1887

Abstract

Rabies virus glycoprotein (G) is a trimeric type I transmembrane glycoprotein that mediates both receptor recognition and low pH-induced membrane fusion. We have previously demonstrated that a soluble form of the ectodomain of G (G), although secreted, is folded in an alternative conformation, which is monomeric and antigenically distinct from the native state of the complete, membrane-anchored glycoprotein. This has raised questions concerning the role of the transmembrane domain (TMD) in the correct native folding of the ectodomain. Here, we show that an ectodomain anchored in the membrane by a glycophosphatidylinositol is also folded in an alternative conformation, whereas replacement of the TMD of G by other peptide TMDs results in correct antigenicity of G. However, mutants with an insertion of a hydrophilic linker between the ectodomain and the TMD also fold in an alternative conformation. The influence of the membrane-anchor type on G ectodomain trimerization and folding is discussed.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-83-6-1465
2002-06-01
2020-01-27
Loading full text...

Full text loading...

/deliver/fulltext/jgv/83/6/0831465a.html?itemId=/content/journal/jgv/10.1099/0022-1317-83-6-1465&mimeType=html&fmt=ahah

References

  1. Anilionis, A., Wunner, W. H. & Curtis, P. J. ( 1981; ). Structure of the glycoprotein gene in rabies virus. Nature 294, 275-278.[CrossRef]
    [Google Scholar]
  2. Benmansour, A., Leblois, H., Coulon, P., Tuffereau, C., Gaudin, Y., Flamand, A. & Lafay, F. ( 1991; ). Antigenicity of rabies virus glycoprotein. Journal of Virology 65, 4198-4203.
    [Google Scholar]
  3. Bogdanov, M. & Dowhan, W. ( 1998; ). Phospholipid-assisted protein folding: phosphatidylethanolamine is required at a late step of the conformational maturation of the polytopic membrane protein lactose permease. EMBO Journal 17, 5255-5264.[CrossRef]
    [Google Scholar]
  4. Bogdanov, M. & Dowhan, W. ( 1999; ). Lipid-assisted protein folding. Journal of Biological Chemistry 274, 36827-36830.[CrossRef]
    [Google Scholar]
  5. Cocquerel, L., Meunier, J. C., Pillez, A., Wychowski, C. & Dubuisson, J. ( 1998; ). A retention signal necessary and sufficient for endoplasmic reticulum localization maps to the transmembrane domain of hepatitis C virus glycoprotein E2. Journal of Virology 72, 2183-2191.
    [Google Scholar]
  6. Cox, J. H., Dietzschold, B. & Schneider, L. G. ( 1977; ). Rabies virus glycoprotein. II. Biological and serological characterization. Infection and Immunity 16, 754-759.
    [Google Scholar]
  7. Crise, B., Ruusala, A., Zagouras, P., Shaw, A. & Rose, J. K. ( 1989; ). Oligomerization of glycolipid-anchored and soluble forms of the vesicular stomatitis virus glycoprotein. Journal of Virology 63, 5328-5333.
    [Google Scholar]
  8. Dietzschold, B., Gore, M., Marchadier, D., Niu, H. S., Bunschoten, H. M., Otvos, L.Jr, Wunner, W. H., Ertl, H. C. J., Osterhaus, A. D. & Koprowski, H. ( 1990; ). Structural and immunological characterization of a linear neutralizing epitope of the rabies virus glycoprotein and its possible use in a synthetic vaccine. Journal of Virology 64, 3804-3809.
    [Google Scholar]
  9. Doms, R. W., Lamb, R. A., Rose, J. K. & Helenius, A. ( 1993; ). Folding and assembly of viral membrane proteins. Virology 193, 545-562.[CrossRef]
    [Google Scholar]
  10. Ellgaard, L., Molinari, M. & Helenius, A. ( 1999; ). Setting the standards: quality control in the secretory pathway. Science 286, 1882-1888.[CrossRef]
    [Google Scholar]
  11. Fuerst, T. R., Niles, E. G., Studier, F. W. & Moss, B. ( 1986; ). Eukaryotic transient expression system based on recombinant vaccinia virus that synthesizes bacteriophage T7 RNA polymerase. Proceedings of the National Academy of Sciences, USA 83, 8122-8126.[CrossRef]
