A36-dependent Actin Filament Nucleation Promotes Release of Vaccinia Virus

PLoS Pathogens

Volumn 9, Issue 3, 2013, Pages

  Horsington, Jacquelyn ^a   Lynn, Helena ^a   Turnbull, Lynne ^b   Cheng, Delfine ^a   Braet, Filip ^a   Diefenbach, Russell J ^a   Whitchurch, Cynthia B ^b   Karupiah, Guna ^c   Newsome, Timothy P ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

^b UNIVERSITY OF TECHNOLOGY SYDNEY   (Australia)

^c Biology and Environment   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

F ACTIN; UNCLASSIFIED DRUG; VIRUS ENVELOPE PROTEIN; VIRUS PROTEIN; VIRUS PROTEIN A36;

ACTIN FILAMENT; ANIMAL CELL; ARTICLE; COMET ASSAY; CONFOCAL MICROSCOPY; EMBRYO; FLUORESCENCE MICROSCOPY; MOLECULAR BIOLOGY; NONHUMAN; NUCLEATION; POINT MUTATION; POLYMERASE CHAIN REACTION; TRANSMISSION ELECTRON MICROSCOPY; VACCINIA VIRUS; VIRUS ATTACHMENT; VIRUS CULTURE; VIRUS RELEASE;

ACTIN CYTOSKELETON; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CELL MEMBRANE; CERCOPITHECUS AETHIOPS; COMET ASSAY; FIBROBLASTS; HOST-PATHOGEN INTERACTIONS; MICE; MICROSCOPY, ELECTRON, TRANSMISSION; NIH 3T3 CELLS; ONCOGENE PROTEINS; VACCINIA; VACCINIA VIRUS; VERO CELLS; VIRAL ENVELOPE PROTEINS; VIRAL STRUCTURAL PROTEINS; VIRUS RELEASE;

VACCINIA VIRUS;

EID: 84875967902     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003239     Document Type: Article

References (82)

