Vaccinia virus immune evasion

Immunological Reviews

Volumn 159, Issue , 1997, Pages 137-154

  Smith, Geoffrey L ^a   Symons, Julian A ^a   Khanna, Anu ^a   Vanderplasschen, Alain ^a   Alcamí, Antonio ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; COMPLEMENT; GAMMA INTERFERON; INTERFERON; INTERFERON RECEPTOR; INTERLEUKIN 1BETA; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; STEROID; TUMOR NECROSIS FACTOR RECEPTOR; VIRUS ANTIBODY; VIRUS PROTEIN; VIRUS VACCINE;

ANTIGEN PRESENTATION; APOPTOSIS; HUMAN; NONHUMAN; PRIORITY JOURNAL; REVIEW; VACCINIA VIRUS; VIRUS CELL INTERACTION; VIRUS IMMUNITY; VIRUS NEUTRALIZATION; VIRUS PATHOGENESIS; VIRUS REPLICATION;

EID: 0030696143     PISSN: 01052896     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1600-065X.1997.tb01012.x     Document Type: Review

References (148)

1. Fenner F, Anderson DA, Arita I, Jezek Z, Ladnyi ID. Smallpox and Its Eradication. Geneva: World Health Organisation; 1988.
2. Panicali D, Paoletti E. 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 1982;79:4927-4931.
3. Mackett M, Smith GL, Moss B. Vaccinia virus: a selectable eukaryotic cloning and expression vector. Proc Natl Acad Sci USA 1982;79:7415-7419.
4. Smith GL, Mackett M, Moss B. Infectious vaccinia virus recombinants that express hepatitis B virus surface antigen. Nature 1983;302:490-495.
5. Smith GL, Moss B. Infectious poxvirus vectors have capacity for at least 25,000 base pairs of foreign DNA. Gene 1983;25:21-28.
6. Brown F, Schild GC, Ada GL. Recombinant vaccinia viruses as vaccines. Nature 1986;319:549-550.
7. Moss B. Poxviridae: the viruses and their replication. In: Fields BN, Knipe DM, Howley PM, eds. Fields Virology. New York: Lippincott Raven Press; 1996. p. 2637-2671.
8. Sodeik B, et al. Assembly of vaccinia virus: role of the intermediate compartment between the endoplasmic reticulum and the Golgi stacks. J Cell Biol 1993;121:521-541.
9. Tooze J, Hollinshead M, Reis B, Radsak K, Kern H. Progeny vaccinia viruses and human cytomegalovirus particles utilize early endosomal cisternae for their envelopes. Eur J Cell Biol 1993;60:163-178.
10. Schmelz M, et al. Assembly of vaccinia virus: the second wrapping cisterna is derived from the trans Golgi network. J Virol 1994;68:130-147.
11. Cudmore S, Cossart P, Griffiths G, Way M. Actin-based motility of vaccinia virus. Nature 1995;378:636-638.
12. Blasco R, Moss B. Role of cell-associated enveloped vaccinia virus in cell-to-cell spread. J Virol 1992;66:4170-4179.
13. Smith GL. Vaccinia virus glycoproteins and immune evasion. The Sixteenth Fleming Lecture. J Gen Virol 1993;74:1725-1741.
14. Goebel SJ, Johnson GP, Perkus ME, Davis SW, Winslow JP, Paoletti E. The complete DNA sequence of vaccinia virus. Virology 1990;179:247-266.
15. Johnson GP, Goebel SJ, Paoletti E. An unpdate on the vaccinia virus genome. Virology 1993;196:381-401.
16. Smith GL, Chan YS, Howard ST. Nucleotide sequence of 42 kbp of vaccinia virus strain WR from near the right inverted terminal repeat. J Gen Virol 1991;72:1349-1376.
17. Appleyard G, Hapel AJ, Boulter EA. An antigenic difference between intracellular and extracellular rabbitpox virus. J Gen Virol 1971;13:9-17.
18. Turner GS, Squires EJ. Inactivated smallpox vaccine: immunogenicity of inactivated intracellular and extracellular vaccinia virus. J Gen Virol 1971;13:19-25.
19. Boulter EA, Appleyard G. Differences between extracellular and intracellular forms of poxviruses and their implications. Prog Med Virol 1973;16:86-108.
