1887

Abstract

Influenza virus is a major human pathogen that causes annual epidemics and occasional pandemics. Moreover, the virus causes outbreaks in poultry and other animals, such as pigs, requiring costly and laborious countermeasures. Therefore, influenza virus has a substantial impact on health and the global economy. Here, we review entry of this important pathogen into target cells, an essential process by which viral genomes are delivered from extracellular virions to sites of transcription/replication in the cell nucleus. We summarize current knowledge on the interaction of influenza viruses with their receptor, sialic acid, and highlight the ongoing search for additional receptors. We describe receptor-mediated endocytosis and the recently discovered macropinocytosis as alternative virus uptake pathways, and illustrate the subsequent endosomal trafficking of the virus with advanced live microscopy techniques. Release of virus from the endosome and import of the viral ribonucleoproteins into the host cell nucleus are also outlined. Although a focus has been on viral protein function during entry, recent studies have revealed exciting information on cellular factors required for influenza virus entry. We highlight these, and discuss established entry inhibitors targeting viral and host factors, as well as the latest prospects for designing novel ‘anti-entry’ compounds. New entry inhibitors are of particular importance for current efforts to develop the next generation of anti-influenza drugs – entry is the first essential step of virus replication and is an ideal target to block infection efficiently.

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2014-02-01
2024-12-08
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References

  1. Baum L. G., Paulson J. C. 1990; Sialyloligosaccharides of the respiratory epithelium in the selection of human influenza virus receptor specificity. Acta Histochem Suppl 40:35–38[PubMed]
    [Google Scholar]
  2. Bodian D. L., Yamasaki R. B., Buswell R. L., Stearns J. F., White J. M., Kuntz I. D. 1993; Inhibition of the fusion-inducing conformational change of influenza hemagglutinin by benzoquinones and hydroquinones. Biochemistry 32:2967–2978 [View Article][PubMed]
    [Google Scholar]
  3. Bourmakina S. V., García-Sastre A. 2003; Reverse genetics studies on the filamentous morphology of influenza A virus. J Gen Virol 84:517–527 [View Article][PubMed]
    [Google Scholar]
  4. Bowman E. J., Siebers A., Altendorf K. 1988; Bafilomycins: a class of inhibitors of membrane ATPases from microorganisms, animal cells, and plant cells. Proc Natl Acad Sci U S A 85:7972–7976 [View Article][PubMed]
    [Google Scholar]
  5. Bright R. A., Medina M. J., Xu X., Perez-Oronoz G., Wallis T. R., Davis X. M., Povinelli L., Cox N. J., Klimov A. I. 2005; Incidence of adamantane resistance among influenza A (H3N2) viruses isolated worldwide from 1994 to 2005: a cause for concern. Lancet 366:1175–1181 [View Article][PubMed]
    [Google Scholar]
  6. Bucci C., Parton R. G., Mather I. H., Stunnenberg H., Simons K., Hoflack B., Zerial M. 1992; The small GTPase rab5 functions as a regulatory factor in the early endocytic pathway. Cell 70:715–728 [View Article][PubMed]
    [Google Scholar]
  7. Bui M., Whittaker G., Helenius A. 1996; Effect of M1 protein and low pH on nuclear transport of influenza virus ribonucleoproteins. J Virol 70:8391–8401[PubMed]
    [Google Scholar]
  8. Bukrinskaya A. G., Vorkunova N. K., Kornilayeva G. V., Narmanbetova R. A., Vorkunova G. K. 1982; Influenza virus uncoating in infected cells and effect of rimantadine. J Gen Virol 60:49–59 [View Article][PubMed]
    [Google Scholar]
  9. Bullido R., Gómez-Puertas P., Albo C., Portela A. 2000; Several protein regions contribute to determine the nuclear and cytoplasmic localization of the influenza A virus nucleoprotein. J Gen Virol 81:135–142[PubMed]
    [Google Scholar]
  10. Bullough P. A., Hughson F. M., Skehel J. J., Wiley D. C. 1994; Structure of influenza haemagglutinin at the pH of membrane fusion. Nature 371:37–43 [View Article][PubMed]
    [Google Scholar]
  11. Calder L. J., Wasilewski S., Berriman J. A., Rosenthal P. B. 2010; Structural organization of a filamentous influenza A virus. Proc Natl Acad Sci U S A 107:10685–10690 [View Article][PubMed]
    [Google Scholar]
  12. Carr C. M., Kim P. S. 1993; A spring-loaded mechanism for the conformational change of influenza hemagglutinin. Cell 73:823–832 [View Article][PubMed]
    [Google Scholar]
  13. Carroll S. M., Paulson J. C. 1985; Differential infection of receptor-modified host cells by receptor-specific influenza viruses. Virus Res 3:165–179 [View Article][PubMed]
    [Google Scholar]
  14. Chandrasekaran A., Srinivasan A., Raman R., Viswanathan K., Raguram S., Tumpey T. M., Sasisekharan V., Sasisekharan R. 2008; Glycan topology determines human adaptation of avian H5N1 virus hemagglutinin. Nat Biotechnol 26:107–113 [View Article][PubMed]
    [Google Scholar]
  15. Chen C., Zhuang X. 2008; Epsin 1 is a cargo-specific adaptor for the clathrin-mediated endocytosis of the influenza virus. Proc Natl Acad Sci U S A 105:11790–11795 [View Article][PubMed]
    [Google Scholar]
  16. Chen J., Skehel J. J., Wiley D. C. 1999; N- and C-terminal residues combine in the fusion-pH influenza hemagglutinin HA2 subunit to form an N cap that terminates the triple-stranded coiled coil. Proc Natl Acad Sci U S A 96:8967–8972 [View Article][PubMed]
    [Google Scholar]
