Genus Orthopoxvirus: Vaccinia virus

  • Geoffrey L. Smith
Part of the Birkhäuser Advances in Infectious Diseases book series (BAID)


Vaccinia virus (VACV) and Cowpox virus (CPXV) have played seminal roles in human medical and biological science. In 1796 Jenner used CPXV as the first human vaccine and, subsequently, widespread immunization with the related orthopoxvirus (OPV), VACV, led to the eradication of smallpox in 1980. VACV was the first animal virus to be purified and chemically analyzed. It was also the first virus to be genetically engineered and the recombinant viruses applied as a vaccine against other infectious diseases. Here the structure, genes and replication of VACV are reviewed and its phylogenetic relationship to other OPVs is described.


Vaccinia Virus Smallpox Vaccination Smallpox Vaccine Cowpox Virus Actin Tail 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Fenner F, Anderson DA, Arita I, Jezek Z, Ladnyi ID (1988) Smallpox and Its Eradication. World Health Organisation, GenevaGoogle Scholar
  2. 2.
    Baxby D (1981) Jenner’s Smallpox Vaccine. The Riddle of the Origin of Vaccinia Virus. Heinemann, LondonGoogle Scholar
  3. 3.
    Mackett M, Smith GL, Moss B (1982) Vaccinia virus: a selectable eukaryotic cloning and expression vector. Proc Natl Acad Sci USA 79: 7415–7419PubMedCrossRefGoogle Scholar
  4. 4.
    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. Proc Natl Acad Sci USA 79: 4927–931PubMedCrossRefGoogle Scholar
  5. 5.
    Smith GL, Mackett M, Moss B (1983) Infectious vaccinia virus recombinants that express hepatitis B virus surface antigen. Nature 302: 490–95PubMedCrossRefGoogle Scholar
  6. 6.
    Panicali D, Davis SW, Weinberg RL, Paoletti E (1983) Construction of live vaccines by using genetically engineered poxviruses: Biological activity of recombinant vaccinia virus expressing influenza virus hemagglutinin. Proc Natl Acad Sci USA 80: 5364–5368PubMedCrossRefGoogle Scholar
  7. 7.
    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. Reprinted by Cassell, 1896, LondonGoogle Scholar
  8. 8.
    Downie AW (1939) Immunological relationship of the virus of spontaneous cowpox to vaccinia virus. Br J Exp Pathol 20: 158–176Google Scholar
  9. 9.
    Downie AW (1939) A study of the lesions produced experimentally by cowpox virus. J Pathol Bacteriol 48: 361–379CrossRefGoogle Scholar
  10. 10.
    Fenner F, Wittek R, Dumbell KR (1989) The Orthopoxviruses. Academic Press, LondonGoogle Scholar
  11. 11.
    Wittek R, Menna A, Schumperli D, Stoffel S, Muller HK, Wyler R (1977) HindIII and SstI restriction sites mapped on rabbit poxvirus and vaccinia virus DNA. J Virol 23: 669–678Google Scholar
  12. 12.
    Mackett M, Archard LC (1979) Conservation and variation in Orthopoxvirus genome structure. J Gen Virol 45: 683–701PubMedGoogle Scholar
  13. 13.
    Esposito JJ, Knight JC (1985) Orthopoxvirus DNA: a comparison of restriction profiles and maps. Virology 143: 230–251PubMedCrossRefGoogle Scholar
  14. 14.
    Fenner F (1958) The biological characters of several strains of vaccinia, cowpox and rabbitpox viruses. Virology 5: 502–529PubMedCrossRefGoogle Scholar
  15. 15.
    Wokatsch R (1972) Vaccinia virus. In: M Majer, SA Plotkin (eds): Strains of human viruses. Karger, Basel, 241–257Google Scholar
  16. 16.
    Polak MF, Beunders BJW, Werff AR, Van der Sanders EW, Klaveren JN, Van Brans LM (1963) A comparative study of clinical reactions observed after application of several smallpox vaccines in primary vaccination of young adults. Bull World Health Organ 29: 311–322PubMedGoogle Scholar
  17. 17.
    Rivers TM (1931) Cultivation of vaccine virus for Jennerian prophylaxis in man. J Exp Med 54: 453–461CrossRefPubMedGoogle Scholar
  18. 18.
    Kempe CH (1968) Smallpox vaccination of eczema patients with attenuated live vaccinia virus. Yale J Biol Med 41: 1–12PubMedGoogle Scholar
  19. 19.
    Stickl H, Hochstein-Mintzel V (1971) [Intracutaneous smallpox vaccination with a weak pathogenic vaccinia virus (“MVA virus”)]. Muench Med Wochenschr 113: 1149–1153Google Scholar
  20. 20.
    Hashizume S, Yoshizawa H, Morita M, Suzuki K (1985) Properties of attenuated mutant of vaccinia virus, LC16m8, derived from Lister strain. In: GV Quinnan (eds): Vaccinia Viruses as Vectors for Vaccine Antigens. Elsevier Science, New York, 87–99Google Scholar
  21. 21.
    Tartaglia J, Perkus ME, Taylor J, Norton EK, Audonnet JC, Cox WI, Davis SW, van der Hoeven J, Meignier B, Riviere M et al (1992) NYVAC: a highly attenuated strain of vaccinia virus. Virology 188: 217–232PubMedCrossRefGoogle Scholar
  22. 22.
    Ober BT, Bruhl P, Schmidt M, Wieser V, Gritschenberger W, Coulibaly S, Savidis-Dacho H, Gerencer M, Falkner FG (2002) Immunogenicity and safety of defective vaccinia virus Lister: comparison with modified vaccinia virus Ankara. J Virol 76: 7713–7723PubMedCrossRefGoogle Scholar
  23. 23.
    Goebel SJ, Johnson GP, Perkus ME, Davis SW, Winslow JP, Paoletti E (1990) The complete DNA sequence of vaccinia virus. Virology 179: 247–266, 517–263PubMedCrossRefGoogle Scholar
  24. 24.
    Parker RF, Bronson LH, Green RH (1941) Further studies on the infectious unit of vaccinia. J Exp Med 74: 268–281CrossRefGoogle Scholar
  25. 25.
    Law M, Putz MM, Smith GL (2005) An investigation of the therapeutic value of vaccinia-immune IgG in a mouse pneumonia model. J Gen Virol 86: 991–1000PubMedCrossRefGoogle Scholar
  26. 26.
    Herrlich A, Mayr A (1954) [Comparative experimental works on cowpox virus vaccines.] [Translated from German]. DeArch Hyg Bakteriol 138: 479–504Google Scholar
  27. 27.
    de Souza Trindade G, da Fonseca FG, Marques JT, Nogueira ML, Mendes LC, Borges AS, Peiro JR, Pituco EM, Bonjardim CA, Ferreira PC et al (2003) Aracatuba virus: a vaccinia-like virus associated with infection in humans and cattle. Emerg Infect Dis 9: 155–160PubMedGoogle Scholar
  28. 28.
    Marques JT, Trindade GD, Da Fonseca FG, Dos Santos JR, Bonjardim CA, Ferreira PC, Kroon EG (2001) Characterization of ATI, TK and IFN-alpha/ betaR genes in the genome of the BeAn 58058 virus, a naturally attenuated wild Orthopoxvirus. Virus Genes 23: 291–301PubMedCrossRefGoogle Scholar
  29. 29.
    Kunert H, Wolff I (1960) Comparative studies on the virulence of the vaccine virus strains Berlin and Bern. Arch Hyg Bakteriol 144: 37–47PubMedGoogle Scholar
  30. 30.
    Lal SM, Singh IP (1973) Buffalopox-a review. Trop Anim Health Prod 9: 107–112CrossRefGoogle Scholar
  31. 31.
    Dumbell K, Richardson M (1993) Virological investigations of specimens from buffaloes affected by buffalopox in Maharashtra State, India between 1985 and 1987. Arch Virol 128: 257–267PubMedCrossRefGoogle Scholar
  32. 32.
    Cragie J (1932) The nature of the vaccinia virus flocculation reaction and observation of the elementary bodies of vaccinia. Br J Exp Pathol 13: 259–268Google Scholar
  33. 33.
    Harada K, Matumoto M (1962) Antigenic relationship between mammalian and avian pox viruses as revealed by complement fixation reaction. Jpn J Exp Med 32: 369–385PubMedGoogle Scholar
  34. 34.
    Oda M (1965) Rescue of dermovaccinia abortive infection by neurovaccinia virus in L cells. Virology 25: 664–666PubMedCrossRefGoogle Scholar
  35. 35.
    Tagaya I, Kitamura T, Sano Y (1961) A new mutant of dermovaccinia virus. Nature 192: 381–382PubMedCrossRefGoogle Scholar
  36. 36.
    Kitamura T (1963) Reactivation of protease-inactivated vaccinia virus. Virology 21: 286–289PubMedCrossRefGoogle Scholar
  37. 37.
    Coulibaly S, Bruhl P, Mayrhofer J, Schmid K, Gerencer M, Falkner FG (2005) The nonreplicating smallpox candidate vaccines defective vaccinia Lister (dVV-L) and modified vaccinia Ankara (MVA) elicit robust long-term protection. Virology 341: 91–101PubMedCrossRefGoogle Scholar
  38. 38.
    Polak MF, Swart-Vanderhoeven JT, Smeenk C, Pel JZ, Van S, Pasdeloup F (1964) [Comparison of 2_vaccinia strains in vaccination of infants]. Ned Tijdschr Geneeskd 108: 459–464PubMedGoogle Scholar
  39. 39.
    Marennikova SS, Chimishkyan KL, Maltseva NN, Shelukhina EMF, Fedorov VV (1969) Characteristics of virus strains for production of smallpox vaccines. In: B Gusic (ed): Proceedings of the Symposium on Smallpox. Yugoslav Academy of Sciences and Arts, Zagreb, 65–69Google Scholar
  40. 40.