20. Appleyard G, Andrews C. Neutralizing activities of antisera to poxvirus soluble antigens. J Gen Virol 1974;23:197-200.
21. Payne LG. Significance of extracellular enveloped virus in the in vitro and in vivo dissemination of vaccinia virus. J Gen Virol 1980;50:89-100.
22. Ichihashi Y. Extracellular enveloped vaccinia virus escapes neutralization. Virology 1996;217:478-485.
23. Vanderplasschen A, Hollinshead M, Smith GL. Antibodies against vaccinia virus do not neutralise extracellular enveloped virus but prevent virus release from infected cells and comet formation. J Gen Virol 1997;78:2041-2048.
24. Czerny CP, Mahnel H. Structural and functional analysis of orthopoxvirus epitopes with neutralizing monoclonal antibodies. J Gen Virol 1990;71:2341-2352.
25. Baxby D. Jenner's Smallpox Vaccine. The Riddle of the Origin of Vaccinia Virus. London: Heinemann; 1981.
26. Wiertz EJHJ, Mukherjee S, Ploegh HL. Viruses use stealth technology to escape from the host immune system. Mol Med Today 1997;3:116-123.
27. Boshkov LK, Macen JL, McFadden G. Virus-induced loss of class I MHC antigens from the surface of cells infected with myxoma virus and malignant rabbit fibroma virus. J Immunol 1992;148:881-887.
28. Bennink JR, Yewdell JW. Recombinant vaccinia viruses as vectors for studying T lymphocyte specificity and function. Curr Top Microbiol Immunol 1990;163: 153-184.
29. Coupar BEH, Andrew ME, Both GW, Boyle DB. Temporal regulation of influenza hemagglutinin expression in vaccinia virus recombinants and effects on the immune response. Eur J Immunol 1986;16:1479-1487.
30. Townsend A, et al. Defective presentation to class I-restricted cytotoxic T lymphocytes in vaccinia-infected cells is overcome by enhanced degradation of antigen. J Exp Med 1988;168:1211-1224.
31. k-restricted cytotoxic T cell epitope in the NS1 protein of influenza virus using an MHC allele-specific motif. Virology 1993;193:289-295.
32. Pickup DJ, Ink BS, Hu W, Ray CA, Joklik WK. Hemorrhage in lesions caused by cowpox virus is induced by a viral protein that is related to plasma protein inhibitors of serine proteases. Proc Natl Acad Sci USA 1986;83:7698-7702.
33. Boursnell MEG, Foulds IJ, Campbell JI, Binns MM. Non-essential genes in the vaccinia virus HindIII K fragment: a gene related to serine protease inhibitors and a gene related to the 37K vaccinia virus major envelope antigen. J Gen Virol 1988;69:2995-3003.
34. Kotwal GJ, Moss B. Vaccinia virus encodes two proteins that are structurally related to members of the plasma serine protease inhibitor superfamily [published erratum appears in J Virol 1990;64:966]. J Virol 1989;63:600-606.
35. Smith GL, Howard ST, Chan YS. Vaccinia virus encodes a family of genes with homology to serine proteinase inhibitors. J Gen Virol 1989;70:2333-2343.
36. Law KM, Smith GL. A vaccinia serine protease inhibitor which prevents virus induced cell fusion. J Gen Virol 1992;73:549-557.
37. r 38.5 and 40 K, intracellular polypeptides that do not affect virus virulence in a murine intranasal model. Virology 1995;206:136-147.
38. Blake NW, et al. Vaccinia virus serpins B13R and B22R do not inhibit antigen presentation to class-I restricted cytotoxic T lymphocytes. J Gen Virol 1995;76:2693-2698.
39. Ray CA, et al. Viral inhibition of inflammation: cowpox virus encodes an inhibitor of the interleukin-1β converting enzyme. Cell 1992;69:597-604.
40. Tewari M, Telford WG, Miller RA, Dixit VM. CrmA, a poxvirus-encoded serpin, inhibits cytotoxic T-lymphocyte-mediated apoptosis. J Biol Chem 1995;270:22705-22708.
