{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,16]],"date-time":"2026-06-16T10:54:03Z","timestamp":1781607243832,"version":"3.54.5"},"reference-count":76,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2022,10,17]],"date-time":"2022-10-17T00:00:00Z","timestamp":1665964800000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2022,10,17]],"date-time":"2022-10-17T00:00:00Z","timestamp":1665964800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/100006492","name":"Division of Intramural Research, National Institute of Allergy and Infectious Diseases","doi-asserted-by":"publisher","award":["R01AI129988"],"award-info":[{"award-number":["R01AI129988"]}],"id":[{"id":"10.13039\/100006492","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000057","name":"U.S. Department of Health & Human Services | NIH | National Institute of General Medical Sciences","doi-asserted-by":"publisher","award":["T32GM135134"],"award-info":[{"award-number":["T32GM135134"]}],"id":[{"id":"10.13039\/100000057","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Commun Biol"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Avian species are the major natural reservoir from which pandemic influenza A viruses can be introduced to humans. Avian influenza A virus genes, including the three viral polymerase genes, PA, PB1 and PB2, require host-adaptive mutations to allow for viral replication and transmission in humans. Previously, PA from the 2009 pH1N1 viral polymerase was found to harbor host-adaptive mutations leading to enhanced viral polymerase activity. By quantifying translation and mRNA transcription, we found that the 2009 pH1N1 PA, and the associated host-adaptive mutations, led to greater translation efficiency. This was due to enhanced cytosolic accumulation of viral mRNA, which was dependent on the host RNA binding protein GRSF1. Mutations to the GRSF1 binding site in viral mRNA, as well as GRSF1 knockdown, reduced cytosolic accumulation and translation efficiency of viral mRNAs. This study identifies a previously unrecognized mechanism by which host-adaptive mutations in PA regulate viral replication and host adaptation. Importantly, these results provide greater insight into the host adaptation process of IAVs and reveal the importance of GRSF1 in the lifecycle of IAV.<\/jats:p>","DOI":"10.1038\/s42003-022-04082-5","type":"journal-article","created":{"date-parts":[[2022,10,17]],"date-time":"2022-10-17T18:02:54Z","timestamp":1666029774000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":13,"title":["Host adaptive mutations in the 2009 H1N1 pandemic influenza A virus PA gene regulate translation efficiency of viral mRNAs via GRSF1"],"prefix":"10.1038","volume":"5","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-3318-0808","authenticated-orcid":false,"given":"Michael","family":"Lutz","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jordana","family":"Schmierer","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6612-694X","authenticated-orcid":false,"given":"Toru","family":"Takimoto","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2022,10,17]]},"reference":[{"key":"4082_CR1","unstructured":"Centers for Disease Control and Prevention. Avian Influenza Type A viruses. https:\/\/www.cdc.gov\/flu\/avianflu\/influenza-a-virus-subtypes.htm (2017)."},{"key":"4082_CR2","doi-asserted-by":"publisher","first-page":"3","DOI":"10.1038\/s41572-018-0002-y","volume":"4","author":"F Krammer","year":"2018","unstructured":"Krammer, F. et al. Influenza. Nat. Rev. Dis. Prim. 4, 3 (2018).","journal-title":"Nat. Rev. Dis. Prim."},{"key":"4082_CR3","doi-asserted-by":"publisher","first-page":"7200","DOI":"10.1128\/JVI.00980-13","volume":"87","author":"B M\u00e4nz","year":"2013","unstructured":"M\u00e4nz, B., Schwemmle, M. & Brunotte, L. Adaptation of avian influenza A virus polymerase in mammals to overcome the host species barrier. J. Virol. 