1887

Abstract

Mutants of the haemagglutinin (HA) gene of human influenza virus A/Aichi/2/68 (H3N2) encoding HA proteins that are proteolytically cleaved intracellularly, defective in binding to cellular receptors or defective for acylation within the cytoplasmic C terminus have been generated. Here, the properties of these mutated HA molecules are described and their incorporation into the lipid membrane of released human immunodeficiency virus (HIV)-like particles is analysed. It is demonstrated that, when produced from cells coexpressing any of the binding-competent Aichi-HA molecules, release of HIV-like particles into the extracellular medium is reduced and the particles that are released fail to incorporate Aichi-HA. These blocks in release and incorporation, respectively, can both be overcome. The release of normal amounts of particles with incorporated HA can be achieved either by mutation of the receptor-binding site on the Aichi-HA molecule or by removal of sialic acid from surface proteins with neuraminidase. In contrast, as a result of blockage of the sialic acid-binding site by sialidated oligosaccharides on the HA itself, the HA of influenza virus A/FPV/Rostock/34 (H7N1) is efficiently incorporated into HIV-like particles. These results, namely that particle release can be inhibited by interactions between the incorporated glycoprotein and the cell surface and/or that interactions with other cellular components can be inhibitory to incorporation into retrovirus envelopes, probably reflect general principles that may hold for many viral and cellular glycoproteins.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-82-10-2485
2001-10-01
2019-08-23
Loading full text...

Full text loading...

/deliver/fulltext/jgv/82/10/0822485a.html?itemId=/content/journal/jgv/10.1099/0022-1317-82-10-2485&mimeType=html&fmt=ahah

