Structure and Diversity of Influenza Virus Neuraminidase

  • P. M. Colman
  • C. W. Ward
Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 114)


Despite all that has been learned about influenza virus in the years since its isolation (SMITH et al. 1933), no method of cure or control has yet been found. Vaccination, so successful against polio and smallpox, is frustrated by antigenic variation of the two surface glycoproteins of the virus, and prospects for chemotherapy are uncertain.


Influenza Virus Sialic Acid Antigenic Drift Stalk Region Influenza Virus Hemagglutinin 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Ada GL, Gottschalk A (1956) The component sugars of the influenza virus particle. Biochem J 62: 686 - 689PubMedGoogle Scholar
  2. Air GM (1979) Nucleotide sequence for the signal peptide and N-terminus of the hemagglutinin from an Asian (H2N2) strain of influenza virus. Virology 97: 468 - 472PubMedGoogle Scholar
  3. Air GM (1981) Sequence relationships among the hemagglutinin genes of 12 subtypes of influenza A virus. Proc Natl Acad Sci USA 78: 7639 - 7643PubMedGoogle Scholar
  4. Allen AK, Skehel JJ, Yuferof VJ (1977) The amino acid and carbohydrate composition of the neuraminidase of B/Lee/40 influenza virus. J Gen Virol 37: 625 - 628Google Scholar
  5. Allen H, McCauley J, Waterfield MD, Gething MJ (1980) Influenza virus RNA segment 7 has the coding capacity for two polypeptides. Virology 107: 548 - 551PubMedGoogle Scholar
  6. Amzel LM, Polzak RJ, Saul F, Vargha JM, Richards FF (1974) The three-dimensional structure of a combining region - ligand complex of immunoglobulin NEW at 3.5 A resolution. Proc Natl Acad Sci USA 71: 1427 - 1430PubMedGoogle Scholar
  7. Anflnsen CB (1973) Principles that govern the folding of protein chains. Science 181: 223 - 230Google Scholar
  8. Ashwell G, Morrell AG (1974) The role of surface carbohydrates in the hepatic recognition and transport circulating glycoproteins, Adv Enzymol 41: 99 - 128PubMedGoogle Scholar
  9. Azad AA, Elleman TC, Laver WG, Ward CW (1983) Sequence changes associated with antigenic shift and drift in influenza virus neuraminidase. In: Laver WG (ed) The origins of pandemic influenza viruses. Elsevier, New York, pp 59 - 76Google Scholar
  10. Bachmeyer H (1972) Effect of tryptophan modification on the activity of bacterial and viral neuraminidase. FEBS Lett 23: 217 - 219Google Scholar
  11. Baker NJ, Gandhi SS (1976) Effect of Ca+ + on the stability of influenza virus neuraminidase. Arch Virol 52: 7 - 18PubMedGoogle Scholar
  12. Basak S, Compans RW (1983) Studies on the role of glycosylation in the function and antigenic properties of influenza virus glycoproteins. Virology 128: 77 - 91PubMedGoogle Scholar
  13. Basak S, Pritchard DG, Bhown AS, Compans RW (1981) Glycosylation sites of influenza viralglycoproteins - characterization of tryptic glycopeptides from the A/USSR (H1N1) hemagglutinin glycoprotein. J Virol 37: 549 - 558PubMedGoogle Scholar
  14. Battula N, Loeb L (1974) The infidelity of avian myeloblastosis virus deoxyribonucleic acid polymerase in polynucleotide replication. J Biol Chem 249: 4086 - 4093PubMedGoogle Scholar
  15. Bentley DR, Brownlee GG (1982) Sequence of the N2 neuraminidase from influenza virus A/NT/60/68. Nucleic Acids Res 10: 5033 - 5042PubMedGoogle Scholar
  16. Bergman LW, Kuehl WM (1978) Temporal relationship of translation and glycosylation of immunoglobulin heavy and light chains. Biochemistry 17: 5174 - 5180PubMedGoogle Scholar
  17. Bishop DHL, Huddleston J A, Brownlee GG (1982) The complete sequence of RNA segment 2 of influenza A/NT/60/68 and its encoded PI protein. Nucleic Acids Res 10: 1335 - 1343PubMedGoogle Scholar
  18. Blok J, Air GM (1980) Comparative nucleotide sequences at the 3’ end of the neuraminidase gene from eleven influenza type A viruses. Virology 107: 50 - 60PubMedGoogle Scholar
  19. Blok J, Air GM (1982 a) Block deletions in the neuraminidase genes from some influenza A viruses of the N1 subtype. Virology 118:229–234Google Scholar
  20. Blok J, Air GM (1982b) Variation in the membrane - insertion and “stalk” sequences in eight subtypes of influenza type A virus neuraminidase. Biochemistry 21: 4001 - 4007PubMedGoogle Scholar
  21. Blok J, Air GM (1982 c) Sequence variation at the 3’ end of the neuraminidase gene from 39 influenza type A viruses. Virology 121:211-229Google Scholar
  22. Blok J, Air GM, Laver WG, Ward CW, Lilley GG, Woods EF, Roxburgh CM, Inglis AS (1982) Studies on the size, chemical composition and partial sequence of the neuraminidase ( NA) from type A influenza virus show that the N-terminal region of the NA is not processed and serves to anchor the NA in the viral membrane. Virology 119: 109–121Google Scholar
  23. Blundell TL (1981) Protein-protein recognition and assembly in structural aspects of recognition and assembly in biological macromolecules. In: Balaban M (ed) International Science Services, Rehovot, pp 281–286Google Scholar
  24. Breidis DJ, Lamb RA (1982) Influenza B virus genome: sequences and structural organization of RNA segment 8 and the mRNAs coding for the NSt and NS2 proteins. J Virol 42: 186 - 193Google Scholar
