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Repurposing existing drugs to augment the antifungal activity of well-tolerated antifungals is a promising antifungal strategy with the potential to be implemented rapidly. Here, we explored the mechanism by which colistin, a positively charged lipopeptide antibiotic, enhances the antifungal activity of fluconazole, the most widely used orally available antifungal. In a range of susceptible and drug-resistant isolates and species, colistin was primarily effective at reducing fluconazole tolerance, a property of subpopulations of cells that grow slowly in the presence of a drug and may promote the emergence of persistent infections and resistance. Clinically relevant concentrations of colistin synergized with fluconazole, reducing fluconazole minimum inhibitory concentration 4-fold. Combining fluconazole and colistin also increased survival in a C. albicans Galleria mellonella infection, especially for a highly fluconazole-tolerant isolate. Mechanistically, colistin increased permeability to fluorescent antifungal azole probes and to intracellular dyes, accompanied by an increase in cell death that was dependent upon pharmacological or genetic inhibition of the ergosterol biosynthesis pathway. The positive charge of colistin is critical to its antifungal, and antibacterial, activity: colistin directly binds to several eukaryotic membrane lipids (i.e., l-\u03b1-phosphatidylinositol, l-\u03b1-phosphatidyl-l-serine, and l-\u03b1-phosphatidylethanolamine) that are enriched in the membranes of ergosterol-depleted cells. These results support the idea that colistin binds to fungal membrane lipids and permeabilizes fungal cells in a manner that depends upon the degree of ergosterol depletion.<\/jats:p>","DOI":"10.1021\/acsinfecdis.0c00721","type":"journal-article","created":{"date-parts":[[2021,1,20]],"date-time":"2021-01-20T14:57:35Z","timestamp":1611154655000},"page":"377-389","source":"Crossref","is-referenced-by-count":40,"title":["Combining Colistin and Fluconazole Synergistically\nIncreases Fungal Membrane Permeability and Antifungal Cidality"],"prefix":"10.1021","volume":"7","author":[{"given":"Maayan","family":"Bibi","sequence":"first","affiliation":[{"name":"Tel Aviv University , , ,","place":["Ramat Aviv, Israel, 6997801"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sarah","family":"Murphy","sequence":"additional","affiliation":[{"name":"St George\u2019s University , , Cranmer Terrace , ,","place":["London, United Kingdom, SW17 0RE"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1743-0886","authenticated-orcid":true,"given":"Raphael I.","family":"Benhamou","sequence":"additional","affiliation":[{"name":"Tel Aviv University , , ,","place":["Ramat Aviv, Israel, 6997801"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alex","family":"Rosenberg","sequence":"additional","affiliation":[{"name":"Tel Aviv University , , ,","place":["Ramat Aviv, Israel, 6997801"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Adi","family":"Ulman","sequence":"additional","affiliation":[{"name":"Tel Aviv University , , ,","place":["Ramat Aviv, Israel, 6997801"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tihana","family":"Bicanic","sequence":"additional","affiliation":[{"name":"St George\u2019s University , , Cranmer Terrace , ,","place":["London, United Kingdom, SW17 0RE"]},{"name":"St George\u2019s Hospital NHS Trust , , ,","place":["London, United Kingdom, SW17 0QT"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2009-7490","authenticated-orcid":true,"given":"Micha","family":"Fridman","sequence":"additional","affiliation":[{"name":"Tel