128/MCB.20.3.892-899.2000
Ignatiadis N., B. Klaus, J. B. Zaugg, and W. Huber, 2016 Data-driven hypothesis weighting increases detection power in genome-scale multiple testing. Nat. METHODS 13: 577–580. https://doi.org/10.1038/NMETH.3885
Inglis D. O., M. B. Arnaud, J. Binkley, P. Shah, M. S. Skrzypek, et al., 2012 The Candida genome database incorporates multiple Candida species: multispecies search and analysis tools with curated gene and protein information for Candida albicans and Candida glabrata. Nucleic Acids Res. 40: D667-674. https://doi.org/10.1093/nar/gkr945
Iraqui I., S. Vissers, B. André, and A. Urrestarazu, 1999 Transcriptional Induction by Aromatic Amino Acids in Saccharomyces cerevisiae. Mol. Cell. Biol. 19: 3360–3371. https://doi.org/10.1128/MCB.19.5.3360
Issi L., R. A. Farrer, K. Pastor, B. Landry, T. Delorey, et al., 2017 Zinc Cluster Transcription Factors Alter Virulence in Candida albicans. Genetics 205: 559–576. https://doi.org/10.1534/genetics.116.195024
Jansuriyakul S., P. Somboon, N. Rodboon, O. Kurylenko, A. Sibirny, et al., 2016 The zinc cluster transcriptional regulator Asg1 transcriptionally coordinates oleate utilization and lipid accumulation in Saccharomyces cerevisiae. Appl. Microbiol. Biotechnol. 100: 4549–4560. https://doi.org/10.1007/s00253-016-7356-4
Jenull S., M. Tscherner, M. Gulati, C. J. Nobile, N. Chauhan, et al., 2017 The Candida albicans HIR histone chaperone regulates the yeast-to-hyphae transition by controlling the sensitivity to morphogenesis signals. Sci. Rep. 7: 1–17.
Jiang H., R. Lei, S.-W. Ding, and S. Zhu, 2014 Skewer: a fast and accurate adapter trimmer for next-generation sequencing paired-end reads. BMC Bioinformatics 15: 182. https://doi.org/10.1186/1471-2105-15-182
Jiménez-López C., J. R. Collette, K. M. Brothers, K. M. Shepardson, R. A. Cramer, et al., 2013 Candida albicans induces arginine biosynthetic genes in response to host-derived reactive oxygen species. Eukaryot. Cell 12: 91–100.
Johnson D. C., K. E. Cano, E. C. Kroger, and D. S. McNabb, 2005 Novel Regulatory Function for the CCAAT-Binding Factor in Candida albicans. Eukaryot. Cell 4: 1662–1676. https://doi.org/10.1128/EC.4.10.1662-1676.2005
Jungwirth H., and K. Kuchler, 2006 Yeast ABC transporters – A tale of sex, stress, drugs and aging. FEBS Lett. 580: 1131–1138. https://doi.org/10.1016/j.febslet.2005.12.050
Kadosh D., and A. D. Johnson, 2005 Induction of the Candida albicans filamentous growth program by relief of transcriptional repression: A genome-wide analysis. Mol. Biol. Cell 16: 2903–2912. https://doi.org/10.1091/mbc.E05-01-0073
Kafri R., M. Levy, and Y. Pilpel, 2006 The regulatory utilization of genetic redundancy through responsive backup circuits. Proc. Natl. Acad. Sci. U. S. A. 103: 11653–11658.
Kaiser B., T. Munder, H.-P. Saluz, W. Künkel, and R. Eck, 1999 Identification of a gene encoding the pyruvate decarboxylase gene regulator CaPdc2p from Candida albicans. Yeast 15: 585–591. https://doi.org/10.1002/(SICI)1097-0061(199905)15:7<585::AID-YEA401>3.0.CO;2-9
Kakade P., P. Sadhale, K. Sanyal, and V. Nagaraja, 2016 ZCF32, a fungus specific Zn (II) 2 Cys6 transcription factor, is a repressor of the biofilm development in the human pathogen Candida albicans. Sci. Rep. 6: 31124.
Kasten M. M., and D. J. Stillman, 1997 Identification of the Saccharomyces cerevisiae genes STB1–STB5 encoding Sin3p binding proteins. Mol. Gen. Genet. MGG 256: 376–386. https://doi.org/10.1007/s004380050581
Kim J., and P. Sudbery, 2011 Candida albicans, a major human fungal pathogen. J. Microbiol. 49: 171.
Kim D., B. Langmead, and S. L. Salzberg, 2015 HISAT: a fast spliced aligner with low memory requirements. Nat. Methods 12: 357–360.