  25. Breidis DJ, Lamb RA, Choppin PW (1982) Sequence of RNA segment 7 of the influenza B virus genome; partial amino acid homology between the membrane proteins ( Mi) of the influenza A and B viruses and conservation of a second open reading frame. Virology 116: 581-588Google Scholar
  26. Brown LE, Ward CW, Jackson DC (1982) Antigenic determinants of influenza virus hemagglutinin. IX. The carbohydrate side chains from an Asian strain. Mol Immunol 19: 329-338Google Scholar
  27. Bucher DJ, Kilbourne ED (1972) A2 (N2) neuraminidase of the X-7 influenza virus recombinant: determination of molecular size and subunit composition of the active unit. J Virol 10: 60 - 66PubMedGoogle Scholar
  28. Bucher DJ, Palese P (1975) The biologically active proteins of influenza virus neuraminidase. In: Kilbourne ED (ed) Influenza virus and influenza. Academic, New York, pp 83 - 123Google Scholar
  29. Burnet FM (1948) Mucins and mucoids in relation to influenza virus action. IV. Inhibition by purified mucoid of infection and haemagglutinin with the virus strain WSE. Aust J Exp Biol Med Sci 26: 381 - 387PubMedGoogle Scholar
  30. Burnet FM, Stone JD (1947) The receptor-destroying enzyme of V. cholerae. Aust J Exp Biol Med Sci 25: 227 - 233PubMedGoogle Scholar
  31. Burnet FM, McCrea JF, Anderson SG (1947) Mucin as substrate of enzyme action by viruses of the mumps influenza group. Nature 160: 404 - 405PubMedGoogle Scholar
  32. Carroll SM, Paulson JC (1982) Complete metal ion requirement of influenza virus N j neuraminidases. Arch Virol 71: 273 - 277Google Scholar
  33. Caton AJ, Brownlee GG, Yewdell JW, Gerhard W (1982) The antigenic structure of the influenza virus A/PR/8/34 hemagglutinin ( HI subtype ). Cell 31: 417-427Google Scholar
  34. Choppin PW (1969) Replication on influenza virus in a continuous cell line: high yield of infective virus from cells infected at high multiplicity. Virology 38: 130 - 134Google Scholar
  35. Chothia C (1973) Conformation of twisted -pleated sheets in proteins. J Mol Biol 75: 295 - 302PubMedGoogle Scholar
  36. Chothia C, Janin J (1975) Principles of protein-protein recognition. Nature 256: 705 - 708PubMedGoogle Scholar
  37. Chothia C, Janin J (1981) Relative orientation of close-packed -pleated sheets in proteins (twisted -sheets/protein secondary and tertiary structure). Proc Natl Acad Sci USA 78: 4146 - 4150PubMedGoogle Scholar
  38. Chothia C, Levitt M, Richardson D (1977) Structure of proteins: packing of a-helices and pleated sheets. Proc Natl Acad Sci USA 74: 4130 - 4134PubMedGoogle Scholar
  39. Clamp JR (1975) Structure and function of glycoproteins. In: Puttnam FW (ed) The plasma proteins. 2nd ed, vol 2. Academic New York, pp 163 - 211Google Scholar
  40. Clement J-M (1983) On the insertion of proteins into membranes. Biochemistry 65: 325 - 338Google Scholar
  41. Cohen FE, Sternberg MJE, Taylor WR (1981) Analysis of the tertiary structure of protein /?-sheet sandwiches. J Mol Biol 148: 253 - 272PubMedGoogle Scholar
  42. Collins JK, Knight CA (1978) Purification of the influenza hemagglutinin glycoprotein and characterization of its carbohydrate components. J Virol 26: 457 - 467PubMedGoogle Scholar
  43. Colman PM (1984) The structure and function of neuraminidase. Peptide Protein Rev 4: 215 - 255Google Scholar
  44. Colman PM, Laver WG (1981) The structure of influenza virus neuraminidase heads at 5 A resolution. In: Balaban M (ed) Structural aspects of recognition and assembly in biological macromolecules. I.S.S., Rehovot, pp 869 - 872Google Scholar
  45. Colman PM, Jansonius JN, Matthews BW (1972) The structure of thermolysin: an electron density map at 2.3 A resolution. J Mol Biol 70: 701 - 724PubMedGoogle Scholar
  46. Colman PM, Deisenhofer J, Huber R, Palm W (1976) The structure of the human antibody molecule KOL: An electron density map at 5 A resolution. J Mol Biol 100: 257 - 282PubMedGoogle Scholar
  47. Colman PM, Tulloch PA, Laver WG (1980) Preliminary structural studies on two influenza virus neuraminidases. In: Laver WG, Air GM (eds) Structure and variation in influenza virus. Elsevier, New York, pp 351 - 356Google Scholar
  48. Colman PM, Gough KH, Lilley GG, Blagrove RJ, Webster RG, Laver WG (1981) Crystalline monoclonal Fab fragment with specificity towards an influenza virus neuraminidase. J Mol Biol 152: 609 - 614PubMedGoogle Scholar
  49. Colman PM, Varghese JN, Laver WG (1983) Structure of the catalytic and antigenic sites in influenza virus neuraminidase. Nature 303: 41 - 44PubMedGoogle Scholar
  50. Compans RW, Klenk H-D (1979) Viral membranes. Compr Virol 13: 293 - 377Google Scholar
  51. Compans RW, Dimmock NJ, Meier-Ewert H (1969) Effect of antibody to neuraminidase on the maturation and hemagglutinating activity of influenza A2 virus. J Virol 4: 528 - 534PubMedGoogle Scholar
  52. Corfield AP, Wember M, Schauer R, Rott R (1982) The specificity of viral sialidases. The use of oligosaccharide substrates to probe enzyme characteristics and strain specific differences. Eur J Biochem 124: 521-525Google Scholar
  53. Corfield AP, Higa H, Paulson JC, Schauer R (1983) The specificity of viral and bacterial sialidases for a(2-3) and a(2-6) linked sialic acids in glycoproteins. Biochim Biophys Acta 744: 121 - 126PubMedGoogle Scholar
