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There is no effective antiviral therapy currently available for CVB infection primarily due to that the pathogenesis of CVB has not been completely understood. Viruses are obligate intracellular pathogens which subvert cellular processes to ensure viral replication. Dysregulation of ubiquitination has been implicated in CVB infection. However, how ubiquitination is involved in CVB infection remains unclear. Here we found that the 3D protein of CVB3, the RNA-dependent RNA polymerase, was modified at K220 by K48-linked polyubiquitination which promoted its degradation through proteasome. Proteomic analysis showed that the E3 ligase TRIM56 was upregulated in CVB3-infected cells, while the majority of TRIMs remained unchanged. Pull-down and immunoprecipitation analyses showed that TRIM56 interacted with CVB3 3D. Immunofluorescence observation showed that viral 3D protein was colocalized with TRIM56. TRIM56 overexpression resulted in enhanced ubiquitination of CVB3 3D and decreased virus yield. Moreover, TRIM56 was cleaved by viral 3C protease in CVB3-infected cells. Taken together, this study demonstrated that TRIM56 mediates the ubiquitination and proteasomal degradation of the CVB3 3D protein. These findings demonstrate that TRIM56 is an intrinsic cellular restriction factor against CVB infection, and enhancing viral protein degradation could be a potential strategy to control CVB infection.<\/jats:p>","DOI":"10.1371\/journal.ppat.1012594","type":"journal-article","created":{"date-parts":[[2024,9,30]],"date-time":"2024-09-30T17:40:14Z","timestamp":1727718014000},"page":"e1012594","update-policy":"https:\/\/doi.org\/10.1371\/journal.ppat.corrections_policy","source":"Crossref","is-referenced-by-count":12,"title":["TRIM56 restricts Coxsackievirus B infection by mediating the ubiquitination of viral RNA-dependent RNA polymerase 3D"],"prefix":"10.1371","volume":"20","author":[{"given":"Yao","family":"Wang","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yanyan","family":"Dong","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tian","family":"Luan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yang","family":"Chen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lexun","family":"Lin","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Siwei","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Danxiang","family":"Feng","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jianwei","family":"Wei","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yanru","family":"Fei","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Guangtian","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jiahui","family":"Pan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yan","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhaohua","family":"Zhong","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2495-5138","authenticated-orcid":true,"given":"Wenran","family":"Zhao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2024,9,30]]},"reference":[{"issue":"20","key":"ppat.1012594.ref001","doi-asserted-by":"crossref","first-page":"2326","DOI":"10.1161\/CIRCULATIONAHA.118.035966","article-title":"Enterovirus Persistence in Cardiac Cells of Patients With Idiopathic Dilated Cardiomyopathy Is Linked to 5\u2019 Terminal Genomic RNA-Deleted Viral Populations With Viral-Encoded Proteinase Activities","volume":"139","author":"A Bouin","year":"2019","journal-title":"Circulation"},{"issue":"4","key":"ppat.1012594.ref002","doi-asserted-by":"crossref","first-page":"629","DOI":"10.2217\/fmb.15.5","article-title":"Coxsackievirus B3 replication and pathogenesis","volume":"10","author":"FS Garmaroudi","year":"2015","journal-title":"Future Microbiol"},{"issue":"5","key":"ppat.1012594.ref003","doi-asserted-by":"crossref","first-page":"551","DOI":"10.2217\/fmb.11.40","article-title":"Viral myocarditis: potential defense mechanisms within the cardiomyocyte against virus infection","volume":"6","author":"T. 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Liu","year":"2024","journal-title":"The Journal of biological chemistry"},{"issue":"1","key":"ppat.1012594.ref066","doi-asserted-by":"crossref","first-page":"e28400","DOI":"10.1002\/jmv.28400","article-title":"Phosphorylation of enteroviral 2A(pro) at Ser\/Thr125 benefits its proteolytic activity and viral pathogenesis","volume":"95","author":"Y Wang","year":"2023","journal-title":"Journal of medical virology"},{"issue":"2","key":"ppat.1012594.ref067","doi-asserted-by":"crossref","first-page":"153","DOI":"10.1016\/j.virusres.2005.04.018","article-title":"Coxsackievirus B3 replication is related to activation of the late extracellular signal-regulated kinase (ERK) signal","volume":"113","author":"BK Lim","year":"2005","journal-title":"Virus research"},{"issue":"1","key":"ppat.1012594.ref068","doi-asserted-by":"crossref","first-page":"613","DOI":"10.1038\/s41467-018-02936-3","article-title":"TRIM56-mediated monoubiquitination of cGAS for cytosolic DNA sensing","volume":"9","author":"GJ Seo","year":"2018","journal-title":"Nature communications"},{"issue":"43","key":"ppat.1012594.ref069","doi-asserted-by":"crossref","first-page":"36404","DOI":"10.1074\/jbc.M112.397075","article-title":"TRIM56 is an essential component of the TLR3 antiviral signaling pathway","volume":"287","author":"Y Shen","year":"2012","journal-title":"The Journal of biological chemistry"},{"issue":"5","key":"ppat.1012594.ref070","doi-asserted-by":"crossref","first-page":"756","DOI":"10.1161\/01.CIR.103.5.756","article-title":"Cardioselective infection with coxsackievirus B3 requires intact type I interferon signaling: implications for mortality and early viral replication","volume":"103","author":"R Wessely","year":"2001","journal-title":"Circulation"},{"issue":"23","key":"ppat.1012594.ref071","doi-asserted-by":"crossref","first-page":"3540","DOI":"10.1161\/01.CIR.0000136824.73458.20","article-title":"Protective role for interferon-beta in coxsackievirus B3 infection","volume":"110","author":"R 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