The role of site-specific N-glycosylation in secretion of soluble forms of rabies virus glycoprotein

Glycobiology

Volumn 8, Issue 2, 1998, Pages 121-130

  Wojczyk, Boguslaw S ^a,c   Stwora Wojczyk, Magda ^a   Shakin Eshleman, Susan ^b,d   Wunner, William H ^a   Spitalnik, Steven L ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c JAGIELLONIAN UNIVERSITY   (Poland)

^d JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Glycoproteins; N linked glycosylation; Rabies virus; Sequon

Indexed keywords

1 DEOXYMANNONOJIRIMYCIN; CELL SURFACE PROTEIN; VIRUS GLYCOPROTEIN;

ARTICLE; CONTROLLED STUDY; DNA TRANSFECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN GLYCOSYLATION; PROTEIN SECRETION; RABIES VIRUS; SITE DIRECTED MUTAGENESIS;

ANIMALS; ANTIGENS, VIRAL; CARRIER PROTEINS; CELL LINE; CHO CELLS; CRICETINAE; GLYCOPROTEINS; GLYCOSYLATION; HEAT-SHOCK PROTEINS; INDOLIZINES; INTRACELLULAR FLUID; KINETICS; MOLECULAR CHAPERONES; MUTAGENESIS, SITE-DIRECTED; RABIES VIRUS; RECOMBINANT FUSION PROTEINS; SOLUBILITY; SWAINSONINE; TRANSFECTION; VIRAL ENVELOPE PROTEINS;

EUKARYOTA; RABIES VIRUS;

EID: 0031908813     PISSN: 09596658     EISSN: None     Source Type: Journal    
DOI: 10.1093/glycob/8.2.121     Document Type: Article

References (45)

