1887

Abstract

Release of fowlpox virus (FWPV) as extracellular enveloped virus (EEV) appears to proceed both by the budding of intracellular mature virus (IMV) through the plasma membrane and by the fusion of intracellular enveloped virus (IEV) with the plasma membrane. Based on the frequency of budding events compared to wrapping events observed by electron microscopy, FWPV FP9 strain seems to exit chick embryo fibroblast cells predominantly by budding. In contrast to vaccinia virus (VV), the production of FWPV extracellular virus particles is not affected by -isonicotinoyl- -3-methyl-4-chlorobenzoylhydrazine (IMCBH). Comparison of the sequence of the VV F13L gene product with its FWPV orthologue showed a mutation, in the fowlpox protein, at the residue involved in IMCBH resistance in a mutant VV. Glucosamine, monensin or brefeldin A did not have any specific effect on FWPV extracellular virus production. Cytochalasin D, which inhibits the formation of actin filaments, reduces the production of extracellular virus particles by inhibiting the release of cell-associated enveloped virus (CEV) particles from the plasma membrane. Involvement of actin filaments in this mechanism is further supported by the co-localization of actin with viral particles close to the plasma membrane in the absence of cytochalasin D. Actin is also co-localized with virus factories.

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2000-03-01
2020-01-23
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References

  1. Arhelger, R. B. & Randall, C. C. ( 1964; ). Electron microscopic observations on the development of fowlpox virus in chorioallantoic membrane. Virology 22, 59-66.[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. Journal of Virology 65, 5910-5920.
    [Google Scholar]
  3. Blasco, R. & Moss, B. ( 1992; ). Role of cell-associated enveloped vaccinia virus in cell-to-cell spread. Journal of Virology 66, 4170-4179.
    [Google Scholar]
  4. 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. Journal of Virology 67, 3319-3325.
    [Google Scholar]
  5. Bohn, W., Rutter, G., Hohenberg, H., Mannweiler, K. & Nobis, P. ( 1986; ). Involvement of actin filaments in budding of measles virus: studies on cytoskeletons of infected cells. Virology 149, 91-106.[CrossRef]
    [Google Scholar]
  6. Boulanger, D., Green, P., Smith, T., Czerny, C. P. & Skinner, M. A. ( 1998; ). The 131-amino-acid repeat region of the essential 39-kilodalton core protein of fowlpox virus FP9, equivalent to vaccinia virus A4L protein, is nonessential and highly immunogenic. Journal of Virology 72, 170-179.
    [Google Scholar]
  7. Calvert, J. G., Ogawa, R., Yanagida, N. & Nazerian, K. ( 1992; ). Identification and functional analysis of the fowlpox virus homolog of the vaccinia virus p37K major envelope antigen gene. Virology 191, 783-792.[CrossRef]
    [Google Scholar]
  8. Cudmore, S., Cossart, P., Griffiths, G. & Way, M. ( 1995; ). Actin-based motility of vaccinia virus. Nature 378, 636-638.[CrossRef]
    [Google Scholar]
  9. Cudmore, S., Reckmann, I. & Way, M. ( 1997; ). Viral manipulations of the actin cytoskeleton. Trends in Microbiology 5, 142-148.[CrossRef]
    [Google Scholar]
  10. Dales, S. ( 1963; ). The uptake and development of vaccinia virus in strain L cells followed with labeled viral deoxyribonucleic acid. Journal of Cell Biology 18, 51-72.[CrossRef]
    [Google Scholar]
  11. Dales, S. & Mosbach, E. H. ( 1968; ). Vaccinia as a model for membrane biogenesis. Virology 35, 564-583.[CrossRef]
    [Google Scholar]
  12. Duncan, S. A. & Smith, G. L. ( 1992; ). Identification and characterization of an extracellular envelope glycoprotein affecting vaccinia virus egress. Journal of Virology 66, 1610-1621.
    [Google Scholar]
  13. 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]
  14. 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]
  15. Hiller, G., Weber, K., Schneider, L., Parajsz, C. & Jungwirth, C. ( 1979; ). Interaction of assembled progeny pox viruses with the cellular cytoskeleton. Virology 98, 142-153.[CrossRef]
    [Google Scholar]
  16. Hirt, P., Hiller, G. & Wittek, R. ( 1986; ). Localization and fine structure of a vaccinia virus gene encoding an envelope antigen. Journal of Virology 58, 757-764.
