Initial characterization of Vaccinia Virus B4 suggests a role in virus spread

Virology

Volumn 456-457, Issue 1, 2014, Pages 108-120

  Burles, Kristin ^a   Irwin, Chad R ^a   Burton, Robyn Lee ^a   Schriewer, Jill ^b   Evans, David H ^a   Buller, R Mark ^b   Barry, Michele ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Actin tails; B4R; Ectromelia virus; Poxvirus; Vaccinia virus; Virulence; Virus plaque; Virus spread

Indexed keywords

ACTIN; ANKYRIN; PROTEIN B4; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B4R GENE; DELETION MUTANT; ECTROMELIA VIRUS; FEMALE; GENE DELETION; GENE SYNTHESIS; GROWTH CURVE; MOUSE; MOUSEPOX; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; TISSUE CULTURE; TRANSMISSION ELECTRON MICROSCOPY; VACCINIA VIRUS; VIRUS ATTENUATION; VIRUS CULTURE; VIRUS GENE; VIRUS INFECTIVITY; VIRUS MORPHOGENESIS; VIRUS PARTICLE; VIRUS PLAQUE; VIRUS RELEASE; VIRUS STRAIN; VIRUS TRANSMISSION; VIRUS VIRULENCE;

ACTIN TAILS; B4R; ECTROMELIA VIRUS; POXVIRUS; VACCINIA VIRUS; VIRULENCE; VIRUS PLAQUE; VIRUS SPREAD;

ANIMAL STRUCTURES; ANIMALS; ECTROMELIA VIRUS; ECTROMELIA, INFECTIOUS; FEMALE; GENE DELETION; MICE; MICE, INBRED C57BL; MICROSCOPY, ELECTRON, TRANSMISSION; VACCINIA VIRUS; VIRAL LOAD; VIRAL PLAQUE ASSAY; VIRAL PROTEINS; VIRION; VIRULENCE;

EID: 84897503768     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2014.03.019     Document Type: Article

References (137)

1. Arakawa Y., Cordeiro J.V., Schleich S., Newsome T.P., Way M. The release of vaccinia virus from infected cells requires RhoA-mDia modulation of cortical actin. Cell Host Microbe 2007, 1:227-240.
2. Arakawa Y., Cordeiro J.V., Way M. F11L-mediated inhibition of RhoA-mDia signaling stimulates microtubule dynamics during vaccinia virus infection. Cell Host Microbe 2007, 1:213-226.
3. Assarsson E., Greenbaum J.A., Sundstrom M., Schaffer L., Hammond J.A., Pasquetto V., Oseroff C., Hendrickson R.C., Lefkowitz E.J., Tscharke D.C., Sidney J., Grey H.M., Head S.R., Peters B., Sette A. Kinetic analysis of a complete poxvirus transcriptome reveals an immediate-early class of genes. Proc. Natl. Acad. Sci. USA 2008, 105:2140-2145.
4. Bai C., Sen P., Hofmann K., Ma L., Goebl M., Harper J.W., Elledge S.J. SKP1 connects cell cycle regulators to the ubiquitin proteolysis machinery through a novel motif, the F-box. Cell 1996, 86:263-274.
5. Bisht H., Weisberg A.S., Moss B. Vaccinia virus l1 protein is required for cell entry and membrane fusion. J. Virol. 2008, 82:8687-8694.
6. Blasco R., Cole N.B., 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.
7. Blasco R., Moss B. 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. 1991, 65:5910-5920.
8. Blasco R., Moss B. Role of cell-associated enveloped vaccinia virus in cell-to-cell spread. J. Virol. 1992, 66:4170-4179.
9. Blasco R., Sisler J.R., Moss B. 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. 1993, 67:3319-3325.
10. Borrego B., Lorenzo M.M., Blasco R. Complementation of P37 (F13L gene) knock-out in vaccinia virus by a cell line expressing the gene constitutively. J. Gen. Virol. 1999, 80(Pt 2):425-432.
11. Breiman A., Carpentier D.C., Ewles H.A., Smith G.L. Transport and stability of the vaccinia virus A34 protein is affected by the A33 protein. J. Gen. Virol. 2013, 94:720-725.
