Convergent and divergent roles of the glucose-responsive kinase SNF4 in Candida tropicalis

References

• Brown GD, Denning DW, Gow NAR, et al. Hidden killers: human fungal infections. Sci Transl Med. 2012;4(165):165rv13.
   PubMed Web of Science ®Google Scholar
• Bertagnolio S, de Gaetano Donati K, Tacconelli E, et al. Hospital-acquired candidemia in HIV-infected patients. Incidence, risk factors and predictors of outcome. J Chemother. 2004;16(2):172–17. DOI:10.1179/joc.2004.16.2.172
   PubMed Web of Science ®Google Scholar
• Erdogan A, Lee YY, Sifuentes H, et al. Small intestinal fungal overgrowth (SIFO): a cause of gastrointestinal symptoms. Gastroenterology. 2014;146(5):S358.
   Web of Science ®Google Scholar
• Nucci M, Queiroz-Telles F, Tobón AM, et al. Epidemiology of opportunistic fungal infections in Latin America. Clin Infect Dis. 2010;51:561–570.
   PubMed Web of Science ®Google Scholar
• Pfaller MA, Diekema DJ. Epidemiology of invasive candidiasis: a persistent public health problem. Clin Microbiol Rev. 2007;20:133–163.
   PubMed Web of Science ®Google Scholar
• Silva S, Negri M, Henriques M, et al. Candida glabrata, Candida parapsilosis and Candida tropicalis: biology, epidemiology, pathogenicity and antifungal resistance. FEMS Microbiol Rev. 2012;36:288–305.
   PubMed Web of Science ®Google Scholar
• Falagas ME, Roussos N, Vardakas KZ. Relative frequency of albicans and the various non-albicans Candida spp among candidemia isolates from inpatients in various parts of the world: a systematic review. Int J Infect Dis. 2010;14:E954–966.
   PubMed Web of Science ®Google Scholar
• Guinea J. Global trends in the distribution of Candida species causing candidemia. Clin Microbiol Infect. 2014;20(Suppl 6):5–10.
   Web of Science ®Google Scholar
• Barchiesi F, Calabrese D, Sanglard D, et al. Experimental induction of fluconazole resistance in Candida tropicalis ATCC 750. Antimicrob Agents Chemother. 2000;44(6):1578–1584. DOI:10.1128/AAC.44.6.1578-1584.2000
   PubMed Web of Science ®Google Scholar
• Yang YL, Ho YA, Cheng HH, et al. Susceptibilities of Candida species to amphotericin B and fluconazole: the emergence of fluconazole resistance in Candida tropicalis. Infect Control Hosp Epidemiol. 2004;25:60–64.
   PubMed Web of Science ®Google Scholar
• Yang YL, Lin CC, Chang TP, et al. Comparison of human and soil Candida tropicalis isolates with reduced susceptibility to fluconazole. PLoS ONE. 2012;7:e34609.
   PubMed Web of Science ®Google Scholar
• Biswas S, Van Dijck P, Datta A. Environmental sensing and signal transduction pathways regulating morphopathogenic determinants of Candida albicans. Microbiol Mol Biol Rev. 2007;71(2):348–376.
   PubMed Web of Science ®Google Scholar
• Celenza JL, Carlson M. Mutational analysis of the Saccharomyces cerevisiae Snf1 protein kinase and evidence for functional interaction with the Snf4 protein. Mol Cell Biol. 1989;9(11):5034–5044.
   PubMed Web of Science ®Google Scholar
• Coccetti P, Nicastro R, Tripodi F. Conventional and emerging roles of the energy sensor SNF1/AMPK in Saccharomyces cerevisiae. Microb Cell. 2018;5(11):482–494.
   PubMed Web of Science ®Google Scholar
• Hedbacker K, Carlson M. SNF1/AMPK pathways in yeast. Front Biosci. 2008;13:2408–2420.
   PubMed Web of Science ®Google Scholar
• Celenza JL, Carlson M. A yeast gene that is essential for release from glucose repression encodes a protein kinase. Science. 1986;233(4769):1175–1180.