41. Macen JL, et al. Differential inhibition of the Fas- and granule-mediated cytolysis pathways by the orthopoxvirus cytokine response modifier A/SPI-2 and SPI-1 protein. Proc Natl Acad Sci USA 1996;93:9108-9113.
42. Gillet G, Brun G. Viral inhibition of apoptosis. Trends Microbiol 1996;4:312-317.
43. Komiyama T, et al. Inhibition of interleukin-1 beta converting enzyme by the cowpox virus serpin CrmA. An example of cross-class inhibition. J Biol Chem 1994;269:19331-19337.
44. Quan LT, Caputo A, Bleackley RC, Pickup DJ, Salvesen GS. Granzyme B is inhibited by the cowpox virus serpin cytokine response modifier A. J Biol Chem 1995;270:10377-10379.
45. Gagliardini V, et al. Prevention of vertebrate neuronal death by the crmA gene [published erratum appears in Science 1994;264:1388]. Science 1994;263:826-828.
46. Enari M, Hug H, Nagata S. Involvement of an ICE-like protease in Fas-mediated apoptosis. Nature 1995;375:78-81.
47. Los M, et al. Requirement of an ICE/CED-3 protease for Fas/APO-1-mediated apoptosis. Nature 1995;375:81-83.
48. Miura M, Friedlander RM, Yuan J. Tumor necrosis factor-induced apoptosis is mediated by a CrmA-sensitive cell death pathway. Proc Natl Acad Sci USA 1995;92:8318-8322.
49. Tewari M, Dixit VM. Fas- and tumor necrosis factor-induced apoptosis is inhibited by the poxvirus crmA gene product. J Biol Chem 1995;270:3255-3260.
50. Ray CA, Pickup DJ. The mode of death of pig kidney cells infected with cowpox virus is governed by the expression of the crmA gene. Virology 1996;217:384-391.
51. Heinkelein M, Pilz S, Jassoy C. Inhibition of CD95 (Fas/Apo1)-mediated apoptosis by vaccinia virus WR. Clin Exp Immunol 1996;103:8-14.
52. Dobbelstein M, Shenk T. Protection against apoptosis by the vaccinia virus SPI-2 (B13R) gene product. J Virol 1996;70:6479-6485.
53. Kettle S, Alcamí A, Khanna A, Ehret R, Jassoy C, Smith GL. Vaccinia virus serpin B13R (SPI-2) inhibits interleukin-1β converting enzyme and protects virus-infected cells from TNF- and Fas-mediated apoptosis but does not prevent IL-1β-induced fever. J Gen Virol 1997;78:677-685.
54. Ali AN, Turner PC, Brooks MA, Moyer RW. The SPI-1 gene of rabbitpox virus determines host range and is required for hemorrhagic pock formation. Virology 1994;202:305-314.
55. Brooks MA, Ali AN, Turner PC, Moyer RW. A rabbitpox virus serpin gene controls host range by inhibiting apoptosis in restrictive cells. J Virol 1995;69:7688-7698.
56. Lee SB, Esteban M. The interferon-induced double-stranded RNA-activated protein kinase induces apoptosis. Virology 1994;199:491-496.
57. Drillien R, Spehner D, Kirn A. Host range restriction of vaccinia virus in Chinese hamster ovary cells: relationship to shut off of host protein synthesis. J Virol 1978;28:843-850.
58. Hruby DE, Lynn DL, Condit RC, Kates JR. Cellular differences in the molecular mechanisms of vaccinia virus host range restriction. J Gen Virol 1980;47:485-488.
59. Spehner D, Gillard S, Drillien R, Kirn A. A cowpox virus gene required for multiplication in Chinese hamster ovary cells. J Virol 1988;62:1297-1304.
60. Ink BS, Gilbert CS, Evan GI. Delay of vaccinia virus-induced apoptosis in nonpermissive Chinese hamster ovary cells by the cowpox virus CHOhr and adenovirus E1B 19K genes. J Virol 1995;69:661-668.
61. Bertin J, et al. Death effector domain-containing herpesvirus and poxvirus proteins inhibit both Fas- and TNFR1-induced apoptosis. Proc Natl Acad Sci USA 1997;94:1172-1176.
62. Thome M, et al. Viral FLICE-inhibitory proteins (FLIPS) prevent apoptosis induced by death receptors. Nature 1997;386:517-521.