  17. Chernomordik L. V., Frolov V. A., Leikina E., Bronk P., Zimmerberg J. 1998; The pathway of membrane fusion catalyzed by influenza hemagglutinin: restriction of lipids, hemifusion, and lipidic fusion pore formation. J Cell Biol 140:1369–1382 [View Article][PubMed]
    [Google Scholar]
  18. Chizhmakov I. V., Geraghty F. M., Ogden D. C., Hayhurst A., Antoniou M., Hay A. J. 1996; Selective proton permeability and pH regulation of the influenza virus M2 channel expressed in mouse erythroleukaemia cells. J Physiol 494:329–336[PubMed] [CrossRef]
    [Google Scholar]
  19. Chou Y. Y., Heaton N. S., Gao Q., Palese P., Singer R., Lionnet T. 2013; Colocalization of different influenza viral RNA segments in the cytoplasm before viral budding as shown by single-molecule sensitivity FISH analysis. PLoS Pathog 9:e1003358 [View Article][PubMed]
    [Google Scholar]
  20. Christoforidis S., McBride H. M., Burgoyne R. D., Zerial M. 1999a; The Rab5 effector EEA1 is a core component of endosome docking. Nature 397:621–625 [View Article][PubMed]
    [Google Scholar]
  21. Christoforidis S., Miaczynska M., Ashman K., Wilm M., Zhao L., Yip S. C., Waterfield M. D., Backer J. M., Zerial M. 1999b; Phosphatidylinositol-3-OH kinases are Rab5 effectors. Nat Cell Biol 1:249–252 [View Article][PubMed]
    [Google Scholar]
  22. Chu V. C., Whittaker G. R. 2004; Influenza virus entry and infection require host cell N-linked glycoprotein. Proc Natl Acad Sci U S A 101:18153–18158 [View Article][PubMed]
    [Google Scholar]
  23. Clementi N., Criscuolo E., Castelli M., Mancini N., Clementi M., Burioni R. 2012; Influenza B-cells protective epitope characterization: a passkey for the rational design of new broad-range anti-influenza vaccines. Viruses 4:3090–3108 [View Article][PubMed]
    [Google Scholar]
  24. Cocucci E., Aguet F., Boulant S., Kirchhausen T. 2012; The first five seconds in the life of a clathrin-coated pit. Cell 150:495–507 [View Article][PubMed]
    [Google Scholar]
  25. Connor R. J., Kawaoka Y., Webster R. G., Paulson J. C. 1994; Receptor specificity in human, avian, and equine H2 and H3 influenza virus isolates. Virology 205:17–23 [View Article][PubMed]
    [Google Scholar]
  26. Corti D., Lanzavecchia A. 2013; Broadly neutralizing antiviral antibodies. Annu Rev Immunol 31:705–742 [View Article][PubMed]
    [Google Scholar]
  27. Corti D., Voss J., Gamblin S. J., Codoni G., Macagno A., Jarrossay D., Vachieri S. G., Pinna D., Minola A. other authors 2011; A neutralizing antibody selected from plasma cells that binds to group 1 and group 2 influenza A hemagglutinins. Science 333:850–856 [View Article][PubMed]
    [Google Scholar]
  28. Cros J. F., Palese P. 2003; Trafficking of viral genomic RNA into and out of the nucleus: influenza, Thogoto and Borna disease viruses. Virus Res 95:3–12 [View Article][PubMed]
    [Google Scholar]
  29. Daniels R. S., Downie J. C., Hay A. J., Knossow M., Skehel J. J., Wang M. L., Wiley D. C. 1985; Fusion mutants of the influenza virus hemagglutinin glycoprotein. Cell 40:431–439 [View Article][PubMed]
    [Google Scholar]
  30. Davies W. L., Grunert R. R., Haff R. F., McGahen J. W., Neumayer E. M., Paulshock M., Watts J. C., Wood T. R., Hermann E. C., Hoffmann C. E. 1964; Antiviral activity of 1-adamantanamine (amantadine). Science 144:862–863 [View Article][PubMed]
    [Google Scholar]
  31. De Conto F., Covan S., Arcangeletti M. C., Orlandini G., Gatti R., Dettori G., Chezzi C. 2011; Differential infectious entry of human influenza A/NWS/33 virus (H1N1) in mammalian kidney cells. Virus Res 155:221–230 [View Article][PubMed]
    [Google Scholar]
  32. De Conto F., Di Lonardo E., Arcangeletti M. C., Chezzi C., Medici M. C., Calderaro A. 2012; Highly dynamic microtubules improve the effectiveness of early stages of human influenza A/NWS/33 virus infection in LLC-MK2 cells. PLoS ONE 7:e41207 [View Article][PubMed]
    [Google Scholar]
  33. de Vries E., Tscherne D. M., Wienholts M. J., Cobos-Jiménez V., Scholte F., García-Sastre A., Rottier P. J., de Haan C. A. 2011; Dissection of the influenza A virus endocytic routes reveals macropinocytosis as an alternative entry pathway. PLoS Pathog 7:e1001329 [View Article][PubMed]
    [Google Scholar]
  34. de Vries E., de Vries R. P., Wienholts M. J., Floris C. E., Jacobs M. S., van den Heuvel A., Rottier P. J., de Haan C. A. 2012; Influenza A virus entry into cells lacking sialylated N-glycans. Proc Natl Acad Sci U S A 109:7457–7462 [View Article][PubMed]
    [Google Scholar]
  35. Durrer P., Galli C., Hoenke S., Corti C., Glück R., Vorherr T., Brunner J. 1996; H+-induced membrane insertion of influenza virus hemagglutinin involves the HA2 amino-terminal fusion peptide but not the coiled coil region. J Biol Chem 271:13417–13421 [View Article][PubMed]
    [Google Scholar]
  36. Eierhoff T., Hrincius E. R., Rescher U., Ludwig S., Ehrhardt C. 2010; The epidermal growth factor receptor (EGFR) promotes uptake of influenza A viruses (IAV) into host cells. PLoS Pathog 6:e1001099 [View Article][PubMed]
    [Google Scholar]
  37. Ekiert D. C., Wilson I. A. 2012; Broadly neutralizing antibodies against influenza virus and prospects for universal therapies. Curr Opin Virol 2:134–141 [View Article][PubMed]
    [Google Scholar]
  38. Ekiert D. C., Bhabha G., Elsliger M. A., Friesen R. H., Jongeneelen M., Throsby M., Goudsmit J., Wilson I. A. 2009; Antibody recognition of a highly conserved influenza virus epitope. Science 324:246–251 [View Article][PubMed]
    [Google Scholar]
