Structures of influenza A virus RNA polymerase offer insight into viral genome replication.
Journal
Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462
Informations de publication
Date de publication:
09 2019
09 2019
Historique:
received:
12
03
2019
accepted:
07
08
2019
pubmed:
6
9
2019
medline:
26
3
2020
entrez:
6
9
2019
Statut:
ppublish
Résumé
Influenza A viruses are responsible for seasonal epidemics, and pandemics can arise from the transmission of novel zoonotic influenza A viruses to humans
Identifiants
pubmed: 31485076
doi: 10.1038/s41586-019-1530-7
pii: 10.1038/s41586-019-1530-7
pmc: PMC6795553
mid: EMS83961
doi:
Substances chimiques
Single-Domain Antibodies
0
RNA-Dependent RNA Polymerase
EC 2.7.7.48
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
287-290Subventions
Organisme : Wellcome Trust
ID : 200835/Z/16/Z
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/R009945/1
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/K000241/1
Pays : United Kingdom
Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 200835
Pays : United Kingdom
Organisme : Medical Research Council
ID : MC_PC_17137
Pays : United Kingdom
Références
Taubenberger, J. K. & Kash, J. C. Influenza virus evolution, host adaptation, and pandemic formation. Cell Host Microbe 7, 440–451 (2010).
doi: 10.1016/j.chom.2010.05.009
Mostafa, A., Abdelwhab, E. M., Mettenleiter, T. C. & Pleschka, S. Zoonotic potential of influenza A viruses: a comprehensive overview. Viruses 10, 497 (2018).
doi: 10.3390/v10090497
Pflug, A., Lukarska, M., Resa-Infante, P., Reich, S. & Cusack, S. Structural insights into RNA synthesis by the influenza virus transcription-replication machine. Virus Res. 234, 103–117 (2017).
doi: 10.1016/j.virusres.2017.01.013
te Velthuis, A. J. & Fodor, E. Influenza virus RNA polymerase: insights into the mechanisms of viral RNA synthesis. Nat. Rev. Microbiol. 14, 479–493 (2016).
doi: 10.1038/nrmicro.2016.87
Walker, A. P. & Fodor, E. Interplay between influenza virus and the host RNA polymerase II transcriptional machinery. Trends Microbiol. 27, 398–407 (2019).
doi: 10.1016/j.tim.2018.12.013
Pflug, A., Guilligay, D., Reich, S. & Cusack, S. Structure of influenza A polymerase bound to the viral RNA promoter. Nature 516, 355–360 (2014).
doi: 10.1038/nature14008
Jorba, N., Coloma, R. & Ortín, J. Genetic trans-complementation establishes a new model for influenza virus RNA transcription and replication. PLoS Pathog. 5, e1000462 (2009).
doi: 10.1371/journal.ppat.1000462
York, A., Hengrung, N., Vreede, F. T., Huiskonen, J. T. & Fodor, E. Isolation and characterization of the positive-sense replicative intermediate of a negative-strand RNA virus. Proc. Natl Acad. Sci. USA 110, E4238–E4245 (2013).
doi: 10.1073/pnas.1315068110
Jorba, N., Area, E. & Ortín, J. Oligomerization of the influenza virus polymerase complex in vivo. J. Gen. Virol. 89, 520–524 (2008).
doi: 10.1099/vir.0.83387-0
Moeller, A., Kirchdoerfer, R. N., Potter, C. S., Carragher, B. & Wilson, I. A. Organization of the influenza virus replication machinery. Science 338, 1631–1634 (2012).
doi: 10.1126/science.1227270
Chang, S. et al. Cryo-EM structure of influenza virus RNA polymerase complex at 4.3 Å resolution. Mol. Cell 57, 925–935 (2015).
doi: 10.1016/j.molcel.2014.12.031
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, 7789–7798 (2006).
doi: 10.1128/JVI.00600-06
Mänz, B., Brunotte, L., Reuther, P. & Schwemmle, M. Adaptive mutations in NEP compensate for defective H5N1 RNA replication in cultured human cells. Nat. Commun. 3, 802 (2012).
doi: 10.1038/ncomms1804
Deng, T., Vreede, F. T. & Brownlee, G. G. Different de novo initiation strategies are used by influenza virus RNA polymerase on its cRNA and viral RNA promoters during viral RNA replication. J. Virol. 80, 2337–2348 (2006).
doi: 10.1128/JVI.80.5.2337-2348.2006
Hengrung, N. et al. Crystal structure of the RNA-dependent RNA polymerase from influenza C virus. Nature 527, 114–117 (2015).
doi: 10.1038/nature15525
Thierry, E. et al. Influenza polymerase can adopt an alternative configuration involving a radical repacking of PB2 domains. Mol. Cell 61, 125–137 (2016).
doi: 10.1016/j.molcel.2015.11.016
Serna Martin, I. et al. A mechanism for the activation of the influenza virus transcriptase. Mol. Cell 70, 1101–1110 (2018).
doi: 10.1016/j.molcel.2018.05.011
Reich, S. et al. Structural insight into cap-snatching and RNA synthesis by influenza polymerase. Nature 516, 361–366 (2014).
