{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,29]],"date-time":"2026-09-29T18:01:31Z","timestamp":1790704891959,"version":"4.1.0"},"reference-count":70,"publisher":"MDPI AG","issue":"12","license":[{"start":{"date-parts":[[2021,12,2]],"date-time":"2021-12-02T00:00:00Z","timestamp":1638403200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000057","name":"National Institute of General Medical Sciences","doi-asserted-by":"publisher","award":["P20GM103546"],"award-info":[{"award-number":["P20GM103546"]}],"id":[{"id":"10.13039\/100000057","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000060","name":"National Institute of Allergy and Infectious Diseases","doi-asserted-by":"publisher","award":["AI137620"],"award-info":[{"award-number":["AI137620"]}],"id":[{"id":"10.13039\/100000060","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Viruses"],"abstract":"<jats:p>Rift Valley fever virus (RVFV) is a negative-sense, tripartite RNA virus that is endemic to Africa and the Arabian Peninsula. It can cause severe disease and mortality in humans and domestic livestock and is a concern for its potential to spread more globally. RVFV\u2019s nucleocapsid protein (N) is an RNA-binding protein that is necessary for viral transcription, replication, and the production of nascent viral particles. We have conducted crosslinking, immunoprecipitation, and sequencing (CLIP-seq) to characterize N interactions with host and viral RNAs during infection. In parallel, to precisely measure intracellular N levels, we employed multiple reaction monitoring mass spectrometry (MRM-MS). Our results show that N binds mostly to host RNAs at early stages of infection, yielding nascent virus particles of reduced infectivity. The expression of N plateaus 10 h post-infection, whereas the intracellular viral RNA concentration continues to increase. Moreover, the virions produced later in infection have higher infectivity. Taken together, the detailed examination of these N\u2013RNA interactions provides insight into how the regulated expression of N and viral RNA produces both infectious and incomplete, noninfectious particles.<\/jats:p>","DOI":"10.3390\/v13122417","type":"journal-article","created":{"date-parts":[[2021,12,7]],"date-time":"2021-12-07T03:21:05Z","timestamp":1638847265000},"page":"2417","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":5,"title":["Time-Resolved Analysis of N-RNA Interactions during RVFV Infection Shows Qualitative and Quantitative Shifts in RNA Encapsidation and Packaging"],"prefix":"10.3390","volume":"13","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-8098-3024","authenticated-orcid":false,"given":"Miyuki","family":"Hayashi","sequence":"first","affiliation":[{"name":"Department of Chemistry and Biochemistry, University of Montana, Missoula, MT 59812, USA"},{"name":"Center for Biomolecular Structure and Dynamics, Missoula, MT 59812, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2259-6912","authenticated-orcid":false,"given":"Eric P.","family":"Schultz","sequence":"additional","affiliation":[{"name":"Center for Biomolecular Structure and Dynamics, Missoula, MT 59812, USA"},{"name":"Division of Biological Sciences, University of Montana, Missoula, MT 59812, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jean-Marc","family":"Lanchy","sequence":"additional","affiliation":[{"name":"Division of Biological Sciences, University of Montana, Missoula, MT 59812, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8087-5362","authenticated-orcid":false,"given":"J. Stephen","family":"Lodmell","sequence":"additional","affiliation":[{"name":"Center for Biomolecular Structure and Dynamics, Missoula, MT 59812, USA"},{"name":"Division of Biological Sciences, University of Montana, Missoula, MT 59812, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,12,2]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"245","DOI":"10.1046\/j.1365-2915.2002.00371.x","article-title":"The 2000 epidemic of Rift Valley fever in Saudi Arabia: Mosquito vector studies","volume":"16","author":"Jupp","year":"2002","journal-title":"Med. Vet. Entomol."