Vaccinia virus membrane proteins p8 and p16 are cotranslationally inserted into the rough endoplasmic reticulum and retained in the intermediate compartment

Journal of Virology

Volumn 71, Issue 10, 1997, Pages 7404-7420

  Salmons, Tessa ^a   Kuhn, Annett ^a   Wylie, Fiona ^a,c   Schleich, Sibylle ^a   Rodriguez, Juan Ramon ^b   Rodriguez, Dolores ^b   Esteban, Mariano ^b   Griffiths, Gareth ^a   Locker, Jacomine Krijnse ^a  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^b CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

^c UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS PROTEIN;

ARTICLE; ENDOPLASMIC RETICULUM; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; VACCINIA VIRUS; VIRUS ENVELOPE;

EID: 0030806017     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.71.10.7404-7420.1997     Document Type: Article

References (38)

1. Blasco, R., and B. Moss. 1991. Extracellular vaccinia virus formation and cell-to-cell virus transmission are prevented by a deletion of the gene encoding the 37,000-dalton outer envelope protein. J. Virol. 65:5910-5920.
2. Cairns, H. J. F. 1960. The initiation of vaccinia infection. Virology 11:603-623.
3. Cobbold, C., J. T. Whittle, and T. Wileman. 1996. Involvement of the endoplasmic reticulum in the assembly and envelopment of African swine fever virus. J. Virol. 70:8382-8390.
4. Cudmore, S., P. Cossart, G. Griffiths, and M. Way. 1995. Actin-based motility of vaccinia virus. Nature 378:636-638.
5. Cudmore, S., R. Blasco, R. Vincentelli, M. Esteban, B. Sodeik, G. Griffiths, and J. Krijnse Locker. 1996. A vaccinia virus core protein, p38, is membrane associated. J. Virol. 70:6909-6921.
6. Dales, S., and B. G. T. Pogo. 1981. Biology of poxviruses. Virology monographs. Springer Verlag, Vienna, Austria.
7. Dales, S., and E. H. Mosbach. 1968. Vaccinia as a model for membrane biogenesis. Virology 35:564-583.
8. Ericsson, M., S. Cudmore, S. Shuman, R. C. Condit, G. Griffiths, and J. Krijnse Locker. 1995. Characterization of ts16, a temperature-sensitive mutant of vaccinia virus. J. Virol. 69:7072-7086.
9. Essani, K., and S. Dales. 1979. Biogenesis of vaccinia: evidence for more than 100 polypeptides in the virion. Virology 95:385-394.
10. Goebel, S. J., G. P. Johnson, M. E. Perkus, S. W. Davis, J. P. Winslow, and E. Paoletti. 1990. The complete DNA sequence of vaccinia virus. Virology 179:247-266.
11. Griffiths, G. 1993. Fine structure immunocytochemistry. Springer Verlag, Heidelberg, Germany.
12. Griffiths, G., R. Pepperkok, J. Krijnse Locker, and T. E. Kreis. 1995. Immunocytochemical localization of beta-COP to the ER-Golgi boundary and the TGN. J. Cell Sci. 108:2839-2856.
13. Griffiths, G. 1996. On vesicle and membrane compartments. Protoplasma 195:37-58.
14. Griffiths, G., M. Ericsson, J. Krijnse Locker, T. Nilsson, H. D. Soeling, B. L. Tang, S. H. Wong, and W. Hong. 1994. Ultrastructural localization of the mammalian KDEL receptor in cultured cells and tissues. J. Cell Biol. 127: 1557-1574.
15. Grimley, P. M., E. N. Rosenblum, S. J. Mims, and B. Moss. 1970. Interruption by rifampicin of an early stage in vaccinia virus morphogenesis: accumulation of membranes which are precursors of virus envelopes. J. Virol. 6:651-659.
16. Hammond, C., and A. Helenius. 1994. Quality control in the secretory pathway: retention of a misfolded viral membrane glycoprotein involves recycling between the ER, intermediate compartment and the Golgi apparatus. J. Cell Biol. 126-41-52.
17. Hiller, G., and K. Weber. 1985. Golgi-derived membranes that contain an acylated viral polypeptide are used for vaccinia virus envelopment. J. Virol. 55:651-659.
18. Jensen, O. N., T. Houthaeve, A. Shevchenko, S. Cudmore, T. Ashford, M. Mann, G. Griffiths, and J. Krijnse Locker. 1996. Identification of the major membrane and core proteins of vaccinia virus by two-dimensional electrophoresis. J. Virol. 70:7485-7497.
