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Efforts toward antimicrobial discovery typically identify compounds that prevent bacterial growth in microbiological media. However, the microenvironments to which pathogens are exposed during infection differ from rich media and alter the biology of the pathogen. We and others have therefore developed screening platforms that identify compounds that disrupt pathogen growth within cultured mammalian cells. Our platform focuses on Gram-negative bacterial pathogens, which are of particular clinical concern. We screened a panel of 707 drugs to identify those with efficacy against Salmonella enterica Typhimurium growth within macrophages. One of the drugs identified, clofazimine (CFZ), is an antibiotic used to treat mycobacterial infections that is not recognized for potency against Gram-negative bacteria. We demonstrated that in macrophages CFZ enabled the killing of S.\u00a0Typhimurium at single digit micromolar concentrations, and in mice, CFZ reduced tissue colonization. We confirmed that CFZ does not inhibit the growth of S.\u00a0Typhimurium and E.\u00a0coli in standard microbiological media. However, CFZ prevents bacterial replication under conditions consistent with the microenvironment of macrophage phagosomes, in which S.\u00a0Typhimurium resides during infection: low pH, low magnesium and phosphate, and the presence of certain cationic antimicrobial peptides. These observations suggest that in macrophages and mice the efficacy of CFZ against S.\u00a0Typhimurium is facilitated by multiple aspects of soluble innate immunity. Thus, systematic screens of existing drugs for infection-based potency are likely to identify unexpected opportunities for repurposing drugs to treat difficult pathogens.<\/jats:p>","DOI":"10.1021\/acsinfecdis.0c00023","type":"journal-article","created":{"date-parts":[[2020,4,9]],"date-time":"2020-04-09T20:16:30Z","timestamp":1586463390000},"page":"1238-1249","source":"Crossref","is-referenced-by-count":23,"title":["Clofazimine Reduces the Survival of\n                    <i>Salmonella\nenterica<\/i>\n                    in Macrophages and Mice"],"prefix":"10.1021","volume":"6","author":[{"given":"Toni A.","family":"Nagy","sequence":"first","affiliation":[{"name":"University of Colorado , , , ,","place":["Boulder, Colorado, United States, 80309"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Amy L.","family":"Crooks","sequence":"additional","affiliation":[{"name":"University of Colorado , , , ,","place":["Boulder, Colorado, United States, 80309"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Joaquin L. J.","family":"Quintana","sequence":"additional","affiliation":[{"name":"University of Colorado , , , ,","place":["Boulder, Colorado, United States, 80309"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7783-0876","authenticated-orcid":true,"given":"Corrella S.","family":"Detweiler","sequence":"additional","affiliation":[{"name":"University of Colorado , , , ,","place":["Boulder, Colorado, United States, 80309"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"316","published-online":{"date-parts":[[2020,4,9]]},"reference":[{"issue":"5","key":"2026081806114910300_cit1","doi-asserted-by":"publisher","first-page":"371","DOI":"10.1038\/nrd3975","article-title":"Platforms\nfor Antibiotic Discovery","volume":"12","author":"Lewis","year":"2013","journal-title":"Nat. Rev. 