1887

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Volume 91, Issue 7

Vaccinia virus B5 protein affects the glycosylation, localization and stability of the A34 protein Open Access

Abstract

Vaccinia virus has two infectious forms, the intracellular mature virus, which has a single envelope, and the extracellular enveloped virus (EEV), which is surrounded by two lipid bilayers. The outer membrane of the EEV contains at least six viral proteins. Among them A34, a type II membrane glycoprotein, and B5, a type I membrane glycoprotein, form a complex and are involved in processes such as morphogenesis and EEV entry. A34 is required for normal incorporation of B5 into the EEV membrane. Here, we used a virus lacking B5 and viruses with mutations in the B5 membrane-proximal stalk region and looked at the effect of those modifications on A34. Data presented show that B5 is required for the correct glycosylation, trafficking and stability of A34, emphasizing the complex interactions and mutual dependence of these vaccinia EEV proteins.

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2010-07-01
2024-04-24
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References

  1. Blasco, R. & Moss, B.(1991). Extracellular vaccinia virus formation and cell-to-cell virus transmission are prevented by deletion of the gene encoding the 37,000-Dalton outer envelope protein. J Virol 65, 5910–5920. [Google Scholar]
  2. Blasco, R., Sisler, J. R. & Moss, B.(1993). Dissociation of progeny vaccinia virus from the cell membrane is regulated by a viral envelope glycoprotein: effect of a point mutation in the lectin homology domain of the A34R gene. J Virol 67, 3319–3325. [Google Scholar]
  3. Condit, R. C., Moussatche, N. & Traktman, P.(2006). In a nutshell: structure and assembly of the vaccinia virion. Adv Virus Res 66, 31–124. [Google Scholar]
  4. Dales, S. & Siminovitch, L.(1961). The development of vaccinia virus in Earle’s L strain cells as examined by electron microscopy. J Biophys Biochem Cytol 10, 475–503.[CrossRef] [Google Scholar]
  5. Duncan, S. A. & Smith, G. L.(1992). Identification and characterization of an extracellular envelope glycoprotein affecting vaccinia virus egress. J Virol 66, 1610–1621. [Google Scholar]
  6. Earley, A. K., Chan, W. M. & Ward, B. M.(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.[CrossRef] [Google Scholar]
  7. Engelstad, M. & Smith, G. L.(1993). The vaccinia virus 42-kDa envelope protein is required for the envelopment and egress of extracellular virus and for virus virulence. Virology 194, 627–637.[CrossRef] [Google Scholar]
  8. Engelstad, M., Howard, S. T. & Smith, G. L.(1992). A constitutively expressed vaccinia gene encodes a 42-kDa glycoprotein related to complement control factors that forms part of the extracellular virus envelope. Virology 188, 801–810.[CrossRef] [Google Scholar]
  9. Herrera, E., Lorenzo, M. M., Blasco, R. & Isaacs, S. N.(1998). Functional analysis of vaccinia virus B5R protein: essential role in virus envelopment is independent of a large portion of the extracellular domain. J Virol 72, 294–302. [Google Scholar]
  10. Hollinshead, M., Vanderplasschen, A., Smith, G. L. & Vaux, D. J.(1999). Vaccinia virus intracellular mature virions contain only one lipid membrane. J Virol 73, 1503–1517. [Google Scholar]
  11. Isaacs, S. N., Wolffe, E. J., Payne, L. G. & Moss, B.(1992). Characterization of a vaccinia virus-encoded 42-kilodalton class I membrane glycoprotein component of the extracellular virus envelope. J Virol 66, 7217–7224. [Google Scholar]
  12. Katz, E., Wolffe, E. J. & Moss, B.(1997). The cytoplasmic and transmembrane domains of the vaccinia virus B5R protein target a chimeric human immunodeficiency virus type 1 glycoprotein to the outer envelope of nascent vaccinia virions. J Virol 71, 3178–3187. [Google Scholar]
  13. Law, M., Putz, M. M. & Smith, G. L.(2005). An investigation of the therapeutic value of vaccinia-immune IgG in a mouse pneumonia model. J Gen Virol 86, 991–1000.[CrossRef] [Google Scholar]
  14. Law, M., Carter, G. C., Roberts, K. L., Hollinshead, M. & Smith, G. L.(2006). Ligand-induced and nonfusogenic dissolution of a viral membrane. Proc Natl Acad Sci U S A 103, 5989–5994.[CrossRef] [Google Scholar]
  15. Lorenzo, M. M., Herrera, E., Blasco, R. & Isaacs, S. N.(1998). Functional analysis of vaccinia virus B5R protein: role of the cytoplasmic tail. Virology 252, 450–457.[CrossRef] [Google Scholar]
  16. Lorenzo, M. M., Galindo, I., Griffiths, G. & Blasco, R.(2000). Intracellular localization of vaccinia virus extracellular enveloped virus envelope proteins individually expressed using a Semliki Forest virus replicon. J Virol 74, 10535–10550.[CrossRef] [Google Scholar]
