{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,17]],"date-time":"2026-08-17T22:31:25Z","timestamp":1787005885501,"version":"build-2736575974"},"reference-count":46,"publisher":"Elsevier BV","issue":"35","license":[{"start":{"date-parts":[[2019,8,1]],"date-time":"2019-08-01T00:00:00Z","timestamp":1564617600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"},{"start":{"date-parts":[[2020,8,31]],"date-time":"2020-08-31T00:00:00Z","timestamp":1598832000000},"content-version":"vor","delay-in-days":396,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100003329","name":"Ministerio de Econom\u00eda y Competitividad (MEC)","doi-asserted-by":"publisher","award":["BFU2016\u201375792-R"],"award-info":[{"award-number":["BFU2016\u201375792-R"]}],"id":[{"id":"10.13039\/501100003329","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["jbc.org","elsevier.com","sciencedirect.com"],"crossmark-restriction":true},"short-container-title":["Journal of Biological Chemistry"],"published-print":{"date-parts":[[2019,8]]},"DOI":"10.1074\/jbc.ra119.009291","type":"journal-article","created":{"date-parts":[[2019,7,11]],"date-time":"2019-07-11T14:45:10Z","timestamp":1562856310000},"page":"12933-12946","update-policy":"https:\/\/doi.org\/10.1016\/elsevier_cm_policy","source":"Crossref","is-referenced-by-count":17,"title":["Live-cell assays reveal selectivity and sensitivity of the multidrug response in budding yeast"],"prefix":"10.1016","volume":"294","author":[{"given":"Elena","family":"Vanacloig-Pedros","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Carlos","family":"Lozano-P\u00e9rez","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Benito","family":"Alarc\u00f3n","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Amparo","family":"Pascual-Ahuir","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6788-5830","authenticated-orcid":false,"given":"Markus","family":"Proft","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"78","reference":[{"key":"10.1074\/jbc.RA119.009291_bib1","doi-asserted-by":"crossref","first-page":"119","DOI":"10.2174\/156802609787521553","article-title":"ABC pumps and their role in active drug transport","volume":"9","author":"Colabufo","year":"2009","journal-title":"Curr. Top. Med. Chem"},{"key":"10.1074\/jbc.RA119.009291_bib2","doi-asserted-by":"crossref","first-page":"725","DOI":"10.1016\/j.bbapap.2008.12.004","article-title":"Molecular basis of multidrug transport by ABC transporters","volume":"1794","author":"Seeger","year":"2009","journal-title":"Biochim. Biophys. Acta"},{"key":"10.1074\/jbc.RA119.009291_bib3","doi-asserted-by":"crossref","first-page":"592","DOI":"10.1134\/S0006297908050118","article-title":"Transport proteins of the ABC family and multidrug resistance of tumor cells","volume":"73","author":"Stavrovskaya","year":"2008","journal-title":"Biochemistry (Mosc)"},{"key":"10.1074\/jbc.RA119.009291_bib4","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1146\/annurev-micro-092611-150111","article-title":"Yeast ATP-binding cassette transporters conferring multidrug resistance","volume":"66","author":"Prasad","year":"2012","journal-title":"Annu. Rev. Microbiol"},{"key":"10.1074\/jbc.RA119.009291_bib5","doi-asserted-by":"crossref","first-page":"63","DOI":"10.1104\/pp.106.084533","article-title":"A gain-of-function mutation in the Arabidopsis pleiotropic drug resistance transporter PDR9 confers resistance to auxinic herbicides","volume":"142","author":"Ito","year":"2006","journal-title":"Plant Physiol"},{"key":"10.1074\/jbc.RA119.009291_bib6","doi-asserted-by":"crossref","first-page":"1131","DOI":"10.1016\/j.febslet.2005.12.050","article-title":"Yeast ABC transporters\u2014a tale of sex, stress, drugs and