{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,6]],"date-time":"2026-10-06T06:09:00Z","timestamp":1791266940053,"version":"4.1.0"},"update-to":[{"DOI":"10.1371\/journal.ppat.1007176","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2018,7,18]],"date-time":"2018-07-18T00:00:00Z","timestamp":1531872000000}}],"reference-count":109,"publisher":"Public Library of Science (PLoS)","issue":"7","license":[{"start":{"date-parts":[[2018,7,6]],"date-time":"2018-07-06T00:00:00Z","timestamp":1530835200000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100000024","name":"Canadian Institutes of Health Research","doi-asserted-by":"publisher","award":["153014"],"award-info":[{"award-number":["153014"]}],"id":[{"id":"10.13039\/501100000024","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Conacyt","award":["263525"],"award-info":[{"award-number":["263525"]}]}],"content-domain":{"domain":["www.plospathogens.org"],"crossmark-restriction":false},"short-container-title":["PLoS Pathog"],"DOI":"10.1371\/journal.ppat.1007176","type":"journal-article","created":{"date-parts":[[2018,7,6]],"date-time":"2018-07-06T17:59:20Z","timestamp":1530899960000},"page":"e1007176","update-policy":"https:\/\/doi.org\/10.1371\/journal.ppat.corrections_policy","source":"Crossref","is-referenced-by-count":38,"title":["A genome-wide screen of Epstein-Barr virus proteins that modulate host SUMOylation identifies a SUMO E3 ligase conserved in herpesviruses"],"prefix":"10.1371","volume":"14","author":[{"given":"Carlos F.","family":"De La Cruz-Herrera","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kathy","family":"Shire","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Umama Z.","family":"Siddiqi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0110-5472","authenticated-orcid":true,"given":"Lori","family":"Frappier","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2018,7,6]]},"reference":[{"issue":"12","key":"ref1","doi-asserted-by":"crossref","first-page":"779","DOI":"10.1016\/j.tibs.2015.09.006","article-title":"SUMOylation-Mediated Regulation of Cell Cycle Progression and Cancer","volume":"40","author":"K Eifler","year":"2015","journal-title":"Trends Biochem Sci"},{"key":"ref2","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1146\/annurev-biochem-061909-093311","article-title":"Sumoylation: a regulatory protein modification in health and disease","volume":"82","author":"A Flotho","year":"2013","journal-title":"Annu Rev Biochem"},{"issue":"7","key":"ref3","doi-asserted-by":"crossref","first-page":"1542","DOI":"10.1158\/0008-5472.CAN-16-2958","article-title":"The Role of PIAS SUMO E3-Ligases in Cancer","volume":"77","author":"A Rabellino","year":"2017","journal-title":"Cancer Res"},{"issue":"3","key":"ref4","doi-asserted-by":"crossref","first-page":"184","DOI":"10.1038\/nrc.2016.143","article-title":"SUMO and the robustness of cancer","volume":"17","author":"JS Seeler","year":"2017","journal-title":"Nat Rev Cancer"},{"key":"ref5","doi-asserted-by":"crossref","first-page":"4234","DOI":"10.1038\/ncomms5234","article-title":"SUMO1 modification stabilizes CDK6 protein and drives the cell cycle and glioblastoma progression","volume":"5","author":"AC Bellail","year":"2014","journal-title":"Nat Commun"},{"issue":"1","key":"ref6","doi-asserted-by":"crossref","first-page":"70","DOI":"10.1111\/cas.12047","article-title":"Small ubiquitin-like modifier 1\u20133 conjugation [corrected] is activated in human astrocytic brain tumors and is required for glioblastoma cell survival","volume":"104","author":"W Yang","year":"2013","journal-title":"Cancer Sci"},{"issue":"13","key":"ref7","doi-asserted-by":"crossref","first-page":"2081","DOI":"10.1182\/blood-2014-06-584524","article-title":"Myc-induced SUMOylation is a therapeutic vulnerability for B-cell lymphoma","volume":"124","author":"A Hoellein","year":"2014","journal-title":"Blood"},{"issue":"1","key":"ref8","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1002\/iub.1240","article-title":"SUMO Ubc9 enzyme as a viral target","volume":"66","author":"A Varadaraj","year":"2014","journal-title":"IUBMB Life"},{"issue":"1\u20132","key":"ref9","doi-asserted-by":"crossref","first-page":"199","DOI":"10.1016\/j.virusres.2011.04.001","article-title":"HPV E6 proteins target Ubc9, the SUMO conjugating enzyme","volume":"158","author":"PR Heaton","year":"2011","journal-title":"Virus Res"},{"issue":"23","key":"ref10","doi-asserted-by":"crossref","first-page":"12210","DOI":"10.1128\/JVI.01442-10","article-title":"Adenovirus