87, 7200\u20137209 (2013).","journal-title":"J. Virol."},{"key":"4082_CR4","doi-asserted-by":"publisher","first-page":"67","DOI":"10.1038\/s41579-018-0115-z","volume":"17","author":"JS Long","year":"2019","unstructured":"Long, J. S., Mistry, B., Haslam, S. M. & Barclay, W. S. Host and viral determinants of influenza A virus species specificity. Nat. Rev. Microbiol 17, 67\u201381 (2019).","journal-title":"Nat. Rev. Microbiol"},{"key":"4082_CR5","doi-asserted-by":"publisher","first-page":"1193","DOI":"10.1099\/vir.0.062836-0","volume":"95","author":"AV Cauldwell","year":"2014","unstructured":"Cauldwell, A. V., Long, J. S., Moncorge, O. & Barclay, W. S. Viral determinants of influenza A virus host range. J. Gen. Virol. 95, 1193\u20131210 (2014).","journal-title":"J. Gen. Virol."},{"key":"4082_CR6","doi-asserted-by":"crossref","unstructured":"Lutz Iv, M. M., Dunagan, M. M., Kurebayashi, Y. & Takimoto, T. Key role of the influenza A virus PA gene segment in the emergence of pandemic viruses. Viruses 12, 365 (2020).","DOI":"10.3390\/v12040365"},{"key":"4082_CR7","doi-asserted-by":"publisher","first-page":"5928","DOI":"10.1128\/JVI.00130-16","volume":"90","author":"B M\u00e4nz","year":"2016","unstructured":"M\u00e4nz, B. et al. Multiple natural substitutions in avian influenza A virus PB2 facilitate efficient replication in human cells. J. Virol. 90, 5928\u20135938 (2016).","journal-title":"J. Virol."},{"key":"4082_CR8","doi-asserted-by":"crossref","unstructured":"Soh, Y. S., Moncla, L. H., Eguia, R., Bedford, T. & Bloom, J. D. Comprehensive mapping of adaptation of the avian influenza polymerase protein PB2 to humans. Elife 8, e45079 (2019).","DOI":"10.7554\/eLife.45079"},{"key":"4082_CR9","doi-asserted-by":"crossref","unstructured":"Subbarao, E. K., London, W., & Murphy, B. R. A single amino acid in the PB2 gene of influenza A virus is a determinant of host range. 67, 1761\u20131764 (1993).","DOI":"10.1128\/jvi.67.4.1761-1764.1993"},{"key":"4082_CR10","doi-asserted-by":"publisher","DOI":"10.1038\/srep14170","volume":"5","author":"W Zhu","year":"2015","unstructured":"Zhu, W. et al. Dual E627K and D701N mutations in the PB2 protein of A(H7N9) influenza virus increased its virulence in mammalian models. Sci. Rep. 5, 14170 (2015).","journal-title":"Sci. Rep."},{"key":"4082_CR11","doi-asserted-by":"publisher","first-page":"1840","DOI":"10.1126\/science.1062882","volume":"293","author":"M Hatta","year":"2001","unstructured":"Hatta, M., Gao, P., Halfmann, P. & Kawaoka, Y. Molecular basis for high virulence of Hong Kong H5N1 influenza A viruses. Science 293, 1840\u20131842 (2001).","journal-title":"Science"},{"key":"4082_CR12","doi-asserted-by":"publisher","first-page":"258","DOI":"10.1016\/j.virol.2003.11.030","volume":"320","author":"K Shinya","year":"2004","unstructured":"Shinya, K. et al. PB2 amino acid at position 627 affects replicative efficiency, but not cell tropism, of Hong Kong H5N1 influenza A viruses in mice. Virology 320, 258\u2013266 (2004).","journal-title":"Virology"},{"key":"4082_CR13","doi-asserted-by":"publisher","first-page":"101","DOI":"10.1038\/nature16474","volume":"529","author":"JS Long","year":"2016","unstructured":"Long, J. S. et al. Species difference in ANP32A underlies influenza A virus polymerase host restriction. Nature 529, 101\u2013104 (2016).","journal-title":"Nature"},{"key":"4082_CR14","doi-asserted-by":"crossref","unstructured":"Long, J. S. et al. Species specific differences in use of ANP32 proteins by influenza A virus. Elife 8, e45066 (2019).","DOI":"10.7554\/eLife.45066"},{"key":"4082_CR15","doi-asserted-by":"publisher","first-page":"638","DOI":"10.1038\/s41586-020-2927-z","volume":"587","author":"L Carrique","year":"2020","unstructured":"Carrique, L. et al. Host ANP32A mediates the assembly of the influenza virus replicase. Nature 587, 638\u2013643 (2020).","journal-title":"Nature"},{"key":"4082_CR16","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-020-17407-x","volume":"11","author":"AR Camacho-Zarco","year":"2020","unstructured":"Camacho-Zarco, A. R. et al. Molecular basis of host-adaptation interactions between influenza virus polymerase PB2 subunit and ANP32A. Nat. Commun. 