aging","volume":"580","author":"Jungwirth","year":"2006","journal-title":"FEBS Lett"},{"key":"10.1074\/jbc.RA119.009291_bib7","doi-asserted-by":"crossref","first-page":"143","DOI":"10.3389\/fphys.2014.00143","article-title":"Multidrug resistance in fungi: Regulation of transporter-encoding gene expression","volume":"5","author":"Paul","year":"2014","journal-title":"Front. Physiol"},{"key":"10.1074\/jbc.RA119.009291_bib8","doi-asserted-by":"crossref","first-page":"195","DOI":"10.1002\/yea.3354","article-title":"Unveiling the transcriptional control of pleiotropic drug resistance in Saccharomyces cerevisiae: Contributions of Andr\u00e9 Goffeau and his group","volume":"36","author":"Balzi","year":"2018","journal-title":"Yeast"},{"key":"10.1074\/jbc.RA119.009291_bib9","doi-asserted-by":"crossref","first-page":"291","DOI":"10.1128\/CMR.00051-08","article-title":"Efflux-mediated antifungal drug resistance","volume":"22","author":"Cannon","year":"2009","journal-title":"Clin. Microbiol. Rev"},{"key":"10.1074\/jbc.RA119.009291_bib10","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1007\/s00294-018-0870-4","article-title":"Multiple interfaces control activity of the Candida glabrata Pdr1 transcription factor mediating azole drug resistance","volume":"65","author":"Moye-Rowley","year":"2019","journal-title":"Curr. Genet"},{"key":"10.1074\/jbc.RA119.009291_bib11","doi-asserted-by":"crossref","first-page":"173","DOI":"10.1016\/j.mycmed.2012.04.004","article-title":"The cellular and molecular defense mechanisms of the Candida yeasts against azole antifungal drugs","volume":"22","author":"No\u00ebl","year":"2012","journal-title":"J. Mycol. M\u00e9d"},{"key":"10.1074\/jbc.RA119.009291_bib12","doi-asserted-by":"crossref","first-page":"419","DOI":"10.1101\/gad.1743009","article-title":"Nuclear receptor-like transcription factors in fungi","volume":"23","author":"N\u00e4\u00e4r","year":"2009","journal-title":"Genes Dev"},{"key":"10.1074\/jbc.RA119.009291_bib13","doi-asserted-by":"crossref","first-page":"5063","DOI":"10.1074\/jbc.M610197200","article-title":"The central role of PDR1 in the foundation of yeast drug resistance","volume":"282","author":"Fardeau","year":"2007","journal-title":"J. Biol. Chem"},{"key":"10.1074\/jbc.RA119.009291_bib14","first-page":"4653","article-title":"Transcriptional control of the yeast PDR5 gene by the PDR3 gene product","volume":"14","author":"Katzmann","year":"1994","journal-title":"Mol. Cell. Biol"},{"key":"10.1074\/jbc.RA119.009291_bib15","doi-asserted-by":"crossref","first-page":"52641","DOI":"10.1074\/jbc.M309580200","article-title":"Competitive promoter occupancy by two yeast paralogous transcription factors controlling the multidrug resistance phenomenon","volume":"278","author":"Lucau-Danila","year":"2003","journal-title":"J. Biol. Chem"},{"key":"10.1074\/jbc.RA119.009291_bib16","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1016\/j.gene.2004.02.003","article-title":"Analysis of gene network regulating yeast multidrug resistance by artificial activation of transcription factors: Involvement of Pdr3 in salt tolerance","volume":"332","author":"Onda","year":"2004","journal-title":"Gene"},{"key":"10.1074\/jbc.RA119.009291_bib17","doi-asserted-by":"crossref","first-page":"27855","DOI":"10.1074\/jbc.M403487200","article-title":"Complex interplay among regulators of drug resistance genes in Saccharomyces cerevisiae","volume":"279","author":"Akache","year":"2004","journal-title":"J. Biol. Chem"},{"key":"10.1074\/jbc.RA119.009291_bib18","doi-asserted-by":"crossref","first-page":"1307","DOI":"10.1046\/j.1365-2958.1998.01027.x","article-title":"Yeast gene YRR1, which is required for resistance to 4-nitroquinoline N-oxide, mediates transcriptional