Intracellular assembly and secretion of recombinant subviral particles from tick-borne encephalitis virus

Journal of Virology

Volumn 77, Issue 7, 2003, Pages 4370-4382

  Lorenz, Ivo C ^a   Kartenbeck, Jürgen ^b   Mezzacasa, Anna ^a   Allison, Steven L ^c   Heinz, Franz X ^c   Helenius, Ari ^a  

^a ETH ZURICH   (Switzerland)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c UNIVERSITY OF VIENNA   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

DIMER; GLUCOSIDASE; UNCLASSIFIED DRUG; VIRUS ENVELOPE PROTEIN; VIRUS ENVELOPE PROTEIN E; VIRUS ENVELOPE PROTEIN PRM;

ARTICLE; ELECTRON MICROSCOPY; ENDOPLASMIC RETICULUM; FLAVIVIRUS; IMMUNOFLUORESCENCE MICROSCOPY; MAMMAL CELL; NONHUMAN; PARTICLE SIZE; PRIORITY JOURNAL; PROTEIN EXPRESSION; TICK BORNE ENCEPHALITIS FLAVIVIRUS; VIRUS ASSEMBLY; VIRUS NUCLEOCAPSID; VIRUS PARTICLE;

ANIMALS; COS CELLS; ENCEPHALITIS VIRUSES, TICK-BORNE; INCLUSION BODIES, VIRAL; KINETICS; MICROSCOPY, ELECTRON; POLYSACCHARIDES; RECOMBINANT PROTEINS; TRANSFECTION; VIRAL ENVELOPE PROTEINS; VIRUS ASSEMBLY;

EID: 0037378495     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.77.7.4370-4382.2003     Document Type: Article

References (59)