Kim D., J. M. Paggi, C. Park, C. Bennett, and S. L. Salzberg, 2019 Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nat. Biotechnol. 37: 907–915. https://doi.org/10.1038/s41587-019-0201-4
Klengel T., W.-J. Liang, J. Chaloupka, C. Ruoff, K. Schröppel, et al., 2005 Fungal adenylyl cyclase integrates CO2 sensing with cAMP signaling and virulence. Curr. Biol. CB 15: 2021–2026. https://doi.org/10.1016/j.cub.2005.10.040
Köhler G. A., T. C. White, and N. Agabian, 1997 Overexpression of a cloned IMP dehydrogenase gene of Candida albicans confers resistance to the specific inhibitor mycophenolic acid. J. Bacteriol. 179: 2331–2338. https://doi.org/10.1128/jb.179.7.2331-2338.1997
Kohlhaw G. B., 2003 Leucine Biosynthesis in Fungi: Entering Metabolism through the Back Door. Microbiol. Mol. Biol. Rev. 67: 1–15. https://doi.org/10.1128/MMBR.67.1.1-15.2003
Kopylova E., L. Noé, and H. Touzet, 2012 SortMeRNA: fast and accurate filtering of ribosomal RNAs in metatranscriptomic data. Bioinformatics 28: 3211–3217. https://doi.org/10.1093/bioinformatics/bts611
Kornitzer D., 2019 Regulation of Candida albicans hyphal morphogenesis by endogenous signals. J. Fungi 5: 21.
Kullberg B. J., and M. C. Arendrup, 2015 Invasive Candidiasis. http://dx.doi.org/10.1056/NEJMra1315399.
Kumamoto C. A., and M. D. Vinces, 2005 Contributions of hyphae and hypha-co-regulated genes to Candida albicans virulence. Cell. Microbiol. 7: 1546–1554. https://doi.org/10.1111/j.1462-5822.2005.00616
Laity J. H., B. M. Lee, and P. E. Wright, 2001 Zinc finger proteins: new insights into structural and functional diversity. Curr. Opin. Struct. Biol. 11: 39–46. https://doi.org/10.1016/S0959-440X(00)00167-6
Lan C.-Y., G. Newport, L. A. Murillo, T. Jones, S. Scherer, et al., 2002 Metabolic specialization associated with phenotypic switching in Candida albicans. Proc. Natl. Acad. Sci. U. S. A. 99: 14907–14912. https://doi.org/10.1073/pnas.232566499
Latchman D. S., 1997 Transcription factors: an overview. Int. J. Biochem. Cell Biol. 29: 1305–1312. https://doi.org/10.1016/s1357-2725(97)00085-x
Lavoie H., A. Sellam, C. Askew, A. Nantel, and M. Whiteway, 2008 A toolbox for epitope-tagging and genome-wide location analysis in Candida albicans. BMC Genomics 9: 578. https://doi.org/10.1186/1471-2164-9-578
Lavoie H., H. Hogues, J. Mallick, A. Sellam, A. Nantel, et al., 2010 Evolutionary Tinkering with Conserved Components of a Transcriptional Regulatory Network. PLOS Biol. 8: e1000329. https://doi.org/10.1371/journal.pbio.1000329
Leberer E., D. Harcus, D. Dignard, L. Johnson, S. Ushinsky, et al., 2001 Ras links cellular morphogenesis to virulence by regulation of the MAP kinase and cAMP signalling pathways in the pathogenic fungus Candida albicans. Mol. Microbiol. 42: 673–687. https://doi.org/10.1046/j.1365-2958.2001.02672.x
Lee K. L., H. R. Buckley, and C. C. Campbell, 1975 An amino acid liquid synthetic medium for the development of mycelial and yeast forms of Candida albicans. Sabouraudia 13: 148–153. https://doi.org/10.1080/00362177585190271
Leverentz M. K., and R. J. Reece, 2006 Phosphorylation of Zn(II)2Cys6 proteins: a cause or effect of transcriptional activation? Biochem. Soc. Trans. 34: 794–797. https://doi.org/10.1042/BST0340794
Leverentz M. K., R. N. Campbell, Y. Connolly, A. D. Whetton, and R. J. Reece, 2009 Mutation of a phosphorylatable residue in Put3p affects the magnitude of rapamycin-induced PUT1 activation in a Gat1p-dependent manner. J. Biol. Chem. 284: 24115–24122. https://doi.org/10.1074/jbc.M109.030361
Li H., B. Handsaker, A. Wysoker, T. Fennell, J. Ruan, et al., 2009 The sequence alignment/map format and SAMtools. Bioinformatics 25: 2078–2079.