E1B 55-kilodalton protein is a p53-SUMO1 E3 ligase that represses p53 and stimulates its nuclear export through interactions with promyelocytic leukemia nuclear bodies","volume":"84","author":"MA Pennella","year":"2010","journal-title":"J Virol"},{"issue":"6","key":"ref11","doi-asserted-by":"crossref","first-page":"754","DOI":"10.4161\/cc.7.6.5495","article-title":"The adenovirus E1B-55K oncoprotein induces SUMO modification of p53","volume":"7","author":"S Muller","year":"2008","journal-title":"Cell Cycle"},{"issue":"24","key":"ref12","doi-asserted-by":"crossref","first-page":"6725","DOI":"10.1073\/pnas.1603872113","article-title":"The adenovirus E4-ORF3 protein functions as a SUMO E3 ligase for TIF-1gamma sumoylation and poly-SUMO chain elongation","volume":"113","author":"SY Sohn","year":"2016","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"8","key":"ref13","doi-asserted-by":"crossref","first-page":"5266","DOI":"10.1074\/jbc.M109.088088","article-title":"Kaposi&apos;s sarcoma-associated herpesvirus (KSHV) encodes a SUMO E3 ligase that is SIM-dependent and SUMO-2\/3-specific","volume":"285","author":"PC Chang","year":"2010","journal-title":"J Biol Chem"},{"issue":"9","key":"ref14","doi-asserted-by":"crossref","first-page":"4854","DOI":"10.3390\/v7092849","article-title":"Viral Mimicry to Usurp Ubiquitin and SUMO Host Pathways","volume":"7","author":"P Wimmer","year":"2015","journal-title":"Viruses"},{"issue":"8","key":"ref15","doi-asserted-by":"crossref","first-page":"e1003506","DOI":"10.1371\/journal.ppat.1003506","article-title":"Kaposi&apos;s sarcoma-associated herpesvirus K-Rta exhibits SUMO-targeting ubiquitin ligase (STUbL) like activity and is essential for viral reactivation","volume":"9","author":"Y Izumiya","year":"2013","journal-title":"PLoS Pathog"},{"issue":"Pt 3","key":"ref16","doi-asserted-by":"crossref","first-page":"465","DOI":"10.1099\/vir.0.048900-0","article-title":"Regulation of alphaherpesvirus infections by the ICP0 family of proteins","volume":"94","author":"C Boutell","year":"2013","journal-title":"J Gen Virol"},{"issue":"1","key":"ref17","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1016\/j.bbamcr.2013.08.022","article-title":"SUMO-targeted ubiquitin ligases","volume":"1843","author":"AM Sriramachandran","year":"2014","journal-title":"Biochim Biophys Acta"},{"issue":"4","key":"ref18","doi-asserted-by":"crossref","first-page":"1930","DOI":"10.1128\/JVI.06127-11","article-title":"Murine gammaherpesvirus 68 evades host cytokine production via replication transactivator-induced RelA degradation","volume":"86","author":"X Dong","year":"2012","journal-title":"J Virol"},{"issue":"9","key":"ref19","doi-asserted-by":"crossref","first-page":"e1002245","DOI":"10.1371\/journal.ppat.1002245","article-title":"A viral ubiquitin ligase has substrate preferential SUMO targeted ubiquitin ligase activity that counteracts intrinsic antiviral defence","volume":"7","author":"C Boutell","year":"2011","journal-title":"PLoS Pathog"},{"issue":"5","key":"ref20","doi-asserted-by":"crossref","first-page":"538","DOI":"10.1038\/ncb1716","article-title":"RNF4 is a poly-SUMO-specific E3 ubiquitin ligase required for arsenic-induced PML degradation","volume":"10","author":"MH Tatham","year":"2008","journal-title":"Nat Cell Biol"},{"issue":"8","key":"ref21","doi-asserted-by":"crossref","first-page":"e1002157","DOI":"10.1371\/journal.ppat.1002157","article-title":"Disruption of PML nuclear bodies is mediated by ORF61 SUMO-interacting motifs and required for varicella-zoster virus pathogenesis in skin","volume":"7","author":"L Wang","year":"2011","journal-title":"PLoS Pathog"},{"issue":"3","key":"ref22","doi-asserted-by":"crossref","first-page":"1240","DOI":"10.3390\/v1031240","article-title":"Interplay between Herpesvirus Infection and Host Defense by PML Nuclear Bodies","volume":"1","author":"N Tavalai","year":"2009","journal-title":"Viruses"},{"issue":"4","key":"ref23","doi-asserted-by":"crossref","first-page":"1905","DOI":"10.3390\/cancers6041905","article-title":"SUMO and KSHV Replication","volume":"6","author":"PC Chang","year":"2014","journal-title":"Cancers (Basel)"},{"issue":"12","key":"ref24","doi-asserted-by":"crossref","first-page":"1358","DOI":"10.1136\/jcp.2006.044586","article-title":"Epstein Barr virus-associated tumours: an update for the attention of the working pathologist","volume":"60","author":"HJ Delecluse","year":"2007","journal-title":"J Clin Pathol"},{"issue":"5","key":"ref25","doi-asserted-by":"crossref","first-page":"255","DOI":"10.1136\/mp.53.5.255","article-title":"Epstein-Barr virus and gastric carcinoma","volume":"53","author":"K Takada","year":"2000","journal-title":"Mol Pathol"},{"issue":"6","key":"ref26","doi-asserted-by":"crossref","first-page":"431","DOI":"10.1016\/S1044579X0200086X","article-title":"Epstein-Barr virus in the pathogenesis of NPC","volume":"12","author":"N Raab-Traub","year":"2002","journal-title":"Semin Cancer Biol"},{"key":"ref27","doi-asserted-by":"crossref","DOI":"10.1007\/978-3-319-38882-3_13","article-title":"Manipulation of PML Nuclear Bodies and DNA Damage Responses by DNA Viruses: The Functional Nucleus","author":"L Frappier","year":"2016"},{"issue":"8","key":"ref28","doi-asserted-by":"crossref","first-page":"4480","DOI":"10.1128\/JVI.00059-14","article-title":"Identification of herpesvirus proteins that contribute to G1\/S arrest","volume":"88","author":"P Paladino","year":"2014","journal-title":"J Virol"},{"issue":"22","key":"ref29","doi-asserted-by":"crossref","first-page":"12251","DOI":"10.1128\/JVI.01407-12","article-title":"Epstein-Barr virus latent membrane protein 1 regulates the function of interferon regulatory factor 7 by inducing its sumoylation","volume":"86","author":"GL Bentz","year":"2012","journal-title":"J Virol"},{"issue":"19","key":"ref30","doi-asserted-by":"crossref","first-page":"10144","DOI":"10.1128\/JVI.05035-11","article-title":"Epstein-Barr virus latent membrane protein 1 (LMP1) C-terminal-activating region 3 contributes to LMP1-mediated cellular migration via its interaction with Ubc9","volume":"85","author":"GL Bentz","year":"2011","journal-title":"J Virol"},{"issue":"15","key":"ref31","doi-asserted-by":"crossref","first-page":"7465","DOI":"10.1128\/JVI.00711-15","article-title":"LMP1-Induced Sumoylation Influences the Maintenance of Epstein-Barr Virus Latency through KAP1","volume":"89","author":"GL Bentz","year":"2015","journal-title":"J Virol"},{"issue":"4","key":"ref32","doi-asserted-by":"crossref","first-page":"e1006338","DOI":"10.1371\/journal.ppat.1006338","article-title":"The Epstein-Barr virus miR-BHRF1-1 targets RNF4 during productive infection to promote the accumulation of SUMO conjugates and the release of infectious virus","volume":"13","author":"J Li","year":"2017","journal-title":"PLoS Pathog"},{"issue":"7","key":"ref33","doi-asserted-by":"crossref","first-page":"e1000100","DOI":"10.1371\/journal.ppat.1000100","article-title":"Genome-wide screen of three herpesviruses for protein subcellular localization and alteration of PML nuclear bodies","volume":"4","author":"J Salsman","year":"2008","journal-title":"PLoS Pathog"},{"key":"ref34","article-title":"A Screen for Epstein-Barr Virus Proteins that Inhibit the DNA Damage Response Reveals a Novel Histone Binding Protein","author":"T-H Ho","year":"2018","journal-title":"J Virol"},{"issue":"1","key":"ref35","doi-asserted-by":"crossref","first-page":"1809","DOI":"10.1038\/s41467-017-01900-x","article-title":"The STUbL RNF4 regulates protein group SUMOylation by targeting the SUMO conjugation machinery","volume":"8","author":"R Kumar","year":"2017","journal-title":"Nat Commun"},{"issue":"1","key":"ref36","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1016\/S0092-8674(01)00633-X","article-title":"The nucleoporin RanBP2 has SUMO1 E3 ligase activity","volume":"108","author":"A Pichler","year":"2002","journal-title":"Cell"},{"issue":"12","key":"ref37","doi-asserted-by":"crossref","first-page":"5577","DOI":"10.1128\/MCB.24.12.5577-5586.2004","article-title":"Protein inhibitor of activated STAT Y (PIASy) and a splice variant lacking exon 6 enhance sumoylation but are not essential for embryogenesis and adult life","volume":"24","author":"KA Wong","year":"2004","journal-title":"Mol Cell Biol"},{"issue":"12","key":"ref38","doi-asserted-by":"crossref","first-page":"2298","DOI":"10.1074\/mcp.M600212-MCP200","article-title":"Distinct and overlapping sets of SUMO-1 and SUMO-2 target proteins revealed by quantitative proteomics","volume":"5","author":"AC Vertegaal","year":"2006","journal-title":"Mol Cell Proteomics"},{"issue":"18","key":"ref39","doi-asserted-by":"crossref","first-page":"12866","DOI":"10.1074\/jbc.M112.413393","article-title":"Role of RNF4 in the ubiquitination of Rta of Epstein-Barr virus","volume":"288","author":"YC