    Koegh EV (1936) Titration of vaccinia virus on the chorioallantoic membrane of the chick embryo and its application to immunological studies of neuro-vaccinia. J Pathol Bacteriol 43: 441–454CrossRefGoogle Scholar
  41. 41.
    Thompson RA, Minton SA Jr, Officer LE, Hutchings GH (1953) Effect of heterocyclic and other thiocarbazones on vaccinia infection in the mouse. J Immunol 70: 229–234PubMedGoogle Scholar
  42. 42.
    Ichihashi Y, Dales S (1971) Biogenesis of poxviruses: interrelationship between hemagglutinin production and polykaryocytosis.Virology 46: 533–543PubMedCrossRefGoogle Scholar
  43. 43.
    Horgan ES, Haseeb MA (1939) Cross immunity experiments in monkeys between variola, alstrim and vaccinia. J Hyg 39: 615–637CrossRefGoogle Scholar
  44. 44.
    Morikawa S, Sakiyama T, Hasegawa H, Saijo M, Maeda A, Kurane I, Maeno G, Kimura J, Hirama C, Yoshida T et al (2005) An attenuated LC16m8_smallpox vaccine: analysis of full-genome sequence and induction of immune protection. J Virol 79: 11873–11891PubMedCrossRefGoogle Scholar
  45. 45.
    Mayr A (1976) [TC marker of the attenuated vaccinia vaccide strain “MVA” in human cell cultures and protective immunization against orthopox diseases in animals]. Zentralbl Veterinarmed B 23: 417–430Google Scholar
  46. 46.
    Antoine G, Scheiflinger F, Dorner F, Falkner FG (1998) The complete genomic sequence of the modified vaccinia Ankara strain: comparison with other orthopoxviruses. Virology 244: 365–396PubMedCrossRefGoogle Scholar
  47. 47.
    Jansen J (1946) Immunity in rabbit plague-immunological relationship with cowpox. Antonie van Leeuwenhowek J Microbiol Serol 11: 139–167CrossRefGoogle Scholar
  48. 48.
    da Fonseca FG, Trindade GS, Silva RL, Bonjardim CA, Ferreira PC, Kroon EG (2002) Characterization of a vaccinia-like virus isolated in a Brazilian forest. J Gen Virol 83: 223–228PubMedGoogle Scholar
  49. 49.
    Turner GS (1967) Respiratory infection of mice with vaccinia virus. J Gen Virol 1: 399–402PubMedGoogle Scholar
  50. 50.
    Minton SA Jr, Officer JE, Thompson RL (1953) Effect of thiosemicarbazones and dichlorophenoxy thiouracil on multiplication of a recently isolated strain of variola-vaccinia virus in the brain of the mouse. J Immunol 70: 222–228PubMedGoogle Scholar
  51. 51.
    Lane JM, Ruben FL, Neff JM, Millar JD (1969) Complications of smallpox vaccination, 1968. National surveillance in the United States. N Engl J Med 281: 1201–1208PubMedCrossRefGoogle Scholar
  52. 52.
    Chen RT, Lane JM (2003) Myocarditis: the unexpected return of smallpox vaccine adverse events. Lancet 362: 1345–1346PubMedCrossRefGoogle Scholar
  53. 53.
    Meyer H, Sutter G, Mayr A (1991) Mapping of deletions in the genome of the highly attenuated vaccinia virus MVA and their influence on virulence. J Gen Virol 72: 1031–1038PubMedGoogle Scholar
  54. 54.
    Sutter G, Moss B (1992) Nonreplicating vaccinia vector efficiently expresses recombinant genes. Proc Natl Acad Sci USA 89: 10847–10851PubMedCrossRefGoogle Scholar
  55. 55.
    Carroll MW, Moss B (1997) Host range and cytopathogenicity of the highly attenuated MVA strain of vaccinia virus: propagation and generation of recombinant viruses in a nonhuman mammalian cell line. Virology 238: 198–211PubMedCrossRefGoogle Scholar
  56. 56.
    Okeke MI, Nilssen O, Traavik T (2006) Modified vaccinia virus Ankara multiplies in rat IEC-6_cells and limited production of mature virions occurs in other mammalian cell lines. J Gen Virol 87: 21–27PubMedCrossRefGoogle Scholar
  57. 57.
    Mayr A, Stickl H, Muller HK, Danner K, Singer H (1978) [The smallpox vaccination strain MVA: marker, genetic structure, experience gained with the parenteral vaccination and behavior in organisms with a debilitated defence mechanism (author’s transl)]. Zentralbl Bakteriol B 167: 375–390PubMedGoogle Scholar
  58. 58.
    Cebere I, Dorrell L, McShane H, Simmons A, McCormack S, Schmidt C, Smith C, Brooks M, Roberts JE, Darwin SC et al (2006) Phase I clinical trial safety of DNA-and modified virus Ankara-vectored human immunodeficiency virus type 1 (HIV-1) vaccines administered alone and in a prime-boost regime to healthy HIV-1-uninfected volunteers. Vaccine 24: 417–425PubMedCrossRefGoogle Scholar
  59. 59.
    Stickl H, Hochstein-Mintzel V, Mayr A, Huber HC, Schafer H, Holzner A (1974) [MVA vaccination against smallpox: clinical tests with an attenuated live vaccinia virus strain (MVA) (author’s transl)]. Dtsch Med Wochenschr 99: 2386–2392PubMedCrossRefGoogle Scholar
  60. 60.
    Drexler I, Staib C, Kastenmuller W, Stevanovic S, Schmidt B, Lemonnier FA, Rammensee HG, Busch DH, Bernhard H, Erfle V et al (2003) Identification of vaccinia virus epitope-specific HLA-A*0201-restricted T cells and comparative analysis of smallpox vaccines. Proc Natl Acad Sci USA 100: 217–222PubMedCrossRefGoogle Scholar
  61. 61.
    Earl PL, Americo JL, Wyatt LS, Eller LA, Whitbeck JC, Cohen GH, Eisenberg RJ, Hartmann CJ, Jackson DL, Kulesh DA et al (2004) Immunogenicity of a highly attenuated MVA smallpox vaccine and protection against monkeypox. Nature 428: 182–185PubMedCrossRefGoogle Scholar
  62. 62.
    Staib C, Drexler I, Sutter G (2004) Construction and isolation of recombinant MVA. Methods Mol Biol 269: 77–100PubMedGoogle Scholar
  63. 63.
    Blanchard TJ, Alcami A, Andrea P, Smith GL (1998) Modified vaccinia virus Ankara undergoes limited replication in human cells and lacks several immunomodulatory proteins: implications for use as a human vaccine. J Gen Virol 79: 1159–1167PubMedGoogle Scholar
  64. 64.
    Staib C, Kisling S, Erfle V, Sutter G (2005) Inactivation of the viral interleukin 1ta receptor improves CD8+ T-cell memory responses elicited upon immunization with modified vaccinia virus Ankara. J Gen Virol 86: 1997–2006Google Scholar
  65. 65.
    Clark RH, Kenyon JC, Bartlett NW, Tscharke DC, Smith GL (2006) Deletion of gene A41L enhances vaccinia virus immunogenicity and vaccine efficacy.J Gen Virol 87: 29–38PubMedCrossRefGoogle Scholar
  66. 66.
    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: 158–164PubMedCrossRefGoogle Scholar
  67. 67.
    Takahashi-Nishimaki F, Suzuki K, Morita M, Maruyama T, Miki K, Hashizume S, Sugimoto M (1987) Genetic analysis of vaccinia virus Lister strain and its attenuated mutant LC16m8: production of intermediate variants by homologous recombination. J Gen Virol 68: 2705–2710PubMedGoogle Scholar
  68. 68.
    Engelstad M, Howard ST, Smith GL (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: 801–810PubMedCrossRefGoogle Scholar
  69. 69.
    Isaacs SN, Wolffe EJ, Payne LG, Moss B (1992) Characterization of a vaccinia virus-encoded 42-kilodalton class I membrane glycoprotein component of the extracellular virus envelope. J Virol 66: 7217–7224PubMedGoogle Scholar
  70. 70.
    Galmiche MC, Goenaga J, Wittek R, Rindisbacher L (1999) Neutralizing and protective antibodies directed against vaccinia virus envelope antigens. Virology 254: 71–80PubMedCrossRefGoogle Scholar
  71. 71.
    Law M, Smith GL (2001) Antibody neutralization of the extracellular enveloped form of vaccinia virus. Virology 280: 132–142PubMedCrossRefGoogle Scholar
  72. 72.
    Bell E, Shamim M, Whitbeck JC, Sfyroera G, Lambris JD, Isaacs SN (2004) Antibodies against the extracellular enveloped virus B5R protein are mainly responsible for the EEV neutralizing capacity of vaccinia immune globulin. Virology 325: 425–431PubMedCrossRefGoogle Scholar
  73. 73.
    Putz MM, Midgley CM, Law M, Smith GL (2006) Quantification of antibody responses against multiple antigens of the two infectious forms of Vaccinia virus provides a benchmark for smallpox vaccination. Nat Med; in press Google Scholar
  74. 74.
    Kidokoro M, Tashiro M, Shida H (2005) Genetically stable and fully effective smallpox vaccine strain constructed from highly attenuated vaccinia LC16m8. Proc Natl Acad Sci USA 102: 4152–4157PubMedCrossRefGoogle Scholar
  75. 75.
    Seet BT, Johnston JB, Brunetti CR, Barrett JW, Everett H, Cameron C, Sypula J, Nazarian SH, Lucas A, McFadden G (2003) Poxviruses and immune evasion. Annu Rev Immunol 21: 377–423PubMedCrossRefGoogle Scholar
  76. 76.
