1887

Abstract

Vaccinia virus produces four different types of virion from each infected cell called intracellular mature virus (IMV), intracellular enveloped virus (IEV), cell-associated enveloped virus (CEV) and extracellular enveloped virus (EEV). These virions have different abundance, structure, location and roles in the virus life-cycle. Here, the formation and function of these virions are considered with emphasis on the EEV form and its precursors, IEV and CEV. IMV is the most abundant form of virus and is retained in cells until lysis; it is a robust, stable virion and is well suited to transmit infection between hosts. IEV is formed by wrapping of IMV with intracellular membranes, and is an intermediate between IMV and CEV/EEV that enables efficient virus dissemination to the cell surface on microtubules. CEV induces the formation of actin tails that drive CEV particles away from the cell and is important for cell-to-cell spread. Lastly, EEV mediates the long-range dissemination of virus in cell culture and, probably, . Seven virus-encoded proteins have been identified that are components of IEV, and five of them are present in CEV or EEV. The roles of these proteins in virus morphogenesis and dissemination, and as targets for neutralizing antibody are reviewed. The production of several different virus particles in the VV replication cycle represents a coordinated strategy to exploit cell biology to promote virus spread and to aid virus evasion of antibody and complement.

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2002-12-01
2019-10-17
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References

  1. Afonso, C. L., Tulman, E. R., Lu, Z., Zsak, L., Sandybaev, N. T., Kerembekova, U. Z., Zaitsev, V. L., Kutish, G. F. & Rock, D. L. ( 2002; ). The genome of camelpox virus. Virology 295, 1-9.[CrossRef]
    [Google Scholar]
  2. Aguado, B., Selmes, I. P. & Smith, G. L. ( 1992; ). Nucleotide sequence of 21·8 kbp of variola major virus strain Harvey and comparison with vaccinia virus. Journal of General Virology 73, 2887-2902.[CrossRef]
    [Google Scholar]
  3. Amies, C. R. ( 1961; ). Loss of immunogenic properties of vaccinia virus inactivated by formaldehyde. Canadian Journal of Microbiology 7, 141-152.[CrossRef]
    [Google Scholar]
  4. Appleyard, G. & Andrews, C. ( 1974; ). Neutralizing activities of antisera to poxvirus soluble antigens. Journal of General Virology 23, 197-200.[CrossRef]
    [Google Scholar]
  5. Appleyard, G., Hapel, A. J. & Boulter, E. A. ( 1971; ). An antigenic difference between intracellular and extracellular rabbitpox virus. Journal of General Virology 13, 9-17.[CrossRef]
    [Google Scholar]
  6. Armstrong, J. A., Metz, D. H. & Young, M. R. ( 1973; ). The mode of entry of vaccinia virus into L cells. Journal of General Virology 21, 533-537.[CrossRef]
    [Google Scholar]
  7. Baek, S. H., Kwak, J. Y., Lee, S. H., Lee, T., Ryu, S. H., Uhlinger, D. J. & Lambeth, J. D. ( 1997; ). Lipase activities of p37, the major envelope protein of vaccinia virus. Journal of Biological Chemistry 272, 32042-32049.[CrossRef]
    [Google Scholar]
  8. Bednarek, S. Y., Orci, L. & Schekman, R. ( 1996; ). Traffic COPS and the formation of vesicle coats. Trends in Cell Biology 6, 468-473.[CrossRef]
    [Google Scholar]
  9. Blackman, K. E. & Bubel, H. C. ( 1972; ). Origin of the vaccinia virus hemagglutinin. Journal of Virology 9, 290-296.
    [Google Scholar]
  10. 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]
  11. 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]
  12. Blasco, R., Cole, N. B. & Moss, B. ( 1991; ). Sequence analysis, expression, and deletion of a vaccinia virus gene encoding a homolog of profilin, a eukaryotic actin-binding protein. Journal of Virology 65, 4598-4608.
    [Google Scholar]
  13. 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]
  14. Boulter, E. A. ( 1969; ). Protection against poxviruses. Proceedings of the Royal Society of Medicine 62, 295-297.
    [Google Scholar]
  15. Boulter, E. A. & Appleyard, G. ( 1973; ). Differences between extracellular and intracellular forms of poxviruses and their implications. Progress in Medical Virology 16, 86-108.
