1887

Abstract

Orf virus (ORFV) is the type species of the genus , but little is known about the structure or morphogenesis of the virus. In contrast, the structure and morphogenesis of vaccinia virus (VACV) has been extensively studied. VACV has two main infectious forms, mature virion (MV) and extracellular virion (EV). The MV is wrapped by two additional membranes derived from the -Golgi to produce a wrapped virion (WV), the outermost of which is lost by cellular membrane fusion during viral egress to form the EV. Genome sequencing of ORFV has revealed that it has homologues of almost all of the VACV structural genes. Notable exceptions are A36R, K2L, A56R and B5R, which are associated with WV and EV envelopes. This study investigated the morphogenesis and structure of ORFV by fusing FLAG peptide to the structural proteins 10 kDa, F1L and ORF-110 to form recombinant viruses. 10 kDa and F1L are homologues of VACV A27L and H3L MV membrane proteins, whilst ORF-110 is homologous to VACV A34R, an EV membrane protein. Immunogold labelling of FLAG proteins on virus particles isolated from lysed cells showed that FLAG–F1L and FLAG–10 kDa were displayed on the surface of infectious particles, whereas ORF-110–FLAG could not be detected. Western blot analysis of solubilized recombinant ORF-110–FLAG particles revealed that ORF-110–FLAG was abundant and undergoes post-translational modification indicative of endoplasmic reticulum trafficking. Fluorescent microscopy confirmed the prediction that ORF-110–FLAG localized to the Golgi in virus-infected cells. Finally, immunogold labelling of EVs showed that ORF-110–FLAG became exposed on the surface of EV-like particles as a result of egress from the cell.

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2009-03-01
2024-03-29
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References

  1. Balassu T. C., Robinson A. J. 1987; Orf virus replication in bovine testis cells: kinetics of viral DNA, polypeptide, and infectious virus production and analysis of virion polypeptides. Arch Virol 97:267–281 [CrossRef]
    [Google Scholar]
  2. 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]
  3. Boulanger D., Green P., Jones B., Henriquet G., Hunt L. G., Laidlaw S. M., Monaghan P., Skinner M. A. 2002; Identification and characterization of three immunodominant structural proteins of fowlpox virus. J Virol 76:9844–9855 [CrossRef]
    [Google Scholar]
  4. Collado M., Rodriguez D., Rodriguez J. R., Vazquez I., Gonzalo R. M., Esteban M. 2000; Chimeras between the human immunodeficiency virus (HIV-1) Env and vaccinia virus immunogenic proteins p14 and p39 generate in mice broadly reactive antibodies and specific activation of CD8+ T cell responses to Env. Vaccine 18:3123–3133 [CrossRef]
    [Google Scholar]
  5. 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]
  6. Czerny C. P., Waldmann R., Scheubeck T. 1997; Identification of three distinct antigenic sites in parapoxviruses. Arch Virol 142:807–821 [CrossRef]
    [Google Scholar]
  7. da Fonseca F. G., Wolffe E. J., 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 [CrossRef]
    [Google Scholar]
  8. Delhon G., Tulman E. R., Afonso C. L., Lu Z., de la Concha-Bermejillo A., Lehmkuhl H. D., Piccone M. E., Kutish G. F., Rock D. L. 2004; Genomes of the parapoxviruses orf virus and bovine papular stomatitis virus. J Virol 78:168–177 [CrossRef]
    [Google Scholar]
  9. Easterbrook K. B. 1966; Controlled degradation of vaccinia virions in vitro: an electron microscopic study. J Ultrastruct Res 14:484–496 [CrossRef]
    [Google Scholar]
  10. Fleming S. B., McCaughan C. A., Andrews A. E., Nash A. D., Mercer A. A. 1997; A homologue of interleukin-10 is encoded by the poxvirus orf virus. J Virol 71:4857–4861