1. Morita E, Sundquist WI, (2004) Retrovirus budding. Annu Rev Cell Dev Biol 20: 395-425.
2. Nayak DP, Balogun RA, Yamada H, Zhou ZH, Barman S, (2009) Influenza virus morphogenesis and budding. Virus Res 143: 147-161.
3. Weiss ER, Gottlinger H, (2011) The role of cellular factors in promoting HIV budding. J Mol Biol 410: 525-533.
4. Mettenleiter TC, Klupp BG, Granzow H, (2009) Herpesvirus assembly: an update. Virus Res 143: 222-234.
5. Roberts KL, Smith GL, (2008) Vaccinia virus morphogenesis and dissemination. Trends Microbiol 16: 472-479.
6. 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: 3319-3325.
7. 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: 294-302.
8. Mathew E, Sanderson CM, Hollinshead M, Smith GL, (1998) The extracellular domain of vaccinia virus protein B5R affects plaque phenotype, extracellular enveloped virus release, and intracellular actin tail formation. J Virol 72: 2429-2438.
9. 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: 801-810.
10. 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: 7217-7224.
11. Roper RL, Payne LG, Moss B, (1996) Extracellular vaccinia virus envelope glycoprotein encoded by the A33R gene. J Virol 70: 3753-3762.
12. Duncan SA, Smith GL, (1992) Identification and characterization of an extracellular envelope glycoprotein affecting vaccinia virus egress. J Virol 66: 1610-1621.
13. 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: 12266-12275.
14. Katz E, Wolffe E, Moss B, (2002) Identification of second-site mutations that enhance release and spread of vaccinia virus. J Virol 76: 11637-11644.
15. Payne LG, Kristensson K, (1982) The effect of cytochalasin D and monensin on enveloped vaccinia virus release. Arch Virol 74: 11-20.
16. Yang H, Kim SK, Kim M, Reche PA, Morehead TJ, et al. (2005) Antiviral chemotherapy facilitates control of poxvirus infections through inhibition of cellular signal transduction. J Clin Invest 115: 379-387.
17. McNulty S, Powell K, Erneux C, Kalman D, (2011) The host phosphoinositide 5-phosphatase SHIP2 regulates dissemination of vaccinia virus. J Virol 85: 7402-7410.
18. Reeves PM, Smith SK, Olson VA, Thorne SH, Bornmann W, et al. (2011) Variola and monkeypox viruses utilize conserved mechanisms of virion motility and release that depend on abl and SRC family tyrosine kinases. J Virol 85: 21-31.
19. Reeves PM, Bommarius B, Lebeis S, McNulty S, Christensen J, et al. (2005) Disabling poxvirus pathogenesis by inhibition of Abl-family tyrosine kinases. [erratum appears in Nat Med. 2005 Dec;11(12):1361]. Nat Med 11: 731-739.
20. Newsome TP, Weisswange I, Frischknecht F, Way M, (2006) Abl collaborates with Src family kinases to stimulate actin-based motility of vaccinia virus. Cell Microbiol 8: 233-241.
21. 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: 26-36.
22. 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: 195-207.
23. Dodding MP, Mitter R, Humphries AC, Way M, (2011) A kinesin-1 binding motif in vaccinia virus that is widespread throughout the human genome. The EMBO journal 30: 4523-4538.
24. Rietdorf J, Ploubidou A, Reckmann I, Holmstrom A, Frischknecht F, et al. (2001) Kinesin-dependent movement on microtubules precedes actin-based motility of vaccinia virus. Nature Cell Biology 3: 992-1000.
25. 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: 2486-2493.
26. Scaplehorn N, Holmstrom A, Moreau V, Frischknecht F, Reckmann I, et al. (2002) Grb2 and Nck act cooperatively to promote actin-based motility of vaccinia virus. Curr Biol 12: 740-745.
27. Frischknecht F, Moreau V, Rottger S, Gonfloni S, Reckmann I, et al. (1999) Actin-based motility of vaccinia virus mimics receptor tyrosine kinase signalling. Nature 401: 926-929.
28. Weisswange I, Newsome TP, Schleich S, Way M, (2009) The rate of N-WASP exchange limits the extent of Arp2/3 complex dependent actin-based motility. Nature 458: 87-91.
29. Moreau V, Frischknecht F, Reckmann I, Vincentelli R, Rabut G, et al. (2000) A complex of N-WASP and WIP integrates signalling cascades that lead to actin polymerization. Nature Cell Biology 2: 441-448.