    [Google Scholar]
  16. Boulter, E. A., Zwartouw, H. T., Titmuss, D. H. I. & Maber, H. B. ( 1971; ). The nature of the immune state produced by inactivated vaccinia virus in rabbits. American Journal of Epidemiology 94, 612-620.
    [Google Scholar]
  17. Brown, C. K., Bloom, D. C. & Moyer, R. W. ( 1991a; ). The nature of naturally occurring mutations in the hemagglutinin gene of vaccinia virus and the sequence of immediately adjacent genes. Virus Genes 5, 235-242.[CrossRef]
    [Google Scholar]
  18. Brown, C. K., Turner, P. C. & Moyer, R. W. ( 1991b; ). Molecular characterization of the vaccinia virus hemagglutinin gene. Journal of Virology 65, 3598-3606.
    [Google Scholar]
  19. Cavallaro, K. F. & Esposito, J. J. ( 1992; ). Sequences of the raccoon poxvirus hemagglutinin protein. Virology 190, 434-439.[CrossRef]
    [Google Scholar]
  20. Chang, A. & Metz, D. H. ( 1976; ). Further investigations on the mode of entry of vaccinia virus into cells. Journal of General Virology 32, 275-282.[CrossRef]
    [Google Scholar]
  21. Chang, W., Hsiao, J. C., Chung, C. S. & Bair, C. H. ( 1995; ). Isolation of a monoclonal antibody which blocks vaccinia virus infection. Journal of Virology 69, 517-522.
    [Google Scholar]
  22. Child, S. J. & Hruby, D. E. ( 1992; ). Evidence for multiple species of vaccinia virus-encoded palmitylated proteins. Virology 191, 262-271.[CrossRef]
    [Google Scholar]
  23. Chu, C. M. ( 1948; ). Studies on the vaccinia haemagglutinin. I. Some physiochemical properties. Journal of Hygiene 46, 42-48.[CrossRef]
    [Google Scholar]
  24. Chung, C. S., Hsiao, J. C., Chang, Y. S. & Chang, W. ( 1998; ). A27L protein mediates vaccinia virus interaction with cell surface heparan sulfate. Journal of Virology 72, 1577-1585.
    [Google Scholar]
  25. Colley, W. C., Sung, T. C., Roll, R., Hammond, S. M., Altshuller, Y. M., Bar-Sagi, D., Morris, A. J. & Frohman, M. A. ( 1997; ). Phospholipase D2, a distinct phospoholipase D isoform with novel regulatory properties that provokes cytoskeletal reorganisation. Current Biology 7, 191-201.[CrossRef]
    [Google Scholar]
  26. Collier, L. H., McClean, D. & Vallet, L. ( 1955; ). The antigenicity of ultra-violet irradiated vaccinia virus. Journal of Hygiene 53, 513-534.[CrossRef]
    [Google Scholar]
  27. Cudmore, S., Cossart, P., Griffiths, G. & Way, M. ( 1995; ). Actin-based motility of vaccinia virus. Nature 378, 636-638.[CrossRef]
    [Google Scholar]
  28. Cudmore, S., Reckmann, I., Griffiths, G. & Way, M. ( 1996; ). Vaccinia virus: a model system for actin–membrane interactions. Journal of Cell Science 109, 1739-1747.
    [Google Scholar]
  29. 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]
  30. Dales, S. ( 1965; ). Penetration of animal viruses into cells. Progress in Medical Virology 7, 1-43.
    [Google Scholar]
  31. Dales, S. & Mosbach, E. H. ( 1968; ). Vaccinia as a model for membrane biogenesis. Virology 35, 564-583.[CrossRef]
    [Google Scholar]
  32. 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]
  33. 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]
  34. Downie, A. W. ( 1939; ). Immunological relationship of the virus of spontaneous cowpox to vaccinia virus. British Journal of Experimental Pathology 20, 158-176.
    [Google Scholar]
  35. 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]
  36. Engelstad, M. & Smith, G. L. ( 1993; ). The vaccinia virus 42 kDa envelope protein is required for envelopment and egress of extracellular virus and for virulence. Virology 194, 627-637.[CrossRef]
    [Google Scholar]
  37. Engelstad, M., Howard, S. T. & Smith, G. L. ( 1992; ). A constitutively expressed vaccinia virus gene encodes a 42 kDa glycoprotein related to complement control factors that forms part of the extracellular envelope. Virology 188, 801-810.[CrossRef]
    [Google Scholar]
  38. Eppstein, D. A., Marsh, Y. V., Schreiber, A. B., Newman, S. R., Todaro, G. J. & Nestor, J. J.Jr ( 1985; ). Epidermal growth factor receptor occupancy inhibits vaccinia virus infection. Nature 318, 663-665.[CrossRef]
    [Google Scholar]
  39. Fenner, F., Anderson, D. A., Arita, I., Jezek, Z. & Ladnyi, I. D. (1988). Smallpox and its Eradication. Geneva: World Health Organization.
