Using in vivo transcriptomics and RNA enrichment to identify genes involved in virulence of Candida glabrata

References

• Magill SS, Edwards JR, Bamberg W, et al. Multistate point-prevalence survey of health care-associated infections. N Engl J Med. 2014 Mar 27;370(13):1198–1208.
   PubMed Web of Science ®Google Scholar
• Lamoth F, Lockhart SR, Berkow EL, et al. Changes in the epidemiological landscape of invasive candidiasis. J Antimicrob Chemother. 2018 Jan 1;73(suppl_1):i4–i13.
   PubMedGoogle Scholar
• Pfaller MA, Diekema DJ, Turnidge JD, et al. Twenty years of the SENTRY antifungal surveillance program: results for Candida species from 1997-2016. Open Forum Infect Dis. 2019;6(Suppl 1):S79–S94.
   PubMedGoogle Scholar
• Bolotin-Fukuhara M, Fairhead C. Candida glabrata: a deadly companion? Yeast. 2014 Aug;31(8):279–288.
   PubMed Web of Science ®Google Scholar
• Maccallum DM. Hosting infection: experimental models to assay Candida virulence. Int J Microbiol. 2012;2012:363764.
   PubMedGoogle Scholar
• Kurtzman CP, Robnett CJ. Three new insect-associated species of the yeast genus Candida. Can J Microbiol. 1998 Oct;44(10):965–973.
   PubMed Web of Science ®Google Scholar
• Gabaldon T, Martin T, Marcet-Houben M, et al. Comparative genomics of emerging pathogens in the Candida glabrata clade. BMC Genomics. 2013 Sep 14;14:623.
   PubMed Web of Science ®Google Scholar
• Roetzer A, Gabaldon T, Schuller C. From Saccharomyces cerevisiae to Candida glabratain a few easy steps: important adaptations for an opportunistic pathogen. FEMS Microbiol Lett. 2011 Jan;314(1):1–9.
   PubMed Web of Science ®Google Scholar
• Kim J, Sudbery P. Candida albicans, a major human fungal pathogen. J Microbiol. 2011 Apr;49(2):171–177.
   PubMed Web of Science ®Google Scholar
• Calderone RA, Fonzi WA. Virulence factors of Candida albicans. Trends Microbiol. 2001 Jul;9(7):327–335.
   PubMed Web of Science ®Google Scholar
• Poulain D. Candida albicans, plasticity and pathogenesis. Crit Rev Microbiol. 2015 Jun;41(2):208–217.
   PubMed Web of Science ®Google Scholar
• Padder SA, Ramzan A, and Tahir I, et al. Metabolic flexibility and extensive adaptability governing multiple drug resistance and enhanced virulence in Candida albicans. Crit Rev Microbiol. 2021;48(2): 1–20.
   PubMedGoogle Scholar
• Kaur R, Ma B, Cormack BP. A family of glycosylphosphatidylinositol-linked aspartyl proteases is required for virulence of Candida glabrata. Proc Natl Acad Sci U S a. 2007 May 1;104(18):7628–7633.
   PubMed Web of Science ®Google Scholar
• Lopez-Fuentes E, Gutierrez-Escobedo G, and Timmermans B, et al. Candida glabrata’s genome plasticity confers a unique pattern of expressed cell wall proteins. J Fungi (Basel). 2018 Jun 5;4:(2). DOI:10.3390/jof4020067
   PubMedGoogle Scholar
• Kasper L, Seider K, Hube B. Intracellular survival of Candida glabrata in macrophages: immune evasion and persistence. FEMS Yeast Res. 2015 Aug;15(5):fov042.
   PubMed Web of Science ®Google Scholar
• Cuellar-Cruz M, Briones-Martin-Del-Campo M, Canas-Villamar I, et al. High resistance to oxidative stress in the fungal pathogen Candida glabrata is mediated by a single catalase, Cta1p, and is controlled by the transcription factors Yap1p, Skn7p, Msn2p, and Msn4p. Eukaryot Cell. 2008;7(5):814–825.