Yang","year":"2013","journal-title":"J Biol Chem"},{"issue":"1","key":"ref40","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1016\/j.immuni.2004.11.011","article-title":"The KSHV immediate-early transcription factor RTA encodes ubiquitin E3 ligase activity that targets IRF7 for proteosome-mediated degradation","volume":"22","author":"Y Yu","year":"2005","journal-title":"Immunity"},{"issue":"2","key":"ref41","doi-asserted-by":"crossref","first-page":"438","DOI":"10.3390\/cells3020438","article-title":"HSV-1 ICP0: An E3 Ubiquitin Ligase That Counteracts Host Intrinsic and Innate Immunity","volume":"3","author":"MP Lanfranca","year":"2014","journal-title":"Cells"},{"issue":"1","key":"ref42","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1089\/jir.2010.0111","article-title":"Role of promyelocytic leukemia protein in host antiviral defense","volume":"31","author":"MC Geoffroy","year":"2011","journal-title":"J Interferon Cytokine Res"},{"issue":"49","key":"ref43","doi-asserted-by":"crossref","first-page":"7266","DOI":"10.1038\/sj.onc.1204759","article-title":"DNA viruses and viral proteins that interact with PML nuclear bodies","volume":"20","author":"RD Everett","year":"2001","journal-title":"Oncogene"},{"issue":"20","key":"ref44","doi-asserted-by":"crossref","first-page":"11209","DOI":"10.1128\/JVI.01145-12","article-title":"Herpes simplex virus 1 ubiquitin ligase ICP0 interacts with PML isoform I and induces its SUMO-independent degradation","volume":"86","author":"D Cuchet-Lourenco","year":"2012","journal-title":"J Virol"},{"issue":"8","key":"ref45","doi-asserted-by":"crossref","first-page":"4058","DOI":"10.1128\/JVI.02665-06","article-title":"Multiple roles of Epstein-Barr virus SM protein in lytic replication","volume":"81","author":"Z Han","year":"2007","journal-title":"J Virol"},{"issue":"22","key":"ref46","doi-asserted-by":"crossref","first-page":"11781","DOI":"10.1128\/JVI.01359-10","article-title":"Epstein-Barr Virus SM protein utilizes cellular splicing factor SRp20 to mediate alternative splicing","volume":"84","author":"D Verma","year":"2010","journal-title":"J Virol"},{"issue":"17","key":"ref47","doi-asserted-by":"crossref","first-page":"9412","DOI":"10.1128\/JVI.78.17.9412-9422.2004","article-title":"Epstein-Barr virus (EBV) SM protein induces and recruits cellular Sp110b to stabilize mRNAs and enhance EBV lytic gene expression","volume":"78","author":"J Nicewonger","year":"2004","journal-title":"J Virol"},{"issue":"14","key":"ref48","doi-asserted-by":"crossref","first-page":"7180","DOI":"10.1128\/JVI.00344-08","article-title":"Epstein-Barr virus SM protein functions as an alternative splicing factor","volume":"82","author":"D Verma","year":"2008","journal-title":"J Virol"},{"issue":"1","key":"ref49","doi-asserted-by":"crossref","first-page":"335","DOI":"10.1074\/jbc.M208656200","article-title":"A novel nuclear export signal and a REF interaction domain both promote mRNA export by the Epstein-Barr virus EB2 protein","volume":"278","author":"E Hiriart","year":"2003","journal-title":"J Biol Chem"},{"key":"ref50","doi-asserted-by":"crossref","first-page":"2939","DOI":"10.2741\/2899","article-title":"The human cytomegalovirus regulatory protein UL69 and its effect on mRNA export","volume":"13","author":"Z Toth","year":"2008","journal-title":"Front Biosci"},{"issue":"11","key":"ref51","doi-asserted-by":"crossref","first-page":"1261","DOI":"10.2217\/fmb.11.119","article-title":"The many roles of the highly interactive HSV protein ICP27, a key regulator of infection","volume":"6","author":"RM Sandri-Goldin","year":"2011","journal-title":"Future Microbiol"},{"issue":"5","key":"ref52","doi-asserted-by":"crossref","first-page":"651","DOI":"10.1038\/sj.onc.1202062","article-title":"Characterization of the oligomerization defects of two p53 mutants found in families with Li-Fraumeni and Li-Fraumeni-like syndrome","volume":"17","author":"TS Davison","year":"1998","journal-title":"Oncogene"},{"issue":"7","key":"ref53","doi-asserted-by":"crossref","first-page":"445","DOI":"10.4161\/epi.4.7.10030","article-title":"p53 sumoylation: mechanistic insights from reconstitution studies","volume":"4","author":"SY Wu","year":"2009","journal-title":"Epigenetics"},{"issue":"2","key":"ref54","doi-asserted-by":"crossref","first-page":"140","DOI":"10.1016\/j.virol.2013.02.014","article-title":"Murine gammaherpesvirus 68 ORF75c contains ubiquitin E3 ligase activity and requires PML SUMOylation but