    Moss B (2006) Poxvirus entry and membrane fusion.Virology 344: 48–54PubMedCrossRefGoogle Scholar
  77. 77.
    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: 475–503PubMedCrossRefGoogle Scholar
  78. 78.
    Sodeik B, Doms RW, Ericsson M, Hiller G, Machamer CE, 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. J Cell Biol 121: 521–541PubMedCrossRefGoogle Scholar
  79. 79.
    Risco C, Rodriguez JR, Lopez-Iglesias C, Carrascosa JL, Esteban M, Rodriguez D (2002) Endoplasmic reticulum-Golgi intermediate compartment membranes and vimentin filaments participate in vaccinia virus assembly. J Virol 76: 1839–1855PubMedCrossRefGoogle Scholar
  80. 80.
    Roos N, Cyrklaff M, Cudmore S, Blasco R, Krijnse-Locker J, Griffiths G (1996) A novel immunogold cryoelectron microscopic approach to investigate the structure of the intracellular and extracellular forms of vaccinia virus. EMBO J 15: 2343–2355PubMedGoogle Scholar
  81. 81.
    Hollinshead M, Vanderplasschen A, Smith GL, Vaux DJ (1999) Vaccinia virus intracellular mature virions contain only one lipid membrane. J Virol 73: 1503–1000517PubMedGoogle Scholar
  82. 82.
    Cyrklaff M, Risco C, Fernandez JJ, Jimenez MV, Esteban M, Baumeister W, Carrascosa JL (2005) Cryo-electron tomography of vaccinia virus. Proc Natl Acad Sci USA 102: 2772–2777PubMedCrossRefGoogle Scholar
  83. 83.
    Munyon W, Paoletti E, Grace JT Jr (1967) RNA polymerase activity in purified infectious vaccinia virus. Proc Natl Acad Sci USA 58: 2280–2287PubMedCrossRefGoogle Scholar
  84. 84.
    Morgan C (1976) Vaccinia virus reexamined: development and release. Virology 73: 43–58PubMedCrossRefGoogle Scholar
  85. 85.
    Dubochet J, Adrian M, Richter K, Garces J, Wittek R (1994) Structure of intracellular mature vaccinia virus observed by cryoelectron microscopy. J Virol 68: 1935–1941PubMedGoogle Scholar
  86. 86.
    Schmelz M, Sodeik B, Ericsson M, Wolffe EJ, 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: 130–147PubMedGoogle Scholar
  87. 87.
    Tooze J, Hollinshead M, Reis B, Radsak K, Kern H (1993) Progeny vaccinia and human cytomegalovirus particles utilize early endosomal cisternae for their envelopes. Eur J Cell Biol 60: 163–178PubMedGoogle Scholar
  88. 88.
    Berns KI, Silverman C (1970) Natural occurrence of cross-linked vaccinia virus deoxyribonucleic acid. J Virol 5: 299–304PubMedGoogle Scholar
  89. 89.
    Baroudy BM, Venkatesan S, Moss B (1982) Incompletely base-paired flip-flop terminal loops link the two DNA strands of the vaccinia virus genome into one uninterrupted polynucleotide chain. Cell 28: 315–324PubMedCrossRefGoogle Scholar
  90. 90.
    Garon CF, Barbosa E, Moss B (1978) Visualization of an inverted terminal repetition in vaccinia virus DNA. Proc Natl Acad Sci USA 75: 4863–4867PubMedCrossRefGoogle Scholar
  91. 91.
    Colinas RJ, Goebel SJ, Davis SW, Johnson GP, Norton EK, Paoletti E (1990) A DNA ligase gene in the Copenhagen strain of vaccinia virus is nonessential for viral replication and recombination. Virology 179: 267–275PubMedCrossRefGoogle Scholar
  92. 92.
    Gubser C, Smith GL (2002) The sequence of camelpox virus shows it is most closely related to variola virus, the cause of smallpox. J Gen Virol 83: 855–872PubMedGoogle Scholar
  93. 93.
    Massung RF, Liu LI, Qi J, Knight JC, Yuran TE, Kerlavage AR, Parsons JM, Venter JC, Esposito JJ (1994) Analysis of the complete genome of smallpox variola major virus strain Bangladesh-1975. Virology 201: 215–240PubMedCrossRefGoogle Scholar
  94. 94.
    Pickup DJ, Ink BS, Parsons BL, Hu W, Joklik WK (1984) Spontaneous deletions and duplications of sequences in the genome of cowpox virus. Proc Natl Acad Sci USA81: 6817–6821PubMedCrossRefGoogle Scholar
  95. 95.
    Wittek R, Moss B (1980) Tandem repeats within the inverted terminal repetition of vaccinia virus DNA. Cell 21: 277–284PubMedCrossRefGoogle Scholar
  96. 96.
    Baroudy BM, Moss B (1982) Sequence homologies of diverse length tandem repetitions near ends of vaccinia virus genome suggest unequal crossing over. Nucleic Acids Res 10: 5673–5679PubMedCrossRefGoogle Scholar
  97. 97.
    Merchlinsky M, Moss B (1989) Nucleotide sequence required for resolution of the concatemer junction of vaccinia virus DNA. J Virol 63: 4354–4361PubMedGoogle Scholar
  98. 98.
    Merchlinsky M (1990) Mutational analysis of the resolution sequence of vaccinia virus DNA: essential sequence consists of two separate AT-rich regions highly conserved among poxviruses. J Virol 64: 5029–5035PubMedGoogle Scholar
  99. 99.
    Upton C, Slack S, Hunter AL, Ehlers A, Roper RL (2003) Poxvirus orthologous clusters: toward defining the minimum essential poxvirus genome. J Virol 77: 7590–7600PubMedCrossRefGoogle Scholar
  100. 100.
    Gubser C, Hué S, Kellam P, Smith GL (2004) Poxvirus genomes: a phylogenetic analysis. J Gen Virol 85: 105–117PubMedCrossRefGoogle Scholar
  101. 101.
    Smith GL, Vanderplasschen A, Law M (2002) The formation and function of extracellular enveloped vaccinia virus. J Gen Virol 83: 2915–2931PubMedGoogle Scholar
  102. 102.
    Armstrong JA, Metz DH, Young MR (1973) The mode of entry of vaccinia virus into L cells. J Gen Virol 21: 533–537PubMedGoogle Scholar
  103. 103.
    Chang A, Metz DH (1976) Further investigations on the mode of entry of vaccinia virus into cells. J Gen Virol 32: 275–282PubMedGoogle Scholar
  104. 104.
    Doms RW, Blumenthal R, Moss B (1990) Fusion of intra-and extracellular forms of vaccinia virus with the cell membrane. J Virol 64: 4884–4892PubMedGoogle Scholar
  105. 105.
    Griffiths G, Wepf R, Wendt T, Locker JK, Cyrklaff M, Roos N (2001) Structure and assembly of intracellular mature vaccinia virus: isolated-particle analysis. J Virol 75: 11034–11055PubMedCrossRefGoogle Scholar
  106. 106.
    Locker JK, 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 membane is signaling-dependent for the IMV but not the EEV. Mol Biol Cell 11: 2497–2511PubMedGoogle Scholar
  107. 107.
    Vanderplasschen A, Hollinshead M, Smith GL (1998) Intracellular and extracellular vaccinia virions enter cells by different mechanisms. J Gen Virol 79: 877–887PubMedGoogle Scholar
  108. 108.
    Senkevich TG, Ward BM, Moss B (2004) Vaccinia virus entry into cells is dependent on a virion surface protein encoded by the A28L gene. J Virol 78: 2357–2366PubMedCrossRefGoogle Scholar
  109. 109.
    Carter GC, Law M, Hollinshead M, Smith GL (2005) PThe entry of the vaccinia virus intracellular mature virion and its interactions with glycosaminoglycans. J Gen Virol 86: 1279–1290PubMedCrossRefGoogle Scholar
  110. 110.
    Law M, Carter GC, Roberts KL, Hollinshead M, Smith GL (2006) Ligandinduced and non-fusogenic dissolution of a virus membrane. Proc Natl Acad Sci USA 103: 5989–5994PubMedCrossRefGoogle Scholar
  111. 111.
    Eppstein DA, Marsh YV, Schreiber AB, Newman SR, Todaro GJ, Nestor JJ Jr (1985) Epidermal growth factor receptor occupancy inhibits vaccinia virus infection. Nature 318: 663–665PubMedCrossRefGoogle Scholar
  112. 112.
    Hugin AW, Hauser C (1994) The epidermal growth factor receptor is not a receptor for vaccinia virus. J Virol 68: 8409–8412PubMedGoogle Scholar
  113. 113.
    Lalani AS, Masters J, Zeng W, Barrett J, Pannu R, Everett H, Arendt CW, McFadden G (1999) Use of chemokine receptors by poxviruses. Science 286: 1968–1971PubMedCrossRefGoogle Scholar
  114. 114.
    Masters J, Hinek AA, Uddin S, Platanias LC, Zeng W, McFadden G, Fish EN (2001) Poxvirus infection rapidly activates tyrosine kinase signal transduction. J Biol Chem 276: 48371–48375PubMedCrossRefGoogle Scholar
  115. 115.
    Chung CS, Hsiao JC, Chang YS, Chang W (1998) A27L protein mediates vaccinia virus interaction with cell surface heparan sulfate. J Virol 72: 1577–1585PubMedGoogle Scholar
  116. 116.
    Hsiao JC, Chung CS, 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: 8374–8379PubMedGoogle Scholar
  117. 117.
    Hsiao JC, Chung CS, Chang W (1999) Vaccinia virus envelope D8L protein binds to cell surface chondroitin sulfate and mediates the adsorption of intracellular mature virions to cells. J Virol 73: 8750–8761PubMedGoogle Scholar
  118. 118.