   PubMedGoogle Scholar
• Chew SY, Ho KL, and Cheah YK, et al. Physiologically relevant alternative carbon sources modulate biofilm formation, cell wall architecture, and the stress and antifungal resistance of Candida glabrata. Int J Mol Sci. 2019 Jun 28;20:(13). DOI:10.3390/ijms20133172
   Web of Science ®Google Scholar
• Freese S, Vogts T, Speer F, et al. C- and N-catabolic utilization of tricarboxylic acid cycle-related amino acids by Scheffersomyces stipitis and other yeasts. Yeast. 2011;28(5):375–390. DOI:10.1002/yea.1845
   PubMed Web of Science ®Google Scholar
• Rasheed M, Battu A, Kaur R. Host-Pathogen interaction in Candida glabrata infection: current knowledge and implications for antifungal therapy. Expert Rev Anti Infect Ther. 2020 Nov;18(11):1093–1103.
   PubMed Web of Science ®Google Scholar
• Vale-Silva LA, Sanglard D. Tipping the balance both ways: drug resistance and virulence in Candida glabrata. FEMS Yeast Res. 2015 Jun;15(4):fov025.
   PubMed Web of Science ®Google Scholar
• Whaley SG, Rogers PD. Azole resistance in Candida glabrata. Curr Infect Dis Rep. 2016 Dec;18(12):41.
   PubMed Web of Science ®Google Scholar
• Healey KR, Zhao Y, Perez WB, et al. Prevalent mutator genotype identified in fungal pathogen Candida glabrata promotes multi-drug resistance. Nat Commun. 2016 Mar 29;7:11128.
   PubMed Web of Science ®Google Scholar
• Ferrari S, Sanguinetti M, De Bernardis F, et al. Loss of mitochondrial functions associated with azole resistance in Candida glabrata results in enhanced virulence in mice. Antimicrob Agents Chemother. 2011;55(5):1852–1860.
   PubMed Web of Science ®Google Scholar
• Ferrari S, Sanguinetti M, Torelli R, et al. Contribution of CgPDR1-regulated genes in enhanced virulence of azole-resistant Candida glabrata. PLoS One. 2011 Mar 9;6(3):e17589. DOI:10.1371/journal.pone.0017589
   PubMed Web of Science ®Google Scholar
• Nakayama H, Ueno K, Uno J, et al. Growth defects resulting from inhibiting ERG20 and RAM2 in Candida glabrata. FEMS Microbiol Lett. 2011;317(1):27–33.
   PubMed Web of Science ®Google Scholar
• Schrevens S, and Sanglard D. Investigating Candida glabrata urinary tract infections (UTIs) in mice using bioluminescence imaging. J Fungi (Basel). 2021 Oct 9;7(10). DOI:10.3390/jof7100844
   PubMedGoogle Scholar
• Rasheed M, Battu A, Kaur R. Aspartyl proteases in Candida glabrata are required for suppression of the host innate immune response. J Biol Chem. 2018 Apr 27;293(17):6410–6433.
   PubMed Web of Science ®Google Scholar
• Kammer P, McNamara S, and Wolf T, et al. Survival strategies of pathogenic Candida species in human blood show independent and specific adaptations. Mbio. 2020 Oct 6;11(5):e02435–20.
   PubMed Web of Science ®Google Scholar
• Pekmezovic M, Hovhannisyan H, Gresnigt MS, et al. Candida pathogens induce protective mitochondria-associated type I interferon signalling and a damage-driven response in vaginal epithelial cells. Nat Microbiol. 2021;6(5):643–657.
   PubMed Web of Science ®Google Scholar
• Amorim-Vaz S, Tran Vdu T, and Pradervand S, et al. RNA enrichment method for quantitative transcriptional analysis of pathogens in vivo applied to the fungus Candida albicans. Mbio. 2015 Sep 22;6(5): e00942–15.
