Vaccinia virus A6 is essential for virion membrane biogenesis and localization of virion membrane proteins to sites of virion assembly

Journal of Virology

Volumn 86, Issue 10, 2012, Pages 5603-5613

  Meng, Xiangzhi ^a   Embry, Addie ^a   Rose, Lloyd ^a   Yan, Bo ^a   Xu, Chungui ^a   Xiang, Yan ^a  

^a UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS PROTEIN;

A6L GENE; ARTICLE; CELLULAR DISTRIBUTION; GENE EXPRESSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN SYNTHESIS; VACCINIA VIRUS; VIRION; VIRUS ASSEMBLY; VIRUS ENVELOPE; VIRUS GENE;

CELL MEMBRANE; HUMANS; PROTEIN TRANSPORT; VACCINIA; VACCINIA VIRUS; VIRAL CORE PROTEINS; VIRAL ENVELOPE PROTEINS; VIRION; VIRUS ASSEMBLY;

POXVIRIDAE; VACCINIA VIRUS;

EID: 84861312428     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00330-12     Document Type: Article

References (49)

1. Chung CS, et al. 2006. Vaccinia virus proteome: identification of proteins in vaccinia virus intracellular mature virion particles. J. Virol. 80:2127-2140.
2. Condit RC, Moussatche N, Traktman P. 2006. In a nutshell: structure and assembly of the vaccinia virion. Adv. Virus Res. 66:31-124.
3. da Fonseca FG, Weisberg AS, Caeiro MF, Moss B. 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.
4. da Fonseca FG, Wolffe EJ, Weisberg A, Moss B. 2000. Characterization of the vaccinia virus H3L envelope protein: topology and posttranslational membrane insertion via the C-terminal hydrophobic tail. J. Virol. 74: 7508-7517.
5. Dales S, Mosbach EH. 1968. Vaccinia as a model for membrane biogenesis. Virology 35:564 -583.
6. D'Costa SM, et al. 2010. Vaccinia H5 is a multifunctional protein involved in viral DNA replication, postreplicative gene transcription, and virion morphogenesis. Virology 401:49-60.
7. DeMasi J, Traktman P. 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.
8. Earl PL, Moss B, Wyatt LS, Carroll MW. 2001. Generation of recombinant vaccinia viruses. Curr. Protoc. Mol. Biol. Chapter 16:Unit16.17.
9. Earley AK, Chan WM, Ward BM. 2008. The vaccinia virus B5 protein requires A34 for efficient intracellular trafficking from the endoplasmic reticulum to the site of wrapping and incorporation into progeny virions. J. Virol. 82:2161-2169.
10. Garcia AD, Moss B. 2001. Repression of vaccinia virus Holliday junction resolvase inhibits processing of viral DNA into unit-length genomes. J. Virol. 75:6460-6471.
11. 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.
12. Husain M, Moss B. 2003. Evidence against an essential role of COPIImediated cargo transport to the endoplasmic reticulum-Golgi intermediate compartment in the formation of the primary membrane of vaccinia virus. J. Virol. 77:11754 -11766.
13. Husain M, Weisberg AS, Moss B. 2006. Existence of an operative pathway from the endoplasmic reticulum to the immature poxvirus membrane. Proc. Natl. Acad. Sci. U. S. A. 103:19506 -19511.
14. Husain M, Weisberg AS, Moss B. 2007. Sequence-independent targeting of transmembrane proteins synthesized within vaccinia virus factories to nascent viral membranes. J. Virol. 81:2646 -2655.
15. Ishii K, Moss B. 2001. Role of vaccinia virus A20R protein in DNA replication: construction and characterization of temperature-sensitive mutants. J. Virol. 75:1656 -1663.
16. Katsafanas GC, Moss B. 2007. Colocalization of transcription and translation within cytoplasmic poxvirus factories coordinates viral expression and subjugates host functions. Cell Host Microbe 2:221-228.
17. Katz E, Moss B. 1970. Formation of a vaccinia virus structural polypeptide from a higher molecular weight precursor: inhibition by rifampicin. Proc. Natl. Acad. Sci. U. S. A. 66:677-684.
18. Klemperer N, Ward J, Evans E, Traktman P. 1997. The vaccinia virus I1 protein is essential for the assembly of mature virions. J. Virol. 71:9285-9294.
19. Kovacs GR, Moss B. 1996. The vaccinia virus H5R gene encodes late gene transcription factor 4: purification, cloning, and overexpression. J. Virol. 70:6796-6802.
20. Lin S, Broyles SS. 1994. Vaccinia protein kinase 2: a second essential serine/threonine protein kinase encoded by vaccinia virus. Proc. Natl. Acad. Sci. U. S. A. 91:7653-7657.
21. Maruri-Avidal L, Domi A, Weisberg AS, Moss B. 2011. Participation of vaccinia virus l2 protein in the formation of crescent membranes and immature virions. J. Virol. 85:2504 -2511.
22. Maruri-Avidal L, Weisberg AS, Moss B. 2011. Vaccinia virus L2 protein associates with the endoplasmic reticulum near the growing edge of crescent precursors of immature virions and stabilizes a subset of viral membrane proteins. J. Virol. 85:12431-12441.
23. McCausland MM, et al. 2010. Combination therapy of vaccinia virus infection with human anti-H3 and anti-B5 monoclonal antibodies in a small animal model. Antivir. Ther. 15:661-675.
