دورية أكاديمية
BTN3A3 evasion promotes the zoonotic potential of influenza A viruses.
العنوان: | BTN3A3 evasion promotes the zoonotic potential of influenza A viruses. |
---|---|
المؤلفون: | Pinto RM; MRC-University of Glasgow Centre for Virus Research, Glasgow, UK.; The Roslin Institute, University of Edinburgh, Edinburgh, UK., Bakshi S; MRC-University of Glasgow Centre for Virus Research, Glasgow, UK., Lytras S; MRC-University of Glasgow Centre for Virus Research, Glasgow, UK., Zakaria MK; MRC-University of Glasgow Centre for Virus Research, Glasgow, UK., Swingler S; MRC-University of Glasgow Centre for Virus Research, Glasgow, UK., Worrell JC; School of Infection and Immunity, University of Glasgow, Glasgow, UK., Herder V; MRC-University of Glasgow Centre for Virus Research, Glasgow, UK., Hargrave KE; School of Infection and Immunity, University of Glasgow, Glasgow, UK., Varjak M; MRC-University of Glasgow Centre for Virus Research, Glasgow, UK.; Faculty of Science and Technology, Institute of Technology, University of Tartu, Tartu, Estonia., Cameron-Ruiz N; MRC-University of Glasgow Centre for Virus Research, Glasgow, UK., Collados Rodriguez M; MRC-University of Glasgow Centre for Virus Research, Glasgow, UK., Varela M; MRC-University of Glasgow Centre for Virus Research, Glasgow, UK., Wickenhagen A; MRC-University of Glasgow Centre for Virus Research, Glasgow, UK., Loney C; MRC-University of Glasgow Centre for Virus Research, Glasgow, UK., Pei Y; Department of Pathobiology, University of Guelph, Guelph, Ontario, Canada., Hughes J; MRC-University of Glasgow Centre for Virus Research, Glasgow, UK., Valette E; MRC-University of Glasgow Centre for Virus Research, Glasgow, UK., Turnbull ML; MRC-University of Glasgow Centre for Virus Research, Glasgow, UK., Furnon W; MRC-University of Glasgow Centre for Virus Research, Glasgow, UK., Gu Q; MRC-University of Glasgow Centre for Virus Research, Glasgow, UK., Orr L; MRC-University of Glasgow Centre for Virus Research, Glasgow, UK., Taggart A; MRC-University of Glasgow Centre for Virus Research, Glasgow, UK., Diebold O; The Roslin Institute, University of Edinburgh, Edinburgh, UK., Davis C; MRC-University of Glasgow Centre for Virus Research, Glasgow, UK., Boutell C; MRC-University of Glasgow Centre for Virus Research, Glasgow, UK., Grey F; The Roslin Institute, University of Edinburgh, Edinburgh, UK., Hutchinson E; MRC-University of Glasgow Centre for Virus Research, Glasgow, UK., Digard P; The Roslin Institute, University of Edinburgh, Edinburgh, UK., Monne I; Istituto Zooprofilattico Sperimentale delle Venezie (IZSVe), Legnaro, Italy., Wootton SK; Department of Pathobiology, University of Guelph, Guelph, Ontario, Canada., MacLeod MKL; School of Infection and Immunity, University of Glasgow, Glasgow, UK., Wilson SJ; MRC-University of Glasgow Centre for Virus Research, Glasgow, UK., Palmarini M; MRC-University of Glasgow Centre for Virus Research, Glasgow, UK. massimo.palmarini@glasgow.ac.uk. |
المصدر: | Nature [Nature] 2023 Jul; Vol. 619 (7969), pp. 338-347. Date of Electronic Publication: 2023 Jun 28. |
نوع المنشور: | Journal Article |
اللغة: | English |
بيانات الدورية: | Publisher: Nature Publishing Group Country of Publication: England NLM ID: 0410462 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1476-4687 (Electronic) Linking ISSN: 00280836 NLM ISO Abbreviation: Nature Subsets: MEDLINE |
أسماء مطبوعة: | Publication: Basingstoke : Nature Publishing Group Original Publication: London, Macmillan Journals ltd. |