63. Macen JL, Graham KA, Lee SF, Schreiber M, Boshkov LK, McFadden G. Expression of the myxoma virus tumor necrosis factor receptor homologue and M11L genes is required to prevent virus-induced apoptosis in infected rabbit T lymphocytes. Virology 1996;218:232-237.
64. Schreiber M, Sedger L, McFadden G. Distinct domains of M-T2, the myxoma virus tumor necrosis factor (TNF) receptor homolog, mediate extracellular TNF binding and intracellular apoptosis inhibition. J Virol 1997;71:2171-2181.
65. Mossman K, Lee SF, Barry M, Boshkov L, McFadden G. Disruption of M-T5, a novel myxoma virus gene member of poxvirus host range superfamily, results in dramatic attenuation of myxomatosis in infected European rabbits. J Virol 1996;70:4394-4410.
66. Essani K, Chalasani S, Eversole R, Beuving L, Birmingham L. Multiple anti-cytokine activities secreted from tanapox virus-infected cells. Microb Pathog 1994;17:347-353.
67. Dinarello CA. Biological basis for interleukin-1 in disease. Blood 1996;87:2095-2147.
68. Symons JA, Eastgate JA, Duff GW. Purification and characterisation of a novel soluble receptor for interleukin-1. J Exp Med 1991;174:1251-1254.
69. Colotta F, et al. Interleukin-1 type II receptor: a decoy target for IL-1 that is regulated by IL-4. Science 1993;261:472-475.
70. Spriggs M, et al. Vaccinia and cowpox viruses encode a novel secreted interleukin-1 binding protein. Cell 1992;71:145-152.
71. Alcamí A, Smith GL. A soluble receptor for interleukin-1β encoded by vaccinia virus: a novel mechanism of virus modulation of the host response to infection. Cell 1992;71:153-167.
72. Turner PC, Musy PY, Moyer RW. Poxvirus serpins. In: McFadden G, ed. Viroceptors, virokines and related immune modulators encoded by DNA viruses. Austin: R.G. Landes Company; 1995. p. 67-88.
73. Alcamí A, Smith GL. A mechanism for the inhibition of fever by a virus. Proc Natl Acad Sci USA 1996;93: 11029-11034.
74. Ghayur T, et al. Caspase-1 processes IFN-γ-inducing factor and regulates LPS-induced IFN-γ production. Nature 1997;386:619-623.
75. Smith GL, Chan YS. Two vaccinia virus proteins structurally related to interleukin-1 receptor and the immunoglobulin superfamily. J Gen Virol 1991;72:511-518.
76. McMahan CJ, et al. A novel IL-1 receptor, cloned from B cells by mammalian expression, is expressed in many cell types. EMBO J 1991;10:2821-2832.
77. Zheng H, et al. Resistance to fever induction and impaired acute-phase response in interleukin-1β-deficient mice. Immunity 1995;3:9-19.
78. Kozak W, Zheng H, Conn CA, Soszynski D, van der Ploeg LH, Kluger MJ. Thermal and behavioral effects of lipopolysaccharide and influenza in interleukin-1 beta-deficient mice. Am J Physiol 1995;269:R969-977.
79. Shchelkunov SN, Blinov VM, Sandakhchiev LS. Genes of variola and vaccinia viruses necessary to overcome the host protective mechanisms. FEBS Lett 1993;319:80-83.
80. Alcamí A, Smith GL. Two genes encoding poxvirus cytokine receptors are disrupted or deleted in variola virus. [Commentary on the paper by Shchelkunov SN, et al. FEBS Lett 1993;319:80-83. FEBS Lett 1993;335:136-137.
81. Massung RF, et al. Analysis of the complete genome of smallpox variola major virus strain Bangladesh-1975. Virology 1994;201:215-240.
82. Smith CA, et al. A receptor for tumor necrosis factor defines an unusual family of cellular and viral proteins. Science 1990;248:1019-1023.
83. Loetscher H, et al. Molecular cloning and expression of the human 55 kd tumor necrosis factor receptor. Cell 1990;61:351-359.
84. Schall TJ, et al. Molecular cloning and expression of a receptor for human tumor necrosis factor. Cell 1990;61:361-370.