not other known cellular PML regulators, CK2 and E6AP, to mediate PML degradation","volume":"440","author":"J Sewatanon","year":"2013","journal-title":"Virology"},{"issue":"6","key":"ref55","doi-asserted-by":"crossref","first-page":"4599","DOI":"10.1128\/JVI.71.6.4599-4613.1997","article-title":"The major immediate-early proteins IE1 and IE2 of human cytomegalovirus colocalize with and disrupt PML-associated nuclear bodies at very early times in infected permissive cells","volume":"71","author":"JH Ahn","year":"1997","journal-title":"J Virol"},{"issue":"12","key":"ref56","doi-asserted-by":"crossref","first-page":"6527","DOI":"10.1128\/JVI.78.12.6527-6542.2004","article-title":"Ability of the human cytomegalovirus IE1 protein to modulate sumoylation of PML correlates with its functional activities in transcriptional regulation and infectivity in cultured fibroblast cells","volume":"78","author":"HR Lee","year":"2004","journal-title":"J Virol"},{"issue":"5","key":"ref57","doi-asserted-by":"crossref","first-page":"2388","DOI":"10.1128\/JVI.75.5.2388-2399.2001","article-title":"Epstein-Barr virus immediate-early protein BZLF1 is SUMO-1 modified and disrupts promyelocytic leukemia bodies","volume":"75","author":"AL Adamson","year":"2001","journal-title":"J Virol"},{"issue":"2","key":"ref58","doi-asserted-by":"crossref","first-page":"335","DOI":"10.1006\/viro.1999.0147","article-title":"Herpes simplex virus type 1 infection imposes a G(1)\/S block in asynchronously growing cells and prevents G(1) entry in quiescent cells","volume":"267","author":"GL Ehmann","year":"2000","journal-title":"Virology"},{"issue":"2","key":"ref59","doi-asserted-by":"crossref","first-page":"1629","DOI":"10.1128\/JVI.71.2.1629-1634.1997","article-title":"Human cytomegalovirus infection inhibits G1\/S transition","volume":"71","author":"D Dittmer","year":"1997","journal-title":"J Virol"},{"issue":"12","key":"ref60","doi-asserted-by":"crossref","first-page":"8850","DOI":"10.1128\/JVI.70.12.8850-8857.1996","article-title":"Human cytomegalovirus infection inhibits cell cycle progression at multiple points, including the transition from G1 to S","volume":"70","author":"M Lu","year":"1996","journal-title":"J Virol"},{"issue":"10","key":"ref61","doi-asserted-by":"crossref","first-page":"4482","DOI":"10.1128\/JVI.75.10.4482-4489.2001","article-title":"Cell cycle analysis of Epstein-Barr virus-infected cells following treatment with lytic cycle-inducing agents","volume":"75","author":"A Rodriguez","year":"2001","journal-title":"J Virol"},{"issue":"4","key":"ref62","doi-asserted-by":"crossref","first-page":"383","DOI":"10.2217\/fvl.15.18","article-title":"HSV-I and the cellular DNA damage response","volume":"10","author":"S Smith","year":"2015","journal-title":"Future Virol"},{"issue":"6","key":"ref63","doi-asserted-by":"crossref","first-page":"e1002084","DOI":"10.1371\/journal.ppat.1002084","article-title":"The intrinsic antiviral defense to incoming HSV-1 genomes includes specific DNA repair proteins and is counteracted by the viral protein ICP0","volume":"7","author":"CE Lilley","year":"2011","journal-title":"PLoS Pathog"},{"issue":"5","key":"ref64","doi-asserted-by":"crossref","first-page":"2155","DOI":"10.3390\/v6052155","article-title":"The DNA damage response induced by infection with human cytomegalovirus and other viruses","volume":"6","author":"E Xiaofei","year":"2014","journal-title":"Viruses"},{"key":"ref65","article-title":"A Screen for Epstein-Barr Virus Proteins that Inhibit the DNA Damage Response Reveals a Novel Histone Binding Protein","author":"TH Ho","year":"2018","journal-title":"J Virol"},{"issue":"5","key":"ref66","doi-asserted-by":"crossref","first-page":"e37636","DOI":"10.1371\/journal.pone.0037636","article-title":"NF-kappaB repression by PIAS3 mediated RelA SUMOylation","volume":"7","author":"Y Liu","year":"2012","journal-title":"PLoS ONE"},{"issue":"37","key":"ref67","doi-asserted-by":"crossref","first-page":"38803","DOI":"10.1074\/jbc.M405470200","article-title":"Post-translational modification of Rta of Epstein-Barr virus by SUMO-1","volume":"279","author":"LK Chang","year":"2004","journal-title":"J Biol Chem"},{"issue":"2","key":"ref68","doi-asserted-by":"crossref","first-page":"231","DOI":"10.1016\/j.jmb.2008.04.011","article-title":"Enhancement of transactivation activity of Rta of Epstein-Barr virus by RanBPM","volume":"379","author":"LK Chang","year":"2008","journal-title":"J Mol