Aviv University , , ,","place":["Ramat Aviv, Israel, 6997801"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8577-0084","authenticated-orcid":true,"given":"Judith","family":"Berman","sequence":"additional","affiliation":[{"name":"Tel Aviv University , , ,","place":["Ramat Aviv, Israel, 6997801"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"316","published-online":{"date-parts":[[2021,1,20]]},"reference":[{"key":"2026090313172503200_cit1","doi-asserted-by":"publisher","first-page":"133","DOI":"10.1128\/CMR.00029-06","article-title":"Epidemiology of\nInvasive Candidiasis: A Persistent\nPublic Health Problem","volume":"20","author":"Pfaller","year":"2007","journal-title":"Clin. Microbiol. Rev."},{"key":"2026090313172503200_cit2","doi-asserted-by":"publisher","first-page":"e449","DOI":"10.1093\/cid\/ciaa193","article-title":"Burden of\nCandidemia in the United States, 2017","author":"Tsay","year":"2020","journal-title":"Clin.\nInfect. Dis."},{"key":"2026090313172503200_cit3","doi-asserted-by":"publisher","first-page":"31","DOI":"10.3390\/mps2020031","article-title":"High Efficiency\nDrug Repurposing\nDesign for New Antifungal Agents","volume":"2","author":"Kim","year":"2019","journal-title":"Methods Protoc."},{"key":"2026090313172503200_cit4","doi-asserted-by":"publisher","first-page":"198","DOI":"10.1080\/21505594.2016.1216283","article-title":"Antifungal\nAdjuvants: Preserving\nand Extending the Antifungal Arsenal","volume":"8","author":"Butts","year":"2017","journal-title":"Virulence."},{"key":"2026090313172503200_cit5","doi-asserted-by":"publisher","first-page":"237","DOI":"10.2147\/IDR.S118892","article-title":"Fluconazole Resistance\nin Candida Species: A Current\nPerspective","volume":"10","author":"Berkow","year":"2017","journal-title":"Infect. Drug Resist."},{"key":"2026090313172503200_cit6","doi-asserted-by":"publisher","first-page":"3037","DOI":"10.1128\/AAC.45.11.3037-3045.2001","article-title":"In Vitro and in Vivo\nEffects of 14alpha-Demethylase (ERG11) Depletion in Candida glabrata","volume":"45","author":"Nakayama","year":"2001","journal-title":"Antimicrob. Agents Chemother."},{"key":"2026090313172503200_cit7","doi-asserted-by":"publisher","first-page":"2470","DOI":"10.1038\/s41467-018-04926-x","article-title":"Antifungal\nTolerance Is a Subpopulation Effect Distinct from Resistance and Is\nAssociated with Persistent Candidemia","volume":"9","author":"Rosenberg","year":"2018","journal-title":"Nat.\nCommun."},{"key":"2026090313172503200_cit8","doi-asserted-by":"publisher","first-page":"319","DOI":"10.1038\/s41579-019-0322-2","article-title":"Drug Resistance\nand Tolerance in Fungi","volume":"18","author":"Berman","year":"2020","journal-title":"Nat. Rev. Microbiol."},{"key":"2026090313172503200_cit9","doi-asserted-by":"publisher","first-page":"70","DOI":"10.1016\/j.mib.2018.02.005","article-title":"Antifungal Drug\nResistance: Evolution, Mechanisms and Impact","volume":"45","author":"Revie","year":"2018","journal-title":"Curr. Opin. Microbiol."},{"key":"2026090313172503200_cit10","doi-asserted-by":"publisher","first-page":"1059","DOI":"10.1099\/mic.0.000295","article-title":"diskImageR:\nQuantification\nof Resistance and Tolerance to Antimicrobial Drugs Using Disk Diffusion\nAssays","volume":"162","author":"Gerstein","year":"2016","journal-title":"Microbiology"},{"key":"2026090313172503200_cit11","doi-asserted-by":"publisher","first-page":"62","DOI":"10.1128\/AAC.01624-18","article-title":"Implications\nof the EUCAST Trailing Phenomenon in Candida tropicalis for the In Vivo Susceptibility in Invertebrate and Murine Models","volume":"62","author":"Astvad","year":"2018","journal-title":"Antimicrob. Agents Chemother."