12. Breiman A., Smith G.L. Vaccinia virus B5 protein affects the glycosylation, localization and stability of the A34 protein. J. Gen. Virol. 2010, 91:1823-1827.
13. Brown E., Senkevich T.G., Moss B. Vaccinia virus F9 virion membrane protein is required for entry but not virus assembly, in contrast to the related L1 protein. J. Virol. 2006, 80:9455-9464.
14. Broyles S.S. Vaccinia virus transcription. J. Gen. Virol. 2003, 84:2293-2303.
15. Chan W.M., Kalkanoglu A.E., Ward B.M. The inability of vaccinia virus A33R protein to form intermolecular disulfide-bonded homodimers does not affect the production of infectious extracellular virus. Virology 2010, 408:109-118.
16. Chan W.M., Ward B.M. There is an A33-dependent mechanism for the incorporation of B5-GFP into vaccinia virus extracellular enveloped virions. Virology 2010, 402:83-93.
17. Chan W.M., Ward B.M. Increased interaction between vaccinia virus proteins A33 and B5 is detrimental to infectious extracellular enveloped virion production. J. Virol. 2012, 86:8232-8244.
18. Chan W.M., Ward B.M. The A33-dependent incorporation of B5 into extracellular enveloped vaccinia virions is mediated through an interaction between their lumenal domains. J. Virol. 2012, 86:8210-8220.
19. Chiu W.L., Lin C.L., Yang M.H., Tzou D.L., Chang W. Vaccinia virus 4c (A26L) protein on intracellular mature virus binds to the extracellular cellular matrix laminin. J. Virol. 2007, 81:2149-2157.
20. Chung C.S., Hsiao J.C., Chang Y.S., Chang W. A27L protein mediates vaccinia virus interaction with cell surface heparan sulfate. J. Virol. 1998, 72:1577-1585.
21. Condit R.C., Moussatche N., Traktman P. In a nutshell: structure and assembly of the vaccinia virion. Adv. Virus Res. 2006, 66:31-124.
22. Cordeiro J.V., Guerra S., Arakawa Y., Dodding M.P., Esteban M., Way M. F11-mediated inhibition of RhoA signalling enhances the spread of vaccinia virus in vitro and in vivo in an intranasal mouse model of infection. PLoS One 2009, 4:e8506.
23. Cudmore S., Cossart P., Griffiths G., Way M. Actin-based motility of vaccinia virus. Nature 1995, 378:636-638.
24. Cunha S.R., Mohler P.J. Ankyrin protein networks in membrane formation and stabilization. J. Cell. Mol. Med. 2009, 13:4364-4376.
25. Dales S., Mosbach E.H. Vaccinia as a model for membrane biogenesis. Virology 1968, 35:564-583.
26. Dodding M.P., Newsome T.P., Collinson L.M., Edwards C., Way M. An E2-F12 complex is required for intracellular enveloped virus morphogenesis during vaccinia infection. Cell. Microbiol. 2009, 11:808-824.
27. Domi A., Weisberg A.S., Moss B. Vaccinia virus E2L null mutants exhibit a major reduction in extracellular virion formation and virus spread. J. Virol. 2008, 82:4215-4226.
28. Duncan S.A., Smith G.L. Identification and characterization of an extracellular envelope glycoprotein affecting vaccinia virus egress. J. Virol. 1992, 66:1610-1621.
29. Earley A.K., Chan W.M., Ward B.M. The vaccinia virus B5 protein requires A34 for efficient intracellular trafficking from the endoplasmic reticulum to the site of wrapping and incorporation into progeny virions. J. Virol. 2008, 82:2161-2169.
30. Engelstad M., Howard S.T., Smith G.L. A constitutively expressed vaccinia gene encodes a 42-kDa glycoprotein related to complement control factors that forms part of the extracellular virus envelope. Virology 1992, 188:801-810.
31. Engelstad M., Smith G.L. The vaccinia virus 42-kDa envelope protein is required for the envelopment and egress of extracellular virus and for virus virulence. Virology 1993, 194:627-637.
32. Esteban D., Parker S., Schriewer J., Hartzler H., Buller R.M. Mousepox, a small animal model of smallpox. Methods Mol. Biol. 2012, 890:177-198.