    Lin CL, Chung CS, Heine HG, Chang W (2000) Vaccinia virus envelope H3L protein binds to cell surface heparan sulfate and is important for intracellular mature virion morphogenesis and virus infectionin vitro and in vivo. J Virol 74: 3353–3365PubMedCrossRefGoogle Scholar
  119. 119.
    Rodriguez JF, Smith GL (1990) IPTG-dependent vaccinia virus: identification of a virus protein enabling virion envelopment by Golgi membrane and egress. Nucleic Acids Res 18: 5347–5351PubMedCrossRefGoogle Scholar
  120. 120.
    Ward BM (2005) Visualization and characterization of the intracellular movement of vaccinia virus intracellular mature virions. J Virol 79: 4755–4763PubMedCrossRefGoogle Scholar
  121. 121.
    Vanderplasschen A, Smith GL (1997) A novel virus binding assay using confocal microscopy: demonstration that the intracellular and extracellular vaccinia virions bind to different cellular receptors. J Virol 71: 4032–4041PubMedGoogle Scholar
  122. 122.
    Chang W, Hsiao JC, Chung CS, Bair CH (1995) Isolation of a monoclonal antibody which blocks vaccinia virus infection. J Virol 69: 517–522PubMedGoogle Scholar
  123. 123.
    Young JAT (2001) Virus entry and uncoating. In: DM Knipe, PM Howley (eds): Fields Virology. Lippincott-Raven Publishers, Philadephia, 87–103Google Scholar
  124. 124.
    Townsley AC, Senkevich TG, Moss B (2005) Vaccinia virus A21_virion membrane protein is required for cell entry and fusion. J Virol 79: 9458–9469PubMedCrossRefGoogle Scholar
  125. 125.
    Townsley AC, Senkevich TG, Moss B (2005) The product of the vaccinia virus L5R gene is a fourth membrane protein encoded by all poxviruses that is required for cell entry and cell-cell fusion. J Virol79: 10988–10998PubMedCrossRefGoogle Scholar
  126. 126.
    Senkevich TG, Moss B (2005) Vaccinia virus H2_protein is an essential component of a complex involved in virus entry and cell-cell fusion. J Virol 79: 4744–4754PubMedCrossRefGoogle Scholar
  127. 127.
    Ojeda S, Senkevich TG, Moss B (2006) Entry of vaccinia virus and cell-cell fusion require a highly conserved cysteine-rich membrane protein encoded by the A16L gene. J Virol 80: 51–61PubMedCrossRefGoogle Scholar
  128. 128.
    Senkevich TG, Ojeda S, Townsley A, Nelson GE, Moss B (2005) Poxvirus multiprotein entry-fusion complex. Proc Natl Acad Sci USA 102: 18572–18577PubMedCrossRefGoogle Scholar
  129. 129.
    Röttger S, Frischknecht F, Reckmann I, Smith GL, Way M (1999) Interactions between vaccinia virus IEV membrane proteins and their roles in IEV assembly and actin tail formation. J Virol 73: 2863–2875PubMedGoogle Scholar
  130. 130.
    Earp LJ, Delos SE, Park HE, White JM (2005) The many mechanisms of viral membrane fusion proteins. Curr Top Microbiol Immunol 285: 25–66PubMedGoogle Scholar
  131. 131.
    Carter GC, Rodger G, Murphy BJ, Law M, Krauss O, Hollinshead M, Smith GL (2003) Vaccinia virus cores are transported on microtubules. J Gen Virol 84: 2443–2458PubMedCrossRefGoogle Scholar
  132. 132.
    Kates JR, McAuslan BR (1967) Poxvirus DNA-dependent RNA polymerase. Proc Natl Acad Sci USA 58: 134–141PubMedCrossRefGoogle Scholar
  133. 133.
    Kates J, Beeson J (1970) Ribonucleic acid synthesis in vaccinia virus. II. Synthesis of polyriboadenylic acid. J Mol Biol 50: 19–33Google Scholar
  134. 134.
    Wei CM, Moss B (1974) Methylation of newly synthesized viral messenger RNA by an enzyme in vaccinia virus. Proc Natl Acad Sci USA 71: 3014–3018PubMedCrossRefGoogle Scholar
  135. 135.
    Wei CM, Moss B (1975) Methylated nucleotides block 5’-terminus of vaccinia virus messenger RNA. Proc Natl Acad Sci USA 72: 318–322PubMedCrossRefGoogle Scholar
  136. 136.
    Broyles SS (2003) Vaccinia virus transcription. J Gen Virol 84: 2293–2303PubMedCrossRefGoogle Scholar
  137. 137.
    Yuen L, Davison AJ, Moss B (1987) Early promoter-binding factor from vaccinia virions. Proc Natl Acad Sci USA 84: 6069–6073PubMedCrossRefGoogle Scholar
  138. 138.
    Broyles SS, Moss B (1988) DNA-dependent ATPase activity associated with vaccinia virus early transcription factor. J Biol Chem 263: 10761–10765PubMedGoogle Scholar
  139. 139.
    Shuman S, Broyles SS, Moss B (1987) Purification and characterization of a transcription termination factor from vaccinia virions. J Biol Chem 262: 12372–12380PubMedGoogle Scholar
  140. 140.
    Paoletti E, Grady LJ (1977) Transcriptional complexity of vaccinia virus in vivo and in vitro. J Virol 23: 608–615PubMedGoogle Scholar
  141. 141.
    Boone RF, Moss B (1978) Sequence complexity and relative abundance of vaccinia virus mRNA’synthesized in vivo and in vitro. J Virol 26: 554–569PubMedGoogle Scholar
  142. 142.
    Davison AJ, Moss B (1989) Structure of vaccinia virus early promoters. J Mol Biol 210: 749–769PubMedCrossRefGoogle Scholar
  143. 143.
    Yuen L, Moss B (1987) Oligonucleotide sequence signaling transcriptional termination of vaccinia virus early genes. Proc Natl Acad Sci USA 84: 6417–6421PubMedCrossRefGoogle Scholar
  144. 144.
    Shuman S, Moss B (1988) Factor-dependent transcription termination by vaccinia virus RNA polymerase. Evidence that the cis-acting termination signal is in nascent RNA. J Biol Chem 263: 6220–6225PubMedGoogle Scholar
  145. 145.
    Mallardo M, Schleich S, Krijnse Locker J (2001) Microtubule-dependent organization of vaccinia virus core-derived early mRNAs into distinct cytoplasmic structures. Mol Biol Cell 12: 3875–3891PubMedGoogle Scholar
  146. 146.
    Vos JC, Stunnenberg HG (1988) Derepression of a novel class of vaccinia virus genes upon DNA replication. EMBO J7: 3487–3492PubMedGoogle Scholar
  147. 147.
    Baldick CJ Jr, Keck JG, Moss B (1992) Mutational analysis of the core, spacer, and initiator regions of vaccinia virus intermediate-class promoters. J Virol 66: 4710–4719PubMedGoogle Scholar
  148. 148.
    Harris N, Rosales R, Moss B (1993) Transcription initiation factor activity of vaccinia virus capping enzyme is independent of mRNA guanylylation. Proc Natl Acad Sci USA 90: 2860–2864PubMedCrossRefGoogle Scholar
  149. 149.
    Rosales R, Harris N, Ahn BY, Moss B (1994) Purification and identification of a vaccinia virus-encoded intermediate stage promoter-specific transcription factor that has homology to eukaryotic transcription factor SII (TFIIS) and an additional role as a viral RNA polymerase subunit. J Biol Chem 269: 14260–14267PubMedGoogle Scholar
  150. 150.
    Sanz P, Moss B (1999) Identification of a transcription factor, encoded by two vaccinia virus early genes, that regulates the intermediate stage of viral gene expression. Proc Natl Acad Sci USA 96: 2692–2697PubMedCrossRefGoogle Scholar
  151. 151.
    Rosales R, Sutter G, Moss B (1994) A cellular factor is required for transcription of vaccinia viral intermediate-stage genes. Proc Natl Acad Sci USA 91: 3794–3798PubMedCrossRefGoogle Scholar
  152. 152.
    Keck JG, Baldick CJ Jr, Moss B (1990) Role of DNA replication in vaccinia virus gene expression: a naked template is required for transcription of three late trans-activator genes. Cell 61: 801–809PubMedCrossRefGoogle Scholar
  153. 153.
    Rosel JL, Earl PL, Weir JP, 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 HindIII H genome fragment. J Virol 60: 436–449PubMedGoogle Scholar
  154. 154.
    Davison AJ, Moss B (1989) Structure of vaccinia virus late promoters. J Mol Biol 210: 771–784PubMedCrossRefGoogle Scholar
  155. 155.
    Wright CF, Coroneos AM (1993) Purification of the late transcription system of vaccinia virus: identification of a novel transcription factor. J Virol 67: 7264–7270PubMedGoogle Scholar
  156. 156.
    Kovacs GR, Rosales R, Keck JG, Moss B (1994) Modification of the cascade model for regulation of vaccinia virus gene expression: purification of a prereplicative, late-stage-specific transcription factor. J Virol 68: 3443–3447PubMedGoogle Scholar
  157. 157.
    Wright CF, Hubbs AE, Gunasinghe SK, Oswald BW (1998) A vaccinia virus late transcription factor copurifies with a factor that binds to a viral late pro.moter and is complemented by extracts from uninfected HeLa cells. J Virol 72: 1446–1451PubMedGoogle Scholar
  158. 158.
    Gunasinghe SK, Hubbs AE, Wright CF (1998) A vaccinia virus late transcription factor with biochemical and molecular identity to a human cellular protein. J Biol Chem 273: 27524–27530PubMedCrossRefGoogle Scholar
  159. 159.
    Bertholet C, Van Meir E, ten Heggeler-Bordier B, Wittek R (1987) Vaccinia virus produces late mRNAs by discontinous synthesis. Cell 50: 153–162PubMedCrossRefGoogle Scholar
  160. 160.