    [Google Scholar]
  11. Frischknecht F., Moreau V., Röttger S., Gonfloni S., Reckmann I., Superti-Furga G., Way M. 1999; Actin based motility of vaccinia virus mimics receptor tyrosine kinase signalling. Nature 401:926–929 [CrossRef]
    [Google Scholar]
  12. Hammond J. M., Oke P. G., Coupar B. E. 1997; A synthetic vaccinia virus promoter with enhanced early and late activity. J Virol Methods 66:135–138 [CrossRef]
    [Google Scholar]
  13. Hiller G., Weber K. 1985; Golgi-derived membranes that contain an acylated viral polypeptide are used for vaccinia virus envelopment. J Virol 55:651–659
    [Google Scholar]
  14. Hiramatsu Y., Uno F., Yoshida M., Hatano Y., Nii S. 1999; Poxvirus virions: their surface ultrastructure and interaction with the surface membrane of host cells. J Electron Microsc (Tokyo 48:937–946 [CrossRef]
    [Google Scholar]
  15. Housawi F. M., Roberts G. M., Gilray J. A., Pow I., Reid H. W., Nettleton P. F., Sumption K. J., Hibma M. H., Mercer A. A. 1998; The reactivity of monoclonal antibodies against orf virus with other parapoxviruses and the identification of a 39 kDa immunodominant protein. Arch Virol 143:2289–2303 [CrossRef]
    [Google Scholar]
  16. Hsiao J. C., Chung C. S., Chang W. 1998; Cell surface proteoglycans are necessary for A27L protein-mediated cell fusion: identification of the N-terminal region of A27L protein as the glycosaminoglycan-binding domain. J Virol 72:8374–8379
    [Google Scholar]
  17. Husain M., Moss B. 2001; Vaccinia virus F13L protein with a conserved phospholipase catalytic motif induces colocalization of the B5R envelope glycoprotein in post-Golgi vesicles. J Virol 75:7528–7542 [CrossRef]
    [Google Scholar]
  18. Jefferson R. A. 1989; The GUS reporter gene system. Nature 342:837–838 [CrossRef]
    [Google Scholar]
  19. Katz E., Moss B. 1997; Immunogenicity of recombinant vaccinia viruses that display the HIV type 1 envelope glycoprotein on the surface of infectious virions. AIDS Res Hum Retroviruses 13:1497–1500 [CrossRef]
    [Google Scholar]
  20. Krauss O., Hollinshead R., Hollinshead M., Smith G. L. 2002; An investigation of incorporation of cellular antigens into vaccinia virus particles. J Gen Virol 83:2347–2359
    [Google Scholar]
  21. Laemmli U. K. 1970; Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685 [CrossRef]
    [Google Scholar]
  22. 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]
  23. Lin C. L., Chung C. S., Heine H. G., Chang W. 2000; Vaccinia virus envelope H3L protein binds to cell surface heparan sulfate and is important for intracellular mature virion morphogenesis and virus infection in vitro and in vivo. J Virol 74:3353–3365 [CrossRef]
    [Google Scholar]
  24. Loewinger M., Katz E. 2002; Ultraviolet-irradiated vaccinia virus recombinants, exposing HIV-envelope on their outer membrane, induce antibodies against this antigen in rabbits. Viral Immunol 15:473–479 [CrossRef]
    [Google Scholar]
  25. 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]
  26. 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]
  27. Mercer A. A., Fraser K., Barns G., Robinson A. J. 1987; The structure and cloning of orf virus DNA. Virology 157:1–12 [CrossRef]
    [Google Scholar]
  28. Mercer A., Fleming S., Robinson A., Nettleton P., Reid H. 1997; Molecular genetic analyses of parapoxviruses pathogenic for humans. Arch Virol Suppl 13:25–34
    [Google Scholar]
  29. Mercer A. A., Ueda N., Friederichs S. M., Hofmann K., Fraser K. M., Bateman T., Fleming S. B. 2006; Comparative analysis of genome sequences of three isolates of Orf virus reveals unexpected sequence variation. Virus Res 116:146–158 [CrossRef]
    [Google Scholar]