},{"key":"2026090313172503200_cit12","doi-asserted-by":"publisher","first-page":"78","DOI":"10.1111\/myc.13191","article-title":"Impact of Tolerance to Fluconazole on Treatment Response\nin Candida albicans Bloodstream Infection","volume":"64","author":"Levinson","year":"2021","journal-title":"Mycoses"},{"key":"2026090313172503200_cit13","doi-asserted-by":"publisher","first-page":"219","DOI":"10.1590\/S1517-83822008000200004","article-title":"Membrane Fluidity\nand Lipid Composition of Fluconazole Resistant and Susceptible Strains\nof Candida albicans Isolated from Diabetic Patients","volume":"39","author":"Mishra","year":"2008","journal-title":"Braz. J. Microbiol."},{"key":"2026090313172503200_cit14","doi-asserted-by":"publisher","first-page":"3597","DOI":"10.1128\/AAC.00653-06","article-title":"Unexpected Link between\nIron and Drug Resistance of Candida Spp.: Iron Depletion Enhances\nMembrane Fluidity and Drug Diffusion, Leading to Drug-Susceptible\nCells","volume":"50","author":"Prasad","year":"2006","journal-title":"Antimicrob. Agents Chemother."},{"key":"2026090313172503200_cit15","doi-asserted-by":"publisher","first-page":"905","DOI":"10.1093\/jac\/dki112","article-title":"Squalene Epoxidase\nEncoded by ERG1 Affects Morphogenesis and Drug Susceptibilities of Candida albicans","volume":"55","author":"Pasrija","year":"2005","journal-title":"J. Antimicrob. Chemother."},{"key":"2026090313172503200_cit16","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.1001126","article-title":"Azole Drugs\nAre Imported by Facilitated\nDiffusion in Candida albicans and Other Pathogenic\nFungi","volume":"6","author":"Mansfield","year":"2010","journal-title":"PLoS Pathog."},{"key":"2026090313172503200_cit17","doi-asserted-by":"publisher","first-page":"244","DOI":"10.1128\/AAC.31.2.244","article-title":"Entry of Ketoconazole\ninto Candida albicans","volume":"31","author":"Boiron","year":"1987","journal-title":"Antimicrob.\nAgents Chemother."},{"key":"2026090313172503200_cit18","doi-asserted-by":"publisher","first-page":"520","DOI":"10.3389\/fcimb.2017.00520","article-title":"Candida albicans Heat Shock Proteins and Hsps-Associated Signaling Pathways as Potential\nAntifungal Targets","volume":"7","author":"Gong","year":"2017","journal-title":"Front. Cell. Infect. Microbiol."},{"key":"2026090313172503200_cit19","doi-asserted-by":"publisher","first-page":"557","DOI":"10.1128\/CMR.00064-16","article-title":"Polymyxins:\nAntibacterial Activity,\nSusceptibility Testing, and Resistance Mechanisms Encoded by Plasmids\nor Chromosomes","volume":"30","author":"Poirel","year":"2017","journal-title":"Clin. Microbiol. Rev."},{"key":"2026090313172503200_cit20","doi-asserted-by":"publisher","first-page":"1333","DOI":"10.1086\/429323","article-title":"Colistin:\nThe Revival of Polymyxins\nfor the Management of Multidrug-Resistant Gram-Negative Bacterial\nInfections","volume":"40","author":"Falagas","year":"2005","journal-title":"Clin. Infect. Dis."},{"key":"2026090313172503200_cit21","doi-asserted-by":"publisher","first-page":"418","DOI":"10.1016\/S0140-6736(97)80051-7","article-title":"Peptide\nAntibiotics","volume":"349","author":"Hancock","year":"1997","journal-title":"Lancet"},{"key":"2026090313172503200_cit22","first-page":"157","article-title":"Colistin:\nAn Antibiotic and Its Role in Multiresistant\nGram-Negative Infections","volume":"47","author":"Loho","year":"2015","journal-title":"Acta Med. Indones."