   PubMed Web of Science ®Google Scholar
• Silva S, Negri M, Henriques M, et al. Silicone colonization by non-Candida albicans Candida species in the presence of urine. J Med Microbiol. 2010;59(Pt 7):747–754.
   PubMed Web of Science ®Google Scholar
• Gharaghani M, Taghipour S, Halvaeezadeh M, et al. Candiduria; a review article with specific data from Iran. Turk J Urol. 2018;44(6):445–452.
   PubMed Web of Science ®Google Scholar
• Sierra-Diaz E, Hernandez-Rios CJ, Bravo-Cuellar A. Antibiotic resistance: microbiological profile of urinary tract infections in Mexico. Cir Cir. 2019;87(2):176–182.
   PubMed Web of Science ®Google Scholar
• Peng D, Li X, Liu P, et al. Epidemiology of pathogens and antimicrobial resistance of catheter-associated urinary tract infections in intensive care units: a systematic review and meta-analysis. Am J Infect Control. 2018;46(12):e81–e90.
   PubMed Web of Science ®Google Scholar
• Santana MMP, Hoffmann-Santos HD, Dias LB, et al. Epidemiological profile of patients hospitalized with candiduria in the Central-Western region of Brazil. Rev Iberoam Micol. 2019;36(4):175–180.
   PubMed Web of Science ®Google Scholar
• Jain AK, Misra V, Ranjan N, et al. Speciation, Biofilm formation and antifungal susceptibility of Candida isolates from clinically diagnosed patient of UTI in a tertiary care hospital. J Assoc Physicians India. 2019;67(9):42–45.
   PubMedGoogle Scholar
• Gajdacs M, Doczi I, Abrok M, et al. Epidemiology of candiduria and Candida urinary tract infections in inpatients and outpatients: results from a 10-year retrospective survey. Cent European J Urol. 2019;72(2):209–214.
   PubMed Web of Science ®Google Scholar
• Denis B, Chopin D, Piron P, et al. Candiduria in kidney transplant recipients: is antifungal therapy useful? Mycoses. 2018;61(5):298–304. DOI:10.1111/myc.12740
   PubMed Web of Science ®Google Scholar
• Robinson MD, Oshlack A. A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol. 2010;11(3):R25.
   PubMed Web of Science ®Google Scholar
• Law CW, Chen Y, Shi W, et al. Voom: precision weights unlock linear model analysis tools for RNA-seq read counts. Genome Biol. [2014 Feb 3];15(2):R29.
   PubMed Web of Science ®Google Scholar
• Leek JT, Johnson WE, Parker HS, et al. The sva package for removing batch effects and other unwanted variation in high-throughput experiments. Bioinformatics. 2012 Mar 15 28;(6):882–883. DOI:10.1093/bioinformatics/bts034
   PubMed Web of Science ®Google Scholar
• Ge SX, Jung D, Yao R. ShinyGO: a graphical gene-set enrichment tool for animals and plants. Bioinformatics. 2020 Apr 15; 36(8):2628–2629. DOI:10.1093/bioinformatics/btz931
   PubMed Web of Science ®Google Scholar
• Wu T, Hu E, Xu S, et al. clusterProfiler 4.0: a universal enrichment tool for interpreting omics data. The Innovation. 2021;2(3):100141. 2021/08/28/. DOI:10.1016/j.xinn.2021.100141
   PubMedGoogle Scholar
• Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Royal Statistical Soc Ser B Methodol. 1995;57(1):289–300.
   Google Scholar
• Yu G. Gene ontology semantic similarity analysis using GOSemSim. In: Kidder B, editor. Stem cell transcriptional networks: Methods and protocols. New York, NY: Springer US; 2020. pp. 207–215.
   Google Scholar
• Kannan A, Asner SA, Trachsel E, et al. Comparative genomics for the elucidation of multidrug resistance in Candida lusitaniae. mBio. 2019 Dec 24;10(6). DOI:10.1128/mBio.02512-19
   Web of Science ®Google Scholar
• Vale-Silva L, Ischer F, Leibundgut-Landmann S, et al. Gain of function mutations in CgPDR1, a regulator of antifungal drug resistance in Candida glabrata, control adherence to host cells. Infect Immun. 2013 Mar 4;81(5):1709–1720.