    Schwer B, Visca P, Vos JC, Stunnenberg HG (1987) Discontinuous transcription or RNA processing of vaccinia virus late messengers results in a 5’ poly(A) leader. Cell 50: 163–169PubMedCrossRefGoogle Scholar
  161. 161.
    Cooper JA, Wittek R, Moss B (1981) Extension of the transcriptional and translational map of the left end of the vaccinia virus genome to 21 kilobase pairs. J Virol 39: 733–745PubMedGoogle Scholar
  162. 162.
    Salzman NP (1960) The rate of formation of vaccinia deoxyribonucleic acid and vaccinia virus. Virology 10: 150–152PubMedCrossRefGoogle Scholar
  163. 163.
    Challberg MD, Englund PT (1979) Purification and properties of the deoxyribonucleic acid polymerase induced by vaccinia virus. J Biol Chem 254: 7812–7819PubMedGoogle Scholar
  164. 164.
    Klemperer N, McDonald W, Boyle K, Unger B, Traktman P (2001) The A20R protein is a stoichiometric component of the processive form of vaccinia virus DNA polymerase. J Virol 75: 12298–12307PubMedCrossRefGoogle Scholar
  165. 165.
    Lin S, Chen W, Broyles SS (1992) The vaccinia virus B1R gene product is a serine/threonine protein kinase. J Virol 66: 2717–2723PubMedGoogle Scholar
  166. 166.
    Banham AH, Smith GL (1992) Vaccinia virus gene B1R encodes a 34-kDa serine/threonine protein kinase that localizes in cytoplasmic factories and is packaged into virions. Virology 191: 803–812PubMedCrossRefGoogle Scholar
  167. 167.
    Evans E, Klemperer N, Ghosh R, Traktman P (1995) The vaccinia virus D5 protein, which is required for DNA replication, is a nucleic acid-independent nucleoside triphosphatase. J Virol 69: 5353–5361PubMedGoogle Scholar
  168. 168.
    Millns AK, Carpenter MS, DeLange AM (1994) The vaccinia virus-encoded uracil DNA glycosylase has an essential role in viral DNA replication. Virology 198: 504–513PubMedCrossRefGoogle Scholar
  169. 169.
    Moss B (2001) Poxviridae: the viruses and their replication. In: BN Fields, DM Knipe, PM Howley, RM Chanock, J Melnick, TP Monath, B Roizman, SE Straus (eds): Virology. Lippincott-Raven Publishers, Philadelphia, 2849–2883Google Scholar
  170. 170.
    Kerr SM, Smith GL (1989) Vaccinia virus encodes a polypeptide with DNA ligase activity. Nucleic Acids Res 17: 9039–9050PubMedCrossRefGoogle Scholar
  171. 171.
    Smith GL, Chan YS, Kerr SM (1989) Transcriptional mapping and nucleotide sequence of a vaccinia virus gene encoding a polypeptide with extensive homology to DNA ligases. Nucleic Acids Res 17: 9051–9062PubMedCrossRefGoogle Scholar
  172. 172.
    Kerr SM, Smith GL (1991) Vaccinia virus DNA ligase is nonessential for virus replication: recovery of plasmids from virus-infected cells. Virology 180: 625–632PubMedCrossRefGoogle Scholar
  173. 173.
    Kerr SM, Johnston LH, Odell M, Duncan SA, Law KM, Smith GL (1991) Vaccinia DNA ligase complements Saccharomyces cerevisiae cdc9, localizes in cytoplasmic factories and affects virulence and virus sensitivity to DNA damaging agents. EMBO J 10: 4343–4350PubMedGoogle Scholar
  174. 174.
    Slabaugh MB, Mathews CK (1984) Vaccinia virus-induced ribonucleotide reductase can be distinguished from host cell activity. J Virol 52: 501–506PubMedGoogle Scholar
  175. 175.
    Slabaugh M, Roseman N, Davis R, Mathews C (1988) Vaccinia virus-encoded ribonucleotide reductase: sequence conservation of the gene for the small subunit and its amplification in hydroxyurea-resistant mutants. J Virol 62: 519–527PubMedGoogle Scholar
  176. 176.
    Tengelsen LA, Slabaugh MB, Bibler JK, Hruby DE (1988) Nucleotide sequence and molecular genetic analysis of the large subunit of ribonucleotide reductase encoded by vaccinia virus Virology 164: 121–131PubMedCrossRefGoogle Scholar
  177. 177.
    Child SJ, Palumbo GJ, Buller RM, Hruby DE (1990) Insertional inactivation of the large subunit of ribonucleotide reductase encoded by vaccinia virus is associated with reduced virulence in vivo. Virology 174: 625–629PubMedCrossRefGoogle Scholar
  178. 178.
    Howell ML, Sanders-Loehr J, Loehr TM, Roseman NA, Mathews CK, Slabaugh MB (1992) Cloning of the vaccinia virus ribonucleotide reductase small subunit gene. Characterization of the gene product expressed in Escherichia coli. J Biol Chem 267: 1705–1711Google Scholar
  179. 179.
    Bajszar G, Wittek R, Weir JP, Moss B (1983) Vaccinia virus thymidine kinase and neighboring genes: mRNAs and polypeptides of wild-type virus and putative nonsense mutants. J Virol 45: 62–72PubMedGoogle Scholar
  180. 180.
    Hruby DE, Maki RA, Miller DB, Ball LA (1983) Fine structure analysis and nucleotide sequence of the vaccinia virus thymidine kinase gene. Proc Natl Acad Sci USA 80: 3411–3415PubMedCrossRefGoogle Scholar
  181. 181.
    Black ME, Hruby DE (1992) Site-directed mutagenesis of a conserved domain in vaccinia virus thymidine kinase. Evidence for a potential role in magnesium binding. J Biol Chem 267: 6801–6806Google Scholar
  182. 182.
    Black ME, Hruby DE (1992) A single amino acid substitution abolishes feedback inhibition of vaccinia virus thymidine kinase. J Biol Chem 267: 9743–9748PubMedGoogle Scholar
  183. 183.
    Buller RM, Smith GL, Cremer K, Notkins AL, Moss B (1985) Decreased virulence of recombinant vaccinia virus expression vectors is associated with a thymidine kinase-negative phenotype. Nature 317: 813–815PubMedCrossRefGoogle Scholar
  184. 184.
    Smith GL, de Carlos A, Chan YS (1989) Vaccinia virus encodes a thymidylate kinase gene: sequence and transcriptional mapping. Nucleic Acids Res 17: 7581–7590PubMedCrossRefGoogle Scholar
  185. 185.
    Hughes SJ, Johnston LH, de Carlos A, Smith GL (1991) Vaccinia virus encodes an active thymidylate kinase that complements a cdc8_mutant of Saccharomyces cerevisiae. J Biol Chem 266: 20103–20109PubMedGoogle Scholar
  186. 186.
    Slabaugh MB, Roseman NA (1989) Retroviral protease-like gene in the vaccinia virus genome. Proc Natl Acad Sci USA 86: 4152–4155PubMedCrossRefGoogle Scholar
  187. 187.
    McGeoch DJ (1990) Protein sequence comparisons show that the #x2018;qpseudoproteases’ encoded by poxviruses and certain retroviruses belong to the deoxyuridine triphosphatase family. Nucleic Acids Res 18: 4105–4110PubMedCrossRefGoogle Scholar
  188. 188.
    Broyles SS (1993) Vaccinia virus encodes a functional dUTPase. Virology 195: 863–865PubMedCrossRefGoogle Scholar
  189. 189.
    Perkus ME, Goebel SJ, Davis SW, Johnson GP, Norton EK, Paoletti E (1991) Deletion of 55 open reading frames from the termini of vaccinia virus. Virology 180: 406–410PubMedCrossRefGoogle Scholar
  190. 190.
    Smith GL, Chan YS, Howard ST (1991) Nucleotide sequence of 42 kbp of vaccinia virus strain WR from near the right inverted terminal repeat. J Gen Virol 72: 1349–1376PubMedGoogle Scholar
  191. 191.
    Aguado B, Selmes IP, Smith GL (1992) Nucleotide sequence of 21.8 kbp of variola major virus strain Harvey and comparison with vaccinia virus. J Gen Virol 73: 2887–2902PubMedGoogle Scholar
  192. 192.
    DeLange AM (1989) Identification of temperature-sensitive mutants of vaccinia virus that are defective in conversion of concatemeric replicative intermediates to the mature linear DNA genome. J Virol 63: 2437–2444PubMedGoogle Scholar
  193. 193.
    Shuman S, Moss B (1987) Identification of a vaccinia virus gene encoding a type I DNA topoisomerase. Proc Natl Acad Sci USA 84: 7478–7482PubMedCrossRefGoogle Scholar
  194. 194.
    Klemperer N, Traktman P (1993) Biochemical analysis of mutant alleles of the vaccinia virus topoisomerase I carrying targeted substitutions in a highly conserved domain. J Biol Chem 268: 15887–15899PubMedGoogle Scholar
  195. 195.
    Eckert D, Williams O, Meseda CA, Merchlinsky M (2005) Vaccinia virus nicking-joining enzyme is encoded by K4L (VACWR035). J Virol 79: 15084–15090PubMedCrossRefGoogle Scholar
  196. 196.
    Garcia AD, Aravind L, Koonin EV, Moss B (2000) Bacterial-type DNA holliday junction resolvases in eukaryotic viruses. Proc Natl Acad Sci USA 97: 8926–8931PubMedCrossRefGoogle Scholar
  197. 197.
    Garcia AD, Moss B (2001) Repression of vaccinia virus Holliday junction resolvase inhibits processing of viral DNA into unit-length genomes. J Virol 75: 6460–6471PubMedCrossRefGoogle Scholar
  198. 198.
