Interdependence of hemagglutinin glycosylation and neuraminidase as regulators of influenza virus growth: A study by reverse genetics

Journal of Virology

Volumn 74, Issue 14, 2000, Pages 6316-6323

  Wagner, Ralf ^a   Wolff, Thorsten ^a,c   Herwig, Astrid ^a   Pleschka, Stephan ^b   Klenk, Hans Dieter ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b JUSTUS LIEBIG UNIVERSITY   (Germany)

^c ROBERT KOCH INSTITUTE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DNA DIRECTED RNA POLYMERASE; HEMAGGLUTININ; OLIGOSACCHARIDE; SIALIDASE; VIRUS VECTOR;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; ENZYME ACTIVITY; GLYCOSYLATION; INFLUENZA VIRUS; NONHUMAN; PRIORITY JOURNAL; RECEPTOR BINDING; SIMIAN VIRUS 40; VIRAL GENETICS; VIROGENESIS; VIRUS INFECTION; VIRUS RECOMBINANT;

ANIMALS; CATTLE; CELL LINE; CHICKENS; ERYTHROCYTES; GLYCOSYLATION; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; INFLUENZA A VIRUS; MUTAGENESIS, SITE-DIRECTED; NEURAMINIDASE; PLAQUE ASSAY; RECEPTORS, VIRUS; RECOMBINATION, GENETIC;

EID: 0033934134     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.74.14.6316-6323.2000     Document Type: Article

References (40)