1. Adams, S. C., A. K. Broom, L. M. Sammels, A. C. Hartnett, M. J. Howard, R. J. Coelen, J. S. Mackenzie, and R. A. Hall. 1995. Glycosylation and antigenic variation among Kunjin virus isolates. Virology 206:49-56.
2. Allison, S. L., C. W. Mandl, C. Kunz, and F. X. Heinz. 1994. Expression of cloned envelope protein genes from the flavivirus tick-borne encephalitis virus in mammalian cells and random mutagenesis by PCR. Virus Genes 8:187-198.
3. Allison, S. L., J. Schalich, K. Stiasny, C. W. Mandl, and F. X. Heinz. 2001. Mutational evidence for an internal fusion peptide in flavivirus envelope protein E. J. Virol. 75:4268-4275.
4. Allison, S. L., J. Schalich, K. Stiasny, C. W. Mandl, C. Kunz, and F. X. Heinz. 1995. Oligomeric rearrangement of tick-borne encephalitis virus envelope proteins induced by an acidic pH. J. Virol. 69:695-700.
5. Allison, S. L., K. Stadler, C. W. Mandl, C. Kunz, and F. X. Heinz. 1995. Synthesis and secretion of recombinant tick-borne encephalitis virus protein E in soluble and particulate form. J. Virol. 69:5816-5820.
6. Allison, S. L., K. Stiasny, K. Stadler, C. W. Mandl, and F. X. Heinz. 1999. Mapping of functional elements in the stem-anchor region of tick-borne encephalitis virus envelope protein E. J. Virol. 73:5605-5612.
7. Blanchard, E., D. Brand, S. Trassard, A. Goudeau, and P. Roingeard. 2002. Hepatitis C virus-like particle morphogenesis. J. Virol. 76:4073-4079.
8. Bolt, G., I. R. Pedersen, and M. Blixenkrone-Moller. 1999. Processing of N-linked oligosaccharides on the measles virus glycoproteins: importance for antigenicity and for production of infectious virus particles. Virus Res. 61:43-51.
9. 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.
10. Chambers, T. J., C. S. Hahn, R. Galler, and C. M. Rice. 1990. Flavivirus genome organization, expression, and replication. Annu. Rev. Microbiol. 44:649-688.
11. Chambers, T. J., M. Halevy, A. Nestorowicz, C. M. Rice, and S. Lustig. 1998. West Nile virus envelope proteins: nucleotide sequence analysis of strains differing in mouse neuroinvasiveness. J. Gen. Virol. 79:2375-2380.
12. Corver, J., A. Ortiz, S. L. Allison, J. Schalich, F. X. Heinz, and J. Wilschut. 2000. Membrane fusion activity of tick-borne encephalitis virus and recombinant subviral particles in a liposomal model system. Virology 269:37-46.
13. Conrageot, M. P., M. P. Frenkiel, C. D. Dos Santos, V. Deubel, and P. Despres. 2000. Alpha-glucosidase inhibitors reduce dengue virus production by affecting the initial steps of virion morphogenesis in the endoplasmic reticulum. J. Virol. 74:564-572.
14. Crooks, A. J., J. M. Lee, L. M. Easterbrook, A. V. Timofeev, and J. R. Stephenson. 1994. The NS1 protein of tick-borne encephalitis virus forms multimeric species upon secretion from the host cell. J. Gen. Virol. 75:3453-3460.
15. Doms, R. W., R. A. Lamb, J. K. Rose, and A. Helenius, 1993. Folding and assembly of viral membrane proteins. Virology 193:545-562.
16. Donaldson, J. G., D. Finazzi, and R. D. Klausner. 1992. Brefeldin A inhibits Golgi membrane-catalysed exchange of guanine nucleotide onto ARF protein. Nature 360:350-352.
17. Elbein, A. D. 1987. Glycosylation inhibitors for N-linked glycoproteins. Methods Enzymol. 138:661-709.
18. Ellgaard, L., M. Molinari, and A. Helenius. 1999. Setting the standards: quality control in the secretory pathway. Science 286:1882-1888.
19. Ferlenghi, I., M. Clarke, T. Ruttan, S. L. Allison, J. Schalich, F. X. Heinz, S. C. Harrison, F. A. Rey, and S. D. Fuller. 2001. Molecular organization of a recombinant subviral particle from tick-borne encephalitis virus. Mol. Cell 7:593-602.
20. Freedman, R. B. 1989. Protein disulfide isomerase: multiple roles in the modification of nascent secretory proteins. Cell 57:1069-1072.
21. Garoff, H., R. Hewson, and D. J. Opstelten. 1998. Virus maturation by budding. Microbiol. Mol. Biol. Rev. 62:1171-1190.
