{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,20]],"date-time":"2026-09-20T12:03:19Z","timestamp":1789905799827,"version":"4.0.1"},"reference-count":72,"publisher":"American Society for Microbiology","issue":"16","license":[{"start":{"date-parts":[[2018,8,15]],"date-time":"2018-08-15T00:00:00Z","timestamp":1534291200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/journals.asm.org\/non-commercial-tdm-license"}],"funder":[{"name":"ANR Labex ECOFECT"},{"DOI":"10.13039\/501100004099","name":"La Ligue Contre le Cancer","doi-asserted-by":"crossref","id":[{"id":"10.13039\/501100004099","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100001711","name":"Swiss National Science Foundation","doi-asserted-by":"crossref","award":["310030-149626"],"award-info":[{"award-number":["310030-149626"]}],"id":[{"id":"10.13039\/501100001711","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100011723","name":"Canton of Geneva","doi-asserted-by":"crossref","id":[{"id":"10.13039\/501100011723","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/100001117","name":"amfAR, The Foundation for AIDS Research","doi-asserted-by":"publisher","award":["109140-58-RKHF"],"award-info":[{"award-number":["109140-58-RKHF"]}],"id":[{"id":"10.13039\/100001117","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100002915","name":"Fondation pour la Recherche M\u00e9dicale","doi-asserted-by":"publisher","award":["ING20160435028"],"award-info":[{"award-number":["ING20160435028"]}],"id":[{"id":"10.13039\/501100002915","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100003323","name":"Agence Nationale de Recherches sur le Sida et les H\u00e9patites Virales","doi-asserted-by":"publisher","award":["ECTZ19143"],"award-info":[{"award-number":["ECTZ19143"]}],"id":[{"id":"10.13039\/501100003323","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100008656","name":"Fondation Innovations en Infectiologie","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100008656","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["journals.asm.org"],"crossmark-restriction":true},"short-container-title":["J Virol"],"published-print":{"date-parts":[[2018,8,15]]},"abstract":"<jats:p>Infection with hepatitis B virus (HBV) led to 887,000 human deaths in 2015. HBV has been coevolving with mammals for millions of years. Recently, the Smc5\/6 complex, which has essential housekeeping functions, was identified as a restriction factor of human HBV antagonized by the regulatory HBx protein. Here we address whether the antiviral activity of Smc5\/6 is an important evolutionarily conserved function. We found that all six subunits of Smc5\/6 have been conserved in primates, with only Smc6 showing signatures of an \u201cevolutionary arms race.\u201d Using evolution-guided functional analyses that included infections of primary human hepatocytes, we demonstrated that HBx proteins from very divergent mammalian HBVs could all efficiently antagonize Smc5\/6, independently of the host species and sites under positive selection. These findings show that Smc5\/6 antiviral activity against HBV is an important function in mammals. They also raise the intriguing possibility that Smc5\/6 may restrict other, yet-unidentified viruses.<\/jats:p>","DOI":"10.1128\/jvi.00769-18","type":"journal-article","created":{"date-parts":[[2018,5,28]],"date-time":"2018-05-28T06:14:22Z","timestamp":1527488062000},"update-policy":"https:\/\/doi.org\/10.1128\/asmj-crossmark-policy-page","source":"Crossref","is-referenced-by-count":46,"title":["Smc5\/6 Antagonism by HBx Is an Evolutionarily Conserved Function of Hepatitis B Virus Infection in Mammals"],"prefix":"10.1128","volume":"92","author":[{"given":"Fabien","family":"Abdul","sequence":"first","affiliation":[{"name":"Department of Microbiology and Molecular Medicine, University Medical Centre (CMU)\/University of Geneva, Geneva, Switzerland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fabien","family":"Filleton","sequence":"additional","affiliation":[{"name":"CIRI\u2014International Center for Infectiology Research, Inserm, U1111, Universit\u00e9 Claude Bernard Lyon 1, CNRS, UMR5308, Ecole Normale Sup\u00e9rieure de Lyon, Universit\u00e9 Lyon, Lyon, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Laetitia","family":"Gerossier","sequence":"additional","affiliation":[{"name":"CRCL-UMR Inserm 1052-CNRS 5286, Lyon, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alexia","family":"Paturel","sequence":"additional","affiliation":[{"name":"CRCL-UMR Inserm 1052-CNRS 