    Cassetti MC, Merchlinsky M, Wolffe EJ, Weisberg AS, Moss B (1998) DNA packaging mutant: repression of the vaccinia virus A32_gene results in noninfectious, DNA-deficient, spherical, enveloped particles. J Virol 72: 5769–5780PubMedGoogle Scholar
  199. 199.
    Joklik WK, Becker Y (1964) The replication and coating of vaccinia DNA. J Mol Biol 10: 452–474PubMedCrossRefGoogle Scholar
  200. 200.
    Dales S, Mosbach EH (1968) Vaccinia as a model for membrane biogenesis. Virology 35: 564–583PubMedCrossRefGoogle Scholar
  201. 201.
    Grimley PM, Rosenblum EN, Mims SJ, Moss B (1970) Interruption by Rifampin of an early stage in vaccinia virus morphogenesis: accumulation of membranes which are precursors of virus envelopes. J Virol 6: 519–533PubMedGoogle Scholar
  202. 202.
    Griffiths G, Roos N, Schleich S, Locker JK (2001) Structure and assembly of intracellular mature vaccinia virus: thin-section analyses. J Virol 75: 11056–11070PubMedCrossRefGoogle Scholar
  203. 203.
    Heuser J (2005) Deep-etch EM reveals that the early poxvirus envelope is a single membrane bilayer stabilized by a geodetic “honeycomb” surface coat. J Cell Biol 169: 269–283PubMedCrossRefGoogle Scholar
  204. 204.
    Traktman P, Caligiuri A, Jesty SA, Liu K, Sankar U (1995) Temperature-sensitive mutants with lesions in the vaccinia virus F10 kinase undergo arrest at the earliest stage of virion morphogenesis. J Virol 69: 6581–6587PubMedGoogle Scholar
  205. 205.
    Wang S, Shuman S (1995) Vaccinia virus morphogenesis is blocked by temperature-sensitive mutations in the F10 gene, which encodes protein kinase 2. J Virol 69: 6376–6388PubMedGoogle Scholar
  206. 206.
    DeMasi J, Traktman P (2000) Clustered charge-to-alanine mutagenesis of the vaccinia virus H5_gene: isolation of a dominant, temperature-sensitive mutant with a profound defect in morphogenesis. J Virol 74: 2393–2405PubMedCrossRefGoogle Scholar
  207. 207.
    Wolffe EJ, Moore DM, Peters PJ, Moss B (1996) Vaccinia virus A17L open reading frame encodes an essential component of nascent viral membranes that is required to initiate morphogenesis. J Virol 70: 2797–2808PubMedGoogle Scholar
  208. 208.
    Rodriguez JR, Risco C, Carrascosa JL, Esteban M, Rodriguez D (1997) Characterization of early stages in vaccinia virus membrane biogenesis: implications of the 21-kilodalton protein and a newly identified 15-kilodalton envelope protein. J Virol 71: 1821–1833PubMedGoogle Scholar
  209. 209.
    Rodriguez JR, Risco C, Carrascosa JL, Esteban M, Rodriguez D (1998) Vaccinia virus 15-kilodalton (A14L) protein is essential for assembly and attachment of viral crescents to virosomes. J Virol 72: 1287–1296PubMedGoogle Scholar
  210. 210.
    Traktman P, Liu K, DeMasi J, Rollins R, Jesty S, Unger B (2000) Elucidating the essential role of the A14 phosphoprotein in vaccinia virus morphogenesis: construction and characterization of a tetracycline-inducible recombinant. J Virol 74: 3682–3695PubMedCrossRefGoogle Scholar
  211. 211.
    da Fonseca FG, Weisberg AS, Caeiro MF, Moss B (2004) Vaccinia virus mutants with alanine substitutions in the conserved G5R gene fail to initiate morphogenesis at the nonpermissive temperature. J Virol 78: 10238–10248PubMedCrossRefGoogle Scholar
  212. 212.
    Moss B, Rosenblum EN, Katz E, Grimley PM (1969) Rifampicin: a specific inhibitor of vaccinia virus assembly. Nature 224: 1280–1284PubMedCrossRefGoogle Scholar
  213. 213.
    Tartaglia J, Piccini A, Paoletti E (1986) Vaccinia virus rifampicin-resistance locus specifies a late 63,000 Da gene product. Virology 150: 45–54PubMedCrossRefGoogle Scholar
  214. 214.
    Baldick CJ Jr, Moss B (1987) Resistance of vaccinia virus to rifampicin conferred by a single nucleotide substitution near the predicted NH2 terminus of a gene encoding an Mr 62,000 polypeptide. Virology 156: 138–145PubMedCrossRefGoogle Scholar
  215. 215.
    Zhang Y, Moss B (1992) Immature viral envelope formation is interrupted at the same stage by lac operator-mediated repression of the vaccinia virus D13L gene and by the drug rifampicin. Virology 187: 643–653PubMedCrossRefGoogle Scholar
  216. 216.
    Szajner P, Weisberg AS, Lebowitz J, Heuser J, Moss B (2005) External scaffold of spherical immature poxvirus particles is made of protein trimers, forming a honeycomb lattice. J Cell Biol 170: 971–981PubMedCrossRefGoogle Scholar
  217. 217.
    Resch W, Weisberg AS, Moss B (2005) Vaccinia virus nonstructural protein encoded by the A11R gene is required for formation of the virion membrane. J Virol 79: 6598–6609PubMedCrossRefGoogle Scholar
  218. 218.
    Szajner P, Weisberg AS, Wolffe EJ, Moss B (2001) Vaccinia virus A30L protein is required for association of viral membranes with dense viroplasm to form immature virions. J Virol 75: 5752–5761PubMedCrossRefGoogle Scholar
  219. 219.
    Szajner P, Jaffe H, Weisberg AS, Moss B (2003) Vaccinia virus G7L protein interacts with the A30L protein and is required for association of viral membranes with dense viroplasm to form immature virions. J Virol 77: 3418–3429PubMedCrossRefGoogle Scholar
  220. 220.
    Yeh WW, Moss B, Wolffe EJ (2000) The vaccinia virus A9L gene encodes a membrane protein required for an early step in virion morphogenesis. J Virol 74: 9701–9711PubMedCrossRefGoogle Scholar
  221. 221.
    Ravanello MP, Hruby DE (1994) Characterization of the vaccinia virus L1R myristylprotein as a component of the intracellular virion envelope. J Gen Virol 75: 1479–1483PubMedGoogle Scholar
  222. 222.
    Ravanello MP, Hruby DE (1994) Conditional lethal expression of the vaccinia virus L1R myristylated protein reveals a role in virion assembly. J Virol 68: 6401–6410PubMedGoogle Scholar
  223. 223.
    da Fonseca FG, Wolffe EJ, Weisberg A, Moss B (2000) Effects of deletion or stringent repression of the H3L envelope gene on vaccinia virus replication. J Virol 74: 7518–7528PubMedCrossRefGoogle Scholar
  224. 224.
    da Fonseca FG, Wolffe EJ, 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: 7508–7517PubMedCrossRefGoogle Scholar
  225. 225.
    Zhang YF, Moss B (1991) Vaccinia virus morphogenesis is interrupted when expression of the gene encoding an 11-kilodalton phosphorylated protein is prevented by the Escherichia coli lac repressor. J Virol 65: 6101–6110PubMedGoogle Scholar
  226. 226.
    Klemperer N, Ward J, Evans E, Traktman P (1997) The vaccinia virus I1 protein is essential for the assembly of mature virions. J Virol 71: 9285–9294PubMedGoogle Scholar
  227. 227.
    Moss B, Rosenblum EN (1973) Protein cleavage and poxvirus morphogenesis: tryptic peptide analysis of core precursors accumulated by blocking assembly with rifampicin. J Mol Biol 81: 267–269PubMedCrossRefGoogle Scholar
  228. 228.
    Lee P, Hruby DE (1994) Proteolytic cleavage of vaccinia virus virion proteins. Mutational analysis of the specificity determinants. J Biol Chem 269: 8616–8622Google Scholar
  229. 229.
    Katz E, Moss B (1970) Formation of a vaccinia virus structural polypeptide from a higher molecular weight precursor: inhibition by rifampicin. Proc Natl Acad Sci USA 66: 677–684PubMedCrossRefGoogle Scholar
  230. 230.
    Niles EG, Seto J (1988) Vaccinia virus gene D8 encodes a virion transmembrane protein. J Virol 62: 3772–3778PubMedGoogle Scholar
  231. 231.
    Rodriguez JF, Esteban M (1987) Mapping and nucleotide sequence of the vaccinia virus gene that encodes a 14-kilodalton fusion protein. J Virol 61: 3550–3554PubMedGoogle Scholar
  232. 232.
    Betakova T, Wolffe EJ, Moss B (2000) The vaccinia virus A14.5L gene encodes a hydrophobic 53-amino-acid virion membrane protein that enhances virulence in mice and is conserved among vertebrate poxviruses. J Virol 74: 4085–4092PubMedCrossRefGoogle Scholar
  233. 233.
    Rodriguez D, Rodriguez JR, 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. J Virol 67: 3435–3440PubMedGoogle Scholar
  234. 234.
    Rodriguez D, Esteban M, Rodriguez JR (1995) Vaccinia virus A17L gene product is essential for an early step in virion morphogenesis. J Virol 69: 4640–4648PubMedGoogle Scholar
  235. 235.
    Wallengren K, Risco C, Krijnse-Locker J, Esteban M, Rodriguez D (2001) The A17L gene product of vaccinia virus is exposed on the surface of IMV. Virology 290: 143–152PubMedCrossRefGoogle Scholar
  236. 236.