1. Anilionis, A., Wunner, W.H. and Curtis, P.J. (1981) Structure of the glycoprotein gene in rabies virus. Nature, 294, 275-278.
2. Bischoff, J., Liscum, L. and Kornfeld, R. (1986) The use of 1-deoxymannojirimycin to evaluate the role of various α-mannosidases in oligosaccharide processing in intact cells. J. Biol. Chem., 261, 4766-4774.
3. Bole, D.G., Hendershot, L.M. and Kearney, J.F. (1986) Posttranslational association of immunoglobulin heavy chain binding protein with nascent heavy chains in nonsecreting and secreting hybridomas. J. Cell Biol., 102, 1558-1566.
4. Burger, S.R., Remaley, A.T., Danley, J.M., Moore, J., Muschel, R.J., Wunner, W.H. and Spitalnik, S.L. (1991) Stable expression of rabies virus glycoprotein in Chinese hamster ovary cells. J. Gen. Virol., 72, 359-367.
5. Coll, J.M. (1995) The glycoprotein G of rhabdoviruses. Arch. Virol., 140, 827-851.
6. Conzelmann, K.K., Cox, J.M. Schneider, L.G. and Thiel, H.J. (1990) Molecular cloning and complete nucleotide sequence of the attenuated rabies virus SAD B19. Virology, 175, 485-499.
7. Davis, S.J., Ward, H.A., Puklavec, M.J., Willis, A.C., Williams, A.F. and Barclay, A.N. (1990) High level expression in Chinese hamster ovary cells of soluble forms of CD4 T lymphocyte glycoprotein including glycosylation variants. J. Biol. Chem., 265, 10410-10418.
8. Doms, R.W., Keller, D.S., Helenius, A. and Balch, W.E. (1987) Role for adenosine triphosphate in regulating the assembly and transport of vesicular stomatitis virus G protein trimers. J. Cell Biol., 105, 1957-1969.
9. Elbein, A.D. (1991) Glycosidase inhibitors: inhibitors of N-linked oligosaccharide processing. FASEB J., 5, 3055-3063.
10. Fishbein, D.B. and Robinson, L.E. (1993) Rabies. New Engl. J. Med., 329, 1632-1638.
11. Flamand, A., Wiktor, T.J. and Koprowski, H. (1980) Use of hybridoma monoclonal antibodies in the detection of antigenic differences between rabies and rabies-related virus proteins. II. The glycoprotein. J. Gen. Virol., 48, 105-109.
12. Freedman, R.B., Hirst, T.R. and Tuite, M.F. (1994) Protein disulphide isomerase: building bridges in protein folding. Trends Biochem. Sci., 19, 331-336.
13. Gaudin, Y., Ruigrok, R.W.H., Tuffereau, C., Knossow, M., and Flamand, A. (1992) Rabies virus glycoprotein is a trimer. Virology, 187, 627-632.
14. Green, S., Issemann, I. and Sheer, E. (1988) A versatile in vivo and in vitro eukaryotic expression vector for protein engineering. Nucleic Acids Res., 16, 369.
15. Guan, J.L., Cao, H. and Rose, J.K. (1988) Cell-surface expression of a membrane-anchored form of the human chorionic gonadotropin alpha subunit. J. Biol. Chem., 263, 5306-5613.
16. Guan, J.L., Machamer, C.E. and Rose, J.K. (1985) Glycosylation allows cell-surface transport of an anchored secretory proteins. Cell, 42, 489-496.
17. Hurtley, S.M., Bole, D.G., Hoover-Litty, H., Helenius, A. and Copeland, C.S. (1989) Interactions of misfolded influenza virus hemagglutinin with binding protein (BiP). J. Cell Biol., 108, 2117-2126,
18. Kasturi, L., Eshleman, J.R., Wunner, W.H. and Shakin-Eshleman, S.H. (1995) The hydroxy amino acid in an Asn-X-Ser/Thr sequon can influence N-linked core glycosylation efficiency and the level of expression of a cell surface glycoprotein. J. Biol. Chem., 270, 14756-14761.
19. Kieny, M.P., Lathe, R., Drillien, R., Spehner, D., Skory, S., Schmitt, D., Wiktor, T., Koprowski, H. and Lecocq, J.P. (1984) Expression of rabies virus glycoprotein from a recombinant vaccinia virus. Nature, 312, 163-166.
20. Konig, R., Ashwell, G. and Hanover, J.A. (1988) Glycosylation of CD4. Tunicamycin inhibits surface expression. J. Biol. Chem., 263, 9502-9507.
21. Lafon, M., Wiktor, T.J. and Macfarlan, R.I. (1983) Antigenic sites on the CVS rabies virus glycoprotein: analysis with monoclonal antibodies. J. Gen. Virol., 64, 843-851.
22. Lathe, R.F., Kieny, M.P., Schmitt, D., Curtis, P. and Lecocq, J.P. (1984) M13 bacteriophage vectors for the expression of foreign proteins in Escherichia coli: the rabies glycoprotein. J. Molec. Appl. Genet., 2, 331-342.
23. Machamer, C.E. and Rose, J.K. (1988) Vesicular stomatitis virus G proteins with altered glycosylation sites display temperature-sensitive intracellular transport and are subject to aberrant intermolecular disulfide bonding. J. Biol. Chem., 263, 5955-5960.