5286, Lyon, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Janet","family":"Hall","sequence":"additional","affiliation":[{"name":"CRCL-UMR Inserm 1052-CNRS 5286, Lyon, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michel","family":"Strubin","sequence":"additional","affiliation":[{"name":"Department of Microbiology and Molecular Medicine, University Medical Centre (CMU)\/University of Geneva, Geneva, Switzerland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8585-7534","authenticated-orcid":false,"given":"Lucie","family":"Etienne","sequence":"additional","affiliation":[{"name":"CIRI\u2014International Center for Infectiology Research, Inserm, U1111, Universit\u00e9 Claude Bernard Lyon 1, CNRS, UMR5308, Ecole Normale Sup\u00e9rieure de Lyon, Universit\u00e9 Lyon, Lyon, France"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"235","reference":[{"key":"e_1_3_2_2_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pgen.1004559"},{"key":"e_1_3_2_3_2","doi-asserted-by":"publisher","DOI":"10.1128\/JVI.00832-16"},{"key":"e_1_3_2_4_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.chom.2017.07.019"},{"key":"e_1_3_2_5_2","doi-asserted-by":"publisher","DOI":"10.1517\/14728222.2014.867947"},{"key":"e_1_3_2_6_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0065-230X(09)03004-8"},{"key":"e_1_3_2_7_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.jhep.2011.02.015"},{"key":"e_1_3_2_8_2","doi-asserted-by":"publisher","DOI":"10.1038\/nature17170"},{"key":"e_1_3_2_9_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.celrep.2016.08.026"},{"key":"e_1_3_2_10_2","doi-asserted-by":"publisher","DOI":"10.1093\/molbev\/msh023"},{"key":"e_1_3_2_11_2","doi-asserted-by":"publisher","DOI":"10.1038\/nrm.2016.30"},{"key":"e_1_3_2_12_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.tcb.2016.04.002"},{"key":"e_1_3_2_13_2","doi-asserted-by":"publisher","DOI":"10.1038\/ncb0405-329"},{"key":"e_1_3_2_14_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.molcel.2015.10.023"},{"key":"e_1_3_2_15_2","doi-asserted-by":"publisher","DOI":"10.1101\/sqb.2010.75.047"},{"key":"e_1_3_2_16_2","doi-asserted-by":"publisher","DOI":"10.1080\/15384101.2015.1137713"},{"key":"e_1_3_2_17_2","doi-asserted-by":"publisher","DOI":"10.1242\/dev.145607"},{"key":"e_1_3_2_18_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0169648"},{"key":"e_1_3_2_19_2","doi-asserted-by":"publisher","DOI":"10.1038\/nri3295"},{"key":"e_1_3_2_20_2","first-page":"123","article-title":"Rapid adversarial co-evolution of viruses and cellular restriction factors","volume":"371","author":"Johnson WE","year":"2013","unstructured":"Johnson WE. 2013. Rapid adversarial co-evolution of viruses and cellular restriction factors. Curr Top Microbiol Immunol 371:123\u2013151.","journal-title":"Curr Top Microbiol Immunol"},{"key":"e_1_3_2_21_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.0409853102"},{"key":"e_1_3_2_22_2","doi-asserted-by":"publisher","DOI":"10.1146\/annurev-genet-110711-155522"},{"key":"e_1_3_2_23_2","doi-asserted-by":"publisher","DOI":"10.1128\/JVI.00468-10"},{"key":"e_1_3_2_24_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.1000429"},{"key":"e_1_3_2_25_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.chom.2009.10.004"},{"key":"e_1_3_2_26_2","doi-asserted-by":"crossref","unstructured":"Filleton F Abdul F Gerossier L Paturel A Hall J Strubin M Etienne L. 1 December 2017. Smc5\/6-antagonism by HBx is an evolutionary-conserved function of hepatitis B virus infection in mammals. bioRxiv doi:10.1101\/202671.","DOI":"10.1101\/202671"},{"key":"e_1_3_2_27_2","doi-asserted-by":"publisher","DOI":"10.1093\/molbev\/msu399"},{"key":"e_1_3_2_28_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pgen.1001342"},{"key":"e_1_3_2_29_2","doi-asserted-by":"publisher","DOI":"10.1093\/molbev\/msl051"},{"key":"e_1_3_2_30_2","doi-asserted-by":"publisher","DOI":"10.1093\/molbev\/msv035"},{"key":"e_1_3_2_31_2","doi-asserted-by":"publisher","DOI":"10.1093\/bioinformatics\/btl427"},{"key":"e_1_3_2_32_2","doi-asserted-by":"publisher","DOI":"10.1093\/molbev\/msm088"},{"key":"e_1_3_2_33_2","doi-asserted-by":"publisher","DOI":"10.1093\/molbev\/mst097"},{"key":"e_1_3_2_34_2","doi-asserted-by":"crossref","unstructured":"Gueguen L Duret L. 6 April 2017. Unbiased estimate of synonymous and non-synonymous substitution rates with non-stationary base composition. bioRxiv