33. Esteban D.J., Buller R.M. Ectromelia virus: the causative agent of mousepox. J. Gen. Virol. 2005, 86:2645-2659.
34. Fagan-Garcia K., Barry M. A vaccinia virus deletion mutant reveals the presence of additional inhibitors of NF-kappaB. J. Virol. 2011, 85:883-894.
35. Fenner F., Henderson D.A., Arita I., Jezek Z., Ladnyi I.D. Smallpox and its Eradication 1988, World Health Organization.
36. Frischknecht F., Moreau V., Rottger S., Gonfloni S., Reckmann I., Superti-Furga G., Way M. Actin-based motility of vaccinia virus mimics receptor tyrosine kinase signalling. Nature 1999, 401:926-929.
37. Gammon D.B., Gowrishankar B., Duraffour S., Andrei G., Upton C., Evans D.H. Vaccinia virus-encoded ribonucleotide reductase subunits are differentially required for replication and pathogenesis. PLoS Pathog. 2010, 6:e1000984.
38. Geada M.M., Galindo I., Lorenzo M.M., Perdiguero B., Blasco R. Movements of vaccinia virus intracellular enveloped virions with GFP tagged to the F13L envelope protein. J. Gen. Virol. 2001, 82:2747-2760.
39. Grosenbach D.W., Ulaeto D.O., Hruby D.E. Palmitylation of the vaccinia virus 37-kDa major envelope antigen. Identification of a conserved acceptor motif and biological relevance. J. Biol. Chem. 1997, 272:1956-1964.
40. Handa Y., Durkin C.H., Dodding M.P., Way M. Vaccinia virus F11 promotes viral spread by acting as a PDZ-containing scaffolding protein to bind myosin-9A and inhibit RhoA signaling. Cell Host Microbe 2013, 14:51-62.
41. Herrera E., Lorenzo M.M., Blasco R., Isaacs S.N. Functional analysis of vaccinia virus B5R protein: essential role in virus envelopment is independent of a large portion of the extracellular domain. J. Virol. 1998, 72:294-302.
42. Herrero-Martinez E., Roberts K.L., Hollinshead M., Smith G.L. Vaccinia virus intracellular enveloped virions move to the cell periphery on microtubules in the absence of the A36R protein. J. Gen. Virol. 2005, 86:2961-2968.
43. Heuser J. Deep-etch EM reveals that the early poxvirus envelope is a single membrane bilayer stabilized by a geodetic "honeycomb" surface coat. J. Cell Biol. 2005, 169:269-283.
44. Hiller G., Weber K., Schneider L., Parajsz C., Jungwirth C. Interaction of assembled progeny pox viruses with the cellular cytoskeleton. Virology 1979, 98:142-153.
45. Hollinshead M., Rodger G., Van Eijl H., Law M., Hollinshead R., Vaux D.J., Smith G.L. Vaccinia virus utilizes microtubules for movement to the cell surface. J. Cell Biol. 2001, 154:389-402.
46. Honeychurch K.M., Yang G., Jordan R., Hruby D.E. The vaccinia virus F13L YPPL motif is required for efficient release of extracellular enveloped virus. J. Virol. 2007, 81:7310-7315.
47. Horsington J., Lynn H., Turnbull L., Cheng D., Braet F., Diefenbach R.J., Whitchurch C.B., Karupiah G., Newsome T.P. A36-dependent actin filament nucleation promotes release of vaccinia virus. PLoS Pathog. 2013, 9:e1003239.
48. Howard A.R., Weisberg A.S., Moss B. Congregation of orthopoxvirus virions in cytoplasmic A-type inclusions is mediated by interactions of a bridging protein (A26p) with a matrix protein (ATIp) and a virion membrane-associated protein (A27p). J. Virol. 2010, 84:7592-7602.
49. Hsiao J.C., Chung C.S., Chang W. 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. 1998, 72:8374-8379.
50. Hsiao J.C., Chung C.S., Chang W. Vaccinia virus envelope D8L protein binds to cell surface chondroitin sulfate and mediates the adsorption of intracellular mature virions to cells. J. Virol. 1999, 73:8750-8761.
51. Humphries A.C., Dodding M.P., Barry D.J., Collinson L.M., Durkin C.H., Way M. Clathrin potentiates vaccinia-induced actin polymerization to facilitate viral spread. Cell Host Microbe 2012, 12:346-359.
