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The viral large (L) protein catalyzes viral transcription by stealing host mRNA caps via a process known as cap-snatching. Here, we establish an in vitro cap-snatching assay and present three high-quality electron cryo-microscopy (cryo-EM) structures of the SFTSV L protein in biologically relevant, transcription-specific states. In a priming-state structure, we show capped RNA bound to the L protein cap-binding domain (CBD). The L protein conformation in this priming structure is significantly different from published replication-state structures, in particular the N- and C-terminal domains. The capped-RNA is positioned in a way that it can feed directly into the RNA-dependent RNA polymerase (RdRp) ready for elongation. We also captured the L protein in an early-elongation state following primer-incorporation demonstrating that this priming conformation is retained at least in the very early stages of primer extension. This structural data is complemented by in vitro biochemical and cell-based assays. Together, these insights further our mechanistic understanding of how SFTSV and other bunyaviruses incorporate stolen host mRNA fragments into their viral transcripts thereby allowing the virus to hijack host cell translation machinery.<\/jats:p>","DOI":"10.1093\/nar\/gkae330","type":"journal-article","created":{"date-parts":[[2024,4,19]],"date-time":"2024-04-19T12:49:34Z","timestamp":1713530974000},"page":"6049-6065","source":"Crossref","is-referenced-by-count":14,"title":["Structural snapshots of phenuivirus cap-snatching and transcription"],"prefix":"10.1093","volume":"52","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-9108-9933","authenticated-orcid":false,"given":"Harry M","family":"Williams","sequence":"first","affiliation":[{"name":"Bernhard Nocht Institute for Tropical Medicine (BNITM) , Hamburg , Germany"},{"name":"Centre for Structural Systems Biology (CSSB) , Hamburg , Germany"},{"name":"Leibniz Institute of Virology , Hamburg , Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sigurdur\u00a0R","family":"Thorkelsson","sequence":"additional","affiliation":[{"name":"Centre for Structural Systems Biology (CSSB) , Hamburg , Germany"},{"name":"Leibniz Institute of Virology , Hamburg , Germany"},{"name":"University of Hamburg , Hamburg , Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6797-9696","authenticated-orcid":false,"given":"Dominik","family":"Vogel","sequence":"additional","affiliation":[{"name":"Bernhard Nocht Institute for Tropical Medicine (BNITM) , Hamburg , Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Carola","family":"Busch","sequence":"additional","affiliation":[{"name":"Bernhard Nocht Institute for Tropical Medicine (BNITM) , Hamburg , Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Morlin","family":"Milewski","sequence":"additional","affiliation":[{"name":"Bernhard Nocht Institute for Tropical Medicine (BNITM) , Hamburg , Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9324-0796","authenticated-orcid":false,"given":"Stephen","family":"Cusack","sequence":"additional","affiliation":[{"name":"European Molecular Biology Laboratory , Grenoble , France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kay","family":"Gr\u00fcnewald","sequence":"additional","affiliation":[{"name":"Centre for Structural Systems Biology (CSSB) , Hamburg , Germany"},{"name":"Leibniz Institute of Virology , Hamburg , Germany"},{"name":"University of Hamburg , Hamburg , Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Emmanuelle\u00a0R J","family":"Quemin","sequence":"additional","affiliation":[{"name":"Centre for Structural Systems Biology (CSSB) , Hamburg , Germany"},{"name":"Leibniz Institute of Virology , Hamburg , Germany"},{"name":"Department of Virology, Institute for Integrative Biology of the Cell (I2BC) , Centre National de la Recherche Scientifique (CNRS) UMR9198, Gif-sur-Yvette , France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2986-936X","authenticated-orcid":false,"given":"Maria","family":"Rosenthal","sequence":"additional","affiliation":[{"name":"Bernhard Nocht Institute for Tropical Medicine (BNITM) , Hamburg , Germany"},{"name":"Centre for Structural Systems Biology (CSSB) , Hamburg , Germany"},{"name":"Fraunhofer Institute for Translational Medicine and Pharmacology (ITMP) , Discovery Research ScreeningPort, Hamburg , Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2024,5,6]]},"reference":[{"key":"2024061000012914800_B1","doi-asserted-by":"crossref","first-page":"713","DOI":"10.1038\/s12276-021-00610-1","article-title":"Severe fever with thrombocytopenia syndrome virus: emerging novel phlebovirus and their control strategy","volume":"53","author":"Casel","year":"2021","journal-title":"Exp. Mol. Med."},{"key":"2024061000012914800_B2","doi-asserted-by":"crossref","first-page":"1892","DOI":"10.3201\/eid1911.130792","article-title":"Severe fever with thrombocytopenia syndrome, South Korea, 2012","volume":"19","author":"Kim","year":"2013","journal-title":"Emerg. Infect. Dis."},{"key":"2024061000012914800_B3","doi-asserted-by":"crossref","first-page":"816","DOI":"10.1093\/infdis\/jit603","article-title":"The first identification and retrospective study of Severe Fever with Thrombocytopenia Syndrome in Japan","volume":"209","author":"Takahashi","year":"2014","journal-title":"J. Infect. Dis."},{"key":"2024061000012914800_B4","doi-asserted-by":"crossref","first-page":"1029","DOI":"10.3201\/eid2505.181463","article-title":"Endemic severe fever with thrombocytopenia syndrome, Vietnam","volume":"25","author":"Tran","year":"2019","journal-title":"Emerg. Infect. Dis."},{"key":"2024061000012914800_B5","doi-asserted-by":"crossref","first-page":"1878","DOI":"10.3201\/eid2608.200135","article-title":"Genotypic heterogeneity of Orientia tsutsugamushi in scrub typhus patients and thrombocytopenia syndrome co-infection, Myanmar","volume":"26","author":"Win","year":"2020","journal-title":"Emerg. Infect. Dis."},{"key":"2024061000012914800_B6","doi-asserted-by":"crossref","first-page":"1523","DOI":"10.1056\/NEJMoa1010095","article-title":"Fever with thrombocytopenia associated with a novel bunyavirus in China","volume":"364","author":"Yu","year":"2011","journal-title":"N. Engl. J. Med."},{"key":"2024061000012914800_B7","doi-asserted-by":"crossref","first-page":"204","DOI":"10.31524\/bkkmedj.2020.22.001","article-title":"Severe fever with thrombocytopenia syndrome virus: the first case report in Thailand","volume":"16","author":"Daengnoi","year":"2020","journal-title":"Bangkok Med. J."},{"key":"2024061000012914800_B8","doi-asserted-by":"crossref","first-page":"56","DOI":"10.1186\/s40249-019-0569-x","article-title":"Prevalence of severe fever with thrombocytopenia syndrome virus in animals in Henan Province, China","volume":"8","author":"Huang","year":"2019","journal-title":"Infect. Dis. Poverty"},{"key":"2024061000012914800_B9","doi-asserted-by":"crossref","first-page":"185","DOI":"10.1016\/j.jcv.2014.03.020","article-title":"Seroprevalence of antibodies against SFTS virus infection in farmers and animals, Jiangsu, China","volume":"60","author":"Li","year":"2014","journal-title":"J. Clin. Virol."},{"key":"2024061000012914800_B10","doi-asserted-by":"crossref","first-page":"756","DOI":"10.3201\/eid1905.120245","article-title":"Severe fever with thrombocytopenia syndrome virus among domesticated animals, China","volume":"19","author":"Niu","year":"2013","journal-title":"Emerg. Infect. 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