24. Masuno, H., Blanchette-Mackie, E.J., Schultz, C.J., Spaeth, A.E., Scow, R.O. and Okuda, H. (1992) Retention of glucose by N-linked oligosaccharide chains impedes expression of lipoprotein lipase activity: effect of castanospermine. J. Lipid Res., 33, 1343-1349.
25. Morimoto, K., Ni, Y.J. and Kawai, A. (1992) Syncytium formation is induced in the murine neuroblastoma cell cultures which produce pathogenic type G proteins of the rabies virus. Virology, 189, 203-216.
26. Nauseef, W.M., McCormick, S.J. and Clark R.A. (1995) Calreticulin functions as a molecular chaperone in the biosynthesis of myeloperoxidase. J. Biol. Chem., 270, 4741-4747.
27. Ou, W.J., Cameron, P.H., Thomas, D.Y. and Bergeron, J.J.M. (1993) Association of folding intermediates of glycoproteins with calnexin during protein maturation. Nature, 364, 771-776.
28. Peyrieras, N., Bause, E., Legler, G., Vasilov, R., Claesson, L., Peterson, P. and Ploegh, H. (1983) Effects of glucosidase inhibitors nojirimycin and deoxynojirimycin on the biosynthesis of membrane and secretory glycoproteins. EMBO J., 2, 823-832.
29. Prehaud, C. Takehara, K., Flamand, A. and Bishop, D.H.L. (1989) Immunogenic and protective properties of rabies virus glycoprotein expressed by baculovirus vectors. Virology, 173, 390-399.
30. Seif, I., Coulon, P., Rollin, P.E. and Flamand, A. (1985) Rabies virulence: effect on pathogeneicity and sequence characterization of rabies virus mutations affecting antigenic site III of the glycoprotein. J. Virol., 53, 926-934.
31. Shakin-Eshleman, S.H., Remaley, A.T., Eshleman, J.R., Wunner, W.H. and Spitalnik, S.L. (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.
32. Shakin-Eshleman, S.H., Wunner, W.H. and Spitalnik, S.L. (1993) Efficiency of N-linked core glycosylation: Glycosylation at Asn319 of rabies virus glycoprotein is altered by deletions C-terminal to the glycosylation sequon. Biochemistry, 32, 9465-9472.
33. Smith, J.S., Sumner, J.W., and Roumillat, L.F. (1984) Enzyme immunoassay for rabies antibody in hybridoma culture fluids and its application to differentiation of street and laboratory strains of rabies virus. J. Clin. Microbiol., 19, 267-272.
34. Sontheimer, R.D., Nguyen, T.Q., Cheng, S.T., Lieu, T.S. and Capra, J.D. (1995) The unveiling of calreticulin - a clinically relevant tour of modern cell biology. J. Invest. Med., 43, 362-370.
35. Southern, P.J. and Berg, P. (1982) Transformation of mammalian cells to antibiotic resistance with a bacterial gene under the control of the SV40 early region promoter. J. Mol. Appl. Genet., 1, 327-241.
36. Stanley, P., Caillibot, V. and Siminovich, L. (1975) Selection and characterization of eight phenotypically distinct lines of lectin-resistant Chinese hamster ovary cells. Cell, 6, 121-128.
37. Tifft, C.J., Proia, R.L. and Camerini-Otero, R.D. (1992) The folding and cell surface expression of CD4 requires glycosylation. J. Biol. Chem., 267, 3268-3273.
38. Tuffereau, C., Leblois, H., Benejean, J., Coulon, P., Lafay, F. and Flamand, A. (1989) Arginine or lysine in position 333 of ERA and CVS glycoprotein is necessary for rabies virulence in adult mice. Virology, 172, 206-212.
39. Whitt, M.A., Buonocore, L., Prehaud, C. and Rose, J.K. (1991) Membrane fusion activity, oligomerization, and assembly of the rabies virus glycoprotein. Virology, 185, 681-688.
40. Wiktor, T.J., Gyorgy, E., Schlumberger, H.D., Sokol, F. and Koprowski, H. (1973) Antigenic properties of rabies virus components. J. Immunol., 110, 269-276.
41. Wojczyk, B.S. Shakin-Eshleman, S.H., Doms, R.W., Xiang, Z.Q., Ertl, H.C.J., Wunner, W.H. and Spitalnik, S.L. (1995) Influence of N-glycan processing on secretion of a secreted form of rabies virus glycoprotein. Biochemistry, 34, 2599-2609.
42. Wojczyk, B.S., Czerwinski, M., Stwora-Wojczyk, M.M., Siegel, D.L., Wunner, W.H. and Spitalnik, S.L. (1996) Purification of a secreted recombinant form of rabies virus glycoprotein: Comparison of two affinity tags. Protein Exp. Purif., 7, 183-193.
43. Xiang, Z.Q., Spitalnik, S., Tran, M., Wunner, W.H., Cheng, J. and Ertl, H.C.J. (1994) Vaccination with a plasmid vector carrying the rabies virus glycoprotein gene induces protective immunity against rabies virus. Virology, 199, 132-140.
44. Xiang, Z.Q., Spitalnik, S.L., Cheng, J., Erikson, J., Wojczyk, B.S. and Ertl, H.C.J. (1995) Immune responses to nucleic acid vaccines to rabies virus. Virology, 209, 569-579.
45. Yelverton, E., Norton, S., Obijeski, J.F. and Goeddel, D.V. (1983) Rabies virus glycoprotein analogs: Biosynthesis in Escherichia coli. Science, 219, 614-620.