85. Smith CA, et al. T2 open reading frame from Shope fibroma virus encodes a soluble form of the TNF receptor. Biochem Biophys Res Commun 1991;176: 335-342.
86. Upton C, Macen JL, Schreiber M, McFadden G. Myxoma virus expresses a secreted protein with homology to the tumor necrosis factor receptor gene family that contributes to viral virulence. Virology 1991;184:370-382.
87. Howard ST, Chan YS, Smith GL. Vaccinia virus homologues of the Shope fibroma virus inverted terminal repeat proteins and a discontinuous ORF related to the tumour necrosis factor receptor family. Virology 1991;180:633-647.
88. Schreiber M, McFadden G. The myxoma virus TNF-receptor homologue (T2) inhibits tumor necrosis factor-alpha in a species-specific fashion. Virology 1994;204:692-705.
89. Hu F-Q, Smith CA, Pickup DJ. Cowpox virus contains two copies of an early gene encoding a soluble secreted form of the type II TNF receptor. Virology 1994;204:343-356.
90. Smith CA, et al. Cowpox virus genome encodes a second soluble homologue of cellular TNF receptors, distinct from CrmB, that binds TNF but not LT alpha. Virology 1996;223:132-147.
91. Massung RF, et al. Potential virulence determinants in terminal regions of variola smallpox virus genome. Nature 1993;366:748-751.
92. Aguado B, Selmes IP, Smith GL. Nucleotide sequence of 21.8 kbp of variola major virus strain Harvey and comparison with vaccinia virus. J Gen Virol 1992;73:2887-2902.
93. Wold WM, Tollefson AE, Hermiston TH. Strategies of immune modulation by adenoviruses. In: McFadden G, ed. Viroceptors, virokines and related immune modulators encoded by DNA viruses. Austin: R.G. Landes Company; 1995. p. 147-185.
94. Howard OMZ, Ben-Baruch A, Oppenheim JJ. Chemokines: progress toward identifying molecular targets for therapeutic agents. Trends Biotechnol 1996;14:46-51.
95. Cao JX, Gershon PD, Black DN. Sequence analysis of HindIII Q2 fragment of capripoxvirus reveals a putative gene encoding a G-protein-coupled chemokine receptor homologue. Virology 1995;209:207-212.
96. Massung RF, Jayarama V, Moyer RW. DNA sequence analysis of conserved and unique regions of swinepox virus: identification of genetic elements supporting phenotypic observations including a novel G protein-coupled receptor homologue. Virology 1993;197:511-528.
97. Senkevich TG, Bugert JJ, Sisler JR, Koonin EV, Darai G, Moss B. Genome sequence of a human tumorigenic poxvirus: prediction of specific host response-evasion genes. Science 1996;273:813-816.
98. Lalani AS, et al. The purified myxoma virus gamma interferon receptor homolog M-T7 interacts with the heparin-binding domains of chemokines. J Virol 1997;71:4356-4363.
99. Mossman K, Nation P, Macen J, Garbutt M, Lucas A, McFadden G. Myxoma virus M-T7, a secreted homolog of the interferon-gamma receptor, is a critical virulence factor for the development of myxomatosis in European rabbits. Virology 1996;215:17-30.
100. Graham KA, et al. The T1/35kDa family of poxvirus-secreted proteins bind chemokines and modulate leukocyte influx into virus-infected tissues. Virology 1997;229:12-24.
101. Patel AH, Gaffney DF, Subak-Sharpe JH, Stow ND. DNA sequence of the gene encoding a major secreted protein of vaccinia virus, strain Lister. J Gen Virol 1990;71:2013-2021.
102. Martínez-Pomares L, Thompson JP, Moyer RW. Mapping and investigation of the role in pathogenesis of the major unique secreted 35-kDa protein of rabbitpox virus. Virology 1995;206:591-600.
103. Venkatesan S, Gershowitz A, Moss B. Complete nucleotide sequences of two adjacent early vaccinia virus genes located within the inverted terminal repetition. J Virol 1982;44:637-646.
104. Shchelkunov SN, et al. Analysis of the nucleotide sequence of 53 kbp from the right terminus of the genome of variola virus strain India-1967. Virus Res 1994;34:207-236.