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Mueller and Hinton","volume":"22","author":"Nizet","year":"2017","journal-title":"EBioMedicine"},{"key":"2026081806114910300_cit4","doi-asserted-by":"publisher","first-page":"173","DOI":"10.1016\/j.ebiom.2017.05.026","article-title":"Correcting a Fundamental\nFlaw in the Paradigm for Antimicrobial Susceptibility Testing","volume":"20","author":"Ersoy","year":"2017","journal-title":"EBioMedicine"},{"issue":"2","key":"2026081806114910300_cit5","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.1003946","article-title":"Identification\nof Host-Targeted Small Molecules That Restrict Intracellular Mycobacterium\nTuberculosis Growth","volume":"10","author":"Stanley","year":"2014","journal-title":"PLoS Pathog."},{"issue":"3","key":"2026081806114910300_cit6","doi-asserted-by":"publisher","first-page":"292","DOI":"10.1016\/j.ijantimicag.2009.10.011","article-title":"Inhibition of Listeria\nMonocytogenes Infection by Neurological\nDrugs","volume":"35","author":"Lieberman","year":"2010","journal-title":"Int. J. Antimicrob. Agents"},{"issue":"6","key":"2026081806114910300_cit7","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.1007115","article-title":"A Cell-Based\nInfection Assay Identifies Efflux Pump Modulators That Reduce Bacterial\nIntracellular Load","volume":"14","author":"Reens","year":"2018","journal-title":"PLoS Pathog."},{"issue":"1","key":"2026081806114910300_cit8","doi-asserted-by":"publisher","first-page":"197","DOI":"10.1038\/s41467-018-08190-x","article-title":"A Macrophage-Based\nScreen Identifies Antibacterial Compounds Selective for Intracellular\nSalmonella Typhimurium","volume":"10","author":"Ellis","year":"2019","journal-title":"Nat. Commun."},{"issue":"9","key":"2026081806114910300_cit9","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0201915","article-title":"Galleria Mellonella\nas an Insect Model for P. Destructans, the Cause of White-Nose Syndrome\nin Bats","volume":"13","author":"Beekman","year":"2018","journal-title":"PLoS One"},{"issue":"4","key":"2026081806114910300_cit10","doi-asserted-by":"publisher","first-page":"331","DOI":"10.1038\/s41589-018-0018-3","article-title":"Whole-Organism\nPhenotypic Screening\nfor Anti-Infectives Promoting Host Health","volume":"14","author":"Clatworthy","year":"2018","journal-title":"Nat.\nChem. Biol."},{"key":"2026081806114910300_cit11","doi-asserted-by":"publisher","first-page":"43","DOI":"10.1016\/j.mib.2019.12.003","article-title":"Infection-Based\nChemical Screens Uncover Host-Pathogen Interactions","volume":"54","author":"Detweiler","year":"2020","journal-title":"Curr. Opin. Microbiol."},{"key":"2026081806114910300_cit12","doi-asserted-by":"publisher","first-page":"5","DOI":"10.1111\/nyas.14134","article-title":"Permeability Barriers of Gram-Negative\nPathogens","volume":"1459","author":"Zgurskaya","year":"2020","journal-title":"Ann. N. Y. Acad. Sci."},{"key":"2026081806114910300_cit13","doi-asserted-by":"crossref","DOI":"10.1201\/9781315533247","volume-title":"Janeway\u2019s\nImmunobiology","author":"Murphy","year":"2016"},{"issue":"5","key":"2026081806114910300_cit14","doi-asserted-by":"publisher","first-page":"1806","DOI":"10.1128\/IAI.01369-10","article-title":"How to\nBecome a Top Model: Impact of Animal Experimentation on Human Salmonella\nDisease Research","volume":"79","author":"Tsolis","year":"2011","journal-title":"Infect. Immun."},{"key":"2026081806114910300_cit15","doi-asserted-by":"publisher","first-page":"145","DOI":"10.1146\/annurev.mi.49.100195.001045","article-title":"How Salmonella Survive against the Odds","volume":"49","author":"Foster","year":"1995","journal-title":"Annu. Rev. 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Immun."