Folding of rabies virus glycoprotein: Epitope acquisition and interaction with endoplasmic reticulum chaperones

Journal of Virology

Volumn 71, Issue 5, 1997, Pages 3742-3750

  Gaudin, Yves ^a  

^a CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CALNEXIN; CASTANOSPERMINE; EPITOPE; MONOCLONAL ANTIBODY; TUNICAMYCIN; VIRUS PROTEIN;

ANTIGEN RECOGNITION; ARTICLE; CONFORMATIONAL TRANSITION; ENDOPLASMIC RETICULUM; PH MEASUREMENT; PRIORITY JOURNAL; PROTEIN FOLDING; RABIES VIRUS; VIRUS PATHOGENESIS;

EID: 0031000682     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.71.5.3742-3750.1997     Document Type: Article

References (58)

1. Anilionis, A., W. H. Wunner, and P. J. Curtis. 1981. Structure of the glycoprotein gene in rabies virus. Nature (London) 294:275-278.
2. Arita, M., and P. Atanasiu. 1980. Etude comparative du poids moléculaire de plusieurs souches de virus rabique par électrophorèse sur gel de polyacrylamide. Ann. Virol. (Paris) 131E:201-215.
3. Benmansour, A., H. Leblois, P. Coulon, C. Tuffereau, Y. Gaudin, A. Flamand, and F. Lafay. 1991. Antigenicity of rabies virus glycoprotein. J. Virol. 65:4198-4203.
4. Braakman, I., H. Hoover-Litty, K. R. Wagner, and A. Helenius. 1991. Folding of influenza hemagglutinin in the endoplasmic reticulum. J. Cell Biol. 114:401-411.
5. Cannon, K. S., D. N. Hebert, and A. Helenius. 1996. Glycan-dependent and -independent association of vesicular stomatitis virus G protein with calnexin. J. Biol. Chem. 271:14280-14284.
6. Chen, W., J. Helenius, I. Braakman, and A. Helenius. 1995. Cotranslational folding and calnexin binding during glycoproteins synthesis. Proc. Natl. Acad. Sci. USA 92:6229-6233.
7. Coulon, P., P. E. Rollin, and A. Flamand. 1983. Molecular basis of rabies virus virulence. II. Identification of a site on the CVS glycoprotein associated with virulence. J. Gen. Virol. 64:693-696.
8. Dietzschold, B. 1977. Oligosaccharides of the glycoprotein of rabies virus. J. Virol. 23:286-293.
9. Dietzschold, B., J. H. Cox, and L. G. Schneider. 1979. Rabies virus strains: a comparison study by polypeptide analysis of vaccine strains with different pathogenic patterns. Virology 98:63-75.
10. Doms, R. W., R. A. Lamb, J. K. Rose, and A. Helenius. 1993. Folding and assembly of viral membrane proteins. Virology 193:545-562.
11. Dunphy, W. G., and J. E. Rothman. 1985. Compartimental organization of the Golgi stack. Cell 42:13-21.
12. Gaudin, Y., H. Raux, A. Flamand, and R. W. H. Ruigrok. 1996. Identification of amino acids controlling the low-pH-induced conformational change of rabies virus glycoprotein. J. Virol. 70:7371-7378.
13. Gaudin, Y., R. W. H. Ruigrok, M. Knossow, and A. Flamand. 1993. Low-pH conformational changes of rabies virus glycoprotein and their role in membrane fusion. J. Virol 67:1365-1372.
14. Gaudin, Y., R. W. H. Ruigrok, C. Tuffereau, M. Knossow, and A. Flamand. 1992. Rabies virus glycoprotein is a trimer. Virology 187:627-632.
15. Gaudin, Y., C. Tuffereau, P. Durrer, A. Flamand, and R. W. H. Ruigrok. 1995. Biological function of the low-pH, fusion-inactive conformation of rabies virus glycoprotein (G): G is transported in a fusion-inactive state-like conformation. J. Virol. 69:5528-5534.
16. Gaudin, Y., C. Tuffereau, D. Segretain, M. Knossow, and A. Flamand. 1991. Reversible conformational changes and fusion activity of rabies virus glycoprotein. J. Virol. 65:4853-4859.
17. Gething, M. J., K. McCammon, and J. Sambrook. 1986. Expression of wild-type and mutant forms of influenza hemagglulinin: the role of folding in intracellular transport. Cell 46:939-950.
18. Gething, M. J., and J. Sambrook. 1992. Protein folding in the cell. Nature (London) 355:33-45.
19. Hammond, C., I. Braakman, and A. Helenius. 1994. Role of N-linked oligosaccharide recognition, glucose trimming, and calnexin in glycoprotein folding and quality control. Proc. Natl. Acad. Sci. USA 91:913-917.