22. Graeve, L., C. Garreis-Wabnitz, M. Zauke, M. Breindl, and J. Kruppa. 1986. The soluble glycoprotein of vesicular stomatitis virus is formed during or shortly after the translation process. J. Virol. 57:968-975.
23. Guirakhoo, F., F. X. Heinz, and C. Kunz. 1989. Epitope model of tick-borne encephalitis virus envelope glycoprotein E: analysis of structural properties, role of carbohydrate side chain, and conformational changes occurring at acidic pH. Virology 169:90-99.
24. Hallenberger, S., S. P. Tucker, R. J. Owens, H. B. Bernstein, and R. W. Compans. 1993. Secretion of a truncated form of the human immunodeficiency virus type 1 envelope glycoprotein. Virology 193:510-514.
25. 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.
26. Hammond, C., and A. Helenius. 1994. Quality control in the secretory pathway: retention of a misfolded viral membrane glycoprotein involves cycling between the ER, intermediate compartment, and Golgi apparatus. J. Cell Biol. 126:41-52.
27. Heinz, F. X., and S. L. Allison. 2000. Structures and mechanisms in flavivirus fusion. Adv. Virus Res. 55:231-269.
28. Heinz, F. X., G. Auer, K. Stiasny, H. Holzmann, C. Mandl, F. Guirakhoo, and C. Kunz. 1994. The interactions of the flavivirus envelope proteins: implications for virus entry and release. Arch. Virol. Suppl. 9:339-348.
29. Heinz, F. X., and C. Kunz. 1981. Homogeneity of the structural glycoprotein from European isolates of tick-borne encephalitis virus: comparison with other flaviviruses. J. Gen. Virol. 57:263-274.
30. Herscovics, A. 1999. Importance of glycosidases in mammalian glycoprotein biosynthesis. Biochim. Biophys. Acta 1473:96-107.
31. Iacono-Connors, L. C., J. F. Smith, T. G. Ksiazek, C. L. Kelley, and C. S. Schmaljohn. 1996. Characterization of Langat virus antigenic determinants defined by monoclonal antibodies to E, NS1 and preM and identification of a protective, non-neutralizing preM-specific monoclonal antibody. Virus Res. 43:125-136.
32. Ishak, R., D. G. Tovey, and C. R. Howard. 1988. Morphogenesis of yellow fever virus 17D in infected cell cultures. J. Gen. Virol. 69:325-335.
33. Karlsson, G. B., T. D. Butters, R. A. Dwek, and F. M. Platt. 1993. Effects of the imino sugar N-butyldeoxynojirimycin on the N-glycosylation of recombinant gp120. J. Biol. Chem. 268:570-576.
34. Konishi, E., and P. W. Mason. 1993. Proper maturation of the Japanese encephalitis virus envelope glycoprotein requires cosynthesis with the premembrane protein. J. Virol. 67:1672-1675.
35. Kuhn, R. J., W. Zhang, M. G. Rossmann, S. V. Pletnev, J. Corver, E. Lenches, C. T. Jones, S. Mukhopadhyay, P. R. Chipman, E. G. Strauss, T. S. Baker, and J. H. Strauss. 2002. Structure of dengue virus: implications for flavivirus organization, maturation, and fusion. Cell 108:717-725.
36. Lindenbach, B. D., and C. M. Rice. 2001. Flaviviridae: the viruses and their replication, p. 991-1041. In D. M. Knipe, P. M. Howley, D. E. Griffin, R. A. Lamb, M. A. Martin, B. Roizman, and S. E. Straus (ed.), Fields virology, 4th ed. Lippincott Williams & Wilkins, Philadelphia, Pa.
37. Linstedt, A. D., and H. P. Hauri. 1993. Giantin, a novel conserved Golgi membrane protein containing a cytoplasmic domain of at least 350 kDa. Mol. Biol. Cell 4:679-693.
38. Lorenz, I. C., S. L. Allison, F. X. Heinz, and A. Helenius. 2002. Folding and dimerization of tick-borne encephalitis virus envelope proteins prM and E in the endoplasmic reticulum. J. Virol. 76:5480-5491.
39. Mackenzie, J. M., and E. G. Westaway. 2001. Assembly and maturation of the flavivirus Kunjin virus appear to occur in the rough endoplasmic reticulum and along the secretory pathway, respectively. J. Virol. 75:10787-10799.
40. Mandl, C. W., F. X. Heinz, and C. Kunz. 1988. Sequence of the structural proteins of tick-borne encephalitis virus (western subtype) and comparative analysis with other flaviviruses. Virology 166:197-205.
