1887

Abstract

Vaccinia virus (VV) infection produces several types of virus particle called intracellular mature virus (IMV), intracellular enveloped virus (IEV), cell-associated enveloped virus (CEV) and extracellular enveloped virus (EEV). Some cellular antigens are associated with EEV and these vary with the cell type used to grow the virus. To investigate if specific cell antigens are associated with VV particles, and to address the origin of membranes used to envelope IMV and IEV/CEV/EEV, we have studied whether cell antigens and foreign antigens expressed by recombinant VVs are incorporated into VV particles. Membrane proteins that are incorporated into the endoplasmic reticulum (ER), intermediate compartment (IC), /-Golgi, -Golgi network (TGN) or plasma membrane were not detected in purified IMV particles. In contrast, proteins present in the TGN or membrane compartments further downstream in the exocytic pathway co-purify with EEV particles when analysed by immunoblotting. Immunoelectron microscopy found only low levels of these proteins in IEV, CEV/EEV. The incorporation of foreign antigens into VV particles was not affected by loss of individual IEV or EEV-specific proteins or by redirection of B5R to the ER. These data suggest that (i) host cell antigens are excluded from the lipid envelope surrounding the IMV particle and (ii) membranes of the ER, IC and /-Golgi are not used to wrap IMV particles to form IEV. Lastly, the VV haemagglutinin was absent from one-third of IEV and CEV/EEV particles, whereas other EEV antigens were present in all these virions.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-83-10-2347
2002-10-01
2020-01-24
Loading full text...

Full text loading...

/deliver/fulltext/jgv/83/10/0832347a.html?itemId=/content/journal/jgv/10.1099/0022-1317-83-10-2347&mimeType=html&fmt=ahah