52. Husain M., Moss B. Vaccinia virus F13L protein with a conserved phospholipase catalytic motif induces colocalization of the B5R envelope glycoprotein in post-Golgi vesicles. J. Virol. 2001, 75:7528-7542.
53. Husain M., Moss B. Similarities in the induction of post-Golgi vesicles by the vaccinia virus F13L protein and phospholipase D. J. Virol. 2002, 76:7777-7789.
54. Husain M., Moss B. Intracellular trafficking of a palmitoylated membrane-associated protein component of enveloped vaccinia virus. J. Virol. 2003, 77:9008-9019.
55. Husain M., Weisberg A., Moss B. Topology of epitope-tagged F13L protein, a major membrane component of extracellular vaccinia virions. Virology 2003, 308:233-242.
56. Husain M., Weisberg A.S., Moss B. Existence of an operative pathway from the endoplasmic reticulum to the immature poxvirus membrane. Proc. Natl. Acad. Sci. USA 2006, 103:19506-19511.
57. Husain M., Weisberg A.S., Moss B. Resistance of a vaccinia virus A34R deletion mutant to spontaneous rupture of the outer membrane of progeny virions on the surface of infected cells. Virology 2007, 366:424-432.
58. Husain M., Weisberg A.S., Moss B. Sequence-independent targeting of transmembrane proteins synthesized within vaccinia virus factories to nascent viral membranes. J. Virol. 2007, 81:2646-2655.
59. Irwin C.R., Evans D.H. Modulation of the myxoma virus plaque phenotype by vaccinia virus protein f11. J. Virol. 2012, 86:7167-7179.
60. Isaacs S.N., Wolffe E.J., Payne L.G., Moss B. Characterization of a vaccinia virus-encoded 42-kilodalton class I membrane glycoprotein component of the extracellular virus envelope. J. Virol. 1992, 66:7217-7224.
61. Izmailyan R.A., Huang C.Y., Mohammad S., Isaacs S.N., Chang W. The envelope G3L protein is essential for entry of vaccinia virus into host cells. J. Virol. 2006, 80:8402-8410.
62. Johnston S.C., Ward B.M. Vaccinia virus protein F12 associates with intracellular enveloped virions through an interaction with A36. J. Virol. 2009, 83:1708-1717.
63. Katz E., Ward B.M., Weisberg A.S., Moss B. 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. 2003, 77:12266-12275.
64. Katz E., Wolffe E., Moss B. Identification of second-site mutations that enhance release and spread of vaccinia virus. J. Virol. 2002, 76:11637-11644.
65. Katz E., Wolffe E.J., Moss B. The cytoplasmic and transmembrane domains of the vaccinia virus B5R protein target a chimeric human immunodeficiency virus type 1 glycoprotein to the outer envelope of nascent vaccinia virions. J. Virol. 1997, 71:3178-3187.
66. Kipreos E.T., Pagano M. The F-box protein family. Genome Biol. 2000, (1). (REVIEWS3002).
67. Li J., Mahajan A., Tsai M.D. Ankyrin repeat: a unique motif mediating protein-protein interactions. Biochemistry 2006, 45:15168-15178.
68. Lin C.L., Chung C.S., Heine H.G., Chang W. Vaccinia virus envelope H3L protein binds to cell surface heparan sulfate and is important for intracellular mature virion morphogenesis and virus infection in vitro and in vivo. J. Virol. 2000, 74:3353-3365.
69. Lin L., Ghosh S. A glycine-rich region in NF-kappaB p105 functions as a processing signal for the generation of the p50 subunit. Mol. Cell. Biol. 1996, 16:2248-2254.
70. Lin Y.C., Li J., Irwin C.R., Jenkins H., DeLange L., Evans D.H. Vaccinia virus DNA ligase recruits cellular topoisomerase II to sites of viral replication and assembly. J. Virol. 2008, 82:5922-5932.
71. Mathew E., Sanderson C.M., Hollinshead M., Smith G.L. The extracellular domain of vaccinia virus protein B5R affects plaque phenotype, extracellular enveloped virus release, and intracellular actin tail formation. J. Virol. 1998, 72:2429-2438.