105. Isaacs A, Lindenmann J. Virus interference I. The interferon. Proc R Soc Lond B 1957;147:258-267.
106. Farrar MA, Schreiber RD. The molecular cell biology of interferon-γ and its receptor. Annu Rev Immunol 1993;11:571-611.
107. Pestka S, Langer JA, Zoon KC, Samuel CE. Interferons and their actions. Annu Rev Biochem 1987;56:727-777.
108. Chang H-W, Watson JC, Jacobs BL. The E3L gene of vaccinia virus encodes an inhibitor of the interferon-induced, double-stranded RNA-dependent protein kinase. Proc Natl Acad Sci USA 1992;89:4825-4829.
109. Beattie E, Tartaglia J, Paoletti E. Vaccinia-virus encoded eIF-2α homolog abrogates the antiviral effect of interferon. Virology 1991;183:419-422.
110. Davies MV, Elroy-Stein O, Jagus R, Moss B, Kaufman RJ. The vaccinia virus K3L gene product potentiates translation by inhibiting double-stranded RNA-activated protein kinase and phosphorylation of the alpha subunit of eukaryotic initiation factor 2. J Virol 1992;66:1945-1950.
111. Davies MV, Chang H-W, Jacobs BL, Kaufman RJ. The E3L and K3L vaccinia virus gene products stimulate translation through inhibition of the double-stranded RNA-dependent protein kinase by different mechanisms. J Virol 1993;67:1688-1692.
112. - mutant viruses. Virology 1995;210:254-263.
113. Beattie E, Denzler KL, Tartaglia J, Perkus ME, Paoletti E, Jacobs BL. Reversal of the interferon-sensitive phenotype of a vaccinia virus lacking E3L by expression of the reovirus S4 gene. J Virol 1995;69:499-505.
114. Beattie E, et al. Host-range restriction of vaccinia virus E3L-specific deletion mutants. Virus Genes 1996;12:89-94.
115. Upton C, Mossman K, McFadden G. Encoding of a homolog of IFN-γ receptor by myxoma virus. Science 1992;258:1369-1372.
116. Mossman K, Upton C, Buller RM, McFadden G. Species specificity of ectromelia virus and vaccinia virus interferon-gamma binding proteins. Virology 1995;208:762-769.
117. Alcamí A, Smith GL. Vaccinia, cowpox and camelpox viruses encode soluble interferon-γ receptors with novel broad species specificity. J Virol 1995;69:4633-4639.
118. Mossman K, Barry M, McFadden G. Interferon-γ receptors encoded by poxviruses. In: McFadden G, ed. Viroceptors, virokines and related immune modulators encoded by DNA viruses. Austin: R.G. Landes Company; 1995. p. 41-54.
119. Alcamí A, Smith GL. Receptors for gamma-interferon encoded by poxviruses: implications for the unknown origin of vaccinia virus. Trends Microbiol 1996;4:321-326.
120. Alcamí A, Smith GL. Soluble interferon-γ receptors encoded by poxviruses. Comp Immunol Microbiol Infect Dis 1996;19:305-317.
121. Mossman K, Upton C, McFadden G. The myxoma virus-soluble interferon-γ receptor homolog, M-T7, inhibits interferon-γ in a species-specific manner. J Biol Chem 1995;270:3031-3038.
122. Symons JA, Alcami A, Smith GL. Vaccinia virus encodes a soluble type I interferon receptor of novel structure and broad species specificity. Cell 1995;81:551-560.
123. Colamonici OR, Domanski P, Sweitzer SM, Larner A, Buller RML. Vaccinia virus B18R gene encodes a type I interferon-binding protein that blocks interferon alpha transmembrane signaling. J Biol Chem 1995;270:15974-15978.
124. Ueda Y, Morikawa S, Matsuura Y. Identification and nucleotide sequence of the gene encoding a surface antigen induced by vaccinia virus. Virology 1990;177:588-594.
125. Ueda Y, Ito M, Tagaya I. A specific surface antigen induced by poxvirus. Virology 1969;38:180-182.
126. Ueda Y, Tagaya I, Amano H, Ito M. Studies on the early antigens induced by vaccinia virus. Virology 1972;49:794-800.
127. Morikawa S, Ueda Y. Characterization of vaccinia surface antigen expressed by recombinant baculovirus. Virology 1993;193:753-761.