doi: 10.1038/nature14009
Gerlach, P., Malet, H., Cusack, S. & Reguera, J. Structural insights into bunyavirus replication and its regulation by the vRNA promoter. Cell 161, 1267–1279 (2015).
doi: 10.1016/j.cell.2015.05.006
Oymans, J. & Te Velthuis, A. J. W. A mechanism for priming and realignment during influenza A virus replication. J. Virol. 92, e01773-17 (2018).
pubmed: 29118119
pmcid: 5774886
te Velthuis, A. J., Robb, N. C., Kapanidis, A. N. & Fodor, E. The role of the priming loop in influenza A virus RNA synthesis. Nat. Microbiol. 1, 16029 (2016).
doi: 10.1038/nmicrobiol.2016.29
Killip, M. J., Fodor, E. & Randall, R. E. Influenza virus activation of the interferon system. Virus Res. 209, 11–22 (2015).
doi: 10.1016/j.virusres.2015.02.003
te Velthuis, A. J. W. et al. Mini viral RNAs act as innate immune agonists during influenza virus infection. Nat. Microbiol. 3, 1234–1242 (2018).
doi: 10.1038/s41564-018-0240-5
Bieniossek, C., Imasaki, T., Takagi, Y. & Berger, I. MultiBac: expanding the research toolbox for multiprotein complexes. Trends Biochem. Sci. 37, 49–57 (2012).
doi: 10.1016/j.tibs.2011.10.005
Weissmann, F. et al. biGBac enables rapid gene assembly for the expression of large multisubunit protein complexes. Proc. Natl Acad. Sci. USA 113, E2564–E2569 (2016).
doi: 10.1073/pnas.1604935113
Pardon, E. et al. A general protocol for the generation of nanobodies for structural biology. Nat. Protocols 9, 674–693 (2014).
doi: 10.1038/nprot.2014.039
Walter, T. S. et al. A procedure for setting up high-throughput nanolitre crystallization experiments. Crystallization workflow for initial screening, automated storage, imaging and optimization. Acta Crystallogr. D 61, 651–657 (2005).
doi: 10.1107/S0907444905007808
Kabsch, W. Xds. Acta Crystallogr. D 66, 125–132 (2010).
doi: 10.1107/S0907444909047337
Tickle, I. J. et al. STARANISO. http://staraniso.globalphasing.org/cgi-bin/staraniso.cgi (2018).
McCoy, A. J. et al. Phaser crystallographic software. J. Appl. Crystallogr. 40, 658–674 (2007).
doi: 10.1107/S0021889807021206
Adams, P. D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D 66, 213–221 (2010).
doi: 10.1107/S0907444909052925
Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D 60, 2126–2132 (2004).
doi: 10.1107/S0907444904019158
Smart, O. S. et al. Exploiting structure similarity in refinement: automated NCS and target-structure restraints in BUSTER. Acta Crystallogr. D 68, 368–380 (2012).
doi: 10.1107/S0907444911056058
Rasmussen, S. G. et al. Crystal structure of the β
doi: 10.1038/nature10361
Zheng, S. Q. et al. MotionCor2: anisotropic correction of beam-induced motion for improved cryo-electron microscopy. Nat. Methods 14, 331–332 (2017).
doi: 10.1038/nmeth.4193
Zhang, K. Gctf: real-time CTF determination and correction. J. Struct. Biol. 193, 1–12 (2016).
doi: 10.1016/j.jsb.2015.11.003
Scheres, S. H. RELION: implementation of a Bayesian approach to cryo-EM structure determination. J. Struct. Biol. 180, 519–530 (2012).
doi: 10.1016/j.jsb.2012.09.006
Punjani, A., Rubinstein, J. L., Fleet, D. J. & Brubaker, M. A. cryoSPARC: algorithms for rapid unsupervised cryo-EM structure determination. Nat. Methods 14, 290–296 (2017).
doi: 10.1038/nmeth.4169
Pettersen, E. F. et al. UCSF Chimera—a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605–1612 (2004).
doi: 10.1002/jcc.20084
Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D 66, 486–501 (2010).
doi: 10.1107/S0907444910007493
Davis, I. W. et al. MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res. 35, W375–W383 (2007).
doi: 10.1093/nar/gkm216
Shkumatov, A. V. & Strelkov, S. V. DATASW, a tool for HPLC-SAXS data analysis. Acta Crystallogr. D 71, 1347–1350 (2015).
doi: 10.1107/S1399004715007154
Deng, T., Sharps, J., Fodor, E. & Brownlee, G. G. In vitro assembly of PB2 with a PB1-PA dimer supports a new model of assembly of influenza A virus polymerase subunits into a functional trimeric complex. J. Virol. 79, 8669–8674 (2005).
doi: 10.1128/JVI.79.13.8669-8674.2005
Fodor, E. et al. A single amino acid mutation in the PA subunit of the influenza virus RNA polymerase inhibits endonucleolytic cleavage of capped RNAs. J. Virol. 76, 8989–9001 (2002).