Liu H., J. Kohler, and G. R. Fink, 1994 Suppression of hyphal formation in Candida albicans by mutation of a STE12 homolog. Science 266: 1723–1726. https://doi.org/10.1126/science.7992058
Liu Y., and S. G. Filler, 2011 Candida albicans Als3, a Multifunctional Adhesin and Invasin. Eukaryot. Cell 10: 168–173. https://doi.org/10.1128/EC.00279-10
Lo H.-J., J. R. Köhler, G. R. Fink, B. Didomenico, D. Loebenberg, et al., 1997 Nonfilamentous Candida. albicans mutants are avirulent. Cell 90: 939–949. https://doi.org/10.1016/S0092-8674(00)80358
Lorenz M. C., J. A. Bender, and G. R. Fink, 2004 Transcriptional Response of Candida albicans upon Internalization by Macrophages. Eukaryot. Cell 3: 1076–1087. https://doi.org/10.1128/EC.3.5.1076-1087.2004
Love M. I., W. Huber, and S. Anders, 2014 Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15: 550. https://doi.org/10.1186/s13059-014-0550-8
Lu Y., C. Su, X. Mao, P. P. Raniga, H. Liu, et al., 2008 Efg1-mediated Recruitment of NuA4 to Promoters Is Required for Hypha-specific Swi/Snf Binding and Activation in Candida albicans. Mol. Biol. Cell 19: 4260–4272. https://doi.org/10.1091/mbc.E08-02-0173
Lu Y., C. Su, A. Wang, and H. Liu, 2011 Hyphal Development in Candida albicans Requires Two Temporally Linked Changes in Promoter Chromatin for Initiation and Maintenance. PLoS Biol. 9: 1–17. https://doi.org/10.1371/journal.pbio.1001105
Lu Y., C. Su, and H. Liu, 2012 A GATA transcription factor recruits Hda1 in response to reduced Tor1 signaling to establish a hyphal chromatin state in Candida albicans. PLoS Pathog. 8: e1002663. https://doi.org/10.1371/journal.ppat.1002663
Lu Y., C. Su, and H. Liu, 2014 Candida albicans hyphal initiation and elongation. Trends Microbiol. 22: 707–714.
Lu A. X., T. Zarin, I. S. Hsu, and A. M. Moses, 2019 YeastSpotter: accurate and parameter-free web segmentation for microscopy images of yeast cells. Bioinformatics 35: 4525–4527.
MacPherson S., B. Akache, S. Weber, X. De Deken, M. Raymond, et al., 2005 Candida albicans zinc cluster protein Upc2p confers resistance to antifungal drugs and is an activator of ergosterol biosynthetic genes. Antimicrob. Agents Chemother. 49: 1745–1752.
MacPherson S., M. Larochelle, and B. Turcotte, 2006 A fungal family of transcriptional regulators: the zinc cluster proteins. Microbiol. Mol. Biol. Rev. MMBR 70: 583–604.
Maicas S., I. Moreno, A. Nieto, M. Gomez, R. Sentandreu, et al., 2005 In silico analysis for transcription factors with Zn(II)(2)C(6) binuclear cluster DNA-binding domains in Candida albicans. Comp. Funct. Genomics 6: 345–356. https://doi.org/10.1002/cfg.492
Martchenko M., A. Levitin, H. Hogues, A. Nantel, and M. Whiteway, 2007 Transcriptional Rewiring of Fungal Galactose-Metabolism Circuitry. Curr. Biol. CB 17: 1007–1013. https://doi.org/10.1016/j.cub.2007.05.017
Martin M., 2011 Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.journal 17: 10–12.
Martin R., D. Albrecht-Eckardt, S. Brunke, B. Hube, K. Hunniger, et al., 2013 A core filamentation response network in Candida albicans is restricted to eight genes. PloS One 8: e58613. https://doi.org/10.1371/journal.pone.0058613
Martínez P., and P. O. Ljungdahl, 2004 An ER packaging chaperone determines the amino acid uptake capacity and virulence of Candida albicans. Mol. Microbiol. 51: 371–384. https://doi.org/10.1046/j.1365-2958.2003.03845.x
Marzluf G. A., 1997 Genetic regulation of nitrogen metabolism in the fungi. Microbiol. Mol. Biol. Rev. MMBR 61: 17–32. https://doi.org/10.1128/.61.1.17-32.1997
Mayer F. L., D. Wilson, and B. Hube, 2013 Candida albicans pathogenicity mechanisms. Virulence 4: 119–128.
Mendizabal I., G. Rios, J. M. Mulet, R. Serrano, and I. F. de Larrinoa, 1998 Yeast putative transcription factors involved in salt tolerance. FEBS Lett. 425: 323–328. https://doi.org/10.1016/s0014-5793(98)00249-x
Middelhoven W. J., 1964 The pathway of arginine breakdown in Saccharomyces cerevisiae. Biochim. Biophys. Acta BBA - Gen. Subj. 93: 650–652. https://doi.org/10.1016/0304-4165(64)90349-6
Miller M. G., and A. D. Johnson, 2002 White-opaque switching in Candida albicans is controlled by mating-type locus homeodomain proteins and allows efficient mating. Cell 110: 293–302. https://doi.org/10.1016/s0092-8674(02)00837-1
Min K., Y. Ichikawa, C. A. Woolford, and A. P. Mitchell, 2016 Candida albicans Gene Deletion with a Transient CRISPR-Cas9 System. mSphere 1: 10.1128/mSphere.00130-16. eCollection 2016 May-Jun. https://doi.org/10.1128/mSphere.00130-16
Miramón P., and M. C. Lorenz, 2017 A feast for Candida: Metabolic plasticity confers an edge for virulence. PLOS Pathog. 13: e1006144. https://doi.org/10.1371/journal.ppat.1006144
Morschhäuser J., 2010 Regulation of multidrug resistance in pathogenic fungi. Fungal Genet. Biol. 47: 94–106. https://doi.org/10.1016/j.fgb.2009.08.002
Müller C. W., 2001 Transcription factors: global and detailed views. Curr. Opin. Struct. Biol. 11: 26–32. https://doi.org/10.1016/S0959-440X(00)00163-9
Murad A. M. A., P. Leng, M. Straffon, J. Wishart, S. Macaskill, et al., 2001 NRG1 represses yeast–hypha morphogenesis and hypha-specific gene expression in Candida albicans. EMBO J. 20: 4742–4752. https://doi.org/10.1093/emboj/20.17.4742
Naglik J., A. Albrecht, O. Bader, and B. Hube, 2004 Candida albicans proteinases and host/pathogen interactions. Cell. Microbiol. 6: 915–926. https://doi.org/10.1111/j.1462-5822.2004.00439.x
Nantel A., T. Rigby, H. Hogues, and M. Whiteway, 2006 Microarrays for Studying Pathogenicity in Candida albicans, pp. 181–209 in Medical Mycology, John Wiley & Sons, Ltd.