11, 3656 (2020).","journal-title":"Nat. Commun."},{"key":"4082_CR17","doi-asserted-by":"publisher","first-page":"889","DOI":"10.1038\/nature04230","volume":"437","author":"JK Taubenberger","year":"2005","unstructured":"Taubenberger, J. K. et al. Characterization of the 1918 influenza virus polymerase genes. Nature 437, 889\u2013893 (2005).","journal-title":"Nature"},{"key":"4082_CR18","doi-asserted-by":"publisher","first-page":"197","DOI":"10.1126\/science.1176225","volume":"325","author":"RJ Garten","year":"2009","unstructured":"Garten, R. J. et al. Antigenic and genetic characteristics of swine-origin 2009 A(H1N1) influenza viruses circulating in humans. Science 325, 197\u2013201 (2009).","journal-title":"Science"},{"key":"4082_CR19","doi-asserted-by":"publisher","first-page":"1122","DOI":"10.1038\/nature08182","volume":"459","author":"GJ Smith","year":"2009","unstructured":"Smith, G. J. et al. Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic. Nature 459, 1122\u20131125 (2009).","journal-title":"Nature"},{"key":"4082_CR20","doi-asserted-by":"publisher","first-page":"4395","DOI":"10.1128\/JVI.02642-09","volume":"84","author":"KA Bussey","year":"2010","unstructured":"Bussey, K. A., Bousse, T. L., Desmet, E. A., Kim, B. & Takimoto, T. PB2 residue 271 plays a key role in enhanced polymerase activity of influenza A viruses in mammalian host cells. J. Virol. 84, 4395\u20134406 (2010).","journal-title":"J. Virol."},{"key":"4082_CR21","doi-asserted-by":"publisher","first-page":"21312","DOI":"10.1073\/pnas.0911915106","volume":"106","author":"A Mehle","year":"2009","unstructured":"Mehle, A. & Doudna, J. A. Adaptive strategies of the influenza virus polymerase for replication in humans. Proc. Natl Acad. Sci. 106, 21312\u201321316 (2009).","journal-title":"Proc. Natl Acad. Sci."},{"key":"4082_CR22","doi-asserted-by":"publisher","first-page":"e1001034","DOI":"10.1371\/journal.ppat.1001034","volume":"6","author":"S Yamada","year":"2010","unstructured":"Yamada, S. et al. Biological and structural characterization of a host-adapting amino acid in influenza virus. PLoS Pathog. 6, e1001034 (2010).","journal-title":"PLoS Pathog."},{"key":"4082_CR23","doi-asserted-by":"publisher","first-page":"7020","DOI":"10.1128\/JVI.00522-11","volume":"85","author":"KA Bussey","year":"2011","unstructured":"Bussey, K. A. et al. PA residues in the 2009 H1N1 pandemic influenza virus enhance avian influenza virus polymerase activity in mammalian cells. J. Virol. 85, 7020\u20137028 (2011).","journal-title":"J. Virol."},{"key":"4082_CR24","doi-asserted-by":"publisher","first-page":"1750","DOI":"10.1128\/JVI.06203-11","volume":"86","author":"A Mehle","year":"2012","unstructured":"Mehle, A., Dugan, V. G., Taubenberger, J. K. & Doudna, J. A. Reassortment and mutation of the avian influenza virus polymerase PA subunit overcome species barriers. J. Virol. 86, 1750\u20131757 (2012).","journal-title":"J. Virol."},{"key":"4082_CR25","doi-asserted-by":"crossref","unstructured":"Nogales, A., Martinez-Sobrido, L., Chiem, K., Topham, D. J. & DeDiego, M. L. Functional evolution of the 2009 pandemic H1N1 influenza virus NS1 and PA in humans. J. Virol. 92, e01206\u2013e01218 (2018).","DOI":"10.1128\/JVI.01206-18"},{"key":"4082_CR26","doi-asserted-by":"publisher","first-page":"e1003460","DOI":"10.1371\/journal.ppat.1003460","volume":"9","author":"PL Tsai","year":"2013","unstructured":"Tsai, P. L. et al. Cellular RNA binding proteins NS1-BP and hnRNP K regulate influenza A virus RNA splicing. PLoS Pathog. 