},{"key":"ref_2","first-page":"8","article-title":"Molecular biology of rift valley Fever virus","volume":"4","author":"Bouloy","year":"2010","journal-title":"Open Virol. J."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"395","DOI":"10.1146\/annurev-ento-010715-023819","article-title":"Rift Valley Fever: An Emerging Mosquito-Borne Disease","volume":"61","author":"Linthicum","year":"2016","journal-title":"Annu. Rev. Entomol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"663","DOI":"10.4269\/ajtmh.1994.50.663","article-title":"Rift Valley fever in rural northern Senegal: Human risk factors and potential vectors","volume":"50","author":"Wilson","year":"1994","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1126\/sciadv.aau9812","article-title":"Rift Valley fever virus induces fetal demise in Sprague-Dawley rats through direct placental infection","volume":"4","author":"McMillen","year":"2018","journal-title":"Sci. Adv."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"e864","DOI":"10.1016\/S2214-109X(16)30176-0","article-title":"Association of Rift Valley fever virus infection with miscarriage in Sudanese women: A cross-sectional study","volume":"4","author":"Baudin","year":"2016","journal-title":"Lancet Glob. Health"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"493","DOI":"10.3390\/v3050493","article-title":"The pathogenesis of rift valley fever","volume":"3","author":"Ikegami","year":"2011","journal-title":"Viruses"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"9798","DOI":"10.1128\/JVI.78.18.9798-9806.2004","article-title":"NSs Protein of Rift Valley Fever Virus Blocks Interferon Production by Inhibiting Host Gene Transcription","volume":"78","author":"Billecocq","year":"2004","journal-title":"J. Virol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1371","DOI":"10.1128\/JVI.75.3.1371-1377.2001","article-title":"Genetic Evidence for an Interferon-Antagonistic Function of Rift Valley Fever Virus Nonstructural Protein NSs","volume":"75","author":"Bouloy","year":"2001","journal-title":"J. Virol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"3198","DOI":"10.1128\/JVI.02655-06","article-title":"The Glycoprotein Cytoplasmic Tail of Uukuniemi Virus (Bunyaviridae) Interacts with Ribonucleoproteins and Is Critical for Genome Packaging","volume":"81","author":"Overby","year":"2007","journal-title":"J. Virol."},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Piper, M.E., Sorenson, D.R., and Gerrard, S.R. (2011). Efficient cellular release of Rift Valley fever virus requires genomic RNA. PLoS ONE, 6.","DOI":"10.1371\/journal.pone.0018070"},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Tercero, B., Narayanan, K., Terasaki, K., and Makino, S. (2021). Characterization of the Molecular Interactions That Govern the Packaging of Viral RNA Segments into Rift Valley Fever Phlebovirus Particles. J. Virol., 95.","DOI":"10.1128\/JVI.00429-21"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"5246","DOI":"10.1128\/JVI.02778-06","article-title":"A shared transcription termination signal on negative and ambisense RNA genome segments of Rift Valley fever, sandfly fever Sicilian, and Toscana viruses","volume":"81","author":"Albarino","year":"2007","journal-title":"J. Virol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"8421","DOI":"10.1128\/JVI.02641-06","article-title":"Characterization of Rift Valley fever virus transcriptional terminations","volume":"81","author":"Ikegami","year":"2007","journal-title":"J. Virol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"664","DOI":"10.1128\/jvi.20.3.664-675.1976","article-title":"Segmented genome and nucleocapsid of La Crosse virus","volume":"20","author":"Obijeski","year":"1976","journal-title":"J. Virol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"386","DOI":"10.1128\/jvi.15.2.386-392.1975","article-title":"Ribonucleoproteins of Uukuniemi virus are circular","volume":"15","author":"Pettersson","year":"1975","journal-title":"J. Virol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"10310","DOI":"10.1128\/JVI.05252-11","article-title":"Creation of a recombinant Rift Valley fever virus with a two-segmented genome","volume":"85","author":"Brennan","year":"2011","journal-title":"J. Virol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"10883","DOI":"10.1128\/JVI.00961-14","article-title":"Creation of Rift Valley fever viruses with four-segmented genomes reveals flexibility in bunyavirus genome packaging","volume":"88","author":"Oreshkova","year":"2014","journal-title":"J. Virol."