},{"key":"2026090313172503200_cit23","doi-asserted-by":"publisher","first-page":"14","DOI":"10.1186\/2110-5820-1-14","article-title":"Renal and Neurological Side Effects\nof Colistin in\nCritically Ill Patients","volume":"1","author":"Spapen","year":"2011","journal-title":"Ann. Intensive Care"},{"key":"2026090313172503200_cit24","doi-asserted-by":"publisher","first-page":"6060","DOI":"10.1039\/C5CC10249A","article-title":"Efficient\nTotal Syntheses and Biological Activities of Two Teixobactin Analogues","volume":"52","author":"Parmar","year":"2016","journal-title":"Chem. Commun."},{"key":"2026090313172503200_cit25","doi-asserted-by":"publisher","DOI":"10.1101\/479618","article-title":"Colistin Kills Bacteria by\nTargeting Lipopolysaccharide in the Cytoplasmic Membrane","volume-title":"bioRxiv","author":"Sabnis"},{"key":"2026090313172503200_cit26","doi-asserted-by":"publisher","first-page":"985","DOI":"10.1093\/femsre\/fuv026","article-title":"Transport\nof Lipopolysaccharide to\nthe Gram-Negative Bacterial Cell Surface","volume":"39","author":"Putker","year":"2015","journal-title":"FEMS\nMicrobiol. Rev."},{"key":"2026090313172503200_cit27","doi-asserted-by":"publisher","first-page":"66","DOI":"10.1186\/s13756-019-0521-7","article-title":"In Vitro Polymyxin\nActivity against Clinical Multidrug-Resistant Fungi","volume":"8","author":"Yousfi","year":"2019","journal-title":"Antimicrob. Resist. Infect. Control"},{"key":"2026090313172503200_cit28","doi-asserted-by":"publisher","first-page":"21448","DOI":"10.1038\/s41598-020-78588-5","article-title":"In Vitro Synergy of\nIsavuconazole\nin Combination with Colistin against Candida auris","volume":"10","author":"Schwarz","year":"2020","journal-title":"Sci. Rep."},{"key":"2026090313172503200_cit29","doi-asserted-by":"publisher","first-page":"1285","DOI":"10.1093\/jac\/dks538","article-title":"Synergy of\nthe Antibiotic Colistin\nwith Echinocandin Antifungals in Candida Species","volume":"68","author":"Zeidler","year":"2013","journal-title":"J. Antimicrob. Chemother."},{"key":"2026090313172503200_cit30","doi-asserted-by":"publisher","first-page":"931","DOI":"10.1093\/jac\/dkq046","article-title":"Polymyxin B, in Combination\nwith Fluconazole, Exerts a Potent Fungicidal Effect","volume":"65","author":"Zhai","year":"2010","journal-title":"J. Antimicrob. Chemother."},{"key":"2026090313172503200_cit31","doi-asserted-by":"publisher","first-page":"529","DOI":"10.1099\/00222615-3-3-529","article-title":"Polymyxin\nSensitivity Of Candida tropicalis","volume":"3","author":"Nicholls","year":"1970","journal-title":"J. Med. Microbiol."},{"key":"2026090313172503200_cit32","doi-asserted-by":"publisher","first-page":"31","DOI":"10.3390\/antibiotics8010031","article-title":"A Review of the\nClinical Pharmacokinetics of Polymyxin\nB","volume":"8","author":"Avedissian","year":"2019","journal-title":"Antibiotics (Basel, Switz.)"},{"key":"2026090313172503200_cit33","doi-asserted-by":"publisher","first-page":"140","DOI":"10.1128\/JCM.43.1.140-143.2005","article-title":"Synergy Tests\nby E\nTest and Checkerboard Methods of Antimicrobial Combinations against Brucella melitensis","volume":"43","author":"Orhan","year":"2005","journal-title":"J. Clin. Microbiol."},{"key":"2026090313172503200_cit34","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1093\/jac\/dkg301","article-title":"Synergy,\nAntagonism, and What the Chequerboard Puts between Them","volume":"52","author":"Odds","year":"2003","journal-title":"J. Antimicrob. Chemother."