{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,3]],"date-time":"2026-09-03T18:12:44Z","timestamp":1788459164060,"version":"build-2803163510"},"reference-count":51,"publisher":"American Chemical Society (ACS)","issue":"9","license":[{"start":{"date-parts":[[2020,8,12]],"date-time":"2020-08-12T00:00:00Z","timestamp":1597190400000},"content-version":"vor","delay-in-days":23,"URL":"https:\/\/pubs.acs.org\/page\/policy\/authorchoice_termsofuse.html"}],"funder":[{"DOI":"10.13039\/501100006769","name":"Russian Science Foundation","doi-asserted-by":"publisher","award":["17-74-20049"],"award-info":[{"award-number":["17-74-20049"]}],"id":[{"id":"10.13039\/501100006769","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2020,9,11]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>Viruses require host cell metabolites to productively infect, and the mechanisms by which viruses usurp these molecules are diverse. One group of cellular metabolites important in virus infection is the polyamines, small positively charged molecules involved in cell cycle, translation, and nucleic acid metabolism, among other cellular functions. Polyamines support replication of diverse viruses, and they are important for processes such as transcription, translation, and viral protein enzymatic activity. Rift Valley fever virus (RVFV) is a negative and ambisense RNA virus that requires polyamines to produce infectious particles. In polyamine depleted conditions, noninfectious particles are produced that interfere with virus replication and stimulate immune signaling. Here, we find that RVFV relies on virion-associated polyamines to maintain infectivity and enhance viral entry. We show that RVFV replication is facilitated by a limited set of polyamines and that spermidine and closely related molecules associate with purified virions and transmit from cell to cell during infection. Virion-associated spermidine maintains virion infectivity, as virions devoid of polyamines rapidly lose infectivity and are temperature sensitive. Further, virions without polyamines bind to cells but exhibit a defect in entry, requiring more acidic conditions than virions containing spermidine. These data highlight a unique role for polyamines, and spermidine particularly, to maintain virus infectivity. Further, these studies are the first to identify polyamines associated with RVFV virions. Targeting polyamines represents a promising antiviral strategy, and this work highlights a new mechanism by which we can inhibit virus replication through FDA-approved polyamine depleting pharmaceuticals.<\/jats:p>","DOI":"10.1021\/acsinfecdis.0c00402","type":"journal-article","created":{"date-parts":[[2020,7,20]],"date-time":"2020-07-20T19:04:40Z","timestamp":1595271880000},"page":"2490-2501","source":"Crossref","is-referenced-by-count":19,"title":["Virion-Associated Polyamines Transmit with Bunyaviruses\nto Maintain Infectivity and Promote Entry"],"prefix":"10.1021","volume":"6","author":[{"given":"Vincent","family":"Mastrodomenico","sequence":"first","affiliation":[{"name":"Loyola University Chicago , , , ,","place":["Maywood, Illinois, United States, 60153"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jeremy J.","family":"Esin","sequence":"additional","affiliation":[{"name":"Loyola University Chicago , , , ,","place":["Maywood, Illinois, United States, 60153"]},{"name":"Loyola University Chicago , , , ,","place":["Maywood, Illinois, United States, 60153"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shefah","family":"Qazi","sequence":"additional","affiliation":[{"name":"Indiana