{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,19]],"date-time":"2026-09-19T17:12:30Z","timestamp":1789837950941,"version":"4.0.1"},"reference-count":56,"publisher":"American Chemical Society (ACS)","issue":"13","license":[{"start":{"date-parts":[[2020,3,23]],"date-time":"2020-03-23T00:00:00Z","timestamp":1584921600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/pubs.acs.org\/page\/policy\/authorchoice_termsofuse.html"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2020,4,7]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>Listeria monocytogenes, a human foodborne pathogen that causes listeriosis with high-rate mortality, has been reported to be resistant to commonly used antibiotics. New antibiotics or cocktails of existing antibiotics with synergistic compounds are in high demand for treating this multi-drug-resistant pathogen. Fosfomycin is one of the novel and promising therapeutic antibiotics for the treatment of listeriosis. However, some L. monocytogenes strains with the FosX gene were recently reported to survive from the fosfomycin treatment. This work aims to identify FosX inhibitors that can revive fosfomycin in treating resistant L. monocytogenes. Since structures and activities of the FosX protein in L. monocytogenes have been well studied, we used an integrated computational and experimental approach to identify FosX inhibitors that show synergistic effect with fosfomycin in treating resistant L. monocytogenes. Specifically, automated ligand docking was implemented to perform virtual screening of the Indofine natural-product database and FDA-approved drugs to identify potential inhibitors. An in vitro bacterial growth inhibition test was then utilized to verify the effectiveness of identified compounds combined with fosfomycin in inhibiting the resistant L. monocytogenes strains. Two phenolic acids, i.e., caffeic acid and chlorogenic acid, were predicted as high-affinity FosX inhibitors from the ligand-docking platform. Experiments with these compounds indicated that the cocktail of either caffeic acid (1.5 mg\/mL) or chlorogenic acid (3 mg\/mL) with fosfomycin (50 mg\/L) was able to significantly inhibit the growth of the pathogen. The finding of this work implies that the combination of fosfomycin with either caffeic acid or chlorogenic acid is of potential to be used in the clinical treatment of Listeria infections.<\/jats:p>","DOI":"10.1021\/acsomega.0c00352","type":"journal-article","created":{"date-parts":[[2020,3,23]],"date-time":"2020-03-23T17:23:17Z","timestamp":1584984197000},"page":"7537-7544","source":"Crossref","is-referenced-by-count":34,"title":["Synergistic Effect of Chlorogenic Acid and Caffeic\nAcid with Fosfomycin on Growth Inhibition of a Resistant\n                    <i>Listeria monocytogenes<\/i>\n                    Strain"],"prefix":"10.1021","volume":"5","author":[{"given":"Fangyuan","family":"Zhang","sequence":"first","affiliation":[{"name":"Villanova University , , 800 E Lancaster Avenue , , ,","place":["Villanova, Pennsylvania, United States, 19085"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tianhua","family":"Zhai","sequence":"additional","affiliation":[{"name":"Villanova University , , 800 E Lancaster Avenue , , ,","place":["Villanova, Pennsylvania, United States, 19085"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2650-2925","authenticated-orcid":true,"given":"Shozeb","family":"Haider","sequence":"additional","affiliation":[{"name":"University College London (UCL) , , ,","place":["London, U.K., WC1E 6BT"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yanhong","family":"Liu","sequence":"additional","affiliation":[{"name":"U.S. Department of Agriculture , , , ,","place":["Wyndmoor, Pennsylvania, United States, 19038"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1393-2961","authenticated-orcid":true,"given":"Zuyi Jacky","family":"Huang","sequence":"additional","affiliation":[{"name":"Villanova University , , 800 E Lancaster Avenue , , ,","place":["Villanova, Pennsylvania, United States, 19085"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"316","published-online":{"date-parts":[[2020,3,23]]},"reference":[{"key":"2026090205264535400_cit1","doi-asserted-by":"publisher","first-page":"32","DOI":"10.1038\/nrmicro.2017.126","article-title":"Listeria monocytogenes: towards a complete picture of its physiology\nand pathogenesis","volume":"16","author":"Radoshevich","year":"2018","journal-title":"Nat. Rev. Microbiol."