},{"key":"2026081806114910300_cit19","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1128\/AAC.01536-19","article-title":"Autophagy\nInduction by a Small Molecule Inhibits Salmonella Survival in Macrophages\nand Mice","volume":"63","author":"Nagy","year":"2019","journal-title":"Antimicrob. Agents Chemother."},{"issue":"1","key":"2026081806114910300_cit20","doi-asserted-by":"publisher","first-page":"330","DOI":"10.3181\/00379727-48-13311","article-title":"A Protein-Free Medium\nfor Primary Isolation of the\nGonococcus and Meningococcus","volume":"48","author":"Mueller","year":"1941","journal-title":"Exp. Biol. Med."},{"issue":"suppl_1","key":"2026081806114910300_cit21","doi-asserted-by":"publisher","first-page":"5","DOI":"10.1093\/jac\/48.suppl_1.5","article-title":"Determination\nof Minimum Inhibitory Concentrations","volume":"48","author":"Andrews","year":"2001","journal-title":"J. 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Spectrum"},{"issue":"4","key":"2026081806114910300_cit24","doi-asserted-by":"publisher","first-page":"202","DOI":"10.1038\/nrmicro.2018.8","article-title":"Ecology and\nEvolution of Mycobacterium Tuberculosis","volume":"16","author":"Gagneux","year":"2018","journal-title":"Nat.\nRev. Microbiol."},{"issue":"9","key":"2026081806114910300_cit25","doi-asserted-by":"publisher","first-page":"e293","DOI":"10.1016\/S1473-3099(17)30418-8","article-title":"Multidrug Therapy for Leprosy: A Game Changer on the\nPath to Elimination","volume":"17","author":"Smith","year":"2017","journal-title":"Lancet Infect. 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Cell Biol."},{"key":"2026081806114910300_cit29","doi-asserted-by":"publisher","first-page":"3","DOI":"10.5935\/0305-7518.19650002","article-title":"THE ANTIMYCOBACTERIAL\nACTIVITY OF B 663","volume":"36","author":"Barry","year":"1965","journal-title":"Lepr. Rev."},{"issue":"12","key":"2026081806114910300_cit30","doi-asserted-by":"publisher","first-page":"2729","DOI":"10.1128\/AAC.36.12.2729","article-title":"Antimicrobial Activities of Clofazimine and B669 Are\nMediated by Lysophospholipids","volume":"36","author":"Van\nRensburg","year":"1992","journal-title":"Antimicrob. Agents\nChemother."},{"issue":"6","key":"2026081806114910300_cit31","doi-asserted-by":"publisher","first-page":"3042","DOI":"10.1128\/AAC.00260-15","article-title":"Pharmacokinetics\nand Pharmacodynamics of Clofazimine in a Mouse Model of Tuberculosis","volume":"59","author":"Swanson","year":"2015","journal-title":"Antimicrob. Agents Chemother."},{"issue":"7","key":"2026081806114910300_cit32","doi-asserted-by":"publisher","first-page":"472","DOI":"10.1055\/s-0031-1296634","article-title":"Tissue\nDistribution and Deposition of Clofazimine in\nMice Following Oral Administration with or without Isoniazid","volume":"57","author":"Venkatesan","year":"2007","journal-title":"Arzneim. Forsch."},{"issue":"6","key":"2026081806114910300_cit33","doi-asserted-by":"publisher","first-page":"1116","DOI":"10.4269\/ajtmh.1974.23.1116","article-title":"Tissue\nConcentrations of Clofazimine (B663) in Man","volume":"23","author":"Mansfield","year":"1974","journal-title":"Am. J. Trop. Med. Hyg."},{"issue":"2","key":"2026081806114910300_cit34","first-page":"479","article-title":"The Antileprosy\nAgent B.663 (Clofazimine)\nand the Reticuloendothelial System","volume":"39","author":"Conalty","year":"1971","journal-title":"Int. J.\nLepr. Other Mycobact. Dis."