University , , , ,","place":["Bloomington, Indiana, United States, 47405"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Maxim A.","family":"Khomutov","sequence":"additional","affiliation":[{"name":"Russian Academy of Sciences , , ,","place":["Moscow, Russia, 119991"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alexander V.","family":"Ivanov","sequence":"additional","affiliation":[{"name":"Russian Academy of Sciences , , ,","place":["Moscow, Russia, 119991"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9230-4746","authenticated-orcid":true,"given":"Suchetana","family":"Mukhopadhyay","sequence":"additional","affiliation":[{"name":"Indiana University , , , ,","place":["Bloomington, Indiana, United States, 47405"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1710-5362","authenticated-orcid":true,"given":"Bryan C.","family":"Mounce","sequence":"additional","affiliation":[{"name":"Loyola University Chicago , , , ,","place":["Maywood, Illinois, United States, 60153"]},{"name":"Loyola University Chicago , , , ,","place":["Maywood, Illinois, United States, 60153"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"316","published-online":{"date-parts":[[2020,7,20]]},"reference":[{"issue":"7","key":"2026090313172095800_cit1","doi-asserted-by":"publisher","first-page":"e263","DOI":"10.1371\/journal.pmed.0030263","article-title":"Genome Microevolution\nof Chikungunya Viruses Causing the Indian Ocean Outbreak","volume":"3","author":"Schuffenecker","year":"2006","journal-title":"PLOS Med."},{"issue":"7","key":"2026090313172095800_cit2","doi-asserted-by":"publisher","first-page":"e119","DOI":"10.1016\/S1473-3099(16)30010-X","article-title":"Zika Virus: History of a Newly Emerging\nArbovirus","volume":"16","author":"Wikan","year":"2016","journal-title":"Lancet Infect. Dis."},{"issue":"4","key":"2026090313172095800_cit3","doi-asserted-by":"publisher","first-page":"722","DOI":"10.4269\/ajtmh.14-0421","article-title":"A Review of Mosquitoes Associated\nwith Rift Valley Fever Virus in Madagascar","volume":"92","author":"Tantely","year":"2015","journal-title":"Am. J. Trop. Med. Hyg."},{"issue":"2","key":"2026090313172095800_cit4","doi-asserted-by":"publisher","first-page":"e0005341","DOI":"10.1371\/journal.pntd.0005341","article-title":"Distribution\nand Abundance of Key Vectors of Rift Valley Fever and Other Arboviruses\nin Two Ecologically Distinct Counties in Kenya","volume":"11","author":"Sang","year":"2017","journal-title":"PLoS Neglected Trop. Dis."},{"issue":"1","key":"2026090313172095800_cit5","doi-asserted-by":"publisher","first-page":"65","DOI":"10.1186\/1471-2334-10-65","article-title":"Role of Culex and Anopheles Mosquito\nSpecies as Potential Vectors of Rift Valley Fever Virus in Sudan Outbreak,\n2007","volume":"10","author":"Seufi","year":"2010","journal-title":"BMC Infect. Dis."},{"issue":"5","key":"2026090313172095800_cit6","doi-asserted-by":"publisher","first-page":"e0006474","DOI":"10.1371\/journal.pntd.0006474","article-title":"Attenuation\nand Efficacy of Live-Attenuated Rift Valley Fever Virus Vaccine Candidates\nin Non-Human Primates","volume":"12","author":"Smith","year":"2018","journal-title":"PLoS Neglected Trop.\nDis."