72. Mathew E.C., Sanderson C.M., Hollinshead R., Hollinshead M., Grimley R., Smith G.L. The effects of targeting the vaccinia virus B5R protein to the endoplasmic reticulum on virus morphogenesis and dissemination. Virology 1999, 265:131-146.
73. Mathew E.C., Sanderson C.M., Hollinshead R., Smith G.L. A mutational analysis of the vaccinia virus B5R protein. J. Gen. Virol. 2001, 82:1199-1213.
74. McIntosh A.A., Smith G.L. Vaccinia virus glycoprotein A34R is required for infectivity of extracellular enveloped virus. J. Virol. 1996, 70:272-281.
75. Mercer A.A., Fleming S.B., Ueda N. F-box-like domains are present in most poxvirus ankyrin repeat proteins. Virus Genes 2005, 31:127-133.
76. Morgan G.W., Hollinshead M., Ferguson B.J., Murphy B.J., Carpentier D.C., Smith G.L. Vaccinia protein F12 has structural similarity to kinesin light chain and contains a motor binding motif required for virion export. PLoS Pathog. 2010, 6:e1000785.
77. Moss B. Poxviridae: the viruses and their replication. Fields Virology, 5th ed. 2007, Elsevier, Seattle, Washington.
78. Nakayama K.I., Nakayama K. Ubiquitin ligases: cell-cycle control and cancer. Nat. Rev. Cancer 2006, 6:369-381.
79. Nelson G.E., Wagenaar T.R., Moss B. A conserved sequence within the H2 subunit of the vaccinia virus entry/fusion complex is important for interaction with the A28 subunit and infectivity. J. Virol. 2008, 82:6244-6250.
80. Newsome T.P., Scaplehorn N., Way M. SRC mediates a switch from microtubule- to actin-based motility of vaccinia virus. Science 2004, 306:124-129.
81. Newsome T.P., Weisswange I., Frischknecht F., Way M. Abl collaborates with Src family kinases to stimulate actin-based motility of vaccinia virus. Cell. Microbiol. 2006, 8:233-241.
82. Nichols R.J., Stanitsa E., Unger B., Traktman P. The vaccinia virus gene I2L encodes a membrane protein with an essential role in virion entry. J. Virol. 2008, 82:10247-10261.
83. Ojeda S., Domi A., Moss B. Vaccinia virus G9 protein is an essential component of the poxvirus entry-fusion complex. J. Virol. 2006, 80:9822-9830.
84. Ojeda S., Senkevich T.G., Moss B. Entry of vaccinia virus and cell-cell fusion require a highly conserved cysteine-rich membrane protein encoded by the A16L gene. J. Virol. 2006, 80:51-61.
85. Parkinson J.E., Smith G.L. Vaccinia virus gene A36R encodes a M(r) 43-50 K protein on the surface of extracellular enveloped virus. Virology 1994, 204:376-390.
86. Perdiguero B., Lorenzo M.M., Blasco R. Vaccinia virus A34 glycoprotein determines the protein composition of the extracellular virus envelope. J. Virol. 2008, 82:2150-2160.
87. Perkus M.E., Goebel S.J., Davis S.W., Johnson G.P., Norton E.K., Paoletti E. Deletion of 55 open reading frames from the termini of vaccinia virus. Virology 1991, 180:406-410.
88. Reed K.D., Melski J.W., Graham M.B., Regnery R.L., Sotir M.J., Wegner M.V., Kazmierczak J.J., Stratman E.J., Li Y., Fairley J.A., Swain G.R., Olson V.A., Sargent E.K., Kehl S.C., Frace M.A., Kline R., Foldy S.L., Davis J.P., Damon I.K. The detection of monkeypox in humans in the Western Hemisphere. N. Engl. J. Med. 2004, 350:342-350.
89. Reeves P.M., Bommarius B., Lebeis S., McNulty S., Christensen J., Swimm A., Chahroudi A., Chavan R., Feinberg M.B., Veach D., Bornmann W., Sherman M., Kalman D. Disabling poxvirus pathogenesis by inhibition of Abl-family tyrosine kinases. Nat. Med. 2005, 11:731-739.