20. Hammond, C., and A. Helenius. 1994. Folding of VSV G protein: sequential interaction with BiP and calnexin. Science 266:456-458.
21. Hammond, C., and A. Helenius. 1995. Quality control in the secretory pathway. Curr. Opin. Cell Biol. 7:523-529.
22. Hebert, D. N., B. Foellmer, and A. Helenius. 1995. Glucose trimming and reglucosylation determine glycoprotein association with calnexin in the endoplasmic reticulum. Cell 81:425-433.
23. Hebert, D. N., B. Foellmer, and A. Helenius. 1996. Calnexin and calreticulin promote folding, delay oligomerization and suppress degradation of influenza hemagglutinin in microsomes. EMBO J. 15:2961-2968.
24. Hurtley, S. M., D. G. Bole, H. Hoover-Litty, A. Helenius, and C. S. Copeland. 1989. Interactions of misfolded influenza virus hemagglutinin with binding protein (BiP). J. Cell Biol. 108:2117-2126.
25. Jackson, M. R., M. F. Cohen-Doyle, P. A. Peterson, and D. B. Williams. 1994. Regulation of MHC class I transport by the molecular chaperone, calnexin (p88, IP90). Science 263:384-397.
26. Kim, P. S., and P. Arvan. 1995. Calnexin and BiP act as sequential molecular chaperones during thyroglobulin folding in the endoplasmic reticulum. J. Cell Biol. 128:29-38.
27. Kornfeld, R., and S. Kornfeld. 1985. Assembly of asparagine-linked oligosaccharides. Annu. Rev. Bioehem. 54:631-664.
28. Lafay, F., A. Benmansour, K. Chebli, and A. Flamand. 1996. Immunodominant epitopes defined by a yeast-expressed library of random fragments of the rabies virus glycoprotein map outside major antigenic sites. J. Gen. Virol. 77:339-346.
29. Lafay, F., P. Coulon, L. Astic, D. Saucier, D. Riche, A. Holley, and A. Flamand. 1991. spread of the CVS strain of rabies virus and of the avirulent mutant AvO1 along the olfactory pathways of the mouse after intranasal inoculation. Virology 183:320-330.
30. Lentz, T. L., P. T. Wilson, E. Hawrot, and D. W. Speicher. 1984. Amino acid sequence similarity between rabies virus glycoprotein and snake venom curaremimetic neurotoxins. Science 226:847-848.
31. Loo, T. W., and D. M. Clarke. 1994. Prolonged association of temperature-sensitive mutants of human P-glycoprotein with calnexin during biogenesis. J. Biol. Chem. 269:28683-28689.
32. Machamer, C. E., R. W. Doms, D. G. Bole, A. Helenius, and J. K. Rose. 1990. Heavy chain binding protein recognizes incompletely disulfide-bonded forms of vesicular stomatitis virus G protein. J. Biol. Chem. 265:6879-6883.
33. Margolese, L., G. L. Waneck, C. K. Suzuki, E. Degen, R. A. Flavell, and D. B. Williams. 1993. Identification of the region on the class I histocompatibility molecule that interacts with the molecular chaperone, p88 (Calnexin, IP90). J. Biol. Chem. 268:17959-17966.
34. Mathieu, M. E., P. R. Grigera, A. Helenius, and R. R. Wagner. 1996. Folding, unfolding, and refolding of the vesicular stomatitis virus glycoprotein. Biochemistry 35:4084-4093.
35. Mebatsion, T., M. J. Schnell, and K. K. Conzelmann. 1995. Mokola virus glycoprotein and chimeric proteins can replace rabies virus glycoprotein in the rescue of infectious defective rabies virus particles. J. Virol. 69:1444-1451.
36. Melnick, J. M., J. L. Dul, and Y. Argon. 1994. Sequential interaction of the chaperones BiP and GRP94 with immunoglobulin chains in the endoplasmic reticulum. Nature (London) 370:373-375.
37. Mifune, K., M. Ohuchi, and K. Mannen. 1982. Hemolysis and cell fusion by rhabdoviruses. FEBS Lett. 137:293-297.
38. Munro, S., and H. R. B. Pelham. 1986. An HSP70-like protein in the ER: identity with the 78 kd glucose-regulated protein and immunoglobulin heavy chain binding protein. Cell 46:291-300.
39. Ora, A., and A. Helenius. 1995. Calnexin fails to associate with substrate proteins in glucosidase-deficient cell lines. J. Biol. Chem. 270:26060-26062.