References

  1. Arthur, L. O., Bess, J. W.Jr, Sowder, R. C.II, Benveniste, R. E., Mann, D. L., Chermann, J. C. & Henderson, L. E. ( 1992; ). Cellular proteins bound to immunodeficiency viruses: implications for pathogenesis and vaccines. Science 258, 1935-1938.[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. Chakrabarti, S., Brechling, K. & Moss, B. ( 1985; ). Vaccinia virus expression vector: coexpression of β-galactosidase provides visual screening of recombinant virus plaques. Molecular and Cellular Biology 5, 3403-3409.
    [Google Scholar]
  6. Dales, S. & Siminovitch, L. ( 1961; ). The development of vaccinia virus in Earles L strain cells as examined by electron microscopy. Journal of Biophysical and Biochemical Cytology 10, 475-503.[CrossRef]
    [Google Scholar]
  7. Dales, S. & Mosbach, E. H. ( 1968; ). Vaccinia as a model for membrane biogenesis. Virology 35, 564-583.[CrossRef]
    [Google Scholar]
  8. Doms, R. W., Blumenthal, R. & Moss, B. ( 1990; ). Fusion of intra- and extracellular forms of vaccinia virus with the cell membrane. Journal of Virology 64, 4884-4892.
    [Google Scholar]
  9. Duncan, J. R. & Kornfeld, S. ( 1988; ). Intracellular movement of two mannose 6-phosphate receptors: return to the Golgi apparatus. Journal of Cell Biology 106, 617-628.[CrossRef]
    [Google Scholar]
  10. 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]
  11. 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]
  12. 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]
  13. Essani, K. & Dales, S. ( 1979; ). Biogenesis of vaccinia: evidence for more than 100 polypeptides in the virion. Virology 95, 385-394.[CrossRef]
    [Google Scholar]
  14. Fenner, F., Anderson, D. A., Arita, I., Jezek, Z. & Ladnyi, I. D. (1988). Smallpox and Its Eradication. Geneva: World Health Organization.
  15. Fortin, J. F., Cantin, R., Lamontagne, G. & Tremblay, M. ( 1997; ). Host-derived ICAM-1 glycoproteins incorporated on human immunodeficiency virus type 1 are biologically active and enhance viral infectivity. Journal of Virology 71, 3588-3596.
    [Google Scholar]
  16. Frischknecht, F., Moreau, V., Röttger, S., Gonfloni, S., Rechmann, 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]
  17. Geada, M. M., Galindo, I., Lorenzo, M. M., Perdiguero, B. & Blasco, R. ( 2001; ). Movements of vaccinia virus intracellular enveloped virions with GFP tagged to the F13L envelope protein. Journal of General Virology 82, 2747-2760.
    [Google Scholar]
  18. Goda, Y. & Pfeffer, S. R. ( 1988; ). Selective recycling of the mannose 6-phosphate/IGF-II receptor to the trans Golgi network in vitro. Cell 55, 309-320.[CrossRef]
    [Google Scholar]
  19. Griffiths, G., Roos, N., Schleich, S. & Locker, J. K. ( 2001; ). Structure and assembly of intracellular mature vaccinia virus: thin-section analyses. Journal of Virology 75, 11056-11070.[CrossRef]
    [Google Scholar]
  20. Hiller, G. & Weber, K. ( 1985; ). Golgi-derived membranes that contain an acylated viral polypeptide are used for vaccinia virus envelopment. Journal of Virology 55, 651-659.
    [Google Scholar]
  21. 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]
  22. 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]
  23. Hollinshead, M., Rodger, G., van Eijl, H., Law, M., Hollinshead, R., Vaux, D. T. & Smith, G. L. ( 2001; ). Vaccinia virus utilizes microtubules for movement to the cell surface. Journal of Cell Biology 154, 389-402.[CrossRef]
    [Google Scholar]
  24. Ichihashi, Y. & Dales, S. ( 1971; ). Biogenesis of poxviruses: interrelationship between hemagglutinin production and polykaryocytosis. Virology 46, 533-543.[CrossRef]
    [Google Scholar]
  25. 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]
  26. 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]
  27. 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. Journal of Virology 71, 3178-3187.
    [Google Scholar]
  28. Klumperman, J., Locker, J. K., Meijer, A., Horzinek, M. C., Geuze, H. J. & Rottier, P. J. ( 1994; ). Coronavirus M proteins accumulate in the Golgi complex beyond the site of virion budding. Journal of Virology 68, 6523-6534.
    [Google Scholar]
  29. Lappin, D. F., Nakitare, G. W., Palfreyman, J. W. & Elliott, R. M. ( 1994; ). Localization of Bunyamwera bunyavirus G1 glycoprotein to the Golgi requires association with G2 but not with NSm. Journal of General Virology 75, 3441-3451.[CrossRef]
    [Google Scholar]
  30. Law, M., Hollinshead, R. & Smith, G. L. ( 2002; ). Antibody-sensitive and antibody-resistant cell-to-cell spread by vaccinia virus: role of the A33R protein in antibody-resistant spread. Journal of General Virology 83, 209-222.
    [Google Scholar]