  17. Mathew, E., Sanderson, C. M., Hollinshead, M. & Smith, G. L.(1998). The extracellular domain of vaccinia virus protein B5R affects plaque phenotype, extracellular enveloped virus release, and intracellular actin tail formation. J Virol 72, 2429–2438. [Google Scholar]
  18. Mathew, E. C., Sanderson, C. M., Hollinshead, R. & Smith, G. L.(2001). A mutational analysis of the vaccinia virus B5R protein. J Gen Virol 82, 1199–1213. [Google Scholar]
  19. McIntosh, A. A. & Smith, G. L.(1996). Vaccinia virus glycoprotein A34R is required for infectivity of extracellular enveloped virus. J Virol 70, 272–281. [Google Scholar]
  20. Olivari, S. & Molinari, M.(2007). Glycoprotein folding and the role of EDEM1, EDEM2 and EDEM3 in degradation of folding-defective glycoproteins. FEBS Lett 581, 3658–3664.[CrossRef] [Google Scholar]
  21. Parkinson, J. E. & Smith, G. L.(1994). Vaccinia virus gene A36R encodes a Mr 43–50 K protein on the surface of extracellular enveloped virus. Virology 204, 376–390.[CrossRef] [Google Scholar]
  22. Perdiguero, B., Lorenzo, M. M. & Blasco, R.(2008). Vaccinia virus A34 glycoprotein determines the protein composition of the extracellular virus envelope. J Virol 82, 2150–2160.[CrossRef] [Google Scholar]
  23. Pütz, M. M., Alberini, I., Midgley, C. M., Manini, I., Montomoli, E. & Smith, G. L.(2005). Prevalence of antibodies to vaccinia virus after smallpox vaccination in Italy. J Gen Virol 86, 2955–2960.[CrossRef] [Google Scholar]
  24. Roberts, K. L. & Smith, G. L.(2008). Vaccinia virus morphogenesis and dissemination. Trends Microbiol 16, 472–479.[CrossRef] [Google Scholar]
  25. Roberts, K. L., Breiman, A., Carter, G. C., Ewles, H. A., Hollinshead, M., Law, M. & Smith, G. L.(2009). Acidic residues in the membrane-proximal stalk region of vaccinia virus protein B5 are required for glycosaminoglycan-mediated disruption of the extracellular enveloped virus outer membrane. J Gen Virol 90, 1582–1591.[CrossRef] [Google Scholar]
  26. Roper, R. L., Payne, L. G. & Moss, B.(1996). Extracellular vaccinia virus envelope glycoprotein encoded by the A33R gene. J Virol 70, 3753–3762. [Google Scholar]
  27. Rottger, S., Frischknecht, F., Reckmann, I., Smith, G. L. & Way, M.(1999). Interactions between vaccinia virus IEV membrane proteins and their roles in IEV assembly and actin tail formation. J Virol 73, 2863–2875. [Google Scholar]
  28. Sanderson, C. M., Frischknecht, F., Way, M., Hollinshead, M. & Smith, G. L.(1998). Roles of vaccinia virus EEV-specific proteins in intracellular actin tail formation and low pH-induced cell-cell fusion. J Gen Virol 79, 1415–1425. [Google Scholar]
  29. Shida, H.(1986). Nucleotide sequence of the vaccinia virus hemagglutinin gene. Virology 150, 451–462.[CrossRef] [Google Scholar]
  30. Smith, G. L., Vanderplasschen, A. & Law, M.(2002). The formation and function of extracellular enveloped vaccinia virus. J Gen Virol 83, 2915–2931. [Google Scholar]
  31. Takahashi-Nishimaki, F., Funahashi, S., Miki, K., Hashizume, S. & Sugimoto, M.(1991). Regulation of plaque size and host range by a vaccinia virus gene related to complement system proteins. Virology 181, 158–164.[CrossRef] [Google Scholar]
  32. Turner, P. C. & Moyer, R. W.(2006). The cowpox virus fusion regulator proteins SPI-3 and hemagglutinin interact in infected and uninfected cells. Virology 347, 88–99.[CrossRef] [Google Scholar]
  33. Wagenaar, T. R. & Moss, B.(2007). Association of vaccinia virus fusion regulatory proteins with the multicomponent entry/fusion complex. J Virol 81, 6286–6293.[CrossRef] [Google Scholar]
  34. Ward, B. M. & Moss, B.(2000). Golgi network targeting and plasma membrane internalization signals in vaccinia virus B5R envelope protein. J Virol 74, 3771–3780.[CrossRef] [Google Scholar]
  35. Wolffe, E. J., Isaacs, S. N. & Moss, B.(1993). Deletion of the vaccinia virus B5R gene encoding a 42-kilodalton membrane glycoprotein inhibits extracellular virus envelope formation and dissemination. J Virol 67, 4732–4741. [Google Scholar]
  36. Wolffe, E. J., Katz, E., Weisberg, A. & Moss, B.(1997). The A34R glycoprotein gene is required for induction of specialized actin-containing microvilli and efficient cell-to-cell transmission of vaccinia virus. J Virol 71, 3904–3915. [Google Scholar]
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Vaccinia virus B5 protein affects the glycosylation, localization and stability of the A34 protein
J. Gen. Virol. 91, 1823 (2010); https://doi.org/10.1099/vir.0.020677-0
/content/journal/jgv/10.1099/vir.0.020677-0
/content/journal/jgv/10.1099/vir.0.020677-0
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