},{"key":"2026090313172503200_cit35","doi-asserted-by":"publisher","first-page":"305","DOI":"10.1016\/j.ijantimicag.2014.10.020","article-title":"Determination of in Vitro Synergy\nfor Dual Antimicrobial Therapy against Resistant Neisseria gonorrhoeae Using Etest and Agar Dilution","volume":"45","author":"Wind","year":"2015","journal-title":"Int. J. Antimicrob. Agents"},{"key":"2026090313172503200_cit36","doi-asserted-by":"publisher","first-page":"11","DOI":"10.1186\/s12879-016-2117-7","article-title":"Impact\nof Colistin Plasma Levels\non the Clinical Outcome of Patients with Infections Caused by Extremely\nDrug-Resistant Pseudomonas aeruginosa","volume":"17","author":"Sorli\u0301","year":"2017","journal-title":"BMC Infect. Dis."},{"issue":"3","key":"2026090313172503200_cit37","doi-asserted-by":"publisher","first-page":"100","DOI":"10.3390\/antibiotics8030100","article-title":"An Approach to Measuring Colistin\nPlasma Levels Regarding the Treatment of Multidrug-Resistant Bacterial\nInfection","volume":"8","author":"Pacheco","year":"2019","journal-title":"Antibiotics (Basel)"},{"issue":"6\u20137","key":"2026090313172503200_cit38","doi-asserted-by":"publisher","first-page":"315","DOI":"10.1016\/j.mad.2011.06.007","article-title":"Quick and\nReliable Assessment of Chronological Life\nSpan in Yeast Cell Populations by Flow Cytometry","volume":"132","author":"Ocampo","year":"2011","journal-title":"Mech. Ageing Dev."},{"key":"2026090313172503200_cit39","doi-asserted-by":"publisher","first-page":"1769","DOI":"10.1021\/acschembio.7b00339","article-title":"Real-Time Imaging of\nthe Azole Class of Antifungal Drugs in Live Candida Cells","volume":"12","author":"Benhamou","year":"2017","journal-title":"ACS Chem. Biol."},{"issue":"21","key":"2026090313172503200_cit40","doi-asserted-by":"publisher","first-page":"6230","DOI":"10.1002\/anie.201802509","article-title":"Localizing\nAntifungal\nDrugs to the Correct Organelle Can Markedly Enhance Their Efficacy","volume":"57","author":"Benhamou","year":"2018","journal-title":"Angew. Chem., Int. Ed."},{"key":"2026090313172503200_cit41","doi-asserted-by":"publisher","first-page":"3325","DOI":"10.1021\/acschembio.8b00782","article-title":"Fluorescent\nTracking of the Endoplasmic Reticulum in Live Pathogenic Fungal Cells","volume":"13","author":"Benhamou","year":"2018","journal-title":"ACS Chem. Biol."},{"key":"2026090313172503200_cit42","doi-asserted-by":"publisher","first-page":"649","DOI":"10.1080\/21505594.2016.1188236","article-title":"The Synthesis, Regulation,\nand Functions of Sterols\nin Candida albicans: Well-Known but Still Lots to\nLearn","volume":"7","author":"Lv","year":"2016","journal-title":"Virulence"},{"key":"2026090313172503200_cit43","doi-asserted-by":"publisher","first-page":"2404","DOI":"10.1128\/AAC.47.8.2404-2412.2003","article-title":"Candida albicans Mutations in the Ergosterol Biosynthetic Pathway\nand Resistance to Several Antifungal Agents","volume":"47","author":"Sanglard","year":"2003","journal-title":"Antimicrob. Agents Chemother."},{"key":"2026090313172503200_cit44","doi-asserted-by":"publisher","first-page":"63","DOI":"10.1128\/AAC.01337-18","article-title":"Loss of\nC-5 Sterol Desaturase Activity\nin Candida albicans: Azole Resistance or Merely Trailing\nGrowth?","volume":"63","author":"Luna-Tapia","year":"2019","journal-title":"Antimicrob. Agents Chemother."