Nicholls S., M. D. Leach, C. L. Priest, and A. J. P. Brown, 2009 Role of the heat shock transcription factor, Hsf1, in a major fungal pathogen that is obligately associated with warm-blooded animals. Mol. Microbiol. 74: 844–861. https://doi.org/10.1111/j.1365-2958.2009.06883.x
Nishida I., D. Watanabe, and H. Takagi, 2016 Putative mitochondrial α-ketoglutarate-dependent dioxygenase Fmp12 controls utilization of proline as an energy source in Saccharomyces cerevisiae. Microb. Cell 3: 522–528. https://doi.org/10.15698/mic2016.10.535
Nobile C. J., V. M. Bruno, M. L. Richard, D. A. Davis, and A. P. Mitchell, 2003 Genetic control of chlamydospore formation in Candida albicans. Microbiol. Read. Engl. 149: 3629–3637. https://doi.org/10.1099/mic.0.26640-0
Nobile C. J., and A. P. Mitchell, 2005 Regulation of Cell-Surface Genes and Biofilm Formation by the Candida. albicans Transcription Factor Bcr1p. Curr. Biol. 15: 1150–1155. https://doi.org/10.1016/j.cub.2005.05.047
Nobile C. J., E. P. Fox, J. E. Nett, T. R. Sorrells, Q. M. Mitrovich, et al., 2012 A recently evolved transcriptional network controls biofilm development in Candida albicans. Cell 148: 126–138. https://doi.org/10.1016/j.cell.2011.10.048
Nobile C. J., and A. D. Johnson, 2015 Candida albicans Biofilms and Human Disease. Annu. Rev. Microbiol. 69: 71–92. https://doi.org/10.1146/annurev-micro-091014-104330
Noble S. M., and A. D. Johnson, 2005 Strains and strategies for large-scale gene deletion studies of the diploid human fungal pathogen Candida albicans. Eukaryot. Cell 4: 298–309.
Noble S. M., S. French, L. A. Kohn, V. Chen, and A. D. Johnson, 2010 Systematic screens of a Candida albicans homozygous deletion library decouple morphogenetic switching and pathogenicity. Nat. Genet. 42: 590–598. https://doi.org/10.1038/ng.605
Noble S. M., B. A. Gianetti, and J. N. Witchley, 2017 Candida albicans cell-type switching and functional plasticity in the mammalian host. Nat. Rev. Microbiol. 15: 96–108. https://doi.org/10.1038/nrmicro.2016.157
Odds F. C., A. J. Brown, and N. A. Gow, 2004 Candida albicans genome sequence: a platform for genomics in the absence of genetics. Genome Biol. 5: 230. https://doi.org/10.1186/gb-2004-5-7-230
Oh J., E. Fung, U. Schlecht, R. W. Davis, G. Giaever, et al., 2010 Gene annotation and drug target discovery in Candida albicans with a tagged transposon mutant collection. PLoS Pathog. 6: e1001140. https://doi.org/10.1371/journal.ppat.1001140
Oliveira-Pacheco J., R. Alves, A. Costa-Barbosa, B. Cerqueira-Rodrigues, P. Pereira-Silva, et al., 2018 The Role of Candida albicans Transcription Factor RLM1 in Response to Carbon Adaptation. Front. Microbiol. 9. https://doi.org/10.3389/fmicb.2018.01127
Omran R. P., B. Ramírez-Zavala, W. Aji Tebung, S. Yao, J. Feng, et al., 2021 The zinc cluster transcription factor Rha1 is a positive filamentation regulator in Candida albicans. Genetics. https://doi.org/10.1093/genetics/iyab155
Onda M., K. Ota, T. Chiba, Y. Sakaki, and T. Ito, 2004 Analysis of gene network regulating yeast multidrug resistance by artificial activation of transcription factors: involvement of Pdr3 in salt tolerance. Gene 332: 51–59. https://doi.org/10.1016/j.gene.2004.02.003
