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The mechanisms regulating VP35\u2019s engagement in different functions are not well-understood. We previously showed that the host E3 ubiquitin ligase TRIM6 ubiquitinates VP35 at lysine 309 (K309) to facilitate virus replication. However, how K309 ubiquitination regulates the function of VP35 as the viral polymerase co-factor and the precise stage(s) of the EBOV replication cycle that require VP35 ubiquitination are not known. Here, we generated recombinant EBOVs encoding glycine (G) or arginine (R) mutations at VP35\/K309 (rEBOV-VP35\/K309G\/-R) and show that both mutations prohibit VP35\/K309 ubiquitination. The K309R mutant retains dsRNA binding and efficient type-I Interferon (IFN-I) antagonism due to the basic residue conservation. The rEBOV-VP35\/K309G mutant loses the ability to efficiently antagonize the IFN-I response, while the rEBOV-VP35\/K309R mutant\u2019s suppression is enhanced. The replication of both mutants was significantly attenuated in both IFN-competent and -deficient cells due to impaired interactions with the viral polymerase. The lack of ubiquitination on VP35\/K309 or TRIM6 deficiency disrupts viral transcription with increasing severity along the transcriptional gradient. This disruption of the transcriptional gradient results in unbalanced viral protein production, including reduced synthesis of the viral transcription factor VP30. In addition, lack of ubiquitination on K309 results in enhanced interactions with the viral nucleoprotein and premature nucleocapsid packaging, leading to dysregulation of virus assembly. Overall, we identified a novel role of VP35 ubiquitination in coordinating viral transcription and assembly.<\/jats:p>","DOI":"10.1371\/journal.ppat.1010532","type":"journal-article","created":{"date-parts":[[2022,5,9]],"date-time":"2022-05-09T17:45:43Z","timestamp":1652118343000},"page":"e1010532","update-policy":"https:\/\/doi.org\/10.1371\/journal.ppat.corrections_policy","source":"Crossref","is-referenced-by-count":23,"title":["Ubiquitination of Ebola virus VP35 at lysine 309 regulates viral transcription and assembly"],"prefix":"10.1371","volume":"18","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-9905-920X","authenticated-orcid":true,"given":"Sarah","family":"van Tol","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Birte","family":"Kalveram","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Philipp A.","family":"Ilinykh","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Adam","family":"Ronk","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kai","family":"Huang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Leopoldo","family":"Aguilera-Aguirre","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Preeti","family":"Bharaj","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Adam","family":"Hage","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Colm","family":"Atkins","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Maria I.","family":"Giraldo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Maki","family":"Wakamiya","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Maria","family":"Gonzalez-Orozco","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Abbey N.","family":"Warren","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alexander","family":"Bukreyev","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alexander N.","family":"Freiberg","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5058-5444","authenticated-orcid":true,"given":"Ricardo","family":"Rajsbaum","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2022,5,9]]},"reference":[{"issue":"6","key":"ppat.1010532.ref001","article-title":"ICTV Virus Taxonomy Profile: Filoviridae","volume":"100","author":"JH Kuhn","year":"2019","journal-title":"The Journal of general virology"},{"issue":"1","key":"ppat.1010532.ref002","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1038\/s41572-020-0147-3","article-title":"Ebola virus disease","volume":"6","author":"ST Jacob","year":"2020","journal-title":"Nat Rev Dis Primers"},{"key":"ppat.1010532.ref003","article-title":"Ebola (Ebola Virus Disease) History of Ebola Outbreaks: CDC","author":"CDC","year":"2021"},{"issue":"19","key":"ppat.1010532.ref004","doi-asserted-by":"crossref","DOI":"10.1056\/NEJMra1901594","article-title":"Ebola","volume":"382","author":"H Feldmann","year":"2020","journal-title":"The New England journal of medicine"},{"issue":"9","key":"ppat.1010532.ref005","doi-asserted-by":"crossref","DOI":"10.1016\/S1473-3099(20)30282-6","article-title":"Recent successes in therapeutics for Ebola virus disease: no time for complacency","volume":"20","author":"PL Iversen","year":"2020","journal-title":"The Lancet Infectious diseases"},{"issue":"3","key":"ppat.1010532.ref006","doi-asserted-by":"crossref","first-page":"2333","DOI":"10.1128\/JVI.73.3.2333-2342.1999","article-title":"Comparison of the transcription and replication strategies of marburg virus and Ebola virus by using artificial replication systems","volume":"73","author":"E Muhlberger","year":"1999","journal-title":"Journal of virology"},{"issue":"2","key":"ppat.1010532.ref007","doi-asserted-by":"crossref","first-page":"205","DOI":"10.2217\/17460794.2.2.205","article-title":"Filovirus replication and transcription","volume":"2","author":"E. 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