  40. Fenner, F., Wittek, R. & Dumbell, K. R. (1989). The Orthopoxviruses, chapter 4. London: Academic Press.
  41. Flexner, C., Hugin, A. & Moss, B. ( 1987; ). Prevention of vaccinia virus infection in immunodeficient mice by vector-directed IL-2 expression. Nature 330, 259-262.[CrossRef]
    [Google Scholar]
  42. Frischknecht, F., Cudmore, S., Moreau, V., Reckmann, I., Rottger, S. & Way, M. ( 1999a; ). Tyrosine phosphorylation is required for actin-based motility of vaccinia but not Listeria and Shigella. Current Biology 9, 89-92.
    [Google Scholar]
  43. Frischknecht, F., Moreau, V., Röttger, S., Gonfloni, S., Rechmann, I., Superti-Furga, G. & Way, M. ( 1999b; ). Actin-based motility of vaccinia virus mimics receptor tyrosine kinase signalling. Nature 401, 926-929.[CrossRef]
    [Google Scholar]
  44. Galmiche, M. C., Rindisbacher, L., Wels, W., Wittek, R. & Buchegger, F. ( 1997; ). Expression of a functional single chain antibody on the surface of extracellular enveloped vaccinia virus as a step towards selective tumour cell targeting. Journal of General Virology 78, 3019-3027.
    [Google Scholar]
  45. Galmiche, M. C., Goenaga, J., Wittek, R. & Rindisbacher, L. ( 1999; ). Neutralizing and protective antibodies directed against vaccinia virus envelope antigens. Virology 254, 71-80.[CrossRef]
    [Google Scholar]
  46. Garon, C. F. & Moss, B. ( 1971; ). Glycoprotein synthesis in cells infected with vaccinia virus. II. A glycoprotein component of the virion. Virology 46, 233-246.[CrossRef]
    [Google Scholar]
  47. 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]
  48. Goebel, S. J., Johnson, G. P., Perkus, M. E., Davis, S. W., Winslow, J. P. & Paoletti, E. ( 1990; ). The complete DNA sequence of vaccinia virus. Virology 179, 247-266.[CrossRef]
    [Google Scholar]
  49. Goldberg, M. B. & Theriot, J. A. ( 1995; ). Shigella flexneri surface protein IcsA is sufficient to direct actin-based motility. Proceedings of the National Academy of Sciences, USA 92, 6572-6576.[CrossRef]
    [Google Scholar]
  50. Griffiths, G., Wepf, R., Wendt, T., Locker, J. K., Cyrklaff, M. & Roos, N. ( 2001; ). Structure and assembly of intracellular mature vaccinia virus: isolated-particle analysis. Journal of Virology 75, 11034-11055.[CrossRef]
    [Google Scholar]
  51. Grosenbach, D. W. & Hruby, D. E. ( 1998; ). Analysis of a vaccinia virus mutant expressing a nonpalmitylated form of p37, a mediator of virion envelopment. Journal of Virology 72, 5108-5120.
    [Google Scholar]
  52. Grosenbach, D. W., Ulaeto, D. O. & Hruby, D. E. ( 1997; ). Palmitylation of the vaccinia virus 37-kDa major envelope antigen. Identification of a conserved acceptor motif and biological relevance. Journal of Biological Chemistry 272, 1956-1964.[CrossRef]
    [Google Scholar]
  53. Grosenbach, D. W., Hansen, S. G. & Hruby, D. E. ( 2000; ). Identification and analysis of vaccinia virus palmitylproteins. Virology 275, 193-206.[CrossRef]
    [Google Scholar]
  54. Gubser, C. M. & Smith, G. L. ( 2002; ). The sequence of camelpox virus shows it is most closely related to variola virus, the cause of smallpox. Journal of General Virology 83, 855-872.
    [Google Scholar]
  55. Hashizume, S., Yoshizawa, H., Morita, M. & Suzuki, K. ( 1985; ). Properties of attenuated mutant of vaccinia virus, LC16m8, derived from Lister strain. In Vaccinia Viruses as Vectors for Vaccine Antigens , pp. 87-99. Edited by G. V. Quinnan. New York:Elsevier Science Publishing Co.