   PubMed Web of Science ®Google Scholar
• Weinhandl K, Winkler M, Glieder A, et al. Carbon source dependent promoters in yeasts. Microb Cell Fact. 2014;13:5.
   PubMed Web of Science ®Google Scholar
• Westholm JO, Nordberg N, Muren E, et al. Combinatorial control of gene expression by the three yeast repressors Mig1, Mig2 and Mig3. BMC Genomics. 2008;9:601.
   PubMed Web of Science ®Google Scholar
• DeVit MJ, Waddle JA, Johnston M. Regulated nuclear translocation of the Mig1 glucose repressor. Mol Biol Cell. 1997;8(8):1603–1618.
   PubMed Web of Science ®Google Scholar
• Sabina J, Brown V. Glucose sensing network in Candida albicans: a sweet spot for fungal morphogenesis. Eukaryot Cell. 2009;8:1314–1320.
   PubMedGoogle Scholar
• Lagree K, Woolford CA, Huang MNY, et al. Roles of Candida albicans Mig1 and Mig2 in glucose repression, pathogenicity traits, and SNF1 essentiality. PLoS Genet. 2020;16:e1008582.
   PubMed Web of Science ®Google Scholar
• Ramirez-Zavala B, Mottola A, Haubenreisser J, et al. The Snf1-activating kinase Sak1 is a key regulator of metabolic adaptation and in vivo fitness of Candida albicans. Mol Microbiol. 2017;104:989–1007.
   PubMed Web of Science ®Google Scholar
• Petter R, Chang YC, KwonChung KJ. A gene homologous to Saccharomyces cerevisiae SNF1 appears to be essential for the viability of Candida albicans. Infecti Immun. 1997;65:4909–4917.
   PubMed Web of Science ®Google Scholar
• Song YD, Hsu CC, Lew SQ, et al. Candida tropicalis RON1 is required for hyphal formation, biofilm development, and virulence but is dispensable for N-acetylglucosamine catabolism. Med Mycol. 2020;59:379–391.
   Web of Science ®Google Scholar
• Song YD, Hsu CC, Lew SQ, et al. Candida tropicalis RON1 is required for hyphal formation, biofilm development, and virulence but is dispensable for N-acetylglucosamine catabolism. Med Mycol. 2021;59:379–391.
   PubMed Web of Science ®Google Scholar
• Xie J, Du H, Guan G, et al. N-acetylglucosamine induces white-to-opaque switching and mating in Candida tropicalis, providing new insights into adaptation and fungal sexual evolution. Eukaryot Cell. 2012;11:773–782.
   PubMedGoogle Scholar
• Zhang Q, Tao L, Guan G, et al. Regulation of filamentation in the human fungal pathogen Candida tropicalis. Mol Microbiol. 2016b;99:528–545.
   PubMed Web of Science ®Google Scholar
• Brown DH Jr., Giusani AD, Chen X, et al. Filamentous growth of Candida albicans in response to physical environmental cues and its regulation by the unique CZF1 gene. Mol Microbiol. 1999;34(4):651–662.
   PubMed Web of Science ®Google Scholar
• Nobile CJ, Mitchell AP. Regulation of cell-surface genes and biofilm formation by the C. albicans transcription factor Bcr1p. Curr Biol. 2005;15:1150–1155.
   PubMed Web of Science ®Google Scholar
• Nobile CJ, Nett JE, Hernday AD, et al. Biofilm matrix regulation by Candida albicans Zap1. PLoS Biol. 2009;7:e1000133.
   PubMed Web of Science ®Google Scholar
• Vinces MD, Haas C, Kumamoto CA. Expression of the Candida albicans morphogenesis regulator gene CZF1 and its regulation by Efg1p and Czf1p. Eukaryot Cell. 2006;5:825–835.
   PubMedGoogle Scholar
• Liang SH, Cheng JH, Deng FS, et al. A novel function for Hog1 stress-activated protein kinase in controlling white-opaque switching and mating in Candida albicans. Eukaryot Cell. 2014;12:1557–1566.
   Google Scholar
• Butler G, Rasmussen MD, Lin MF, et al. Evolution of pathogenicity and sexual reproduction in eight Candida genomes. Nature. 2009;459(7247):657–662. DOI:10.1038/nature08064
   PubMed Web of Science ®Google Scholar
• Mancera E, Frazer C, Porman AM, et al. Genetic modification of closely related Candida species. Front Microbiol. 2019;10:357.