},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Wichgers Schreur, P.J., and Kortekaas, J. (2016). Single-Molecule FISH Reveals Non-selective Packaging of Rift Valley Fever Virus Genome Segments. PLoS Pathog., 12.","DOI":"10.1371\/journal.ppat.1005800"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"804","DOI":"10.1073\/pnas.1013155108","article-title":"Mechanism of tripartite RNA genome packaging in Rift Valley fever virus","volume":"108","author":"Terasaki","year":"2011","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"345","DOI":"10.1038\/s42003-021-01821-y","article-title":"Visualizing the ribonucleoprotein content of single bunyavirus virions reveals more efficient genome packaging in the arthropod host","volume":"4","author":"Katrukha","year":"2021","journal-title":"Commun. Biol."},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Ferron, F., Li, Z., Danek, E.I., Luo, D., Wong, Y., Coutard, B., Lantez, V., Charrel, R., Canard, B., and Walz, T. (2011). The hexamer structure of the Rift Valley fever virus nucleoprotein suggests a mechanism for its assembly into ribonucleoprotein complexes. PLoS Pathog., 7.","DOI":"10.1371\/journal.ppat.1002030"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"11769","DOI":"10.1073\/pnas.1001760107","article-title":"Structure of the Rift Valley fever virus nucleocapsid protein reveals another architecture for RNA encapsidation","volume":"107","author":"Raymond","year":"2010","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"19208","DOI":"10.1073\/pnas.1213553109","article-title":"Phleboviruses encapsidate their genomes by sequestering RNA bases","volume":"109","author":"Raymond","year":"2012","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Hornak, K.E., Lanchy, J.-m., and Lodmell, J.S. (2016). RNA Encapsidation and Packaging in the Phleboviruses. Viruses, 8.","DOI":"10.3390\/v8070194"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"11381","DOI":"10.1128\/JVI.00767-07","article-title":"The cytoplasmic tails of Uukuniemi Virus (Bunyaviridae) G(N) and G(C) glycoproteins are important for intracellular targeting and the budding of virus-like particles","volume":"81","author":"Overby","year":"2007","journal-title":"J. Virol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"330","DOI":"10.1016\/j.antiviral.2012.01.002","article-title":"Characterization of RNA aptamers directed against the nucleocapsid protein of Rift Valley fever virus","volume":"93","author":"Ellenbecker","year":"2012","journal-title":"Antivir. Res."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"7405","DOI":"10.1128\/AAC.03595-14","article-title":"Inhibition of Rift Valley fever virus replication and perturbation of nucleocapsid-RNA interactions by suramin","volume":"58","author":"Ellenbecker","year":"2014","journal-title":"Antimicrob Agents Chemother"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"6829","DOI":"10.1128\/JVI.00672-13","article-title":"Structure of Severe Fever with Thrombocytopenia Syndrome Virus Nucleocapsid Protein in Complex with Suramin Reveals Therapeutic Potential","volume":"87","author":"Jiao","year":"2013","journal-title":"J. Virol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.virol.2013.09.023","article-title":"Role of the cytosolic tails of Rift Valley fever virus envelope glycoproteins in viral morphogenesis","volume":"448","author":"Carnec","year":"2014","journal-title":"Virology"},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Sanju\u00e1n, R., and