مواضيع طبية MeSH: | Birds*/virology , Host Microbial Interactions* , Influenza A virus*/classification , Influenza A virus*/genetics , Influenza A virus*/growth & development , Influenza A virus*/isolation & purification , Influenza in Birds*/transmission , Influenza in Birds*/virology , Influenza, Human*/prevention & control , Influenza, Human*/transmission , Influenza, Human*/virology , Viral Zoonoses*/prevention & control , Viral Zoonoses*/transmission , Viral Zoonoses*/virology, Animals ; Humans ; Primates ; Respiratory System/metabolism ; Respiratory System/virology ; Risk Assessment ; Virus Replication |
مستخلص: | Spillover events of avian influenza A viruses (IAVs) to humans could represent the first step in a future pandemic 1 . Several factors that limit the transmission and replication of avian IAVs in mammals have been identified. There are several gaps in our understanding to predict which virus lineages are more likely to cross the species barrier and cause disease in humans 1 . Here, we identified human BTN3A3 (butyrophilin subfamily 3 member A3) 2 as a potent inhibitor of avian IAVs but not human IAVs. We determined that BTN3A3 is expressed in human airways and its antiviral activity evolved in primates. We show that BTN3A3 restriction acts primarily at the early stages of the virus life cycle by inhibiting avian IAV RNA replication. We identified residue 313 in the viral nucleoprotein (NP) as the genetic determinant of BTN3A3 sensitivity (313F or, rarely, 313L in avian viruses) or evasion (313Y or 313V in human viruses). However, avian IAV serotypes, such as H7 and H9, that spilled over into humans also evade BTN3A3 restriction. In these cases, BTN3A3 evasion is due to substitutions (N, H or Q) in NP residue 52 that is adjacent to residue 313 in the NP structure 3 . Thus, sensitivity or resistance to BTN3A3 is another factor to consider in the risk assessment of the zoonotic potential of avian influenza viruses. (© 2023. The Author(s), under exclusive licence to Springer Nature Limited.) |
التعليقات: | Comment in: Nat Rev Microbiol. 2023 Sep;21(9):551. (PMID: 37407721) |
References: | Lipsitch, M. et al. Viral factors in influenza pandemic risk assessment. eLife https://doi.org/10.7554/eLife.18491 (2016). Afrache, H., Gouret, P., Ainouche, S., Pontarotti, P. & Olive, D. The butyrophilin (BTN) gene family: from milk fat to the regulation of the immune response. Immunogenetics 64, 781–794 (2012). (PMID: 2300094410.1007/s00251-012-0619-z) Ye, Q., Krug, R. M. & Tao, Y. J. The mechanism by which influenza A virus nucleoprotein forms oligomers and binds RNA. Nature 444, 1078–1082 (2006). (PMID: 1715160310.1038/nature05379) Yoon, S.-W., Webby, R. J. & Webster, R. G. in Influenza Pathogenesis and Control Vol. I (eds W. Compans, R. A. & Oldstone, M. B. A.) 359–375 (Springer International Publishing, 2014). Krammer, F. et al. Influenza. Nat. Rev. Dis. Primers 4, 3 (2018). (PMID: 29955068709746710.1038/s41572-018-0002-y) Harrington, W. N., Kackos, C. M. & Webby, R. J. The evolution and future of influenza pandemic preparedness. Exp. Mol. Med. 53, 737–749 (2021). (PMID: 33953324809971210.1038/s12276-021-00603-0) Short, K. R. et al. One health, multiple challenges: the inter-species transmission of influenza A virus. One Health 1, 1–13 (2015). (PMID: 26309905454201110.1016/j.onehlt.2015.03.001) Liu, D. et al. Origin and diversity of novel avian influenza A H7N9 viruses causing human infection: phylogenetic, structural, and coalescent analyses. Lancet 381, 1926–1932 (2013). (PMID: 2364311110.1016/S0140-6736(13)60938-1) Wang, X. et al. Epidemiology of avian influenza A H7N9 virus in human beings across five epidemics in mainland China, 2013–17: an epidemiological study