Structural and functional specificity of Influenza virus haemagglutinin and paramyxovirus fusion protein anchoring peptides

Agrawal, 2010, A solid-state NMR study of changes in lipid phase induced by membrane-fusogenic LV-peptides, Biochim. Biophys. Acta, 1798, 202, 10.1016/j.bbamem.2009.10.015 Armstrong, 2000, The transmembrane domain of influenza hemagglutinin exhibits a stringent length requirement to support the hemifusion to fusion transition, J. Cell Biol., 151, 425, 10.1083/jcb.151.2.425 Böttcher, 1999, Structure of influenza haemagglutinin at neutral and at fusogenic pH by electron cryo-microscopy, FEBS Lett., 463, 255, 10.1016/S0014-5793(99)01475-1 Ballesteros, 1995, Integrated methods for the construction of three dimensional models and computational probing of structure-function relations in G-protein coupled receptors, Methods Neurosci., 25, 366, 10.1016/S1043-9471(05)80049-7 Bissonnette, 2009, Functional analysis of the transmembrane domain in paramyxovirus F protein-mediated membrane fusion, J. Mol. Biol., 386, 14, 10.1016/j.jmb.2008.12.029 Björkholm, 2014, Identification of novel sphingolipid-binding motifs in mammalian membrane proteins, Biochim. Biophys. Acta, 1838, 2066, 10.1016/j.bbamem.2014.04.026 Bose, 2015, Timing is everything: fine-tuned molecular machines orchestrate paramyxovirus entry, Virology, 479–480, 518, 10.1016/j.virol.2015.02.037 Branigan, 2006, The cytoplasmic domain of the F protein of human respiratory syncytial virus is not required for cell fusion, J. Gen. Virol., 87, 395, 10.1099/vir.0.81481-0 Brett, 2014, Site-specific S-acylation of influenza virus hemagglutinin: the location of the acylation site relative to the membrane border is the decisive factor for attachment of stearate, J. Biol. Chem., 289, 34978, 10.1074/jbc.M114.586180 Bullough, 1994, Structure of influenza haemagglutinin at the pH of membrane fusion, Nature, 371, 37, 10.1038/371037a0 Caballero, 1998, Measles virus fusion protein is palmitoylated on transmembrane-intracytoplasmic cysteine residues which participate in cell fusion, J. Virol., 72, 8198, 10.1128/JVI.72.10.8198-8204.1998 Calder, 2010, Structural organization of a filamentous influenza A virus, Proc. Natl. Acad. Sci. U. S. A., 107, 10685, 10.1073/pnas.1002123107 Chamberlain, 2015, The physiology of protein S-acylation, Physiol. Rev., 95, 341, 10.1152/physrev.00032.2014 Chang, 2008, Membrane interaction and structure of the transmembrane domain of influenza hemagglutinin and its fusion peptide complex, BMC Biol., 6, 2, 10.1186/1741-7007-6-2 Chen, 2005, Influenza virus hemagglutinin (H3 subtype) requires palmitoylation of its cytoplasmic tail for assembly: M1 proteins of two subtypes differ in their ability to support assembly, J. Virol., 79, 13673, 10.1128/JVI.79.21.13673-13684.2005 Chernomordik, 2008, Mechanics of membrane fusion, Nat. Struct. Mol. Biol., 15, 675, 10.1038/nsmb.1455 Contreras, 2012, Molecular recognition of a single sphingolipid species by a protein's transmembrane domain, Nature, 481, 525, 10.1038/nature10742 Cox, 2015, Human metapneumovirus is capable of entering cells by fusion with endosomal membranes, PLoS Pathog., 11, e1005303, 10.1371/journal.ppat.1005303 Doms, 1986, Quaternary structure of influenza virus hemagglutinin after acid treatment, J. Virol., 60, 833, 10.1128/JVI.60.3.833-839.1986 Dopheide, 1981, The location of the bromelain cleavage site in a Hong Kong influenza virus Haemagglutinin, J. Gen. Virol., 52, 367, 10.1099/0022-1317-52-2-367 Efremov, 2007, Molecular lipophilicity in protein modeling and drug design, Curr. Med. Chem., 14, 393, 10.2174/092986707779941050 Engel, 2010, FLIM-FRET and FRAP reveal association of influenza virus haemagglutinin with membrane rafts, Biochem. J., 425, 567, 10.1042/BJ20091388 Epand, 2010, Cholesterol interaction with proteins that partition into membrane domains: an overview, Subcell. Biochem., 51, 253, 10.1007/978-90-481-8622-8_9 