Patro R., G. Duggal, M. I. Love, R. A. Irizarry, and C. Kingsford, 2017 Salmon provides fast and bias-aware quantification of transcript expression. Nat. Methods 14: 417–419. https://doi.org/10.1038/nmeth.4197
Perez J. C., C. A. Kumamoto, and A. D. Johnson, 2013 Candida albicans commensalism and pathogenicity are intertwined traits directed by a tightly knit transcriptional regulatory circuit. PLoS Biol. 11: e1001510. https://doi.org/10.1371/journal.pbio.1001510
Perlin D. S., 2011 Current perspectives on echinocandin class drugs. Future Microbiol. 6: 441–457. https://doi.org/10.2217/fmb.11.19
Pertea M., G. M. Pertea, C. M. Antonescu, T.-C. Chang, J. T. Mendell, et al., 2015 StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat. Biotechnol. 33: 290–295. https://doi.org/10.1038/nbt.3122
Pfaller M. A., and D. J. Diekema, 2010 Epidemiology of Invasive Mycoses in North America. Crit. Rev. Microbiol. 36: 1–53. https://doi.org/10.3109/10408410903241444
Pfeifer K., K. S. Kim, S. Kogan, and L. Guarente, 1989 Functional dissection and sequence of yeast HAP1 activator. Cell 56: 291–301. https://doi.org/10.1016/0092-8674(89)90903-3
Polke M., B. Hube, and I. D. Jacobsen, 2015 Chapter Three - Candida Survival Strategies, pp. 139–235 in Advances in Applied Microbiology, edited by Sariaslani S., Gadd G. M. Academic Press.
Prelich G., 2012 Gene overexpression: uses, mechanisms, and interpretation. Genetics 190: 841–854. https://doi.org/10.1534/genetics.111.136911
Priyadarshini Y., and K. Natarajan, 2016 Reconfiguration of Transcriptional Control of Lysine Biosynthesis in Candida albicans Involves a Central Role for the Gcn4 Transcriptional Activator. mSphere 1: e00016-15. https://doi.org/10.1128/mSphere.00016-15
R Core Team, 2020,
Ramachandra S., J. Linde, M. Brock, R. Guthke, B. Hube, et al., 2014 Regulatory Networks Controlling Nitrogen Sensing and Uptake in Candida albicans. PLoS ONE 9. https://doi.org/10.1371/journal.pone.0092734
Ramírez M. A., and M. C. Lorenz, 2009 The Transcription Factor Homolog CTF1 Regulates β-Oxidation in Candida albicans. Eukaryot. Cell 8: 1604–1614. https://doi.org/10.1128/EC.00206-09
Raz-Pasteur A., Y. Ullmann, and I. Berdicevsky, 2011 The Pathogenesis of Candida Infections in a Human Skin Model: Scanning Electron Microscope Observations. ISRN Dermatol. 2011. https://doi.org/10.5402/2011/150642
Remm M., C. E. Storm, and E. L. Sonnhammer, 2001 Automatic clustering of orthologs and in-paralogs from pairwise species comparisons. J. Mol. Biol. 314: 1041–1052. https://doi.org/10.1006/jmbi.2000.5197
Reuß O., Å. Vik, R. Kolter, and J. Morschhäuser, 2004 The SAT1 flipper, an optimized tool for gene disruption in Candida albicans. Gene 341: 119–127. https://doi.org/10.1016/j.gene.2004.06.021
Rodriguez D. L., M. M. Quail, A. D. Hernday, and C. J. Nobile, 2020 Transcriptional Circuits Regulating Developmental Processes in Candida albicans. Front. Cell. Infect. Microbiol. 10: 605711. https://doi.org/10.3389/fcimb.2020.605711
Rooney P. J., and B. S. Klein, 2002 Linking fungal morphogenesis with virulence. Cell. Microbiol. 4: 127–137. https://doi.org/10.1046/j.1462-5822.2002.00179
Rose M. D., F. M. Winston, and P. Heiter, 1990 Methods in yeast genetics: a laboratory course manual. Cold Spring Harbor Laboratory Press.