30. Newsome TP, Scaplehorn N, Way M, (2004) SRC mediates a switch from microtubule- to actin-based motility of vaccinia virus. Science 306: 124-129.
31. Capdeville R, Buchdunger E, Zimmermann J, Matter A, (2002) Glivec (STI571, imatinib), a rationally developed, targeted anticancer drug. Nature Reviews Drug Discovery 1: 493-502.
32. Doceul V, Hollinshead M, van der Linden L, Smith GL, (2010) Repulsion of Superinfecting Virions: A Mechanism for Rapid Virus Spread. Science 327: 873-876.
33. Carabeo R, (2011) Bacterial subversion of host actin dynamics at the plasma membrane. Cell Microbiol 13: 1460-1469.
34. Taylor MP, Koyuncu OO, Enquist LW, (2011) Subversion of the actin cytoskeleton during viral infection. Nat Rev Microbiol 9: 427-439.
35. Law M, Hollinshead R, Smith GL, (2002) Antibody-sensitive and antibody-resistant cell-to-cell spread by vaccinia virus: role of the A33R protein in antibody-resistant spread.[erratum appears in J Gen Virol 2002 May;83(Pt 5):1251]. J Gen Virol 83: 209-222.
36. Ward BM, Moss B, (2001) Vaccinia virus intracellular movement is associated with microtubules and independent of actin tails. J Virol 75: 11651-11663.
37. 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: 376-390.
38. 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: 20-26.
39. 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: 2961-2968.
40. McIntosh AA, Smith GL, (1996) Vaccinia virus glycoprotein A34R is required for infectivity of extracellular enveloped virus. J Virol 70: 272-281.
41. 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: 4732-4741.
42. 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: 5108-5120.
43. 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: 4192-4204.
44. Doceul V, Hollinshead M, Breiman A, Laval K, Smith GL, (2012) Protein B5 is required on extracellular enveloped vaccinia virus for repulsion of super-infecting virions. J Gen Virol 93: 1876-1886.
45. Bladt F, Aippersbach E, Gelkop S, Strasser GA, Nash P, et al. (2003) The murine Nck SH2/SH3 adaptors are important for the development of mesoderm-derived embryonic structures and for regulating the cellular actin network. Mol Cell Biol 23: 4586-4597.
46. Arakawa Y, Cordeiro JV, Schleich S, Newsome TP, Way M, (2007) The release of vaccinia from infected cells requires RhoA-mDia modulation of cortical actin. Cell Host Microbe 1: 227-240.
47. Meiser A, Sancho C, Krijnse Locker J, (2003) Plasma membrane budding as an alternative release mechanism of the extracellular enveloped form of vaccinia virus from HeLa cells. J Virol 77: 9931-9942.
48. Smith GL, Vanderplasschen A, Law M, (2002) The formation and function of extracellular enveloped vaccinia virus. J Gen Virol 83: 2915-2931.
49. Gustafsson MG, (2000) Surpassing the lateral resolution limit by a factor of two using structured illumination microscopy. J Microsc 198: 82-87.
50. Riedl J, Crevenna AH, Kessenbrock K, Yu JH, Neukirchen D, et al. (2008) Lifeact: a versatile marker to visualize F-actin. Nat Methods 5: 605-607.
51. Horsington J, Turnbull L, Whitchurch CB, Newsome TP, (2012) Sub-viral imaging of vaccinia virus using super-resolution microscopy. J Virol Methods 186: 132-136.
52. Blasco R, Moss B, (1992) Role of cell-associated enveloped vaccinia virus in cell-to-cell spread.[erratum appears in J Virol 1992 Sep;66(9):5703-4]. J Virol 66: 4170-4179.
53. 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: 5347-5351.
54. Payne LG, (1980) Significance of extracellular enveloped virus in the in vitro and in vivo dissemination of vaccinia. J Gen Virol 50: 89-100.
55. Payne LG, Kristenson K, (1979) Mechanism of vaccinia virus release and its specific inhibition by N1-isonicotinoyl-N2-3-methyl-4-chlorobenzoylhydrazine. J Virol 32: 614-622.
56. Smith GL, Law M, (2004) The exit of vaccinia virus from infected cells. Virus Res 106: 189-197.
57. Fogg C, Lustig S, Whitbeck JC, Eisenberg RJ, Cohen GH, et al. (2004) Protective immunity to vaccinia virus induced by vaccination with multiple recombinant outer membrane proteins of intracellular and extracellular virions. J Virol 78: 10230-10237.
58. Carter GC, Rodger G, Murphy BJ, Law M, Krauss O, et al. (2003) Vaccinia virus cores are transported on microtubules. J Gen Virol 84: 2443-2458.