   PubMed Web of Science ®Google Scholar
• Smith DL, McClure JM, Matecic M, et al. Calorie restriction extends the chronological lifespan of Saccharomyces cerevisiae independently of the Sirtuins. Aging Cell. 2007;6:649–662.
   PubMed Web of Science ®Google Scholar
• Wierman MB, Maqani N, Strickler E, et al. Caloric restriction extends yeast chronological life span by optimizing the Snf1 (AMPK) signaling pathway. Mol Cell Biol. 2017;37:e00562–16. DOI:10.1128/MCB.00562-16.
   PubMed Web of Science ®Google Scholar
• Hageage GJ, Harrington BJ. Use of calcofluor white in clinical mycology. Lab Med. 1984;15:109–112.
   Google Scholar
• Francois JM. A simple method for quantitative determination of polysaccharides in fungal cell walls. Nat Protoc. 2006;1:2995–3000.
   PubMed Web of Science ®Google Scholar
• Yeh YC, Wang HY, Lan CY. Candida albicans Aro1 affects cell wall integrity, biofilm formation and virulence. J Microbiol Immun Infect. 2020;53:115–124.
   Web of Science ®Google Scholar
• Lin CH, Kabrawala S, Fox EP, et al. Genetic control of conventional and pheromone-stimulated biofilm formation in Candida albicans. PLOS Pathog. 2013;9:e1003305.
   PubMed Web of Science ®Google Scholar
• Tseng YK, Chen YC, Hou CJ, et al. Evaluation of biofilm formation in Candida tropicalis using a silicone-based platform with synthetic urine medium. Microorganisms. 2020;8:660.
   PubMed Web of Science ®Google Scholar
• Jacobsen ID. Galleria mellonella as a model host to study virulence of Candida. Virulence. 2014;5:237–239.
   PubMed Web of Science ®Google Scholar
• Vilela SFG, Barbosa JO, Rossoni RDet al, Lactobacillus acidophilus ATCC 4356 inhibits biofilm formation by C. albicans and attenuates the experimental candidiasis in Galleria mellonella. Virulence. 2015;6:29–39.
   PubMed Web of Science ®Google Scholar
• Conti HR, Huppler AR, Whibley N, et al. Animal models for candidiasis. Curr Protoc Immunol. 2014;105(1):.19.16.11–19.16.17.
   Google Scholar
• Wilson WA, Hawley SA, Hardie DG. Glucose repression/derepression in budding yeast: sNF1 protein kinase is activated by phosphorylation under derepressing conditions, and this correlates with a high AMP: aTP ratio. Curr Biol. 1996;6:1426–1434.
   PubMed Web of Science ®Google Scholar
• Greer EL, Dowlatshahi D, Banko MR, et al. An AMPK-FOXO pathway mediates longevity induced by a novel method of dietary restriction in C. elegans. Curr Biol. 2007;17:1646–1656.
   PubMed Web of Science ®Google Scholar
• Slack C, Foley A, Partridge L. Activation of AMPK by the putative dietary restriction mimetic metformin is insufficient to extend lifespan in Drosophila. PLoS ONE. 2012;7:e47699.
   PubMed Web of Science ®Google Scholar
• Stancu AL. AMPK activation can delay aging. Discoveries (Craiova). 2015;3:e53.
   PubMedGoogle Scholar
• Francois J, Parrou JL. Reserve carbohydrates metabolism in the yeast Saccharomyces cerevisiae. FEMS Microbiol Rev. 2001;25:125–145.
   PubMed Web of Science ®Google Scholar
• Ram AF, Wolters A, Ten Hoopen R, et al. A new approach for isolating cell wall mutants in Saccharomyces cerevisiae by screening for hypersensitivity to calcofluor white. Yeast. 1994;10:1019–1030.
   PubMed Web of Science ®Google Scholar
• Roncero C, Duran A. Effect of calcofluor white and congo red on fungal cell wall morphogenesis: in vivo activation of chitin polymerization. J Bacteriol. 1985;163:1180–1185.