    [Google Scholar]
  17. Hollinshead, M., Vanderplasschen, A., Smith, G. L. & Vaux, D. J. ( 1999; ). Vaccinia virus intracellular mature virions contain only one lipid membrane. Journal of Virology 73, 1503-1517.
    [Google Scholar]
  18. Ichihashi, Y., Matsumoto, S. & Dales, S. ( 1971; ). Biogenesis of poxviruses: role of A-type inclusions and host cell membranes in virus dissemination. Virology 46, 507-532.[CrossRef]
    [Google Scholar]
  19. 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. Journal of Virology 66, 7217-7224.
    [Google Scholar]
  20. Kato, N., Eggers, H. J. & Rolly, H. ( 1969; ). Inhibition of release of vaccinia virus by N1-isonicotinoly-N2–3-methyl-4-chlorobenzoylhydrazine. Journal of Experimental Medicine 129, 795-808.[CrossRef]
    [Google Scholar]
  21. Limbach, K. J. & Paoletti, E. ( 1996; ). Non-replicating expression vectors: applications in vaccine development and gene therapy. Epidemiology and Infection 116, 241-256.[CrossRef]
    [Google Scholar]
  22. McIntosh, A. A. & Smith, G. L. ( 1996; ). Vaccinia virus glycoprotein A34R is required for infectivity of extracellular enveloped virus. Journal of Virology 70, 272-281.
    [Google Scholar]
  23. Maiti, N. K., Oberoi, M. S. & Sharma, S. N. ( 1991; ). Comparative-studies on the antigenicity of extracellular and intracellular viruses of fowlpox. Comparative Immunology Microbiology and Infectious Diseases 14, 59-62.[CrossRef]
    [Google Scholar]
  24. Meyer, R. K., Burger, M. M., Tschannen, R. & Schafer, R. ( 1981; ). Actin filament bundles in vaccinia virus infected fibroblasts. Archives of Virology 67, 11-18.[CrossRef]
    [Google Scholar]
  25. Morgan, C. ( 1976; ). Vaccinia virus reexamined: development and release. Virology 73, 43-58.[CrossRef]
    [Google Scholar]
  26. Murti, K. G. & Goorha, R. ( 1983; ). Interaction of frog virus-3 with the cytoskeleton. I. Altered organization of microtubules, intermediate filaments, and microfilaments. Journal of Cell Biology 96, 1248-1257.[CrossRef]
    [Google Scholar]
  27. Murti, K. G., Chen, M. & Goorha, R. ( 1985; ). Interaction of frog virus 3 with the cytomatrix. III. Role of microfilaments in virus release. Virology 142, 317-325.[CrossRef]
    [Google Scholar]
  28. Ogawa, R., Calvert, J. G., Yanagida, N. & Nazerian, K. ( 1993; ). Insertional inactivation of a fowlpox virus homolog of the vaccinia virus F12L gene inhibits the release of enveloped virions. Journal of General Virology 74, 55-64.[CrossRef]
    [Google Scholar]
  29. Parkinson, J. E. & Smith, G. L. ( 1994; ). Vaccinia virus gene A36R encodes a M(r) 43–50 K protein on the surface of extracellular enveloped virus. Virology 204, 376-390.[CrossRef]
    [Google Scholar]
  30. Payne, L. G. & Kristenson, K. ( 1979; ). Mechanism of vaccinia virus release and its specific inhibition by N1-isonicotinoyl-N2–3-methyl-4-chlorobenzoylhydrazine. Journal of Virology 32, 614-622.
    [Google Scholar]
  31. Payne, L. G. & Kristensson, K. ( 1982a; ). The effect of cytochalasin-D and monensin on enveloped vaccinia virus release. Archives of Virology 74, 11-20.[CrossRef]
    [Google Scholar]
  32. Payne, L. G. & Kristensson, K. ( 1982b; ). Effect of glycosylation inhibitors on the release of enveloped vaccinia virus. Journal of Virology 41, 367-375.
    [Google Scholar]
  33. Pulford, D. J. & Britton, P. ( 1990; ). Expression and cellular localisation of porcine transmissible gastroenteritis virus N and M proteins by recombinant vaccinia viruses. Virus Research 18, 203-218.
    [Google Scholar]
  34. Rodriguez, J. F. & Smith, G. L. ( 1990; ). Inducible gene-expression from vaccinia virus vectors. Virology 177, 239-250.[CrossRef]
    [Google Scholar]
  35. Roper, R. L., Payne, L. G. & Moss, B. ( 1996; ). Extracellular vaccinia virus envelope glycoprotein encoded by the A33R gene. Journal of Virology 70, 3753-3762.