1. Aytay, S., and I. T. Schulze. 1991. Single amino acid substitutions in the hemagglutinin can alter the host range and receptor binding properties of H1 strains of influenza A virus. J. Virol. 65:3022-3028.
2. Castrucci, M. R., and Y. Kawaoka. 1993. Biologic importance of neuraminidase stalk length in influenza A virus. J. Virol. 67:759-764.
3. Colman, P. 1998. Structure and function of the neuraminidase, p. 65-73. In K. G. Nicholson, R. G. Webster, and A. J. Hay (ed.). Textbook of influenza. Blackwell Science, London, England.
4. Compans, R. W., N. J. Dimmock, and H. Meier-Ewert. 1969. Effect of antibody to neuraminidase on the maturation and hemagglutinating activity of an influenza A2 virus. J. Virol. 4:528-534.
5. Connor, R. J., Y. Kawaoka, R. G. Webster, and J. C. Paulson. 1994. Receptor specificity in human, avian, and equine H2 and H3 influenza virus isolates. Virology 205:17-23.
6. Deom, C. M., A. J. Caton, and I. T. Schulze. 1986. Host cell-mediated selection of a mutant influenza A virus that has lost a complex oligosaccharide from the tip of the hemagglutinin. Proc. Natl. Acad. Sci. USA 83:3771-3775.
7. Eisen, M. B., S. Sabesan, J. J. Skehel, and D. C. Wiley. 1997. Binding of the influenza A virus to cell-surface receptors: structures of five hemagglutininsialyloligosaccharide complexes determined by X-ray crystallography. Virology 232:19-31.
8. Els, M. C., G. M. Air, K. G. Murti, R. G. Webster, and W. G. Laver. 1985. An 18-amino acid deletion in an influenza neuraminidase. Virology 142:241-247.
9. Enami, M., and P. Palese. 1991. High-efficiency formation of influenza virus transfectants. J. Virol. 65:2711-2713.
10. Gambaryan, A. S., V. P. Marinina, A. B. Tuzikov, N. V. Bovin, I. A. Rudneva, B. V. Sinitsyn, A. A. Shilov, and M. N. Matrosovich. 1998. Effects of host-dependent glycosylation of hemagglutinin on receptor-binding properties on HINI human influenza A virus grown in MDCK cells and in embryonated eggs. Virology 247:170-177.
11. Griffin, J. A., S. Basak, and R. W. Compans. 1983. Effects of hexose starvation and the role of sialic acid in influenza virus release. Virology 125:324-334.
12. Gubareva, L. V., R. Bethell, G. J. Hart, K. G. Murti, C. R. Penn, and R. G. Webster. 1996. Characterization of mutants of influenza A virus selected with the neuraminidase inhibitor 4-guanidino-Neu5Ac2en. J. Virol. 70:1818-1827.
13. Günther, I., B. Glatthaar, G. Doller, and W. Garten. 1993. A H1 hemagglutinin of a human influenza A virus with a carbohydrate-modulated receptor binding site and an unusual cleavage site. Virus Res. 27:147-160.
14. Hausmann, J., E. Kretzschmar, W. Garten, and H. D. Klenk. 1997. Biosynthesis, intracellular transport and enzymatic activity of an avian influenza A virus neuraminidase: role of unpaired cysteines and individual oligosaccharides. J. Gen. Virol. 78:3233-3245.
15. Kaverin, N. V., A. S. Gambaryan, N. V. Bovin, I. A. Rudneva, A. A. Shilov, O. M. Khodova, N. L. Varich, B. V. Sinitsin, N. V. Makarova, and E. A. Kropotkina. 1998. Postreassortment changes in influenza A virus hemagglutinin restoring HA-NA functional match. Virology 244:315-321.
16. Kaverin, N. V., and H. D. Klenk. 1999. Strain-specific differences in the effect of influenza A virus neuraminidase on vector-expressed hemagglutinin. Arch. Virol. 144:781-786.
17. 1H n.m.r. and methylation analysis. EMBO J. 4:2711-2720.
18. Kilbourne, E. D. 1987. Influenza. Plenum Press, New York, N.Y.
19. Lamb, R. A., and R. M. Krug. 1996. Orthomyxoviridae: the viruses and their replication, p. 1353-1395. In B. N. Fields, D. M. Knipe, and P. M. Howley (ed.), Fields virology. Lippincott-Raven Publishers, Philadelphia, Pa.
20. Liu, C., M. C. Eichelberger, R. W. Compans, and G. M. Air. 1995. Influenza type A virus neuraminidase does not play a role in viral entry, replication, assembly, or budding. J. Virol. 69:1099-1106.
21. Luo, G., J. Chung, and P. Palese. 1993. Alterations of the stalk of the influenza virus neuraminidase: deletions and insertions. Virus Res. 29:141-153.
22. Matrosovich, M., N. Zhou, Y. Kawaoka, and 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.
23. Matrosovich, M. N., A. S. Gambaryan, S. Teneberg, V. E. Piskarev, S. S. Yamnikova, D. K. Lvov, J. S. Robertson, and K. A. Karlsson. 1997. Avian influenza A viruses differ from human viruses by recognition of sialyloligosaccharides and gangliosides and by a higher conservation of the HA receptor-binding site. Virology 233:224-234.
24. Mitnaul, L. J., M. R. Castrucci, K. G. Murti, and Y. Kawaoka. 1996. The cytoplasmic tail of influenza A virus neuraminidase (NA) affects NA incorporation into virions, virion morphology, and virulence in mice but is not essential for virus replication. J. Virol. 70:873-879.
25. Neumann, G., A. Zobel, and G. Hobom. 1994. RNA polymerase I-mediated expression of influenza viral RNA molecules. Virology 202:477-471.
26. Ohuchi, M., R. Ohuchi, A. Feldmann, and H. D. Klenk. 1997. Regulation of receptor binding affinity of influenza virus hemagglutinin by its carbohydrate moiety. J. Virol. 71:8377-8384.
27. Palese, P., and R. W. Compans. 1976. Inhibition of influenza virus replication in tissue culture by 2-deoxy-2,3-dehydro-N-trifluoroacetylneuraminic acid (FANA): mechanism of action. J. Gen. Virol. 33:159-163.
28. Palese, P., K. Tobita, M. Ueda, and R. W. Compans. 1974. Characterization of temperature sensitive influenza virus mutants defective in neuraminidase. Virology 61:397-410.
29. Perdue, M. L., J. W. Latimer, and J. M. Crawford. 1995. A novel carbohydrate addition site on the hemagglutinin protein of a highly pathogenic H7 subtype avian influenza virus. Virology 213:276-281.
30. Pleschka, S., R. Jaskunas, O. G. Engelhardt, T. Zurcher, P. Palese, and A. Garcia-Sastre. 1996. A plasmid-based reverse genetics system for influenza A virus. J. Virol. 70:4188-4192.
31. Rogers, G. N., J. C. Paulson, R. S. Daniels, J. J. Skehel, I. A. Wilson, and D. C. Wiley. 1983. Single amino acid substitutions in influenza haemagglutinin change receptor binding specificity. Nature 304:76-78.
32. Rudneva, I. A., E. I. Sklyanskaya, O. S. Barulina, S. S. Yamnikova, V. P. Kovaleva, I. V. Tsvetkova, and N. V. Kaverin. 1996. Phenotypic expression of HA-NA combinations in human-avian influenza A virus reassortants. Arch. Virol. 141:1091-1099.
33. Schulman, J. L., and P. Palese. 1977. Virulence factors of influenza A viruses: WSN virus neuraminidase required for plaque production in MDBK cells. J. Virol. 24:170-176.
34. Stieneke-Gröber, A., M. Vey, H. Angliker, E. Shaw, G. Thomas, C. Roberts, H. D. Klenk, and W. Garten. 1992. Influenza virus hemagglutinin with multibasic cleavage site is activated by furin, a subtilisin-like endoprotease. EMBO J. 11:2407-2414.
35. Vines, A., K. Wells, M. Matrosovich, M. R. Castrucci, T. Ito, and Y. Kawaoka. 1998. The role of influenza A virus hemagglutinin residues 226 and 228 in receptor specificity and host range restriction. J. Virol. 72:7626-7631.
36. Warner, T. G., and J. S. O'Brien. 1979. Synthesis of 2′-(4-methylumhelliferyl)-alpha-D-N-acetylneuraminic acid and detection of skin fibroblast neuraminidase in normal humans and in sialidosis. Biochemistry 18:2783-2787.
37. Weis, W., J. H. Brown, S. Cusack, J. C. Paulson, J. J. Skehel, and D. C. Wiley. 1988. Structure of the influenza virus haemagglutinin complexed with its receptor, sialic acid. Nature 333:426-431.
38. Wiley, D. C., and J. J. Skehel. 1987. The structure and function of the hemagglutinin membrane glycoprotein of influenza virus. Annu. Rev. Biochem. 56:365-394.
39. Wilson, I. A., J. J. Skehel, and D. C. Wiley. 1981. Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 A resolution. Nature 289:366-373.
40. Zobel, A., G. Neumann, and G. Hobom. 1993. RNA polymerase I catalysed transcription of insert viral cDNA. Nucleic Acids Res. 21:3607-3614.