    Rodriguez JF, Janeczko R, Esteban M (1985) Isolation and characterization of neutralizing monoclonal antibodies to vaccinia virus. J Virol 56: 482–488PubMedGoogle Scholar
  237. 237.
    Davies DH, McCausland MM, Valdez C, Huynh D, Hernandez JE, Mu Y, Hirst S, Villarreal L, Felgner PL, Crotty S (2005) Vaccinia virus H3L envelope protein is a major target of neutralizing antibodies in humans and elicits protection against lethal challenge in mice. J Virol 79: 11724–11733PubMedCrossRefGoogle Scholar
  238. 238.
    Ichihashi Y, Oie M (1996) Neutralizing epitope on penetration protein of vaccinia virus. Virology 220: 491–494PubMedCrossRefGoogle Scholar
  239. 239.
    Senkevich TG, White CL, Koonin EV, Moss B (2002) Complete pathway for protein disulfide bond formation encoded by poxviruses. Proc Natl Acad Sci USA 99: 6667–6672PubMedCrossRefGoogle Scholar
  240. 240.
    Senkevich TG, Weisberg AS, Moss B (2000) Vaccinia virus E10R protein is associated with the membranes of intracellular mature virions and has a role in morphogenesis. Virology 278: 244–252PubMedCrossRefGoogle Scholar
  241. 241.
    Senkevich TG, White CL, Koonin EV, Moss B (2000) A viral member of the ERV1/ALR protein family participates in a cytoplasmic pathway of disulfide bond formation. Proc Natl Acad Sci USA 97: 12068–12073PubMedCrossRefGoogle Scholar
  242. 242.
    White CL, Senkevich TG, Moss B (2002) Vaccinia virus G4L glutaredoxin is an essential intermediate of a cytoplasmic disulfide bond pathway required for virion assembly. J Virol 76: 467–472PubMedCrossRefGoogle Scholar
  243. 243.
    Senkevich TG, White CL, Weisberg A, Granek JA, Wolffe EJ, Koonin EV, Moss B (2002) Expression of the vaccinia virus A2.5L redox protein is required for virion morphogenesis. Virology 300: 296–303PubMedCrossRefGoogle Scholar
  244. 244.
    Sanderson CM, Hollinshead M, Smith GL (2000) The vaccinia virus A27L protein is needed for the microtubule-dependent transport of intracellular mature virus particles. J Gen Virol 81: 47–58PubMedGoogle Scholar
  245. 245.
    Hiller G, Weber K (1985) Golgi-derived membranes that contain an acylated viral polypeptide are used for vaccinia virus envelopment. J Virol 55: 651–659PubMedGoogle Scholar
  246. 246.
    Hirt P, Hiller G, Wittek R (1986) Localization and fine structure of a vaccinia virus gene encoding an envelope antigen. J Virol 58: 757–764PubMedGoogle Scholar
  247. 247.
    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: 5910–5920PubMedGoogle Scholar
  248. 248.
    Hiller G, Eibl H, Weber K (1981) Characterization of intracellular and extracellular vaccinia virus variants: N1-isonicotinoyl-N2-3-methyl-4-chlorobenzoylhydrazine interferes with cytoplasmic virus dissemination and release. J Virol 39: 903–913PubMedGoogle Scholar
  249. 249.
    Yang G, Pevear DC, Davies MH, Collett MS, Bailey T, Rippen S, Barone L, Burns C, Rhodes G, Tohan S et al (2005) An orally bioavailable antipoxvirus compound (ST-246) inhibits extracellular virus formation and protects mice from lethal orthopoxvirus challenge. J Virol 79: 13139–13149PubMedCrossRefGoogle Scholar
  250. 250.
    Schmutz C, Payne LG, 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. J Virol 65: 3435–3442PubMedGoogle Scholar
  251. 251.
    Ponting CP, Kerr ID (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 Sci 5: 914–922PubMedCrossRefGoogle Scholar
  252. 252.
    Baek SH, Kwak JY, Lee SH, Lee T, Ryu SH, Uhlinger DJ, Lambeth JD (1997) Lipase activities of p37, the major envelope protein of vaccinia virus. J Biol Chem 272: 32042–32049PubMedCrossRefGoogle Scholar
  253. 253.
    Sung TC, Roper RL, Zhang Y, Rudge SA, Temel R, Hammond SM, Morris AJ, Moss B, Engebrecht J, Frohman MA (1997) Mutagenesis of phospholipase D defines a superfamily including a trans-Golgi viral protein required for poxvirus pathogenicity. EMBO J 16: 4519–4530PubMedCrossRefGoogle Scholar
  254. 254.
    Schmutz C, Rindisbacher L, Galmiche MC, Wittek R (1995) Biochemical analysis of the major vaccinia virus envelope antigen. Virology 213: 19–27PubMedCrossRefGoogle Scholar
  255. 255.
    Grosenbach DW, Hansen SG, Hruby DE (2000) Identification and analysis of vaccinia virus palmitylproteins. Virology 275: 193–206PubMedCrossRefGoogle Scholar
  256. 256.
    Grosenbach DW, Hruby DE (1998) Analysis of a vaccinia virus mutant expressing a nonpalmitylated form of p37, a mediator of virion envelopment. J Virol 72: 5108–5120PubMedGoogle Scholar
  257. 257.
    Husain M, Moss B (2002) Similarities in the induction of post-Golgi vesicles by the vaccinia virus F13L protein and phospholipase D. J Virol 76: 7777–7789PubMedCrossRefGoogle Scholar
  258. 258.
    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: 7528–7542PubMedCrossRefGoogle Scholar
  259. 259.
    Roper RL, Moss B (1999) Envelope formation is blocked by mutation of a sequence related to the HKD phospholipid metabolism motif in the vaccinia virus F13L protein. J Virol 73: 1108–1117PubMedGoogle Scholar
  260. 260.
    Martinez-Pomares L, Stern RJ, Moyer RW (1993) The ps/hr gene (B5R open reading frame homolog) of rabbitpox virus controls pock color, is a component of extracellular enveloped virus, and is secreted into the medium. J Virol 67: 5450–5462PubMedGoogle Scholar
  261. 261.
    Engelstad M, Smith GL (1993) The vaccinia virus 42-kDa envelope protein is required for the envelopment and egress of extracellular virus and for virus virulence. Virology 194: 627–637PubMedCrossRefGoogle Scholar
  262. 262.
    Wolffe EJ, Isaacs SN, 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: 4732–4741PubMedGoogle Scholar
  263. 263.
    Herrera E, Lorenzo MM, Blasco R, Isaacs SN (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: 294–302PubMedGoogle Scholar
  264. 264.
    Cudmore S, Cossart P, Griffiths G, Way M (1995) Actin-based motility of vaccinia virus. Nature 378: 636–638PubMedCrossRefGoogle Scholar
  265. 265.
    Hollinshead M, Rodger G, Van Eijl H, Law M, Hollinshead R, Vaux DJ, Smith GL (2001) Vaccinia virus utilizes microtubules for movement to the cell surface. J Cell Biol 154: 389–402PubMedCrossRefGoogle Scholar
  266. 266.
    Ward BM, Moss B (2001) Vaccinia virus intracellular movement is associated with microtubules and independent of actin tails. J Virol 75: 11651–11663PubMedCrossRefGoogle Scholar
  267. 267.
    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. Nat Cell Biol 3: 992–1000PubMedCrossRefGoogle Scholar
  268. 268.
    Geada MM, Galindo I, Lorenzo MM, Perdiguero B, Blasco R (2001) Movements of vaccinia virus intracellular enveloped virions with GFP tagged to the F13L envelope protein. J Gen Virol 82: 2747–2760PubMedGoogle Scholar
  269. 269.
    Ward BM, Moss B (2001) Visualization of intracellular movement of vaccinia virus virions containing a green fluorescent protein-B5R membrane protein chimera. J Virol 75: 4802–4813PubMedCrossRefGoogle Scholar
  270. 270.
    Zhang WH, Wilcock D, Smith GL (2000) Vaccinia virus F12L protein is required for actin tail formation, normal plaque size, and virulence. J Virol 74: 11654–11662PubMedCrossRefGoogle Scholar
  271. 271.
    Ward BM, Moss B (2004) Vaccinia virus A36R membrane protein provides a direct link between intracellular enveloped virions and the microtubule motor kinesin. J Virol 78: 2486–2493PubMedCrossRefGoogle Scholar
  272. 272.
    Sanderson CM, Frischknecht F, Way M, Hollinshead M, Smith GL (1998) Roles of vaccinia virus EEV-specific proteins in intracellular actin tail formation and low pH-induced cell-cell fusion. J Gen Virol 79: 1415–1425PubMedGoogle Scholar
  273. 273.
    Wolffe EJ, Weisberg AS, 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: 20–26PubMedCrossRefGoogle Scholar
  274. 274.
    van Eijl H, Hollinshead M, Smith GL (2000) The vaccinia virus A36R protein is a type Ib membrane protein present on intracellular but not extracellular enveloped virus particles. Virology 271: 26–36PubMedCrossRefGoogle Scholar
  275. 275.
    Herrero-Martinez E, Roberts KL, Hollinshead M, Smith GL (2005) Vaccinia virus intracellular enveloped virions move to the cell periphery on microtubules in the absence of the A36R protein.J Gen Virol 86: 2961–2968PubMedCrossRefGoogle Scholar
  276. 276.
    van Eijl H, Hollinshead M, Rodger G, Zhang WH, Smith GL (2002) The vaccinia virus F12L protein is associated with intracellular enveloped virus particles and is required for their egress to the cell surface. J Gen Virol 83: 195–207PubMedGoogle Scholar
  277. 277.
    Hiller G, Weber K, Schneider L, Parajsz C, Jungwirth C (1979) Interaction of assembled progeny pox viruses with the cellular cytoskeleton. Virology 98: 142–153PubMedCrossRefGoogle Scholar
  278. 278.