   PubMed Web of Science ®Google Scholar
• Brown HE, Esher SK, Alspaugh JA. Chitin: a “hidden figure” in the fungal cell wall. Curr Top Microbiol Immunol. 2020;425:83–111.
   PubMed Web of Science ®Google Scholar
• Durán A, Nombela C. Fungal cell wall biogenesis: building a dynamic interface with the environment. Microbiology. 2004;150(10):3099–3103.
   PubMedGoogle Scholar
• Garcia-Rubio R, de Oliveira HC, Rivera J, et al. The fungal cell wall: Candida, Cryptococcus, and Aspergillus species. Front Microbiol. 2020;10:2993.
   PubMed Web of Science ®Google Scholar
• Hall RA, Gow NA. Mannosylation in Candida albicans: role in cell wall function and immune recognition. Mol Microbiol. 2013;90:1147–1161.
   PubMed Web of Science ®Google Scholar
• Paul S, Singh S, Chakrabarti A, et al. Selection and evaluation of appropriate reference genes for RT-qPCR based expression analysis in Candida tropicalis following azole treatment. Sci Rep. 2020;10:1972.
   PubMed Web of Science ®Google Scholar
• Hobson RP, Munro CA, Bates S, et al. Loss of cell wall mannosylphosphate in Candida albicans does not influence macrophage recognition. J Biol Chem. 2004;279:39628–39635.
   PubMed Web of Science ®Google Scholar
• Bates S, Hughes HB, Munro CA, et al. Outer chain N‐glycans are required for cell wall integrity and virulence of Candida albicans. J Biol Chem. 2006;281(1):90–98. DOI:10.1074/jbc.M510360200
   PubMed Web of Science ®Google Scholar
• Peltroche‐llacsahuanga H, Goyard S, D′enfert C, et al. Protein O‐mannosyltransferase isoforms regulate biofilm formation in Candida albicans. Antimicrob Agents Chemother. 2006;50:3488–3491.
   PubMed Web of Science ®Google Scholar
• Prill SKH, Klinkert B, Timpel C, et al. PMT family of Candida albicans: five protein mannosyltransferase isoforms affect growth, morphogenesis and antifungal resistance. Mol Microbiol. 2005;55:546–560.
   PubMed Web of Science ®Google Scholar
• Rouabhia M, Schaller M, Corbucci C, et al. Virulence of the fungal pathogen Candida albicans requires the five isoforms of protein mannosyltransferases. Infect Immun. 2005;73:4571–4580.
   PubMed Web of Science ®Google Scholar
• Carlisle PL, Banerjee M, Lazzell A, et al. Expression levels of a filament-specific transcriptional regulator are sufficient to determine Candida albicans morphology and virulence. Proc Natl Acad Sci U S A. 2009;106(2):599–604.
   PubMed Web of Science ®Google Scholar
• Simpson-Lavy K, Kupiec M. A reversible liquid drop aggregation controls glucose response in yeast. Curr Genet. 2018;64:785–788.
   PubMed Web of Science ®Google Scholar
• Braun BR, Johnson AD. TUP1, CPH1 and EFG1 make independent contributions to filamentation in Candida albicans. Genetics. 2000;155(1):57–67.
   PubMed Web of Science ®Google Scholar
• Kadosh D, Johnson AD. Induction of the Candida albicans filamentous growth program by relief of transcriptional repression: a genome-wide analysis. Mol Biol Cell. 2005;16:2903–2912.
   PubMed Web of Science ®Google Scholar
• Leberer E, Harcus D, Broadbent ID, et al. Signal transduction through homologs of the Ste20p and Ste7p protein kinases can trigger hyphal formation in the pathogenic fungus Candida albicans. Proc Natl Acad Sci U S A. 1996;93:13217–13222.
   PubMed Web of Science ®Google Scholar
• Lo HJ, Kohler JR, DiDomenico B, et al. Nonfilamentous C. albicans mutants are avirulent. Cell. 1997;90:939–949.
   PubMed Web of Science ®Google Scholar
• Nantel A, Dignard D, Bachewich C, et al. Transcription profiling of Candida albicans cells undergoing the yeast-to-hyphal transition. Mol Biol Cell. 2002;13:3452–3465.