   PubMed Web of Science ®Google Scholar
• Domergue R, Castaño I, De Las Peñas A, et al. Nicotinic acid limitation regulates silencing of Candida adhesins during UTI. Sci. 2005 May 6;308(5723):866–870.
   PubMed Web of Science ®Google Scholar
• Landry DW, Bazari H. 116 - Approach to the patient with renal disease. In: Goldman L, Schafer AI, editors. Goldman’s cecil medicine (Twenty Fourth Edition). Philadelphia: W.B. Saunders; 2012. pp. 708–716.
   Google Scholar
• Domergue R, Castano I, De Las Penas A, et al. Nicotinic acid limitation regulates silencing of Candida adhesins during UTI. Sci. 2005 May 6;308(5723):866–870.
   PubMed Web of Science ®Google Scholar
• Ferrari S, Ischer F, Calabrese D, et al. Gain of function mutations in CgPDR1 of Candida glabrata not only mediate antifungal resistance but also enhance virulence. PLoS Pathog. 2009 Jan 16;5(1):e1000268.
   PubMed Web of Science ®Google Scholar
• Naglik J, Albrecht A, Bader O, et al. Candida albicans proteinases and host/pathogen interactions. Cell Microbiol. 2004;6(10):915–926.
   PubMed Web of Science ®Google Scholar
• Vale-Silva L, Beaudoing E, and Tran VDT, et al. Comparative genomics of two sequential Candida glabrata clinical isolates. G3 (Bethesda). 2017 Aug 7; 7(8):2413–2426.
   PubMedGoogle Scholar
• Xu Z, Green B, Benoit N, et al. De Novo genome assembly of Candida glabrata reveals cell wall protein complement and structure of dispersed tandem repeat arrays. Mol Microbiol. 2020;113(6):1209–1224.
   PubMed Web of Science ®Google Scholar
• Shimamura S, Miyazaki T, Tashiro M, et al. Autophagy-Inducing factor Atg1 is required for virulence in the pathogenic fungus Candida glabrata. Front Microbiol. 2019;10:27.
   PubMed Web of Science ®Google Scholar
• Nagi M, Tanabe K, Ueno K, et al. The Candida glabrata sterol scavenging mechanism, mediated by the ATP-binding cassette transporter Aus1p, is regulated by iron limitation. Mol Microbiol. 2013;88(2):371–381.
   PubMed Web of Science ®Google Scholar
• Srivastava VK, Suneetha KJ, Kaur R. The mitogen-activated protein kinase CgHog1 is required for iron homeostasis, adherence and virulence in Candida glabrata. Febs J. 2015 Jun;282(11):2142–2166.
   PubMed Web of Science ®Google Scholar
• Saijo T, Miyazaki T, Izumikawa K, et al. Skn7p is involved in oxidative stress response and virulence of Candida glabrata. Mycopathologia. 2010;169(2):81–90. DOI:10.1007/s11046-009-9233-5
   PubMed Web of Science ®Google Scholar
• Minematsu A, Miyazaki T, Shimamura S, et al. Vacuolar proton-translocating ATPase is required for antifungal resistance and virulence of Candida glabrata. PLoS One. 2019;14(1):e0210883. DOI:10.1371/journal.pone.0210883
   PubMed Web of Science ®Google Scholar
• Rai MN, Sharma V, Balusu S, et al. An essential role for phosphatidylinositol 3-kinase in the inhibition of phagosomal maturation, intracellular survival and virulence in Candida glabrata. Cell Microbiol. 2015;17(2):269–287.
   PubMed Web of Science ®Google Scholar
• Chen YL, Konieczka JH, and Springer DJ, et al. Convergent Evolution of calcineurin pathway roles in thermotolerance and virulence in Candida glabrata. G3 (Bethesda). 2012;2(6):675–691.