  39. Ekiert D. C., Kashyap A. K., Steel J., Rubrum A., Bhabha G., Khayat R., Lee J. H., Dillon M. A., O’Neil R. E. other authors 2012; Cross-neutralization of influenza A viruses mediated by a single antibody loop. Nature 489:526–532 [View Article][PubMed]
    [Google Scholar]
  40. Elleman C. J., Barclay W. S. 2004; The M1 matrix protein controls the filamentous phenotype of influenza A virus. Virology 321:144–153 [View Article][PubMed]
    [Google Scholar]
  41. Elster C., Fourest E., Baudin F., Larsen K., Cusack S., Ruigrok R. W. 1994; A small percentage of influenza virus M1 protein contains zinc but zinc does not influence in vitro M1-RNA interaction. J Gen Virol 75:37–42 [View Article][PubMed]
    [Google Scholar]
  42. Fontana J., Steven A. C. 2013; At low pH, influenza virus matrix protein M1 undergoes a conformational change prior to dissociating from the membrane. J Virol 87:5621–5628 [View Article][PubMed]
    [Google Scholar]
  43. Fontana J., Cardone G., Heymann J. B., Winkler D. C., Steven A. C. 2012; Structural changes in Influenza virus at low pH characterized by cryo-electron tomography. J Virol 86:2919–2929 [View Article][PubMed]
    [Google Scholar]
  44. Forgac M. 2007; Vacuolar ATPases: rotary proton pumps in physiology and pathophysiology. Nat Rev Mol Cell Biol 8:917–929 [View Article][PubMed]
    [Google Scholar]
  45. Fujioka Y., Tsuda M., Hattori T., Sasaki J., Sasaki T., Miyazaki T., Ohba Y. 2011; The Ras-PI3K signaling pathway is involved in clathrin-independent endocytosis and the internalization of influenza viruses. PLoS ONE 6:e16324 [View Article][PubMed]
    [Google Scholar]
  46. Galloway C. J., Dean G. E., Marsh M., Rudnick G., Mellman I. 1983; Acidification of macrophage and fibroblast endocytic vesicles in vitro. Proc Natl Acad Sci U S A 80:3334–3338 [View Article][PubMed]
    [Google Scholar]
  47. Galloway S. E., Reed M. L., Russell C. J., Steinhauer D. A. 2013; Influenza HA subtypes demonstrate divergent phenotypes for cleavage activation and pH of fusion: implications for host range and adaptation. PLoS Pathog 9:e1003151 [View Article][PubMed]
    [Google Scholar]
  48. Gambaryan A. S., Tuzikov A. B., Pazynina G. V., Desheva J. A., Bovin N. V., Matrosovich M. N., Klimov A. I. 2008; 6-Sulfo sialyl Lewis X is the common receptor determinant recognized by H5, H6, H7 and H9 influenza viruses of terrestrial poultry. Virol J 5:85 [View Article][PubMed]
    [Google Scholar]
  49. Gamblin S. J., Haire L. F., Russell R. J., Stevens D. J., Xiao B., Ha Y., Vasisht N., Steinhauer D. A., Daniels R. S. other authors 2004; The structure and receptor binding properties of the 1918 influenza hemagglutinin. Science 303:1838–1842 [View Article][PubMed]
    [Google Scholar]
  50. Gottlieb T. A., Ivanov I. E., Adesnik M., Sabatini D. D. 1993; Actin microfilaments play a critical role in endocytosis at the apical but not the basolateral surface of polarized epithelial cells. J Cell Biol 120:695–710 [View Article][PubMed]
    [Google Scholar]
  51. Grambas S., Bennett M. S., Hay A. J. 1992; Influence of amantadine resistance mutations on the pH regulatory function of the M2 protein of influenza A viruses. Virology 191:541–549 [View Article][PubMed]
    [Google Scholar]
  52. Guinea R., Carrasco L. 1995; Requirement for vacuolar proton-ATPase activity during entry of influenza virus into cells. J Virol 69:2306–2312 [View Article][PubMed]
    [Google Scholar]
  53. Hay A. J., Wolstenholme A. J., Skehel J. J., Smith M. H. 1985; The molecular basis of the specific anti-influenza action of amantadine. EMBO J 4:3021–3024[PubMed]
    [Google Scholar]
  54. Hay A. J., Zambon M. C., Wolstenholme A. J., Skehel J. J., Smith M. H. 1986; Molecular basis of resistance of influenza A viruses to amantadine. J Antimicrob Chemother 18:Suppl B19–29 [View Article][PubMed]
    [Google Scholar]
  55. Hayden F. G., Sperber S. J., Belshe R. B., Clover R. D., Hay A. J., Pyke S. 1991; Recovery of drug-resistant influenza A virus during therapeutic use of rimantadine. Antimicrob Agents Chemother 35:1741–1747 [View Article][PubMed]
    [Google Scholar]
  56. He J., Sun E., Bujny M. V., Kim D., Davidson M. W., Zhuang X. 2013; Dual function of CD81 in influenza virus uncoating and budding. PLoS Pathog 9:e1003701 [View Article][PubMed]
    [Google Scholar]
  57. Hendricks G. L., Weirich K. L., Viswanathan K., Li J., Shriver Z. H., Ashour J., Ploegh H. L., Kurt-Jones E. A., Fygenson D. K. other authors 2013; Sialylneolacto-N-tetraose c (LSTc)-bearing liposomal decoys capture influenza A virus. J Biol Chem 288:8061–8073 [View Article][PubMed]
    [Google Scholar]
  58. Holsinger L. J., Lamb R. A. 1991; Influenza virus M2 integral membrane protein is a homotetramer stabilized by formation of disulfide bonds. Virology 183:32–43 [View Article][PubMed]
    [Google Scholar]
  59. Huang R. T., Lichtenberg B., Rick O. 1996; Involvement of annexin V in the entry of influenza viruses and role of phospholipids in infection. FEBS Lett 392:59–62 [View Article][PubMed]
    [Google Scholar]
  60. Huotari J., Helenius A. 2011; Endosome maturation. EMBO J 30:3481–3500 [View Article][PubMed]
    [Google Scholar]
  61. Huotari J., Meyer-Schaller N., Hubner M., Stauffer S., Katheder N., Horvath P., Mancini R., Helenius A., Peter M. 2012; Cullin-3 regulates late endosome maturation. Proc Natl Acad Sci U S A 109:823–828 [View Article][PubMed]
    [Google Scholar]
  62. Huss M., Wieczorek H. 2009; Inhibitors of V-ATPases: old and new players. J Exp Biol 212:341–346 [View Article][PubMed]