Field, 2016, Hendra virus ecology and transmission, Curr. Opin. Virol., 16, 120, 10.1016/j.coviro.2016.02.004 Fontana, 2015, Influenza virus-mediated membrane fusion: structural insights from electron microscopy, Arch. Biochem. Biophys., 581, 86, 10.1016/j.abb.2015.04.011 Forrester, 2011, Site-specific analysis of protein S-acylation by resin-assisted capture, J. Lipid Res., 52, 393, 10.1194/jlr.D011106 Fouchier, 2004, Avian influenza A virus (H7N7) associated with human conjunctivitis and a fatal case of acute respiratory distress syndrome, Proc. Natl. Acad. Sci. U. S. A., 101, 1356, 10.1073/pnas.0308352100 Frisz, 2013, Direct chemical evidence for sphingolipid domains in the plasma membranes of fibroblasts, Proc. Natl. Acad. Sci. U. S. A., 110, E613, 10.1073/pnas.1216585110 Fusaro, 2011, Phylogeography and evolutionary history of reassortant H9N2 viruses with potential human health implications, J. Virol., 85, 8413, 10.1128/JVI.00219-11 Gamblin, 2004, The structure and receptor binding properties of the 1918 influenza hemagglutinin, Science, 303, 1838, 10.1126/science.1093155 Garcia, 2016, Dynamic viral glycoprotein machines: approaches for probing transient states that drive membrane fusion, Viruses, 8, 10.3390/v8010015 Garcia, 2015, Dynamic changes during acid-induced activation of influenza hemagglutinin, Structure, 23, 665, 10.1016/j.str.2015.02.006 Ge, 2011, Two conserved residues are important for inducing highly ordered membrane domains by the transmembrane domain of influenza hemagglutinin, Biophys. J., 100, 90, 10.1016/j.bpj.2010.11.014 Gerl, 2012, Quantitative analysis of the lipidomes of the influenza virus envelope and MDCK cell apical membrane, J. Cell Biol., 196, 213, 10.1083/jcb.201108175 Goh, 2009, Protein intrinsic disorder and influenza virulence: the 1918 H1N1 and H5N1 viruses, Virol. J., 6, 69, 10.1186/1743-422X-6-69 Gravel, 2011, The transmembrane domain sequence affects the structure and function of the Newcastle disease virus fusion protein, J. Virol., 85, 3486, 10.1128/JVI.02308-10 Gruenke, 2002, New insights into the spring-loaded conformational change of influenza virus hemagglutinin, J. Virol., 76, 4456, 10.1128/JVI.76.9.4456-4466.2002 Gui, 2015, Electron tomography imaging of surface glycoproteins on human parainfluenza virus 3: association of receptor binding and fusion proteins before receptor engagement, MBio, 6, e02393, 10.1128/mBio.02393-14 Ha, 2002, H5 avian and H9 swine influenza virus haemagglutinin structures: possible origin of influenza subtypes, EMBO J., 21, 865, 10.1093/emboj/21.5.865 Han, 2000, pH-dependent self-association of influenza hemagglutinin fusion peptides in lipid bilayers, J. Mol. Biol., 304, 953, 10.1006/jmbi.2000.4251 Hanson, 2008, A specific cholesterol binding site is established by the 2.8A structure of the human beta2-adrenergic receptor, Structure, 16, 897, 10.1016/j.str.2008.05.001 Harris, 2006, Influenza virus pleiomorphy characterized by cryoelectron tomography, Proc. Natl. Acad. Sci. U. S. A., 103, 19123, 10.1073/pnas.0607614103 Harrison, 2015, Viral membrane fusion, Virology, 479–480, 498, 10.1016/j.virol.2015.03.043 Hause, 2013, Isolation of a novel swine influenza virus from Oklahoma in 2011 which is distantly related to human influenza C viruses, PLoS Pathog., 9, e1003176, 10.1371/journal.ppat.1003176 He, 2011, Detecting nanodomains in living cell membrane by fluorescence correlation spectroscopy, Annu. Rev. Phys. Chem., 62, 417, 10.1146/annurev-physchem-032210-103402 Hess, 2007, Dynamic clustered distribution of hemagglutinin resolved at 40nm in living cell membranes discriminates between raft theories, Proc. Natl. Acad. Sci. U. S. A., 104, 17370, 10.1073/pnas.0708066104 Hofmann, 2004, De novo design of conformationally flexible transmembrane peptides driving membrane fusion, Proc. Natl. Acad. Sci. U. S. A., 101, 14776, 10.1073/pnas.0405175101 Imai, 2012, The cytoplasmic tail domain of