  54. Daniels RS, Douglas AR, Gonsalues-Scarano F, Palu G, Skehel JJ, Brown E, Knossow M, Wilson IA, Wiley DC (1983) Antigenic structure of influenza virus hemagglutinin. In: Laver WG (ed) Origin of pandemic influenza viruses. Elsevier, New York, pp 9 - 18Google Scholar
  55. Deisenhofer J (1981) Crystallographic refinement and atomic models of a human Fc fragment and its complex with fragment B of protein A from Staphylococcus aureus at 2.9 and 2.8 A resolution. Biochemistry 20: 2361 - 2370PubMedGoogle Scholar
  56. Deisenhofer J, Colman PM, Epp O, Huber R (1976) Crystallographic studies of a human Fc fragment. II. A complete model based on a Fourier map at 3.5 A resolution. Hoppe-Seylers Z Physiol Chem 357: 1421 - 1434PubMedGoogle Scholar
  57. Desselberger U, Racaniello VR, Zazra JJ, Palese P (1980) The 3’ and S’-terminal sequences of influenza A, B and C virus RNA segments are highly conserved and show partial inverted complementarity. Gene 8: 315-328Google Scholar
  58. Dopheide TAA, Ward CW (1981) The location of the bromelain-cleavage site in a Hong Kong influenza virus hemagglutinin. J Gen Virol 52: 367 - 370PubMedGoogle Scholar
  59. Drzenick R, Frank H, Rott R (1968) Electron microscopy of purified influenza virus neuraminidase. Virology 36: 703 - 707Google Scholar
  60. Edmond JD, Johnston RG, Kidd D, Rylance HJ, Sommerville RG (1966) Inhibition of neuraminidase and antiviral action. Br J Pharmacol Chemother 27: 415 - 426PubMedGoogle Scholar
  61. Elleman TC, Azad AA, Ward CW (1982) Neuraminidase gene from the early Asian strain of human influenza virus A/RI/5″/57 (H2N2). Nucleic Acids Res 10: 7005 - 7015PubMedGoogle Scholar
  62. Fazekas de St. Groth S (1978) Antigenic, adaptive and adsorptive variants of the influenza A hemagglutinin. In: Laver WG, Bachmayer H, Weil R (eds) The influenza virus hemagglutinin. Springer, Vienna New York, pp 25 - 48Google Scholar
  63. Fields S, Winter G (1981) Nucleotide sequence heterogeneity and sequence rearrangement in influenza virus cDNA. Gene 15: 207 - 214PubMedGoogle Scholar
  64. Fields S, Winter G (1982) Nucleotide sequences of influenza virus segments 1 and 3 reveal mosaic structure of a small viral RNA segment. Cell 28: 303 - 313PubMedGoogle Scholar
  65. Fields S, Winter G, Brownlee GG (1981) Structure of the neuraminidase in human influenza virus A/PR/8/34. Nature 290: 213 - 217PubMedGoogle Scholar
  66. Francis T, Moore AE (1940) A study of the neurotropic tendency in strains of the virus of epidemic influenza. J Exp Med 72: 717 - 728PubMedGoogle Scholar
  67. French S, Robson B (1983) What is a conservation substitution? J Mol Evol 19: 171 - 175Google Scholar
  68. Galloway G, Leung AYT, Hunneyball IM, Stanworth DR (1983) The successful use of asialylated IgG as an immunogen and arthritogen in the rabbit. Immunology 49: 511 - 518PubMedGoogle Scholar
  69. Gamier J, Osguthorpe DJ, Robson B (1978) Analysis of the accuracy and implication of simple methods for predicting the secondary structure of globular proteins. J Mol Biol 120: 97 - 120Google Scholar
  70. Gopinathan KP, Weymouth LA, Kunkel TA, Loeb LA (1979) Mutagenesis in vitro by DNA polymerase from an RNA tumour virus. Nature 278: 857 - 859PubMedGoogle Scholar
  71. Gottschalk A (1957) Neuraminidase: the specific enzyme of influenza virus and vibrio cholerae. Biochim Biophys Acta 23: 645 - 646PubMedGoogle Scholar
  72. Gottschalk A (1958) Neuraminidase: its substrate and mode of action. Adv Enzymol 20: 135 - 145Google Scholar
  73. Gottschalk A (1972) Historical introduction. In: Gottschalk A (ed) Glycoproteins. Their composition, structure and function. Elsevier, Amsterdam, pp 2 - 23Google Scholar
  74. Green N, Alexander H, Olson A, Alexander S, Shinnick TM, Sutcliffe JG, Lerner RA (1982) Immunogenic structure of the influenza virus hemagglutinin. Cell 28: 477 - 487PubMedGoogle Scholar
  75. Gregoriades A (1972) Isolation of neuraminidase from the WSN strain of influenza virus. Virology 49: 333 - 336PubMedGoogle Scholar
  76. Griffin JA, Compans RW (1979) Effect of cytochalasin B on the maturation of enveloped viruses. J Exp Med 150: 379 - 391PubMedGoogle Scholar
  77. Griffin JA, Basak S, Compans RW (1983) Effects of hexose starvation and the role of sialic acid in influenza virus release. Virology 125: 324 - 334PubMedGoogle Scholar
  78. Griffith IP (1975) The fine structure of influenza virus. In: Mahy BWJ, Barry RD (eds) Negative strand viruses, vol 1. Academic, London, pp 121 - 132Google Scholar
  79. Harrison SC, Olson AJ, Schutt CE, Winkler FK, Bricogne G (1978) Tomato bushy stunt virus at 2.9 A resolution. Nature 276: 368 - 373PubMedGoogle Scholar
  80. Haslam EA, Hampson AW, Radiskevics I, White DO (1970) The polypeptides of influenza virus. III. Identification of the hemagglutinin, neuraminidase and nucleocapsid proteins. Virology 42: 566-575Google Scholar
  81. Haugen DA, Armes LG, Yasunobu KT, Coon MJ (1977) Amino-terminal sequence of phenobarbitalinducible cytochrome P-450 from rabbit liver microsomes: similarity to hydrophobic aminoterminal segments of pre-proteins. Biochem Biophys Res Comm 77: 967 - 973PubMedGoogle Scholar
