Vaccinia protein F12 has structural similarity to kinesin light chain and contains a motor binding motif required for virion export

PLoS Pathogens

Volumn 6, Issue 2, 2010, Pages

  Morgan, Gareth W ^a   Hollinshead, Michael ^a   Ferguson, Brian J ^a   Murphy, Brendan J ^a   Carpentier, David C J ^a   Smith, Geoffrey L ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARTIC ACID; CALSYNTENIN; KINESIN; KINESIN 1; MOLECULAR MOTOR; MUTANT PROTEIN; TRYPTOPHAN; UNCLASSIFIED DRUG; VACCINIA PROTEIN F12; VIRUS PROTEIN; KINESIN LIGHT CHAIN PROTEINS; KINESIN LIGHT-CHAIN PROTEINS; MICROTUBULE ASSOCIATED PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; HUMAN; HUMAN CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SEQUENCE ALIGNMENT; TETRATRICOPEPTIDE REPEAT; VACCINIA VIRUS; VIRION; CHEMICAL STRUCTURE; CHEMISTRY; CRYOELECTRON MICROSCOPY; GENETICS; HELA CELL; IMMUNOELECTRON MICROSCOPY; METABOLISM; MOLECULAR GENETICS; MOLECULAR MIMICRY; PATHOGENICITY; PHYSIOLOGY; POLYMERASE CHAIN REACTION; PROTEIN TERTIARY STRUCTURE;

VACCINIA VIRUS;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; CONSERVED SEQUENCE; CRYOELECTRON MICROSCOPY; HELA CELLS; HUMANS; MICROSCOPY, IMMUNOELECTRON; MICROTUBULE-ASSOCIATED PROTEINS; MODELS, MOLECULAR; MOLECULAR MIMICRY; MOLECULAR SEQUENCE DATA; POLYMERASE CHAIN REACTION; PROTEIN STRUCTURE, TERTIARY; VACCINIA VIRUS; VIRAL PROTEINS; VIRION;

EID: 77649253974     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000785     Document Type: Article

References (80)