influenza B virus hemagglutinin is important for its incorporation into virions but is not essential for virus replication in cell culture in the presence of compensatory mutations, J. Virol., 86, 11633, 10.1128/JVI.01479-12 Imai, 2013, Transmission of influenza A/H5N1 viruses in mammals, Virus Res., 178, 15, 10.1016/j.virusres.2013.07.017 Influenza Research Database (http://www.udb.org/). Jardetzky, 2014, Activation of paramyxovirus membrane fusion and virus entry, Curr. Opin. Virol., 5, 24, 10.1016/j.coviro.2014.01.005 Johnson, 2007, Aromatic and cation-pi interactions enhance helix–helix association in a membrane environment, Biochemistry, 46, 9208, 10.1021/bi7008773 Kong, 2015, Novel reassortant influenza viruses between pandemic (H1N1) 2009 and other influenza viruses pose a risk to public health, Microb. Pathog., 89, 62, 10.1016/j.micpath.2015.09.002 Kordyukova, 2012, Mass spectrometric approaches to study enveloped viruses: new possibilities for structural biology and prophylactic medicine, Biochemistry (Mosc.), 77, 830, 10.1134/S0006297912080044 Kordyukova, 2004, Influenza A hemagglutinin C-terminal anchoring peptide: identification and mass spectrometric study, Protein Pept. Lett., 11, 385, 10.2174/0929866043406850 Kordyukova, 2008, S acylation of the hemagglutinin of influenza viruses: mass spectrometry reveals site-specific attachment of stearic acid to a transmembrane cysteine, J. Virol., 82, 9288, 10.1128/JVI.00704-08 Kordyukova, 2010, Site-specific attachment of palmitate or stearate to cytoplasmic versus transmembrane cysteines is a common feature of viral spike proteins, Virology, 398, 49, 10.1016/j.virol.2009.11.039 Kordyukova, 2011, Linker and/or transmembrane regions of influenza A/group-1, A/group-2 and type B virus hemagglutinins are packed differently within trimers, Biochim. Biophys. Acta, 1808, 1843, 10.1016/j.bbamem.2011.03.005 Kordyukova, 2016, S-acylation of proteins, Methods Mol. Biol. Krzyzaniak, 2013, Host cell entry of respiratory syncytial virus involves macropinocytosis followed by proteolytic activation of the F protein, PLoS Pathog., 9, e1003309, 10.1371/journal.ppat.1003309 Lai, 2015, The interaction between influenza HA fusion peptide and transmembrane domain affects membrane structure, Biophys. J., 109, 2523, 10.1016/j.bpj.2015.10.044 Lakkaraju, 2012, Palmitoylated calnexin is a key component of the ribosome-translocon complex, EMBO J., 31, 1823, 10.1038/emboj.2012.15 Lamb, 2007, Structural basis of viral invasion: lessons from paramyxovirus F, Curr. Opin. Struct. Biol., 17, 427, 10.1016/j.sbi.2007.08.016 Langosch, 2001, Peptide mimics of the vesicular stomatitis virus G-protein transmembrane segment drive membrane fusion in vitro, J. Biol. Chem., 276, 32016, 10.1074/jbc.M102579200 Lee, 2010, Architecture of a nascent viral fusion pore, EMBO J., 29, 1299, 10.1038/emboj.2010.13 Levental, 2010, Palmitoylation regulates raft affinity for the majority of integral raft proteins, Proc. Natl. Acad. Sci. U. S. A., 107, 22050, 10.1073/pnas.1016184107 Li, 2008, Length requirements for membrane fusion of influenza virus hemagglutinin peptide linkers to transmembrane or fusion peptide domains, J. Virol., 82, 6337, 10.1128/JVI.02576-07 Liang, 2002, Mass spectrometric analysis of GAP-43/neuromodulin reveals the presence of a variety of fatty acylated species, J. Biol. Chem., 277, 33032, 10.1074/jbc.M204607200 Lin, 1998, Mutations in the middle of the transmembrane domain reverse the polarity of transport of the influenza virus hemagglutinin in MDCK epithelial cells, J. Cell Biol., 142, 51, 10.1083/jcb.142.1.51 Liu, 2009, Structures of receptor complexes formed by hemagglutinins from the Asian Influenza pandemic of 1957, Proc. Natl. Acad. Sci. U. S. A., 106, 17175, 10.1073/pnas.0906849106 Liu, 2014, Recombinant influenza H1, H5 and H9 hemagglutinins containing replaced H3 hemagglutinin transmembrane domain showed enhanced heterosubtypic