Functional significance of the hemadsorption activity of influenza virus neuraminidase and its alteration in pandemic viruses

Archives of Virology

Volumn 154, Issue 6, 2009, Pages 945-957

  Uhlendorff, Jennifer ^a   Matrosovich, Tatyana ^a   Klenk, Hans Dieter ^a   Matrosovich, Mikhail ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

SIALIDASE; VIRUS PROTEIN;

AMINO ACID SUBSTITUTION; ANIMAL; ARTICLE; BINDING SITE; CELL LINE; CERCOPITHECUS; DOG; EPIDEMIC; GENETICS; HEMADSORPTION; HUMAN; INFLUENZA; INFLUENZA VIRUS A H1N1; INFLUENZA VIRUS A H2N2; METABOLISM; MISSENSE MUTATION; PATHOGENICITY; SITE DIRECTED MUTAGENESIS; VIROLOGY;

AMINO ACID SUBSTITUTION; ANIMALS; BINDING SITES; CELL LINE; CERCOPITHECUS AETHIOPS; DISEASE OUTBREAKS; DOGS; HEMADSORPTION; HUMANS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA A VIRUS, H2N2 SUBTYPE; INFLUENZA, HUMAN; MUTAGENESIS, SITE-DIRECTED; MUTATION, MISSENSE; NEURAMINIDASE; VIRAL PROTEINS;

AVES; AVIAN INFLUENZA VIRUS; HUMAN INFLUENZA VIRUS; ORTHOMYXOVIRIDAE;

EID: 67349192219     PISSN: 03048608     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00705-009-0393-x     Document Type: Article

References (56)