Sabina J., and V. Brown, 2009 Glucose Sensing Network in Candida albicans: a Sweet Spot for Fungal Morphogenesis. Eukaryot. Cell 8: 1314–1320. https://doi.org/10.1128/EC.00138-09
Santos R., N. Buisson, S. Knight, A. Dancis, J.-M. Camadro, et al., 2003 Haemin uptake and use as an iron source by Candida albicans: role of CaHMX1-encoded haem oxygenase. Microbiol. Read. Engl. 149: 579–588. https://doi.org/10.1099/mic.0.26108-0
Santos M., and I. F. de Larrinoa, 2005 Functional characterization of the Candida albicans CRZ1 gene encoding a calcineurin-regulated transcription factor. Curr. Genet. 48: 88–100. https://doi.org/10.1007/s00294-005-0003-8
Sasse C., R. Schillig, F. Dierolf, M. Weyler, S. Schneider, et al., 2011 The Transcription Factor Ndt80 Does Not Contribute to Mrr1-, Tac1-, and Upc2-Mediated Fluconazole Resistance in Candida albicans. PLOS ONE 6: e25623. https://doi.org/10.1371/journal.pone.0025623
Saville S. P., A. L. Lazzell, C. Monteagudo, and J. L. Lopez-Ribot, 2003 Engineered control of cell morphology in vivo reveals distinct roles for yeast and filamentous forms of Candida albicans during infection. Eukaryot. Cell 2: 1053–1060. https://doi.org/10.1128/ec.2.5.1053-1060.2003
Schillig R., and J. Morschhäuser, 2013 Analysis of a fungus‐specific transcription factor family, the Candida. albicans zinc cluster proteins, by artificial activation. Mol. Microbiol. 89: 1003–1017.
Segal E. S., V. Gritsenko, A. Levitan, B. Yadav, N. Dror, et al., 2018 Gene Essentiality Analyzed by In Vivo Transposon Mutagenesis and Machine Learning in a Stable Haploid Isolate of Candida albicans. mBio 9: e02048-18. https://doi.org/10.1128/mBio.02048-18
Sellick C. A., R. N. Campbell, and R. J. Reece, 2008 Chapter 3 Galactose Metabolism in Yeast—Structure and Regulation of the Leloir Pathway Enzymes and the Genes Encoding Them, pp. 111–150 in International Review of Cell and Molecular Biology, Academic Press.
Shannon P., A. Markiel, O. Ozier, N. S. Baliga, J. T. Wang, et al., 2003 Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13: 2498–2504. https://doi.org/10.1101/gr.1239303
Shapiro R. S., P. Uppuluri, A. K. Zaas, C. Collins, H. Senn, et al., 2009 Hsp90 orchestrates temperature-dependent Candida albicans morphogenesis via Ras1-PKA signaling. Curr. Biol. CB 19: 621–629. https://doi.org/10.1016/j.cub.2009.03.017
Shapiro R. S., N. Robbins, and L. E. Cowen, 2011 Regulatory Circuitry Governing Fungal Development, Drug Resistance, and Disease. Microbiol. Mol. Biol. Rev. 75: 213–267. https://doi.org/10.1128/MMBR.00045-10
Shen L., 2013 GeneOverlap: An R package to test and visualize gene overlaps. 12.
Shen X.-X., X. Zhou, J. Kominek, C. P. Kurtzman, C. T. Hittinger, et al., 2016 Reconstructing the Backbone of the Saccharomycotina Yeast Phylogeny Using Genome-Scale Data. G3 GenesGenomesGenetics 6: 3927–3939. https://doi.org/10.1534/g3.116.034744
Sheppard D. C., M. R. Yeaman, W. H. Welch, Q. T. Phan, Y. Fu, et al., 2004 Functional and structural diversity in the Als protein family of Candida albicans. J. Biol. Chem. 279: 30480–30489. https://doi.org/10.1074/jbc.M401929200
Sikorski T. W., and S. Buratowski, 2009 The basal initiation machinery: beyond the general transcription factors. Curr. Opin. Cell Biol. 21: 344–351. https://doi.org/10.1016/j.ceb.2009.03.006
Silao F. G. S., M. Ward, K. Ryman, A. Wallström, B. Brindefalk, et al., 2019 Mitochondrial proline catabolism activates Ras1/cAMP/PKA-induced filamentation in Candida albicans. PLOS Genet. 15: e1007976. https://doi.org/10.1371/journal.pgen.1007976
Simonetti N., V. Strippoli, and A. Cassone, 1974 Yeast-mycelial conversion induced by N-acetyl-D-glucosamine in Candida albicans. Nature 250: 344–346. https://doi.org/10.1038/250344a0
Skrzypek M. S., J. Binkley, G. Binkley, S. R. Miyasato, M. Simison, et al., 2017 The Candida Genome Database (CGD): incorporation of Assembly 22, systematic identifiers and visualization of high throughput sequencing data. Nucleic Acids Res. 45: D592–D596. https://doi.org/10.1093/nar/gkw924