protection in mice, Vaccine, 32, 3041, 10.1016/j.vaccine.2014.03.058 Liu, 2015, Influenza bivalent vaccine comprising recombinant H3 hemagglutinin (HA) and H1 HA containing replaced H3 hemagglutinin transmembrane domain exhibited improved heterosubtypic protection immunity in mice, Vaccine, 33, 4035, 10.1016/j.vaccine.2015.05.044 Liu, 2016, Avian influenza virus in pregnancy, Rev. Med. Virol., 10.1002/rmv.1884 Ludwig, 2008, Electron cryomicroscopy reveals different F1+F2 protein States in intact parainfluenza virions, J. Virol., 82, 3775, 10.1128/JVI.02154-07 Ma, 2015, Expected and unexpected features of the newly discovered bat influenza A-like viruses, PLoS Pathog., 11, e1004819, 10.1371/journal.ppat.1004819 Martin, 2009, Large-scale profiling of protein palmitoylation in mammalian cells, Nat. Methods, 6, 135, 10.1038/nmeth.1293 McLellan, 2013, Structure of RSV fusion glycoprotein trimer bound to a prefusion-specific neutralizing antibody, Science, 340, 1113, 10.1126/science.1234914 Melkonian, 1999, Role of lipid modifications in targeting proteins to detergent-resistant membrane rafts. Many raft proteins are acylated, while few are prenylated, J. Biol. Chem., 274, 3910, 10.1074/jbc.274.6.3910 Mineev, 2013, Structural investigation of influenza virus hemagglutinin membrane-anchoring peptide, Protein Eng. Des. Sel., 26, 547, 10.1093/protein/gzt034 Mintaev, 2014, Co-evolution analysis to predict protein–protein interactions within influenza virus envelope, J. Bioinform. Comput. Biol., 12, 1441008, 10.1142/S021972001441008X Morozova, 2010, On the role of acylation of transmembrane proteins, Biophys. J., 98, 800, 10.1016/j.bpj.2009.11.014 Munro, 2003, Lipid rafts: elusive or illusive?, Cell, 115, 377, 10.1016/S0092-8674(03)00882-1 Naeve, 1990, Fatty acids on the A/Japan/305/57 influenza virus hemagglutinin have a role in membrane fusion, EMBO J., 9, 3857, 10.1002/j.1460-2075.1990.tb07604.x Nagy, 2016, Recombinant Newcastle disease virus expressing H9 HA protects chickens against heterologous avian influenza H9N2 virus challenge, Vaccine, 34, 2537, 10.1016/j.vaccine.2016.04.022 Neumann, 2015, Transmission of influenza A viruses, Virology, 479–480, 234, 10.1016/j.virol.2015.03.009 Neumann, 2010, H5N1 influenza viruses: outbreaks and biological properties, Cell Res., 20, 51, 10.1038/cr.2009.124 Nobusawa, 1991, Comparison of complete amino acid sequences and receptor-binding properties among 13 serotypes of hemagglutinins of influenza A viruses, Virology, 182, 475, 10.1016/0042-6822(91)90588-3 Ohkura, 2014, Influenza A virus hemagglutinin and neuraminidase mutually accelerate their apical targeting through clustering of lipid rafts, J. Virol., 88, 10039, 10.1128/JVI.00586-14 Ollesch, 2008, Secondary structure and distribution of fusogenic LV-peptides in lipid membranes, Eur. Biophys. J., 37, 435, 10.1007/s00249-007-0233-4 Ong, 2015, Henipavirus encephalitis: recent developments and advances, Brain Pathol., 25, 605, 10.1111/bpa.12278 Paramyxoviridae Database (http://viralzone.expasy.org/all_by_protein/556. html). Park, 2003, Leash in the groove mechanism of membrane fusion, Nat. Struct. Biol., 10, 1048, 10.1038/nsb1012 Parton, 2013, Formation of raft-like assemblieswithin clusters of influenza hemagglutinin observed by MD simulations, PLoS Comput. Biol., 9, e1003034, 10.1371/journal.pcbi.1003034 Peng, 2016, Proteomic analysis of fatty-acylated proteins, Curr. Opin. Chem. Biol., 30, 77, 10.1016/j.cbpa.2015.11.008 Pica, 2013, Toward a universal influenza virus vaccine: prospects and challenges, Annu. Rev. Med., 64, 189, 10.1146/annurev-med-120611-145115 Podbilewicz, 2014, Virus and cell fusion mechanisms, Annu. Rev. Cell Dev. Biol., 30, 111, 10.1146/annurev-cellbio-101512-122422 Ponimaskin, 1998, Domain-structure of cytoplasmic border region is main determinant for palmitoylation of influenza virus hemagglutinin (H7), Virology, 249, 325, 10.1006/viro.1998.9303 Popa, 2012, Residues