9, e1003460 (2013).","journal-title":"PLoS Pathog."},{"key":"4082_CR27","doi-asserted-by":"publisher","first-page":"e0188214","DOI":"10.1371\/journal.pone.0188214","volume":"12","author":"CK Chang","year":"2017","unstructured":"Chang, C. K. et al. Cellular hnRNP A2\/B1 interacts with the NP of influenza A virus and impacts viral replication. PLoS One 12, e0188214 (2017).","journal-title":"PLoS One"},{"key":"4082_CR28","doi-asserted-by":"publisher","first-page":"167460","DOI":"10.1016\/j.jmb.2022.167460","volume":"434","author":"CM de Rozieres","year":"2022","unstructured":"de Rozieres, C. M. et al. PABP1 drives the selective translation of influenza A virus mRNA. J. Mol. Biol. 434, 167460 (2022).","journal-title":"J. Mol. Biol."},{"key":"4082_CR29","doi-asserted-by":"publisher","first-page":"166922","DOI":"10.1016\/j.jmb.2021.166922","volume":"433","author":"B Dumoulin","year":"2021","unstructured":"Dumoulin, B., Ufer, C., Kuhn, H. & Sofi, S. Expression regulation, protein chemistry and functional biology of the Guanine-Rich Sequence Binding Factor 1 (GRSF1). J. Mol. Biol. 433, 166922 (2021).","journal-title":"J. Mol. Biol."},{"key":"4082_CR30","doi-asserted-by":"publisher","first-page":"6694","DOI":"10.1073\/pnas.96.12.6694","volume":"96","author":"YW Park","year":"1999","unstructured":"Park, Y. W., Wilusz, J. & Katze, M. G. Regulation of eukaryotic protein synthesis: selective influenza viral mRNA translation is mediated by the cellular RNA-binding protein GRSF-1. Proc. Natl Acad. Sci. USA 96, 6694\u20136699 (1999).","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"4082_CR31","doi-asserted-by":"publisher","first-page":"10417","DOI":"10.1128\/JVI.76.20.10417-10426.2002","volume":"76","author":"JC Kash","year":"2002","unstructured":"Kash, J. C. et al. Selective translation of eukaryotic mRNAs: functional molecular analysis of GRSF-1, a positive regulator of influenza virus protein synthesis. J. Virol. 76, 10417\u201310426 (2002).","journal-title":"J. Virol."},{"key":"4082_CR32","doi-asserted-by":"publisher","first-page":"239","DOI":"10.1128\/MMBR.64.2.239-280.2000","volume":"64","author":"M Gale Jr.","year":"2000","unstructured":"Gale, M. Jr., Tan, S. L. & Katze, M. G. Translational control of viral gene expression in eukaryotes. Microbiol Mol. Biol. Rev. 64, 239\u2013280 (2000).","journal-title":"Microbiol Mol. Biol. Rev."},{"key":"4082_CR33","doi-asserted-by":"publisher","first-page":"e104631","DOI":"10.1371\/journal.pone.0104631","volume":"9","author":"A Nieradka","year":"2014","unstructured":"Nieradka, A. et al. Grsf1-induced translation of the SNARE protein Use1 is required for expansion of the erythroid compartment. PLoS One 9, e104631 (2014).","journal-title":"PLoS One"},{"key":"4082_CR34","doi-asserted-by":"publisher","first-page":"1838","DOI":"10.1101\/gad.466308","volume":"22","author":"C Ufer","year":"2008","unstructured":"Ufer, C. et al. Translational regulation of glutathione peroxidase 4 expression through guanine-rich sequence-binding factor 1 is essential for embryonic brain development. Genes Dev. 22, 1838\u20131850 (2008).","journal-title":"Genes Dev."},{"key":"4082_CR35","doi-asserted-by":"publisher","first-page":"851","DOI":"10.1007\/s00439-016-1683-5","volume":"135","author":"T Geuens","year":"2016","unstructured":"Geuens, T., Bouhy, D. & Timmerman, V. The hnRNP family: insights into their role in health and disease. Hum. Genet 135, 851\u2013867 (2016).","journal-title":"Hum. Genet"},{"key":"4082_CR36","doi-asserted-by":"publisher","first-page":"8042","DOI":"10.1128\/JVI.00901-15","volume":"89","author":"T Hayashi","year":"2015","unstructured":"Hayashi, T., Wills, S., Bussey, K. A. & Takimoto, T. Identification of influenza A virus PB2 residues involved in enhanced polymerase activity and virus growth in mammalian cells at low temperatures. J. Virol. 