The evolutionary potential of influenza A virus hemagglutinin is highly constrained by epistatic interactions with neuraminidase

Bloom, 2010, Permissive secondary mutations enable the evolution of influenza oseltamivir resistance, Science, 328, 1272, 10.1126/science.1187816 Bloom, 2006, Protein stability promotes evolvability, Proc. Natl. Acad. Sci. USA, 103, 5869, 10.1073/pnas.0510098103 Brooke, 2017, Population diversity and collective interactions during influenza virus infection, J. Virol., 91, 10.1128/JVI.01164-17 Brooke, 2014, Influenza A virus nucleoprotein selectively decreases neuraminidase gene-segment packaging while enhancing viral fitness and transmissibility, Proc. Natl. Acad. Sci. USA, 111, 16854, 10.1073/pnas.1415396111 Brown, 2001, Pattern of mutation in the genome of influenza A virus on adaptation to increased virulence in the mouse lung: identification of functional themes, Proc. Natl. Acad. Sci. USA, 98, 6883, 10.1073/pnas.111165798 Carrat, 2007, Influenza vaccine: the challenge of antigenic drift, Vaccine, 25, 6852, 10.1016/j.vaccine.2007.07.027 Caton, 1982, The antigenic structure of the influenza virus A/PR/8/34 hemagglutinin (H1 subtype), Cell, 31, 417, 10.1016/0092-8674(82)90135-0 Cock, 2009, Biopython: freely available Python tools for computational molecular biology and bioinformatics, Bioinformatics, 25, 1422, 10.1093/bioinformatics/btp163 Das, 2013, Defining influenza A virus hemagglutinin antigenic drift by sequential monoclonal antibody selection, Cell Host Microbe, 13, 314, 10.1016/j.chom.2013.02.008 de Visser, 2003, Perspective: evolution and detection of genetic robustness, Evolution, 57, 1959 de Vries, 2020, Influenza A virus hemagglutinin–neuraminidase–receptor balance: preserving virus motility, Trends Microbiol., 28, 57, 10.1016/j.tim.2019.08.010 Doud, 2016, Accurate measurement of the effects of all amino-acid mutations on influenza hemagglutinin, Viruses, 8, 155, 10.3390/v8060155 Doud, 2017, Complete mapping of viral escape from neutralizing antibodies, PLoS Pathog., 13, e1006271, 10.1371/journal.ppat.1006271 Draghi, 2010, Mutational robustness can facilitate adaptation, Nature, 463, 353, 10.1038/nature08694 Elena, 2012, RNA virus genetic robustness: possible causes and some consequences, Curr. Opin. Virol., 2, 525, 10.1016/j.coviro.2012.06.008 Fowler, 2014, Deep mutational scanning: a new style of protein science, Nat. Methods, 11, 801, 10.1038/nmeth.3027 Fraczkiewicz, 1998, Exact and efficient analytical calculation of the accessible surface areas and their gradients for macromolecules, J. Comput. Chem., 19, 319, 10.1002/(SICI)1096-987X(199802)19:3<319::AID-JCC6>3.0.CO;2-W Gaymard, 2016, Functional balance between neuraminidase and haemagglutinin in influenza viruses, Clin. Microbiol. Infect., 22, 975, 10.1016/j.cmi.2016.07.007 Gerstung, 2012, Reliable detection of subclonal single-nucleotide variants in tumour cell populations, Nat. Commun., 3, 811, 10.1038/ncomms1814 Gerstung, 2014, Subclonal variant calling with multiple samples and prior knowledge, Bioinformatics, 30, 1198, 10.1093/bioinformatics/btt750 Harris, 2006, Influenza virus pleiomorphy characterized by cryoelectron tomography, Proc. Natl. Acad. Sci. USA, 103, 19123, 10.1073/pnas.0607614103 Hensley, 2011, Influenza A virus hemagglutinin antibody escape promotes neuraminidase antigenic variation and drug resistance, PLoS One, 6, e15190, 10.1371/journal.pone.0015190 Ives, 2002, The H274Y mutation in the influenza A/H1N1 neuraminidase active site following oseltamivir phosphate treatment leave virus severely compromised both in vitro and in vivo, Antiviral Res., 55, 307, 10.1016/S0166-3542(02)00053-0 Koel, 2013, Substitutions near the receptor binding site determine major antigenic change during influenza virus evolution, Science, 342, 976, 10.1126/science.1244730 Koelle, 2015, The effects of a deleterious mutation load on patterns of influenza A/H3N2’s antigenic evolution in humans, eLife, 4, e07361, 10.7554/eLife.07361 Kosik, 2018, Influenza A virus hemagglutinin glycosylation compensates for antibody escape fitness costs, PLoS Pathog., 14, e1006796, 10.1371/journal.ppat.1006796 Kosik, 2019, Influenza hemagglutinin and neuraminidase: Yin⁻Yang proteins coevolving to thwart immunity, Viruses, 11, 346, 10.3390/v11040346 Kryazhimskiy, 2011, Prevalence of epistasis in the evolution of influenza A surface proteins, PLoS Genet., 7, e1001301, 10.1371/journal.pgen.1001301 Lauring, 2013, The role of mutational robustness in RNA virus evolution, Nat. Rev. Microbiol., 11, 327, 