90. Rietdorf J., Ploubidou A., Reckmann I., Holmstrom A., Frischknecht F., Zettl M., Zimmermann T., Way M. Kinesin-dependent movement on microtubules precedes actin-based motility of vaccinia virus. Nat. Cell Biol. 2001, 3:992-1000.
91. Rintoul J.L., Wang J., Gammon D.B., van Buuren N.J., Garson K., Jardine K., Barry M., Evans D.H., Bell J.C. A selectable and excisable marker system for the rapid creation of recombinant poxviruses. PLoS One 2011, 6:e24643.
92. Roberts K.L., Smith G.L. Vaccinia virus morphogenesis and dissemination. Trends Microbiol. 2008.
93. Roberts K.L., Smith G.L. Vaccinia virus morphogenesis and dissemination. Trends Microbiol. 2008, 16:472-479.
94. Roper R.L., Moss B. Envelope formation is blocked by mutation of a sequence related to the HKD phospholipid metabolism motif in the vaccinia virus F13L protein. J. Virol. 1999, 73:1108-1117.
95. Roper R.L., Payne L.G., Moss B. Extracellular vaccinia virus envelope glycoprotein encoded by the A33R gene. J. Virol. 1996, 70:3753-3762.
96. Roper R.L., Wolffe E.J., Weisberg A., Moss B. 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. 1998, 72:4192-4204.
97. Rottger S., Frischknecht F., Reckmann I., Smith G.L., Way M. Interactions between vaccinia virus IEV membrane proteins and their roles in IEV assembly and actin tail formation. J. Virol. 1999, 73:2863-2875.
98. Sanderson C.M., Frischknecht F., Way M., Hollinshead M., Smith G.L. Roles of vaccinia virus EEV-specific proteins in intracellular actin tail formation and low pH-induced cell-cell fusion. J. Gen. Virol. 1998, 79:1415-1425.
99. Satheshkumar P.S., Moss B. Characterization of a newly identified 35-amino-acid component of the vaccinia virus entry/fusion complex conserved in all chordopoxviruses. J. Virol. 2009, 83:12822-12832.
100. Satheshkumar P.S., Moss B. Sequence-divergent chordopoxvirus homologs of the o3 protein maintain functional interactions with components of the vaccinia virus entry-fusion complex. J. Virol. 2012, 86:1696-1705.
101. Schmelz M., Sodeik B., Ericsson M., Wolffe E.J., Shida H., Hiller G., Griffiths G. Assembly of vaccinia virus: the second wrapping cisterna is derived from the trans Golgi network. J. Virol. 1994, 68:130-147.
102. Seet B.T., Johnston J.B., Brunetti C.R., Barrett J.W., Everett H., Cameron C., Sypula J., Nazarian S.H., Lucas A., McFadden G. Poxviruses and immune evasion. Annu. Rev. Immunol. 2003, 21:377-423.
103. Senkevich T.G., Moss B. Vaccinia virus H2 protein is an essential component of a complex involved in virus entry and cell-cell fusion. J. Virol. 2005, 79:4744-4754.
104. Senkevich T.G., Ojeda S., Townsley A., Nelson G.E., Moss B. Poxvirus multiprotein entry-fusion complex. Proc. Natl. Acad. Sci. USA 2005, 102:18572-18577.
105. Senkevich T.G., Ward B.M., Moss B. Vaccinia virus A28L gene encodes an essential protein component of the virion membrane with intramolecular disulfide bonds formed by the viral cytoplasmic redox pathway. J. Virol. 2004, 78:2348-2356.
106. Senkevich T.G., Ward B.M., Moss B. Vaccinia virus entry into cells is dependent on a virion surface protein encoded by the A28L gene. J. Virol. 2004, 78:2357-2366.
107. Smith G.L., Law M. The exit of Vaccinia virus from infected cells. Virus Res. 2004, 106:189-197.
108. Smith G.L., Murphy B.J., Law M. Vaccinia virus motility. Annu. Rev. Microbiol. 2003, 57:323-342.
109. Smith G.L., Vanderplasschen A., Law M. The formation and function of extracellular enveloped vaccinia virus. J. Gen. Virol. 2002, 83:2915-2931.