1. UB Aamir U Wernery N Ilyushina RG Webster 2007 Characterization of avian H9N2 influenza viruses from United Arab Emirates 2000 to 2003 Virology 361 45 55 (Pubitemid 46551216)
2. GM Air WG Laver 1989 The neuraminidase of influenza virus Proteins 6 341 356 (Pubitemid 20036940)
3. GM Air WG Laver 1995 Red cells bound to influenza virus N9 neuraminidase are not released by the N9 neuraminidase activity Virology 211 278 284
4. AT Baker JN Varghese WG Laver GM Air PM Colman 1987 Three-dimensional structure of neuraminidase of subtype N9 from an avian influenza virus Proteins 2 111 117
5. LG Baum JC Paulson 1991 The N2 neuraminidase of human influenza virus has acquired a substrate specificity complementary to the hemagglutinin receptor specificity Virology 180 10 15
6. JA Belser O Blixt LM Chen C Pappas TR Maines N Van Hoeven R Donis J Busch R McBride JC Paulson JM Katz TM Tumpey 2008 Contemporary North American influenza H7 viruses possess human receptor specificity: Implications for virus transmissibility Proc Natl Acad Sci USA 105 58 7563
7. T Bousse T Takimoto 2006 Mutation at residue 523 creates a second receptor binding site on human parainfluenza virus type 1 hemagglutinin- neuraminidase protein J Virol 80 9009 9016 (Pubitemid 44359975)
8. TL Bousse G Taylor S Krishnamurthy A Portner SK Samal T Takimoto 2004 Biological significance of the second receptor binding site of Newcastle disease virus hemagglutinin-neuraminidase protein J Virol 78 13351 13355 (Pubitemid 39507840)
9. NV Bovin 1998 Polyacrylamide-based glycoconjugates as tools in glycobiology Glycoconj J 15 31 446
10. Bucher D, Palese P (1975) The biologically active proteins of influenza virus: neuraminidase. In: Kilbourne E (ed) The influenza viruses and influenza. Academic Press, New York
11. WP Burmeister RW Ruigrok S Cusack 1992 The 2.2 A resolution crystal structure of influenza B neuraminidase and its complex with sialic acid EMBO J 11 49 56
12. E de Wit RA Fouchier 2008 Emerging influenza J Clin Virol 41 1 6 (Pubitemid 350298977)
13. L Glaser J Stevens D Zamarin IA Wilson A Garcia-Sastre TM Tumpey CF Basler JK Taubenberger P Palese 2005 A single amino acid substitution in 1918 influenza virus hemagglutinin changes receptor binding specificity J Virol 79 11533 11536 (Pubitemid 41170697)
14. TE Gray K Guzman CW Davis LH Abdullah P Nettesheim 1996 Mucociliary differentiation of serially passaged normal human tracheobronchial epithelial cells Am J Respir Cell Mol Biol 14 104 112 (Pubitemid 126443096)
15. Y Ha DJ Stevens JJ Skehel DC Wiley 2003 X-ray structure of the hemagglutinin of a potential H3 avian progenitor of the 1968 Hong Kong pandemic influenza virus Virology 309 209 218 (Pubitemid 36579216)
16. J Hausmann E Kretzschmar W Garten HD Klenk 1995 N1 neuraminidase of influenza virus A/FPV/Rostock/34 has haemadsorbing activity J Gen Virol 76 1719 1728
17. E Hoffmann G Neumann Y Kawaoka G Hobom RG Webster 2000 A DNA transfection system for generation of influenza A virus from eight plasmids Proc Natl Acad Sci USA 97 6108 6113 (Pubitemid 30367531)
18. E Hoffmann J Stech Y Guan RG Webster DR Perez 2001 Universal primer set for the full-length amplification of all influenza A viruses Arch Virol 146 2275 2289 (Pubitemid 34682391)
19. D Kobasa S Kodihalli M Luo M Castrucci I Donatelli Y Suzuki T Suzuki Y Kawaoka 1999 Amino acid residues contributing to the substrate specificity of the influenza A virus neuraminidase J Virol 73 6743 6751 (Pubitemid 29327857)
20. D Kobasa ME Rodgers K Wells Y Kawaoka 1997 Neuraminidase hemadsorption activity, conserved in avian influenza A viruses, does not influence viral replication in ducks J Virol 71 6706 6713 (Pubitemid 27355330)
21. D Kobasa K Wells Y Kawaoka 2001 Amino acids responsible for the absolute sialidase activity of the influenza A virus neuraminidase: relationship to growth in the duck intestine J Virol 75 11773 11780 (Pubitemid 33063268)
22. A Kongchanagul O Suptawiwat P Kanrai M Uiprasertkul P Puthavathana P Auewarakul 2008 Positive selection at the receptor-binding site of haemagglutinin H5 in viral sequences derived from human tissues J Gen Virol 89 1805 1810
23. WG Laver PM Colman RG Webster VS Hinshaw GM Air 1984 Influenza virus neuraminidase with hemagglutinin activity Virology 137 314 323 (Pubitemid 14000576)
24. JH Liu K Okazaki A Mweene WM Shi QM Wu JL Su GZ Zhang GR Bai H Kida 2004 Genetic conservation of hemagglutinin gene of H9 influenza virus in chicken population in Mainland China Virus Genes 29 329 334 (Pubitemid 40941266)
25. M Matrosovich T Matrosovich J Uhlendorff W Garten HD Klenk 2007 Avian-virus-like receptor specificity of the hemagglutinin impedes influenza virus replication in cultures of human airway epithelium Virology 361 384 390 (Pubitemid 46574852)
26. M Matrosovich A Tuzikov N Bovin A Gambaryan A Klimov MR Castrucci I Donatelli Y Kawaoka 2000 Early alterations of the receptor-binding properties of H1, H2, and H3 avian influenza virus hemagglutinins after their introduction into mammals J Virol 74 8502 8512 (Pubitemid 30666701)
27. M Matrosovich N Zhou Y Kawaoka R Webster 1999 The surface glycoproteins of H5 influenza viruses isolated from humans, chickens, and wild aquatic birds have distinguishable properties J Virol 73 1146 1155 (Pubitemid 29036766)