},{"issue":"6505","key":"2026081806114910300_cit35","doi-asserted-by":"publisher","first-page":"425","DOI":"10.1038\/372425a0","article-title":"Positional Cloning of the Mouse Obese Gene and Its\nHuman Homologue","volume":"372","author":"Zhang","year":"1994","journal-title":"Nature"},{"issue":"1","key":"2026081806114910300_cit36","doi-asserted-by":"publisher","first-page":"637","DOI":"10.1128\/AAC.02005-12","article-title":"The Target\nof Daptomycin Is Absent from Escherichia Coli and Other Gram-Negative\nPathogens","volume":"57","author":"Randall","year":"2013","journal-title":"Antimicrob. Agents Chemother."},{"issue":"3","key":"2026081806114910300_cit37","doi-asserted-by":"publisher","first-page":"576","DOI":"10.1111\/j.1462-5822.2007.01111.x","article-title":"The Salmonellae PhoQ Sensor: Mechanisms of Detection\nof Phagosome Signals","volume":"10","author":"Prost","year":"2008","journal-title":"Cell. Microbiol."},{"issue":"3","key":"2026081806114910300_cit38","doi-asserted-by":"crossref","first-page":"491","DOI":"10.1093\/genetics\/122.3.491","article-title":"Identification and Characterization\nof a New Gene of Escherichia Coli K-12 Involved in Outer Membrane\nPermeability","volume":"122","author":"Sampson","year":"1989","journal-title":"Genetics"},{"issue":"31","key":"2026081806114910300_cit39","doi-asserted-by":"publisher","first-page":"11754","DOI":"10.1073\/pnas.0604744103","article-title":"Identification\nof a Protein Complex That Assembles Lipopolysaccharide\nin the Outer Membrane of Escherichia Coli","volume":"103","author":"Wu","year":"2006","journal-title":"Proc.\nNatl. Acad. Sci. U. S. A."},{"issue":"13","key":"2026081806114910300_cit40","doi-asserted-by":"publisher","first-page":"4460","DOI":"10.1128\/JB.00270-08","article-title":"Functional\nAnalysis of the Protein Machinery Required for Transport of Lipopolysaccharide\nto the Outer Membrane of Escherichia Coli","volume":"190","author":"Sperandeo","year":"2008","journal-title":"J.\nBacteriol."},{"issue":"2","key":"2026081806114910300_cit41","doi-asserted-by":"publisher","first-page":"307","DOI":"10.1016\/j.cell.2005.02.014","article-title":"Chemical Conditionality:\nA Genetic Strategy to Probe Organelle Assembly","volume":"121","author":"Ruiz","year":"2005","journal-title":"Cell"},{"issue":"5","key":"2026081806114910300_cit42","doi-asserted-by":"publisher","first-page":"353","DOI":"10.1038\/ja.2015.116","article-title":"Application of Bacterial Cytological\nProfiling to Crude Natural Product Extracts Reveals the Antibacterial\nArsenal of Bacillus Subtilis","volume":"69","author":"Nonejuie","year":"2016","journal-title":"J. Antibiot."},{"issue":"1","key":"2026081806114910300_cit43","doi-asserted-by":"publisher","first-page":"62","DOI":"10.1128\/AAC.47.1.62-69.2003","article-title":"Mannopeptimycins,\nNew Cyclic Glycopeptide Antibiotics Produced by Streptomyces Hygroscopicus\nLL-AC98: Antibacterial and Mechanistic Activities","volume":"47","author":"Singh","year":"2003","journal-title":"Antimicrob. Agents Chemother."},{"issue":"5917","key":"2026081806114910300_cit44","doi-asserted-by":"publisher","first-page":"526","DOI":"10.1038\/303526a0","article-title":"Sensitization of Gram-Negative\nBacteria to Antibiotics and Complement\nby a Nontoxic Oligopeptide","volume":"303","author":"Vaara","year":"1983","journal-title":"Nature"},{"issue":"16","key":"2026081806114910300_cit45","doi-asserted-by":"publisher","first-page":"E77","DOI":"10.1073\/pnas.1101130108","article-title":"Real-Time\nAttack on Single Escherichia Coli Cells by the Human Antimicrobial\nPeptide LL-37","volume":"108","author":"Sochacki","year":"2011","journal-title":"Proc. Natl. Acad. Sci. U. S.\nA."},{"issue":"1","key":"2026081806114910300_cit46","doi-asserted-by":"publisher","first-page":"4780","DOI":"10.1038\/s41598-019-41246-6","article-title":"Cathelicidins PMAP-36, LL-37 and CATH-2 Are Similar\nPeptides with Different Modes of Action","volume":"9","author":"Scheenstra","year":"2019","journal-title":"Sci.