89, 8042\u20138049 (2015).","journal-title":"J. Virol."},{"key":"4082_CR37","first-page":"22","volume":"15","author":"HA King","year":"2016","unstructured":"King, H. A. & Gerber, A. P. Translatome profiling: methods for genome-scale analysis of mRNA translation. Brief. Funct. Genomics 15, 22\u201331 (2016).","journal-title":"Brief. Funct. Genomics"},{"key":"4082_CR38","doi-asserted-by":"publisher","first-page":"113","DOI":"10.1038\/nrm2838","volume":"11","author":"RJ Jackson","year":"2010","unstructured":"Jackson, R. J., Hellen, C. U. & Pestova, T. V. The mechanism of eukaryotic translation initiation and principles of its regulation. Nat. Rev. Mol. Cell Biol. 11, 113\u2013127 (2010).","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"4082_CR39","doi-asserted-by":"crossref","unstructured":"Panda AC, Martindale JL & Gorospe M. Polysome fractionation to analyze mRNA distribution profiles. Bio. Protoc. 7, e2126 (2017).","DOI":"10.21769\/BioProtoc.2126"},{"key":"4082_CR40","doi-asserted-by":"crossref","unstructured":"Gandin, V. et al. Polysome fractionation and analysis of mammalian translatomes on a genome-wide scale. J. Vis. Exp. 1, 51455 (2014).","DOI":"10.3791\/51455"},{"key":"4082_CR41","doi-asserted-by":"publisher","first-page":"7789","DOI":"10.1128\/JVI.00600-06","volume":"80","author":"K Hara","year":"2006","unstructured":"Hara, K., Schmidt, F. I., Crow, M. & Brownlee, G. G. Amino acid residues in the N-terminal region of the PA subunit of influenza A virus RNA polymerase play a critical role in protein stability, endonuclease activity, cap binding, and virion RNA promoter binding. J. Virol. 80, 7789\u20137798 (2006).","journal-title":"J. Virol."},{"key":"4082_CR42","doi-asserted-by":"publisher","first-page":"914","DOI":"10.1038\/nature07745","volume":"458","author":"A Dias","year":"2009","unstructured":"Dias, A. et al. The cap-snatching endonuclease of influenza virus polymerase resides in the PA subunit. Nature 458, 914\u2013918 (2009).","journal-title":"Nature"},{"key":"4082_CR43","doi-asserted-by":"publisher","first-page":"13269","DOI":"10.1128\/JVI.01636-14","volume":"88","author":"RA Elderfield","year":"2014","unstructured":"Elderfield, R. A. et al. Accumulation of human-adapting mutations during circulation of A(H1N1)pdm09 influenza virus in humans in the United Kingdom. J. Virol. 88, 13269\u201313283 (2014).","journal-title":"J. Virol."},{"key":"4082_CR44","doi-asserted-by":"publisher","DOI":"10.1038\/s41598-019-42614-y","volume":"9","author":"TR Klingen","year":"2019","unstructured":"Klingen, T. R., Loers, J., Stanelle-Bertram, S., Gabriel, G. & McHardy, A. C. Structures and functions linked to genome-wide adaptation of human influenza A viruses. Sci. Rep. 9, 6267 (2019).","journal-title":"Sci. Rep."},{"key":"4082_CR45","doi-asserted-by":"publisher","first-page":"3472","DOI":"10.1093\/gbe\/evv240","volume":"7","author":"SS Belanov","year":"2015","unstructured":"Belanov, S. S. et al. Genome-wide analysis of evolutionary markers of human influenza A(H1N1)pdm09 and A(H3N2) viruses may guide selection of vaccine strain candidates. Genome Biol. Evol. 7, 3472\u20133483 (2015).","journal-title":"Genome Biol. Evol."},{"key":"4082_CR46","doi-asserted-by":"publisher","first-page":"199","DOI":"10.1126\/science.1222213","volume":"337","author":"B Jagger","year":"2012","unstructured":"Jagger, B. et al. An overlapping protein-coding region in influenza A virus segment 3 modulates the host response. Science 337, 199\u2013204 (2012).","journal-title":"Science"},{"key":"4082_CR47","doi-asserted-by":"publisher","first-page":"7131","DOI":"10.1128\/JVI.00954-16","volume":"90","author":"T Hayashi","year":"2016","unstructured":"Hayashi, T., Chaimayo, C., McGuinness, J. & Takimoto, T. Critical role of the PA-X C-terminal domain of influenza A virus in its subcellular localization and shutoff activity. J. Virol. 