Sequence-independent targeting of transmembrane proteins synthesized within vaccinia virus factories to nascent viral membranes

Journal of Virology

Volumn 81, Issue 6, 2007, Pages 2646-2655

  Husain, Matloob ^a   Weisberg, Andrea S ^a   Moss, Bernard ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; MEMBRANE PROTEIN; VIRUS PROTEIN;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CYTOPLASM; ENDOPLASMIC RETICULUM; GOLGI COMPLEX; HUMAN; HUMAN CELL; NONHUMAN; POXVIRUS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; VACCINIA VIRUS; VIRUS ENVELOPE;

AMINO ACID SEQUENCE; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; FLUORESCENT DYES; HELA CELLS; HUMANS; IMMUNOPRECIPITATION; INDOLES; MEMBRANE PROTEINS; MICROSCOPY, CONFOCAL; MICROSCOPY, IMMUNOELECTRON; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; VACCINIA VIRUS; VIRAL MATRIX PROTEINS; VIRION;

BRYOPHYTA; POXVIRIDAE; VACCINIA VIRUS;

EID: 33947428809     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02631-06     Document Type: Article

References (38)

1. Carter, G. C., M. Law, M. Hollinshead, and G. L. Smith. 2005. Entry of the vaccinia virus intracellular mature virion and its interactions with glycosaminoglycans. J. Gen. Virol. 86:1279-1290.
2. Condit, R. C., N. Moussatche, and P. Traktman. 2006. In a nutshell: structure and assembly of the vaccinia virion. Adv. Virus Res. 66:31-124.
3. Cyrklaff, M., C. Risco, J. J. Fernandez, M. V. Jimenez, M. Esteban, W. Baumeister, and J. L. Carrascosa. 2005. Cryo-electron tomography of vaccinia virus. Proc. Natl. Acad. Sci. USA 102:2772-2777.
4. Dales, S., and E. H. Mosbach. 1968. Vaccinia as a model for membrane biogenesis. Virology 35:564-583.
5. Ericsson, M., B. Sodeik, J. K. Locker, and G. Griffiths. 1997. In vitro reconstitution of an intermediate assembly stage of vaccinia virus. Virology 235:218-227.
6. Griffiths, G., N. Roos, S. Schleich, and J. K. Locker. 2001. Structure and assembly of intracellular mature vaccinia virus: thin-section analyses. J. Virol. 75:11056-11070.
7. Grimley, P. M., E. N. Rosenblum, S. J. Mims, and B. Moss. 1970. Interruption by rifampin of an early stage in vaccinia virus morphogenesis: accumulation of membranes which are precursors of virus envelopes. J. Virol. 6:519-533.
8. Heuser, J. 2005. Deep-etch EM reveals that the early poxvirus envelope is a single membrane bilayer stabilized by a geodetic "honeycomb" surface coat. J. Cell Biol. 169:269-283.
9. Hoepfner, D., D. Schildknegt, I. Braakman, P. Philippsen, and H. F. Tabak. 2005. Contribution of the endoplasmic reticulum to peroxisome formation. Cell 122:85-95.
10. Hollinshead, M., A. Vanderplasschen, G. L. Smith, and D. J. Vaux. 1999. Vaccinia virus intracellular mature virions contain only one lipid membrane. J. Virol. 73:1503-1517.
11. Husain, M., and B. Moss. 2003. Evidence against an essential role of COPII-mediated cargo transport to the endoplasmic reticulum-Golgi intermediate compartment in the formation of the primary membrane of vaccinia virus. J. Virol. 77:11754-11766.
12. Husain, M., A. S. Weisberg, and B. Moss. 2006. Existence of an operative pathway from the endoplasmic reticulum to the immature poxvirus membrane. Proc. Natl. Acad. Sci. USA 103:19506-19511.
13. 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.
14. Law, M., G. C. Carter, K. L. Roberts, M. Hollinshead, and G. L. Smith. 2006. Ligand-induced and non-fusogenic dissolution of a viral membrane. Proc. Natl. Acad. Sci. USA 103:5989-5994.
15. Mercer, J., and P. Traktman. 2003. Investigation of structural and functional motifs within the vaccinia virus A14 phosphoprotein, an essential component of the virion membrane. J. Virol. 77:8857-8871.