},{"key":"2026090205264535400_cit2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pgen.1007525","article-title":"Epistatic\ncontrol of intrinsic resistance by virulence\ngenes in Listeria","volume":"14","author":"Scortti","year":"2018","journal-title":"PLoS Genet."},{"key":"2026090205264535400_cit3","doi-asserted-by":"publisher","DOI":"10.3390\/toxins12010038","article-title":"An Inducible Cre-lox\nSystem to Analyze the Role of\nLLO in Listeria monocytogenes Pathogenesis","volume":"12","author":"Nguyen","year":"2020","journal-title":"Toxins"},{"key":"2026090205264535400_cit4","doi-asserted-by":"publisher","DOI":"10.1016\/j.vetmic.2019.108528","article-title":"Experimental\nlisteriosis: A study\nof purinergic and cholinergic inflammatory pathway","volume":"241","author":"Jaguezeski","year":"2020","journal-title":"Vet. Microbiol."},{"key":"2026090205264535400_cit5","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2019.01388","article-title":"TLR2 Promotes\nMonocyte\/Macrophage\nRecruitment Into the Liver and Microabscess Formation to Limit the\nSpread of Listeria monocytogenes","volume":"10","author":"Wang","year":"2019","journal-title":"Front. Immunol."},{"key":"2026090205264535400_cit6","doi-asserted-by":"publisher","first-page":"M1392","DOI":"10.1111\/1750-3841.12181","article-title":"Construction\nof Listeria monocytogenes mutants with\nin-frame deletions in the phosphotransferase transport system (PTS)\nand analysis of their growth under stress conditions","volume":"78","author":"Liu","year":"2013","journal-title":"J. Food Sci."},{"key":"2026090205264535400_cit7","doi-asserted-by":"publisher","first-page":"141","DOI":"10.4172\/1948-5948.1000085","article-title":"Construction\nof Listeria monocytogenes mutants with\nin-frame deletions in putative ATP-binding cassette (ABC) transporters\nand analysis of their growth under stress conditions","volume":"04","author":"Liu","year":"2012","journal-title":"J. Microb. Biochem. Technol."},{"key":"2026090205264535400_cit8","doi-asserted-by":"crossref","DOI":"10.1007\/978-3-319-16286-7","volume-title":"Listeria monocytogenes\nin the Food Processing Environment","author":"Jordan","year":"2015"},{"key":"2026090205264535400_cit9","doi-asserted-by":"publisher","DOI":"10.1016\/j.jprot.2019.103534","article-title":"Milk microbiota: Characterization\nmethods and role in cheese production","volume":"210","author":"Tilocca","year":"2020","journal-title":"J. Proteomics"},{"key":"2026090205264535400_cit10","doi-asserted-by":"crossref","DOI":"10.1007\/978-3-319-25277-3","volume-title":"Microbes\nin Food and\nHealth","author":"Garg","year":"2016"},{"key":"2026090205264535400_cit11","unstructured":"CDC Listeria Outbreaks. https:\/\/www.cdc.gov\/listeria\/outbreaks\/index.html (accessed July 2019)."},{"key":"2026090205264535400_cit12","doi-asserted-by":"publisher","first-page":"2","DOI":"10.1016\/j.ijbiomac.2018.01.030","article-title":"Biological\nmacromolecules based targeted nanodrug delivery systems for the treatment\nof intracellular infections","volume":"110","author":"Aparna","year":"2018","journal-title":"Int. J. Biol. Macromol."},{"key":"2026090205264535400_cit13","doi-asserted-by":"publisher","first-page":"656","DOI":"10.1345\/aph.19315","article-title":"Treatment of Listeriosis","volume":"34","author":"Temple","year":"2000","journal-title":"Ann.\nPharmacother."},{"key":"2026090205264535400_cit14","doi-asserted-by":"publisher","first-page":"438","DOI":"10.1016\/j.bjm.2015.11.033","article-title":"Occurrence and antimicrobial resistance patterns of Listeria monocytogenes isolated from vegetables","volume":"47","author":"de Vasconcelos Byrne","year":"2016","journal-title":"Braz. J. Microbiol."