90, 7131\u20137141 (2016).","journal-title":"J. Virol."},{"key":"4082_CR48","doi-asserted-by":"publisher","first-page":"3108","DOI":"10.1128\/JVI.02826-12","volume":"87","author":"EA Desmet","year":"2013","unstructured":"Desmet, E. A., Bussey, K. A., Stone, R. & Takimoto, T. Identification of the N-terminal domain of the influenza virus PA responsible for the suppression of host protein synthesis. J. Virol. 87, 3108\u20133118 (2013).","journal-title":"J. Virol."},{"key":"4082_CR49","doi-asserted-by":"publisher","first-page":"e1005427","DOI":"10.1371\/journal.ppat.1005427","volume":"12","author":"DA Khaperskyy","year":"2016","unstructured":"Khaperskyy, D. A., Schmaling, S., Larkins-Ford, J., McCormick, C. & Gaglia, M. M. Selective degradation of host RNA polymerase II transcripts by influenza A virus PA-X host shutoff protein. PLoS Pathog. 12, e1005427 (2016).","journal-title":"PLoS Pathog."},{"key":"4082_CR50","doi-asserted-by":"publisher","first-page":"391","DOI":"10.1016\/0092-8674(81)90208-7","volume":"26","author":"C Herz","year":"1981","unstructured":"Herz, C., Stavnezer, E., Krug, R. M. & Gurney, T. Influenza virus, an RNA virus, synthesizes its messenger RNA in the nucleus of infected cells. Cell 26, 391\u2013400 (1981).","journal-title":"Cell"},{"key":"4082_CR51","doi-asserted-by":"publisher","first-page":"1290","DOI":"10.1099\/vir.0.018564-0","volume":"91","author":"EK Read","year":"2010","unstructured":"Read, E. K. & Digard, P. Individual influenza A virus mRNAs show differential dependence on cellular NXF1\/TAP for their nuclear export. J. Gen. Virol. 91, 1290\u20131301 (2010).","journal-title":"J. Gen. Virol."},{"key":"4082_CR52","doi-asserted-by":"publisher","first-page":"117","DOI":"10.1038\/nature20594","volume":"541","author":"M Lukarska","year":"2017","unstructured":"Lukarska, M. et al. Structural basis of an essential interaction between influenza polymerase and Pol II CTD. Nature 541, 117\u2013121 (2017).","journal-title":"Nature"},{"key":"4082_CR53","doi-asserted-by":"publisher","first-page":"287","DOI":"10.1038\/s41586-019-1530-7","volume":"573","author":"H Fan","year":"2019","unstructured":"Fan, H. et al. Structures of influenza A virus RNA polymerase offer insight into viral genome replication. Nature 573, 287\u2013290 (2019).","journal-title":"Nature"},{"key":"4082_CR54","doi-asserted-by":"publisher","first-page":"909","DOI":"10.1038\/nature07720","volume":"458","author":"P Yuan","year":"2009","unstructured":"Yuan, P. et al. Crystal structure of an avian influenza polymerase PA(N) reveals an endonuclease active site. Nature 458, 909\u2013913 (2009).","journal-title":"Nature"},{"key":"4082_CR55","doi-asserted-by":"publisher","first-page":"399","DOI":"10.1016\/j.cmet.2013.02.005","volume":"17","author":"AA Jourdain","year":"2013","unstructured":"Jourdain, A. A. et al. GRSF1 regulates RNA processing in mitochondrial RNA granules. Cell Metab. 17, 399\u2013410 (2013).","journal-title":"Cell Metab."},{"key":"4082_CR56","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-018-05007-9","volume":"9","author":"Z Pietras","year":"2018","unstructured":"Pietras, Z. et al. Dedicated surveillance mechanism controls G-quadruplex forming non-coding RNAs in human mitochondria. Nat. Commun. 9, 2558 (2018).","journal-title":"Nat. Commun."},{"key":"4082_CR57","doi-asserted-by":"publisher","first-page":"295","DOI":"10.1159\/000134359","volume":"73","author":"SS Banga","year":"1996","unstructured":"Banga, S. S., Ozer, H. L. & Wilusz, J. Assignment of GRSF1 encoding a poly(A)+ mRNA binding protein to human chromosome 4q13. Cytogenet Cell Genet 73, 295\u2013296 (1996).","journal-title":"Cytogenet Cell Genet"},{"key":"4082_CR58","doi-asserted-by":"publisher","first-page":"946","DOI":"10.1016\/j.bbagen.2017.12.009","volume":"1862","author":"S Sofi","year":"2018","unstructured":"Sofi, S. et al. Functional characterization of isolated RNA-binding domains of the GRSF1 protein. Biochim Biophys. Acta Gen. Subj. 1862, 946\u2013957 (2018).","journal-title":"Biochim Biophys. Acta Gen. Subj."