in the hendra virus fusion protein transmembrane domain are critical for endocytic recycling, J. Virol., 86, 3014, 10.1128/JVI.05826-11 Porotto, 2011, Spring-loaded model revisited: paramyxovirus fusion requires engagement of a receptor binding protein beyond initial triggering of the fusion protein, J. Virol., 85, 12867, 10.1128/JVI.05873-11 Porotto, 2012, Mechanism of fusion triggering by human parainfluenza virus type III: communication between viral glycoproteins during entry, J. Biol. Chem., 287, 778, 10.1074/jbc.M111.298059 Porotto, 2012, Regulation of paramyxovirus fusion activation: the hemagglutinin-neuraminidase protein stabilizes the fusion protein in a pretriggered state, J. Virol., 86, 12838, 10.1128/JVI.01965-12 Poschner, 2009, Sequence-specific conformational dynamics of model transmembrane domains determines their membrane fusogenic function, J. Mol. Biol., 386, 733, 10.1016/j.jmb.2008.12.077 Pyrkov, 2009, PLATINUM: a web tool for analysis of hydrophobic/hydrophilic organization of biomolecular complexes, Bioinformatics, 25, 1201, 10.1093/bioinformatics/btp111 Resh, 2016, Fatty acylation of proteins: the long and the short of it, Prog. Lipid Res., 63, 120, 10.1016/j.plipres.2016.05.002 Reverey, 1996, Differential fatty acid selection during biosynthetic S-acylation of a transmembrane protein (HEF) and other proteins in insect cells (Sf9) and in mammalian cells (CV1), J. Biol. Chem., 271, 23607, 10.1074/jbc.271.39.23607 Ridder, 2005, Tryptophan supports interaction of transmembrane helices, J. Mol. Biol., 354, 894, 10.1016/j.jmb.2005.09.084 Rott, 1980, Cleavability of hemagglutinin determines spread of avian influenza viruses in the chorioallantoic membrane of chicken embryo, Arch. Virol., 65, 123, 10.1007/BF01317323 Russell, 2004, H1 and H7 influenza haemagglutinin structures extend a structural classification of haemagglutinin subtypes, Virology, 325, 287, 10.1016/j.virol.2004.04.040 Russell, 2012, The potential for respiratory droplet-transmissible A/H5N1 influenza virus to evolve in a mammalian host, Science, 336, 1541, 10.1126/science.1222526 Russell, 2014, Acid-induced membrane fusion by the hemagglutinin protein and its role in influenza virus biology, Curr. Top. Microbiol. Immunol., 385, 93 Sakai, 2002, Fatty acids on the A/USSR/77 influenza virus hemagglutinin facilitate the transition from hemifusion to fusion pore formation, J. Virol., 76, 4603, 10.1128/JVI.76.9.4603-4611.2002 Sal-Man, 2007, Specificity in transmembrane helix–helix interactions mediated by aromatic residues, J. Biol. Chem., 282, 19753, 10.1074/jbc.M610368200 Schechter, 1967, On the size of the active site in proteases. I. Papain, Biochem. Biophys. Res. Commun., 27, 157, 10.1016/S0006-291X(67)80055-X Scheiffele, 1997, Interaction of influenza virus haemagglutinin with sphingolipid-cholesterol membrane domains via its transmembrane domain, EMBO J., 16, 5501, 10.1093/emboj/16.18.5501 Scheiffele, 1999, Influenza viruses select ordered lipid domains during budding from the plasma membrane, J. Biol. Chem., 274, 2038, 10.1074/jbc.274.4.2038 Schmidt, 1979, Fatty acid binding to vesicular stomatitis virus glycoprotein: a new type of post-translational modification of the viral glycoprotein, Cell, 17, 813, 10.1016/0092-8674(79)90321-0 Schmidt, 1979, Evidence for covalent attachment of fatty acids to Sindbis virus glycoproteins, Proc Natl Acad Sci U. S. A., 76, 1687, 10.1073/pnas.76.4.1687 Schmidt, 2011, Progress in the development of human parainfluenza virus vaccines, Expert Rev. Respir. Med., 5, 515, 10.1586/ers.11.32 Schmidt, 1984, The transfer of myristic and other fatty acids on lipid and viral protein acceptors in cultured cells infected with Semliki Forest and influenza virus, EMBO J., 3, 2295, 10.1002/j.1460-2075.1984.tb02129.x Scolari, 2009, Lateral distribution of the transmembrane domain of influenza virus hemagglutinin revealed by time-resolved fluorescence