},{"issue":"6","key":"2026090313172095800_cit7","doi-asserted-by":"publisher","first-page":"601","DOI":"10.1080\/14760584.2017.1321482","article-title":"Rift Valley\nFever Vaccines: An Overview of the Safety and Efficacy of the Live-Attenuated\nMP-12 Vaccine Candidate","volume":"16","author":"Ikegami","year":"2017","journal-title":"Expert Rev. Vaccines"},{"issue":"3","key":"2026090313172095800_cit8","doi-asserted-by":"publisher","first-page":"29","DOI":"10.3390\/vaccines5030029","article-title":"Current\nStatus of Rift Valley Fever Vaccine Development","volume":"5","author":"Faburay","year":"2017","journal-title":"Vaccines"},{"issue":"2_Suppl","key":"2026090313172095800_cit9","doi-asserted-by":"publisher","first-page":"28","DOI":"10.4269\/ajtmh.2010.09-0319","article-title":"Rift Valley Fever Virus Epidemic in Kenya, 2006\/2007:\nThe Entomologic Investigations","volume":"83","author":"Sang","year":"2010","journal-title":"Am. J. Trop.\nMed. Hyg."},{"issue":"2","key":"2026090313172095800_cit10","doi-asserted-by":"publisher","first-page":"138","DOI":"10.3201\/eid0802.010023","article-title":"An Outbreak\nof Rift Valley Fever in Northeastern Kenya, 1997\u201398","volume":"8","author":"Woods","year":"2002","journal-title":"Emerging Infect. 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Biomark."},{"issue":"8820","key":"2026090313172095800_cit19","doi-asserted-by":"publisher","first-page":"652","DOI":"10.1016\/0140-6736(92)92180-N","article-title":"Efficacy\nand Toxicity of Eflornithine for Treatment of Trypanosoma Brucei Gambiense\nSleeping Sickness","volume":"340","author":"Milord","year":"1992","journal-title":"Lancet"},{"issue":"S1","key":"2026090313172095800_cit20","doi-asserted-by":"publisher","first-page":"S49","DOI":"10.1007\/s00436-002-0766-5","article-title":"Eflornithine for the\nTreatment of Human African Trypanosomiasis","volume":"90","author":"Burri","year":"2003","journal-title":"Parasitol. Res."},{"issue":"11","key":"2026090313172095800_cit21","doi-asserted-by":"publisher","first-page":"2818","DOI":"10.1073\/pnas.68.11.2818","article-title":"Compartmentalization of Spermine\nand Spermidine in the Herpes Simplex Virion","volume":"68","author":"Gibson","year":"1971","journal-title":"Proc. Natl. Acad. Sci. U. S. 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Chem."},{"issue":"2","key":"2026090313172095800_cit24","doi-asserted-by":"publisher","first-page":"167","DOI":"10.1016\/j.chom.2016.06.011","article-title":"Interferon-Induced Spermidine-Spermine\nAcetyltransferase and Polyamine Depletion Restrict Zika and Chikungunya\nViruses","volume":"20","author":"Mounce","year":"2016","journal-title":"Cell Host Microbe"},{"issue":"21","key":"2026090313172095800_cit25","doi-asserted-by":"publisher","first-page":"9683","DOI":"10.1128\/JVI.01347-16","article-title":"Inhibition of Polyamine Biosynthesis Is a Broad-Spectrum\nStrategy against RNA Viruses","volume":"90","author":"Mounce","year":"2016","journal-title":"J. Virol."},{"issue":"5","key":"2026090313172095800_cit26","doi-asserted-by":"publisher","first-page":"403","DOI":"10.3390\/v11050403","article-title":"Coxsackievirus B3\nResponds to Polyamine Depletion via Enhancement of 2A and 3C Protease\nActivity","volume":"11","author":"Dial","year":"2019","journal-title":"Viruses"},{"key":"2026090313172095800_cit27","doi-asserted-by":"publisher","first-page":"e00530-19","DOI":"10.1128\/JVI.00530-19","article-title":"Polyamine Depletion\nInhibits Bunyavirus Infection via Generation of Noninfectious Interfering\nVirions","volume":"93","author":"Mastrodomenico","year":"2019","journal-title":"J. Virol."},{"key":"2026090313172095800_cit28","doi-asserted-by":"publisher","first-page":"e01054-19","DOI":"10.1128\/JVI.01054-19","article-title":"Polyamine\nDepletion Abrogates Enterovirus Cellular Attachment","volume":"93","author":"Kicmal","year":"2019","journal-title":"J. Virol."