References

  1. Arthur, L. O., Bess, J. W.Jr, Sowder, R. C.II, Benveniste, R. E., Mann, D. L., Chermann, J. C. & Henderson, L. E. ( 1992; ). Cellular proteins bound to immunodeficiency viruses: implications for pathogenesis and vaccines. Science 258, 1935-1938.[CrossRef]
    [Google Scholar]
  2. Bastiani, L., Laal, S., Kim, M. & Zolla-Pazner, S. ( 1997; ). Host cell-dependent alterations in envelope components of human immunodeficiency virus type 1 virions. Journal of Virology 71, 3444-3450.
    [Google Scholar]
  3. Blasco, R. & Moss, B. ( 1995; ). Selection of recombinant vaccinia viruses on the basis of plaque formation. Gene 158, 157-162.[CrossRef]
    [Google Scholar]
  4. 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.[CrossRef]
    [Google Scholar]
  5. Daniels, R. S., Douglas, A. R., Skehel, J. J. & Wiley, D. C. ( 1983; ). Analyses of the antigenicity of influenza haemagglutinin at the pH optimum for virus-mediated membrane fusion. Journal of General Virology 64, 1657-1662.[CrossRef]
    [Google Scholar]
  6. Dong, J., Roth, M. G. & Hunter, E. ( 1992; ). A chimeric avian retrovirus containing the influenza virus hemagglutinin gene has an expanded host range. Journal of Virology 66, 7374-7382.
    [Google Scholar]
  7. Ellens, H., Bentz, J., Mason, D., Zhang, F. & White, J. M. ( 1990; ). Fusion of influenza hemagglutinin-expressing fibroblasts with glycophorin-bearing liposomes: role of hemagglutinin surface density. Biochemistry 29, 9697-9707.[CrossRef]
    [Google Scholar]
  8. Geijtenbeek, T. B., Kwon, D. S., Torensma, R., van Vliet, S. J., van Duijnhoven, G. C., Middel, J., Cornelissen, I. L., Nottet, H. S., KewalRamani, V. N., Littman, D. R., Figdor, C. G. & van Kooyk, Y. ( 2000; ). DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. Cell 100, 587-597.[CrossRef]
    [Google Scholar]
  9. Hammarstedt, M., Wallengren, K., Pedersen, K. W., Roos, N. & Garoff, H. ( 2000; ). Minimal exclusion of plasma membrane proteins during retroviral envelope formation. Proceedings of the National Academy of Sciences, USA 97, 7527-7532.[CrossRef]
    [Google Scholar]
  10. Hatziioannou, T., Valsesia-Wittmann, S., Russell, S. J. & Cosset, F. L. ( 1998; ). Incorporation of fowl plague virus hemagglutinin into murine leukemia virus particles and analysis of the infectivity of the pseudotyped retroviruses. Journal of Virology 72, 5313-5317.
    [Google Scholar]
  11. Henriksson, P. & Bosch, V. ( 1998; ). Inhibition of cellular glycoprotein incorporation into human immunodeficiency virus-like particles by coexpression of additional cellular interaction partner. Virology 251, 16-21.[CrossRef]
    [Google Scholar]
  12. Henriksson, P., Pfeiffer, T., Zentgraf, H., Alke, A. & Bosch, V. ( 1999; ). Incorporation of wild-type and C-terminally truncated human epidermal growth factor receptor into human immunodeficiency virus-like particles: insight into the processes governing glycoprotein incorporation into retroviral particles. Journal of Virology 73, 9294-9302.
    [Google Scholar]
  13. Ho, S. N., Hunt, H. D., Horton, R. M., Pullen, J. K. & Pease, L. R. ( 1989; ). Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77, 51-59.[CrossRef]
    [Google Scholar]
  14. Horton, R. M., Hunt, H. D., Ho, S. N., Pullen, J. K. & Pease, L. R. ( 1989; ). Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension. Gene 77, 61-68.[CrossRef]
    [Google Scholar]
  15. Lama, J., Mangasarian, A. & Trono, D. ( 1999; ). Cell-surface expression of CD4 reduces HIV-1 infectivity by blocking Env incorporation in a Nef-and Vpu-inhibitable manner. Current Biology 9, 622-631.[CrossRef]
    [Google Scholar]
  16. Lin, Y. P., Wharton, S. A., Martin, J., Skehel, J. J., Wiley, D. C. & Steinhauer, D. A. ( 1997; ). Adaptation of egg-grown and transfectant influenza viruses for growth in mammalian cells: selection of hemagglutinin mutants with elevated pH of membrane fusion. Virology 233, 402-410.[CrossRef]
    [Google Scholar]
  17. Liu, C., Eichelberger, M. C., Compans, R. W. & Air, G. M. ( 1995; ). Influenza type A virus neuraminidase does not play a role in viral entry, replication, assembly, or budding. Journal of Virology 69, 1099-1106.
    [Google Scholar]
  18. Martin, J., Wharton, S. A., Lin, Y. P., Takemoto, D. K., Skehel, J. J., Wiley, D. C. & Steinhauer, D. A. ( 1998; ). Studies of the binding properties of influenza hemagglutinin receptor-site mutants. Virology 241, 101-111.[CrossRef]