Biol"},{"issue":"1","key":"ref69","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1016\/j.bbrc.2005.08.036","article-title":"Effects of SUMO-1 upon Epstein-Barr virus BZLF1 function and BMRF1 expression","volume":"336","author":"AL Adamson","year":"2005","journal-title":"Biochem Biophys Res Commun"},{"key":"ref70","doi-asserted-by":"crossref","first-page":"4","DOI":"10.1186\/s13008-015-0010-1","article-title":"Sumo and the cellular stress response","volume":"10","author":"JM Enserink","year":"2015","journal-title":"Cell Div"},{"issue":"2","key":"ref71","doi-asserted-by":"crossref","first-page":"1265","DOI":"10.1128\/JVI.69.2.1265-1270.1995","article-title":"Characterization of the Epstein-Barr virus proteinase and comparison with the human cytomegalovirus proteinase","volume":"69","author":"G Donaghy","year":"1995","journal-title":"J Virol"},{"issue":"2","key":"ref72","doi-asserted-by":"crossref","first-page":"1129","DOI":"10.1128\/JVI.01410-15","article-title":"Epstein-Barr Virus (EBV) Tegument Protein BGLF2 Promotes EBV Reactivation through Activation of the p38 Mitogen-Activated Protein Kinase","volume":"90","author":"X Liu","year":"2015","journal-title":"J Virol"},{"issue":"2","key":"ref73","doi-asserted-by":"crossref","DOI":"10.1128\/mSphere.00138-18","article-title":"BGLF2 Increases Infectivity of Epstein-Barr Virus by Activating AP-1 upon De Novo Infection","volume":"3","author":"N Konishi","year":"2018","journal-title":"mSphere"},{"issue":"12","key":"ref74","doi-asserted-by":"crossref","first-page":"7648","DOI":"10.1128\/JVI.67.12.7648-7653.1993","article-title":"Functional interaction between Epstein-Barr virus DNA polymerase catalytic subunit and its accessory subunit in vitro","volume":"67","author":"T Tsurumi","year":"1993","journal-title":"J Virol"},{"issue":"1","key":"ref75","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1006\/viro.1997.8470","article-title":"The Epstein-Barr virus (EBV) DNA polymerase accessory protein, BMRF1, activates the essential downstream component of the EBV oriLyt","volume":"230","author":"Q Zhang","year":"1997","journal-title":"Virology"},{"issue":"2","key":"ref76","doi-asserted-by":"crossref","first-page":"745","DOI":"10.1128\/JVI.79.2.745-755.2005","article-title":"The Epstein-Barr virus protein BMRF1 activates gastrin transcription","volume":"79","author":"EA Holley-Guthrie","year":"2005","journal-title":"J Virol"},{"issue":"9","key":"ref77","article-title":"The SWI\/SNF Chromatin Regulator BRG1 Modulates the Transcriptional Regulatory Activity of the Epstein-Barr Virus DNA Polymerase Processivity Factor BMRF1","volume":"91","author":"MT Su","year":"2017","journal-title":"J Virol"},{"issue":"39","key":"ref78","doi-asserted-by":"crossref","first-page":"37790","DOI":"10.1074\/jbc.M305925200","article-title":"A region of the Epstein-Barr virus (EBV) mRNA export factor EB2 containing an arginine-rich motif mediates direct binding to RNA","volume":"278","author":"E Hiriart","year":"2003","journal-title":"J Biol Chem"},{"issue":"4","key":"ref79","doi-asserted-by":"crossref","first-page":"1767","DOI":"10.1128\/JVI.01944-08","article-title":"Herpes simplex virus type 1 ICP27 induces p38 mitogen-activated protein kinase signaling and apoptosis in HeLa cells","volume":"83","author":"PA Gillis","year":"2009","journal-title":"J Virol"},{"issue":"21","key":"ref80","doi-asserted-by":"crossref","first-page":"10565","DOI":"10.1128\/JVI.01119-06","article-title":"Herpes simplex virus type 1 ICP27-dependent activation of NF-kappaB","volume":"80","author":"D Hargett","year":"2006","journal-title":"J Virol"},{"issue":"13","key":"ref81","doi-asserted-by":"crossref","first-page":"1385","DOI":"10.15252\/embj.201593458","article-title":"HSV-1 ICP27 targets the TBK1-activated STING signalsome to inhibit virus-induced type I IFN expression","volume":"35","author":"MH Christensen","year":"2016","journal-title":"Embo J"},{"issue":"10","key":"ref82","doi-asserted-by":"crossref","first-page":"927","DOI":"10.1038\/nsmb.2890","article-title":"Uncovering global SUMOylation signaling networks in a site-specific manner","volume":"21","author":"IA Hendriks","year":"2014","journal-title":"Nat Struct Mol Biol"},{"issue":"6","key":"ref83","doi-asserted-by":"crossref","first-page":"1382","DOI":"10.1074\/mcp.M800551-MCP200","article-title":"Novel proteomics strategy brings insight into the prevalence of SUMO-2 target sites","volume":"8","author":"HA