activation of the multidrug resistance transporter gene SNQ2","volume":"29","author":"Cui","year":"1998","journal-title":"Mol. Microbiol"},{"key":"10.1074\/jbc.RA119.009291_bib19","doi-asserted-by":"crossref","first-page":"11427","DOI":"10.1074\/jbc.M208549200","article-title":"A general strategy to uncover transcription factor properties identifies a new regulator of drug resistance in yeast","volume":"278","author":"Hikkel","year":"2003","journal-title":"J. Biol. Chem"},{"key":"10.1074\/jbc.RA119.009291_bib20","doi-asserted-by":"crossref","first-page":"2642","DOI":"10.1128\/MCB.22.8.2642-2649.2002","article-title":"New insights into the pleiotropic drug resistance network from genome-wide characterization of the YRR1 transcription factor regulation system","volume":"22","author":"Le Crom","year":"2002","journal-title":"Mol. Cell. Biol"},{"key":"10.1074\/jbc.RA119.009291_bib21","doi-asserted-by":"crossref","first-page":"8812","DOI":"10.1074\/jbc.M010686200","article-title":"Cross-talk between transcriptional regulators of multidrug resistance in Saccharomyces cerevisiae","volume":"276","author":"Zhang","year":"2001","journal-title":"J. Biol. Chem"},{"key":"10.1074\/jbc.RA119.009291_bib22","doi-asserted-by":"crossref","first-page":"604","DOI":"10.1038\/nature06836","article-title":"A nuclear receptor-like pathway regulating multidrug resistance in fungi","volume":"452","author":"Thakur","year":"2008","journal-title":"Nature"},{"key":"10.1074\/jbc.RA119.009291_bib23","doi-asserted-by":"crossref","first-page":"42677","DOI":"10.1074\/jbc.M406363200","article-title":"On the mechanism of constitutive Pdr1 activator-mediated PDR5 transcription in Saccharomyces cerevisiae: Evidence for enhanced recruitment of coactivators and altered nucleosome structures","volume":"279","author":"Gao","year":"2004","journal-title":"J. Biol. Chem"},{"key":"10.1074\/jbc.RA119.009291_bib24","doi-asserted-by":"crossref","first-page":"2469","DOI":"10.1091\/mbc.e09-10-0899","article-title":"Differential roles of transcriptional Mediator subunits in regulation of multidrug resistance gene expression in Saccharomyces cerevisiae","volume":"21","author":"Shahi","year":"2010","journal-title":"Mol. Biol. Cell"},{"key":"10.1074\/jbc.RA119.009291_bib25","doi-asserted-by":"crossref","first-page":"485","DOI":"10.1038\/nature16963","article-title":"Inhibiting fungal multidrug resistance by disrupting an activator-Mediator interaction","volume":"530","author":"Nishikawa","year":"2016","journal-title":"Nature"},{"key":"10.1074\/jbc.RA119.009291_bib26","doi-asserted-by":"crossref","first-page":"414","DOI":"10.1111\/j.1567-1364.2007.00352.x","article-title":"RPD3 and ROM2 are required for multidrug resistance in Saccharomyces cerevisiae","volume":"8","author":"Borecka-Melkusova","year":"2008","journal-title":"FEMS Yeast Res"},{"key":"10.1074\/jbc.RA119.009291_bib27","doi-asserted-by":"crossref","first-page":"e84092","DOI":"10.1371\/journal.pone.0084092","article-title":"A role for FACT in repopulation of nucleosomes at inducible genes","volume":"9","author":"Voth","year":"2014","journal-title":"PLoS One"},{"key":"10.1074\/jbc.RA119.009291_bib28","doi-asserted-by":"crossref","first-page":"219","DOI":"10.1002\/yea.2905","article-title":"The use of a real-time luciferase assay to quantify gene expression dynamics in the living yeast cell","volume":"29","author":"Rienzo","year":"2012","journal-title":"Yeast"},{"key":"10.1074\/jbc.RA119.009291_bib29","doi-asserted-by":"crossref","first-page":"2228","DOI":"10.1128\/MCB.00240-13","article-title":"Deciphering dynamic dose responses of natural promoters and single cis elements upon osmotic and oxidative stress in