   PubMedGoogle Scholar
• Lebel K, MacPherson S, Turcotte B. New tools for phenotypic analysis in Candida albicans: the WAR1 gene confers resistance to sorbate. Yeast. 2006 Mar;23(4):249–259.
   PubMed Web of Science ®Google Scholar
• Vylkova S, Lorenz MC. Modulation of phagosomal pH by Candida albicans promotes hyphal morphogenesis and requires Stp2p, a regulator of amino acid transport. PLoS Pathog. 2014 Mar;10(3):e1003995.
   PubMed Web of Science ®Google Scholar
• Sprenger M, Brunke S, and Hube B, et al. A TRP1-marker-based system for gene complementation, overexpression, reporter gene expression and gene modification in Candida glabrata. FEMS Yeast Res. 2021 Jan 6;20(8). DOI:10.1093/femsyr/foaa066
   PubMed Web of Science ®Google Scholar
• Van Zeebroeck G, Rubio-Texeira M, Schothorst J, et al. Specific analogues uncouple transport, signalling, oligo-ubiquitination and endocytosis in the yeast Gap1 amino acid transceptor. Mol Microbiol. 2014;93(2):213–233.
   PubMed Web of Science ®Google Scholar
• Donaton MC, Holsbeeks I, Lagatie O, et al. The Gap1 general amino acid permease acts as an amino acid sensor for activation of protein kinase a targets in the yeast Saccharomyces cerevisiae. Mol Microbiol. 2003;50(3):911–929.
   PubMed Web of Science ®Google Scholar
• Van Zeebroeck G, Bonini BM, Versele M, et al. Transport and signaling via the amino acid binding site of the yeast Gap1 amino acid transceptor. Nat Chem Biol. 2009;5(1):45–52.
   PubMed Web of Science ®Google Scholar
• Lee YJ, Jang JW, Kim KJ, et al. TCA cycle-independent acetate metabolism via the glyoxylate cycle in Saccharomyces cerevisiae. Yeast. 2011;28(2):153–166. DOI:10.1002/yea.1828.
   PubMed Web of Science ®Google Scholar
• Chen Y, Siewers V, Nielsen J. Profiling of cytosolic and peroxisomal acetyl-CoA metabolism in Saccharomyces cerevisiae. PLoS One. 2012;7(8):e42475.
   PubMed Web of Science ®Google Scholar
• Nguyen TD, Walker ME, Gardner JM, et al. Appropriate vacuolar acidification in Saccharomyces cerevisiae is associated with efficient high sugar fermentation. Food Microbiol. 2018;70:262–268.
   PubMed Web of Science ®Google Scholar
• Outten CE, Falk RL, Culotta VC. Cellular factors required for protection from hyperoxia toxicity in Saccharomyces cerevisiae. Biochem J. 2005 May 15;388(Pt 1):93–101.
   PubMedGoogle Scholar
• Merz S, Westermann B. Genome-Wide deletion mutant analysis reveals genes required for respiratory growth, mitochondrial genome maintenance and mitochondrial protein synthesis in Saccharomyces cerevisiae. Genome Biol. 2009;10(9):R95.
   PubMed Web of Science ®Google Scholar
• Banerjee M, Thompson DS, Lazzell A, et al. UME6, a novel filament-specific regulator of Candida albicans hyphal extension and virulence. Mol Biol Cell. 2008;19(4):1354–1365.
   PubMed Web of Science ®Google Scholar
• Nagi M, Nakayama H, Tanabe K, et al. Transcription factors CgUPC2A and CgUPC2B regulate ergosterol biosynthetic genes in Candida glabrata. Genes Cells. 2011;16(1):80–89.
   PubMed Web of Science ®Google Scholar
• Van Ende M, Timmermans B, Vanreppelen G, et al. The involvement of the Candida glabrata trehalase enzymes in stress resistance and gut colonization. Virulence. 2021;12(1):329–345.