imaging, J. Biol. Chem., 284, 15708, 10.1074/jbc.M900437200 Scolari, 2016, Modulation of cell surface transport and lipid raft localization by the cytoplasmic tail of the influenza virus hemagglutinin, Cell Microbiol., 18, 125, 10.1111/cmi.12491 Serebryakova, 2006, Mass spectrometric sequencing and acylation character analysis of C-terminal anchoring segment from influenza A hemagglutinin, Eur. J. Mass Spectrom. (Chichester, Engl.), 12, 51, 10.1255/ejms.792 Serebryakova, 2011, Influenza virus hemagglutinin spike neck architectures and interaction with model enzymes evaluated by MALDI-TOF mass spectrometry and bioinformatics tools, Virus Res., 160, 294, 10.1016/j.virusres.2011.07.002 Serebryakova, 2013, Mass spectrometry analysis of influenza virus reassortant clones does not reveal an influence of other viral proteins on S-acylation of hemagglutinin, Arch. Virol., 158, 467, 10.1007/s00705-012-1510-9 Sergel, 1995, Mutations in the cytoplasmic domain of the fusion glycoprotein of Newcastle disease virus depress syncytia formation, Virology, 210, 264, 10.1006/viro.1995.1343 Seth, 2003, Activation of fusion by the SER virus F protein: a low-pH-dependent paramyxovirus entry process, J. Virol., 77, 6520, 10.1128/JVI.77.11.6520-6527.2003 Seth, 2004, Mutations in multiple domains activate paramyxovirus F protein-induced fusion, J. Virol., 78, 8513, 10.1128/JVI.78.16.8513-8523.2004 Shvartsman, 2003, Differently anchored influenza hemagglutinin mutants display distinct interaction dynamics with mutual rafts, J. Cell Biol., 163, 879, 10.1083/jcb.200308142 Siche, 2015, Two cytoplasmic acylation sites and an adjacent hydrophobic residue, but no other conserved amino acids in the cytoplasmic tail of HA from influenza a virus are crucial for virus replication, Viruses, 7, 6458, 10.3390/v7122950 Simons, 1997, Functional rafts in cell membranes, Nature, 387, 569, 10.1038/42408 Skehel, 2000, Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin, Annu. Rev. Biochem., 69, 531, 10.1146/annurev.biochem.69.1.531 Sklyanskaya, 1988, Formation of mixed hemagglutinin trimers in the course of double infection with influenza viruses belonging to different subtypes, Virus Res., 10, 153, 10.1016/0168-1702(88)90012-3 Smith, 2009, Viral entry mechanisms: the increasing diversity of paramyxovirus entry, FEBS J., 276, 7217, 10.1111/j.1742-4658.2009.07401.x Smith, 2012, Beyond anchoring: the expanding role of the hendra virus fusion protein transmembrane domain in protein folding, stability, and function, J. Virol., 86, 3003, 10.1128/JVI.05762-11 Smith, 2013, Trimeric transmembrane domain interactions in paramyxovirus fusion proteins: roles in protein folding, stability, and function, J. Biol. Chem., 288, 35726, 10.1074/jbc.M113.514554 Song, 2016, An open receptor-binding cavity of hemagglutinin-esterase-fusion glycoprotein from newly-identified influenza D virus: basis for its broad cell tropism, PLoS Pathog., 12, e1005411, 10.1371/journal.ppat.1005411 Swanson, 2010, Structure of the Newcastle disease virus F protein in the post-fusion conformation, Virology, 402, 372, 10.1016/j.virol.2010.03.050 Takeda, 2003, Influenza virus hemagglutinin concentrates in lipid raft microdomains for efficient viral fusion, Proc. Natl. Acad. Sci. U. S. A., 100, 14610, 10.1073/pnas.2235620100 Tall, 2003, Features of influenza HA required for apical sorting differ from those required for association with DRMs or MAL, Traffic, 4, 838, 10.1046/j.1398-9219.2003.0138.x Tamm, 2003, Membrane fusion: a structural perspective on the interplay of lipids and proteins, Curr. Opin. Struct. Biol., 13, 453, 10.1016/S0959-440X(03)00107-6 Tatulian, 2000, Secondary structure, orientation, oligomerization, and lipid interactions of the transmembrane domain of influenza hemagglutinin, Biochemistry, 39, 496, 10.1021/bi991594p Teese, 2015, Role of GxxxG motifs in transmembrane domain interactions, Biochemistry, 54, 5125, 10.1021/acs.biochem.5b00495 