28. Matrosovich MN, Klenk HD, Kawaoka Y (2006) Receptor specificity, host range and pathogenicity of influenza viruses. In: Kawaoka Y (ed) Influenza virology: current topics. Caister Academic Press, Wymondham, England, pp 95-137
29. MN Matrosovich S Krauss RG Webster 2001 H9N2 influenza A viruses from poultry in Asia have human virus-like receptor specificity Virology 281 156 162 (Pubitemid 32881133)
30. MN Matrosovich TY Matrosovich T Gray NA Roberts HD Klenk 2004 Neuraminidase is important for the initiation of influenza virus infection in human airway epithelium J Virol 78 12665 12667 (Pubitemid 39458784)
31. I Moustafa H Connaris M Taylor V Zaitsev JC Wilson MJ Kiefel M von Itzstein G Taylor 2004 Sialic acid recognition by Vibrio cholerae neuraminidase J Biol Chem 279 40819 40826 (Pubitemid 39287679)
32. SL Newstead JN Watson AJ Bennet G Taylor 2005 Galactose recognition by the carbohydrate-binding module of a bacterial Sialidase Acta Crystallogr D Biol Crystallogr 61 1483 1491 (Pubitemid 43934584)
33. H Niwa K Yamamura J Miyazaki 1991 Efficient selection for high-expression transfectants with a novel eukaryotic vector Gene 108 193 199
34. JM Nuss GM Air 1991 Transfer of the hemagglutinin activity of influenza virus neuraminidase subtype N9 into an N2 neuraminidase background Virology 183 496 504
35. P Palese K Tobita M Ueda RW Compans 1974 Characterization of temperature sensitive influenza virus mutants defective in neuraminidase Virology 61 397 410
36. JC Paulson GN Rogers 1987 Resialylated erythrocytes for assessment of the specificity of sialyloligosaccharide binding proteins Methods Enzymol 138 162 168 (Pubitemid 17086691)
37. JS Peiris MD de Jong Y Guan 2007 Avian influenza virus (H5N1): a threat to human health Clin Microbiol Rev 20 243 267 (Pubitemid 46709304)
38. EM Rapoport LV Mochalova HJ Gabius J Romanova NV Bovin 2006 Search for additional influenza virus to cell interactions Glycoconj J 23 115 125
39. AH Reid TG Fanning TA Janczewski JK Taubenberger 2000 Characterization of the 1918 "Spanish" influenza virus neuraminidase gene Proc Natl Acad Sci USA 97 6785 6790 (Pubitemid 30412792)
40. AH Reid JK Taubenberger 2003 The origin of the 1918 pandemic influenza virus: a continuing enigma J Gen Virol 84 2285 2292 (Pubitemid 37063116)
41. RJ Russell LF Haire DJ Stevens PJ Collins YP Lin GM Blackburn AJ Hay SJ Gamblin JJ Skehel 2006 The structure of H5N1 avian influenza neuraminidase suggests new opportunities for drug design Nature 443 45 49 (Pubitemid 44344043)
42. JJ Skehel DC Wiley 2000 Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin Ann Rev Biochem 69 531 569 (Pubitemid 30792219)
43. L Skoza S Mohos 1976 Stable thiobarbituric acid chromophore with dimethyl sulphoxide. Application to sialic acid assay in analytical de-O-acetylation Biochem J 159 457 462
44. K Tamura J Dudley M Nei S Kumar 2007 MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0 Mol Biol Evol 24 1596 1599 (Pubitemid 47236692)
45. JK Taubenberger AH Reid RM Lourens R Wang G Jin TG Fanning 2005 Characterization of the 1918 influenza virus polymerase genes Nature 437 889 893 (Pubitemid 41486764)
46. S Thobhani B Ember A Siriwardena GJ Boons 2003 Multivalency and the mode of action of bacterial sialidases J Am Chem Soc 125 7154 7155 (Pubitemid 36798946)
47. TM Tumpey TR Maines N Van Hoeven L Glaser A Solorzano C Pappas NJ Cox DE Swayne P Palese JM Katz A Garcia-Sastre 2007 A two-amino acid change in the hemagglutinin of the 1918 influenza virus abolishes transmission Science 315 655 659 (Pubitemid 46214711)
48. JN Varghese PM Colman A van Donkelaar TJ Blick A Sahasrabudhe JL McKimm-Breschkin 1997 Structural evidence for a second sialic acid binding site in avian influenza virus neuraminidases Proc Natl Acad Sci USA 94 11808 11812 (Pubitemid 27467799)
49. JN Varghese WG Laver PM Colman 1983 Structure of the influenza virus glycoprotein antigen neuraminidase at 2.9 A resolution Nature 303 35 40
50. R Wagner A Herwig N Azzouz HD Klenk 2005 Acylation-mediated membrane anchoring of avian influenza virus hemagglutinin is essential for fusion pore formation and virus infectivity J Virol 79 6449 6458 (Pubitemid 40617248)
51. R Wagner M Matrosovich HD Klenk 2002 Functional balance between haemagglutinin and neuraminidase in influenza virus infections Rev Med Virol 12 159 166 (Pubitemid 34516947)
52. L Warren 1959 The thiobarbituric acid assay of sialic acids J Biol Chem 234 1971 1975
53. RG Webster GM Air DW Metzger PM Colman JN Varghese AT Baker WG Laver 1987 Antigenic structure and variation in an influenza virus N9 neuraminidase J Virol 61 2910 2916 (Pubitemid 17143455)
54. RG Webster WJ Bean OT Gorman TM Chambers Y Kawaoka 1992 Evolution and ecology of influenza A viruses Microbiol Rev 56 152 179
55. S Yamada Y Suzuki T Suzuki MQ Le CA Nidom Y Sakai-Tagawa Y Muramoto M Ito M Kiso T Horimoto K Shinya T Sawada M Kiso T Usui T Murata Y Lin A Hay LF Haire DJ Stevens RJ Russell SJ Gamblin JJ Skehel Y Kawaoka 2006 Haemagglutinin mutations responsible for the binding of H5N1 influenza A viruses to human-type receptors Nature 444 378 382 (Pubitemid 44764114)
56. V Zaitsev M von Itzstein D Groves M Kiefel T Takimoto A Portner G Taylor 2004 Second sialic acid binding site in Newcastle disease virus hemagglutinin-neuraminidase: implications for fusion J Virol 78 3733 3741 (Pubitemid 38568312)