   PubMed Web of Science ®Google Scholar
• Geiss GK, Bumgarner RE, Birditt B, et al. Direct multiplexed measurement of gene expression with color-coded probe pairs. Nat Biotechnol. 2008;26(3):317–325.
   PubMed Web of Science ®Google Scholar
• Cheng S, Clancy CJ, Xu W, et al. Profiling of Candida albicans gene expression during intra-abdominal candidiasis identifies biologic processes involved in pathogenesis. J Infect Dis. 2013 Nov 1;208(9):1529–1537.
   PubMed Web of Science ®Google Scholar
• Xu W, Solis NV, Ehrlich RL, et al. Activation and alliance of regulatory pathways in C. albicans during mammalian infection. PLoS Biol. 2015;13(2):e1002076.
   PubMed Web of Science ®Google Scholar
• O’-Meara TR, Xu W, Selvig KM, et al. The Cryptococcus neoformans Rim101 transcription factor directly regulates genes required for adaptation to the host. Mol Cell Biol. 2014;34(4):673–684.
   PubMed Web of Science ®Google Scholar
• Fanning S, Xu W, Solis N, et al. Divergent targets of Candida albicans biofilm regulator Bcr1 in vitro and in vivo. Eukaryot Cell. 2012;11(7):896–904.
   PubMedGoogle Scholar
• Chung M, Teigen L, Liu H, et al. Targeted enrichment outperforms other enrichment techniques and enables more multi-species RNA-Seq analyses. Sci Rep. 2018 Sep 6;8(1):13377.
   PubMedGoogle Scholar
• Sanglard D, Ischer F, Calabrese D, et al. The ATP binding cassette transporter gene CgCDR1 from Candida glabrata is involved in the resistance of clinical isolates to azole antifungal agents. Antimicrob Agents Chemother. 1999;43(11):2753–2765.
   PubMed Web of Science ®Google Scholar
• Shor E, Garcia-Rubio R, DeGregorio L, et al. A noncanonical DNA damage checkpoint response in a major fungal pathogen. mBio. 2020 Dec 15;11(6). DOI:10.1128/mBio.03044-20
   PubMed Web of Science ®Google Scholar
• Shor E, Perlin DS. DNA damage response of major fungal pathogen Candida glabrata offers clues to explain its genetic diversity. Curr Genet. 2021 Jun;67(3):439–445.
   PubMed Web of Science ®Google Scholar
• Navarathna DH, Lionakis MS, Lizak MJ, et al. Urea amidolyase (DUR1,2) contributes to virulence and kidney pathogenesis of Candida albicans. PLoS One. 2012;7(10):e48475.
   PubMed Web of Science ®Google Scholar
• Brunke S, Quintin J, Kasper L, et al. Of mice, flies–and men? Comparing fungal infection models for large-scale screening efforts. Dis Model Mech. 2015;8(5):473–486.
   PubMed Web of Science ®Google Scholar
• Kraidlova L, Van Zeebroeck G, Van Dijck P, et al. The Candida albicans GAP gene family encodes permeases involved in general and specific amino acid uptake and sensing. Eukaryot Cell. 2011;10(9):1219–1229.
   PubMedGoogle Scholar
• Kraidlova L, Schrevens S, and Tournu H, et al. Characterization of the Candida albicans amino acid permease family: Gap2 is the only general amino acid permease and Gap4 is an S-Adenosylmethionine (SAM) transporter required for SAM-Induced Morphogenesis. mSphere. 2016;1(6). DOI:10.1128/mSphere.00284-1616
   PubMed Web of Science ®Google Scholar
• Zhang W, Du G, and Zhou J, et al. Regulation of Sensing, Transportation, and Catabolism of Nitrogen Sources in Saccharomyces cerevisiae. Microbiol Mol Biol Rev. 2018;82(1). DOI:10.1128/MMBR.00040-17
   PubMed Web of Science ®Google Scholar
• Brega E, Zufferey R, Mamoun CB. Candida albicans Csy1p is a nutrient sensor important for activation of amino acid uptake and hyphal morphogenesis. Eukaryot Cell. 2004 Feb;3(1):135–143.