    Blasco R, Cole NB, Moss B (1991) Sequence analysis, expression, and deletion of a vaccinia virus gene encoding a homolog of profilin, a eukaryotic actinbinding protein. J Virol 65: 4598–4608PubMedGoogle Scholar
  279. 279.
    Frischknecht F, Moreau V, Rottger S, Gonfloni S, Reckmann I, Superti-Furga G, Way M (1999) Actin-based motility of vaccinia virus mimics receptor tyrosine kinase signaling. Nature 401: 926–929PubMedCrossRefGoogle Scholar
  280. 280.
    Scaplehorn N, Holmstrom A, Moreau V, Frischknecht F, Reckmann I, Way M (2002) Grb2_and Nck act cooperatively to promote actin-based motility of vaccinia virus. Curr Biol 12: 740–745PubMedCrossRefGoogle Scholar
  281. 281.
    Newsome TP, Scaplehorn N, Way M (2004) Src mediates a switch from microtubuleto actin-based motility of vaccinia virus. Science 306: 124–129PubMedCrossRefGoogle Scholar
  282. 282.
    Reeves PM, Bommarius B, Lebeis S, McNulty S, Christensen J, Swimm A, Chahroudi A, Chavan R, Feinberg MB, Veach D et al (2005) Disabling poxvirus pathogenesis by inhibition of Abl-family tyrosine kinases. Nat Med 11: 731–739PubMedCrossRefGoogle Scholar
  283. 283.
    Ward BM, Weisberg AS, Moss B (2003) Mapping and functional analysis of interaction sites within the cytoplasmic domains of the vaccinia virus A33R and A36R envelope proteins. J Virol 77: 4113–4126PubMedCrossRefGoogle Scholar
  284. 284.
    Smith GL, Murphy BJ, Law M (2003) Vaccinia virus motility. Annu Rev Microbiol 57: 323–342PubMedCrossRefGoogle Scholar
  285. 285.
    Smith GL, Law M (2004) The exit of Vaccinia virus from infected cells. Virus Res 106: 189–197PubMedCrossRefGoogle Scholar
  286. 286.
    Law M, Hollinshead R, Smith GL (2002) Antibody-sensitive and antibodyresistant cell-to-cell spread by vaccinia virus: role of the A33R protein in antibody-resistant spread. J Gen Virol 83: 209–222PubMedGoogle Scholar
  287. 287.
    Boulter EA, Appleyard G (1973) Differences between extracellular and intracellular forms of poxvirus and their implications. Prog Med Virol 16: 86–108PubMedGoogle Scholar
  288. 288.
    Payne LG (1980) Significance of extracellular enveloped virus in the in vitro and in vivo dissemination of vaccinia. J Gen Virol 50: 89–100PubMedCrossRefGoogle Scholar
  289. 289.
    Sanderson CM, Way M, Smith GL (1998) Virus-induced cell motility. J Virol 72: 1235–1243PubMedGoogle Scholar
  290. 290.
    Valderrama F, Cordeiro JV, Schleich S, Frischknecht F, Way M (2006) Vaccinia virus-induced cell motility requires F11L-mediated inhibition of RhoA signaling. Science 311: 377–381PubMedCrossRefGoogle Scholar
  291. 291.
    Payne LG (1979) Identification of the vaccinia hemagglutinin polypeptide from a cell system yielding large amounts of extracellular enveloped virus. J Virol 31: 147–155PubMedGoogle Scholar
  292. 292.
    Payne L (1978) Polypeptide composition of extracellular enveloped vaccinia virus. J Virol 27: 28–37PubMedGoogle Scholar
  293. 293.
    Roper RL, Payne LG, Moss B (1996) Extracellular vaccinia virus envelope glycoprotein encoded by the A33R gene. J Virol 70: 3753–3762PubMedGoogle Scholar
  294. 294.
    Duncan SA, Smith GL (1992) Identification and characterization of an extracellular envelope glycoprotein affecting vaccinia virus egress. J Virol 66: 1610–1621PubMedGoogle Scholar
  295. 295.
    Shida H (1986) Nucleotide sequence of the vaccinia virus hemagglutinin gene. Virology 150: 451–462PubMedCrossRefGoogle Scholar
  296. 296.
    Brum LM, Turner PC, Devick H, Baquero MT, Moyer RW (2003) Plasma membrane localization and fusion inhibitory activity of the cowpox virus serpin SPI-3 require a functional signal sequence and the virus encoded hemagglutinin. Virology 306: 289–302PubMedCrossRefGoogle Scholar
  297. 297.
    Roper RL, Wolffe EJ, 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. J Virol 72: 4192–4204PubMedGoogle Scholar
  298. 298.
    McIntosh AA, Smith GL (1996) Vaccinia virus glycoprotein A34R is required for infectivity of extracellular enveloped virus. J Virol 70: 272–281PubMedGoogle Scholar
  299. 299.
    Blasco R, Sisler JR, 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: 3319–3325PubMedGoogle Scholar
  300. 300.
    Katz E, Wolffe E, Moss B (2002) Identification of second-site mutations that enhance release and spread of vaccinia virus. J Virol 76: 11637–11644PubMedCrossRefGoogle Scholar
  301. 301.
    Katz E, Ward BM, Weisberg AS, Moss B (2003) Mutations in the vaccinia virus A33R and B5R envelope proteins that enhance release of extracellular virions and eliminate formation of actin-containing microvilli without preventing tyrosine phosphorylation of the A36R protein. J Virol 77: 12266–12275PubMedCrossRefGoogle Scholar
  302. 302.
    Parkinson JE, Smith GL (1994) Vaccinia virus gene A36R encodes a M(r) 43-50 K protein on the surface of extracellular enveloped virus. Virology 204: 376–390PubMedCrossRefGoogle Scholar
  303. 303.
    Delhon G, Tulman ER, Afonso CL, Lu Z, de la Concha-Bermejillo A, Lehmkuhl HD, Piccone ME, Kutish GF, Rock DL (2004) Genomes of the parapoxviruses ORF virus and bovine papular stomatitis virus. J Virol 78: 168–177PubMedCrossRefGoogle Scholar
  304. 304.
    Tikkanen MK, McInnes CJ, Mercer AA, Buttner M, Tuimala J, Hirvela-Koski V, Neuvonen E, Huovilainen A (2004) Recent isolates of parapoxvirus of Finnish reindeer (Rangifer tarandus tarandus) are closely related to bovine pseudocowpox virus. J Gen Virol 85: 1413–1418PubMedCrossRefGoogle Scholar
  305. 305.
    Likos AM, Sammons SA, Olson VA, Frace AM, Li Y, Olsen-Rasmussen M, Davidson W, Galloway R, Khristova ML, Reynolds MG et al (2005) A tale of two clades: monkeypox viruses. J Gen Virol 86: 2661–2672PubMedCrossRefGoogle Scholar
  306. 306.
    Chen N, Li G, Liszewski MK, Atkinson JP, Jahrling PB, Feng Z, Schriewer J, Buck C, Wang C, Lefkowitz EJ et al (2005) Virulence differences between monkeypox virus isolates from West Africa and the Congo basin. Virology 340: 46–63PubMedCrossRefGoogle Scholar
  307. 307.
    Smith GL, Symons JA, Alcamí A (1998) Poxviruses: interfering with interferon. Semin Virol 8: 409–418CrossRefGoogle Scholar
  308. 308.
    Williamson JD, Reith RW, Jeffrey LJ, Arrand JR, Mackett M (1990) Biological characterization of recombinant vaccinia viruses in mice infected by the respiratory route. J Gen Virol 71: 2761–2767PubMedGoogle Scholar
  309. 309.
    Alcami A, Smith GL (1992) A soluble receptor for interleukin-1 beta encoded by vaccinia virus: a novel mechanism of virus modulation of the host response to infection. Cell 71: 153–167PubMedCrossRefGoogle Scholar
  310. 310.
    Lee MS, Roos JM, McGuigan LC, Smith KA, Cormier N, Cohen LK, Roberts BE, Payne LG (1992) Molecular attenuation of vaccinia virus: mutant generation and animal characterization. J Virol 66: 2617–2630PubMedGoogle Scholar
  311. 311.
    Symons JA, Alcami A, Smith GL (1995) Vaccinia virus encodes a soluble type I interferon receptor of novel structure and broad species specificity. Cell 81: 551–560PubMedCrossRefGoogle Scholar
  312. 312.
    Tscharke DC, Smith GL (1999) A model for vaccinia virus pathogenesis and immunity based on intradermal injection of mouse ear pinnae. J Gen Virol 80: 2751–2755PubMedGoogle Scholar
  313. 313.
    Tscharke DC, Reading PC, Smith GL (2002) Dermal infection with vaccinia virus reveals roles for virus proteins not seen using other inoculation routes. J Gen Virol 83: 1977–1986PubMedGoogle Scholar
  314. 314.
    Reading PC, Smith GL (2003) A kinetic analysis of immune mediators in the lungs of mice infected with vaccinia virus and comparison with intradermal infection. J Gen Virol 84: 1973–1983PubMedCrossRefGoogle Scholar
  315. 315.
    Jacobs N, Chen RA-J, Gubser C, Najarro P, Smith GL (2006) Intradermal immune response after infection with Vaccinia virus. J Gen Virol 87: 1157–1161PubMedCrossRefGoogle Scholar
  316. 316.
    Lee H-J, Essani K, Smith GL (2001) The genome sequence of Yaba-like disease virus, a yatapoxvirus. Virology 281: 170–192PubMedCrossRefGoogle Scholar

Copyright information

© Birkhäuser Verlag Basel/Switzerland 2007

Authors and Affiliations

  • Geoffrey L. Smith
    • 1
  1. 1.Department of Virology, Faculty of MedicineImperial College LondonLondonUK

Personalised recommendations