Smith J. J., S. A. Ramsey, M. Marelli, B. Marzolf, D. Hwang, et al., 2007 Transcriptional responses to fatty acid are coordinated by combinatorial control. Mol. Syst. Biol. 3: 115. https://doi.org/10.1038/msb4100157
Soneson C., M. I. Love, and M. D. Robinson, 2016 Differential analyses for RNA-seq: transcript-level estimates improve gene-level inferences [version 2; referees: 2 approved]. F1000Research. https://doi.org/10.12688/f1000research.7563.2
Song L., and L. Florea, 2015 Rcorrector: efficient and accurate error correction for Illumina RNA-seq reads. GigaScience 4: 48. https://doi.org/10.1186/s13742-015-0089-y
Souza M. M. de, A. Zerlotini, L. Geistlinger, P. C. Tizioto, J. F. Taylor, et al., 2018 A comprehensive manually-curated compendium of bovine transcription factors. Sci. Rep. 8: 13747. https://doi.org/10.1038/s41598-018-32146-2
Spitz F., and E. E. M. Furlong, 2012 Transcription factors: from enhancer binding to developmental control. Nat. Rev. Genet. 13: 613–626. https://doi.org/10.1038/nrg3207
Spitzner A., A. F. Perzlmaier, K. E. Geillinger, P. Reihl, and J. Stolz, 2008 The proline-dependent transcription factor Put3 regulates the expression of the riboflavin transporter MCH5 in Saccharomyces cerevisiae. Genetics 180: 2007–2017. https://doi.org/10.1534/genetics.108.094458
Sprenger M., T. S. Hartung, S. Allert, S. Wisgott, M. J. Niemiec, et al., 2020 Fungal biotin homeostasis is essential for immune evasion after macrophage phagocytosis and virulence. Cell. Microbiol. 22: e13197. https://doi.org/10.1111/cmi.13197
Staib P., and J. Morschhäuser, 2007 Chlamydospore formation in Candida albicans and Candida dubliniensis--an enigmatic developmental programme. Mycoses 50: 1–12. https://doi.org/10.1111/j.1439-0507.2006.01308.x
Stoldt V. R., A. Sonneborn, C. E. Leuker, and J. F. Ernst, 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. https://doi.org/10.1093/emboj/16.8.1982
Stothard P., 2000 The sequence manipulation suite: JavaScript programs for analyzing and formatting protein and DNA sequences. BioTechniques 28: 1102, 1104. https://doi.org/10.2144/00286ir01
Sudbery P., N. Gow, and J. Berman, 2004 The distinct morphogenic states of Candida albicans. Trends Microbiol. 12: 317–324. https://doi.org/10.1016/j.tim.2004.05.008
Sudbery P. E., 2011 Growth of Candida albicans hyphae. Nat. Rev. Microbiol. 9: 737–748. https://doi.org/10.1038/nrmicro2636
Sumrada R. A., and T. G. Cooper, 1987 Ubiquitous upstream repression sequences control activation of the inducible arginase gene in yeast. Proc. Natl. Acad. Sci. 84: 3997–4001. https://doi.org/10.1073/pnas.84.12.3997
Swaminathan K., P. Flynn, R. J. Reece, and R. Marmorstein, 1997 Crystal structure of a PUT3–DNA complex reveals a novel mechanism for DMA recognition by a protein containing a Zn2Cys6 binuclear cluster. Nat. Struct. Biol. 4: 751–759. https://doi.org/10.1038/nsb0997-751
Talibi D., and M. Raymond, 1999 Isolation of a Putative Candida albicansTranscriptional Regulator Involved in Pleiotropic Drug Resistance by Functional Complementation of a pdr1 pdr3 Mutation inSaccharomyces cerevisiae. J. Bacteriol. 181: 231–240. https://doi.org/10.1128/JB.181.1.231-240.1999
Taschdjian C. L., J. J. Burchall, and P. J. Kozinn, 1960 Rapid identification of Candida albicans by filamentation on serum and serum substitutes. AMA J. Dis. Child. 99: 212–215. https://doi.org/10.1001/archpedi.1960.02070030214011
Tebung W. A., B. I. Choudhury, F. Tebbji, J. Morschhäuser, and M. Whiteway, 2016 Rewiring of the Ppr1 Zinc Cluster Transcription Factor from Purine Catabolism to Pyrimidine Biogenesis in the Saccharomycetaceae. Curr. Biol. CB 26: 1677–1687. https://doi.org/10.1016/j.cub.2016.04.064
Tebung W. A., R. P. Omran, D. L. Fulton, J. Morschhauser, and M. Whiteway, 2017 Put3 Positively Regulates Proline Utilization in Candida albicans. mSphere 2: e00354-17.