    [Google Scholar]
  12. Gaudin, Y. ( 1997; ). Folding of rabies virus glycoprotein: epitope acquisition and interaction with endoplasmic reticulum chaperones. Journal of Virology 71, 3742-3750.
    [Google Scholar]
  13. Gaudin, Y., Ruigrok, R. W. H., Tuffereau, C., Knossow, M. & Flamand, A. ( 1992; ). Rabies virus glycoprotein is a trimer. Virology 187, 627-632.[CrossRef]
    [Google Scholar]
  14. Gaudin, Y., Ruigrok, R. W. H., Knossow, M. & Flamand, A. ( 1993; ). Low-pH conformational changes of rabies virus glycoprotein and their role in membrane fusion. Journal of Virology 67, 1365-1372.
    [Google Scholar]
  15. Gaudin, Y., Moreira, S., Bénéjean, J., Blondel, D., Flamand, A. & Tuffereau, C. ( 1999; ). Soluble ectodomain of rabies virus glycoprotein expressed in eukaryotic cells folds in a monomeric conformation that is antigenically distinct from the native state of the complete membrane-anchored glycoprotein. Journal of General Virology 80, 1647-1656.
    [Google Scholar]
  16. Gething, M. J., McCammon, K. & Sambrook, J. ( 1986; ). Expression of wild-type and mutant forms of influenza hemagglutinin: the role of folding in intracellular transport. Cell 46, 939-950.[CrossRef]
    [Google Scholar]
  17. Godet, M., Rasschaert, D. & Laude, H. ( 1991; ). Processing and antigenicity of entire and anchor-free spike glycoprotein S of coronavirus TGEV expressed by recombinant baculovirus. Virology 185, 732-740.[CrossRef]
    [Google Scholar]
  18. Hampl, H., Ben-Porat, T., Ehrlicher, L., Habermehl, K. O. & Kaplan, A. S. ( 1984; ). Characterization of the envelope proteins of pseudorabies virus. Journal of Virology 52, 583-590.
    [Google Scholar]
  19. Kemble, G. W., Henis, Y. I. & White, J. M. ( 1993; ). GPI- and transmembrane-anchored influenza hemagglutinin differ in structure and receptor binding activity. Journal of Cell Biology 122, 1253-1265.[CrossRef]
    [Google Scholar]
  20. Kornfeld, R. & Kornfeld, S. ( 1985; ). Assembly of asparagine-linked oligosaccharides. Annual Review of Biochemistry 54, 631-664.[CrossRef]
    [Google Scholar]
  21. Lafay, F., Benmansour, A., Chebli, K. & Flamand, A. ( 1996; ). Immunodominant epitopes defined by a yeast-expressed library of random fragments of the rabies virus glycoprotein map outside major antigenic sites. Journal of General Virology 77, 339-346.[CrossRef]
    [Google Scholar]
  22. Lafon, M., Wiktor, T. J. & Macfarlan, R. I. ( 1983; ). Antigenic sites of the CVS rabies virus glycoprotein: analysis with monoclonal antibodies. Journal of General Virology 64, 843-851.[CrossRef]
    [Google Scholar]
  23. Lazarovits, J., Shia, S. P., Ktistakis, N., Lee, M. S., Bird, C. & Roth, M. G. ( 1990; ). The effects of foreign transmembrane domains on the biosynthesis of the influenza virus hemagglutinin. Journal of Biological Chemistry 265, 4760-4767.
    [Google Scholar]
  24. Odell, D., Wanas, E., Yan, J. & Ghosh, H. P. ( 1997; ). Influence of membrane anchoring and cytoplasmic domains on the fusogenic activity of vesicular stomatitis virus glycoprotein G. Journal of Virology 71, 7996-8000.
    [Google Scholar]
  25. Paterson, R. G. & Lamb, R. A. ( 1990; ). Conversion of a class II integral membrane protein into a soluble and efficiently secreted protein: multiple intracellular and extracellular oligomeric and conformational forms. Journal of Cell Biology 110, 999-1011.[CrossRef]
    [Google Scholar]
  26. Préhaud, C., Coulon, P., Lafay, F., Thiers, C. & Flamand, A. ( 1988; ). Antigenic site II of the rabies virus glycoprotein: structure and role in viral virulence. Journal of Virology 62, 1-7.