},{"issue":"2","key":"2026090313172095800_cit29","doi-asserted-by":"publisher","first-page":"669","DOI":"10.1073\/pnas.64.2.669","article-title":"THE POLYAMINE CONTENT OF THE TRNA\nOF E. Coli","volume":"64","author":"Cohen","year":"1969","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"issue":"10","key":"2026090313172095800_cit30","doi-asserted-by":"publisher","first-page":"1968","DOI":"10.1261\/rna.1994310","article-title":"Probing TRNA Interaction with Biogenic\nPolyamines","volume":"16","author":"Ouameur","year":"2010","journal-title":"RNA"},{"issue":"5","key":"2026090313172095800_cit31","doi-asserted-by":"publisher","first-page":"413","DOI":"10.3109\/10409238.2014.939608","article-title":"The Hypusine-Containing Translation Factor EIF5A","volume":"49","author":"Dever","year":"2014","journal-title":"Crit. Rev. Biochem. Mol. Biol."},{"issue":"6","key":"2026090313172095800_cit32","doi-asserted-by":"publisher","first-page":"3105","DOI":"10.1128\/MCB.11.6.3105","article-title":"Translation Initiation\nFactor 5A and Its Hypusine Modification Are Essential for Cell Viability\nin the Yeast Saccharomyces Cerevisiae","volume":"11","author":"Schnier","year":"1991","journal-title":"Mol.\nCell. Biol."},{"issue":"4","key":"2026090313172095800_cit33","doi-asserted-by":"publisher","first-page":"e00882-16","DOI":"10.1128\/mBio.00882-16","article-title":"Polyamines and Hypusination Are Required\nfor Ebolavirus Gene Expression and Replication","volume":"7","author":"Olsen","year":"2016","journal-title":"mBio"},{"issue":"20","key":"2026090313172095800_cit34","doi-asserted-by":"publisher","first-page":"e01260-18","DOI":"10.1128\/JVI.01260-18","article-title":"Differential Mechanisms\nfor the Involvement of Polyamines and Hypusinated EIF5A in Ebola Virus\nGene Expression","volume":"92","author":"Olsen","year":"2018","journal-title":"J. Virol."},{"issue":"8","key":"2026090313172095800_cit35","doi-asserted-by":"publisher","first-page":"e1005800","DOI":"10.1371\/journal.ppat.1005800","article-title":"Single-Molecule\nFISH Reveals Non-Selective Packaging of Rift Valley Fever Virus Genome\nSegments","volume":"12","author":"Wichgers Schreur","year":"2016","journal-title":"PLoS Pathog."},{"issue":"6","key":"2026090313172095800_cit36","doi-asserted-by":"publisher","first-page":"1533","DOI":"10.1099\/0022-1317-68-6-1533","article-title":"Stability of Belladonna Mottle Virus\nParticles: The Role of Polyamines and Calcium","volume":"68","author":"Savithri","year":"1987","journal-title":"J. Gen. Virol."},{"issue":"2","key":"2026090313172095800_cit37","doi-asserted-by":"publisher","first-page":"351","DOI":"10.1016\/0042-6822(83)90089-2","article-title":"Evidence for PH-Induced\nRelease of RNA from Belladonna Mottle Virus and the Stabilizing Effect\nof Polyamines and Cations","volume":"130","author":"Virudachalam","year":"1983","journal-title":"Virology"},{"issue":"2","key":"2026090313172095800_cit38","doi-asserted-by":"publisher","first-page":"254","DOI":"10.1016\/j.molcel.2018.03.015","article-title":"Polyamine Control of Translation\nElongation Regulates Start Site Selection on Antizyme Inhibitor MRNA\nvia Ribosome Queuing","volume":"70","author":"Ivanov","year":"2018","journal-title":"Mol. 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Virol."