},{"key":"2026090205264535400_cit15","doi-asserted-by":"publisher","first-page":"135","DOI":"10.1016\/j.ijantimicag.2013.10.018","article-title":"In vitro and intracellular\nactivities of fosfomycin against clinical strains of Listeria monocytogenes","volume":"43","author":"Lepe","year":"2014","journal-title":"Int.\nJ. Antimicrob. 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Against Pancreatic Cholesterol Esterase Activity: An In Silico\nApproach","volume":"11","author":"Varghese","year":"2019","journal-title":"Interdiscip. Sci.: Comput. Life Sci."},{"key":"2026090205264535400_cit31","doi-asserted-by":"publisher","first-page":"53","DOI":"10.1016\/j.ijbiomac.2019.12.091","article-title":"Combining in silico\nand in vitro approaches to identification of potent inhibitor against\nphospholipase A2 (PLA2)","volume":"144","author":"Chinnasamy","year":"2020","journal-title":"Int. J. Biol. Macromol."},{"key":"2026090205264535400_cit32","doi-asserted-by":"publisher","first-page":"1923","DOI":"10.2174\/1568026614666140929124445","article-title":"Structure-Based Virtual\nScreening for Drug Discovery: Principles, Applications and Recent\nAdvances","volume":"14","author":"Lionta","year":"2014","journal-title":"Curr. Top. Med. 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Food Sci."},{"key":"2026090205264535400_cit48","doi-asserted-by":"publisher","first-page":"69","DOI":"10.1080\/08927014.2013.845878","article-title":"Antistaphylococcal\nand biofilm inhibitory activities of gallic, caffeic, and chlorogenic\nacids","volume":"30","author":"Lui\u0301s","year":"2014","journal-title":"Biofouling"},{"key":"2026090205264535400_cit49","doi-asserted-by":"publisher","first-page":"67","DOI":"10.1016\/j.biopha.2017.10.064","article-title":"Chlorogenic\nacid (CGA): A pharmacological review and call for further research","volume":"97","author":"Naveed","year":"2018","journal-title":"Biomed. 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Food Agric."},{"key":"2026090205264535400_cit53","doi-asserted-by":"publisher","first-page":"311","DOI":"10.4103\/pm.pm_309_15","article-title":"Mechanism\nof Action of Isolated Caffeic\nAcid and Epicatechin 3-gallate from Euphorbia hirta against Pseudomonas aeruginosa","volume":"13","author":"Perumal","year":"2017","journal-title":"Pharmacogn. Mag."},{"key":"2026090205264535400_cit54","unstructured":"Tice, R.\n          \n          Chlorogenic Acid and\nCaffeic Acid Review of Toxicological Literature; 1998."},{"key":"2026090205264535400_cit55","doi-asserted-by":"publisher","first-page":"6560","DOI":"10.1021\/jm301916b","article-title":"Hit identification\nand optimization in virtual screening: practical recommendations based\non a critical literature analysis","volume":"56","author":"Zhu","year":"2013","journal-title":"J. Med. Chem."},{"key":"2026090205264535400_cit56","doi-asserted-by":"publisher","first-page":"71","DOI":"10.1016\/j.jpha.2015.11.005","article-title":"Methods for in vitro evaluating antimicrobial\nactivity: A review","volume":"6","author":"Balouiri","year":"2016","journal-title":"J. Pharm. Anal."}],"container-title":["ACS Omega"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/pubs.acs.org\/doi\/pdf\/10.1021\/acsomega.0c00352","content-type":"application\/pdf","content-version":"vor","intended-application":"unspecified"},{"URL":"https:\/\/pubs.acs.org\/acsodf\/article-pdf\/5\/13\/7537\/67674635\/acsomega.0c00352.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/pubs.acs.org\/acsodf\/article-pdf\/5\/13\/7537\/67674635\/acsomega.0c00352.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,9,2]],"date-time":"2026-09-02T09:26:55Z","timestamp":1788341215000},"score":1,"resource":{"primary":{"URL":"https:\/\/pubs.acs.org\/acsodf\/article\/5\/13\/7537\/606889\/Synergistic-Effect-of-Chlorogenic-Acid-and-Caffeic"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,3,23]]},"references-count":56,"journal-issue":{"issue":"13","published-online":{"date-parts":[[2020,3,23]]},"published-print":{"date-parts":[[2020,4,7]]}},"URL":"https:\/\/doi.org\/10.1021\/acsomega.0c00352","relation":{},"ISSN":["2470-1343"],"issn-type":[{"value":"2470-1343","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,3,23]]}}}