Thornburg, 2016, H7N9 influenza virus neutralizing antibodies that possess few somatic mutations, J. Clin. Invest., 126, 1482, 10.1172/JCI85317 Tong, 2002, Regulation of fusion activity by the cytoplasmic domain of a paramyxovirus F protein, Virology, 301, 322, 10.1006/viro.2002.1594 Tong, 2012, A distinct lineage of influenza A virus from bats, Proc. Natl. Acad. Sci. U. S. A., 109, 4269, 10.1073/pnas.1116200109 Tong, 2013, New world bats harbor diverse influenza A viruses, PLoS Pathog., 9, e1003657, 10.1371/journal.ppat.1003657 Tran, 2016, Cryo-electron microscopy structures of chimeric hemagglutinin displayed on a universal influenza vaccine candidate, MBio, 7, 00257, 10.1128/mBio.00257-16 Tsukamoto, 2016, X-ray crystallographic structure of thermophilic rhodopsin: implications for high thermal stability and optogenetic function, J. Biol. Chem., 291, 12223, 10.1074/jbc.M116.719815 Tsutsumi, 2008, Discovery of protein-palmitoylating enzymes, Pflugers Arch., 456, 1199, 10.1007/s00424-008-0465-x Ujike, 2004, Influence of acylation sites of influenza B virus hemagglutinin on fusion pore formation and dilation, J. Virol., 78, 11536, 10.1128/JVI.78.21.11536-11543.2004 Veit, 1993, Timing of palmitoylation of influenza virus hemagglutinin, FEBS Lett., 336, 243, 10.1016/0014-5793(93)80812-9 Veit, 2006, Palmitoylation of influenza virus proteins, Berl. Munch. Tierarztl. Wochenschr., 119, 112 Veit, 2015, S-acylation of influenza virus proteins: are enzymes for fatty acid attachment promising drug targets?, Vaccine, 33, 7002, 10.1016/j.vaccine.2015.08.095 Veit, 2011, Association of influenza virus proteins with membrane rafts, Adv. Virol., 2011, 370606, 10.1155/2011/370606 Veit, 2011 Veit, 1989, Different palmitoylation of paramyxovirus glycoproteins, Virology, 168, 173, 10.1016/0042-6822(89)90417-0 Veit, 1990, The hemagglutinating glycoproteins of influenza B and C viruses are acylated with different fatty acids, Virology, 177, 807, 10.1016/0042-6822(90)90554-5 Veit, 1991, Site-specific mutagenesis identifies three cysteine residues in the cytoplasmic tail as acylation sites of influenza virus hemagglutinin, J. Virol., 65, 2491, 10.1128/JVI.65.5.2491-2500.1991 Veit, 1996, Cytoplasmic tail length influences fatty acid selection for acylation of viral glycoproteins, Biochem. J., 318, 163, 10.1042/bj3180163 Veit, 2013, Lipid domain association of influenza virus proteins detected by dynamic fluorescence microscopy techniques, Cell Microbiol., 15, 179, 10.1111/cmi.12045 Veit, 2013, Palmitoylation of influenza virus proteins, Biochem. Soc. Trans., 41, 50, 10.1042/BST20120210 Veit, 2012, Palmitoylation of virus proteins, Biol. Cell, 104, 493, 10.1111/boc.201200006 Victor, 2012, Structural determinants for the membrane insertion of the transmembrane peptide of hemagglutinin from influenza virus, J. Chem. Inf. Model., 52, 3001, 10.1021/ci3003396 Wagner, 2005, Acylation-mediated membrane anchoring of avian influenza virus hemagglutinin is essential for fusion pore formation and virus infectivity, J. Virol., 79, 6449, 10.1128/JVI.79.10.6449-6458.2005 Wan, 2007, Palmitoylated proteins: purification and identification, Nat. Protoc., 2, 1573, 10.1038/nprot.2007.225 Wang, 2008, Crystal structure of unliganded influenza B virus hemagglutinin, J. Virol., 82, 3011, 10.1128/JVI.02477-07 Wasilewski, 2012, Distribution of surface glycoproteins on influenza A virus determined by electron cryotomography, Vaccine, 30, 7368, 10.1016/j.vaccine.2012.09.082 Watanabe, 2014, Pandemic potential of avian influenza A (H7N9) viruses, Trends Microbiol., 22, 623, 10.1016/j.tim.2014.08.008 Wen, 2016, A chimeric pneumovirus fusion protein carrying neutralizing epitopes of both MPV and RSV, PLoS One, 11, e0155917, 10.1371/journal.pone.0155917 White, 2016, Fusion of enveloped viruses in endosomes, Traffic, 17, 593, 10.1111/tra.12389 Wilson, 1981, Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3A