doi:10.1101\/124925.","DOI":"10.1101\/124925"},{"key":"e_1_3_2_35_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pbio.1001571"},{"key":"e_1_3_2_36_2","doi-asserted-by":"publisher","DOI":"10.7554\/eLife.11785"},{"key":"e_1_3_2_37_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.chom.2016.07.003"},{"key":"e_1_3_2_38_2","doi-asserted-by":"publisher","DOI":"10.7554\/eLife.12469"},{"key":"e_1_3_2_39_2","doi-asserted-by":"publisher","DOI":"10.1093\/molbev\/msi097"},{"key":"e_1_3_2_40_2","doi-asserted-by":"publisher","DOI":"10.1093\/molbev\/msr125"},{"key":"e_1_3_2_41_2","doi-asserted-by":"publisher","DOI":"10.1007\/978-1-4614-9610-6_373-1"},{"key":"e_1_3_2_42_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.cell.2015.10.019"},{"key":"e_1_3_2_43_2","doi-asserted-by":"publisher","DOI":"10.1101\/cshperspect.a006940"},{"key":"e_1_3_2_44_2","doi-asserted-by":"publisher","DOI":"10.1038\/nature15400"},{"key":"e_1_3_2_45_2","doi-asserted-by":"publisher","DOI":"10.1038\/nature15399"},{"key":"e_1_3_2_46_2","doi-asserted-by":"publisher","DOI":"10.1128\/JVI.00972-16"},{"key":"e_1_3_2_47_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.chom.2016.08.004"},{"key":"e_1_3_2_48_2","doi-asserted-by":"publisher","DOI":"10.1038\/nature10719"},{"key":"e_1_3_2_49_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.celrep.2015.10.067"},{"key":"e_1_3_2_50_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.celrep.2015.10.068"},{"key":"e_1_3_2_51_2","doi-asserted-by":"publisher","DOI":"10.1002\/hep.29112"},{"key":"e_1_3_2_52_2","doi-asserted-by":"publisher","DOI":"10.1128\/JVI.75.23.11565-11572.2001"},{"key":"e_1_3_2_53_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1308049110"},{"key":"e_1_3_2_54_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.coviro.2012.07.003"},{"key":"e_1_3_2_55_2","doi-asserted-by":"publisher","DOI":"10.7554\/eLife.00049"},{"key":"e_1_3_2_56_2","doi-asserted-by":"publisher","DOI":"10.1128\/JVI.01278-15"},{"key":"e_1_3_2_57_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.1006215"},{"key":"e_1_3_2_58_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.1005304"},{"key":"e_1_3_2_59_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.mib.2013.04.005"},{"key":"e_1_3_2_60_2","doi-asserted-by":"publisher","DOI":"10.1038\/nature07529"},{"key":"e_1_3_2_61_2","doi-asserted-by":"publisher","DOI":"10.1002\/hep.25928"},{"key":"e_1_3_2_62_2","doi-asserted-by":"publisher","DOI":"10.1006\/viro.2001.1036"},{"key":"e_1_3_2_63_2","doi-asserted-by":"publisher","DOI":"10.1128\/JVI.79.7.4238-4245.2005"},{"key":"e_1_3_2_64_2","doi-asserted-by":"publisher","DOI":"10.1038\/nature02777"},{"key":"e_1_3_2_65_2","doi-asserted-by":"publisher","DOI":"10.1091\/mbc.12.6.1583"},{"key":"e_1_3_2_66_2","doi-asserted-by":"publisher","DOI":"10.1006\/viro.1993.1069"},{"key":"e_1_3_2_67_2","doi-asserted-by":"publisher","DOI":"10.1136\/gutjnl-2016-312162"},{"key":"e_1_3_2_68_2","doi-asserted-by":"publisher","DOI":"10.1093\/nar\/gkh340"},{"key":"e_1_3_2_69_2","doi-asserted-by":"publisher","DOI":"10.1093\/bioinformatics\/bti079"},{"key":"e_1_3_2_70_2","doi-asserted-by":"publisher","DOI":"10.1093\/sysbio\/syq010"},{"key":"e_1_3_2_71_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pgen.1002764"},{"key":"e_1_3_2_72_2","doi-asserted-by":"publisher","DOI":"10.1093\/molbev\/mst030"},{"key":"e_1_3_2_73_2","doi-asserted-by":"publisher","DOI":"10.1038\/nsmb.1719"}],"container-title":["Journal of Virology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/journals.asm.org\/doi\/pdf\/10.1128\/JVI.00769-18","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/journals.asm.org\/doi\/pdf\/10.1128\/JVI.00769-18","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,3,5]],"date-time":"2022-03-05T09:37:18Z","timestamp":1646473038000},"score":1,"resource":{"primary":{"URL":"https:\/\/journals.asm.org\/doi\/10.1128\/JVI.00769-18"}},"subtitle":[],"editor":[{"given":"J.-H. James","family":"Ou","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2018,8,15]]},"references-count":72,"journal-issue":{"issue":"16","published-print":{"date-parts":[[2018,8,15]]}},"alternative-id":["10.1128\/JVI.00769-18"],"URL":"https:\/\/doi.org\/10.1128\/jvi.00769-18","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/202671","asserted-by":"object"}]},"ISSN":["0022-538X","1098-5514"],"issn-type":[{"value":"0022-538X","type":"print"},{"value":"1098-5514","type":"electronic"}],"subject":[],"published":{"date-parts":[[2018,8,15]]},"assertion":[{"value":"2018-05-08","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2018-05-09","order":1,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2018-07-31","order":2,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}],"article-number":"e00769-18"}}