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Natl. Acad. Sci. U.S.A."],"published-print":{"date-parts":[[2025,4]]},"abstract":"<jats:p>\n                    Antibiotic resistance, especially in multidrug-resistant ESKAPE pathogens, remains a worldwide problem. Combination antimicrobial therapies may be an important strategy to overcome resistance and broaden the spectrum of existing antibiotics. However, this strategy is limited by the ability to efficiently screen large combinatorial chemical spaces. Here, we deployed a high-throughput combinatorial screening platform, DropArray, to evaluate the interactions of over 30,000 compounds with up to 22 antibiotics and 6 strains of gram-negative ESKAPE pathogens, totaling to over 1.3 million unique strain-antibiotic-compound combinations. In this dataset, compounds more frequently exhibited synergy with known antibiotics than single-agent activity. We identified a compound, P2-56, and developed a more potent analog, P2-56-3, which potentiated rifampin (RIF) against antibiotic-resistant strains of\n                    <jats:italic toggle=\"yes\">Acinetobacter baumannii<\/jats:italic>\n                    and\n                    <jats:italic toggle=\"yes\">Klebsiella pneumoniae<\/jats:italic>\n                    . Using phenotypic assays, we showed P2-56-3 disrupts the outer membrane of\n                    <jats:italic toggle=\"yes\">A. baumannii<\/jats:italic>\n                    . To identify pathways involved in the mechanism of synergy between P2-56-3 and RIF, we performed genetic screens in\n                    <jats:italic toggle=\"yes\">A. baumannii<\/jats:italic>\n                    . CRISPRi-induced partial depletion of lipooligosaccharide transport genes (\n                    <jats:italic toggle=\"yes\">lptA<\/jats:italic>\n                    -\n                    <jats:italic toggle=\"yes\">D<\/jats:italic>\n                    ,\n                    <jats:italic toggle=\"yes\">lptFG<\/jats:italic>\n                    ) resulted in hypersensitivity to P2-56-3\/RIF treatment, demonstrating the genetic dependency of P2-56-3 activity and RIF sensitization on\n                    <jats:italic toggle=\"yes\">lpt<\/jats:italic>\n                    genes in\n                    <jats:italic toggle=\"yes\">A. baumannii.<\/jats:italic>\n                    Consistent with outer membrane homeostasis being an important determinant of P2-56-3\/RIF tolerance, knockout of maintenance of lipid asymmetry complex genes and overexpression of certain resistance-nodulation-division efflux pumps\u2014a phenotype associated with multidrug-resistance\u2014resulted in hypersensitivity to P2-56-3. These findings demonstrate the immense scale of phenotypic antibiotic combination screens using DropArray and the potential for such approaches to discover new small molecule synergies against multidrug-resistant ESKAPE strains.\n                  <\/jats:p>","DOI":"10.1073\/pnas.2402017122","type":"journal-article","created":{"date-parts":[[2025,3,24]],"date-time":"2025-03-24T15:13:45Z","timestamp":1742829225000},"update-policy":"https:\/\/doi.org\/10.1073\/pnas.cm10313","source":"Crossref","is-referenced-by-count":10,"title":["Large-scale combination screens reveal small-molecule sensitization of antibiotic-resistant gram-negative ESKAPE pathogens"],"prefix":"10.1073","volume":"122","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-4968-7072","authenticated-orcid":false,"given":"Megan W.","family":"Tse","sequence":"first","affiliation":[{"name":"Department of Biological Engineering, Massachusetts Institute of Technology","place":["Cambridge"]},{"name":"Broad Institute of Massachusetts Institute of Technology and Harvard","place":["Cambridge"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Meilin","family":"Zhu","sequence":"additional","affiliation":[{"name":"Department of Biological Engineering, Massachusetts Institute of Technology","place":["Cambridge"]},{"name":"Broad Institute of Massachusetts Institute of Technology and Harvard","place":["Cambridge"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Benjamin","family":"Peters","sequence":"additional","affiliation":[{"name":"Broad Institute of Massachusetts Institute of Technology and Harvard","place":["Cambridge"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0008-1950-3587","authenticated-orcid":false,"given":"Efrat","family":"Hamami","sequence":"additional","affiliation":[{"name":"Department of Molecular Biology and Microbiology, Tufts University School of Medicine","place":["Boston"]},{"name":"Stuart B. Levy Center for Integrated Management of Antimicrobial Resistance","place":["Boston"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4648-7478","authenticated-orcid":false,"given":"Julie","family":"Chen","sequence":"additional","affiliation":[{"name":"Department of Biological Engineering, Massachusetts Institute of Technology","place":["Cambridge"]},{"name":"Broad Institute of Massachusetts Institute of Technology and Harvard","place":["Cambridge"]},{"name":"Microbiology Graduate Program, Massachusetts Institute of Technology","place":["Cambridge"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3034-2162","authenticated-orcid":false,"given":"Kathleen P.","family":"Davis","sequence":"additional","affiliation":[{"name":"Department of Molecular Biology and Microbiology, Tufts University School of Medicine","place":["Boston"]},{"name":"Stuart B. 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Hamami Identification of essential genes that support fitness of Acinetobacter baumannii efflux pump overproducers in the presence of fluoroquinolone. bioRxiv [Preprint] (2024). https:\/\/doi.org\/10.1101\/2024.01.04.574119 (Accessed 6 March 2024).","DOI":"10.1101\/2024.01.04.574119"},{"key":"e_1_3_5_36_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.bbalip.2016.10.006"},{"key":"e_1_3_5_37_2","doi-asserted-by":"publisher","DOI":"10.1146\/annurev-biochem-060713-035600"},{"key":"e_1_3_5_38_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-020-18301-2"},{"key":"e_1_3_5_39_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41564-021-00973-1"},{"key":"e_1_3_5_40_2","doi-asserted-by":"crossref","unstructured":"R. D. 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Tse M. Zhu R. Isberg P. Blainey Data from \u201cLarge-scale combination screens reveal small molecule sensitization of antibiotic-resistant Gram-negative ESKAPE pathogens.\u201d Harvard Dataverse. https:\/\/doi.org\/10.7910\/DVN\/YWBFSJ. Deposited 6 February 2024."},{"key":"e_1_3_5_64_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.cels.2020.09.009"},{"key":"e_1_3_5_65_2","doi-asserted-by":"publisher","DOI":"10.1128\/mBio.01127-19"},{"key":"e_1_3_5_66_2","doi-asserted-by":"publisher","DOI":"10.1093\/bioinformatics\/btx320"},{"key":"e_1_3_5_67_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-018-02875-z"},{"key":"e_1_3_5_68_2","unstructured":"M. Tse Abx Combos Droparray. Github. https:\/\/github.com\/megantse\/abxcombos-droparray. Deposited 1 February 2024."},{"key":"e_1_3_5_69_2","unstructured":"M. Tse Abx Combos CRISPRi. Github. https:\/\/github.com\/megantse\/abxcombos-crispri. Deposited 1 February 2024."},{"key":"e_1_3_5_70_2","unstructured":"M. Tse Abx Combos Tn-seq. 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