of laboratory-confirmed case series. Lancet Infect. Dis. 17, 822–832 (2017). (PMID: 28583578598858410.1016/S1473-3099(17)30323-7) Liu, W. J. et al. Avian influenza A (H7N9) virus: from low pathogenic to highly pathogenic. Front. Med. 15, 507–527 (2021). (PMID: 33860875819073410.1007/s11684-020-0814-5) 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, 67–81 (2019). (PMID: 3048753610.1038/s41579-018-0115-z) Rogers, G. N. & Paulson, J. C. Receptor determinants of human and animal influenza virus isolates: differences in receptor specificity of the H3 hemagglutinin based on species of origin. Virology 127, 361–373 (1983). (PMID: 686837010.1016/0042-6822(83)90150-2) Di Lella, S., Herrmann, A. & Mair, C. M. Modulation of the pH stability of influenza virus hemagglutinin: a host cell adaptation strategy. Biophys. J. 110, 2293–2301 (2016). (PMID: 27276248490616010.1016/j.bpj.2016.04.035) Zaraket, H. et al. Increased acid stability of the hemagglutinin protein enhances H5N1 influenza virus growth in the upper respiratory tract but is insufficient for transmission in ferrets. J. Virol. 87, 9911–9922 (2013). (PMID: 23824818375410010.1128/JVI.01175-13) Long, J. S. et al. Species difference in ANP32A underlies influenza A virus polymerase host restriction. Nature 529, 101–104 (2016). (PMID: 26738596471067710.1038/nature16474) Blumenkrantz, D., Roberts, K. L., Shelton, H., Lycett, S. & Barclay, W. S. The short stalk length of highly pathogenic avian influenza H5N1 virus neuraminidase limits transmission of pandemic H1N1 virus in ferrets. J. Virol. 87, 10539–10551 (2013). (PMID: 23864615380740910.1128/JVI.00967-13) Park, S. et al. Adaptive mutations of neuraminidase stalk truncation and deglycosylation confer enhanced pathogenicity of influenza A viruses. Sci. Rep. 7, 10928 (2017). (PMID: 28883554558976710.1038/s41598-017-11348-0) Mänz, B. et al. Pandemic influenza A viruses escape from restriction by human MxA through adaptive mutations in the nucleoprotein. PLoS Pathog. 9, e1003279 (2013). (PMID: 23555271361064310.1371/journal.ppat.1003279) Riegger, D. et al. The nucleoprotein of newly emerged H7N9 influenza A virus harbors a unique motif conferring resistance to antiviral human MxA. J. Virol. 89, 2241–2252 (2015). (PMID: 2550506710.1128/JVI.02406-14) Shaw, A. E. et al. Fundamental properties of the mammalian innate immune system revealed by multispecies comparison of type I interferon responses. PLoS Biol. 15, e2004086 (2017). (PMID: 29253856574750210.1371/journal.pbio.2004086) Kane, M. et al. Identification of interferon-stimulated genes with antiretroviral activity. Cell Host Microbe. 20, 392–405 (2016). (PMID: 27631702502669810.1016/j.chom.2016.08.005) Feeley, E. M. et al. IFITM3 inhibits influenza A virus infection by preventing cytosolic entry. PLoS Pathog. 7, e1002337 (2011). (PMID: 22046135320318810.1371/journal.ppat.1002337) Verhelst, J., Parthoens, E., Schepens, B., Fiers, W. & Saelens, X. Interferon-inducible protein Mx1 inhibits influenza virus by interfering with functional viral ribonucleoprotein complex assembly. J. Virol. 86, 13445–13455 (2012). (PMID: 23015724350304810.1128/JVI.01682-12) Wellington, D., Laurenson-Schafer, H., Abdel-Haq, A. & Dong, T. IFITM3: how genetics influence influenza infection demographically. Biomed. J. 42, 19–26 (2019). (PMID: 30987701646811510.1016/j.bj.2019.01.004) Rhodes, D. A., Stammers, M., Malcherek, G., Beck, S. & Trowsdale, J. The cluster of BTN genes in the extended major histocompatibility complex. Genomics 71, 351–362 (2001). (PMID: 1117075210.1006/geno.2000.6406) Kumar, S., Stecher, G., Suleski, M. & Hedges, S. B. TimeTree: a resource for timelines, timetrees, and divergence times. Mol. Biol. Evol. 34, 1812–1819 (2017). (PMID: 2838784110.1093/molbev/msx116) Afrache, H., Pontarotti, P., Abi-Rached, L. & Olive, D. Evolutionary and polymorphism analyses reveal the central role of BTN3A2 in the concerted evolution of the BTN3 gene family. Immunogenetics 69, 379–390 (2017). (PMID: 2838251510.1007/s00251-017-0980-z) Pinto, R. M., Lycett, S., Gaunt, E. & Digard, P. Accessory gene products of influenza A virus. Cold Spring Harb. Perspect. Med. https://doi.org/10.1101/cshperspect.a038380 (2021). Naffakh, N., Tomoiu, A., Rameix-Welti, M. A. & van der Werf, S. Host restriction of avian influenza viruses at the level of the ribonucleoproteins. Annu. Rev. Microbiol. 62, 403–424 (2008). (PMID: 1878584110.1146/annurev.micro.62.081307.162746) Patrono, L. V. et al. Archival influenza virus genomes from Europe reveal genomic variability during the 1918 pandemic. Nat. Commun. 13, 2314 (2022). (PMID: 35538057909092510.1038/s41467-022-29614-9) van Lieshout, L. P. et al. A novel triple-mutant AAV6 capsid induces rapid and potent transgene expression in the muscle and respiratory tract of mice. Mol. Ther. Methods Clin. Dev. 9, 323–329 (2018). (PMID: 30038936605470210.1016/j.omtm.2018.04.005) Portela, A. & Digard, P. The influenza virus nucleoprotein: a multifunctional RNA-binding protein pivotal to virus replication. J. Gen. Virol. 83, 723–734 (2002). (PMID: 1190732010.1099/0022-1317-83-4-723) Gabriel, G., Herwig, A. & Klenk, H. D. Interaction of polymerase subunit PB2 and NP with importin alpha1 is a determinant of host range of influenza A virus. PLoS Pathog. 4, e11 (2008). (PMID: 18248089222295310.1371/journal.ppat.0040011) Hu, Y., Sneyd, H., Dekant, R. & Wang, J. Influenza A virus nucleoprotein: a highly conserved multi-functional viral protein as a hot antiviral drug target. Curr. Top. Med. Chem. 17, 2271–2285 (2017). (PMID: 28240183596787710.2174/1568026617666170224122508) Beaton, A. R. & Krug, R. M. Transcription antitermination during influenza viral template RNA synthesis requires the nucleocapsid protein and the absence of a 5′ capped end. Proc. Natl Acad. Sci. USA 83, 6282–6286 (1986). (PMID: 346269538648710.1073/pnas.83.17.6282) Chen, Y. et al. Rare variant MX1 alleles increase human susceptibility to zoonotic H7N9 influenza virus. Science 373, 918–922 (2021). (PMID: 3441323610.1126/science.abg5953) Pu, J. et al. Evolution of the H9N2 influenza genotype that facilitated the genesis of the novel H7N9 virus. Proc. Natl Acad. Sci. USA 112, 548–553 (2015). (PMID: 2554818910.1073/pnas.1422456112) He, J. et al. Genetic characterization of the first detected human case of avian influenza A (H5N6) in Anhui Province, East China. Sci. Rep. 8, 15282 (2018). (PMID: 30327485619142410.1038/s41598-018-33356-4) de Jong, J. C., Claas, E. C., Osterhaus, A. D., Webster, R. G. & Lim, W. L. A pandemic warning? Nature 389, 554 (1997). (PMID: 9335492709547710.1038/39218) Neumann, G., Chen, H., Gao, G. F., Shu, Y. & Kawaoka, Y. H5N1 influenza viruses: outbreaks and biological properties. Cell Res. 20, 51–61 (2010). (PMID: 1988491010.1038/cr.2009.124) Su, S. et al. Epidemiology, evolution, and pathogenesis of H7N9 influenza viruses in five epidemic waves since 2013 in China. Trends Microbiol. 25, 713–728 (2017). (PMID: 2873461710.1016/j.tim.2017.06.008) Harly, C. et al. Key implication of CD277/butyrophilin-3 (BTN3A) in cellular stress sensing by a major human γδ T-cell subset. Blood 120, 2269–2279 (2012). (PMID: 22767497367964110.1182/blood-2012-05-430470) Arnett, H. A. & Viney, J. L. Immune modulation by butyrophilins. Nat. Rev. Immunol. 