128. r 43-50 K protein on the surface of extracellular enveloped virus. Virology 1994;204:376-390.
129. McIntosh AAG, Smith GL. Vaccinia virus glycoprotein A34R is required for infectivity of extracellular enveloped virus. J Virol 1996;70:272-281.
130. Liptáková H, Kontseková E, Alcamí A, Smith GL, Kontsek P. Analysis of an interaction between the soluble vaccinia virus-coded type I interferon (IFN)-receptor and human IFN-alpha 1 and IFN-alpha 2. Virology 1997;232:86-90.
131. Kotwal GJ, Moss B. Vaccinia virus encodes a secretory polypeptide structurally related to complement control proteins. Nature 1988;335:176-178.
132. Isaacs SN, Moss B. Inhibition of complement activation by vaccinia virus. In: McFadden G, ed. Viroceptors, virokines and related immune modulators encoded by DNA viruses. Austin: R.G. Landes Company; 1994. p. 55-66.
133. Kotwal GJ, Isaacs SN, McKenzie R, Frank MM, Moss B. Inhibition of the complement cascade by the major secretory protein of vaccinia virus. Science 1990;250:827-830.
134. Isaacs SN, Kotwal GJ, Moss B. Vaccinia virus complement-control protein prevents antibody-dependent complement-enhanced neutralization of infectivity and contributes to virulence. Proc Natl Acad Sci USA 1992;89:628-632.
135. McKenzie R, Kotwal GJ, Moss B, Hammer CH, Frank MM. Regulation of complement activity by vaccinia virus complement-control protein. J Infect Dis 1992;166:1245-1250.
136. Miller CG, Shchelkunov SN, Kotwal GJ. The cowpox virus-encoded homolog of the vaccinia virus complement control protein is an inflammation modulatory protein. Virology 1997;229:126-133.
137. Takahashi-Nishimaki F, Funahashi S, Miki K, Hashizume S, Sugimoto M. Regulation of plaque size and host range by a vaccinia virus gene related to complement system proteins. Virology 1991;181:158-164.
138. Engelstad M, Howard ST, Smith GL. A constitutively expressed vaccinia virus gene encodes a 42 kDa glycoprotein related to complement control factors that forms part of the extracellular envelope. Virology 1992;188:801-810.
139. Martinez-Pomares L, Stern RJ, Moyer RW. 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. J Virol 1993;67:5450-5462.
140. Engelstad M, Smith GL. The vaccinia virus 42 kDa envelope protein is required for envelopment and egress of extracellular virus and for virulence. Virology 1993;194:627-637.
141. Wolffe EJ, Isaacs SN, Moss B. Deletion of the vaccinia virus B5R gene encoding a 42-kilodalton membrane glycoprotein inhibits extracellular virus envelope formation and dissemination. J Virol 1993;67:4732-4741.
142. Blasco R, Cole NB, Moss B. Sequence analysis, expression, and deletion of a vaccinia virus gene encoding a homolog of profilin, a eukaryotic actin-binding protein. J Virol 1991;65:4598-4608.
143. Bongiovanni AM. The adrenogenital syndrome with deficiency of 3β-hydroxysteroid (3β-HSD) dehydrogenase. J Clin Invest 1962;41:2086-2092.
144. Moore JB, Smith GL. Steroid hormone synthesis by a vaccinia enzyme: a new type of virus virulence factor. EMBO J 1992;11:1973-1980.
145. Moore JB. Vaccinia virus 3β-hydroxysteroid dehydrogenase [D.Phil.]. Oxford: University of Oxford; 1994.
146. Cupps TR, Fauci AS. Corticosteroid-mediated immunoregulation in man. Immunol Rev 1982;65:133-155.
147. Skinner MA, Moore JB, Binns MM, Smith GL, Boursnell ME. Deletion of fowlpox virus homologues of vaccinia virus genes between the 3 beta-hydroxysteroid dehydrogenase (A44L) and DNA ligase (A50R) genes. J Gen Virol 1994;75:2495-2498.
148. Shchelkunov SN, Massung RF, Esposito JJ. Comparison of the genome DNA sequences of Bangladesh-1975 and India-1967 variola viruses. Virus Res 1995;36:107-118.