  82. Hirsch RL (1982) The complement system: its importance in the host response to viral infection. Microbiol Rev 46: 71 - 85PubMedGoogle Scholar
  83. Hirsch RL, Winkelstein J A, Griffin DE (1980) The role of complement in viral infections. III. Activation of the classical and alternate pathways by Sindbis virus. J Immunol 124: 2507-2510Google Scholar
  84. Hirsch RL, Griffin DE, Winkelstein J A (1981) Host modification of Sindbis virus sialic acid content influences alternative complement pathway activation and virus clearance. J Immunol 127: 1740 - 1743PubMedGoogle Scholar
  85. Hirst GK (1942) Adsorption of influenza hemagglutinins and virus by red blood cells. J Exp Med 76: 195 - 209PubMedGoogle Scholar
  86. Hiti AL, Nayak DP (1982) Complete nucleotide sequence of the neuraminidase gene of human influenza virus A/WSN/33. J Virol 41: 730 - 734PubMedGoogle Scholar
  87. Hopp TP, Woods KR (1981) Prediction of protein antigenic determinants from amino acid sequences. Proc Natl Acad Sci USA 78: 3824 - 3828PubMedGoogle Scholar
  88. Hoyle L (1952) Structure of the influenza virus. The relation between biological activity and chemical structure of virus fractions. J Hyg (Camb) 50: 229 - 245Google Scholar
  89. Huang RTC, Rott R, Wahn K, Klenk H-D, Kohama T (1980) The function of the neuraminidase in membrane fusion induced by myxoviruses. Virology 107: 313 - 319PubMedGoogle Scholar
  90. Hubbard SC, Ivatt RJ (1981) Synthesis and processing of asparagine-linked oligosaccharides1’2. Annu Rev Biochem 50: 555 - 583PubMedGoogle Scholar
  91. Inglis SC, Barrett T, Brown CM, Almond JW (1979) The smallest genome RNA segment of influenza virus contains two genes that may overlap. Proc Natl Acad Sci USA 76: 3790 - 3794PubMedGoogle Scholar
  92. Jackson DC, Webster RG (1982) A topographic map of the enzyme active center and antigenic sites on the neuraminidase of influenza virus A/Tokyo/3/67 (H2N2). Virology 123: 69 - 77PubMedGoogle Scholar
  93. Jackson DC, Dopheide TAA, Russell RJ, White DO, Ward CW (1979) Antigenic determinants of influenza virus hemagglutinin. II. Antigenic reactivity of the isolated N-terminal cyanogen bromide peptide of A/Memphis/72 hemagglutinin heavy chain. Virology 93: 458 - 465PubMedGoogle Scholar
  94. Jancik JM, Schauer R, Streicher H-J (1975) Influence of membrane-bound N-acetylneuraminic acid on the survival of erythrocytes in man. Z Physiol Chem 356: 1329 - 1331Google Scholar
  95. Jennings PA, Finch JT, Winter G, Robertson JS (1983) Does the higher order structure of the influenza virus ribonucleoprotein guide sequence rearrangements in influenza viral RNA? Cell 34: 619 - 627PubMedGoogle Scholar
  96. Kaptein JS, Nayak DP (1982) Complete nucleotide sequence of the polymerase 3 gene of human influenza virus A/WSN/33. J Virol 42: 55 - 63PubMedGoogle Scholar
  97. Kazatchkine MD, Fearon DT, Austen KF (1979) Human alternative complement pathway: Membrane associated sialic acid regulates the competition between /? and /?1H for cell bound C3b. J Immunol 122: 75 - 81PubMedGoogle Scholar
  98. Keil W, Klenk H-D, Schwarz RT (1979) Carbohydrates of influenza virus. III. Nature of oligosaccharide-protein linkage in viral glycoprotein. J Virol 31: 253-256Google Scholar
  99. Kendal AP, Eckert EA (1972) The preparation and properties of 14C-carboxamido-methylated subunits from A2/1957 influenza neuraminidase. Biochim Biophys Acta 258: 484 - 495PubMedGoogle Scholar
  100. Kendal AP, Kiley MP (1975) Structural comparisons of influenza A neuraminidase. In: Mahy BWJ, Barry RD (eds) Negative strand viruses, vol 1. Academic Press, London, pp 145 - 159Google Scholar
  101. Kendal AP, Madeley CR (1970) Flocculation of influenza virus by specific anti-neuraminidase antibody. Arch Gesamte Virusforsch 31: 219 - 229PubMedGoogle Scholar
  102. Klenk E, Faillard H, Lempfrid H (195) Uber die enzymatische Wirkung von Influenza virus. Z Physiol Chem 301:235–246Google Scholar
  103. Klenk H-D, Rott R (1980) Cotranslational and posttranslational processing of viral glycoproteins. Curr Top Microbiol Immunol 90: 19 - 48PubMedGoogle Scholar
  104. Klenk H-D, Scholtissek C, Rott R (1972) Inhibition of glycoprotein biosynthesis of influenza virus by D-glucosamine and 2-deoxy-D-glucose. Virology 49: 723 - 734PubMedGoogle Scholar
  105. Klenk H-D, Rott, R, Orlich M, Blodorn J (1975) Activation of influenza A viruses by trypsin treatment. Virology 68: 426 - 439PubMedGoogle Scholar
  106. Kolb-Bachofen V, Kolb H (1979) Autoimmune reactions against liver cells by syngeneic neuraminidase- treated lymphocytes. J Immunol 123: 2830 - 2834PubMedGoogle Scholar
  107. Kozak M (1981) Mechanism of mRNA recognition by eubaryotic ribosomes during initiation of protein synthesis. Curr Top Microbiol Immunol 93: 81 - 123PubMedGoogle Scholar
  108. Kreisel W, Volk BA, Buechsel R, Reutter W (1980) Different half-lives of the carbohydrate and protein moieties of a 110000-dalton glycoprotein isolated from the plasma membranes of rat liver. Proc Natl Acad Sci USA 77: 1828 - 1831PubMedGoogle Scholar
  109. Lai C-J, Markoff LJ, Sveda M, Dhar R, Chanock RM (1980) DNA sequences derived from genomic and mRNA species that code for the haemagglutinin and the neuraminidase of influenza A virus. In: Laver G, Air GM (eds) Structure and variation in influenza virus. Elsevier, New York, pp 115 - 124Google Scholar