    [Google Scholar]
  63. Hutchinson E. C., Fodor E. 2012; Nuclear import of the influenza A virus transcriptional machinery. Vaccine 30:7353–7358 [View Article][PubMed]
    [Google Scholar]
  64. Imai M., Kawaoka Y. 2012; The role of receptor binding specificity in interspecies transmission of influenza viruses. Curr Opin Virol 2:160–167 [View Article][PubMed]
    [Google Scholar]
  65. Ito T., Suzuki Y., Suzuki T., Takada A., Horimoto T., Wells K., Kida H., Otsuki K., Kiso M. other authors 2000; Recognition of N-glycolylneuraminic acid linked to galactose by the α2,3 linkage is associated with intestinal replication of influenza A virus in ducks. J Virol 74:9300–9305 [View Article][PubMed]
    [Google Scholar]
  66. Kemler I., Whittaker G., Helenius A. 1994; Nuclear import of microinjected influenza virus ribonucleoproteins. Virology 202:1028–1033 [View Article][PubMed]
    [Google Scholar]
  67. Kesimer M., Scull M., Brighton B., DeMaria G., Burns K., O’Neal W., Pickles R. J., Sheehan J. K. 2009; Characterization of exosome-like vesicles released from human tracheobronchial ciliated epithelium: a possible role in innate defense. FASEB J 23:1858–1868 [View Article][PubMed]
    [Google Scholar]
  68. Kimura K., Mori S., Tomita K., Ohno K., Takahashi K., Shigeta S., Terada M. 2000; Antiviral activity of NMSO3 against respiratory syncytial virus infection in vitro and in vivo. Antiviral Res 47:41–51 [View Article][PubMed]
    [Google Scholar]
  69. Koivusalo M., Welch C., Hayashi H., Scott C. C., Kim M., Alexander T., Touret N., Hahn K. M., Grinstein S. 2010; Amiloride inhibits macropinocytosis by lowering submembranous pH and preventing Rac1 and Cdc42 signaling. J Cell Biol 188:547–563 [View Article][PubMed]
    [Google Scholar]
  70. König R., Stertz S., Zhou Y., Inoue A., Hoffmann H. H., Bhattacharyya S., Alamares J. G., Tscherne D. M., Ortigoza M. B. other authors 2010; Human host factors required for influenza virus replication. Nature 463:813–817 [View Article][PubMed]
    [Google Scholar]
  71. Korte T., Ludwig K., Booy F. P., Blumenthal R., Herrmann A. 1999; Conformational intermediates and fusion activity of influenza virus hemagglutinin. J Virol 73:4567–4574[PubMed]
    [Google Scholar]
  72. Lakadamyali M., Rust M. J., Babcock H. P., Zhuang X. 2003; Visualizing infection of individual influenza viruses. Proc Natl Acad Sci U S A 100:9280–9285 [View Article][PubMed]
    [Google Scholar]
  73. Lamb R. A., Choppin P. W. 1981; Identification of a second protein (M2) encoded by RNA segment 7 of influenza virus. Virology 112:729–737 [View Article][PubMed]
    [Google Scholar]
  74. Leikina E., Ramos C., Markovic I., Zimmerberg J., Chernomordik L. V. 2002; Reversible stages of the low-pH-triggered conformational change in influenza virus hemagglutinin. EMBO J 21:5701–5710 [View Article][PubMed]
    [Google Scholar]
  75. Leneva I. A., Russell R. J., Boriskin Y. S., Hay A. J. 2009; Characteristics of arbidol-resistant mutants of influenza virus: implications for the mechanism of anti-influenza action of arbidol. Antiviral Res 81:132–140 [View Article][PubMed]
    [Google Scholar]
  76. Liu J., Stevens D. J., Haire L. F., Walker P. A., Coombs P. J., Russell R. J., Gamblin S. J., Skehel J. J. 2009; Structures of receptor complexes formed by hemagglutinins from the Asian influenza pandemic of 1957. Proc Natl Acad Sci U S A 106:17175–17180 [View Article][PubMed]
    [Google Scholar]
  77. Londrigan S. L., Turville S. G., Tate M. D., Deng Y. M., Brooks A. G., Reading P. C. 2011; N-Linked glycosylation facilitates sialic acid-independent attachment and entry of influenza A viruses into cells expressing DC-SIGN or L-SIGN. J Virol 85:2990–3000 [View Article][PubMed]
    [Google Scholar]
  78. Luo G., Torri A., Harte W. E., Danetz S., Cianci C., Tiley L., Day S., Mullaney D., Yu K. L. other authors 1997; Molecular mechanism underlying the action of a novel fusion inhibitor of influenza A virus. J Virol 71:4062–4070[PubMed]
    [Google Scholar]
  79. Luzio J. P., Pryor P. R., Bright N. A. 2007; Lysosomes: fusion and function. Nat Rev Mol Cell Biol 8:622–632 [View Article][PubMed]
    [Google Scholar]
  80. Maeda T., Ohnishi S. 1980; Activation of influenza virus by acidic media causes hemolysis and fusion of erythrocytes. FEBS Lett 122:283–287 [View Article][PubMed]
    [Google Scholar]
  81. Markovic I., Leikina E., Zhukovsky M., Zimmerberg J., Chernomordik L. V. 2001; Synchronized activation and refolding of influenza hemagglutinin in multimeric fusion machines. J Cell Biol 155:833–844 [View Article][PubMed]
    [Google Scholar]
  82. Martin K., Helenius A. 1991; Transport of incoming influenza virus nucleocapsids into the nucleus. J Virol 65:232–244[PubMed]
    [Google Scholar]
  83. Martinez O., Tsibane T., Basler C. F. 2009; Neutralizing anti-influenza virus monoclonal antibodies: therapeutics and tools for discovery. Int Rev Immunol 28:69–92 [View Article][PubMed]
    [Google Scholar]
  84. Matlin K. S., Reggio H., Helenius A., Simons K. 1981; Infectious entry pathway of influenza virus in a canine kidney cell line. J Cell Biol 91:601–613 [View Article][PubMed]
    [Google Scholar]
  85. Matrosovich M., Stech J., Klenk H. D. 2009; Influenza receptors, polymerase and host range. Rev Sci Tech 28:203–217[PubMed]
    [Google Scholar]
  86. Matsubara T., Sumi M., Kubota H., Taki T., Okahata Y., Sato T. 2009; Inhibition of influenza virus infections by sialylgalactose-binding peptides selected from a phage library. J Med Chem 52:4247–4256 [View Article][PubMed]
