Vaccinia virus H7 protein contributes to the formation of crescent membrane precursors of immature virions

Journal of Virology

Volumn 83, Issue 17, 2009, Pages 8439-8450

  Satheshkumar, P S ^a   Weisberg, Andrea ^a   Moss, Bernard ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

CORE PROTEIN; ISOPROPYL THIOGALACTOSIDE; MUTANT PROTEIN; PROTEINASE; SCAFFOLD PROTEIN; UNCLASSIFIED DRUG; VACCINIA VIRUS H7 PROTEIN; VIRUS DNA; VIRUS PROTEIN; MATRIX PROTEIN;

ANIMAL CELL; ARTICLE; CELL DENSITY; CELL INCLUSION; CELL ORGANELLE; CONTROLLED STUDY; CYTOPLASM; DNA REPLICATION; ELECTRON; ENDOPLASMIC RETICULUM; LETHAL GENE; MEMBRANE STRUCTURE; NONHUMAN; PHENOTYPE; POXVIRUS; POXVIRUS INFECTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN SYNTHESIS; TRANSMISSION ELECTRON MICROSCOPY; VACCINIA VIRUS; VIRION; VIROGENESIS; VIRUS DETECTION; VIRUS ENVELOPE; VIRUS INFECTIVITY; VIRUS MORPHOGENESIS; AMINO ACID SEQUENCE; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; SEQUENCE ALIGNMENT; ULTRASTRUCTURE; VIRUS ASSEMBLY; VIRUS CULTURE; VIRUS INCLUSION;

POXVIRIDAE; VACCINIA VIRUS; VERTEBRATA;

AMINO ACID SEQUENCE; CYTOPLASM; INCLUSION BODIES, VIRAL; MICROSCOPY, ELECTRON, TRANSMISSION; MOLECULAR SEQUENCE DATA; PLAQUE ASSAY; SEQUENCE ALIGNMENT; VACCINIA VIRUS; VIRAL MATRIX PROTEINS; VIRION; VIRUS ASSEMBLY;

EID: 69249211161     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00877-09     Document Type: Article

References (44)