Tong I. L., and R. A. Young, 2000 Transcription of Eukaryotic Protein-Coding Genes. Annu. Rev. Genet. 34: 77. https://doi.org/10.1146/annurev.genet.34.1.77
Tsao C.-C., Y.-T. Chen, and C.-Y. Lan, 2009 A small G protein Rhb1 and a GTPase-activating protein Tsc2 involved in nitrogen starvation-induced morphogenesis and cell wall integrity of Candida albicans. Fungal Genet. Biol. FG B 46: 126–136. https://doi.org/10.1016/j.fgb.2008.11.008
Turner S. A., and G. Butler, 2014 The Candida pathogenic species complex. Cold Spring Harb. Perspect. Med. 4: a019778. https://doi.org/10.1101/cshperspect.a019778
Uhl M. A., M. Biery, N. Craig, and A. D. Johnson, 2003 Haploinsufficiency-based large-scale forward genetic analysis of filamentous growth in the diploid human fungal pathogen C.albicans. EMBO J. 22: 2668–2678. https://doi.org/10.1093/emboj/cdg256
Uppuluri P., and W. L. Chaffin, 2007 Defining Candida albicans stationary phase by cellular and DNA replication, gene expression and regulation. Mol. Microbiol. 64: 1572–1586. https://doi.org/10.1111/j.1365-2958.2007.05760.x
Valdés-Hevia M. D., R. de la Guerra, and C. Gancedo, 1989 Isolation and characterization of the gene encoding phosphoenolpyruvate carboxykinase from Saccharomyces cerevisiae. FEBS Lett. 258: 313–316. https://doi.org/10.1016/0014-5793(89)81682-5
Vandeputte P., F. Ischer, D. Sanglard, and A. T. Coste, 2011 In vivo systematic analysis of Candida albicans Zn2-Cys6 transcription factors mutants for mice organ colonization. PloS One 6: e26962. https://doi.org/10.1371/journal.pone.0026962
Vik A null, and J. Rine, 2001 Upc2p and Ecm22p, dual regulators of sterol biosynthesis in Saccharomyces cerevisiae. Mol. Cell. Biol. 21: 6395–6405. https://doi.org/10.1128/MCB.21.19.6395-6405.2001
Vincent K., Q. Wang, S. Jay, K. Hobbs, and B. C. Rymond, 2003 Genetic interactions with CLF1 identify additional pre-mRNA splicing factors and a link between activators of yeast vesicular transport and splicing. Genetics 164: 895–907.
Vyas V. K., M. I. Barrasa, and G. R. Fink, 2015 A Candida albicans CRISPR system permits genetic engineering of essential genes and gene families. Sci. Adv. 1. https://doi.org/10.1126/sciadv.1500248
Wang H., Z. Xu, L. Gao, and B. Hao, 2009 A fungal phylogeny based on 82 complete genomes using the composition vector method. BMC Evol. Biol. 9: 195. https://doi.org/10.1186/1471-2148-9-195
Wapinski I., A. Pfeffer, N. Friedman, and A. Regev, 2007 Natural history and evolutionary principles of gene duplication in fungi. Nature 449: 54–61. https://doi.org/10.1038/nature06107
Ward L. D., and H. J. Bussemaker, 2008 Predicting functional transcription factor binding through alignment-free and affinity-based analysis of orthologous promoter sequences. Bioinformatics 24: i165–i171. https://doi.org/10.1093/bioinformatics/btn154
White T. C., K. A. Marr, and R. A. Bowden, 1998 Clinical, Cellular, and Molecular Factors That Contribute to Antifungal Drug Resistance. Clin. Microbiol. Rev. 11: 382–402.
Whiteway M., and C. Bachewich, 2007 Morphogenesis in Candida albicans. Annu. Rev. Microbiol. 61: 529–553. https://doi.org/10.1146/annurev.micro.61.080706.093341
Whiteway M., W. A. Tebung, B. I. Choudhury, and R. Rodríguez-Ortiz, 2015 Metabolic regulation in model ascomycetes--adjusting similar genomes to different lifestyles. Trends Genet. TIG 31: 445–453. https://doi.org/10.1016/j.tig.2015.05.002
Whittington A., N. A. R. Gow, and B. Hube, 2014 1 From Commensal to Pathogen: Candida albicans, pp. 3–18 in Human Fungal Pathogens, The Mycota. edited by Kurzai O. Springer, Berlin, Heidelberg.
Woods K., and T. Höfken, 2016 The zinc cluster proteins Upc2 and Ecm22 promote filamentation in Saccharomyces cerevisiae by sterol biosynthesis-dependent and -independent pathways. Mol. Microbiol. 99: 512–527. https://doi.org/10.1111/mmi.13244
Xu W., N. V. Solis, R. L. Ehrlich, C. A. Woolford, S. G. Filler, et al., 2015 Activation and alliance of regulatory pathways in Candida. albicans during mammalian infection. PLoS Biol. 13: e1002076. https://doi.org/10.1371/journal.pbio.1002076
Zeidler U., T. Lettner, C. Lassnig, M. Müller, R. Lajko, et al., 2009 UME6 is a crucial downstream target of other transcriptional regulators of true hyphal development in Candida albicans. FEMS Yeast Res. 9: 126–142.
Zhao X., S.-H. Oh, K. M. Yeater, and L. L. Y. 2005 Hoyer, 2005 Analysis of the Candida albicans Als2p and Als4p adhesins suggests the potential for compensatory function within the Als family. Microbiology 151: 1619–1630. https://doi.org/10.1099/mic.0.27763-0
Zhu Y., H.-M. Fang, Y.-M. Wang, G.-S. Zeng, X.-D. Zheng, et al., 2009 Ras1 and Ras2 play antagonistic roles in regulating cellular cAMP level, stationary-phase entry and stress response in Candida albicans. Mol. Microbiol. 74: 862–875. https://doi.org/10.1111/j.1365-2958.2009.06898.x
Zhu W., and S. G. Filler, 2010 Interactions of Candida albicans with epithelial cells. Cell. Microbiol. 12: 273–282. https://doi.org/10.1111/j.1462-5822.2009.01412.x
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