41. Mason, P. W., S. Pincus, M. J. Fournier, T. L. Mason, R. E. Shope, and E. Paoletti. 1991. Japanese encephalitis virus-vaccinia recombinants produce particulate forms of the structural membrane proteins and induce high levels of protection against lethal JEV infection. Virology 180:294-305.
42. Molinari, M., and A. Helenius. 2000. Chaperone selection during glycoprotein translocation into the endoplasmic reticulum. Science 288:331-333.
43. Rey, F. A., F. X. Heinz, C. Mandl, C. Kunz, and S. C. Harrison. 1995. The envelope glycoprotein from tick-borne encephalitis virus at 2 A resolution. Nature 375:291-298.
44. Rodan, A. R., J. F. Simons, E. S. Trombetta, and A. Helenius. 1996. N-linked oligosaccharides are necessary and sufficient for association of glycosylated forms of bovine RNase with calnexin and calreticulin. EMBO J. 15:6921-6930.
45. Russell, P. K., W. E. Brandt, and J. M. Dalrymple. 1980. Chemical and antigenic structure of flaviviruses. In R. W. Schlesinger (ed.), The togaviruses. Academic Press, New York, N.Y.
46. Saito, T., and I. Yamaguchi. 2000. Effect of glycosylation and glucose trimming inhibitors on the influenza A virus glycoproteins. J. Vet. Med. Sci. 62:575-581.
47. Saraste, J., and E. Kuismanen. 1984. Pre- and post-Golgi vacuoles operate in the transport of Semliki Forest virus membrane glycoproteins to the cell surface. Cell 38:535-549.
48. Schalich, J., S. L. Allison, K. Stiasny, C. W. Mandl, C. Kunz, and F. X. Heinz. 1996. Recombinant subviral particles from tick-borne encephalitis virus are fusogenic and provide a model system for studying flavivirus envelope glycoprotein functions. J. Virol. 70:4549-4957.
49. Schweizer, A., J. A. Fransen, T. Bachi, L. Ginsel, and H. P. Hauri. 1988. Identification, by a monoclonal antibody, of a 53-kD protein associated with a tubulo-vesicular compartment at the cis-side of the Golgi apparatus. J. Cell Biol. 107:1643-1653.
50. Singh, I., R. W. Doms, K. R. Wagner, and A. Helenius. 1990. Intracellular transport of soluble and membrane-bound glycoproteins: folding, assembly and secretion of anchor-free influenza hemagglutinin. EMBO J. 9:631-639.
51. Stadler, K., S. L. Allison, J. Schalich, and F. X. Heinz. 1997. Proteolytic activation of tick-borne encephalitis virus by furin. J. Virol. 71:8475-8481.
52. Stiasny, K., S. L. Allison, C. W. Mandl, and F. X. Heinz. 2001. Role of metastability and acidic pH in membrane fusion by tick-borne encephalitis virus. J. Virol. 75:7392-7398.
53. Stiasny, K., S. L. Allison, J. Schalich, and F. X. Heinz. 2002. Membrane interactions of the tick-borne encephalitis virus fusion protein E at low pH. J. Virol. 76:3784-3790.
54. Teasdale, R. D., and M. R. Jackson. 1996. Signal-mediated sorting of membrane proteins between the endoplasmic reticulum and the golgi apparatus. Annu. Rev. Cell. Dev. Biol. 12:27-54.
55. Wada, I., D. Rindress, P. H. Cameron, W. J. Ou, J. J. Doherty II, D. Louvard, A. W. Bell, D. Dignard, D. Y. Thomas, and J. J. Bergeron. 1991. SSR alpha and associated calnexin are major calcium binding proteins of the endoplasmic reticulum membrane. J. Biol. Chem. 266:19599-19610.
56. Wang, J. J., C. L. Liao, Y. W. Chiou, C. T. Chiou, Y. L. Huang, and L. K. Chen. 1997. Ultrastructure and localization of E proteins in cultured neuron cells infected with Japanese encephalitis virus. Virology 238:30-39.
57. Winkler, G., F. X. Heinz, and C. Kunz. 1987. Studies on the glycosylation of flavivirus E proteins and the role of carbohydrate in antigenic structure. Virology 159:237-243.
58. Wu, S. F., C. J. Lee, C. L. Liao, R. A. Dwek, N. Zitzmann, and Y. L. Lin. 2002. Antiviral effects of an iminosugar derivative on flavivirus infections. J. Virol. 76:3596-3604.
59. Zitzmann, N., A. S. Mehta, S. Carrouee, T. D. Butters, F. M. Platt, J. McCauley, B. S. Blumberg, R. A. Dwek, and T. M. Block. 1999. Imino sugars inhibit the formation and secretion of bovine viral diarrhea virus, a pestivirus model of hepatitis C virus: implications for the development of broad spectrum anti-hepatitis virus agents. Proc. Natl. Acad. Sci. USA 96:11878-11882.