19. Johnson, G. P., S. J. Goebel, and E. Paoletti. 1993. An update on the vaccinia virus sequence. Virology 196:381-401.
20. Krijnse Locker, J., M. Ericsson, P. J. M. Rottier, and G. Griffiths. 1994. Characterization of the budding compartment of mouse hepatitis virus: evidence that transport from the RER to the Golgi complex requires only one vesicular transport step. J. Cell Biol. 124:55-70.
21. Krijnse Locker, J., J. K. Rose, M. C. Horzinek, and P. J. M. Rottier. 1992. Membrane assembly of the triple-scanning coronavirus M protein. Individual transmembrane domains show preferred orientation. J. Biol. Chem. 267: 21911-21918.
22. Krijnse Locker, J., R. G. Parton, S. D. Fuller, G. Griffiths, and C. G. Dotti. 1995. The organization of the endoplasmic reticulum and the intermediate compartment in cultured rat hippocampal neurons. Mol. Biol. Cell 6:1315-1332.
23. Krijnse Locker, J., S. Schleich, D. Rodriguez, B. Goud, E. J. Snijder, and G. Griffiths. 1996. The role of a 21-kDa viral membrane protein in the assembly of vaccinia virus from the intermediate compartment. J. Biol. Chem. 271: 14950-14958.
24. 23a.Krijnse Locker, J., et al. Unpublished data.
25. Moss, B., E. N. Rosenblum, E. Katz, and P. M. Grimley. 1969. Rifampicin: a specific inhibitor of vaccinia virus assembly. Nature 224:1280-1284.
26. Rapoport, T. A. 1985. Protein translocation across and integration into membranes. Crit. Rev. Biochem. 20:73-137.
27. Rodriguez, D., M. Esteban, and J. R. Rodriguez. 1995. Vaccinia virus A17L gene product is essential for an early step in virion morphogenesis. J. Virol. 69:4640-4648.
28. Rodriguez, J. R., C. Risco, J. L. Carrascosa, M. Esteban, and D. Rodriguez. 1997. Characterization of early stages in vaccinia virus membrane biogenesis: implication of the 21-kDa and a newly identified 15-kDa envelope protein. J. Virol. 71:1821-1833.
29. Roos, N., M. Cyrklaff, S. Cudmore, R. Blasco, J. Krijnse Locker, and G. Griffiths. 1996. A novel immunogold cryoelectron microscopic approach to investigate the structure of the intracellular and extracellular forms of vaccinia virus. EMBO J. 15:2343-2355.
30. Saraste, J., U. Lahtinen, and B. Goud. 1995. Localization of the small GTP-binding protein rab1p to early compartments of the secretory pathway. J. Cell Sci. 108:1541-1552.
31. Schmelz, M., B. Sodeik, M. Ericsson, E. Wolffe, H. Shida, G. Hiller, and G. Griffiths. 1994. Assembly of vaccinia virus: the second wrapping cisterna is derived from the trans Golgi network. J. Virol. 68:130-147.
32. Singer, S. J. 1990. The structure and insertion of integral proteins in membranes. Annu. Rev. Cell Biol. 6:247-296.
33. Slot, J. W., H. J. Geuze, S. Gigengack, G. E. Lienhard, and D. E. James, 1991. Immuno-localization of the insulin regulatable glucose transporter in brown adipose tissue of the rate. J. Cell Biol. 113:123-135.
34. Sodeik, B., G. Griffiths, M. Ericsson, B. Moss, and R. W. Doms. 1994. Assembly of vaccinia virus: effects of rifampin on the intracellular distribution of viral protein p65. J. Virol. 68:1103-1114.
35. Sodeik, B., R. W. Doms, M. Ericsson, G. Hiller, C. E. Machamer, W. van't Hof, G. van Meer, B. Moss, and G. Griffiths. 1993. Assembly of vaccinia virus: role of the intermediate compartment between the endoplasmic reticulum and the Golgi stacks. J. Cell Biol. 121:521-541.
36. Sodeik, B., S. Cudmore, M. Ericsson, M. Esteban, E. G. Niles, and G. Griffiths. 1995. Incorporation of p14 and p32 into the membrane of the intracellular mature virus. J. Virol. 69:3560-3574.
37. Takahashi, T., M. Oie, and Y. Ichihashi. 1994. N-terminal amino acid sequences of vaccinia virus structural proteins. Virology 202:844-852.
38. Wolffe, E. J., D. M. Moore, P. J. Peers, and B. Moss. 1996. Vaccinia virus A17L open reading frame encodes an essential component of nascent viral membranes that is required to initiate morphogenesis. J. Virol. 70:2797-2808.