59. Dodding M, Newsome TP, Collinson L, Edwards C, Way M, (2009) An E2-F12 complex is required for IEV morphogenesis during vaccinia infection. Cell Microbiol 11: 808-824.
60. Morgan GW, Hollinshead M, Ferguson BJ, Murphy BJ, Carpentier DC, et al. (2010) Vaccinia protein F12 has structural similarity to kinesin light chain and contains a motor binding motif required for virion export. PLoS Pathog 6: e1000785.
61. Humphries AC, Dodding MP, Barry DJ, Collinson LM, Durkin CH, et al. (2012) Clathrin potentiates vaccinia-induced actin polymerization to facilitate viral spread. Cell Host Microbe 12: 346-359.
62. Meiser A, Boulanger D, Sutter G, Krijnse Locker J, (2003) Comparison of virus production in chicken embryo fibroblasts infected with the WR, IHD-J and MVA strains of vaccinia virus: IHD-J is most efficient in trans-Golgi network wrapping and extracellular enveloped virus release. J Gen Virol 84: 1383-1392.
63. Chan WM, Ward BM, (2012) The A33-Dependent Incorporation of B5 into Extracellular Enveloped Vaccinia Virions is Mediated Through an Interaction Between Their Lumenal Domains. J Virol 86: 8210-8220.
64. Perdiguero B, Blasco R, (2006) Interaction between vaccinia virus extracellular virus envelope A33 and B5 glycoproteins. J Virol 80: 8763-8777.
65. Perdiguero B, Lorenzo MM, Blasco R, (2008) Vaccinia virus A34 glycoprotein determines the protein composition of the extracellular virus envelope. J Virol 82: 2150-2160.
66. Chan WM, Ward BM, (2012) Increased Interaction between Vaccinia Virus Proteins A33 and B5 is Detrimental to Infectious Extracellular Enveloped Virion Production. J Virol 86: 8232-8244.
67. Olson VA, Karem KL, Smith SK, Hughes CM, Damon IK, (2009) Smallpox virus plaque phenotypes: genetic, geographical and case fatality relationships. J Gen Virol 90: 792-798.
68. Dodding MP, Way M, (2009) Nck- and N-WASP-dependent actin-based motility is conserved in divergent vertebrate poxviruses. Cell Host Microbe 6: 536-550.
69. Davison AJ, Moss B, (1989) Structure of vaccinia virus early promoters. J Mol Biol 210: 749-769.
70. Davison AJ, Moss B, (1989) Structure of vaccinia virus late promoters. J Mol Biol 210: 771-784.
71. Rottner K, Lommel S, Wehland J, Stradal TE, (2004) Pathogen-induced actin filament rearrangement in infectious diseases. J Pathol 204: 396-406.
72. Ohkawa T, Volkman LE, Welch MD, (2010) Actin-based motility drives baculovirus transit to the nucleus and cell surface. J Cell Biol 190: 187-195.
73. Stevens JM, Galyov EE, Stevens MP, (2006) Actin-dependent movement of bacterial pathogens. Nat Rev Microbiol 4: 91-101.
74. Lambrechts A, Gevaert K, Cossart P, Vandekerckhove J, Van Troys M, (2008) Listeria comet tails: the actin-based motility machinery at work. Trends Cell Biol 18: 220-227.
75. Roberts KL, Baines JD, (2011) Actin in herpesvirus infection. Viruses 3: 336-346.
76. Kaksonen M, Toret CP, Drubin DG, (2006) Harnessing actin dynamics for clathrin-mediated endocytosis. Nat Rev Mol Cell Biol 7: 404-414.
77. Sun X, Whittaker GR, (2007) Role of the actin cytoskeleton during influenza virus internalization into polarized epithelial cells. Cell Microbiol 9: 1672-1682.
78. 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: 2747-2760.
79. Lynn H, Horsington J, Ter LK, Han S, Chew YL, et al. (2012) Loss of Cytoskeletal Transport during Egress Critically Attenuates Ectromelia Virus Infection In Vivo. J Virol 86: 7427-7443.
80. Schmelz M, Sodeik B, Ericsson M, Wolffe EJ, Shida H, et al. (1994) Assembly of vaccinia virus: the second wrapping cisterna is derived from the trans Golgi network. J Virol 68: 130-147.
81. Riglar DT, Richard D, Wilson DW, Boyle MJ, Dekiwadia C, et al. (2011) Super-resolution dissection of coordinated events during malaria parasite invasion of the human erythrocyte. Cell Host Microbe 9: 9-20.
82. Strauss MP, Liew AT, Turnbull L, Whitchurch CB, Monahan LG, et al. (2012) 3D-SIM super resolution microscopy reveals a bead-like arrangement for FtsZ and the division machinery: implications for triggering cytokinesis. PLoS Biol 10: e1001389.