110. Sonnberg S., Seet B.T., Pawson T., Fleming S.B., Mercer A.A. Poxvirus ankyrin repeat proteins are a unique class of F-box proteins that associate with cellular SCF1 ubiquitin ligase complexes. Proc. Natl. Acad. Sci. USA 2008, 105:10955-10960.
111. Stuart D., Graham K., Schreiber M., Macaulay C., McFadden G. The target DNA sequence for resolution of poxvirus replicative intermediates is an active late promoter. J. Virol. 1991, 65:61-70.
112. Szajner P., Weisberg A.S., Lebowitz J., Heuser J., Moss B. External scaffold of spherical immature poxvirus particles is made of protein trimers, forming a honeycomb lattice. J. Cell Biol. 2005, 170:971-981.
113. Thorne S.H. Immunotherapeutic potential of oncolytic vaccinia virus. Immunol. Res. 2011, 50:286-293.
114. Townsley A.C., Senkevich T.G., Moss B. 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. Virol. 2005, 79:10988-10998.
115. Townsley A.C., Senkevich T.G., Moss B. Vaccinia virus A21 virion membrane protein is required for cell entry and fusion. J. Virol. 2005, 79:9458-9469.
116. Turner P.C., Dilling B.P., Prins C., Cresawn S.G., Moyer R.W., Condit R.C. Vaccinia virus temperature-sensitive mutants in the A28 gene produce non-infectious virions that bind to cells but are defective in entry. Virology 2007, 366:62-72.
117. Valderrama F., Cordeiro J.V., Schleich S., Frischknecht F., Way M. Vaccinia virus-induced cell motility requires F11L-mediated inhibition of RhoA signaling. Science 2006, 311:377-381.
118. van Buuren N., Couturier B., Xiong Y., Barry M. Ectromelia virus encodes a novel family of F-box proteins that interact with the SCF complex. J. Virol. 2008, 82:9917-9927.
119. van Eijl H., Hollinshead M., Rodger G., Zhang W.H., Smith G.L. 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. 2002, 83:195-207.
120. van Eijl H., Hollinshead M., Smith G.L. The vaccinia virus A36R protein is a type Ib membrane protein present on intracellular but not extracellular enveloped virus particles. Virology 2000, 271:26-36.
121. Vanderplasschen A., Mathew E., Hollinshead M., Sim R.B., Smith G.L. Extracellular enveloped vaccinia virus is resistant to complement because of incorporation of host complement control proteins into its envelope. Proc. Natl. Acad. Sci. USA 1998, 95:7544-7549.
122. Ward B.M. Visualization and characterization of the intracellular movement of vaccinia virus intracellular mature virions. J. Virol. 2005, 79:4755-4763.
123. Ward B.M., Moss B. Vaccinia virus intracellular movement is associated with microtubules and independent of actin tails. J. Virol. 2001, 75:11651-11663.
124. Ward B.M., Moss B. Visualization of intracellular movement of vaccinia virus virions containing a green fluorescent protein-B5R membrane protein chimera. J. Virol. 2001, 75:4802-4813.
125. Ward B.M., Moss B. Vaccinia virus A36R membrane protein provides a direct link between intracellular enveloped virions and the microtubule motor kinesin. J. Virol. 2004, 78:2486-2493.
126. Ward B.M., Weisberg A.S., Moss B. Mapping and functional analysis of interaction sites within the cytoplasmic domains of the vaccinia virus A33R and A36R envelope proteins. J. Virol. 2003, 77:4113-4126.
127. Weaver J.R., Shamim M., Alexander E., Davies D.H., Felgner P.L., Isaacs S.N. The identification and characterization of a monoclonal antibody to the vaccinia virus E3 protein. Virus Res. 2007, 130:269-274.
128. Welch M.D., Way M. Arp2/3-mediated actin-based motility: a tail of pathogen abuse. Cell Host Microbe 2013, 14:242-255.