},{"issue":"3","key":"2026090313172503200_cit45","doi-asserted-by":"publisher","first-page":"e00225-18","DOI":"10.1128\/mBio.00225-18","article-title":"Loss of\nUpc2p-Inducible ERG3 Transcription Is Sufficient\nTo Confer Niche-Specific Azole Resistance without Compromising Candida albicans Pathogenicity","volume":"9","author":"Luna-Tapia","year":"2018","journal-title":"MBio"},{"key":"2026090313172503200_cit46","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pbio.1001815","article-title":"A Tetraploid\nIntermediate Precedes Aneuploid Formation in Yeasts Exposed to Fluconazole","volume":"12","author":"Harrison","year":"2014","journal-title":"PLoS Biol."},{"issue":"46","key":"2026090313172503200_cit47","doi-asserted-by":"publisher","first-page":"13617","DOI":"10.1002\/anie.201506814","article-title":"Di-N-Methylation\nof\nAnti-Gram-Positive Aminoglycoside-Derived Membrane Disruptors Improves\nAntimicrobial Potency and Broadens Spectrum to Gram-Negative Bacteria","volume":"54","author":"Benhamou","year":"2015","journal-title":"Angew. Chem., Int. Ed."},{"issue":"50","key":"2026090313172503200_cit48","doi-asserted-by":"publisher","first-page":"16391","DOI":"10.1002\/anie.201809410","article-title":"Cationic Amphiphiles Induce Macromolecule\nDenaturation\nand Organelle Decomposition in Pathogenic Yeast","volume":"57","author":"Jaber","year":"2018","journal-title":"Angew. Chem., Int. Ed."},{"key":"2026090313172503200_cit49","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1093\/jac\/dkx349","article-title":"Daptomycin","volume":"73","author":"Heidary","year":"2018","journal-title":"J. Antimicrob. Chemother."},{"key":"2026090313172503200_cit50","doi-asserted-by":"publisher","first-page":"707","DOI":"10.1185\/03007995.2015.1018989","article-title":"Colistin, Mechanisms and Prevalence of Resistance","volume":"31","author":"Bialvaei","year":"2015","journal-title":"Curr. Med. Res. Opin."},{"key":"2026090313172503200_cit51","doi-asserted-by":"publisher","first-page":"668","DOI":"10.1128\/AAC.00985-12","article-title":"Colistin Methanesulfonate\nand Colistin Pharmacokinetics in Critically Ill Patients Receiving\nContinuous Venovenous Hemodiafiltration","volume":"57","author":"Karvanen","year":"2013","journal-title":"Antimicrob.\nAgents Chemother."},{"key":"2026090313172503200_cit52","doi-asserted-by":"publisher","first-page":"4241","DOI":"10.1128\/AAC.06426-11","article-title":"Application\nof a Loading Dose of Colistin Methanesulfonate in Critically Ill Patients:\nPopulation Pharmacokinetics, Protein Binding, and Prediction of Bacterial\nKill","volume":"56","author":"Mohamed","year":"2012","journal-title":"Antimicrob. Agents Chemother."},{"key":"2026090313172503200_cit53","doi-asserted-by":"publisher","first-page":"464","DOI":"10.1128\/AAC.00602-11","article-title":"Identification of\nHopanoid Biosynthesis Genes Involved in Polymyxin Resistance in Burkholderia multivorans","volume":"56","author":"Malott","year":"2012","journal-title":"Antimicrob.\nAgents Chemother."},{"key":"2026090313172503200_cit54","doi-asserted-by":"publisher","first-page":"2245","DOI":"10.1101\/gad.1121003","article-title":"Virulence-Related Surface Glycoproteins in the Yeast\nPathogen Candida glabrata Are Encoded in Subtelomeric\nClusters and Subject to RAP1- and SIR-Dependent Transcriptional Silencing","volume":"17","author":"De Las Penas","year":"2003","journal-title":"Genes Dev."},{"key":"2026090313172503200_cit55","doi-asserted-by":"publisher","first-page":"329","DOI":"10.1128\/JCM.36.2.329-334.1998","article-title":"Candida dubliniensis: Characteristics\nand Identification","volume":"36","author":"Sullivan","year":"1998","journal-title":"J. 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