},{"key":"4082_CR59","doi-asserted-by":"publisher","first-page":"495","DOI":"10.1002\/wrna.1113","volume":"3","author":"S Millevoi","year":"2012","unstructured":"Millevoi, S., Moine, H. & Vagner, S. G-quadruplexes in RNA biology. Wiley Interdiscip. Rev. RNA 3, 495\u2013507 (2012).","journal-title":"Wiley Interdiscip. Rev. RNA"},{"key":"4082_CR60","doi-asserted-by":"publisher","DOI":"10.1038\/srep15793","volume":"5","author":"G Song","year":"2015","unstructured":"Song, G. et al. miR-346 and miR-138 competitively regulate hTERT in GRSF1- and AGO2-dependent manners, respectively. Sci. Rep. 5, 15793 (2015).","journal-title":"Sci. Rep."},{"key":"4082_CR61","doi-asserted-by":"publisher","first-page":"22223","DOI":"10.1016\/S0021-9258(18)41511-6","volume":"268","author":"MS Garfinkel","year":"1993","unstructured":"Garfinkel, M. S. & Katze, M. G. Translational control by influenza virus. Selective translation is mediated by sequences within the viral mRNA 5\u2019-untranslated region. J. Biol. Chem. 268, 22223\u201322226 (1993).","journal-title":"J. Biol. Chem."},{"key":"4082_CR62","doi-asserted-by":"publisher","first-page":"479","DOI":"10.1016\/j.cmet.2020.07.017","volume":"32","author":"H Antonicka","year":"2020","unstructured":"Antonicka, H. et al. A high-density human mitochondrial proximity interaction network. Cell Metab. 32, 479\u2013497 e479 (2020).","journal-title":"Cell Metab."},{"key":"4082_CR63","doi-asserted-by":"publisher","first-page":"2552","DOI":"10.1128\/MCB.00230-09","volume":"30","author":"CM Van Dusen","year":"2010","unstructured":"Van Dusen, C. M., Yee, L., McNally, L. M. & McNally, M. T. A glycine-rich domain of hnRNP H\/F promotes nucleocytoplasmic shuttling and nuclear import through an interaction with transportin 1. Mol. Cell Biol. 30, 2552\u20132562 (2010).","journal-title":"Mol. Cell Biol."},{"key":"4082_CR64","doi-asserted-by":"publisher","first-page":"2334","DOI":"10.1093\/nar\/22.12.2334","volume":"22","author":"Z Qian","year":"1994","unstructured":"Qian, Z. & Wilusz, J. GRSF-1: a poly(A)+ mRNA binding protein which interacts with a conserved G-rich element. Nucleic Acids Res 22, 2334\u20132343 (1994).","journal-title":"Nucleic Acids Res"},{"key":"4082_CR65","doi-asserted-by":"publisher","first-page":"129678","DOI":"10.1016\/j.bbagen.2020.129678","volume":"1864","author":"B Dumoulin","year":"2020","unstructured":"Dumoulin, B. et al. Identification of the COMM-domain containing protein 1 as specific binding partner for the guanine-rich RNA sequence binding factor 1. Biochim Biophys. Acta Gen. Subj. 1864, 129678 (2020).","journal-title":"Biochim Biophys. Acta Gen. Subj."},{"key":"4082_CR66","doi-asserted-by":"publisher","first-page":"5052","DOI":"10.1093\/nar\/gkv333","volume":"43","author":"D Koppstein","year":"2015","unstructured":"Koppstein, D., Ashour, J. & Bartel, D. P. Sequencing the cap-snatching repertoire of H1N1 influenza provides insight into the mechanism of viral transcription initiation. Nucleic Acids Res 43, 5052\u20135064 (2015).","journal-title":"Nucleic Acids Res"},{"key":"4082_CR67","doi-asserted-by":"publisher","first-page":"2067","DOI":"10.1261\/rna.054221.115","volume":"21","author":"W Gu","year":"2015","unstructured":"Gu, W. et al. Influenza A virus preferentially snatches noncoding RNA caps. RNA 21, 2067\u20132075 (2015).","journal-title":"RNA"},{"key":"4082_CR68","doi-asserted-by":"publisher","first-page":"e94257","DOI":"10.1371\/journal.pone.0094257","volume":"9","author":"S Kummer","year":"2014","unstructured":"Kummer, S. et al. Alteration of protein levels during influenza virus H1N1 infection in host cells: a proteomic survey of host and virus reveals differential dynamics. PLoS One 9, e94257 (2014).","journal-title":"PLoS One"},{"key":"4082_CR69","doi-asserted-by":"crossref","unstructured":"Phan, T. et al. Segment-specific kinetics of mRNA, cRNA and vRNA accumulation during influenza infection. J. Virol. 