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We discovered that a lysine- and arginine-specific supramolecular ligand (CLR01) destroys enveloped viruses, including HIV, Ebola, and Zika virus, and remodels amyloid fibrils in semen that promote viral infection. Yet, it is unknown how CLR01 exerts these two distinct therapeutic activities. Here, we delineate a novel mechanism of antiviral activity by studying the activity of tweezer variants: the \u201cphosphate tweezer\u201d CLR01, a \u201ccarboxylate tweezer\u201d CLR05, and a \u201cphosphate clip\u201d PC. Lysine complexation inside the tweezer cavity is needed to antagonize amyloidogenesis and is only achieved by CLR01. Importantly, CLR01 and CLR05 but not PC form closed inclusion complexes with lipid head groups of viral membranes, thereby altering lipid orientation and increasing surface tension. This process disrupts viral envelopes and diminishes infectivity but leaves cellular membranes intact. Consequently, CLR01 and CLR05 display broad antiviral activity against all enveloped viruses tested, including herpesviruses, Measles virus, influenza, and SARS-CoV-2. Based on our mechanistic insights, we potentiated the antiviral, membrane-disrupting activity of CLR01 by introducing aliphatic ester arms into each phosphate group to act as lipid anchors that promote membrane targeting. The most potent ester modifications harbored unbranched C4 units, which engendered tweezers that were approximately one order of magnitude more effective than CLR01 and nontoxic. Thus, we establish the mechanistic basis of viral envelope disruption by specific tweezers and establish a new class of potential broad-spectrum antivirals with enhanced activity.<\/jats:p>","DOI":"10.1021\/jacs.0c06400","type":"journal-article","created":{"date-parts":[[2020,9,14]],"date-time":"2020-09-14T18:19:17Z","timestamp":1600107557000},"page":"17024-17038","source":"Crossref","is-referenced-by-count":48,"title":["Supramolecular\nMechanism of Viral Envelope Disruption\nby Molecular Tweezers"],"prefix":"10.1021","volume":"142","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-0925-2426","authenticated-orcid":true,"given":"Tatjana","family":"Weil","sequence":"first","affiliation":[{"name":"Ulm University Medical Center , , ,","place":["Ulm, Germany, 89081"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ru\u0308diger","family":"Gro\u00df","sequence":"additional","affiliation":[{"name":"Ulm University Medical Center , , ,","place":["Ulm, Germany, 89081"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Annika","family":"Ro\u0308cker","sequence":"additional","affiliation":[{"name":"Ulm University Medical Center , , ,","place":["Ulm, Germany, 89081"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kenny","family":"Bravo-Rodriguez","sequence":"additional","affiliation":[{"name":"University of Duisburg-Essen , , ,","place":["Essen, Germany, 45117"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christian","family":"Heid","sequence":"additional","affiliation":[{"name":"University of Duisburg-Essen , , ,","place":["Essen, Germany, 45117"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andrea","family":"Sowislok","sequence":"additional","affiliation":[{"name":"University of Duisburg-Essen , , ,","place":["Essen, Germany, 45117"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"My-Hue","family":"Le","sequence":"additional","affiliation":[{"name":"University of Duisburg-Essen , , ,","place":["Essen, Germany, 45117"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nelli","family":"Erwin","sequence":"additional","affiliation":[{"name":"TU Dortmund University , , ,","place":["Dortmund, Germany, 44227"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mridula","family":"Dwivedi","sequence":"additional","affiliation":[{"name":"TU Dortmund University , , ,","place":["Dortmund, Germany, 44227"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Stephen M.","family":"Bart","sequence":"additional","affiliation":[{"name":"Perelman School of Medicine at the University of Pennsylvania , , , ,","place":["Philadelphia, Pennsylvania, United States, 19104"]},{"name":"Perelman School of Medicine at the University of Pennsylvania , , , ,","place":["Philadelphia, Pennsylvania, United States, 19104"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Paul","family":"Bates","sequence":"additional","affiliation":[{"name":"Perelman School of Medicine at the University of Pennsylvania , , , ,","place":["Philadelphia, Pennsylvania, United States, 19104"]},{"name":"Perelman School of Medicine at the University of Pennsylvania , , , ,","place":["Philadelphia, Pennsylvania, United States, 19104"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lukas","family":"Wettstein","sequence":"additional","affiliation":[{"name":"Ulm