10.1038/nrmicro3003 Lee, 2018, Deep mutational scanning of hemagglutinin helps predict evolutionary fates of human H3N2 influenza variants, Proc. Natl. Acad. Sci. USA, 115, E8276, 10.1073/pnas.1806133115 Magoč, 2011, FLASH: fast length adjustment of short reads to improve genome assemblies, Bioinformatics, 27, 2957, 10.1093/bioinformatics/btr507 Martin, 2011, Cutadapt removes adapter sequences from high-throughput sequencing reads, EMBnet J., 17, 10, 10.14806/ej.17.1.200 Martínez-Sobrido, 2010, Generation of recombinant influenza virus from plasmid DNA, J. Vis. Exp., 42, 2057 McBride, 2008, Robustness promotes evolvability of thermotolerance in an RNA virus, BMC Evol. Biol., 8, 231, 10.1186/1471-2148-8-231 Mitnaul, 2000, Balanced hemagglutinin and neuraminidase activities are critical for efficient replication of influenza A virus, J. Virol., 74, 6015, 10.1128/JVI.74.13.6015-6020.2000 Mölder, 2021, Sustainable data analysis with Snakemake, F1000Res, 10, 33, 10.12688/f1000research.29032.2 Paget, 2019, Global mortality associated with seasonal influenza epidemics: new burden estimates and predictors from the GLaMOR Project, J. Glob. Health, 9, 020421, 10.7189/jogh.09.020421 Pauly, 2017, A novel twelve class fluctuation test reveals higher than expected mutation rates for influenza A viruses, eLife, 6, e26437, 10.7554/eLife.26437 Petrova, 2018, The evolution of seasonal influenza viruses, Nat. Rev. Microbiol., 16, 47, 10.1038/nrmicro.2017.118 Powell, 2020, Neuraminidase antigenic drift of H3N2 clade 3c.2a viruses alters virus replication, enzymatic activity and inhibitory antibody binding, PLoS Pathog., 16, e1008411, 10.1371/journal.ppat.1008411 Randall, 2014, Inhibition of interferon gene activation by death-effector domain-containing proteins from the molluscum contagiosum virus, Proc. Natl. Acad. Sci. USA, 111, E265, 10.1073/pnas.1314569111 Sanjuán, 2010, Mutational fitness effects in RNA and single-stranded DNA viruses: common patterns revealed by site-directed mutagenesis studies, Philos. Trans. R. Soc. Lond. B Biol. Sci., 365, 1975, 10.1098/rstb.2010.0063 Sanjuán, 2004, The distribution of fitness effects caused by single-nucleotide substitutions in an RNA virus, Proc. Natl. Acad. Sci. USA, 101, 8396, 10.1073/pnas.0400146101 Strobel, 2022, Viral protein instability enhances host-range evolvability, PLoS Genet., 18, e1010030, 10.1371/journal.pgen.1010030 Tzarum, 2017, The 150-loop restricts the host specificity of human H10N8 influenza virus, Cell Rep., 19, 235, 10.1016/j.celrep.2017.03.054 Vahey, 2019, Low-fidelity assembly of influenza A virus promotes escape from host cells, Cell, 176, 281, 10.1016/j.cell.2018.10.056 Vahey, 2019, Influenza A virus surface proteins are organized to help penetrate host mucus, eLife, 8, e43764, 10.7554/eLife.43764 Visher, 2016, The mutational robustness of influenza A virus, PLoS Pathog., 12, e1005856, 10.1371/journal.ppat.1005856 Wagner, 2002, Functional balance between haemagglutinin and neuraminidase in influenza virus infections, Rev. Med. Virol., 12, 159, 10.1002/rmv.352 Wang, 2021, Antigenic evolution of human influenza H3N2 neuraminidase is constrained by charge balancing, eLife, 10, e72516, 10.7554/eLife.72516 Wasilewski, 2012, Distribution of surface glycoproteins on influenza A virus determined by electron cryotomography, Vaccine, 30, 7368, 10.1016/j.vaccine.2012.09.082 Wu, 2013, Clinical and molecular characteristics of the 2009 pandemic influenza H1N1 infection with severe or fatal disease from 2009 to 2011 in Shenzhen, China, J. Med. Virol., 85, 405, 10.1002/jmv.23295 Wu, 2018, A complex epistatic network limits the mutational reversibility in the influenza hemagglutinin receptor-binding site, Nat. Commun., 9, 1264, 10.1038/s41467-018-03663-5 Wu, 2014, High-throughput profiling of influenza A virus hemagglutinin gene at single-nucleotide resolution, Sci. Rep., 4, 4942, 10.1038/srep04942 Xu, 2012, Structural characterization of the hemagglutinin receptor specificity from the 2009 H1N1 influenza pandemic, J. Virol., 86, 982, 10.1128/JVI.06322-11 Xu, 2012, Functional balance of the hemagglutinin and neuraminidase activities accompanies the emergence of the 2009 H1N1 influenza pandemic, J. Virol., 86, 9221, 10.1128/JVI.00697-12 Yewdell, 2010, Monoclonal antibodies specific for discontinuous epitopes direct refolding of influenza A virus hemagglutinin, Mol. Immunol., 47, 1132, 10.1016/j.molimm.2009.10.023 Yewdell, 2011, Viva la revolución: rethinking influenza A virus antigenic drift, Curr. Opin. Virol., 1, 177, 10.1016/j.coviro.2011.05.005