Thoulouze, M.I. (2019). Why viruses sometimes disperse in groups?. Virus Evol., 5.","DOI":"10.1093\/ve\/vez025"},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Martin, M. (2011). Cutadapt removes adaptor sequences from high-throughput sequencing reads. EMBnet. J.","DOI":"10.14806\/ej.17.1.200"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1093\/bioinformatics\/bts635","article-title":"STAR: Ultrafast universal RNA-seq aligner","volume":"29","author":"Dobin","year":"2013","journal-title":"Bioinformatics"},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Kondili, M., Fust, A., Preussner, J., Kuenne, C., Braun, T., and Looso, M. (2017). UROPA: A tool for Universal Robust Peak Annotation. Sci. Rep., 7.","DOI":"10.1038\/s41598-017-02464-y"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"24","DOI":"10.1038\/nbt.1754","article-title":"Integrative genomics viewer","volume":"29","author":"Robinson","year":"2011","journal-title":"Nat. Biotechnol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"W537","DOI":"10.1093\/nar\/gky379","article-title":"The Galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2018 update","volume":"46","author":"Afgan","year":"2018","journal-title":"Nucleic. Acids Res."},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Shihavuddin, A., Basu, S., Rexhepaj, E., Delestro, F., Menezes, N., Sigoillot, S.M., Del Nery, E., Selimi, F., Spassky, N., and Genovesio, A. (2017). Smooth 2D manifold extraction from 3D image stack. Nat. Commun., 8.","DOI":"10.1038\/ncomms15554"},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Holden, P., and Horton, W.A. (2009). Crude subcellular fractionation of cultured mammalian cell lines. BMC Res. Notes, 2.","DOI":"10.1186\/1756-0500-2-243"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1016\/j.jviromet.2012.05.012","article-title":"Development of a strand specific real-time RT-qPCR assay for the detection and quantitation of murine norovirus RNA","volume":"184","author":"Vashist","year":"2012","journal-title":"J. Virol. Methods"},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Chen, C., Ridzon, D.A., Broomer, A.J., Zhou, Z., Lee, D.H., Nguyen, J.T., Barbisin, M., Xu, N.L., Mahuvakar, V.R., and Andersen, M.R. (2005). Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic. Acids Res., 33.","DOI":"10.1093\/nar\/gni178"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"1377","DOI":"10.1021\/pr301024c","article-title":"A proteomics search algorithm specifically designed for high-resolution tandem mass spectra","volume":"12","author":"Wenger","year":"2013","journal-title":"J. Proteome Res."},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"Moore, M.J., Zhang, C., Gantman, E.C., Mele, A., Darnell, J.C., and Darnell, R.B. (2016). Erratum: Mapping Argonaute and conventional RNA-binding protein interactions with RNA at single-nucleotide resolution using HITS-CLIP and CIMS analysis. Nat. Protoc., 11.","DOI":"10.1038\/nprot0316-616c"},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"Wheeler, E.C., Van Nostrand, E.L., and Yeo, G.W. (2018). Advances and challenges in the detection of transcriptome-wide protein-RNA interactions. Wiley Interdiscip Rev. RNA, 9.","DOI":"10.1002\/wrna.1436"},{"key":"ref_44","doi-asserted-by":"crossref","unstructured":"Havranek, K.E., White, L.A., Lanchy, J.M., and Lodmell, J.S. (2019). Transcriptome profiling in Rift Valley fever virus infected cells reveals modified transcriptional and alternative splicing programs. PLoS ONE, 14.","DOI":"10.1371\/journal.pone.0217497"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"11659","DOI":"10.1128\/JVI.01434-13","article-title":"Nuclear relocalization of polyadenylate binding protein during rift valley fever virus infection involves expression of the NSs gene","volume":"87","author":"Copeland","year":"2013","journal-title":"J. Virol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"E2920","DOI":"10.1073\/pnas.1418805112","article-title":"Virus-induced translational arrest through 4EBP1\/2-dependent decay of 5\u2019-TOP