resolution, Nature, 289, 366, 10.1038/289366a0 Wilson, 2015, Hemagglutinin clusters in the plasma membrane are not enriched with cholesterol and sphingolipids, Biophys. J., 108, 1652, 10.1016/j.bpj.2015.02.026 Wong, 2016, Structure and stabilization of the Hendra virus F glycoprotein in its prefusion form, Proc. Natl. Acad. Sci. U. S. A., 113, 1056, 10.1073/pnas.1523303113 Wu, 2014, Bat-derived influenza-like viruses H17N10 and H18N11, Trends Microbiol., 22, 183, 10.1016/j.tim.2014.01.010 Xu, 2013, Mutations of two transmembrane cysteines of hemagglutinin (HA) from influenza A H3N2 virus affect HA thermal stability and fusion activity, Virus Genes, 47, 20, 10.1007/s11262-013-0924-0 Xue, 2010, Viral disorder or disordered viruses: do viral proteins possess unique features?, Protein Pept. Lett., 17, 932, 10.2174/092986610791498984 Yang, 2001, Solid-state nuclear magnetic resonance evidence for an extended beta strand conformation of the membrane-bound HIV-1 fusion peptide, Biochemistry, 40, 8126, 10.1021/bi0100283 Yang, 2010, Structures of receptor complexes of a North American H7N2 influenza hemagglutinin with a loop deletion in the receptor binding site, PLoS Pathog., 6, e1001081, 10.1371/journal.ppat.1001081 Yang, 2015, Structure and receptor binding preferences of recombinant hemagglutinins from avian and human H6 and H10 influenza A virus subtypes, J. Virol., 89, 4612, 10.1128/JVI.03456-14 Yang, 2016, Human metapneumovirus uses endocytosis pathway for host cell entry, Mol. Cell Probes, 30, 231, 10.1016/j.mcp.2016.06.003 Yang, 2016, The role of cholesterol in membrane fusion, Chem. Phys. Lipids, 199, 136, 10.1016/j.chemphyslip.2016.05.003 Yao, 2013, Membrane-dependent conformation, dynamics, and lipid interactions of the fusion peptide of the paramyxovirus PIV5 from solid-state NMR, J. Mol. Biol., 425, 563, 10.1016/j.jmb.2012.11.027 Yao, 2014, Conformation and lipid interaction of the fusion peptide of the paramyxovirus PIV5 in anionic and negative-curvature membranes from solid-state NMR, J. Am. Chem. Soc., 136, 2611, 10.1021/ja4121956 Yao, 2015, Viral fusion protein transmembrane domain adopts (-strand structure to facilitate membrane topological changes for virus-cell fusion, Proc. Natl. Acad. Sci. U. S. A., 112, 10926, 10.1073/pnas.1501430112 Yap, 2010, Rapid and selective detection of fatty acylated proteins using omega-alkynyl-fatty acids and click chemistry, J. Lipid Res., 51, 1566, 10.1194/jlr.D002790 Yeste-Velasco, 2015, Protein S-palmitoylation and cancer, Biochim. Biophys. Acta, 1856, 107 Yin, 2005, Structure of the uncleaved ectodomain of the paramyxovirus (hPIV3) fusion protein, Proc. Natl. Acad. Sci. U. S. A., 102, 9288, 10.1073/pnas.0503989102 Yin, 2006, Structure of the parainfluenza virus 5F protein in its metastable, prefusion conformation, Nature, 439, 38, 10.1038/nature04322 Yun, 2015, Trypsin- and low pH-mediated fusogenicity of avian metapneumovirus fusion proteins is determined by residues at positions 100, 101 and 294, Sci. Rep., 5, 15584, 10.1038/srep15584 Zhang, 2000, Influenza virus assembly and lipid raft microdomains: a role for the cytoplasmic tails of the spike glycoproteins, J. Virol., 74, 4634, 10.1128/JVI.74.10.4634-4644.2000 Zhou, 2014, Recombinant influenza A H3N2 viruses with mutations of HA transmembrane cysteines exhibited altered virological characteristics, Virus Genes, 48, 273, 10.1007/s11262-013-1011-2 Zokarkar, 2012, The paramyxovirus fusion protein C-terminal region: mutagenesis indicates an indivisible protein unit, J. Virol., 86, 2600, 10.1128/JVI.06546-11 Zurcher, 1994, Mutations at palmitylation sites of the influenza virus hemagglutinin affect virus formation, J. Virol., 68, 5748, 10.1128/JVI.68.9.5748-5754.1994 de Vries, 2015, A cholesterol consensus motif is required for efficient intracellular transport and raft association of a group 2 HA from influenza virus, Biochem. J., 465, 305, 10.1042/BJ20141114