24. Meng X, Embry A, Sochia D, Xiang Y. 2007. Vaccinia virus A6L encodes a virion core protein required for formation of mature virion. J. Virol. 81:1433-1443.
25. Meng X, Xiang Y. 2006. Vaccinia virus K1L protein supports viral replication in human and rabbit cells through a cell-type-specific set of its ankyrin repeat residues that are distinct from its binding site for ACAP2. Virology 353:220 -233.
26. Meng X, et al. 2011. Generation and characterization of a large panel of murine monoclonal antibodies against vaccinia virus. Virology 409:271-279.
27. Mercer J, Traktman P. 2005. Genetic and cell biological characterization of the vaccinia virus A30 and G7 phosphoproteins. J. Virol. 79:7146 -7161.
28. Mercer J, Traktman P. 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.
29. Moss B. 2007. Poxviridae: the viruses and their replication, p 2905-2946. In Knipe DM, et al (ed), Fields virology, vol 2. Lippincott Williams & Wilkins, Philadelphia, PA.
30. Punjabi A, Traktman P. 2005. Cell biological and functional characterization of the vaccinia virus F10 kinase: implications for the mechanism of virion morphogenesis. J. Virol. 79:2171-2190.
31. Resch W, Hixson KK, Moore RJ, Lipton MS, Moss B. 2007. Protein composition of the vaccinia virus mature virion. Virology 358:233-247.
32. Resch W, Weisberg AS, Moss B. 2005. Vaccinia virus nonstructural protein encoded by the A11R gene is required for formation of the virion membrane. J. Virol. 79:6598-6609.
33. Risco C, et al. 2002. Endoplasmic reticulum-Golgi intermediate compartment membranes and vimentin filaments participate in vaccinia virus assembly. J. Virol. 76:1839 -1855.
34. Rodriguez JR, Risco C, Carrascosa JL, Esteban M, Rodriguez D. 1997. Characterization of early stages in vaccinia virus membrane biogenesis: implications of the 21-kilodalton protein and a newly identified 15-kilodalton envelope protein. J. Virol. 71:1821-1833.
35. Rodriguez JR, Risco C, Carrascosa JL, Esteban M, Rodriguez D. 1998. Vaccinia virus 15-kilodalton (A14L) protein is essential for assembly and attachment of viral crescents to virosomes. J. Virol. 72:1287-1296.
36. Rosel J, Moss B. 1985. Transcriptional and translational mapping and nucleotide sequence analysis of a vaccinia virus gene encoding the precursor of the major core polypeptide 4b. J. Virol. 56:830-838.
37. Salmons T, et al. 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.
38. Satheshkumar PS, Weisberg A, Moss B. 2009. Vaccinia virus H7 protein contributes to the formation of crescent membrane precursors of immature virions. J. Virol. 83:8439-8450.
39. Senkevich TG, Koonin EV, Moss B. 2009. Predicted poxvirus FEN1-like nuclease required for homologous recombination, double-strand break repair and full-size genome formation. Proc. Natl. Acad. Sci. U. S. A. 106:17921-17926.
40. Sodeik B, et al. 1993. Assembly of vaccinia virus: role of the intermediate compartment between the endoplasmic reticulum and the Golgi stacks. J. Cell Biol. 121:521-541.
41. Szajner P, Weisberg AS, Lebowitz J, Heuser J, Moss B. 2005. External scaffold of spherical immature poxvirus particles is made of protein trimers, forming a honeycomb lattice. J. Cell Biol. 170:971-981.
42. Szajner P, Weisberg AS, Moss B. 2004. Evidence for an essential catalytic role of the F10 protein kinase in vaccinia virus morphogenesis. J. Virol. 78:257-265.
43. Traktman P, Caligiuri A, Jesty SA, Liu K, Sankar U. 1995. Temperature-sensitive mutants with lesions in the vaccinia virus F10 kinase undergo arrest at the earliest stage of virion morphogenesis. J. Virol. 69:6581-6587.
44. Traktman P, et al. 2000. Elucidating the essential role of the A14 phos-phoprotein in vaccinia virus morphogenesis: construction and characterization of a tetracycline-inducible recombinant. J. Virol. 74:3682-3695.
45. Ulaeto D, Grosenbach D, Hruby DE. 1995. Brefeldin A inhibits vaccinia virus envelopment but does not prevent normal processing and localization of the putative envelopment receptor P37. J. Gen. Virol. 76:103-111.
46. Ward G, Stover C, Moss B, Fuerst T. 1995. Stringent chemical and thermal regulation of recombinant gene expression by vaccinia virus vectors in mammalian cells. Proc. Natl. Acad. Sci. U. S. A. 92:6773-6777.
47. Wolffe EJ, Moore DM, Peters PJ, Moss B. 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.
48. Xu C, et al. 2011. An epitope conserved in orthopoxvirus A13 envelope protein is the target of neutralizing and protective antibodies. Virology 418:67-73.
49. Zachertowska A, Brewer D, Evans DH. 2006. Characterization of the major capsid proteins of myxoma virus particles using MALDI-TOF mass spectrometry. J. Virol. Methods 132:1-12.