doi: 10.1128/JVI.76.18.8989-9001.2002
Fodor, E. et al. Rescue of influenza A virus from recombinant DNA. J. Virol. 73, 9679–9682 (1999).
pubmed: 10516084
pmcid: 113010
Fodor, E. & Smith, M. The PA subunit is required for efficient nuclear accumulation of the PB1 subunit of the influenza A virus RNA polymerase complex. J. Virol. 78, 9144–9153 (2004).
doi: 10.1128/JVI.78.17.9144-9153.2004
Vreede, F. T., Jung, T. E. & Brownlee, G. G. Model suggesting that replication of influenza virus is regulated by stabilization of replicative intermediates. J. Virol. 78, 9568–9572 (2004).
doi: 10.1128/JVI.78.17.9568-9572.2004
Nilsson-Payant, B. E., Sharps, J., Hengrung, N. & Fodor, E. The surface-exposed PA
doi: 10.1128/JVI.00687-18
Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671–675 (2012).
doi: 10.1038/nmeth.2089
Robb, N. C., Smith, M., Vreede, F. T. & Fodor, E. NS2/NEP protein regulates transcription and replication of the influenza virus RNA genome. J. Gen. Virol. 90, 1398–1407 (2009).
doi: 10.1099/vir.0.009639-0
Reich, S., Guilligay, D. & Cusack, S. An in vitro fluorescence based study of initiation of RNA synthesis by influenza B polymerase. Nucleic Acids Res. 45, 3353–3368 (2017).
pubmed: 28126917
pmcid: 5399792
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, 7020–7028 (2011).
doi: 10.1128/JVI.00522-11
Hu, J. et al. The PA-gene-mediated lethal dissemination and excessive innate immune response contribute to the high virulence of H5N1 avian influenza virus in mice. J. Virol. 87, 2660–2672 (2013).
doi: 10.1128/JVI.02891-12
Ilyushina, N. A. et al. Adaptation of pandemic H1N1 influenza viruses in mice. J. Virol. 84, 8607–8616 (2010).
doi: 10.1128/JVI.00159-10
Kamiki, H. et al. A PB1-K577E mutation in H9N2 influenza virus increases polymerase activity and pathogenicity in mice. Viruses 10, 653 (2018).
doi: 10.3390/v10110653
Lee, C. Y. et al. Novel mutations in avian PA in combination with an adaptive mutation in PR8 NP exacerbate the virulence of PR8-derived recombinant influenza A viruses in mice. Vet. Microbiol. 221, 114–121 (2018).
doi: 10.1016/j.vetmic.2018.05.026
Liedmann, S. et al. New virulence determinants contribute to the enhanced immune response and reduced virulence of an influenza A virus A/PR8/34 variant. J. Infect. Dis. 209, 532–541 (2014).
doi: 10.1093/infdis/jit463
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, 1750–1757 (2012).
doi: 10.1128/JVI.06203-11
Neumann, G., Macken, C. A. & Kawaoka, Y. Identification of amino acid changes that may have been critical for the genesis of A(H7N9) influenza viruses. J. Virol. 88, 4877–4896 (2014).
doi: 10.1128/JVI.00107-14
Peng, X. et al. Amino acid substitutions HA A150V, PA A343T, and PB2 E627K increase the virulence of H5N6 influenza virus in mice. Front. Microbiol. 9, 453 (2018).
doi: 10.3389/fmicb.2018.00453
Slaine, P. D. et al. Adaptive mutations in influenza A/California/07/2009 enhance polymerase activity and infectious virion production. Viruses 10, 272 (2018).
doi: 10.3390/v10050272
Wu, R. et al. Multiple amino acid substitutions are involved in the adaptation of H9N2 avian influenza virus to mice. Vet. Microbiol. 138, 85–91 (2009).
doi: 10.1016/j.vetmic.2009.03.010
Xu, G. et al. Prevailing PA mutation K356R in avian influenza H9N2 virus increases mammalian replication and pathogenicity. J. Virol. 90, 8105–8114 (2016).
doi: 10.1128/JVI.00883-16
Yamaji, R. et al. Mammalian adaptive mutations of the PA protein of highly pathogenic avian H5N1 influenza virus. J. Virol. 89, 4117–4125 (2015).
doi: 10.1128/JVI.03532-14
Zhang, Z. et al. Multiple amino acid substitutions involved in enhanced pathogenicity of LPAI H9N2 in mice. Infect. Genet. Evol. 11, 1790–1797 (2011).
doi: 10.1016/j.meegid.2011.07.025
Zhong, G. et al. Mutations in the PA protein of avian H5N1 influenza viruses affect polymerase activity and mouse virulence. J. Virol. 92, e01557-17 (2018).
pubmed: 29212927
pmcid: 5790930
Tan, Y. Z. et al. Addressing preferred specimen orientation in single-particle cryo-EM through tilting. Nat. Methods 14, 793–796 (2017).
doi: 10.1038/nmeth.4347
Naydenova, K. & Russo, C. J. Measuring the effects of particle orientation to improve the efficiency of electron cryomicroscopy. Nat. Commun. 8, 629 (2017).
doi: 10.1038/s41467-017-00782-3