    [Google Scholar]
  27. Robison, C. S. & Whitt, M. A. ( 2000; ). The membrane-proximal stem region of vesicular stomatitis virus G protein confers efficient virus assembly. Journal of Virology 74, 2239-2246.[CrossRef]
    [Google Scholar]
  28. Rose, J. K., Buonocore, L. & Whitt, M. A. ( 1991; ). A new cationic liposome reagent mediating nearly quantitative transfection of animal cells. Biotechniques 10, 520-525.
    [Google Scholar]
  29. Roth, M. G., Doyle, C., Sambrook, J. & Gething, M. J. ( 1986; ). Heterologous transmembrane and cytoplasmic domains direct functional chimeric influenza virus hemagglutinins into the endocytic pathway. Journal of Cell Biology 102, 1271-1283.[CrossRef]
    [Google Scholar]
  30. Seif, I., Coulon, P., Rollin, P. E. & Flamand, A. ( 1985; ). Rabies virulence: effect on pathogenicity and sequence characterization of rabies virus mutations affecting antigenic site III of the glycoprotein. Journal of Virology 51, 505-514.
    [Google Scholar]
  31. Singh, I., Doms, R. W., Wagner, K. R. & Helenius, A. ( 1990; ). Intracellular transport of soluble and membrane-bound glycoproteins: folding, assembly and secretion of anchor-free influenza hemagglutinin. EMBO Journal 9, 631-639.
    [Google Scholar]
  32. Thoulouze, M. I., Lafage, M., Schachner, M., Hartmann, U., Cremer, H. & Lafon, M. ( 1998; ). The neural cell adhesion molecule is a receptor for rabies virus. Journal of Virology 72, 7181-7190.
    [Google Scholar]
  33. Tuffereau, C., Bénéjean, J., Blondel, D., Kieffer, B. & Flamand, A. ( 1998; ). Low-affinity nerve growth factor receptor (P75NTR) can serve as a receptor for rabies virus. EMBO Journal 17, 7250-7259.[CrossRef]
    [Google Scholar]
  34. Van den Steen, P., Rudd, P. M., Dwek, D. A. & Opdenakker, G. ( 1998; ). Concepts and principles of O-linked glycosylation. Critical Reviews in Biochemistry and Molecular Biology 33, 151-208.[CrossRef]
    [Google Scholar]
  35. Vanlandschoot, P., Beinaert, E., Neirynck, S., Saelens, X., Jou, W. M. & Fiers, W. ( 1996; ). Molecular and immunological characterization of soluble aggregated A/Victoria/3/75 (H3N2) influenza haemagglutinin expressed in insect cells. Archives of Virology 141, 1715-1726.[CrossRef]
    [Google Scholar]
  36. Vanlandschoot, P., Beinaert, E., Grooten, J., Jou, W. M. & Fiers, W. ( 1998; ). pH-dependent aggregation and secretion of soluble monomeric influenza hemagglutinin. Archives of Virology 143, 227-239.[CrossRef]
    [Google Scholar]
  37. Walker, P. J. & Kongsuwan, K. ( 1999; ). Deduced structural model for animal rhabdovirus glycoproteins. Journal of General Virology 80, 1211-1220.
    [Google Scholar]
  38. Whitt, M. A., Buonocore, L., Prehaud, C. & Rose, J. K. ( 1991; ). Membrane fusion activity, oligomerization, and assembly of the rabies virus glycoprotein. Virology 185, 681-688.[CrossRef]
    [Google Scholar]
  39. Wojczyk, B. S., Stwora-Wojczyk, M., Shakin-Eshleman, S., Wunner, W. H. & Spitalnik, S. L. ( 1998; ). The role of site-specific N-glycosylation in secretion of soluble forms of rabies virus glycoprotein. Glycobiology 8, 121-130.[CrossRef]
    [Google Scholar]
  40. Yano, H. & Chao, M. V. ( 2000; ). Neurotrophin receptor structure and interactions. Pharmaceutica Acta Helvetiae 74, 253-260.[CrossRef]
    [Google Scholar]
  41. Zhu, Q. & Courtney, R. J. ( 1988; ). Chemical crosslinking of glycoproteins on the envelope of herpes simplex virus. Virology 167, 377-384.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-83-6-1465
Loading
/content/journal/jgv/10.1099/0022-1317-83-6-1465
Loading

Data & Media loading...

Most cited articles

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