14, 559–569 (2014). (PMID: 2506058110.1038/nri3715) Gu, S., Borowska, M. T., Boughter, C. T. & Adams, E. J. Butyrophilin3A proteins and Vγ9Vδ2 T cell activation. Semin. Cell Dev. Biol. 84, 65–74 (2018). (PMID: 29471037612942310.1016/j.semcdb.2018.02.007) Galão, R. P. et al. TRIM25 and ZAP target the Ebola virus ribonucleoprotein complex to mediate interferon-induced restriction. PLoS Pathog. 18, e1010530 (2022). (PMID: 35533151911968510.1371/journal.ppat.1010530) Kuroda, M. et al. Identification of interferon-stimulated genes that attenuate Ebola virus infection. Nat. Commun. 11, 2953 (2020). (PMID: 32528005728989210.1038/s41467-020-16768-7) Staeheli, P., Grob, R., Meier, E., Sutcliffe, J. G. & Haller, O. Influenza virus-susceptible mice carry Mx genes with a large deletion or a nonsense mutation. Mol. Cell. Biol. 8, 4518–4523 (1988). (PMID: 2903437365527) Guénet, J. L. & Bonhomme, F. Wild mice: an ever-increasing contribution to a popular mammalian model. Trends Genet. 19, 24–31 (2003). (PMID: 1249324510.1016/S0168-9525(02)00007-0) Zhang, B. et al. The nucleoprotein of influenza A virus inhibits the innate immune response by inducing mitophagy. Autophagy https://doi.org/10.1080/15548627.2022.2162798 (2023). Philippon, D. A. M., Wu, P., Cowling, B. J. & Lau, E. H. Y. Avian influenza human infections at the human-animal interface. J. Infect. Dis. 222, 528–537 (2020). (PMID: 3215729110.1093/infdis/jiaa105) Adlhoch, C. et al. Avian influenza overview December 2021 - March 2022. EFSA J. 20, e07289 (2022). (PMID: 353869278978176) Agüero, M. et al. Highly pathogenic avian influenza A(H5N1) virus infection in farmed minks, Spain, October 2022. Euro. Surveill. https://doi.org/10.2807/1560-7917.Es.2023.28.3.2300001 (2023). 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, 4395–4406 (2010). (PMID: 20181719286378710.1128/JVI.02642-09) Burke, S. A. & Trock, S. C. Use of influenza risk assessment tool for prepandemic preparedness. Emerg. Infect. Dis. 24, 471–477 (2018). (PMID: 29460739582335610.3201/eid2403.171852) Ramirez, R. D. et al. Immortalization of human bronchial epithelial cells in the absence of viral oncoproteins. Cancer Res. 64, 9027–9034 (2004). (PMID: 1560426810.1158/0008-5472.CAN-04-3703) Wit, E. D. et al. Efficient generation and growth of influenza virus A/PR/8/34 from eight cDNA fragments. Virus Res. 103, 155–161 (2004). (PMID: 1516350410.1016/j.virusres.2004.02.028) Schoggins, J. W. et al. A diverse range of gene products are effectors of the type I interferon antiviral response. Nature 472, 481–485 (2011). (PMID: 21478870340958810.1038/nature09907) Rihn, S. J. et al. TRIM69 inhibits vesicular stomatitis Indiana virus. J. Virol. https://doi.org/10.1128/JVI.00951-19 (2019). Rihn, S. J. et al. A plasmid DNA-launched SARS-CoV-2 reverse genetics system and coronavirus toolkit for COVID-19 research. PLoS Biol. 19, e3001091 (2021). (PMID: 33630831790641710.1371/journal.pbio.3001091) Kawakami, E. et al. Strand-specific real-time RT-PCR for distinguishing influenza vRNA, cRNA, and mRNA. J. Virol. Methods 173, 1–6 (2011). (PMID: 2118586910.1016/j.jviromet.2010.12.014) Bakshi, S., Taylor, J., Strickson, S., McCartney, T. & Cohen, P. Identification of TBK1 complexes required for the phosphorylation of IRF3 and the production of interferon β. Biochem. J. 474, 1163–1174 (2017). (PMID: 2815991210.1042/BCJ20160992) Zufferey, R., Donello, J. E., Trono, D. & Hope, T. J. Woodchuck hepatitis virus posttranscriptional regulatory element enhances expression of transgenes delivered by retroviral vectors. J. Virol. 