  56. Herrera, E., del Mar Lorenzo, 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. Journal of Virology 72, 294-302.
    [Google Scholar]
  57. 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]
  58. 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]
  59. Hiller, G., Eibl, H. & Weber, K. ( 1981a; ). Characterization of intracellular and extracellular vaccinia virus variants: N1-isonicotinoyl-N2-3-methyl-4-chlorobenzoylhydrazine interferes with cytoplasmic virus dissemination and release. Journal of Virology 39, 903-913.
    [Google Scholar]
  60. Hiller, G., Jungwirth, C. & Weber, K. ( 1981b; ). Fluorescence microscopical analysis of the life cycle of vaccinia virus in chick embryo fibroblasts. Virus–cytoskeleton interactions. Experimental Cell Research 132, 81-87.[CrossRef]
    [Google Scholar]
  61. 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]
  62. 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]
  63. Hollinshead, M., Rodger, G., van Eijl, H., Hollinshead, R., Law, M., 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]
  64. Holowczak, J. A. ( 1970; ). Glycopeptides of vaccinia virus. I. Preliminary characterization and hexosamine content. Virology 42, 87-99.[CrossRef]
    [Google Scholar]
  65. Hooper, J. W., Custer, D. M., Schmaljohn, C. S. & Schmaljohn, A. L. ( 2000; ). DNA vaccination with vaccinia virus L1R and A33R genes protects mice against a lethal poxvirus challenge. Virology 266, 329-339.[CrossRef]
    [Google Scholar]
  66. Hsiao, J. C., Chung, C. S. & Chang, W. ( 1999; ). Vaccinia virus envelope D8L protein binds to cell surface chondroitin sulfate and mediates the adsorption of intracellular mature virions to cells. Journal of Virology 73, 8750-8761.
    [Google Scholar]
  67. Hügin, A. & Hauser, C. ( 1994; ). The epidermal growth factor receptor is not a receptor for vaccinia virus. Journal of Virology 68, 8409-8412.
    [Google Scholar]
  68. 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. Journal of Virology 75, 7528-7542.[CrossRef]
    [Google Scholar]
  69. Husain, M. & Moss, B. ( 2002; ). Similarities in the induction of post-Golgi vesicles by the vaccinia virus F13L protein and phospholipase D. Journal of Virology 76, 7777-7789.[CrossRef]
    [Google Scholar]
  70. Ichihashi, Y. ( 1996; ). Extracellular enveloped vaccinia virus escapes neutralization. Virology 217, 478-485.[CrossRef]
    [Google Scholar]
  71. Ichihashi, Y. & Dales, S. ( 1971; ). Biogenesis of poxviruses: interrelationship between hemagglutinin production and polykaryocytosis. Virology 46, 533-543.[CrossRef]
    [Google Scholar]
  72. 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]
  73. 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]
  74. Janeczko, R. A., Rodriguez, J. F. & Esteban, M. ( 1987; ). Studies on the mechanism of entry of vaccinia virus in animal cells. Archives of Virology 92, 135-150.[CrossRef]
    [Google Scholar]
  75. Jenner, E. (1798). An Enquiry into the Causes and Effects of Variolae Vaccinae, a Disease Discovered in some Western Countries of England, particularly Gloucestershire and known by the Name of Cow Pox. London: Reprinted by Cassell, 1896.
  76. Jin, D., Li, Z., Jin, Q., Yuwen, H. & Hou, Y. ( 1989; ). Vaccinia virus hemagglutinin. A novel member of the immunoglobulin superfamily. Journal of Experimental Medicine 170, 571-576.[CrossRef]
    [Google Scholar]
  77. Kaplan, C. (1962). A non-infectious smallpox vaccine. Lancet ii, 1027–1028.
  78. Kaplan, C., McLean, D. & Vallet, L. ( 1962; ). A note on the immunogenicity of ultraviolet irradiated vaccinia virus in man. Journal of Hygiene 60, 79-83.[CrossRef]
    [Google Scholar]
  79. Kaplan, C., Benson, P. F. & Butler, N. R. (1965). Immunogenicity of ultraviolet irradiated, non-infectious, vaccinia virus in infants and young children. Lancet i, 573–574.