Blomster","year":"2009","journal-title":"Mol Cell Proteomics"},{"key":"ref84","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1007\/978-3-319-50044-7_2","article-title":"Roles of Sumoylation in mRNA Processing and Metabolism","volume":"963","author":"P Richard","year":"2017","journal-title":"Adv Exp Med Biol"},{"issue":"3","key":"ref85","doi-asserted-by":"crossref","first-page":"1155","DOI":"10.1128\/MCB.24.3.1155-1167.2004","article-title":"RanBP2\/Nup358 provides a major binding site for NXF1-p15 dimers at the nuclear pore complex and functions in nuclear mRNA export","volume":"24","author":"D Forler","year":"2004","journal-title":"Mol Cell Biol"},{"issue":"4","key":"ref86","doi-asserted-by":"crossref","first-page":"e1001545","DOI":"10.1371\/journal.pbio.1001545","article-title":"RanBP2\/Nup358 potentiates the translation of a subset of mRNAs encoding secretory proteins","volume":"11","author":"K Mahadevan","year":"2013","journal-title":"PLoS Biol"},{"issue":"12","key":"ref87","doi-asserted-by":"crossref","first-page":"968","DOI":"10.1038\/nsmb.3116","article-title":"Structural basis for catalytic activation by the human ZNF451 SUMO E3 ligase","volume":"22","author":"L Cappadocia","year":"2015","journal-title":"Nat Struct Mol Biol"},{"issue":"12","key":"ref88","doi-asserted-by":"crossref","first-page":"959","DOI":"10.1038\/nsmb.3114","article-title":"A new vertebrate SUMO enzyme family reveals insights into SUMO-chain assembly","volume":"22","author":"N Eisenhardt","year":"2015","journal-title":"Nat Struct Mol Biol"},{"issue":"1","key":"ref89","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1515\/bmc-2016-0030","article-title":"SUMO conjugation\u2014a mechanistic view","volume":"8","author":"A Pichler","year":"2017","journal-title":"Biomol Concepts"},{"issue":"10","key":"ref90","doi-asserted-by":"crossref","first-page":"984","DOI":"10.1038\/nsmb834","article-title":"The RanBP2 SUMO E3 ligase is neither HECT- nor RING-type","volume":"11","author":"A Pichler","year":"2004","journal-title":"Nat Struct Mol Biol"},{"issue":"3","key":"ref91","doi-asserted-by":"crossref","first-page":"585","DOI":"10.1016\/j.jmb.2008.07.016","article-title":"ZNF451 is a novel PML body- and SUMO-associated transcriptional coregulator","volume":"382","author":"U Karvonen","year":"2008","journal-title":"J Mol Biol"},{"issue":"17","key":"ref92","doi-asserted-by":"crossref","first-page":"8828","DOI":"10.1128\/JVI.00441-15","article-title":"Structure of the C-Terminal Domain of the Multifunctional ICP27 Protein from Herpes Simplex Virus 1","volume":"89","author":"V Patel","year":"2015","journal-title":"J Virol"},{"key":"ref93","doi-asserted-by":"crossref","first-page":"11234","DOI":"10.1038\/srep11234","article-title":"The structure of the folded domain from the signature multifunctional protein ICP27 from herpes simplex virus-1 reveals an intertwined dimer","volume":"5","author":"RB Tunnicliffe","year":"2015","journal-title":"Sci Rep"},{"issue":"4","key":"ref94","doi-asserted-by":"crossref","first-page":"491","DOI":"10.1016\/j.dnarep.2009.01.002","article-title":"Regulation of p53 family members by the ubiquitin-like SUMO system","volume":"8","author":"P Stehmeier","year":"2009","journal-title":"DNA Repair (Amst)"},{"issue":"22","key":"ref95","doi-asserted-by":"crossref","first-page":"6462","DOI":"10.1093\/emboj\/18.22.6462","article-title":"Activation of p53 by conjugation to the ubiquitin-like protein SUMO-1","volume":"18","author":"M Gostissa","year":"1999","journal-title":"Embo J"},{"issue":"22","key":"ref96","doi-asserted-by":"crossref","first-page":"6455","DOI":"10.1093\/emboj\/18.22.6455","article-title":"SUMO-1 modification activates the transcriptional response of p53","volume":"18","author":"MS Rodriguez","year":"1999","journal-title":"Embo J"},{"issue":"18","key":"ref97","doi-asserted-by":"crossref","first-page":"3176","DOI":"10.4161\/cc.10.18.17436","article-title":"MDM2 promotes SUMO-2\/3 modification of p53 to modulate transcriptional activity","volume":"10","author":"MH Stindt","year":"2011","journal-title":"Cell Cycle"},{"issue":"7","key":"ref98","doi-asserted-by":"crossref","first-page":"e1005051","DOI":"10.1371\/journal.ppat.1005051","article-title":"K-bZIP Mediated SUMO-2\/3 Specific Modification on the KSHV Genome Negatively Regulates Lytic Gene Expression and Viral Reactivation","volume":"11","author":"WS Yang","year":"2015","journal-title":"PLoS