yeast","volume":"33","author":"Dolz-Edo","year":"2013","journal-title":"Mol. Cell. Biol"},{"key":"10.1074\/jbc.RA119.009291_bib30","doi-asserted-by":"crossref","first-page":"3669","DOI":"10.1128\/MCB.00729-15","article-title":"Different mechanisms confer gradual control and memory at nutrient- and stress-regulated genes in yeast","volume":"35","author":"Rienzo","year":"2015","journal-title":"Mol. Cell. Biol"},{"key":"10.1074\/jbc.RA119.009291_bib31","doi-asserted-by":"crossref","first-page":"E273","DOI":"10.3390\/toxins8100273","article-title":"Different toxicity mechanisms for citrinin and ochratoxin A revealed by transcriptomic analysis in yeast","volume":"8","author":"Vanacloig-Pedros","year":"2016","journal-title":"Toxins (Basel)"},{"key":"10.1074\/jbc.RA119.009291_bib32","doi-asserted-by":"crossref","first-page":"e00995","DOI":"10.1128\/AAC.00995-18","article-title":"A transcriptomics approach to unveiling the mechanisms of in vitro evolution toward fluconazole resistance of a Candida glabrata clinical isolate","volume":"63","author":"Cavalheiro","year":"2019","journal-title":"Antimicrob. Agents Chemother"},{"key":"10.1074\/jbc.RA119.009291_bib33","doi-asserted-by":"crossref","first-page":"E105","DOI":"10.3390\/jof4030105","article-title":"Fungal resistance to echinocandins and the MDR phenomenon in Candida glabrata","volume":"4","author":"Healey","year":"2018","journal-title":"J. Fungi (Basel)"},{"key":"10.1074\/jbc.RA119.009291_bib34","doi-asserted-by":"crossref","first-page":"153","DOI":"10.1007\/s00294-014-0463-9","article-title":"Activation of the mitochondrial signaling pathway in response to organic solvent stress in yeast","volume":"61","author":"Nishida-Aoki","year":"2015","journal-title":"Curr. Genet"},{"key":"10.1074\/jbc.RA119.009291_bib35","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1007\/s00294-002-0274-2","article-title":"PDR2 Gain-of-function mutations eliminate the need for Pdr1 and require the UBP6 product for resistance to translational inhibitors","volume":"41","author":"Keeven","year":"2002","journal-title":"Curr. Genet"},{"key":"10.1074\/jbc.RA119.009291_bib36","doi-asserted-by":"crossref","first-page":"42","DOI":"10.1016\/j.bbrc.2013.03.069","article-title":"Salicylic acid resistance is conferred by a novel YRR1 mutation in Saccharomyces cerevisiae","volume":"434","author":"Kodo","year":"2013","journal-title":"Biochem. Biophys. Res. Commun"},{"key":"10.1074\/jbc.RA119.009291_bib37","doi-asserted-by":"crossref","first-page":"607","DOI":"10.1534\/g3.117.300138","article-title":"Transcriptional profiling of Saccharomyces cerevisiae reveals the impact of variation of a single transcription factor on differential gene expression in 4NQO, fermentable, and nonfermentable carbon sources","volume":"8","author":"Rong-Mullins","year":"2018","journal-title":"G3 (Bethesda)"},{"key":"10.1074\/jbc.RA119.009291_bib38","doi-asserted-by":"crossref","first-page":"1211","DOI":"10.1093\/nar\/gky1188","article-title":"Activation of Haa1 and War1 transcription factors by differential binding of weak acid anions in Saccharomyces cerevisiae","volume":"47","author":"Kim","year":"2018","journal-title":"Nucleic Acids Res"},{"key":"10.1074\/jbc.RA119.009291_bib39","doi-asserted-by":"crossref","first-page":"1775","DOI":"10.1128\/MCB.23.5.1775-1785.2003","article-title":"War1p, a novel transcription factor controlling weak acid stress response in yeast","volume":"23","author":"Kren","year":"2003","journal-title":"Mol. Cell. Biol"},{"key":"10.1074\/jbc.RA119.009291_bib40","doi-asserted-by":"crossref","first-page":"6690","DOI":"10.1128\/MCB.02450-05","article-title":"Oxidative stress-activated zinc cluster protein Stb5 has dual activator\/repressor functions required for pentose phosphate pathway