  80. Kato, N., Eggers, H. J. & Rolly, H. ( 1969; ). Inhibition of release of vaccinia virus by N1-isonicotinoyl-N2-3-methyl-4-chlorobenzoylhydrazine. Journal of Experimental Medicine 129, 795-808.[CrossRef]
    [Google Scholar]
  81. 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]
  82. Koonin, E. V. ( 1996; ). A duplicated catalytic motif in a new superfamily of phosphohydrolases and phospholipid synthases that includes poxvirus envelope proteins. Trends in Biochemical Science 21, 242-243.[CrossRef]
    [Google Scholar]
  83. Kotwal, G. J., Isaacs, S. N., McKenzie, R., Frank, M. M. & Moss, B. ( 1990; ). Inhibition of the complement cascade by the major secretory protein of vaccinia virus. Science 250, 827-830.[CrossRef]
    [Google Scholar]
  84. Krauss, O., Hollinshead, R., Hollinshead, M. & Smith, G. L. ( 2002; ). An investigation of the incorporation of cellular antigens in vaccinia virus particles. Journal of General Virology 83, 2347-2359.
    [Google Scholar]
  85. Krempien, U., Schneider, L., Hiller, G., Weber, K., Katz, E. & Jungwirth, C. ( 1981; ). Conditions for pox virus-specific microvilli formation studied during synchronized virus assembly. Virology 113, 556-564.[CrossRef]
    [Google Scholar]
  86. Krijnse Locker, J., Kuehn, A., Schleich, S., Rutter, G., Hohenberg, H., Wepf, R. & Griffiths, G. ( 2000; ). Entry of the two infectious forms of vaccinia virus at the plasma membrane is signaling-dependent for the IMV but not the EEV. Molecular Biology of the Cell 11, 2497-2511.[CrossRef]
    [Google Scholar]
  87. Lalani, A. S., Masters, J., Zeng, W., Barrett, J., Pannu, R., Everett, H., Arendt, C. W. & McFadden, G. ( 1999; ). Use of chemokine receptors by poxviruses. Science 286, 1968-1971.[CrossRef]
    [Google Scholar]
  88. Law, K. M. & Smith, G. L. ( 1992; ). A vaccinia serine protease inhibitor which prevents virus induced cell fusion. Journal of General Virology 73, 549-557.[CrossRef]
    [Google Scholar]
  89. Law, M. & Smith, G. L. ( 2001; ). Antibody neutralization of the extracellular enveloped form of vaccinia virus. Virology 280, 132-142.[CrossRef]
    [Google Scholar]
  90. Law, M., Hollinshead, R. & Smith, G. L. ( 2002; ). Antibody-sensitive and antibody-resistant cell-to-cell spread of vaccinia virus: role of the A33R protein in antibody-resistant spread. Journal of General Virology 83, 209-222.
    [Google Scholar]
  91. 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. Journal of Virology 74, 3353-3365.[CrossRef]
    [Google Scholar]
  92. 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]
  93. 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]
  94. Maa, J. S., Rodriguez, J. F. & Esteban, M. ( 1990; ). Structural and functional characterization of a cell surface binding protein of vaccinia virus. Journal of Biological Chemistry 265, 1569-1577.
    [Google Scholar]
  95. 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]
  96. Mackett, M., Smith, G. L. & Moss, B. ( 1982; ). Vaccinia virus: a selectable eukaryotic cloning and expression vector. Proceedings of the National Academy of Sciences, USA 79, 7415-7419.[CrossRef]
    [Google Scholar]
  97. Madeley, C. R. ( 1968; ). The immunogenicity of heat-inactivated vaccinia virus in rabbits. Journal of Hygiene 66, 89-107.[CrossRef]
    [Google Scholar]
  98. Martinez-Pomares, L., Stern, R. J. & Moyer, R. W. ( 1993; ). The ps/hr gene (B5R open reading frame homolog) of rabbitpox virus controls pock colour, is a component of extracellular enveloped virus, and is secreted into the medium. Journal of Virology 67, 5450-5462.
    [Google Scholar]
  99. Massung, R. F., Liu, L. I., Qi, J., Knight, J. C., Yuran, T. E., Kerlavage, A. R., Parsons, J. M., Venter, J. C. & Esposito, J. J. ( 1994; ). Analysis of the complete genome of smallpox variola major virus strain Bangladesh-1975. Virology 201, 215-240.[CrossRef]
    [Google Scholar]
  100. Masters, J., Hinek, A. A., Uddin, S., Platanias, L. C., Zeng, W., McFadden, G. & Fish, E. N. ( 2001; ). Poxvirus infection rapidly activates tyrosine kinase signal transduction. Journal of Biological Chemistry 276, 48371-48375.