\nRep."},{"issue":"6","key":"2026081806114910300_cit47","doi-asserted-by":"publisher","first-page":"1511","DOI":"10.1016\/j.bbamem.2013.02.011","article-title":"Real-Time\nAttack of LL-37 on Single Bacillus Subtilis\nCells","volume":"1828","author":"Barns","year":"2013","journal-title":"Biochim. Biophys. Acta, Biomembr."},{"issue":"15","key":"2026081806114910300_cit48","doi-asserted-by":"publisher","first-page":"2479","DOI":"10.1128\/JB.02456-14","article-title":"Importance of Real-Time\nAssays To Distinguish Multidrug Efflux Pump-Inhibiting and Outer Membrane-Destabilizing\nActivities in Escherichia Coli","volume":"197","author":"Misra","year":"2015","journal-title":"J. Bacteriol."},{"issue":"11","key":"2026081806114910300_cit49","doi-asserted-by":"publisher","first-page":"5642","DOI":"10.1128\/AAC.00756-12","article-title":"Rapid Killing\nof Acinetobacter Baumannii by Polymyxins Is Mediated by a Hydroxyl\nRadical Death Pathway","volume":"56","author":"Sampson","year":"2012","journal-title":"Antimicrob. Agents Chemother."},{"issue":"2","key":"2026081806114910300_cit50","doi-asserted-by":"publisher","first-page":"147","DOI":"10.1038\/ja.2013.111","article-title":"A Secondary Mode of\nAction of Polymyxins against Gram-Negative Bacteria Involves the Inhibition\nof NADH-Quinone Oxidoreductase Activity","volume":"67","author":"Deris","year":"2014","journal-title":"J.\nAntibiot."},{"issue":"3","key":"2026081806114910300_cit51","doi-asserted-by":"publisher","first-page":"395","DOI":"10.1128\/MMBR.56.3.395-411.1992","article-title":"Agents That\nIncrease the Permeability of the Outer Membrane","volume":"56","author":"Vaara","year":"1992","journal-title":"Microbiol. Rev."},{"issue":"48","key":"2026081806114910300_cit52","doi-asserted-by":"publisher","first-page":"49804","DOI":"10.1074\/jbc.M404299200","article-title":"Expression\nand Secretion of Salmonella Pathogenicity Island-2 Virulence Genes\nin Response to Acidification Exhibit Differential Requirements of\na Functional Type III Secretion Apparatus and SsaL","volume":"279","author":"Coombes","year":"2004","journal-title":"J. Biol. Chem."},{"issue":"4","key":"2026081806114910300_cit53","doi-asserted-by":"publisher","first-page":"806","DOI":"10.1046\/j.1365-2958.1999.01527.x","article-title":"PH-Dependent\nSecretion of SseB, a Product of the SPI-2 Type III Secretion System\nof Salmonella Typhimurium","volume":"33","author":"Beuzo\u0301n","year":"1999","journal-title":"Mol. Microbiol."},{"issue":"6","key":"2026081806114910300_cit54","doi-asserted-by":"publisher","first-page":"1759","DOI":"10.1046\/j.1365-2958.1999.01312.x","article-title":"Environmental Regulation\nof Salmonella Pathogenicity Island 2 Gene Expression","volume":"31","author":"Deiwick","year":"1999","journal-title":"Mol. Microbiol."},{"key":"2026081806114910300_cit55","doi-asserted-by":"publisher","first-page":"952","DOI":"10.3389\/fmicb.2019.00952","article-title":"Nucleoside Analogues\nas Antibacterial Agents","volume":"10","author":"Thomson","year":"2019","journal-title":"Front. Microbiol."},{"issue":"21","key":"2026081806114910300_cit56","doi-asserted-by":"publisher","first-page":"8333","DOI":"10.1073\/pnas.83.21.8333","article-title":"Phosphorylation of\n3\u2032-Azido-3\u2032-Deoxythymidine\nand Selective Interaction of the 5\u2032-Triphosphate with Human\nImmunodeficiency Virus Reverse Transcriptase","volume":"83","author":"Furman","year":"1986","journal-title":"Proc. Natl. Acad. 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