Biosynthesis, intracellular transport and enzymatic activity of an avian influenza A virus neuraminidase: Role of unpaired cysteines and individual oligosaccharides

Journal of General Virology

Volumn 78, Issue 12, 1997, Pages 3233-3245

  Hausmann, J ^a,b   Kretzschmar, E ^a,c   Garten, W ^a   Klenk, H D ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

^c Duisburg mbH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE; DISULFIDE; OLIGOSACCHARIDE; VIRUS SIALIDASE;

ARTICLE; CELL MEMBRANE; ENZYME ACTIVITY; ENZYME GLYCOSYLATION; FOWL PLAGUE VIRUS; GOLGI COMPLEX; INFLUENZA VIRUS A; INTRACELLULAR TRANSPORT; PRIORITY JOURNAL;

AVES; FOWL PLAGUE VIRUS; GALLIFORMES; INFLUENZA A VIRUS; INFLUENZA VIRUS; INFLUENZAVIRUS A; VACCINIA; VACCINIA VIRUS; VERTEBRATA;

EID: 0030813216     PISSN: 00221317     EISSN: None     Source Type: Journal    
DOI: 10.1099/0022-1317-78-12-3233     Document Type: Article

References (45)

1. Allen, A. K., Skehel, J. J. & Yuferov, V. (1977). The amino acid and carbohydrate composition of the neuraminidase of B/Lee/40 influenza virus. Journal of General Virology 37, 625-628.
2. Alvarez, E., Girones, N. & Davis, R. J. (1989). Intermolecular disulfide bonds are not required for the expression of the dimeric state and functional activity of the transferrin receptor. EMBO Journal 8, 31-40.
3. Aymard-Henry, M., Coleman, M. T., Dowdle, W. R., Laver, W. G., Schild, G. C. & Webster, R. G. (1973). Influenza virus neuraminidase and neuraminidase inhibition test procedures. Bulletin of the World Health Organization 48, 199-202.
4. Becker, S., Huppertz, S., Klenk, H.-D. & Feldmann, H. (1994). The nucleoprotein of Marburg virus is phosphorylated. Journal of General Virology 75, 809-818.
5. Bilsel, P., Castrucci, M. & Kawaoka, Y. (1993). Mutations in the cytoplasmic tail of influenza A virus neuraminidase affect incorporation into virions. Journal of Virology 67, 6762-6767.
6. Blok, J. & Air, G. M. (1982). Variation in the membrane-insertion and 'stalk' sequences in eight subtypes of influenza type A virus neuraminidase. Biochemistry 21, 4001-4007.
7. Blumberg, B. M., Giorgi, C., Roux, L., Raju, R., Dowling, P., Chollet, A. & Kolakofsky, D. (1985). Sequence determination of the Sendai virus HN gene and its comparison to the influenza glycoproteins. Cell 41, 269-278.
8. Bos, T. J., Davis, A. R. & Nayak, D. P. (1984). NH2-terminal hydrophobic region of influenza virus neuraminidase provides the signal function in translocation. Proceedings of the National Academy of Sciences, USA 81, 2327-2331.
9. Bucher, D. J. & Palese, P. (1975). The biologically active proteins of influenza virus. Neuraminidase. In Influenza Virus and Influenza, pp. 83-123. Edited by E. D. Kilbourne. New York: Academic Press.
10. Burnet, F. M. (1948). Mucins and mucoids in relation to influenza virus action. IV. Inhibition by purified mucoid of infection and haemagglutination with the virus strain WSE. Australian Journal of Experimental Biology and Medical Science 26, 387-391.
11. Castrucci, M. R. & Kawaoka, Y. (1993). Biologic importance of neuraminidase stalk length in influenza A virus. Journal of Virology 67, 759-764.
12. Chakrabarti, S., Brechling, K. & Moss, B. (1985). Vaccinia virus expression vector: coexpression of beta-galactosidase provides visual screening of recombinant virus plaques. Molecular and Cellular Biology 5, 3403-3409.
13. Colman, P. M., Varghese, J. N. & Laver, W. G. (1983). Structure of the catalytic and antigenic sites in influenza virus neuraminidase. Nature 303, 41-44.
14. Doms, R. W., Lamb, R. A., Rose, J. K. & Helenius, A. (1993). Folding and assembly of viral membrane proteins. Virology 193, 545-562.
15. Earl, P. L., Moss, B. & Doms, R. W. (1991). Folding, interaction with GRP78-BiP, assembly, and transport of the human immunodeficiency virus type 1 envelope protein. Journal of Virology 65, 2047-2055.
16. Enami, M. & Enami, K. (1996). Influenza virus hemagglutinin and neuraminidase glycoproteins stimulate the membrane association of the matrix protein. Journal of Virology 70, 6653-6657.
17. Garcia-Sastre, A. & Palese, P. (1995). The cytoplasmic tail of the neuraminidase protein of influenza A virus does not play an important role in the packaging of this protein into viral envelopes. Virus Research 37, 37-47.
18. Hausmann, J., Kretzschmar, E., Garten, W. & Klenk, H.-D. (1995). N1 neuraminidase of influenza virus A/FPV/Rostock/34 has haemadsorbing activity. Journal of General Virology 76, 1719-1728.
19. Hogue, B. G. & Nayak, D. P. (1992). Synthesis and processing of the influenza virus neuraminidase, a type II transmembrane glycoprotein. Virology 188, 510-517.