    [Google Scholar]
  101. 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]
  102. 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]
  103. 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]
  104. 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.
  105. Moss, B. & Rosenblum, E. N. ( 1973; ). Protein cleavage and poxvirus morphogenesis: tryptic peptide analysis of core precursors accumulated by blocking assembly with rifampicin. Journal of Molecular Biology 81, 267-269.[CrossRef]
    [Google Scholar]
  106. Nagler, F. P. O. ( 1942; ). Application of Hirst’s phenomenon to the titration of vaccinia virus and vaccinia immune serum. Medical Journal of Australia 1, 281-283.
    [Google Scholar]
  107. Ogawa, R., Calvert, J. G., Yanagida, N. & Nazerian, K. ( 1993; ). Insertional inactivation of a fowlpox virus homologue of the vaccinia virus F12L gene inhibits the release of enveloped virions. Journal of General Virology 74, 55-64.[CrossRef]
    [Google Scholar]
  108. Panicali, D. & Paoletti, E. ( 1982; ). Construction of poxviruses as cloning vectors: insertion of the thymidine kinase gene from herpes simplex virus into the DNA of infectious vaccinia virus. Proceedings of the National Academy of Sciences, USA 79, 4927-4931.[CrossRef]
    [Google Scholar]
  109. 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]
  110. Patel, D. D., Pickup, D. J. & Joklik, W. K. ( 1986; ). Isolation of cowpox virus A-type inclusions and characterization of their major protein component. Virology 149, 174-189.[CrossRef]
    [Google Scholar]
  111. Payne, L. G. ( 1978; ). Polypeptide composition of extracellular enveloped vaccinia virus. Journal of Virology 27, 28-37.
    [Google Scholar]
  112. 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]
  113. 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]
  114. Payne, L. G. ( 1992; ). Characterization of vaccinia virus glycoproteins by monoclonal antibody preparations. Virology 187, 251-260.[CrossRef]
    [Google Scholar]
  115. Payne, L. G. & Kristensson, 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]
  116. Payne, L. G. & Kristensson, K. ( 1982; ). The effect of cytochalasin D and monensin on enveloped vaccinia virus release. Archives of Virology 74, 11-20.[CrossRef]
    [Google Scholar]
  117. Payne, L. G. & Kristensson, K. ( 1985; ). Extracellular release of enveloped vaccinia virus from mouse nasal epithelial cells in vivo. Journal of General Virology 66, 643-646.[CrossRef]
    [Google Scholar]
  118. 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]
  119. Payne, L. G. & Norrby, E. ( 1978; ). Adsorption and penetration of enveloped and naked vaccinia virus particles. Journal of Virology 27, 19-27.
    [Google Scholar]
  120. Ploubidou, A., Moreau, V., Ashman, K., Reckmann, I., Gonzalez, C. & Way, M. ( 2000; ). Vaccinia virus infection disrupts microtubule organization and centrosome function. EMBO Journal 19, 3932-3944.[CrossRef]
    [Google Scholar]
  121. Ponting, C. P. & Kerr, I. D. ( 1996; ). A novel family of phospholipase D homologues that includes phospholipid synthases and putative endonucleases: identification of duplicated repeats and potential active site residues. Protein Science 5, 914-922.
    [Google Scholar]
  122. Pulford, D. J., Meyer, H. & Ulaeto, D. ( 2002; ). Orthologs of the vaccinia A13L and A36R virion membrane protein genes display diversity in species of the genus Orthopoxvirus. Archives of Virology 147, 995-1015.[CrossRef]
    [Google Scholar]
  123. Ramı́rez, J. C., Tapia, E. & Esteban, M. ( 2002; ). Administration to mice of a monoclonal antibody that neutralizes the intracellular mature virus form of vaccinia virus limits virus replication efficiently under prophylactic and therapeutic conditions. Journal of General Virology 83, 1059-1067.
    [Google Scholar]
  124. 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]
  125. 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]
  126. 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]
  127. Rodriguez, J. F. & Smith, G. L. ( 1990; ). IPTG-dependent vaccinia virus: identification of a virus protein enabling virion envelopment by Golgi membrane and egress. Nucleic Acids Research 18, 5347-5351.[CrossRef]
    [Google Scholar]
  128. Rodriguez, J. F., Janezcko, R. & Esteban, M. ( 1985; ). Isolation and characterization of neutralizing monoclonal antibodies to vaccinia virus. Journal of Virology 56, 482-488.