  30. Mitchiner M. B. 1969; The envelope of vaccinia and orf viruses: an electron cytochemical investigation. J Gen Virol 5:211–220 [CrossRef]
    [Google Scholar]
  31. Naase M., Nicholson B. H., Fraser K. M., Mercer A. A., Robinson A. J. 1991; An orf virus sequence showing homology to the ‘fusion’ protein gene of vaccinia virus. J Gen Virol 72:1177–1181 [CrossRef]
    [Google Scholar]
  32. Nagington J., Newton A. J., Horne R. W. 1962; Morphological studies of orf and vaccinia viruses. Virology 16:248–260 [CrossRef]
    [Google Scholar]
  33. Robinson A. J., Ellis G., Ballasu T. 1982; The genome of orf virus: restriction endonuclease analysis of viral DNA isolated from lesions of orf virus in sheep. Arch Virol 71:43–55 [CrossRef]
    [Google Scholar]
  34. Rosel J. L., Earl P. L., Weir J. P., Moss B. 1986; Conserved TAAATG sequence at the transcriptional and translational initiation sites of vaccinia virus late genes deduced by structural and functional analysis of the Hin dIII H genome fragment. J Virol 60:436–449
    [Google Scholar]
  35. Röttger 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]
  36. Savory L. J., Stacker S. A., Fleming S. B., Niven B. E., Mercer A. A. 2000; Viral vascular endothelial growth factor plays a critical role in orf virus infection. J Virol 74:10699–10706 [CrossRef]
    [Google Scholar]
  37. Scagliarini A., Ciulli S., Battilani M., Jacoboni I., Montesi F., Casadio R., Prosperi S. 2002; Characterisation of immunodominant protein encoded by the F1L gene of orf virus strains isolated in Italy. Arch Virol 147:1989–1995 [CrossRef]
    [Google Scholar]
  38. Scagliarini A., Gallina L., Dal Pozzo F., Battilani M., Ciulli S., Prosperi S. 2004; Heparin binding activity of orf virus F1L protein. Virus Res 105:107–112 [CrossRef]
    [Google Scholar]
  39. Schmelz M., Sodeik B., Ericsson M., Wolffe E. J., Shida H., Hiller G., Griffiths G. 1994; Assembly of vaccinia virus: the second wrapping cisterna is derived from the trans Golgi network. J Virol 68:130–147
    [Google Scholar]
  40. Smith G. L., Law M. 2004; The exit of vaccinia virus from infected cells. Virus Res 106:189–197 [CrossRef]
    [Google Scholar]
  41. 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]
  42. Spehner D., De Carlo S., Drillien R., Weiland F., Mildner K., Hanau D., Rziha H. J. 2004; Appearance of the bona fide spiral tubule of orf virus is dependent on an intact 10-kilodalton viral protein. J Virol 78:8085–8093 [CrossRef]
    [Google Scholar]
  43. Takahashi T., Oie M., Ichihashi Y. 1994; N-terminal amino acid sequences of vaccinia virus structural proteins. Virology 202:844–852 [CrossRef]
    [Google Scholar]
  44. Vazquez M. I., Rivas G., Cregut D., Serrano L., Esteban M. 1998; The vaccinia virus 14-kilodalton (A27L) fusion protein forms a triple coiled-coil structure and interacts with the 21-kilodalton (A17L) virus membrane protein through a C-terminal α -helix. J Virol 72:10126–10137
    [Google Scholar]
  45. Wagenaar T. R., Ojeda S., Moss B. 2008; Vaccinia virus A56/K2 fusion regulatory protein interacts with the A16 and G9 subunits of the entry fusion complex. J Virol 82:5153–5160 [CrossRef]
    [Google Scholar]
  46. Ward B. M., Moss B. 2001a; Vaccinia virus intracellular movement is associated with microtubules and independent of actin tails. J Virol 75:11651–11663 [CrossRef]
    [Google Scholar]
  47. Ward B. M., Moss B. 2001b; Visualization of intracellular movement of vaccinia virus virions containing a green fluorescent protein–B5R membrane protein chimera. J Virol 75:4802–4813 [CrossRef]
    [Google Scholar]
  48. 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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