95, e02102\u2013e02120 (2021).","DOI":"10.1128\/JVI.02102-20"},{"key":"4082_CR70","doi-asserted-by":"publisher","first-page":"723","DOI":"10.1099\/0022-1317-83-4-723","volume":"83","author":"A Portela","year":"2002","unstructured":"Portela, A. & Digard, P. The influenza virus nucleoprotein: a multifunctional RNA-binding protein pivotal to virus replication. J. Gen. Virol. 83, 723\u2013734 (2002).","journal-title":"J. Gen. Virol."},{"key":"4082_CR71","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.coviro.2015.01.007","volume":"12","author":"RM Krug","year":"2015","unstructured":"Krug, R. M. Functions of the influenza A virus NS1 protein in antiviral defense. Curr. Opin. Virol. 12, 1\u20136 (2015).","journal-title":"Curr. Opin. Virol."},{"key":"4082_CR72","doi-asserted-by":"publisher","first-page":"2427","DOI":"10.1128\/jvi.69.4.2427-2433.1995","volume":"69","author":"S de la Luna","year":"1995","unstructured":"de la Luna, S., Fortes, P., Beloso, A. & Ortin, J. Influenza virus NS1 protein enhances the rate of translation initiation of viral mRNAs. J. Virol. 69, 2427\u20132433 (1995).","journal-title":"J. Virol."},{"key":"4082_CR73","doi-asserted-by":"publisher","first-page":"e1007465","DOI":"10.1371\/journal.ppat.1007465","volume":"14","author":"C Chaimayo","year":"2018","unstructured":"Chaimayo, C., Dunagan, M., Hayashi, T., Santoso, N. & Takimoto, T. Specificity and functional interplay between influenza virus PA-X and NS1 shutoff activity. PLoS Pathog. 14, e1007465 (2018).","journal-title":"PLoS Pathog."},{"key":"4082_CR74","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.jviromet.2010.12.014","volume":"173","author":"E Kawakami","year":"2011","unstructured":"Kawakami, E. et al. Strand-specific real-time RT-PCR for distinguishing influenza vRNA, cRNA, and mRNA. J. Virol. Methods 173, 1\u20136 (2011).","journal-title":"J. Virol. Methods"},{"key":"4082_CR75","doi-asserted-by":"publisher","first-page":"51","DOI":"10.1016\/j.virol.2012.01.015","volume":"426","author":"LA MacDonald","year":"2012","unstructured":"MacDonald, L. A. et al. Molecular interactions and trafficking of influenza A virus polymerase proteins analyzed by specific monoclonal antibodies. Virology 426, 51\u201359 (2012).","journal-title":"Virology"},{"key":"4082_CR76","doi-asserted-by":"publisher","first-page":"493","DOI":"10.1093\/oxfordjournals.aje.a118408","volume":"27","author":"LJ Reed","year":"1938","unstructured":"Reed, L. J. & Muench, H. A simple method of estimating fifty percent endpoints. Am. J. Epidemiol. 27, 493\u2013497 (1938).","journal-title":"Am. J. Epidemiol."}],"container-title":["Communications Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s42003-022-04082-5.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s42003-022-04082-5","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s42003-022-04082-5.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,10,17]],"date-time":"2022-10-17T18:04:28Z","timestamp":1666029868000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s42003-022-04082-5"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,10,17]]},"references-count":76,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2022,12]]}},"alternative-id":["4082"],"URL":"https:\/\/doi.org\/10.1038\/s42003-022-04082-5","relation":{},"ISSN":["2399-3642"],"issn-type":[{"value":"2399-3642","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,10,17]]},"assertion":[{"value":"20 May 2022","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"6 October 2022","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"17 October 2022","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"1102"}}