   PubMed Web of Science ®Google Scholar
• Stoldt VR, Sonneborn A, Leuker CE, et al. 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. 1997;16:1982–1991.
   PubMed Web of Science ®Google Scholar
• Buffo J, Herman MA, Soll DR. A characterization of pH-regulated dimorphism in Candida albicans. Mycopathologia. 1984;85(1–2):21–30.
   PubMed Web of Science ®Google Scholar
• Mardon D, Balish E, Phillips AW. Control of dimorphism in a biochemical variant of Candida albicans. J Bacteriol. 1969;100:701–707.
   PubMed Web of Science ®Google Scholar
• Simonetti N, Strippoli V, Cassone A. Yeast-mycelial conversion induced by N-acetyl-D-glucosamine in Candida albicans. Nature. 1974;250:344–346.
   PubMed Web of Science ®Google Scholar
• Taschdjian CL, Burchall JJ, Kozinn PJ. Rapid identification of Candida albicans by filamentation on serum and serum substitutes. Am J Dis Child. 1960;99:212–215.
   PubMedGoogle Scholar
• Jiang C, Li Z, Zhang L, et al. Significance of hyphae formation in virulence of Candida tropicalis and transcriptomic analysis of hyphal cells. Microbiol Res. 2016;192:65–72.
   PubMed Web of Science ®Google Scholar
• Zhang QY, Tao L, Guan GB, et al. Regulation of filamentation in the human fungal pathogen Candida tropicalis. Mol Microbiol. 2016c;99:528–545.
   PubMed Web of Science ®Google Scholar
• Karunanithi S, Cullen PJ. The filamentous growth MAPK pathway responds to glucose starvation through the Mig1/2 transcriptional repressors in Saccharomyces cerevisiae. Genetics. 2012;192:869–887.
   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. DOI:10.1091/mbc.e07-11-1110
   PubMed Web of Science ®Google Scholar
• Braun BR, Kadosh D, Johnson AD. NRG1, a repressor of filamentous growth in C. albicans, is down-regulated during filament induction. Embo J. 2001;20(17):4753–4761.
   PubMed Web of Science ®Google Scholar
• Childers DS, Kadosh D. Filament condition-specific response elements control the expression of NRG1 and UME6, key transcriptional regulators of morphology and virulence in Candida albicans. PLoS ONE. 2015;10(3):e0122775.
   PubMed Web of Science ®Google Scholar
• Garcia-Sanchez S, Mavor AL, Russell CL, et al. Global roles of Ssn6 in Tup1- and Nrg1-dependent gene regulation in the fungal pathogen, Candida albicans. Mol Biol Cell. 2005;16:2913–2925.
   PubMed Web of Science ®Google Scholar
• Lackey E, Vipulanandan G, Childers DS, et al. Comparative evolution of morphological regulatory functions in Candida species. Eukaryotic Cell. 2013;12:1356–1368.
   PubMedGoogle Scholar
• Zeidler U, Lettner T, Lassnig C, et al. UME6 is a crucial downstream target of other transcriptional regulators of true hyphal development in Candida albicans. FEMS Yeast Res. 2009;9:126–142.
   PubMed Web of Science ®Google Scholar
• Chen H, Zhou XD, Ren B, et al. The regulation of hyphae growth in Candida albicans. Virulence. 2020;11(1):337–348.
   PubMed Web of Science ®Google Scholar
• Hoyer LL, Clevenger J, Hecht JE, et al. Detection of Als proteins on the cell wall of Candida albicans in murine tissues. Infect Immun. 1999;67:4251–4255.
   PubMed Web of Science ®Google Scholar
• Lipke PN, Ovalle R. Cell wall architecture in yeast: new structure and new challenges. J Bacteriol. 1998;180:3735–3740.
   PubMed Web of Science ®Google Scholar
• Plaine A, Walker L, Da Costa G, et al. Functional analysis of Candida albicans GPI-anchored proteins: roles in cell wall integrity and caspofungin sensitivity. Fungal Genet Biol. 2008;45:1404–1414.