  31. Linstedt, A. D. & Hauri, H. P. ( 1993; ). Giantin, a novel conserved Golgi membrane protein containing a cytoplasmic domain of at least 350 kDa. Molecular Biology of the Cell 4, 679-693.[CrossRef]
    [Google Scholar]
  32. Lorenzo, M. M., Herrera, E., Blasco, R. & Isaacs, S. N. ( 1999; ). Functional analysis of vaccinia virus B5R protein: role of the cytoplasmic tail. Virology 252, 450-457.
    [Google Scholar]
  33. 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. Journal of Virology 74, 10535-10550.[CrossRef]
    [Google Scholar]
  34. 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]
  35. 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. Journal of Virology 72, 2429-2438.
    [Google Scholar]
  36. Mathew, E., Sanderson, C. M., Hollinshead, R., Hollinshead, M., Grimley, R. & Smith, G. L. ( 1999; ). The effects of targeting the vaccinia virus B5R protein to the endoplasmic reticulum on virus morphogenesis and dissemination. Virology 265, 131-146.[CrossRef]
    [Google Scholar]
  37. Mathew, E. C., Sanderson, C. M., Hollinshead, R. & Smith, G. L. ( 2001; ). A mutational analysis of the vaccinia virus B5R protein. Journal of General Virology 82, 1199-1213.
    [Google Scholar]
  38. Mockett, A. P., Cavanagh, D. & Brown, T. D. ( 1984; ). Monoclonal antibodies to the S1 spike and membrane proteins of avian infectious bronchitis coronavirus strain Massachusetts M41. Journal of General Virology 65, 2281-2286.[CrossRef]
    [Google Scholar]
  39. Moss, B. ( 2001; ). Poxviridae: the viruses and their replication. In Fields Virology , pp. 2849-2883. Edited by D. M. Knipe & P. M. Howley. Philadelphia:Lippincott Williams & Wilkins.
  40. Mu, F. T., Callaghan, J. M., Steele-Mortimer, O., Stenmark, H., Parton, R. G., Campbell, P. L., McCluskey, J., Yeo, J. P., Tock, E. P. & Toh, B. H. ( 1995; ). EEA1, an early endosome-associated protein. EEA1 is a conserved alpha-helical peripheral membrane protein flanked by cysteine ‘fingers’ and contains a calmodulin-binding IQ motif. Journal of Biological Chemistry 270, 13503-13511.[CrossRef]
    [Google Scholar]
  41. Nakitare, G. W. & Elliott, R. M. ( 1993; ). Expression of the Bunyamwera virus M genome segment and intracellular localization of NSm. Virology 195, 511-520.[CrossRef]
    [Google Scholar]
  42. Neefjes, J. J., Verkerk, J. M., Broxterman, H. J., van der Marel, G. A., van Boom, J. H. & Ploegh, H. L. ( 1988; ). Recycling glycoproteins do not return to the cis-Golgi. Journal of Cell Biology 107, 79-87.[CrossRef]
    [Google Scholar]
  43. 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]
  44. Payne, L. G. ( 1978; ). Polypeptide composition of extracellular enveloped vaccinia virus. Journal of Virology 27, 28-37.
    [Google Scholar]
  45. Payne, L. G. ( 1979; ). Identification of the vaccinia hemagglutinin polypeptide from a cell system yielding large amounts of extracellular enveloped virus. Journal of Virology 31, 147-155.
    [Google Scholar]
  46. Payne, L. G. ( 1980; ). Significance of extracellular enveloped virus in the in vitro and in vivo dissemination of vaccinia virus. Journal of General Virology 50, 89-100.[CrossRef]
    [Google Scholar]
  47. Payne, L. G. & Norrby, E. ( 1976; ). Presence of haemagglutinin in the envelope of extracellular vaccinia virus particles. Journal of General Virology 32, 63-72.[CrossRef]
    [Google Scholar]
  48. Rietdorf, J., Ploubidou, A., Reckmann, I., Holmstrom, A., Frischknecht, F., Zettl, M., Zimmermann, T. & Way, M. ( 2001; ). Kinesin-dependent movement on microtubules precedes actin-based motility of vaccinia virus. Nature Cell Biology 3, 992-1000.[CrossRef]
    [Google Scholar]
  49. Risco, C., Rodriguez, J. R., Lopez-Iglesias, C., Carrascosa, J. L., Esteban, M. & Rodriguez, D. ( 2002; ). Endoplasmic reticulum–Golgi intermediate compartment membranes and vimentin filaments participate in vaccinia virus assembly. Journal of Virology 76, 1839-1855.[CrossRef]
    [Google Scholar]
  50. Rodger, G. & Smith, G. L. ( 2002; ). Replacing the SCR domains of vaccinia virus protein B5R with EGFP causes a reduction in plaque size and actin tail formation but enveloped virions are still transported to the cell surface. Journal of General Virology 83, 323-332.
    [Google Scholar]
  51. 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]
  52. 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]
  53. 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. Journal of Virology 73, 2863-2875.
    [Google Scholar]
  54. 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]
  55. Sanderson, C. M., Hollinshead, M. & Smith, G. L. ( 2000; ). The vaccinia virus A27L protein is needed for the microtubule-dependent transport of intracellular mature virus particles. Journal of General Virology 81, 47-58.
    [Google Scholar]
  56. 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]