    [Google Scholar]
  87. Matsubara T., Onishi A., Saito T., Shimada A., Inoue H., Taki T., Nagata K., Okahata Y., Sato T. 2010; Sialic acid-mimic peptides as hemagglutinin inhibitors for anti-influenza therapy. J Med Chem 53:4441–4449 [View Article][PubMed]
    [Google Scholar]
  88. Maxfield F. R., Yamashiro D. J. 1987; Endosome acidification and the pathways of receptor-mediated endocytosis. Adv Exp Med Biol 225:189–198 [View Article][PubMed]
    [Google Scholar]
  89. Melen K., Fagerlund R., Franke J., Kohler M., Kinnunen L., Julkunen I. 2003; Importin α nuclear localization signal binding sites for STAT1, STAT2, and influenza A virus nucleoprotein. J Biol Chem 278:28193–28200 [View Article][PubMed]
    [Google Scholar]
  90. Melikyan G. B., Niles W. D., Cohen F. S. 1993a; Influenza virus hemagglutinin-induced cell-planar bilayer fusion: quantitative dissection of fusion pore kinetics into stages. J Gen Physiol 102:1151–1170 [View Article][PubMed]
    [Google Scholar]
  91. Melikyan G. B., Niles W. D., Peeples M. E., Cohen F. S. 1993b; Influenza hemagglutinin-mediated fusion pores connecting cells to planar membranes: flickering to final expansion. J Gen Physiol 102:1131–1149 [View Article][PubMed]
    [Google Scholar]
  92. Mellman I. 1996; Endocytosis and molecular sorting. Annu Rev Cell Dev Biol 12:575–625 [View Article][PubMed]
    [Google Scholar]
  93. Mu F. T., Callaghan J. M., Steele-Mortimer O., Stenmark H., Parton R. G., Campbell P. L., McCluskey J., Yeo J. P., Tock E. P., Toh B. H. 1995; EEA1, an early endosome-associated protein. EEA1 is a conserved α-helical peripheral membrane protein flanked by cysteine “fingers” and contains a calmodulin-binding IQ motif. J Biol Chem 270:13503–13511[PubMed] [CrossRef]
    [Google Scholar]
  94. Müller K. H., Kainov D. E., El Bakkouri K., Saelens X., De Brabander J. K., Kittel C., Samm E., Muller C. P. 2011; The proton translocation domain of cellular vacuolar ATPase provides a target for the treatment of influenza A virus infections. Br J Pharmacol 164:344–357 [View Article][PubMed]
    [Google Scholar]
  95. Nicholls J. M., Moss R. B., Haslam S. M. 2013; The use of sialidase therapy for respiratory viral infections. Antiviral Res 98:401–409 [View Article][PubMed]
    [Google Scholar]
  96. Nicol M. Q., Ligertwood Y., Bacon M. N., Dutia B. M., Nash A. A. 2012; A novel family of peptides with potent activity against influenza A viruses. J Gen Virol 93:980–986 [View Article][PubMed]
    [Google Scholar]
  97. Nielsen E., Severin F., Backer J. M., Hyman A. A., Zerial M. 1999; Rab5 regulates motility of early endosomes on microtubules. Nat Cell Biol 1:376–382 [View Article][PubMed]
    [Google Scholar]
  98. Noton S. L., Medcalf E., Fisher D., Mullin A. E., Elton D., Digard P. 2007; Identification of the domains of the influenza A virus M1 matrix protein required for NP binding, oligomerization and incorporation into virions. J Gen Virol 88:2280–2290 [View Article][PubMed]
    [Google Scholar]
  99. O’Neill R. E., Jaskunas R., Blobel G., Palese P., Moroianu J. 1995; Nuclear import of influenza virus RNA can be mediated by viral nucleoprotein and transport factors required for protein import. J Biol Chem 270:22701–22704 [View Article][PubMed]
    [Google Scholar]
  100. Ochiai H., Sakai S., Hirabayashi T., Shimizu Y., Terasawa K. 1995; Inhibitory effect of bafilomycin A1, a specific inhibitor of vacuolar-type proton pump, on the growth of influenza A and B viruses in MDCK cells. Antiviral Res 27:425–430 [View Article][PubMed]
    [Google Scholar]
  101. Okada A., Miura T., Takeuchi H. 2003; Zinc- and pH-dependent conformational transition in a putative interdomain linker region of the influenza virus matrix protein M1. Biochemistry 42:1978–1984 [View Article][PubMed]
    [Google Scholar]
  102. Okuno Y., Isegawa Y., Sasao F., Ueda S. 1993; A common neutralizing epitope conserved between the hemagglutinins of influenza A virus H1 and H2 strains. J Virol 67:2552–2558[PubMed]
    [Google Scholar]
  103. Palese P., Shaw M. L. 2007; Orthomyxoviridae: the viruses and their replication. In Fields Virology, 5th edn. pp. 1647–1689 Edited by Knipe D. M., Howley P. M. Philadelphia, PA: Lippincott Williams and Wilkins;
    [Google Scholar]
  104. Patterson S., Oxford J. S., Dourmashkin R. R. 1979; Studies on the mechanism of influenza virus entry into cells. J Gen Virol 43:223–229 [View Article][PubMed]
    [Google Scholar]
  105. Pérez L., Carrasco L. 1994; Involvement of the vacuolar H+-ATPase in animal virus entry. J Gen Virol 75:2595–2606 [View Article][PubMed]
    [Google Scholar]
  106. Pinto L. H., Holsinger L. J., Lamb R. A. 1992; Influenza virus M2 protein has ion channel activity. Cell 69:517–528 [View Article][PubMed]
    [Google Scholar]
  107. Plotch S. J., O’Hara B., Morin J., Palant O., LaRocque J., Bloom J. D., Lang S. A. Jr, DiGrandi M. J., Bradley M. other authors 1999; Inhibition of influenza A virus replication by compounds interfering with the fusogenic function of the viral hemagglutinin. J Virol 73:140–151[PubMed]
    [Google Scholar]
  108. Rabinovich S., Baldini J. T., Bannister R. 1969; Treatment of influenza. The therapeutic efficacy of rimantadine HC1 in a naturally occurring influenza A2 outbreak. Am J Med Sci 257:328–335 [CrossRef]
    [Google Scholar]
  109. Reading P. C., Miller J. L., Anders E. M. 2000; Involvement of the mannose receptor in infection of macrophages by influenza virus. J Virol 74:5190–5197 [View Article][PubMed]