1. Alexander, W. A., B. Moss, and T. R. Fuerst. 1992. Regulated expression of foreign genes in vaccinia virus under the control of bacteriophage T7 RNA polymerase and the Escherichia coli lac repressor. J. Virol. 66:2934-2942.
2. Ansarah-Sobrinho, C., and B. Moss. 2004. Role of the I7 protein in proteolytic processing of vaccinia virus membrane and core components. J. Virol. 78:6335-6343. (Pubitemid 38715932)
3. Betakova, T., E. J. Wolffe, and B. Moss. 1999. Regulation of vaccinia virus morphogenesis: phosphorylation of the A14L and A17L membrane proteins and C-terminal truncation of the A17L protein are dependent on the F10L protein kinase. J. Virol. 73:3534-3543. (Pubitemid 29189791)
4. Black, E. P., N. Moussatche, and R. C. Condit. 1998. Characterization of the interactions among vaccinia virus transcription factors G2R, A18R, and H5R. Virology 245:313-322.
5. Chichon, F. J., M. J. Rodriguez, C. Risco, A. Fraile-Ramos, J. J. Fernandez, M. Esteban, and J. L. Carrascosa. 2009. Membrane remodeling during vaccinia virus morphogenesis. Biol. Cell 101:401-414.
6. 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.
7. Da Fonseca, F. G., A. S. Weisberg, M. F. Caeiro, and B. Moss. 2004. Vaccinia virus mutants with alanine substitutions in the conserved G5R gene fail to initiate morphogenesis at the nonpermissive temperature. J. Virol. 78:10238-10248.
8. Dales, S. 1963. The uptake and development of vaccinia virus in strain L cells followed with labeled viral deoxyribonucleic acid. J. Cell Biol. 18:51-72.
9. Dales, S., and E. H. Mosbach. 1968. Vaccinia as a model for membrane biogenesis. Virology 35:564-583.
10. Dales, S., and L. Siminovitch. 1961. The development of vaccinia virus in Earle's L strain cells as examined by electron microscopy. J. Biophys. Biochem. Cytol. 10:475-503.
11. D'Costa, S. M., T. W. Bainbridge, and R. C. Condit. 2008. Purification and properties of the vaccinia virus mRNA processing factor. J. Biol. Chem. 283:5267-5275.
12. DeMasi, J., and P. Traktman. 2000. Clustered charge-to-alanine mutagenesis of the vaccinia virus H5 gene: isolation of a dominant, temperature-sensitive mutant with a profound defect in morphogenesis. J. Virol. 74:2393-2405.
13. Derrien, M., A. Punjabi, R. Khanna, O. Grubisha, and P. Traktman. 1999. Tyrosine phosphorylation of A17 during vaccinia virus infection: involvement of the H1 phosphatase and the F10 kinase. J. Virol. 73:7287-7296. (Pubitemid 29383211)
14. Earl, P. L., N. Cooper, L. S. Wyatt, B. Moss, and M. W. Carroll. 1998. Preparation of cell cultures and vaccinia virus stocks, p. 16.16.1-16.16.3. In F. M. Ausubel, R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl (ed.), Current protocols in molecular biology, vol.2. John Wiley and Sons, New York, NY.
15. Earl, P. L., and B. Moss. 1998. Characterization of recombinant vaccinia viruses and their products, p. 16.18.1-16.18.11. In F. M. Ausubel, R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl (ed.), Current protocols in molecular biology, vol.2. Wiley Interscience, New York, NY.
16. Earl, P. L., B. Moss, L. S. Wyatt, and M. W. Carroll. 1998. Generation of recombinant vaccinia viruses, p. 16.17.1-16.17.19. In F. M. Ausubel, R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl (ed.), Current protocols in molecular biology, vol.2. Wiley Interscience, New York, NY.
17. 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.
18. 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.
19. 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. (Pubitemid 29036806)
20. 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. (Pubitemid 37271673)
21. 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.
22. Kovacs, G. R., and B. Moss. 1996. The vaccinia virus H5R gene encodes late gene transcription factor 4: purification, cloning and overexpression. J. Virol. 70:6796-6802.
23. 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. (Pubitemid 36936097)
24. Mohandas, A. R., and S. Dales. 1995. Involvement of spicules in the formation of vaccinia virus envelopes elucidated by a conditional lethal mutant. Virology 214:494-502.
25. Moss, B. 2007. Poxviridae: the viruses and their replication, p. 2905-2946. 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, 5th ed., vol.2. Lippincott Williams & Wilkins, Philadelphia, PA.
26. Moss, B., E. N. Rosenblum, E. Katz, and P. M. Grimley. 1969. Rifampicin: a specific inhibitor of vaccinia virus assembly. Nature 224:1280-1284.
27. Nelson, G. E., J. R. Sisler, D. Chandran, and B. Moss. 2008. Vaccinia virus entry/fusion complex subunit A28 is a target of neutralizing and protective antibodies. Virology 380:394-401.
28. 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. (Pubitemid 40677291)
29. 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. (Pubitemid 34094631)
30. Rodríguez, D., M. Esteban, and J. R. Rodríguez. 1995. Vaccinia virus A17L gene product is essential for an early step in virion morphogenesis. J. Virol. 69:4640-4648.
31. Rodriguez, J. R., C. Risco, J. L. Carrascosa, M. Esteban, and D. Rodriguez. 1998. Vaccinia virus 15-kilodalton (A14L) protein is essential for assembly and attachment of viral crescents to virosomes. J. Virol. 72:1287-1296.
32. Senkevich, T. G., L. S. Wyatt, A. S. Weisberg, E. V. Koonin, and B. Moss. 2008. A conserved poxvirus NlpC/P60 superfamily protein contributes to vaccinia virus virulence in mice but not to replication in cell culture. Virology 374:506-514.
33. 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.
34. Sodeik, B., and J. Krijnse-Locker. 2002. Assembly of vaccinia virus revisited: de novo membrane synthesis or acquisition from the host? Trends Microbiol. 10:15-24.
35. Sood, C. L., J. M. Ward, and B. Moss. 2008. Vaccinia virus encodes a small hydrophobic virion membrane protein (I5) that enhances replication and virulence in mice. J. Virol. 82:10071-10078.
36. 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. (Pubitemid 41306296)
37. Szajner, P., A. S. Weisberg, and B. Moss. 2004. Evidence for an essential catalytic role of the F10 protein kinase in vaccinia virus morphogenesis. J. Virol. 78:257-265. (Pubitemid 37549738)
38. Traktman, P., A. Caligiuri, S. A. Jesty, and U. Sankar. 1995. Temperature-sensitive mutants with lesions in the vaccinia virus F10 kinase undergo arrest at the earliest stage of morphogenesis. J. Virol. 69:6581-6587.
39. Traktman, P., K. Liu, J. DeMasi, R. Rollins, S. Jesty, and B. Unger. 2000. Elucidating the essential role of the A14 phosphoprotein in vaccinia virus morphogenesis: construction and characterization of a tetracycline-inducible recombinant. J. Virol. 74:3682-3695. (Pubitemid 30180312)
40. Upton, C., S. Slack, A. L. Hunter, A. Ehlers, and R. L. Roper. 2003. Poxvirus orthologous clusters: toward defining the minimum essential poxvirus genome. J. Virol. 77:7590-7600. (Pubitemid 36734529)
41. 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.
42. 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.
43. Zhang, L. L., S. Y. Lee, G. V. Beznoussenko, P. J. Peters, J. S. Yang, H. Y. Gilbert, A. L. Brass, S. J. Elledge, S. N. Isaacs, B. Moss, A. Mironov, and V. W. Hsu. 2009. A role for the host coatomer and KDEL receptor in early vaccinia biogenesis. Proc. Natl. Acad. Sci. USA 106:163-168.
44. Zhang, Y., and B. Moss. 1992. Immature viral envelope formation is interrupted at the same stage by lac operator-mediated repression of the vaccinia virus D13L gene and by the drug rifampicin. Virology 187:643-653.