  110. Lamb RA, Choppin PW (1979) Segment 8 of the influenza virus genome is unique in coding for 2 polypeptides. Proc Natl Acad Sci USA 76: 4908 - 4912PubMedGoogle Scholar
  111. Lamb RA, Choppin PW (1981) Identification of a second protein (M2) encoded by RNA segment 7 of influenza virus. Virology 112: 729 - 737PubMedGoogle Scholar
  112. Lamb RA, Lai CJ (1980) Sequence of interrupted and uninterrupted mRNAs and cloned DNA coding for the two overlapping nonstructural proteins of influenza virus. Cell 21: 475 - 485PubMedGoogle Scholar
  113. Lamb RA, Lai CJ (1981) Conservation of the influenza virus membrane protein (Mt) amino acid sequence and an open reading frame of RNA segment 7 encoding a second protein (M2) in H1H1 and H3N2 strains. Virology 112: 746 - 751PubMedGoogle Scholar
  114. Lamb RA, Shaw MW, Breidis DJ, Choppin PW (1983) The nucleotide sequence of the neuraminidase gene of influenza B virus reveals two overlapping reading frames. In: Laver WG (ed) The origin of pandemic influenza viruses. Elsevier, New York, pp 77 - 86Google Scholar
  115. Lambre CR, Kazatchkine MD, Maillet F, Thibon M (1982) Guinea pig erythrocytes after their contact with influenza virus acquire the ability to activate the alternative complement pathway through virus induced desialation of the cells. J Immunol 128: 629 - 634PubMedGoogle Scholar
  116. Lambre CR, Thibon M, Le Maho S, Di Bella G (1983) Auto antibody dependent activation of the autologous classical complement pathway in guinea pig red cells treated with influenza virus or neuraminidase: in vitro and in vivo study. Virology 49: 311 - 319Google Scholar
  117. Laver WG (1963) The structure of influenza viruses. 3. Disruption of the virus particle and separation of neuraminidase activity. Virology 20: 251 - 262Google Scholar
  118. Laver WG (1973) The polypeptides of influenza viruses. Adv Virus Res 18: 57 - 103Google Scholar
  119. Laver WG (1978) Crystallization and peptide maps of neuraminidase “heads” from H2N2 and H3N2 influenza virus strains. Virology 86: 78 - 87PubMedGoogle Scholar
  120. Laver WG, Baker N (1972) Amino acid composition of polypeptides from influenza virus particles. J Gen Virol 17: 61 - 68PubMedGoogle Scholar
  121. Laver WG, Kilbourne ED (1966) Identification in a recombinant influenza virus of structural proteins derived from both parents. Virology 30: 493 - 501PubMedGoogle Scholar
  122. Laver WG, Valentine RC (1969) Morphology of the isolated hemagglutinin and neuraminidase subunits of influenza virus. Virology 38: 105 - 119PubMedGoogle Scholar
  123. Laver WG, Webster RG (1973) Studies on the origin of pandemic influenza. III. Evidence implicating duck and equine influenza viruses as possible progenitors of the Hong Kong strain of human influenza. Virology 51: 383-391Google Scholar
  124. Laver WG, Air GM, Webster RG, Gerhard W, Ward CW, Dopheide TAA (1979) Antigenic drift in type A influenza virus: sequence differences in the hemagglutinin of Hong Kong (H3N2) variants selected with monoclonal hybridoma antibodies. Virology 98: 226 - 237PubMedGoogle Scholar
  125. Laver WG, Air GM, Webster RG, Markoff LJ (1982) Amino acid sequence changes in antigenic variants of type A influenza virus N2 neuraminidase. Virology 122: 450 - 460PubMedGoogle Scholar
  126. Laver WG, Colman PM, Webster RG, Hinshaw VS, Air GM (1984) Influenza virus neuraminidase with haemagglutinin activity. VirologyGoogle Scholar
  127. Lazarowitz SG, Choppin PW (1975) Enhancement of infectivity of influenza A and B viruses by proteolytic cleavage of the hemagglutinin polypeptide. Virology 68: 440 - 454PubMedGoogle Scholar
  128. Lazarowitz SG, Compans RW, Choppin PW (1971) Influenza virus structural and nonstructural proteins in infected cells and their plasma membranes. Virology 46: 830 - 843PubMedGoogle Scholar
  129. Lazdins I, Haslam EA, White DO (1972) The polypeptides of influenza virus. VI. Composition of the neuraminidase. Virology 49: 758-765Google Scholar
  130. Lentz MR, Air GM, Laver WG, Webster RG (1984) Sequence of the neuraminidase gene from influenza virus A/Tokyo/3/67 and previously uncharacterised monoclonal variants. Virology 135: 257 - 265PubMedGoogle Scholar
  131. Levitt M, Chothia C (1976) Structural patterns in globular proteins. Nature 261: 552 - 558PubMedGoogle Scholar
  132. Maillet F, Kazatehkine MD (1983) Modulation of the formation of the human amplification C3 convertase of complement by polycations. Immunology 50: 27 - 33PubMedGoogle Scholar
  133. Mariuzza RA, Jankovic DL, Boulot G, Amit AG, Saludjian P, Le Guern A, Mazie JC, Poljak RJ (1983) Preliminary crystallographic study of the complex between the Fab fragment of a monoclonal antilysozyme antibody and its antigen. J Mol Biol 170: 1055 - 1088PubMedGoogle Scholar
  134. Markoff L, Lai CJ (1982) Sequence of the influenza A/Udora/72 (H3N2) virus neuraminidase gene as determined from cloned full-length DNA. Virology 119: 288 - 297PubMedGoogle Scholar
  135. Marquart M, Deisenhofer J (1982) The three-dimensional structure of antibodies. Immunol Today 3: 160 - 166Google Scholar