    [Google Scholar]
  129. Rodriguez, J. F., Paez, E. & Esteban, M. ( 1987; ). A 14,000-Mr envelope protein of vaccinia virus is involved in cell fusion and forms covalently linked trimers. Journal of Virology 61, 395-404.
    [Google Scholar]
  130. Rodriguez, D., Rodriguez, J. R. & Esteban, M. ( 1993; ). The vaccinia virus 14-kilodalton fusion protein forms a stable complex with the processed protein encoded by the vaccinia virus A17L gene. Journal of Virology 67, 3435-3440.
    [Google Scholar]
  131. 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]
  132. 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]
  133. 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]
  134. Sanderson, C. M., Frischknecht, F., Way, M., Hollinshead, M. & Smith, G. L. ( 1998a; ). 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]
  135. Sanderson, C. M., Way, M. & Smith, G. L. ( 1998b; ). Virus-induced cell motility. Journal of Virology 72, 1235-1243.
    [Google Scholar]
  136. 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]
  137. Scaplehorn, N., Holmstrom, A., Moreau, V., Frischknecht, F., Rechmann, I. & Way, M. ( 2002; ). Grb2 and Nck act cooperatively to promote actin-based motility of vaccinia virus. Current Biology 12, 740-745.[CrossRef]
    [Google Scholar]
  138. Schmelz, M., Sodeik, B., Ericsson, M., Wolffe, E., 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]
  139. Schmutz, C. & Wittek, R. ( 1995; ). Release of extracellular particles by recombinant vaccinia virus over-expressing the major envelope protein p37K. Journal of General Virology 76, 2963-2968.[CrossRef]
    [Google Scholar]
  140. Schmutz, C., Payne, L. G., Gubser, J. & Wittek, R. ( 1991; ). A mutation in the gene encoding the vaccinia virus 37,000-Mr protein confers resistance to an inhibitor of virus envelopment and release. Journal of Virology 65, 3435-3442.
    [Google Scholar]
  141. Seki, M., Oie, M., Ichihashi, Y. & Shida, H. ( 1990; ). Hemadsorption and fusion inhibition activities of hemagglutinin analyzed by vaccinia virus mutants. Virology 175, 372-384.[CrossRef]
    [Google Scholar]
  142. Shchelkunov, S. N., Safronov, P. F., Totmenin, A. V., Petrov, N. A., Ryazankina, O. I., Gutorov, V. V. & Kotwal, G. J. ( 1998; ). The genomic sequence analysis of the left and right species-specific terminal region of a cowpox virus strain reveals unique sequences and a cluster of intact ORFs for immunomodulatory and host range proteins. Virology 243, 432-460.[CrossRef]
    [Google Scholar]
  143. Shchelkunov, S. N., Totmenin, A. V., Babkin, I. V., Safronov, P. F., Ryazankina, O. I., Petrov, N. A., Gutorov, V. V., Uvarova, E. A., Mikheev, M. V., Sisler, J. R., Esposito, J. J., Jahrling, P. B., Moss, B. & Sandakhchiev, L. S. ( 2001; ). Human monkeypox and smallpox viruses: genomic comparison. FEBS Letters 509, 66-70.[CrossRef]
    [Google Scholar]
  144. Shida, H. ( 1986a; ). Nucleotide sequence of the vaccinia virus hemagglutinin gene. Virology 150, 451-462.[CrossRef]
    [Google Scholar]
  145. Shida, H. ( 1986b; ). Variants of vaccinia virus hemagglutinin altered in intracellular transport. Molecular and Cellular Biology 6, 3734-3745.
    [Google Scholar]
  146. Shida, H. & Dales, S. ( 1981; ). Biogenesis of vaccinia: carbohydrate of the hemagglutinin molecules. Virology 111, 56-72.[CrossRef]
    [Google Scholar]
  147. Shida, H. & Dales, S. ( 1982; ). Biogenesis of vaccinia: molecular basis for the hemagglutinin-negative phenotype of the IHD-W strain. Virology 117, 219-237.[CrossRef]
    [Google Scholar]
  148. Shida, H. & Matsumoto, S. ( 1983; ). Analysis of the hemagglutinin glycoprotein from mutants of vaccinia virus that accumulate on the nuclear envelope. Cell 33, 423-434.[CrossRef]
    [Google Scholar]
  149. 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.