University Medical Center , , ,","place":["Ulm, Germany, 89081"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Janis A.","family":"Mu\u0308ller","sequence":"additional","affiliation":[{"name":"Ulm University Medical Center , , ,","place":["Ulm, Germany, 89081"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mirja","family":"Harms","sequence":"additional","affiliation":[{"name":"Ulm University Medical Center , , ,","place":["Ulm, Germany, 89081"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Konstantin","family":"Sparrer","sequence":"additional","affiliation":[{"name":"Ulm University Medical Center , , ,","place":["Ulm, Germany, 89081"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5400-4427","authenticated-orcid":true,"given":"Yasser B.","family":"Ruiz-Blanco","sequence":"additional","affiliation":[{"name":"University of Duisburg-Essen , , ,","place":["Essen, Germany, 45117"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christina M.","family":"Stu\u0308rzel","sequence":"additional","affiliation":[{"name":"Ulm University Medical Center , , ,","place":["Ulm, Germany, 89081"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jens","family":"von Einem","sequence":"additional","affiliation":[{"name":"Ulm University Medical Center , , ,","place":["Ulm, Germany, 89081"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sina","family":"Lippold","sequence":"additional","affiliation":[{"name":"Ulm University Medical Center , , ,","place":["Ulm, Germany, 89081"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Clarissa","family":"Read","sequence":"additional","affiliation":[{"name":"Ulm University Medical Center , , ,","place":["Ulm, Germany, 89081"]},{"name":"Ulm University , , ,","place":["Ulm, Germany, 89081"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Paul","family":"Walther","sequence":"additional","affiliation":[{"name":"Ulm University , , ,","place":["Ulm, Germany, 89081"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marco","family":"Hebel","sequence":"additional","affiliation":[{"name":"Max Planck Institute for Polymer Research , Ackermannweg 10 , ,","place":["Mainz, Germany, 55128"]},{"name":"Ulm University , , Albert-Einstein-Allee 11 , ,","place":["Ulm, Germany, 89081"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Florian","family":"Kreppel","sequence":"additional","affiliation":[{"name":"University of Witten\/Herdecke , , Stockumer Strasse 10 , ,","place":["Witten, Germany, 58453"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Frank-Gerrit","family":"Kla\u0308rner","sequence":"additional","affiliation":[{"name":"University of Duisburg-Essen , , ,","place":["Essen, Germany, 45117"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7046-3754","authenticated-orcid":true,"given":"Gal","family":"Bitan","sequence":"additional","affiliation":[{"name":"University of California, Los Angeles , , , ,","place":["Los Angeles, California, United States, 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19104"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9211-5803","authenticated-orcid":true,"given":"Elsa","family":"Sanchez-Garcia","sequence":"additional","affiliation":[{"name":"University of Duisburg-Essen , , ,","place":["Essen, Germany, 45117"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7316-7141","authenticated-orcid":true,"given":"Jan","family":"Mu\u0308nch","sequence":"additional","affiliation":[{"name":"Ulm University Medical Center , , ,","place":["Ulm, Germany, 89081"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"316","published-online":{"date-parts":[[2020,9,14]]},"reference":[{"issue":"1","key":"2026090217452432700_cit1","doi-asserted-by":"publisher","first-page":"4","DOI":"10.1021\/acsinfecdis.8b00286","article-title":"Targeting the Achilles Heel of Mosquito-Borne\nViruses for Antiviral 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Dis."},{"key":"2026090217452432700_cit2","first-page":"426","article-title":"Broad-Spectrum\nAntivirals against Viral Fusion","volume-title":"Nature Reviews\nMicrobiology","author":"Vigant","year":"2015"},{"issue":"1","key":"2026090217452432700_cit3","doi-asserted-by":"publisher","first-page":"111","DOI":"10.1083\/jcb.200507075","article-title":"Domain III from Class\nII Fusion Proteins Functions\nas a Dominant-Negative Inhibitor of Virus Membrane Fusion","volume":"171","author":"Liao","year":"2005","journal-title":"J. Cell Biol."},{"issue":"9","key":"2026090217452432700_cit4","doi-asserted-by":"publisher","first-page":"e2430","DOI":"10.1371\/journal.pntd.0002430","article-title":"A Fusion-Inhibiting\nPeptide against Rift Valley Fever Virus Inhibits Multiple, Diverse\nViruses","volume":"7","author":"Koehler","year":"2013","journal-title":"PLoS Neglected Trop. Dis."