    [Google Scholar]
  110. Rink J., Ghigo E., Kalaidzidis Y., Zerial M. 2005; Rab conversion as a mechanism of progression from early to late endosomes. Cell 122:735–749 [View Article][PubMed]
    [Google Scholar]
  111. Roberts P. C., Garten W., Klenk H. D. 1993; Role of conserved glycosylation sites in maturation and transport of influenza A virus hemagglutinin. J Virol 67:3048–3060[PubMed]
    [Google Scholar]
  112. Roberts P. C., Lamb R. A., Compans R. W. 1998; The M1 and M2 proteins of influenza A virus are important determinants in filamentous particle formation. Virology 240:127–137 [View Article][PubMed]
    [Google Scholar]
  113. Roberts K. L., Shelton H., Scull M., Pickles R., Barclay W. S. 2011; Lack of transmission of a human influenza virus with avian receptor specificity between ferrets is not due to decreased virus shedding but rather a lower infectivity in vivo . J Gen Virol 92:1822–1831 [View Article][PubMed]
    [Google Scholar]
  114. Rossman J. S., Lamb R. A. 2011; Influenza virus assembly and budding. Virology 411:229–236 [View Article][PubMed]
    [Google Scholar]
  115. Rossman J. S., Leser G. P., Lamb R. A. 2012; Filamentous influenza virus enters cells via macropinocytosis. J Virol 86:10950–10960 [View Article][PubMed]
    [Google Scholar]
  116. Roy A. M., Parker J. S., Parrish C. R., Whittaker G. R. 2000; Early stages of influenza virus entry into Mv-1 lung cells: involvement of dynamin. Virology 267:17–28 [CrossRef]
    [Google Scholar]
  117. Ruigrok R. W., Barge A., Durrer P., Brunner J., Ma K., Whittaker G. R. 2000; Membrane interaction of influenza virus M1 protein. Virology 267:289–298 [View Article][PubMed]
    [Google Scholar]
  118. Russell R. J., Kerry P. S., Stevens D. J., Steinhauer D. A., Martin S. R., Gamblin S. J., Skehel J. J. 2008; Structure of influenza hemagglutinin in complex with an inhibitor of membrane fusion. Proc Natl Acad Sci U S A 105:17736–17741 [View Article][PubMed]
    [Google Scholar]
  119. Rust M. J., Lakadamyali M., Zhang F., Zhuang X. 2004; Assembly of endocytic machinery around individual influenza viruses during viral entry. Nat Struct Mol Biol 11:567–573 [View Article][PubMed]
    [Google Scholar]
  120. Sauter N. K., Bednarski M. D., Wurzburg B. A., Hanson J. E., Whitesides G. M., Skehel J. J., Wiley D. C. 1989; Hemagglutinins from two influenza virus variants bind to sialic acid derivatives with millimolar dissociation constants: a 500-MHz proton nuclear magnetic resonance study. Biochemistry 28:8388–8396 [View Article][PubMed]
    [Google Scholar]
  121. Schmitt A. P., Lamb R. A. 2005; Influenza virus assembly and budding at the viral budozone. Adv Virus Res 64:383–416 [View Article][PubMed]
    [Google Scholar]
  122. Sieczkarski S. B., Whittaker G. R. 2002; Influenza virus can enter and infect cells in the absence of clathrin-mediated endocytosis. J Virol 76:10455–10464 [View Article][PubMed]
    [Google Scholar]
  123. Sieczkarski S. B., Whittaker G. R. 2003; Differential requirements of Rab5 and Rab7 for endocytosis of influenza and other enveloped viruses. Traffic 4:333–343 [View Article][PubMed]
    [Google Scholar]
  124. Sieczkarski S. B., Whittaker G. R. 2005; Characterization of the host cell entry of filamentous influenza virus. Arch Virol 150:1783–1796 [View Article][PubMed]
    [Google Scholar]
  125. Sieczkarski S. B., Brown H. A., Whittaker G. R. 2003; Role of protein kinase C betaII in influenza virus entry via late endosomes. J Virol 77:460–469 [View Article][PubMed]
    [Google Scholar]
  126. Simonsen A., Lippé R., Christoforidis S., Gaullier J. M., Brech A., Callaghan J., Toh B. H., Murphy C., Zerial M., Stenmark H. 1998; EEA1 links PI(3)K function to Rab5 regulation of endosome fusion. Nature 394:494–498 [View Article][PubMed]
    [Google Scholar]
  127. Skehel J. J., Wiley D. C. 2000; Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Annu Rev Biochem 69:531–569 [View Article][PubMed]
    [Google Scholar]
  128. Skehel J. J., Hay A. J., Armstrong J. A. 1978; On the mechanism of inhibition of influenza virus replication by amantadine hydrochloride. J Gen Virol 38:97–110 [View Article][PubMed]
    [Google Scholar]
  129. Spruce A. E., Iwata A., White J. M., Almers W. 1989; Patch clamp studies of single cell-fusion events mediated by a viral fusion protein. Nature 342:555–558 [View Article][PubMed]
    [Google Scholar]
  130. Steinhauer D. A. 2013; Influenza: pathways to human adaptation. Nature 499:412–413 [View Article][PubMed]
    [Google Scholar]
  131. Steinman R. M., Mellman I. S., Muller W. A., Cohn Z. A. 1983; Endocytosis and the recycling of plasma membrane. J Cell Biol 96:1–27 [View Article][PubMed]
    [Google Scholar]
  132. Stevens J., Blixt O., Glaser L., Taubenberger J. K., Palese P., Paulson J. C., Wilson I. A. 2006a; Glycan microarray analysis of the hemagglutinins from modern and pandemic influenza viruses reveals different receptor specificities. J Mol Biol 355:1143–1155 [View Article][PubMed]
    [Google Scholar]
  133. Stevens J., Blixt O., Tumpey T. M., Taubenberger J. K., Paulson J. C., Wilson I. A. 2006b; Structure and receptor specificity of the hemagglutinin from an H5N1 influenza virus. Science 312:404–410 [View Article][PubMed]
    [Google Scholar]
  134. Stouffer A. L., Acharya R., Salom D., Levine A. S., Di Costanzo L., Soto C. S., Tereshko V., Nanda V., Stayrook S., DeGrado W. F. 2008; Structural basis for the function and inhibition of an influenza virus proton channel. Nature 451:596–599 [View Article][PubMed]