16. Moss, B. 2006. Poxvirus entry and membrane fusion. Virology 344:48-54.
17. Nishimura, N., and W. E. Balch. 1997. A di-acidic signal required for selective export from the endoplasmic reticulum. Science 277:556-558.
18. Nishimura, N., S. Bannykh, S. Slabough, J. Matteson, Y. Altschuler, K. Hahn, and W. E. Balch. 1999. A di-acidic (DXE) code directs concentration of cargo during export from the endoplasmic reticulum. J. Biol. Chem. 274:15937-15946.
19. Resch, W., A. S. Weisberg, and B. Moss. 2005. Vaccinia virus nonstructural protein encoded by the A11R gene is required for formation of the virion membrane. J. Virol. 79:6598-6609.
20. Risco, C., J. R. Rodriguez, C. Lopez-Iglesias, J. L. Carrascosa, M. Esteban, and D. Rodriguez. 2002. Endoplasmic reticulum-Golgi intermediate compartment membranes and vimentin filaments participate in vaccinia virus assembly. J. Virol. 76:1839-1855.
21. 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.
22. Salmons, T., A. Kuhn, F. Wylie, S. Schleich, J. R. Rodriguez, D. Rodriguez, M. Estban, G. Griffiths, and J. K. Locker. 1997. Vaccinia virus membrane proteins p8 and p16 are cotranslationally inserted into the rough endoplasmic reticulum and retained in the intermediate compartment. J. Virol. 71: 7404-7420.
23. Schliebs, W., and W. H. Kunau. 2004. Peroxisome membrane biogenesis: the stage is set. Curr. Biol. 14:R397-R399.
24. Schmelz, M., B. Sodeik, M. Ericsson, E. J. 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.
25. Senkevich, T. G., S. Ojeda, A. Townsley, G. E. Nelson, and B. Moss. 2005. Poxvirus multiprotein entry-fusion complex. Proc. Natl. Acad. Sci. USA 102:18572-18577.
26. Sevier, C. S., O. A. Weisz, M. Davis, and C. E. Machamer. 2000. Efficient export of the vesicular stomatitis virus G protein from the endoplasmic reticulum requires a signal in the cytoplasmic tail that includes both tyrosine-based and di-acidic motifs. Mol. Biol. Cell 11:13-22.
27. Smith, G. L., A. Vanderplasschen, and M. Law. 2002. The formation and function of extracellular enveloped vaccinia virus. J. Gen. Virol. 83:2915-2931.
28. Sodeik, B., S. Cudmore, M. Ericsson, M. Esteban, E. G. Niles, and G. Griffiths. 1995. Assembly of vaccinia virus: incorporation of p14 and p32 into the membrane of the intracellular mature virus. J. Virol. 69:3560-3574.
29. 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.
30. 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.
31. South, S. T., K. A. Sacksteder, X. Li, Y. Liu, and S. J. Gould. 2000. Inhibitors of COPI and COPII do not block PEX3-mediated peroxisome synthesis. J. Cell Biol. 149:1345-1360.
32. Subramani, S. 1998. Components involved in peroxisome import, biogenesis, proliferation, turnover, and movement. Physiol. Rev. 78:171-188.
33. Szajner, P., A. S. Weisberg, J. Lebowitz, J. Heuser, and B. Moss. 2005. External scaffold of spherical immature poxvirus particles is made of protein trimers, forming a honeycomb lattice. J. Cell Biol. 170:971-981.
34. Tabak, H. F., J. L. Murk, I. Braakman, and H. J. Geuze. 2003. Peroxisomes start their life in the endoplasmic reticulum. Traffic 4:512-518.
35. Townsley, A. C., A. S. Weisberg, T. R. Wagenaar, and B. Moss. 2006. Vaccinia virus entry into cells via a low pH-dependent-endosomal pathway. J. Virol. 80:8899-8908.
36. Ward, B. M., and B. Moss. 2000. Golgi network targeting and plasma membrane internalization signals in vaccinia virus B5R envelope protein. J. Virol. 74:3771-3780.
37. Wolffe, E. J., D. M. Moore, P. J. Peters, 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.
38. Yeh, W. W., B. Moss, and E. J. Wolffe. 2000. The vaccinia virus A9L gene encodes a membrane protein required for an early step in virion morphogenesis. J. Virol. 74:9701-9711.