  136. Marquart M, Deisenhofer J, Huber R, Palm W (1980) Crystallographic refinement and atomic models of the intact immunoglobulin molecule Kol and its antigen binding fragment at 3.0 and 2.9 A resolution. J Mol Biol 141: 369 - 392PubMedGoogle Scholar
  137. Marshall RD (1972) Glycoproteins. Annu Rev Biochem 41: 673 - 702Google Scholar
  138. Martinez C, Del Rio L, Portelo A, Domingo E, Ortin J (1983) Evolution of the influenza virus neuraminidase gene during drift of the N2 subtype. Virology 130: 539 - 545PubMedGoogle Scholar
  139. Matlin K, Reggio H, Helenius A, Simons KJ (1981) Infectious entry pathway of influenza virus in a canine kidney cell line. J Cell Biol 91: 601 - 631PubMedGoogle Scholar
  140. Matsushima M, Marquart M, Jones TA, Colman PM, Bartels K, Huber R (1978) Crystal structure of the human Fab fragment Kol and its comparison with the intact Kol molecule. J Mol Biol 121: 441 - 459PubMedGoogle Scholar
  141. McCauley JW, Bye J, Elder K, Gething MJ, Skehel JJ, Smith A, Waterfield MD (1979) Influenza virus hemagglutinin signal sequence. FEBS Lett 108: 422 - 428PubMedGoogle Scholar
  142. McCauley JW, Mahy BWJ, Inglis SC (1982) Nucleotide sequence of fowl plague virus RNA segment 7. J Gen Virol 58: 211 - 215PubMedGoogle Scholar
  143. McSharry JJ, Pickering RJ, Caliguiri LA (1981) Activation of the alternate complement pathway by enveloped viruses containing limited amounts of sialic acid. Virology 114:507-515 Michel H (1983) Crystallisation of membrane proteins. Trends in Biomedical Sciences 8: 56 - 59Google Scholar
  144. Mountford CE, Grossman G, Holmes KT, O’Sullivan WJ, Hampson AW, Raison RL, Webster RG (1982) Effect of monoclonal antineuraminidase antibodies on the kinetic behaviour of influenza virus neuraminidase. Mol Immunol 19: 811 - 816PubMedGoogle Scholar
  145. Nakajima K, Desselberger U, Palese P (1978) Recent human influenza A (H1N1) viruses are closely related genetically to strains isolated in 1950. Nature 274: 334 - 339PubMedGoogle Scholar
  146. Nakajima S, Sugiura A (1980) Neuroviralence of influenza in mice. II. Mechanism of virulence as studied in a neuroblastoma cell line. Virology 101: 450-457Google Scholar
  147. Nakamura K, Compans RW (1978) Glycopeptide components of influenza viral glycoproteins. Virology 86: 432 - 442PubMedGoogle Scholar
  148. Noll H, Aoyagi T, Orlando J (1962) The structural relationship of sialidase to the influenza virus surface. Virology 18: 154 - 157PubMedGoogle Scholar
  149. Palese P (1977) The genes of influenza virus. Cell 10: 1 - 10PubMedGoogle Scholar
  150. Palese P, Compans RW (1976) Inhibition of influenza virus replication in tissue culture by 2-deoxy-2,3-dehydro-N-trifluoro-acetyl-neuraminic acid (FANA): mechanism of action. J Gen Virol 33: 159 - 163PubMedGoogle Scholar
  151. Palese P, Tobita K, Ueda M, Compans RW (1974) Characterization of temperature sensitive influenza virus mutants defective in neuraminidase. Virology 61: 397 - 410PubMedGoogle Scholar
  152. Paulson JC, Weinstein J, Dorland L, Van Halbeek H, Vliegenthart JFG (1982) Newcastle disease virus contains a linkage-specific glycoprotein sialidase. J Biol Chem 257: 12734 - 12738PubMedGoogle Scholar
  153. Poljak RJ, Amzel LM, Avey HP, Chen BL, Phizackerly RP, Saul F (1973) Three dimensional structure of the Fab1 fragment of a human immunoglobulin at 2.8 A resolution. Proc Natl Acad Sci USA 70: 3305 - 3310PubMedGoogle Scholar
  154. Porter AG, Barber C, Carey NH, Hallewell RA, Threlfall G, Emtage JS (1979) Complete nucleotide sequence of an influenza virus hemagglutinin gene from cloned DNA. Nature 282: 471 - 477PubMedGoogle Scholar
  155. Richardson JS (1977) /?-sheet topology and the relatedness of proteins. Nature 268:495-500Google Scholar
  156. Richardson JS (1981) The anatomy and taxonomy of protein structure. Adv Prot Chem 34: 167 - 339Google Scholar
  157. Richardson JS, Getzoff ED, Richardson DC (1978) The /?-bulge: A common small unit of nonrepetitive protein structure. Proc Natl Acad Sci USA 75: 2574-2578Google Scholar
  158. Robertson JS (1979) 5’ and 3’ terminal nucleotide sequences of the RNA genome segments of influenza virus. Nucleic Acids Res 6:3745-3757Google Scholar
  159. Rogers GN, Paulson JC (1983) Receptor determinants of human and animal influenza virus isolates: difference in receptor specificity of the H3 haemagglutinin based on species of origin. Virology 127: 361 - 373PubMedGoogle Scholar
  160. Rogers GN, Paulson JC, Daniels RS, Skehel JJ, Wilson I A, Wiley DC (1983) Single amino acid substitutions in influenza hemagglutinin change receptor binding specificity. Nature 304: 76 - 78PubMedGoogle Scholar
  161. Rosenberg A, Schengrund C-L (1976) Sialidases. In: Rosenburg A, Schengrund C-L (eds) The biological roles of sialic acid Plenum, New York, pp 295 - 359Google Scholar
  162. Rothman JE, Lodish HF (1977) Synchronised transmembrane insertion and glycosylation of a nascent membrane protein. Nature 269: 775 - 780PubMedGoogle Scholar
  163. Rott R, Becht H, Klenk H-D, Scholtissek C (1972) Interactions of concanavalin A with the membrane of influenza virus infected cells and with envelope components of the virus particle. Z Naturforsch 27b: 227 - 233Google Scholar