    [Google Scholar]
  135. Stray S. J., Cummings R. D., Air G. M. 2000; Influenza virus infection of desialylated cells. Glycobiology 10:649–658 [View Article][PubMed]
    [Google Scholar]
  136. Su W. C., Chen Y. C., Tseng C. H., Hsu P. W., Tung K. F., Jeng K. S., Lai M. M. 2013; Pooled RNAi screen identifies ubiquitin ligase Itch as crucial for influenza A virus release from the endosome during virus entry. Proc Natl Acad Sci U S A 110:17516–17521 [View Article][PubMed]
    [Google Scholar]
  137. Sugrue R. J., Hay A. J. 1991; Structural characteristics of the M2 protein of influenza A viruses: evidence that it forms a tetrameric channel. Virology 180:617–624 [View Article][PubMed]
    [Google Scholar]
  138. Sui J., Hwang W. C., Perez S., Wei G., Aird D., Chen L. M., Santelli E., Stec B., Cadwell G. other authors 2009; Structural and functional bases for broad-spectrum neutralization of avian and human influenza A viruses. Nat Struct Mol Biol 16:265–273 [View Article][PubMed]
    [Google Scholar]
  139. Sun X., Whittaker G. R. 2007; Role of the actin cytoskeleton during influenza virus internalization into polarized epithelial cells. Cell Microbiol 9:1672–1682 [View Article][PubMed]
    [Google Scholar]
  140. Sun X., Shi Y., Lu X., He J., Gao F., Yan J., Qi J., Gao G. F. 2013; Bat-derived influenza hemagglutinin H17 does not bind canonical avian or human receptors and most likely uses a unique entry mechanism. Cell Rep 3:769–778 [View Article][PubMed]
    [Google Scholar]
  141. Sweet C., Hayden F. G., Jakeman K. J., Grambas S., Hay A. J. 1991; Virulence of rimantadine-resistant human influenza A (H3N2) viruses in ferrets. J Infect Dis 164:969–972 [View Article][PubMed]
    [Google Scholar]
  142. Tatulian S. A., Hinterdorfer P., Baber G., Tamm L. K. 1995; Influenza hemagglutinin assumes a tilted conformation during membrane fusion as determined by attenuated total reflection FTIR spectroscopy. EMBO J 14:5514–5523[PubMed]
    [Google Scholar]
  143. Terabayashi T., Morita M., Ueno M., Nakamura T., Urashima T. 2006; Inhibition of influenza-virus-induced cytopathy by sialylglycoconjugates. Carbohydr Res 341:2246–2253 [View Article][PubMed]
    [Google Scholar]
  144. Thompson C. I., Barclay W. S., Zambon M. C., Pickles R. J. 2006; Infection of human airway epithelium by human and avian strains of influenza A virus. J Virol 80:8060–8068 [View Article][PubMed]
    [Google Scholar]
  145. Throsby M., van den Brink E., Jongeneelen M., Poon L. L., Alard P., Cornelissen L., Bakker A., Cox F., van Deventer E. other authors 2008; Heterosubtypic neutralizing monoclonal antibodies cross-protective against H5N1 and H1N1 recovered from human IgM+ memory B cells. PLoS ONE 3:e3942 [View Article][PubMed]
    [Google Scholar]
  146. Tong S., Li Y., Rivailler P., Conrardy C., Castillo D. A., Chen L. M., Recuenco S., Ellison J. A., Davis C. T. other authors 2012; A distinct lineage of influenza A virus from bats. Proc Natl Acad Sci U S A 109:4269–4274 [View Article][PubMed]
    [Google Scholar]
  147. Tong S., Zhu X., Li Y., Shi M., Zhang J., Bourgeois M., Yang H., Chen X., Recuenco S. other authors 2013; New world bats harbor diverse influenza a viruses. PLoS Pathog 9:e1003657 [View Article][PubMed]
    [Google Scholar]
  148. Tsurudome M., Glück R., Graf R., Falchetto R., Schaller U., Brunner J. 1992; Lipid interactions of the hemagglutinin HA2 NH2-terminal segment during influenza virus-induced membrane fusion. J Biol Chem 267:20225–20232[PubMed]
    [Google Scholar]
  149. Upham J. P., Pickett D., Irimura T., Anders E. M., Reading P. C. 2010; Macrophage receptors for influenza A virus: role of the macrophage galactose-type lectin and mannose receptor in viral entry. J Virol 84:3730–3737 [View Article][PubMed]
    [Google Scholar]
  150. Vanderlinden E., Göktas F., Cesur Z., Froeyen M., Reed M. L., Russell C. J., Cesur N., Naesens L. 2010; Novel inhibitors of influenza virus fusion: structure-activity relationship and interaction with the viral hemagglutinin. J Virol 84:4277–4288 [View Article][PubMed]
    [Google Scholar]
  151. Vanderlinden E., Naesens L. 2013; Emerging antiviral strategies to interfere with influenza virus entry. Med Res Rev (in press)
    [Google Scholar]
  152. Vigant F., Lee J., Hollmann A., Tanner L. B., Akyol Ataman Z., Yun T., Shui G., Aguilar H. C., Zhang D. other authors 2013; A mechanistic paradigm for broad-spectrum antivirals that target virus-cell fusion. PLoS Pathog 9:e1003297 [View Article][PubMed]
    [Google Scholar]
  153. Wang C., Takeuchi K., Pinto L. H., Lamb R. A. 1993; Ion channel activity of influenza A virus M2 protein: characterization of the amantadine block. J Virol 67:5585–5594[PubMed]
    [Google Scholar]
  154. Wang P., Palese P., O’Neill R. E. 1997; The NPI-1/NPI-3 (karyopherin α) binding site on the influenza a virus nucleoprotein NP is a nonconventional nuclear localization signal. J Virol 71:1850–1856[PubMed]
    [Google Scholar]
  155. Wang S. F., Huang J. C., Lee Y. M., Liu S. J., Chan Y. J., Chau Y. P., Chong P., Chen Y. M. 2008; DC-SIGN mediates avian H5N1 influenza virus infection in cis and in trans. Biochem Biophys Res Commun 373:561–566 [View Article][PubMed]
    [Google Scholar]
  156. Wang J., Ma C., Wang J., Jo H., Canturk B., Fiorin G., Pinto L. H., Lamb R. A., Klein M. L., DeGrado W. F. 2013; Discovery of novel dual inhibitors of the wild-type and the most prevalent drug-resistant mutant, S31N, of the M2 proton channel from influenza A virus. J Med Chem 56:2804–2812 [View Article][PubMed]