40. Otteken, A., P. L. Earl, and B. Moss. 1996. Folding, assembly, and intracellular trafficking of the human immunodeficiency virus type 1 envelope glycoprotein analyzed with monoclonal antibodies recognizing maturational intermediates. J. Virol. 70:3407-3415.
41. Ou, W. J., P. H. Cameron, D. Y. Thomas, and J. J. M. Bergeron. 1993. Association of folding intermediates of glycoproteins with calnexin during protein maturation. Nature (London) 364:771-776.
42. Préhaud, C., P. Coulon, F. Lafay, C. Thiers, and A. Flamand. 1988. Antigenic site II of the rabies virus glycoprotein: structure and role in viral virulence. J. Virol. 62:1-7.
43. Rajagopalan, S., Y. Xu, and M. B. Brenner. 1994. Retention of unassembled components of integral membrane proteins by calnexin. Science 263:387-390.
44. Raux, H., P. Coulon, F. Lafay, and A. Flamand. 1995. Monoclonal antibodies which recognize the acidic configuration of the rabies glycoprotein at the surface of the virion can be neutralizing. Virology 210:400-408.
45. Raux, H., Y. Gaudin, and A. Flamand. Unpublished results.
46. Seif, I., P. Coulon, P. E. Rollin, and A. Flamand. 1985. Rabies virulence: effect on pathogenicity and sequence characterization of rabies virus mutations affecting antigenic site III of the glycoprotein. J. Virol. 51:505-514.
47. Shakin-Eshleman, S. H., A. T. Remaley, J. R. Eshleman, W. H. Wunner, and S. L. Spitalnik. 1992. N-linked glycosylation of rabies virus glycoprotein. Individual sequons differ in their glycosylation efficiencies and influence on cell surface expression. J. Biol. Chem. 267:10690-10698.
48. Sousa, M., and A. J. Parodi. 1995. The molecular basis for the recognition of misfolded glycoproteins by the UDP-Glc:glycoprotein glucosyltransferase. EMBO J. 14:4196-4203.
49. Sousa, M. C., M. A. Ferrero-Garcia, and A. J. Parodi. 1992. Recognition of the oligosaccharide and protein moieties of glycoproteins by the UDP-Glc: glycoprotein glucosyltransferase. Biochemistry 31:97-105.
50. Tatu, U., C. Hammond, and A. Helenius. 1995. Folding and oligomerization of influenza hemagglutinin in the ER and the intermediate compartment. EMBO J. 14:1340-1348.
51. Tuffereau, C., H. Leblois, J. Bénéjean, P. Coulon, F. Lafay, and A. Flamand. 1989. Arginine or lysine in position 333 of ERA and CVS glycoprotein is necessary for rabies virulence in adult mice. Virology 172:206-212.
52. Van Leeuwen, J. E. M., and K. P. Kearse. 1996. Calnexin associates exclusively with individual CD3d and T cell antigen receptor (TCR) a proteins containing incompletely trimmed glycans that are not assembled into multisubunit TCR complexes. J. Biol. Chem. 271:9660-9665.
53. Ware, F. E., A. Vassilakos, P. A. Peterson, M. R. Jackson, M. A. Lehrman, and D. B. Williams. 1995. The molecular chaperone calnexin binds GlclMan9GlcNAc2 oligosaccharide as an initial step in recognizing unfolded glycoproteins. J. Biol. Chem. 270:4697-4704.
54. Whitt, M. A., L. Buonocore, C. Prehaud, and J. K. Rose. 1991. Membrane fusion activity, oligomerization, and assembly of the rabies virus glycoprotein. Virology 185:681-688.
55. Wilson, I. A., J. J. Skehel, and D. C. Wiley. 1981. Structure of the hemagglutinin membrane glycoprotein of influenza virus at 3 Å resolution. Nature (London) 289:368-373.
56. Wunner, W. H., B. Dietzschold, C. L. Smith, M. Lafon, and E. Golub. 1985. Antigenic variants of CVS rabies virus with altered glycosylation sites. Virology 140:1-12.
57. Yelverton, E., S. Norton, J. F. Obijeski, and D. V. Goeddel. 1983. Rabies virus glycoprotein analogs: biosynthesis in E. coli. Science 219:614-620.
58. Yewdell, J. W., A. Yellin, and T. Bächi. 1988. Monoclonal antibodies localize events in the folding, assembly, and intracellular transport of the influenza virus hemagglutinin glycoprotein. Cell 52:843-852.