},{"issue":"1","key":"2026090313172095800_cit43","doi-asserted-by":"publisher","first-page":"222","DOI":"10.1016\/0042-6822(84)90107-7","article-title":"La Crosse\nBunyavirus Can Mediate PH-Dependent Fusion from Without","volume":"132","author":"Gonzalez-Scarano","year":"1984","journal-title":"Virology"},{"issue":"5","key":"2026090313172095800_cit44","doi-asserted-by":"publisher","first-page":"1289","DOI":"10.1128\/JVI.15.5.1289-1292.1975","article-title":"Polyamines in Type 5 Adenovirus-Infected\nCells and Virions","volume":"15","author":"Pett","year":"1975","journal-title":"J. Virol."},{"issue":"1","key":"2026090313172095800_cit45","doi-asserted-by":"publisher","first-page":"408","DOI":"10.1128\/JVI.21.1.408-410.1977","article-title":"Polyamines Contained\nby Two Densonucleosis Viruses","volume":"21","author":"Kelly","year":"1977","journal-title":"J. Virol."},{"issue":"7","key":"2026090313172095800_cit46","doi-asserted-by":"publisher","first-page":"1447","DOI":"10.1016\/j.bpj.2014.02.018","article-title":"PH-Controlled Two-Step Uncoating\nof Influenza Virus","volume":"106","author":"Li","year":"2014","journal-title":"Biophys. J."},{"issue":"23","key":"2026090313172095800_cit47","doi-asserted-by":"publisher","first-page":"12139","DOI":"10.1128\/JVI.00955-09","article-title":"Glycoprotein-Dependent\nAcidification of Vesicular Stomatitis Virus Enhances Release of Matrix\nProtein","volume":"83","author":"Mire","year":"2009","journal-title":"J. Virol."},{"key":"2026090313172095800_cit48","doi-asserted-by":"publisher","first-page":"449","DOI":"10.1007\/978-1-61779-034-8_29","article-title":"Methylated Polyamines as Research\nTools","volume":"720","author":"Khomutov","year":"2011","journal-title":"Methods Mol. Biol."},{"issue":"6","key":"2026090313172095800_cit49","doi-asserted-by":"publisher","first-page":"2933","DOI":"10.1128\/JVI.80.6.2933-2940.2006","article-title":"Rescue of Infectious Rift Valley Fever Virus Entirely\nfrom CDNA, Analysis of Virus Lacking the NSs Gene, and Expression\nof a Foreign Gene","volume":"80","author":"Ikegami","year":"2006","journal-title":"J. Virol."},{"key":"2026090313172095800_cit50","doi-asserted-by":"publisher","first-page":"131","DOI":"10.1385\/0-89603-448-8:131","article-title":"Thin-Layer Chromatographic Method\nfor Assaying Polyamines","volume":"79","author":"Madhubala","year":"1997","journal-title":"Methods Mol. Biol.\nClifton NJ."},{"issue":"10","key":"2026090313172095800_cit51","doi-asserted-by":"publisher","first-page":"2620","DOI":"10.1016\/j.celrep.2019.07.099","article-title":"Ribavirin Induces Polyamine Depletion\nvia Nucleotide Depletion to Limit Virus Replication","volume":"28","author":"Tate","year":"2019","journal-title":"Cell Rep."}],"container-title":["ACS Infectious Diseases"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/pubs.acs.org\/doi\/pdf\/10.1021\/acsinfecdis.0c00402","content-type":"application\/pdf","content-version":"vor","intended-application":"unspecified"},{"URL":"https:\/\/pubs.acs.org\/aidcbc\/article-pdf\/6\/9\/2490\/67303671\/acsinfecdis.0c00402.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/pubs.acs.org\/aidcbc\/article-pdf\/6\/9\/2490\/67303671\/acsinfecdis.0c00402.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,9,3]],"date-time":"2026-09-03T17:17:29Z","timestamp":1788455849000},"score":1,"resource":{"primary":{"URL":"https:\/\/pubs.acs.org\/aidcbc\/article\/6\/9\/2490\/1292438\/Virion-Associated-Polyamines-Transmit-with"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,7,20]]},"references-count":51,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2020,7,20]]},"published-print":{"date-parts":[[2020,9,11]]}},"URL":"https:\/\/doi.org\/10.1021\/acsinfecdis.0c00402","relation":{},"ISSN":["2373-8227"],"issn-type":[{"value":"2373-8227","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,7,20]]}}}