129. Werren J.H., Richards S., Desjardins C.A., Niehuis O., Gadau J., Colbourne J.K., Beukeboom L.W., Desplan C., Elsik C.G., Grimmelikhuijzen C.J., Kitts P., Lynch J.A., Murphy T., Oliveira D.C., Smith C.D., van de Zande L., Worley K.C., Zdobnov E.M., Aerts M., Albert S., Anaya V.H., Anzola J.M., Barchuk A.R., Behura S.K., Bera A.N., Berenbaum M.R., Bertossa R.C., Bitondi M.M., Bordenstein S.R., Bork P., Bornberg-Bauer E., Brunain M., Cazzamali G., Chaboub L., Chacko J., Chavez D., Childers C.P., Choi J.H., Clark M.E., Claudianos C., Clinton R.A., Cree A.G., Cristino A.S., Dang P.M., Darby A.C., de Graaf D.C., Devreese B., Dinh H.H., Edwards R., Elango N., Elhaik E., Ermolaeva O., Evans J.D., Foret S., Fowler G.R., Gerlach D., Gibson J.D., Gilbert D.G., Graur D., Grunder S., Hagen D.E., Han Y., Hauser F., Hultmark D., Hunter H.C.t., Hurst G.D., Jhangian S.N., Jiang H., Johnson R.M., Jones A.K., Junier T., Kadowaki T., Kamping A., Kapustin Y., Kechavarzi B., Kim J., Kiryutin B., Koevoets T., Kovar C.L., Kriventseva E.V., Kucharski R., Lee H., Lee S.L., Lees K., Lewis L.R., Loehlin D.W., Logsdon J.M., Lopez J.A., Lozado R.J., Maglott D., Maleszka R., Mayampurath A., Mazur D.J., McClure M.A., Moore A.D., Morgan M.B., Muller J., Munoz-Torres M.C., Muzny D.M., Nazareth L.V., Neupert S., Nguyen N.B., Nunes F.M., Oakeshott J.G., Okwuonu G.O., Pannebakker B.A., Pejaver V.R., Peng Z., Pratt S.C., Predel R., Pu L.L., Ranson H., Raychoudhury R., Rechtsteiner A., Reese J.T., Reid J.G., Riddle M., Robertson H.M., Romero-Severson J., Rosenberg M., Sackton T.B., Sattelle D.B., Schluns H., Schmitt T., Schneider M., Schuler A., Schurko A.M., Shuker D.M., Simoes Z.L., Sinha S., Smith Z., Solovyev V., Souvorov A., Springauf A., Stafflinger E., Stage D.E., Stanke M., Tanaka Y., Telschow A., Trent C., Vattathil S., Verhulst E.C., Viljakainen L., Wanner K.W., Waterhouse R.M., Whitfield J.B., Wilkes T.E., Williamson M., Willis J.H., Wolschin F., Wyder S., Yamada T., Yi S.V., Zecher C.N., Zhang L., Gibbs R.A. Functional and evolutionary insights from the genomes of three parasitoid Nasonia species. Science 2010, 327:343-348.
130. Wilton B.A., Campbell S., Van Buuren N., Garneau R., Furukawa M., Xiong Y., Barry M. Ectromelia virus BTB/kelch proteins, EVM150 and EVM167, interact with cullin-3-based ubiquitin ligases. Virology 2008, 374:82-99.
131. Wolfe C.L., Ojeda S., Moss B. Transcriptional repression and RNA silencing act synergistically to demonstrate the function of the eleventh component of the vaccinia virus entry-fusion complex. J. Virol. 2012, 86:293-301.
132. Wolffe E.J., Isaacs S.N., 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.
133. Wolffe E.J., Katz E., Weisberg A., Moss B. The A34R glycoprotein gene is required for induction of specialized actin-containing microvilli and efficient cell-to-cell transmission of vaccinia virus. J. Virol. 1997, 71:3904-3915.
134. Wolffe E.J., Weisberg A.S., Moss B. 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 1998, 244:20-26.
135. Wolffe E.J., Weisberg A.S., Moss B. The vaccinia virus A33R protein provides a chaperone function for viral membrane localization and tyrosine phosphorylation of the A36R protein. J. Virol. 2001, 75:303-310.
136. Zhang W.H., Wilcock D., Smith G.L. Vaccinia virus F12L protein is required for actin tail formation, normal plaque size, and virulence. J. Virol. 2000, 74:11654-11662.
137. Zwilling J., Sliva K., Schwantes A., Schnierle B., Sutter G. Functional F11L and K1L genes in modified vaccinia virus Ankara restore virus-induced cell motility but not growth in human and murine cells. Virology 2010, 404:231-239.