   PubMed Web of Science ®Google Scholar
• Chaffin WL. Candida albicans cell wall proteins. Microbiol Mol Biol Rev. 2008;72(3):495–544.
   PubMed Web of Science ®Google Scholar
• Hasim S, Coleman JJ. Targeting the fungal cell wall: current therapies and implications for development of alternative antifungal agents. Future Med Chem. 2019;11:869–883.
   PubMed Web of Science ®Google Scholar
• Lenardon MD, Munro CA, Gow NA. Chitin synthesis and fungal pathogenesis. Curr Opin Microbiol. 2010;13:416–423.
   PubMed Web of Science ®Google Scholar
• Backhaus K, Rippert D, Heilmann CJ, et al. Mutations in SNF1 complex genes affect yeast cell wall strength. Eur J Cell Biol. 2013;92(12):383–395. DOI:10.1016/j.ejcb.2014.01.001
   PubMed Web of Science ®Google Scholar
• Zhang P, Zhao Q, Wei D, et al. Snf1/AMPK affects cell wall integrity through regulating the transcription of cell wall assembly-related genesin Saccharomyces cerevisiae. Wei Sheng Wu Xue Bao. 2016a;56:1132–1140.
   PubMedGoogle Scholar
• Goyard S, Knechtle P, Chauvel M, et al. The Yak1 kinase is involved in the initiation and maintenance of hyphal growth in Candida albicans. Mol Biol Cell. 2008;19:2251–2266.
   PubMed Web of Science ®Google Scholar
• Khan FM, Ueno-Yamanouchi A, Serushago B, et al. Basophil activation test compared to skin prick test and fluorescence enzyme immunoassay for aeroallergen-specific immunoglobulin-E. Allergy, Asthma Clin Immunol. 2012;8:1.
   PubMed Web of Science ®Google Scholar
• Singh RP, Prasad HK, Sinha I, et al. Cap2-HAP complex is a critical transcriptional regulator that has dual but contrasting roles in regulation of iron homeostasis in Candida albicans. J Biol Chem. 2011;286:25154–25170.
   PubMed Web of Science ®Google Scholar
• Hedges D, Proft M, Entian KD. CAT8, a new zinc cluster-encoding gene necessary for derepression of gluconeogenic enzymes in the yeast Saccharomyces cerevisiae. Mol Cell Biol. 1995;15:1915–1922.
   PubMed Web of Science ®Google Scholar
• Lesage P, Yang X, Carlson M. Yeast SNF1 protein kinase interacts with SIP4, a C6 zinc cluster transcriptional activator: a new role for SNF1 in the glucose response. Mol Cell Biol. 1996;16:1921–1928.
   PubMed Web of Science ®Google Scholar
• Desai JV, Mitchell AP. Candida albicans biofilm development and its genetic control. Microbiol Spectr. 2015;3(3). DOI:10.1128/microbiolspec
   PubMedGoogle Scholar
• Finkel JS, Mitchell AP. Genetic control of Candida albicans biofilm development. Nat Rev Microbiol. 2011;9:109–118.
   PubMed Web of Science ®Google Scholar
• Sudbery PE. Growth of Candida albicans hyphae. Nat Rev Microbiol. 2011;9:737–748.
   PubMed Web of Science ®Google Scholar
• Bojang E, Ghuman H, Kumwenda P, et al. Immune sensing of Candida albicans. J Fungi (Basel). 2021;7(2):119.
   PubMedGoogle Scholar
• Halder LD, Jo EAH, Hasan MZ, et al. Immune modulation by complement receptor 3-dependent human monocyte TGF-beta1-transporting vesicles. Nat Commun. 2020;11:2331.
   PubMed Web of Science ®Google Scholar
• Netea MG, Gow NA, Munro CA, et al. Immune sensing of Candida albicans requires cooperative recognition of mannans and glucans by lectin and toll-like receptors. J Clin Invest. 2006;116:1642–1650.
   PubMed Web of Science ®Google Scholar
• Thompson DS, Carlisle PL, Kadosh D. Coevolution of morphology and virulence in Candida species. Eukaryot Cell. 2011;10:1173–1182.
   PubMedGoogle Scholar