  150. Smith, G. A., Portnoy, D. A. & Theriot, J. A. ( 1995; ). Asymmetric distribution of the Listeria monocytogenes ActA protein is required and sufficient to direct actin-based motility. Molecular Microbiology 17, 945-951.[CrossRef]
    [Google Scholar]
  151. Sodeik, B. ( 2000; ). Mechanisms of viral transport in the cytoplasm. Trends in Microbiology 8, 465-472.[CrossRef]
    [Google Scholar]
  152. Sodeik, B. & Krijnse Locker, J. ( 2002; ). Assembly of vaccinia virus revisited: de novo membrane synthesis or acquisition from the host? Trends in Microbiology 10, 15-24.[CrossRef]
    [Google Scholar]
  153. 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]
  154. 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]
  155. Sung, T. C., Roper, R. L., Zhang, Y., Rudge, S. A., Temel, R., Hammond, S. M., Morris, A. J., Moss, B., Engebrecht, J. & Frohman, M. A. ( 1997; ). Mutagenesis of phospholipase D defines a superfamily including a trans-Golgi viral protein required for poxvirus pathogenicity. EMBO Journal 16, 4519-4530.[CrossRef]
    [Google Scholar]
  156. Takahashi-Nishimaki, F., Funahashi, S.-I., 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]
  157. 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]
  158. Tsutsui, K. ( 1983; ). Release of vaccinia virus from FL cells infected with IHD-W strain. Journal of Electron Microscopy 32, 125-140.
    [Google Scholar]
  159. Turner, P. C. & Moyer, R. W. ( 1992; ). An orthopoxvirus serpinlike gene controls the ability of infected cells to fuse. Journal of Virology 66, 2076-2085.
    [Google Scholar]
  160. Turner, G. S. & Squires, E. J. ( 1971; ). Inactivated smallpox vaccine: immunogenicity of inactivated intracellular and extracellular vaccinia virus. Journal of General Virology 13, 19-25.[CrossRef]
    [Google Scholar]
  161. Turner, G. S., Squires, E. J. & Murray, H. G. ( 1970; ). Inactivated smallpox vaccine. A comparison of inactivation methods. Journal of Hygiene 68, 197-210.[CrossRef]
    [Google Scholar]
  162. Ulaeto, D., Grosenbach, D. & Hruby, D. E. ( 1996; ). The vaccinia virus 4c and A-type inclusion proteins are specific markers for the intracellular mature virus particle. Journal of Virology 70, 3372-3377.
    [Google Scholar]
  163. Vanderplasschen, A. & Smith, G. L. ( 1997; ). A novel virus binding assay using confocal microscopy: demonstration that the intracellular and extracellular vaccinia virions bind to different cellular receptors. Journal of Virology 71, 4032-4041.
    [Google Scholar]
  164. Vanderplasschen, A. & Smith, G. L. ( 1999; ). Confocal microscopy: a method to study virus binding and entry into cells. Methods in Enzymology 307, 591-607.
    [Google Scholar]
  165. 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]
  166. Vanderplasschen, A., Hollinshead, M. & Smith, G. L. ( 1998a; ). Intracellular and extracellular vaccinia virions enter cells by different mechanisms. Journal of General Virology 79, 877-887.
    [Google Scholar]
  167. Vanderplasschen, A., Mathew, E., Hollinshead, M., Sim, R. B. & Smith, G. L. ( 1998b; ). 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]
  168. 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]
  169. van Eijl, H., Hollinshead, M., Rodger, G., Zhang, W.-H. & Smith, G. L. ( 2002; ). The vaccinia virus F12L protein 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]
  170. 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]
  171. 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]
  172. 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]
  173. 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]
  174. 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]
  175. Wolffe, E. J., Weisberg, A. S. & Moss, B. ( 2001; ). The vaccinia virus A33R protein provides a chaperone function for viral membrane localization and tyrosine phosphorylation of the A36R protein. Journal of Virology 75, 303-310.[CrossRef]
    [Google Scholar]
  176. 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]
  177. Zhou, J., Sun, X. Y., Fernando, G. J. P. & Frazer, I. H. ( 1992; ). The vaccinia virus K2L gene encodes a serine protease inhibitor which inhibits cell–cell fusion. Virology 189, 678-686.[CrossRef]
    [Google Scholar]
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