   PubMedGoogle Scholar
• Schrevens S, Van Zeebroeck G, Riedelberger M, et al. Methionine is required for cAMP-PKA mediated morphogenesis and virulence of Candida albicans. Mol Microbiol. 2018;109(3):415–416.
   PubMed Web of Science ®Google Scholar
• Perez-Delos Santos FJ, Riego-Ruiz L. Gln3 is a main regulator of nitrogen assimilation in Candida glabrata. Microbiol (Reading). 2016 Aug;162(8):1490–1499.
   PubMed Web of Science ®Google Scholar
• Perez-de Los Santos FJ, Garcia-Ortega LF, Robledo-Marquez K, et al. Transcriptome Analysis Unveils Gln3 Role in Amino Acids Assimilation and Fluconazole Resistance in Candida glabrata. J Microbiol Biotechnol. 2021 May 28;31(5):659–666.
   PubMed Web of Science ®Google Scholar
• Lorenz MC, Fink GR. The glyoxylate cycle is required for fungal virulence. Nature. 2001 Jul 5; 412(6842):83–86. DOI:10.1038/35083594
   PubMed Web of Science ®Google Scholar
• Hill KJ, Stevens TH. Vma22p is a novel endoplasmic reticulum-associated protein required for assembly of the yeast vacuolar H(+)-ATPase complex. J Biol Chem. 1995 Sep 22;270(38):22329–22336.
   PubMed Web of Science ®Google Scholar
• Kane PM. The where, when, and how of organelle acidification by the yeast vacuolar H±ATPase. Microbiol Mol Biol Rev. 2006 Mar;70(1):177–191.
   PubMed Web of Science ®Google Scholar
• Dimmer KS, Fritz S, Fuchs F, et al. Genetic basis of mitochondrial function and morphology in Saccharomyces cerevisiae. Mol Biol Cell. 2002;13(3):847–853.
   PubMed Web of Science ®Google Scholar
• Serrano R, Bernal D, Simon E, et al. Copper and iron are the limiting factors for growth of the yeast Saccharomyces cerevisiae in an alkaline environment. J Biol Chem. 2004 May 7;279(19):19698–19704.
   PubMed Web of Science ®Google Scholar
• Schmidt M, Akasaka K, Messerly JT, et al. Role of Hog1, Tps1 and Sod1 in boric acid tolerance of Saccharomyces cerevisiae. Microbiol (Reading). 2012;158(Pt 10):2667–2678.
   PubMedGoogle Scholar
• Epp E, Vanier G, Harcus D, et al. Reverse genetics in Candida albicans predicts ARF cycling is essential for drug resistance and virulence. PLoS Pathog. 2010 Feb 5;6(2):e1000753.
   PubMed Web of Science ®Google Scholar
• Nishikawa H, Miyazaki T, and Nakayama H, et al. Roles of vacuolar H±ATPase in the oxidative stress response of Candida glabrata. FEMS Yeast Res. 2016;16(5). DOI:10.1093/femsyr/fow054
   PubMed Web of Science ®Google Scholar
• Gale AN, Sakhawala RM, and Levitan A, et al. Identification of essential genes and fluconazole susceptibility genes in Candida glabrata by profiling hermes transposon insertions. G3 (Bethesda). 2020 Oct 5; 10(10):3859–3870.
   PubMedGoogle Scholar
• Allert S, Schulz D, Kammer P, et al. From environmental adaptation to host survival: Attributes that mediate pathogenicity of Candida auris. Virulence. 2022;13(1):191–214.
   PubMed Web of Science ®Google Scholar
• Mahl CD, Behling CS, Hackenhaar FS, et al. Induction of ROS generation by fluconazole in Candida glabrata: activation of antioxidant enzymes and oxidative DNA damage. Diagn Microbiol Infect Dis. 2015;82(3):203–208.
   PubMed Web of Science ®Google Scholar