20. 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.
21. Jin, H., Leser, G. P., Zhang, I. & Lamb, R. A. (1997). Influenza virus hemagglutinin and neuraminidase cytoplasmic tails control particle shape. EMBO Journal 16, 1236-1247.
22. Klenk, H.-D., Rott, R. & Becht, H. (1972). On the structure of the influenza virus envelope. Virology 47, 579-591.
23. Kundu, A., Jabbar, M. A. & Nayak, D. P. (1991). Cell surface transport, oligomerization, and endocytosis of chimeric type II glycoproteins: role of cytoplasmic and anchor domains. Molecular and Cellular Biology 11, 2675-2685.
24. Laver, W. G. (1978). Crystallization and peptide maps of neuraminidase 'heads' from H2N2 and H3N2 influenza virus strains. Virology 86, 78-87.
25. Laver, W. G., Colman, P. M., Webster, R. G., Hinshaw, V. S. & Air, G. M. (1984). Influenza virus neuraminidase with hemagglutinin activity. Virology 137, 314-323.
26. Lentz, M. R., Air, G. M. & Webster, R. G. (1987). Site-directed mutation of the active site of influenza neuraminidase and implications for the catalytic mechanism. Biochemistry 26, 5351-5358.
27. Li, S., Schulman, J. L., Itamura, S. & Palese, P. (1993). Glycosylation of neuraminidase determines the neurovirulence of influenza A/WSN/33 virus. Journal of Virology 67, 6667-6673.
28. Liu, C. & Air, G. M. (1993). Selection and characterisation of a neuraminidase-minus mutant of influenza virus and its rescue by cloned neuraminidase genes. Virology 194, 403-407.
29. Luo, G., Chung, J. & Palese, P. (1993). Alterations of the stalk of the influenza virus neuraminidase: deletions and insertions. Virus Research 29, 141-153.
30. McGinnes, L. W. & Morrison, T. G. (1994). The role of the individual cysteine residues in the formation of the mature, antigenic HN protein of Newcastle disease virus. Virology 200, 470-483.
31. Mackett, M., Smith, G. L. & Moss, B. (1984). General method for production and selection of infectious vaccinia virus recombinants expressing foreign genes. Journal of Virology 49, 857-864.
32. Mitnaul, L. J., Castrucci, M. R., Murti, K. G. & Kawaoka, Y. (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. Journal of Virology 70, 873-879.
33. Ng, D. T. W., Randall, R.E. & Lamb, R. A. (1989). Intracellular maturation and transport of the SV5 type II glycoprotein hemagglutinin-neuraminidase: specific and transient association with GRP78-BiP in the endoplasmic reticulum and extensive internalization from the cell surface. Journal of Cell Biology 109, 3273-3289.
34. Ohuchi, M., Feldmann, A., Ohuchi, R. & Klenk, H.-D. (1995). Neuraminidase is essential for fowl plague hemagglutinin to show hemagglutinating activity. Virology 212, 77-83.
35. Palese, P., Tobita, K., Ueda, M. & Compans, R. W. (1974). Characterisation of temperature-sensitive influenza virus mutants defective in neuraminidase. Virology 61, 397-410.
36. Roberts, C., Garten, W. & Klenk, H.-D. (1993). The role of conserved glycosylation in the maturation and transport of the influenza hemagglutinin. Journal of Virology 67, 3048-3060.
37. Roux, L. (1990). Selective and transient association of Sendai virus HN glycoprotein with BiP. Virology 175, 161-166.
38. Saito, T., Taylor, G. & Webster, R. G. (1995). Steps in maturation of influenza A virus neuraminidase. Journal of Virology 69, 5011-5017.
39. Sanger, F., Nicklen, S. & Coulson, A. R. (1977). DNA sequencing with chain-terminating inhibitors. Proceedings of the National Academy of Sciences, USA 74, 5463-5467.
40. Sivasubramanian, N. & Nayak, D. B. (1987). Mutational analysis of the signal-anchor domain of influenza virus neuraminidase. Proceedings of the National Academy of Sciences, USA 84, 1-5.
41. Sommer, M. & Courtney, R. J. (1991). Differential rates of processing and transport of herpes simplex virus type 1 glycoproteins gB and gC. Journal of Virology 65, 520-525.
42. Taylor, G., Garman, E., Webster, R., Saito, T. & Laver, G. (1993). Crystallization and preliminary X-ray studies of influenza A virus neuraminidase of subtypes N5, N6, N8 and N9. Journal of Molecular Biology 230, 345-348.
43. Taylor, J. W., Ott, J. & Eckstein, F. (1985). The rapid generation of oligonucleotide-directed mutations at high frequency using phosphorothiorate modified DNA. Nucleic Acids Research 13, 8765-8785.
44. Varghese, J. N., Laver, W. G. & Colman, P. M. (1983). Structure of the influenza virus glycoprotein antigen neuraminidase at 2·9 Å resolution. Nature 393, 35-40.
45. Ward, C. W., Murray, J. M., Roxburgh, C. M. & Jackson, D. C. (1983). Chemical and antigenic characterisation of the carbohydrate side chains of an Asian (N2) influenza virus neurammidase. Virology 126, 370-373.