  164. Saber MS, Drzenick R, Kriipe M (1965) Freilegung von ABH-Blutgruppen determinierenden Kohlenhydraten an Erythrozyten durch Neuraminidase-Einwirkung. Z Naturforsch 206: 965 - 973Google Scholar
  165. Schauer R (1982) Sialic acids. Adv Carbohydr Chem Biochem 40: 131 - 234Google Scholar
  166. Schmidt WE, Jung H-D, Palm W, Hilschman N (1983) The primary structure of the crystallisable monoclonal immunoglobulin IgGl, KOL. Hoppe Seylers Z Physiol Chemie 364: 713-747Google Scholar
  167. Scholtissek C (1978) The genome of the influenza virus. Curr Top Microbiol Immunol 80: 139 - 169PubMedGoogle Scholar
  168. Scholtissek C, Rohde W, von Hoyningen V, Rott R (1978 a) On the origin of the human influenza virus subtypes H2N2 and H3N2. Virology 87:13–20Google Scholar
  169. Scholtissek C, von Hoyningen V, Rott R (1978 b) Genetic relatedness between the new 1977 epidemic strains (H1N1) of influenza and human influenza and human influenza strains isolated between 1947 and 1957 (H1N1). Virology 89:613–617Google Scholar
  170. Schulman JL (1975) Immunology of influenza. In: Kilbourne ED (ed) The influenza viruses and influenza. Academic, New York, pp 373 - 393Google Scholar
  171. Schulman JL, Palese P (1977) Virulence factors of influenza A viruses: WSN virus neuraminidase required for plaque production in MDBK cells. J Virol 24: 170-176Google Scholar
  172. Schwarz RT, Klenk H-D (1981) Carbohydrates of influenza virus. IV. Strain dependent variations. Virology 113: 584-593Google Scholar
  173. Schwarz RT, Schmidt MFG, Anwer U, Klenk H-D (1977) Carbohydrates of influenza virus. I. Glycopeptides derived from viral glycoproteins after labelling with radioactive sugars. J Virol 23: 217-226Google Scholar
  174. Segal DM, Paplan EA, Cohen GH, Rudikoff S, Potter M, Davies DR (1974) The three-dimensional structure of a phosphorylcholine-binding mouse immunoglobulin Fab and the nature of the antigen binding site. Proc Natl Acad Sci USA 71: 4298 - 4302PubMedGoogle Scholar
  175. Seto JT, Rott R (1966) Functional significance of sialidase during influenza virus multiplication. Virology 30: 731 - 737PubMedGoogle Scholar
  176. Seto JT, Drzeniek R, Rott R (1966) Isolation of a low molecular weight neuraminidase from influenza virus. Biochim Biophys Acta 113: 402 - 404Google Scholar
  177. Shaw MW, Lamb RA, Erickson BW, Breidis DJ, Choppin PW (1982) Complete nucleotide sequence of the neuraminidase gene of influenza B virus. Proc Natl Acad Sci USA 79: 6817 - 6821PubMedGoogle Scholar
  178. Skehel JJ (1972) Polypeptide synthesis in influenza virus-infected cells. Virology 49: 23 - 36PubMedGoogle Scholar
  179. Skehel JJ, Schild GC (1971) The polypeptide composition of influenza A viruses. Virology 44: 396 - 408PubMedGoogle Scholar
  180. Skehel JJ, Waterfield MD (1975) Studies on the primary structure of the influenza virus hemagglutinin. Proc Natl Acad Sci USA 72: 93 - 97PubMedGoogle Scholar
  181. Smith W, Andrewes CH, Laidlaw PP (1933) A virus obtained from influenza patients. Lancet 2: 66 - 68Google Scholar
  182. Stanley PM, Crook NE, Streader LG, Davidson BE (1973) The polypeptides of influenza virus. VIII. Large-scale purification of hemagglutinin. Virology 56: 640-645Google Scholar
  183. Struck DK, Lennarz WJ (1980) The function of saccharide lipids in synthesis of glycoproteins. In: Lennarz W (ed) The biochemistry of glycoproteins and proteoglycans. Plenum, New York, pp 35 - 83Google Scholar
  184. Sugiuna A, Ueda M (1980) Neurovirulence of influenza in mice. I. Neurovirulence of recombinants between virulent and avirulent viral strains. Virology 101: 440-449Google Scholar
  185. Tettamanti G, Cestaro B, Venerendo B, Preti A (1978) Neuraminidase gangliosides interactions. In: Gatt S, Freysz L, Mandel P (eds) Enzymes of lipid metabolism. Plenum, New York, pp 417 - 437Google Scholar
  186. Ulmanen I, Broni BA, Krug RM (1981) Role of two of the influenza virus core P proteins in recognizing cap 1 structure (m7 Gppp Nm) on RNAs. Proc Natl Acad Sci USA 78: 7355 - 7359PubMedGoogle Scholar
  187. Van Rompuy, Min-Ion W, Huylebroeck D, Fiers W (1982) Complete nucleotide sequence of a human influenza neuraminidase gene of subtype N2 (A/Vic/3/75). J Mol Biol 161: 1 - 11PubMedGoogle Scholar
  188. Varghese JN, Laver WG, Colman PM (1983) Structure of the influenza virus glycoprotein antigen neuraminidase at 2.9 A resolution. Nature 303: 35 - 40PubMedGoogle Scholar
  189. Wagh PV, Bahl OP (1981) Sugar residues on proteins. Crit Rev Biochem 10: 307 - 377Google Scholar
  190. Ward CW (1981) Structure of the influenza virus hemagglutinin. Curr Top Microbiol Immunol 94 /95: 1 - 74PubMedGoogle Scholar
  191. Ward CW, Dopheide TAA (1976) Size and chemical composition of influenza virus hemagglutinin chains. FEBS Lett 65: 365 - 368PubMedGoogle Scholar
  192. Ward CW, Dopheide TAA (1981a) Amino acid sequence and oligosaccharide distribution of the hemagglutinin from an early Hong Kong variant A/Aichi/2/68(x-31). Biochem J 193: 953 - 962PubMedGoogle Scholar
  193. Ward CW, Dopheide TAA (1981b) Evolution of the Hong Kong influenza A sub-type. Structural relationships between the hemagglutinins from A/duck/Ukraine/1/63 (Hav7) and the Hong Kong ( H3) hemagglutinins. Biochem J 195: 337-340Google Scholar