    [Google Scholar]
  19. Melkonian, K. A., Ostermeyer, A. G., Chen, J. Z., Roth, M. G. & Brown, D. A. ( 1999; ). Role of lipid modifications in targeting proteins to detergent-resistant membrane rafts. Many raft proteins are acylated, while few are prenylated. Journal of Biological Chemistry 274, 3910-3917.[CrossRef]
    [Google Scholar]
  20. Nguyen, D. H. & Hildreth, J. E. ( 2000; ). Evidence for budding of human immunodeficiency virus type 1 selectively from glycolipid-enriched membrane lipid rafts. Journal of Virology 74, 3264-3272.[CrossRef]
    [Google Scholar]
  21. Ohuchi, R., Ohuchi, M., Garten, W. & Klenk, H.-D. ( 1991; ). Human influenza virus hemagglutinin with high sensitivity to proteolytic activation. Journal of Virology 65, 3530-3537.
    [Google Scholar]
  22. Ohuchi, M., Feldmann, A., Ohuchi, R. & Klenk, H.-D. ( 1995; ). Neuraminidase is essential for fowl plague virus hemagglutinin to show hemagglutinating activity. Virology 212, 77-83.[CrossRef]
    [Google Scholar]
  23. Ohuchi, M., Ohuchi, R., Feldmann, A. & Klenk, H.-D. ( 1997; ). Regulation of receptor binding affinity of influenza virus hemagglutinin by its carbohydrate moiety. Journal of Virology 71, 8377-8384.
    [Google Scholar]
  24. Pear, W. S., Nolan, G. P., Scott, M. L. & Baltimore, D. ( 1993; ). Production of high-titer helper-free retroviruses by transient transfection. Proceedings of the National Academy of Sciences, USA 90, 8392-8396.[CrossRef]
    [Google Scholar]
  25. Pfeiffer, T., Zentgraf, H., Freyaldenhoven, B. & Bosch, V. ( 1997; ). Transfer of endoplasmic reticulum and Golgi retention signals to human immunodeficiency virus type 1 gp160 inhibits intracellular transport and proteolytic processing of viral glycoprotein but does not influence the cellular site of virus particle budding. Journal of General Virology 78, 1745-1753.
    [Google Scholar]
  26. Rittner, K., Stöppler, H., Pawlita, M. & Sczakiel, G. ( 1991; ). Versatile eucaryotic vectors for strong and constitutive transient and stable gene expression. Methods in Molecular and Cellular Biology 2, 176-181.
    [Google Scholar]
  27. Scheiffele, P., Roth, M. G. & Simons, K. ( 1997; ). Interaction of influenza virus haemagglutinin with sphingolipid-cholesterol membrane domains via its transmembrane domain. EMBO Journal 16, 5501-5508.[CrossRef]
    [Google Scholar]
  28. Schnell, M. J., Johnson, J. E., Buonocore, L. & Rose, J. K. ( 1997; ). Construction of a novel virus that targets HIV-1-infected cells and controls HIV-1 infection. Cell 90, 849-857.[CrossRef]
    [Google Scholar]
  29. Schoen, P., Leserman, L. & Wilschut, J. ( 1996; ). Fusion of reconstituted influenza virus envelopes with liposomes mediated by streptavidin/biotin interactions. FEBS Letters 390, 315-318.[CrossRef]
    [Google Scholar]
  30. Steinhauer, D. A., Wharton, S. A., Wiley, D. C. & Skehel, J. J. ( 1991; ). Deacylation of the hemagglutinin of influenza A/Aichi/2/68 has no effect on membrane fusion properties. Virology 184, 445-448.[CrossRef]
    [Google Scholar]
  31. Vey, M., Schafer, W., Berghofer, S., Klenk, H.-D. & Garten, W. ( 1994; ). Maturation of the trans-Golgi network protease furin: compartmentalization of propeptide removal, substrate cleavage, and COOH-terminal truncation. Journal of Cell Biology 127, 1829-1842.[CrossRef]
    [Google Scholar]
  32. Wharton, S. A., Skehel, J. J. & Wiley, D. C. ( 1986; ). Studies of influenza haemagglutinin-mediated membrane fusion. Virology 149, 27-35.[CrossRef]
    [Google Scholar]
  33. Wilson, I. A., Skehel, J. J. & Wiley, D. C. ( 1981; ). Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3Å resolution. Nature 289, 366-373.[CrossRef]
    [Google Scholar]
  34. Young, J. A., Bates, P., Willert, K. & Varmus, H. E. ( 1990; ). Efficient incorporation of human CD4 protein into avian leukosis virus particles. Science 250, 1421-1423.[CrossRef]
    [Google Scholar]
  35. Zhang, J., Pekosz, A. & Lamb, R. A. ( 2000; ). Influenza virus assembly and lipid raft microdomains: a role for the cytoplasmic tails of the spike glycoproteins. Journal of Virology 74, 4634-4644.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-82-10-2485
Loading
/content/journal/jgv/10.1099/0022-1317-82-10-2485
Loading

Data & Media loading...

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error