regulation and NADPH production","volume":"26","author":"Larochelle","year":"2006","journal-title":"Mol. Cell. Biol"},{"key":"10.1074\/jbc.RA119.009291_bib41","doi-asserted-by":"crossref","first-page":"819","DOI":"10.1111\/j.1567-1364.2010.00672.x","article-title":"The Saccharomyces cerevisiae zinc factor protein Stb5p is required as a basal regulator of the pentose phosphate pathway","volume":"10","author":"Cadi\u00e8re","year":"2010","journal-title":"FEMS Yeast Res"},{"key":"10.1074\/jbc.RA119.009291_bib42","doi-asserted-by":"crossref","first-page":"foy091","DOI":"10.1093\/femsyr\/foy091","article-title":"Integrated analysis of the yeast NADPH-regulator Stb5 reveals distinct differences in NADPH requirements and regulation in different states of yeast metabolism","volume":"18","author":"Ouyang","year":"2018","journal-title":"FEMS Yeast Res"},{"key":"10.1074\/jbc.RA119.009291_bib43","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1016\/S0378-1119(00)00083-4","article-title":"A novel multi-purpose cassette for repeated integrative epitope tagging of genes in Saccharomyces cerevisiae","volume":"246","author":"De Antoni","year":"2000","journal-title":"Gene"},{"key":"10.1074\/jbc.RA119.009291_bib44","doi-asserted-by":"crossref","first-page":"457","DOI":"10.1016\/j.bbagrm.2019.02.009","article-title":"Dose dependent gene expression is dynamically modulated by the history, physiology and age of yeast cells","volume":"1862","author":"Pascual-Ahuir","year":"2019","journal-title":"Biochim. Biophys. Acta Gene Regul. Mech"},{"key":"10.1074\/jbc.RA119.009291_bib45","doi-asserted-by":"crossref","first-page":"841","DOI":"10.1002\/(SICI)1522-2683(20000301)21:5<841::AID-ELPS841>3.0.CO;2-4","article-title":"Direct Blue 71 staining of proteins bound to blotting membranes","volume":"21","author":"Hong","year":"2000","journal-title":"Electrophoresis"},{"key":"10.1074\/jbc.RA119.009291_bib46","doi-asserted-by":"crossref","first-page":"D348","DOI":"10.1093\/nar\/gkx842","article-title":"YEASTRACT, an upgraded database for the analysis of transcription regulatory networks in Saccharomyces cerevisiae","volume":"46","author":"Teixeira","year":"2018","journal-title":"Nucl. Acids Res"}],"container-title":["Journal of Biological Chemistry"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0021925820432314?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0021925820432314?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/syndication.highwire.org\/content\/doi\/10.1074\/jbc.RA119.009291","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,9,23]],"date-time":"2022-09-23T14:12:54Z","timestamp":1663942374000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S0021925820432314"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,8]]},"references-count":46,"journal-issue":{"issue":"35","published-print":{"date-parts":[[2019,8]]}},"alternative-id":["S0021925820432314"],"URL":"https:\/\/doi.org\/10.1074\/jbc.ra119.009291","relation":{},"ISSN":["0021-9258"],"issn-type":[{"value":"0021-9258","type":"print"}],"subject":[],"published":{"date-parts":[[2019,8]]},"assertion":[{"value":"Elsevier","name":"publisher","label":"This article is maintained by"},{"value":"Live-cell assays reveal selectivity and sensitivity of the multidrug response in budding yeast","name":"articletitle","label":"Article Title"},{"value":"Journal of Biological Chemistry","name":"journaltitle","label":"Journal Title"},{"value":"https:\/\/doi.org\/10.1074\/jbc.RA119.009291","name":"articlelink","label":"CrossRef DOI link to publisher maintained version"},{"value":"article","name":"content_type","label":"Content Type"},{"value":"\u00a9 2019 Vanacloig-Pedros et al.","name":"copyright","label":"Copyright"}]}}