},{"issue":"3","key":"2026090217452432700_cit5","doi-asserted-by":"publisher","first-page":"293","DOI":"10.4149\/av_2013_03_293","article-title":"Potential\nRoles of Protein Disulphide\nIsomerase in Viral Infections","volume":"57","author":"Diwaker","year":"2013","journal-title":"Acta Virol."},{"key":"2026090217452432700_cit6","doi-asserted-by":"publisher","first-page":"2180","DOI":"10.1016\/j.bbamem.2014.04.015","article-title":"Peptide\nEntry Inhibitors of Enveloped\nViruses: The Importance of Interfacial Hydrophobicity","volume":"1838","author":"Badani","year":"2014","journal-title":"Biochim. Biophys. Acta, Biomembr."},{"issue":"40","key":"2026090217452432700_cit7","doi-asserted-by":"publisher","first-page":"17176","DOI":"10.1073\/pnas.1009445107","article-title":"Polyunsaturated Liposomes\nAre Antiviral\nagainst Hepatitis B and C Viruses and HIV by Decreasing Cholesterol\nLevels in Infected Cells","volume":"107","author":"Pollock","year":"2010","journal-title":"Proc. Natl. Acad.\nSci. U. S. A."},{"issue":"40","key":"2026090217452432700_cit8","doi-asserted-by":"publisher","first-page":"17339","DOI":"10.1073\/pnas.1010026107","article-title":"Rigid Amphipathic Fusion Inhibitors, Small Molecule\nAntiviral Compounds against Enveloped Viruses","volume":"107","author":"St. Vincent","year":"2010","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"issue":"1","key":"2026090217452432700_cit9","doi-asserted-by":"publisher","first-page":"161","DOI":"10.1042\/BJ20131058","article-title":"Singlet Oxygen Effects\non Lipid Membranes: Implications for the Mechanism of Action of Broad-Spectrum\nViral Fusion Inhibitors","volume":"459","author":"Hollmann","year":"2014","journal-title":"Biochem. J."},{"issue":"42","key":"2026090217452432700_cit10","doi-asserted-by":"publisher","first-page":"16958","DOI":"10.1021\/ja206279b","article-title":"Lysine-Specific Molecular\nTweezers Are Broad-Spectrum Inhibitors of Assembly and Toxicity of\nAmyloid Proteins","volume":"133","author":"Sinha","year":"2011","journal-title":"J. Am. Chem. Soc."},{"issue":"15","key":"2026090217452432700_cit11","doi-asserted-by":"publisher","first-page":"2469","DOI":"10.2174\/13816128113199990496","article-title":"Disrupting Self-Assembly\nand Toxicity of Amyloidogenic Protein Oligomers\nby \u201c Molecular Tweezers\u201d - from the Test Tube to Animal\nModels","volume":"20","author":"Attar","year":"2014","journal-title":"Curr. Pharm. Des."},{"issue":"76","key":"2026090217452432700_cit12","doi-asserted-by":"publisher","first-page":"11318","DOI":"10.1039\/C6CC04640A","article-title":"Molecular\nTweezers for Lysine and\nArginine-Powerful Inhibitors of Pathologic Protein Aggregation","volume":"52","author":"Schrader","year":"2016","journal-title":"Chem. Commun."},{"key":"2026090217452432700_cit13","doi-asserted-by":"publisher","first-page":"657","DOI":"10.3389\/fchem.2019.00657","article-title":"Molecular\nLysine Tweezers Counteract Aberrant Protein Aggregation","volume":"7","author":"Hadrovic","year":"2019","journal-title":"Front. 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Natl. Acad. Sci. U. S. A."},{"issue":"1","key":"2026090217452432700_cit22","doi-asserted-by":"publisher","first-page":"73","DOI":"10.1128\/JVI.01366-08","article-title":"The Cationic Properties\nof SEVI Underlie Its Ability\nTo Enhance Human Immunodeficiency Virus Infection","volume":"83","author":"Roan","year":"2009","journal-title":"J. Virol."},{"issue":"2","key":"2026090217452432700_cit23","doi-asserted-by":"publisher","first-page":"1244","DOI":"10.1128\/JVI.06121-11","article-title":"Naturally Occurring Fragments from Two Distinct Regions of the Prostatic\nAcid Phosphatase Form Amyloidogenic Enhancers of HIV Infection","volume":"86","author":"Arnold","year":"2012","journal-title":"J. Virol."},{"key":"2026090217452432700_cit24","doi-asserted-by":"publisher","first-page":"26","DOI":"10.1016\/j.antiviral.2018.02.003","article-title":"The Molecular\nTweezer CLR01 Inhibits Ebola and Zika Virus Infection","volume":"152","author":"Ro\u0308cker","year":"2018","journal-title":"Antiviral Res."},{"issue":"13","key":"2026090217452432700_cit25","doi-asserted-by":"publisher","first-page":"6721","DOI":"10.1021\/jo4009673","article-title":"Molecular Tweezers\nwith Varying Anions: A Comparative Study","volume":"78","author":"Dutt","year":"2013","journal-title":"J.\nOrg. Chem."},{"issue":"30","key":"2026090217452432700_cit26","doi-asserted-by":"publisher","first-page":"9824","DOI":"10.1021\/ja801441j","article-title":"Molecular Clip and\nTweezer Introduce New Mechanisms of Enzyme Inhibition","volume":"130","author":"Talbiersky","year":"2008","journal-title":"J. Am. Chem. 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