Pathog"},{"issue":"11","key":"ref99","doi-asserted-by":"crossref","first-page":"2011","DOI":"10.1002\/jmv.24882","article-title":"Modulation of global SUMOylation by Kaposi&apos;s sarcoma-associated herpesvirus and its effects on viral gene expression","volume":"89","author":"J Wang","year":"2017","journal-title":"J Med Virol"},{"issue":"24","key":"ref100","doi-asserted-by":"crossref","first-page":"13470","DOI":"10.1128\/JVI.78.24.13470-13478.2004","article-title":"Induction of Id1 and Id3 by latent membrane protein 1 of Epstein-Barr virus and regulation of p27\/Kip and cyclin-dependent kinase 2 in rodent fibroblast transformation","volume":"78","author":"DN Everly Jr.","year":"2004","journal-title":"J Virol"},{"issue":"1","key":"ref101","doi-asserted-by":"crossref","first-page":"417","DOI":"10.1128\/JVI.73.1.417-426.1999","article-title":"The ability of herpes simplex virus type 1 immediate-early protein Vmw110 to bind to a ubiquitin-specific protease contributes to its roles in the activation of gene expression and stimulation of virus replication","volume":"73","author":"RD Everett","year":"1999","journal-title":"J Virol"},{"issue":"2","key":"ref102","doi-asserted-by":"crossref","first-page":"233","DOI":"10.1016\/S1097-2765(00)80133-1","article-title":"SUMO-1 modification of IkappaBalpha inhibits NF-kappaB activation","volume":"2","author":"JM Desterro","year":"1998","journal-title":"Mol Cell"},{"issue":"38","key":"ref103","doi-asserted-by":"crossref","first-page":"35368","DOI":"10.1074\/jbc.M104214200","article-title":"Polymeric chains of SUMO-2 and SUMO-3 are conjugated to protein substrates by SAE1\/SAE2 and Ubc9","volume":"276","author":"MH Tatham","year":"2001","journal-title":"J Biol Chem"},{"issue":"2","key":"ref104","doi-asserted-by":"crossref","first-page":"349","DOI":"10.1016\/j.molcel.2014.11.026","article-title":"Global mapping of herpesvirus-host protein complexes reveals a transcription strategy for late genes","volume":"57","author":"ZH Davis","year":"2015","journal-title":"Mol Cell"},{"issue":"4","key":"ref105","doi-asserted-by":"crossref","first-page":"477","DOI":"10.1016\/j.cell.2010.01.029","article-title":"Merlin\/NF2 suppresses tumorigenesis by inhibiting the E3 ubiquitin ligase CRL4(DCAF1) in the nucleus","volume":"140","author":"W Li","year":"2010","journal-title":"Cell"},{"issue":"9","key":"ref106","doi-asserted-by":"crossref","first-page":"1363","DOI":"10.1038\/nprot.2009.128","article-title":"Detection of protein SUMOylation in vivo","volume":"4","author":"MH Tatham","year":"2009","journal-title":"Nat Protoc"},{"issue":"14","key":"ref107","doi-asserted-by":"crossref","first-page":"6516","DOI":"10.1073\/pnas.89.14.6516","article-title":"An infrequent point mutation of the p53 gene in human nasopharyngeal carcinoma","volume":"89","author":"Y Sun","year":"1992","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"6","key":"ref108","doi-asserted-by":"crossref","first-page":"594","DOI":"10.1038\/nm0602-594","article-title":"Alternate replication in B cells and epithelial cells switches tropism of Epstein-Barr virus","volume":"8","author":"CM Borza","year":"2002","journal-title":"Nat Med"},{"issue":"11","key":"ref109","doi-asserted-by":"crossref","first-page":"1196","DOI":"10.1101\/gad.189274.112","article-title":"SUMO-targeted ubiquitin E3 ligase RNF4 is required for the response of human cells to DNA damage","volume":"26","author":"Y Yin","year":"2012","journal-title":"Genes Dev"}],"updated-by":[{"DOI":"10.1371\/journal.ppat.1007176","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2018,7,18]],"date-time":"2018-07-18T00:00:00Z","timestamp":1531872000000}}],"container-title":["PLOS Pathogens"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/dx.plos.org\/10.1371\/journal.ppat.1007176","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2020,11,5]],"date-time":"2020-11-05T07:28:01Z","timestamp":1604561281000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.ppat.1007176"}},"subtitle":[],"editor":[{"given":"Shannon C.","family":"Kenney","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2018,7,6]]},"references-count":109,"journal-issue":{"issue":"7","published-online":{"date-parts":[[2018,7,6]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.ppat.1007176","relation":{"new_version":[{"id-type":"doi","id":"10.1371\/journal.ppat.1007176","asserted-by":"object"}]},"ISSN":["1553-7374"],"issn-type":[{"value":"1553-7374","type":"electronic"}],"subject":[],"published":{"date-parts":[[2018,7,6]]}}}