  194. Ward CW, Gleeson PA, Dopheide TAA (1980) Carbohydrate composition of the oligosaccharide units on the hemagglutinin from the Hong Kong influenza variant A/Memphis/102/72. Biochem J 189: 649 - 652PubMedGoogle Scholar
  195. Ward CW, Elleman TC, Azad AA (1982) Amino acid sequence of the pronase-released heads of neuraminidase subtype N2 from the Asian strain A/Tokyo/3/67 of influenza virus. Biochem J 207: 91 - 95PubMedGoogle Scholar
  196. Ward CW, Colman PM, Laver WG (1983 a) The disulphide bonds of an Asian influenza virus neuraminidase. FEBS Lett 153:29–33Google Scholar
  197. Ward CW, Murray JM, Roxburgh CM, Jackson DC ( 1983 b) Chemical and antigenic characterization of the carbohydrate side chains of an Asian ( N2) influenza virus neuraminidase. Virology 126: 370-375Google Scholar
  198. Waterfield MD, Espelie K, Elder K, Skehel JJ (1979) Structure of the hemagglutinin of influenza virus. Br Med Bull 35: 57 - 63PubMedGoogle Scholar
  199. Waterfield MD, Gething MJ, Scrace G, Skehel J J (1980) The carbohydrate side chains and disulphide bonds of the hemagglutinin of the influenza virus A/Japan/305/57(H2Nl). In: Laver G, Air G (eds) Structure and variation in influenza virus. ElsevierNorth Holland, New York, pp 11 - 20Google Scholar
  200. Weber E, Papamokos E, Bode W, Huber R, Kato I, Laskowski M (1981) Crystallization, crystal structure analysis and molecular model of the third domain of Japanese quail ovomucoid, a kazal type inhibitor. J Mol Biol 149: 109 - 123PubMedGoogle Scholar
  201. Webster RG (1970) Estimation of the molecular weights of the polypeptide chains from the isolated hemagglutinin and neuraminidase subunits of influenza viruses. Virology 40: 543 - 554Google Scholar
  202. Webster RG, Darlington RW (1969) Disruption of myxoviruses with Tween 20 and isolation of biologically active hemagglutinin and neuraminidase subunits. J Virol 4: 182 - 187PubMedGoogle Scholar
  203. Webster RG, Hinshaw VS, Laver WG (1982) Selection and analysis of antigenic variants of the neuraminidase of N2 influenza viruses with monoclonal antibodies. Virology 117: 93 - 104PubMedGoogle Scholar
  204. Webster RG, Brown LE, Laver WG (1984) Antigenic and biological characterisation of influenza virus neuraminidase ( N2) with monoclonal antibodies. Virology 135: 30-42Google Scholar
  205. Wedgwood RJ, Ginsberg HS, Pillemer L (1956) The properdin system and immunity. VI. The inactivation of Newcastle disease virus by the properdin system. J Exp Med 104: 707-725Google Scholar
  206. Weiler JM, Yurt RM, Fearon DT, Austen KF (1978) Modulation of the formation of the amplification convertase of complement, C3b, Bb, by native and commercial heparin. J Exp Med 147: 409-421Google Scholar
  207. White DO (1974) Influenza viral proteins: identification and synthesis. Curr Top Microbiol Immunol 63: 1 – 48Google Scholar
  208. White J, Helenius A (1980) pH-dependent fusion between the Semliki forest virus membrane and liposomes. Proc Natl Acad Sci USA 77:3273–3277Google Scholar
  209. White J, Helenius A, Gething M-J (1982 a) Haemagglutinin of influenza virus expressed from a cloned gene promotes membrane fusion. Nature 300:658–659Google Scholar
  210. White J, Kartenbeck J, Helenius A (1982 b) Membrane fusion activity of influenza virus. EMBO J 1:217–222Google Scholar
  211. Wiley DC, Wilso JA, Skehel JJ (1981) Structural identification of the antibody binding sites of the Hong Kong influenza haemagglutinin and their involvement in antigenic variation. Nature 298: 373 - 378Google Scholar
  212. Wilson I A, Skehel J J, Wiley DC (1981) Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 A resolution. Nature 289: 366 - 373PubMedGoogle Scholar
  213. Winter G, Fields S (1980) Cloning of influenza cDNA into Ml3: the sequence of the RNA segment encoding the A/PR/8/34 matrix protein. Nucleic Acids Res 8: 1965 - 1974PubMedGoogle Scholar
  214. Winter G, Fields S (1982) Nucleotide sequence of human influenza A/PR/8/34 segment 2. Nucleic Acids Res 10: 2135 - 2143PubMedGoogle Scholar
  215. Winter G, Fields S, Gait MJ (1981) The use of synthetic oligodeoxynucleotide primers in cloning and sequencing segment 8 of influenza virus (A/PR/8/34). Nucleic Acids Res 9: 237 - 245PubMedGoogle Scholar
  216. Woodruff J J, Gesner BM (1969) The effect of neuraminidase on the fate of transfused lymphocytes. J Exp Med 129: 551 - 567PubMedGoogle Scholar
  217. Wright CE, Laver WG (1978) Preliminary crystallographic data for influenza virus neuraminidase “heads”. J Mol Biol 120: 133 - 136PubMedGoogle Scholar
  218. Wrigley NG (1979) Electron microscopy of influenza virus. Br Med Bull 35: 35 - 38PubMedGoogle Scholar
  219. Wrigley NG, Laver WG, Downie JC (1977) Binding of antibodies to isolated hemagglutinin and neuraminidase molecules of influenza virus observed in the electron microscope. J Mol Biol 109: 405 - 421PubMedGoogle Scholar
  220. Wrigley NG, Skehel JJ, Charlwood PA, Brand CM (1973) The size and shape of influenza virus neuraminidase. Virology 51: 525 - 529PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin · Heidelberg 1985

Authors and Affiliations

  • P. M. Colman
    • 1
  • C. W. Ward
    • 1
  1. 1.Division of Protein ChemistryCSIROParkvilleAustralia

Personalised recommendations