    [Google Scholar]
  157. Weber T., Paesold G., Galli C., Mischler R., Semenza G., Brunner J. 1994; Evidence for H+-induced insertion of influenza hemagglutinin HA2 N-terminal segment into viral membrane. J Biol Chem 269:18353–18358[PubMed]
    [Google Scholar]
  158. Weber F., Kochs G., Gruber S., Haller O. 1998; A classical bipartite nuclear localization signal on Thogoto and influenza A virus nucleoproteins. Virology 250:9–18 [View Article][PubMed]
    [Google Scholar]
  159. Weis W., Brown J. H., Cusack S., Paulson J. C., Skehel J. J., Wiley D. C. 1988; Structure of the influenza virus haemagglutinin complexed with its receptor, sialic acid. Nature 333:426–431 [View Article][PubMed]
    [Google Scholar]
  160. Wharton S. A., Belshe R. B., Skehel J. J., Hay A. J. 1994; Role of virion M2 protein in influenza virus uncoating: specific reduction in the rate of membrane fusion between virus and liposomes by amantadine. J Gen Virol 75:945–948 [View Article][PubMed]
    [Google Scholar]
  161. White J. M., Wilson I. A. 1987; Anti-peptide antibodies detect steps in a protein conformational change: low-pH activation of the influenza virus hemagglutinin. J Cell Biol 105:2887–2896 [View Article][PubMed]
    [Google Scholar]
  162. Whittle J. R., Zhang R., Khurana S., King L. R., Manischewitz J., Golding H., Dormitzer P. R., Haynes B. F., Walter E. B. other authors 2011; Broadly neutralizing human antibody that recognizes the receptor-binding pocket of influenza virus hemagglutinin. Proc Natl Acad Sci U S A 108:14216–14221 [View Article][PubMed]
    [Google Scholar]
  163. Wilks S., de Graaf M., Smith D. J., Burke D. F. 2012; A review of influenza haemagglutinin receptor binding as it relates to pandemic properties. Vaccine 30:4369–4376 [View Article][PubMed]
    [Google Scholar]
  164. Wolf M. C., Freiberg A. N., Zhang T., Akyol-Ataman Z., Grock A., Hong P. W., Li J., Watson N. F., Fang A. Q. other authors 2010; A broad-spectrum antiviral targeting entry of enveloped viruses. Proc Natl Acad Sci U S A 107:3157–3162 [View Article][PubMed]
    [Google Scholar]
  165. Xiong X., Coombs P. J., Martin S. R., Liu J., Xiao H., McCauley J. W., Locher K., Walker P. A., Collins P. J. other authors 2013a; Receptor binding by a ferret-transmissible H5 avian influenza virus. Nature 497:392–396 [View Article][PubMed]
    [Google Scholar]
  166. Xiong X., Martin S. R., Haire L. F., Wharton S. A., Daniels R. S., Bennett M. S., McCauley J. W., Collins P. J., Walker P. A. other authors 2013b; Receptor binding by an H7N9 influenza virus from humans. Nature 499:496–499 [View Article][PubMed]
    [Google Scholar]
  167. Xu R., McBride R., Paulson J. C., Basler C. F., Wilson I. A. 2010; Structure, receptor binding, and antigenicity of influenza virus hemagglutinins from the 1957 H2N2 pandemic. J Virol 84:1715–1721 [View Article][PubMed]
    [Google Scholar]
  168. Yamauchi Y., Boukari H., Banerjee I., Sbalzarini I. F., Horvath P., Helenius A. 2011; Histone deacetylase 8 is required for centrosome cohesion and influenza A virus entry. PLoS Pathog 7:e1002316 [View Article][PubMed]
    [Google Scholar]
  169. Yoshida R., Igarashi M., Ozaki H., Kishida N., Tomabechi D., Kida H., Ito K., Takada A. 2009; Cross-protective potential of a novel monoclonal antibody directed against antigenic site B of the hemagglutinin of influenza A viruses. PLoS Pathog 5:e1000350 [View Article][PubMed]
    [Google Scholar]
  170. Yoshimoto J., Kakui M., Iwasaki H., Fujiwara T., Sugimoto H., Hattori N. 1999; Identification of a novel HA conformational change inhibitor of human influenza virus. Arch Virol 144:865–878 [View Article][PubMed]
    [Google Scholar]
  171. Yoshimura A., Kuroda K., Kawasaki K., Yamashina S., Maeda T., Ohnishi S. 1982; Infectious cell entry mechanism of influenza virus. J Virol 43:284–293[PubMed]
    [Google Scholar]
  172. Zebedee S. L., Lamb R. A. 1988; Influenza A virus M2 protein: monoclonal antibody restriction of virus growth and detection of M2 in virions. J Virol 62:2762–2772[PubMed]
    [Google Scholar]
  173. Zerial M., McBride H. 2001; Rab proteins as membrane organizers. Nat Rev Mol Cell Biol 2:107–117 [View Article][PubMed]
    [Google Scholar]
  174. Zhang J., Lamb R. A. 1996; Characterization of the membrane association of the influenza virus matrix protein in living cells. Virology 225:255–266 [View Article][PubMed]
    [Google Scholar]
  175. Zhirnov O. P. 1990; Solubilization of matrix protein M1/M from virions occurs at different pH for orthomyxo- and paramyxoviruses. Virology 176:274–279 [View Article][PubMed]
    [Google Scholar]
  176. Zhu L., Li Y., Li S., Li H., Qiu Z., Lee C., Lu H., Lin X., Zhao R. other authors 2011; Inhibition of influenza A virus (H1N1) fusion by benzenesulfonamide derivatives targeting viral hemagglutinin. PLoS ONE 6:e29120 [View Article][PubMed]
    [Google Scholar]
  177. Zhu L., Ly H., Liang Y. 2013a; PLC-γ1 signaling plays a subtype-specific role in post-binding cell entry of influenza A virus. J Virol [Epub ahead of print] [View Article][PubMed]
    [Google Scholar]
  178. Zhu X., Yu W., McBride R., Li Y., Chen L. M., Donis R. O., Tong S., Paulson J. C., Wilson I. A. 2013b; Hemagglutinin homologue from H17N10 bat influenza virus exhibits divergent receptor-binding and pH-dependent fusion activities. Proc Natl Acad Sci U S A 110:1458–1463 [View Article][PubMed]
    [Google Scholar]
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