mRNAs restricts viral infection","volume":"112","author":"Hopkins","year":"2015","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"504","DOI":"10.1016\/j.mib.2011.07.011","article-title":"Nucleoproteins and nucleocapsids of negative-strand RNA viruses","volume":"14","author":"Ruigrok","year":"2011","journal-title":"Curr. Opin. Microbiol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"2933","DOI":"10.1128\/JVI.80.6.2933-2940.2006","article-title":"Rescue of infectious rift valley fever virus entirely from cDNA, analysis of virus lacking the NSs gene, and expression of a foreign gene","volume":"80","author":"Ikegami","year":"2006","journal-title":"J. Virol."},{"key":"ref_49","doi-asserted-by":"crossref","unstructured":"Murakami, S., Terasaki, K., Ramirez, S.I., Morrill, J.C., and Makino, S. (2014). Development of a novel, single-cycle replicable rift valley Fever vaccine. PLoS Negl. Trop. Dis., 8.","DOI":"10.1371\/journal.pntd.0002746"},{"key":"ref_50","doi-asserted-by":"crossref","unstructured":"Ahsan, N.A., Sampey, G.C., Lepene, B., Akpamagbo, Y., Barclay, R.A., Iordanskiy, S., Hakami, R.M., and Kashanchi, F. (2016). Presence of Viral RNA and Proteins in Exosomes from Cellular Clones Resistant to Rift Valley Fever Virus Infection. Front. Microbiol., 7.","DOI":"10.3389\/fmicb.2016.00139"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1016\/j.virusres.2005.05.007","article-title":"Nuclear\/nucleolar localization properties of C-terminal nucleocapsid protein of SARS coronavirus","volume":"114","author":"Timani","year":"2005","journal-title":"Virus Res."},{"key":"ref_52","doi-asserted-by":"crossref","unstructured":"Wulan, W.N., Heydet, D., Walker, E.J., Gahan, M.E., and Ghildyal, R. (2015). Nucleocytoplasmic transport of nucleocapsid proteins of enveloped RNA viruses. Front. Microbiol., 6.","DOI":"10.3389\/fmicb.2015.00553"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"3164","DOI":"10.1016\/j.febslet.2007.05.082","article-title":"The maximal size of protein to diffuse through the nuclear pore is larger than 60 kDa","volume":"581","author":"Wang","year":"2007","journal-title":"FEBS Lett."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"336","DOI":"10.1016\/j.tcb.2011.03.003","article-title":"Pre-mRNA splicing: Where and when in the nucleus","volume":"21","author":"Han","year":"2011","journal-title":"Trends Cell Biol."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1089\/107999002753452665","article-title":"On the role of IRF in host defense","volume":"22","author":"Barnes","year":"2002","journal-title":"J. Interferon Cytokine Res. Off. J. Int. Soc. Interferon Cytokine Res."},{"key":"ref_56","doi-asserted-by":"crossref","unstructured":"Zhou, A., Dong, X., Liu, M., and Tang, B. (2021). Comprehensive Transcriptomic Analysis Identifies Novel Antiviral Factors Against Influenza A Virus Infection. Front. Immunol., 12.","DOI":"10.3389\/fimmu.2021.632798"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"44412","DOI":"10.1074\/jbc.M111.285205","article-title":"Inhibitor of \u03baB kinase epsilon (IKK(epsilon)), STAT1, and IFIT2 proteins define novel innate immune effector pathway against West Nile virus infection","volume":"286","author":"Perwitasari","year":"2011","journal-title":"J. Biol. Chem."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"8035","DOI":"10.4049\/jimmunol.0902728","article-title":"Distinct antiviral roles for human 2\u2032,5\u2032;-oligoadenylate synthetase family members against dengue virus infection","volume":"183","author":"Lin","year":"2009","journal-title":"J. Immunol."