73, 2886–2892 (1999). (PMID: 1007413610404610.1128/JVI.73.4.2886-2892.1999) Rghei, A. D. et al. Production of adeno-associated virus vectors in cell stacks for preclinical studies in large animal models. J. Vis. Exp. https://doi.org/10.3791/62727 (2021). MacLeod, M. K. et al. Vaccine adjuvants aluminum and monophosphoryl lipid A provide distinct signals to generate protective cytotoxic memory CD8 T cells. Proc. Natl Acad. Sci. USA 108, 7914–7919 (2011). (PMID: 21518876309348310.1073/pnas.1104588108) Camacho, C. et al. BLAST+: architecture and applications. BMC Bioinf. 10, 421 (2009). (PMID: 10.1186/1471-2105-10-421) Cunningham, F. et al. Ensembl 2022. Nucleic Acids Res. 50, D988–d995 (2022). (PMID: 3479140410.1093/nar/gkab1049) Mistry, J., Finn, R. D., Eddy, S. R., Bateman, A. & Punta, M. Challenges in homology search: HMMER3 and convergent evolution of coiled-coil regions. Nucleic Acids Res. 41, e121 (2013). (PMID: 23598997369551310.1093/nar/gkt263) Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013). (PMID: 23329690360331810.1093/molbev/mst010) Suyama, M., Torrents, D. & Bork, P. PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res. 34, W609–W612 (2006). (PMID: 16845082153880410.1093/nar/gkl315) Nguyen, L. T., Schmidt, H. A., von Haeseler, A. & Minh, B. Q. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. 32, 268–274 (2015). (PMID: 2537143010.1093/molbev/msu300) Steinegger, M. & Söding, J. MMseqs2 enables sensitive protein sequence searching for the analysis of massive data sets. Nat. Biotechnol. 35, 1026–1028 (2017). (PMID: 2903537210.1038/nbt.3988) Sagulenko, P., Puller, V. & Neher, R. A. TreeTime: maximum-likelihood phylodynamic analysis. Virus Evol. 4, vex042 (2018). (PMID: 29340210575892010.1093/ve/vex042) Yu, G. Using ggtree to visualize data on tree-like structures. Curr. Protoc. Bioinformatics 69, e96 (2020). (PMID: 32162851) Huerta-Cepas, J., Serra, F. & Bork, P. ETE 3: reconstruction, analysis, and visualization of phylogenomic data. Mol. Biol. Evol. 33, 1635–1638 (2016). (PMID: 26921390486811610.1093/molbev/msw046) Beare, A. S. & Hall, T. S. Recombinant influenza-A viruses as live vaccines for man. Report to the Medical Research Council’s Committee on Influenza and other Respiratory Virus Vaccines. Lancet 2, 1271–1273 (1971). (PMID: 414353110.1016/S0140-6736(71)90597-6) Beare, A. S., Schild, G. C. & Craig, J. W. Trials in man with live recombinants made from A/PR/8/34 (H0 N1) and wild H3 N2 influenza viruses. Lancet 2, 729–732 (1975). (PMID: 5276810.1016/S0140-6736(75)90720-5) |
معلومات مُعتمدة: | MC_UU_00034/2 United Kingdom MRC_ Medical Research Council; MR/T029188/1 United Kingdom MRC_ Medical Research Council; MR/N008618/1 United Kingdom MRC_ Medical Research Council; MR/K024752/1 United Kingdom MRC_ Medical Research Council; 210703/Z/18/Z United Kingdom WT_ Wellcome Trust; MC_UU_12014/10 United Kingdom MRC_ Medical Research Council; MR/V01157X/1 United Kingdom MRC_ Medical Research Council; MC_UU_00034/8 United Kingdom MRC_ Medical Research Council; MC_UU_12014/5 United Kingdom MRC_ Medical Research Council; MR/P022642/1 United Kingdom MRC_ Medical Research Council; MC_UU_00034/3 United Kingdom MRC_ Medical Research Council; MR/V035789/1 United Kingdom MRC_ Medical Research Council; 206369/Z/17/Z United Kingdom WT_ Wellcome Trust |
المشرفين على المادة: | 0 (NP protein, Influenza A virus) 0 (transcription factor BTF3) |
تواريخ الأحداث: | Date Created: 20230628 Date Completed: 20240116 Latest Revision: 20240403 |
رمز التحديث: | 20240403 |
DOI: | 10.1038/s41586-023-06261-8 |
PMID: | 37380775 |
قاعدة البيانات: | MEDLINE |
تدمد: | 1476-4687 |
---|---|
DOI: | 10.1038/s41586-023-06261-8 |