    [Google Scholar]
  36. Roper, R. L., Wolffe, E. J., Weisberg, A. & Moss, B. ( 1998; ). The envelope protein encoded by the A33R gene is required for formation of actin-containing microvilli and efficient cell-to-cell spread of vaccinia virus. Journal of Virology 72, 4192-4204.
    [Google Scholar]
  37. 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. Journal of Virology 73, 2863-2875.
    [Google Scholar]
  38. Sanders, M. C. & Theriot, J. A. ( 1996; ). Tails from the hall of infection: actin-based motility of pathogens. Trends in Microbiology 4, 211-213.[CrossRef]
    [Google Scholar]
  39. 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. Journal of General Virology 79, 1415-1425.
    [Google Scholar]
  40. 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. Journal of Virology 68, 130-147.
    [Google Scholar]
  41. Schmutz, C., Payne, L. G., Gubser, J. & Wittek, R. ( 1991; ). A mutation in the gene encoding the vaccinia virus 37,000-M(r) protein confers resistance to an inhibitor of virus envelopment and release. Journal of Virology 65, 3435-3442.
    [Google Scholar]
  42. Shida, H. ( 1986; ). Nucleotide sequence of the vaccinia virus hemagglutinin gene. Virology 150, 451-462.[CrossRef]
    [Google Scholar]
  43. Smith, G. L., Chan, Y. S. & Howard, S. T. ( 1991; ). Nucleotide sequence of 42 kbp of vaccinia virus strain WR from near the right inverted terminal repeat. Journal of General Virology 72, 1349-1376.[CrossRef]
    [Google Scholar]
  44. Sodeik, B., Doms, R. W., Ericsson, M., Hiller, G., Machamer, C. E., Vanthof, W., Vanmeer, G., Moss, B. & Griffiths, G. ( 1993; ). Assembly of vaccinia virus: role of the intermediate compartment between the endoplasmic reticulum and the Golgi stacks. Journal of Cell Biology 121, 521-541.[CrossRef]
    [Google Scholar]
  45. Stokes, G. V. ( 1976; ). High-voltage electron microscope study of the release of vaccinia virus from whole cells. Journal of Virology 18, 636-643.
    [Google Scholar]
  46. Tooze, J., Hollinshead, M., Reis, B., Radsak, K. & Kern, H. ( 1993; ). Progeny vaccinia and human cytomegalovirus particles utilize early endosomal cisternae for their envelopes. European Journal of Cell Biology 60, 163-178.
    [Google Scholar]
  47. Tsukita, S., Oishi, K., Sato, N., Sagara, J., Kawai, A. & Tsukita, S. ( 1994; ). ERM family members as molecular linkers between the cell surface glycoprotein CD44 and actin-based cytoskeletons. Journal of Cell Biology 126, 391-401.[CrossRef]
    [Google Scholar]
  48. Tsutsui, K. ( 1983; ). Release of vaccinia virus from FL cells infected with the IHD-W strain. Journal of Electron Microscopy 32, 125-140.
    [Google Scholar]
  49. Tsutsui, K., Uno, F., Akatsuka, K. & Nii, S. ( 1983; ). Electron microscopic study on vaccinia virus release. Archives of Virology 75, 213-218.[CrossRef]
    [Google Scholar]
  50. Ulaeto, D., Grosenbach, D. & Hruby, D. E. ( 1995; ). Brefeldin A inhibits vaccinia virus envelopment but does not prevent normal processing and localization of the putative envelopment receptor p37. Journal of General Virology 76, 103-111.[CrossRef]
    [Google Scholar]
  51. Weintraub, S., Stern, W. & Dales, S. ( 1977; ). Biogenesis of vaccinia. Effects of inhibitors of glycosylation on virus-mediated activities. Virology 78, 315-322.[CrossRef]
    [Google Scholar]
  52. 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. Journal of Virology 67, 4732-4741.
    [Google Scholar]
  53. 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. Journal of Virology 71, 3904-3915.
    [Google Scholar]
  54. Wolffe, E. J., Weisberg, A. S. & Moss, B. ( 1998; ). Role for the vaccinia virus A36R outer envelope protein in the formation of virus-tipped actin-containing microvilli and cell-to-cell virus spread. Virology 244, 20-26.[CrossRef]
    [Google Scholar]
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