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"216","DOI":"10.1016\/j.virol.2008.10.021","article-title":"The large form of human 2\u2032,5\u2032-Oligoadenylate Synthetase (OAS3) exerts antiviral effect against Chikungunya virus","volume":"384","author":"Frenkiel","year":"2009","journal-title":"Virology"},{"key":"ref_60","doi-asserted-by":"crossref","unstructured":"Liu, Y., Liang, Q.Z., Lu, W., Yang, Y.L., Chen, R., Huang, Y.W., and Wang, B. (2021). A Comparative Analysis of Coronavirus Nucleocapsid (N) Proteins Reveals the SADS-CoV N Protein Antagonizes IFN-\u03b2 Production by Inducing Ubiquitination of RIG-I. Front. Immunol., 12.","DOI":"10.3389\/fimmu.2021.688758"},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1007\/s11262-010-0544-x","article-title":"SARS-CoV nucleocapsid protein antagonizes IFN-\u03b2 response by targeting initial step of IFN-\u03b2 induction pathway, and its C-terminal region is critical for the antagonism","volume":"42","author":"Lu","year":"2011","journal-title":"Virus Genes"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"12093","DOI":"10.1128\/JVI.00429-11","article-title":"Lassa virus nucleoprotein mutants generated by reverse genetics induce a robust type I interferon response in human dendritic cells and macrophages","volume":"85","author":"Carnec","year":"2011","journal-title":"J. Virol."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1016\/j.virol.2010.02.018","article-title":"Modulation of apoptosis and immune signaling pathways by the Hantaan virus nucleocapsid protein","volume":"401","author":"Ontiveros","year":"2010","journal-title":"Virology"},{"key":"ref_64","doi-asserted-by":"crossref","unstructured":"Brennan, B., Welch, S.R., and Elliott, R.M. (2014). The consequences of reconfiguring the ambisense S genome segment of Rift Valley fever virus on viral replication in mammalian and mosquito cells and for genome packaging. PLoS Pathog., 10.","DOI":"10.1371\/journal.ppat.1003922"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"4034","DOI":"10.1128\/JVI.06700-11","article-title":"Roles of the coding and noncoding regions of rift valley Fever virus RNA genome segments in viral RNA packaging","volume":"86","author":"Murakami","year":"2012","journal-title":"J. Virol."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"5023","DOI":"10.1074\/jbc.RA118.004976","article-title":"Crimean-Congo hemorrhagic fever virus nucleocapsid protein harbors distinct RNA-binding sites in the stalk and head domains","volume":"294","author":"Jeeva","year":"2019","journal-title":"J. Biol. Chem."},{"key":"ref_67","doi-asserted-by":"crossref","unstructured":"Cubuk, J., Alston, J.J., Incicco, J.J., Singh, S., Stuchell-Brereton, M.D., Ward, M.D., Zimmerman, M.I., Vithani, N., Griffith, D., and Wagoner, J.A. (2021). The SARS-CoV-2 nucleocapsid protein is dynamic, disordered, and phase separates with RNA. Nat. Commun., 12.","DOI":"10.1038\/s41467-021-21953-3"},{"key":"ref_68","doi-asserted-by":"crossref","unstructured":"Brocca, S., Grandori, R., Longhi, S., and Uversky, V. (2020). Liquid-Liquid Phase Separation by Intrinsically Disordered Protein Regions of Viruses: Roles in Viral Life Cycle and Control of Virus-Host Interactions. Int. J. Mol. Sci., 21.","DOI":"10.3390\/ijms21239045"},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"11354","DOI":"10.1002\/anie.201703191","article-title":"Reentrant Phase Transition Drives Dynamic Substructure Formation in Ribonucleoprotein Droplets","volume":"56","author":"Banerjee","year":"2017","journal-title":"Angew. Chem. Int. Ed. Engl."},{"key":"ref_70","doi-asserted-by":"crossref","unstructured":"Oymans, J., Wichgers Schreur, P.J., van Keulen, L., Kant, J., and Kortekaas, J. (2020). Rift Valley fever virus targets the maternal-foetal interface in ovine and human placentas. PLoS Negl. Trop. Dis., 14.","DOI":"10.1371\/journal.pntd.0007898"}],"container-title":["Viruses"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1999-4915\/13\/12\/2417\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T07:39:00Z","timestamp":1760168340000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1999-4915\/13\/12\/2417"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,12,2]]},"references-count":70,"journal-issue":{"issue":"12","published-online":{"date-parts":[[2021,12]]}},"alternative-id":["v13122417"],"URL":"https:\/\/doi.org\/10.3390\/v13122417","relation":{},"ISSN":["1999-4915"],"issn-type":[{"value":"1999-4915","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,12,2]]}}}