  57. Schweizer, A., Fransen, J. A., Matter, K., Kreis, T. E., Ginsel, L. & Hauri, H. P. ( 1990; ). Identification of an intermediate compartment involved in protein transport from endoplasmic reticulum to Golgi apparatus. European Journal of Cell Biology 53, 185-196.
    [Google Scholar]
  58. Schweizer, A., Ericsson, M., Bachi, T., Griffiths, G. & Hauri, H. P. ( 1993; ). Characterization of a novel 63 kDa membrane protein. Implications for the organization of the ER-to-Golgi pathway. Journal of Cell Science 104, 671-683.
    [Google Scholar]
  59. Shida, H. ( 1986; ). Nucleotide sequence of the vaccinia virus hemagglutinin gene. Virology 150, 451-462.[CrossRef]
    [Google Scholar]
  60. Slot, J. W. & Geuze, H. J. ( 1985; ). A new method of preparing gold probes for multiple-labeling cytochemistry. European Journal of Cell Biology 38, 87-93.
    [Google Scholar]
  61. Smith, G. L. & Vanderplasschen, A. ( 1998; ). Extracellular enveloped vaccinia virus: entry, egress and evasion. In Coronaviruses and Arteriviruses , pp. 395-414. Edited by L. Enjuanes, S. G. Siddell & W. Spaan. London:Plenum Press.
  62. Smith, G. L., Levin, J. Z., Palese, P. & Moss, B. ( 1987; ). Synthesis and cellular location of the ten influenza polypeptides individually expressed by recombinant vaccinia viruses. Virology 160, 336-345.[CrossRef]
    [Google Scholar]
  63. Sodeik, B., Doms, R. W., Ericsson, M., Hiller, G., Machamer, C. E., van’t Hof, W., van Meer, 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]
  64. Stam, N. J., Vroom, T. M., Peters, P. J., Pastoors, E. B. & Ploegh, H. L. ( 1990; ). HLA-A- and HLA-B-specific monoclonal antibodies reactive with free heavy chains in western blots, in formalin-fixed, paraffin-embedded tissue sections and in cryo-immuno-electron microscopy. International Immunology 2, 113-125.[CrossRef]
    [Google Scholar]
  65. 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]
  66. Vanderplasschen, A., Hollinshead, M. & Smith, G. L. ( 1997; ). Antibodies against vaccinia virus do not neutralize extracellular enveloped virus but prevent virus release from infected cells and comet formation. Journal of General Virology 78, 2041-2048.
    [Google Scholar]
  67. Vanderplasschen, A., Mathew, E., Hollinshead, M., Sim, R. B. & Smith, G. L. ( 1998; ). Extracellular enveloped vaccinia virus is resistant to complement because of incorporation of host complement control proteins into its envelope. Proceedings of the National Academy of Sciences, USA 95, 7544-7549.[CrossRef]
    [Google Scholar]
  68. van Eijl, H., Hollinshead, M. & Smith, G. L. ( 2000; ). The vaccinia virus A36R protein is a type Ib membrane protein present on intracellular but not extracellular enveloped particles. Virology 271, 26-36.[CrossRef]
    [Google Scholar]
  69. van Eijl, H., Hollinshead, M., Rodger, G., Zhang, W.-H. & Smith, G. L. ( 2002; ). The vaccinia virus F12L is associated with intracellular enveloped virus particles and is required for their egress to the cell surface. Journal of General Virology 83, 195-207.
    [Google Scholar]
  70. Ward, B. M. & Moss, B. ( 2000; ). Golgi network targeting and plasma membrane internalization signals in vaccinia virus B5R envelope protein. Journal of Virology 74, 3771-3780.[CrossRef]
    [Google Scholar]
  71. Ward, B. M. & Moss, B. ( 2001; ). Visualization of intracellular movement of vaccinia virus virions containing a green fluorescent protein-B5R membrane protein chimera. Journal of Virology 75, 4802-4813.[CrossRef]
    [Google Scholar]
  72. Watret, G. E., Pringle, C. R. & Elliott, R. M. ( 1985; ). Synthesis of bunyavirus-specific proteins in a continuous cell line (XTC-2) derived from Xenopus laevis. Journal of General Virology 66, 473-482.[CrossRef]
    [Google Scholar]
  73. Watzele, G., Bachofner, R. & Berger, E. G. ( 1991; ). Immunocytochemical localization of the Golgi apparatus using protein-specific antibodies to galactosyltransferase. European Journal of Cell Biology 56, 451-458.
    [Google Scholar]
  74. White, S., Miller, K., Hopkins, C. & Trowbridge, I. S. ( 1992; ). Monoclonal antibodies against defined epitopes of the human transferrin receptor cytoplasmic tail. Biochimica et Biophysica Acta 1136, 28-34.[CrossRef]
    [Google Scholar]
  75. 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]
  76. 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]
  77. Zhang, W.-H., Wilcock, D. & Smith, G. L. ( 2000; ). The vaccinia virus F12L protein is required for actin tail formation, normal plaque size and virulence. Journal of Virology 74, 11654-11662.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-83-10-2347
Loading
/content/journal/jgv/10.1099/0022-1317-83-10-2347
Loading

Data & Media loading...

Most cited articles

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error