1. Moss B (2007) Fields' virology Fields BN, Knipe DM, Howley PM, eds. Philadelphia: Wolters Kluwer Health/Lippincott Williams & Wilkins. 2 v. (xix, 3091, 3086 p.) p.
2. Roberts KL, Smith GL (2008) Vaccinia virus morphogenesis and dissemination. Trends Microbiol 16: 472-479.
3. Smith GL, Vanderplasschen A, Law M (2002) The formation and function of extracellular enveloped vaccinia virus. J Gen Virol 83: 2915-2931.
4. Dales S, Mosbach EH (1968) Vaccinia as a model for membrane biogenesis. Virology 35: 564-583.
5. Condit RC, Moussatche N, Traktman P (2006) In a nutshell: structure and assembly of the vaccinia virion. Adv Virus Res 66: 31-124.
6. 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: 47-58.
7. Ward BM (2005) Visualization and characterization of the intracellular movement of vaccinia virus intracellular mature virions. J Virol 79: 4755-4763.
8. Ichihashi Y, Matsumoto S, Dales S (1971) Biogenesis of poxviruses: role of A-type inclusions and host cell membranes in virus dissemination. Virology 46: 507-532.
9. 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.
10. Morgan C (1976) Vaccinia virus reexamined: development and release. Virology 73: 43-58.
11. Hiller G, Weber K (1985) Golgi-derived membranes that contain an acylated viral polypeptide are used for vaccinia virus envelopment. J Virol 55: 651-659.
12. 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: 163-178.
13. 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.
14. Hollinshead M, Rodger G, Van Eijl H, Law M, Hollinshead R, et al. (2001) Vaccinia virus utilizes microtubules for movement to the cell surface. J Cell Biol 154: 389-402.
15. Ward BM, Moss B (2001) Vaccinia virus intracellular movement is associated with microtubules and independent of actin tails. J Virol 75: 11651-11663.
16. 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.
17. 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. Nat Cell Biol 3: 992-1000.
18. 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.
19. 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.
20. 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: 11654-11662.
21. 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.
22. Schnapp BJ (2003) Trafficking of signaling modules by kinesin motors. J Cell Sci 116: 2125-2135.
23. Gauger AK, Goldstein LS (1993) The Drosophila kinesin light chain. Primary structure and interaction with kinesin heavy chain. J Biol Chem 268: 13657-13666.
24. Adio S, Reth J, Bathe F, Woehlke G (2006) Review: regulation mechanisms of Kinesin-1. J Muscle Res Cell Motil 27: 153-160.
25. Hirokawa N, Takemura R (2005) Molecular motors and mechanisms of directional transport in neurons. Nat Rev Neurosci 6: 201-214.
26. Gindhart JG Jr, Goldstein LS (1996) Tetratrico peptide repeats are present in the kinesin light chain. Trends Biochem Sci 21: 52-53.
27. D'Andrea LD, Regan L (2003) TPR proteins: the versatile helix. Trends Biochem Sci 28: 655-662.
28. Bowman AB, Kamal A, Ritchings BW, Philp AV, McGrail M, et al. (2000) Kinesin-dependent axonal transport is mediated by the sunday driver (SYD) protein. Cell 103: 583-594.
29. Bracale A, Cesca F, Neubrand VE, Newsome TP, Way M, et al. (2007) Kidins220/ARMS is transported by a kinesin-1-based mechanism likely to be involved in neuronal differentiation. Mol Biol Cell 18: 142-152.
30. Konecna A, Frischknecht R, Kinter J, Ludwig A, Steuble M, et al. (2006) Calsyntenin-1 docks vesicular cargo to kinesin-1. Mol Biol Cell 17: 3651-3663.
31. Kimura T, Watanabe H, Iwamatsu A, Kaibuchi K (2005) Tubulin and CRMP-2 complex is transported via Kinesin-1. J Neurochem 93: 1371-1382.
32. McGuire JR, Rong J, Li SH, Li XJ (2006) Interaction of Huntingtin-associated protein-1 with kinesin light chain: implications in intracellular trafficking in neurons. J Biol Chem 281: 3552-3559.
33. Kamm C, Boston H, Hewett J, Wilbur J, Corey DP, et al. (2004) The early onset dystonia protein torsinA interacts with kinesin light chain 1. J Biol Chem 279: 19882-19892.
34. Ichimura T, Wakamiya-Tsuruta A, Itagaki C, Taoka M, Hayano T, et al. (2002) Phosphorylation-dependent interaction of kinesin light chain 2 and the 14-3-3 protein. Biochemistry 41: 5566-5572.
35. Kamal A, Stokin GB, Yang Z, Xia CH, Goldstein LS (2000) Axonal transport of amyloid precursor protein is mediated by direct binding to the kinesin light chain subunit of kinesin-I. Neuron 28: 449-459.
36. Aoyama T, Hata S, Nakao T, Tanigawa Y, Oka C, et al. (2009) Cayman ataxia protein caytaxin is transported by kinesin along neurites through binding to kinesin light chains. J Cell Sci 122: 4177-4185.
37. Henry T, Couillault C, Rockenfeller P, Boucrot E, Dumont A, et al. (2006) The Salmonella effector protein PipB2 is a linker for kinesin-1. Proc Natl Acad Sci U S A 103: 13497-13502.
38. Wozniak MJ, Allan VJ (2006) Cargo selection by specific kinesin light chain 1 isoforms. EMBO J 25: 5457-5468.
39. Hammond JW, Griffin K, Jih GT, Stuckey J, Verhey KJ (2008) Co-operative versus independent transport of different cargoes by Kinesin-1. Traffic 9: 725-741.
40. Morfini G, Szebenyi G, Elluru R, Ratner N, Brady ST (2002) Glycogen synthase kinase 3 phosphorylates kinesin light chains and negatively regulates kinesin-based motility. Embo J 21: 281-293.
41. Morfini G, Szebenyi G, Brown H, Pant HC, Pigino G, et al. (2004) A novel CDK5-dependent pathway for regulating GSK3 activity and kinesin-driven motility in neurons. Embo J 23: 2235-2245.
42. Newsome TP, Scaplehorn N, Way M (2004) SRC mediates a switch from microtubule- to actin-based motility of vaccinia virus. Science 306: 124-129.
43. Arakawa Y, Cordeiro JV, Schleich S, Newsome TP, Way M (2007) The release of vaccinia virus from infected cells requires RhoA-mDia modulation of cortical actin. Cell Host Microbe 1: 227-240.
44. 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.
45. Reeves PM, Bommarius B, Lebeis S, McNulty S, Christensen J, et al. (2005) Disabling poxvirus pathogenesis by inhibition of Abl-family tyrosine kinases. Nat Med 11: 731-739.
46. 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. Nat Cell Biol 2: 441-448.
47. 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.
48. Frischknecht F, Cudmore S, Moreau V, Reckmann I, Rottger S, et al. (1999) Tyrosine phosphorylation is required for actin-based motility of vaccinia but not Listeria or Shigella. Curr Biol 9: 89-92.
49. 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.
50. 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.
51. 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(Pt 6): 1415-1425.
52. 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.
53. Ogawa R, Calvert JG, Yanagida N, Nazerian K (1993) Insertional inactivation of a fowlpox virus homologue of the vaccinia virus F12L gene inhibits the release of enveloped virions. J Gen Virol 74(Pt 1): 55-64.
54. Domi A, Weisberg AS, Moss B (2008) Vaccinia virus E2L null mutants exhibit a major reduction in extracellular virion formation and virus spread. J Virol 82: 4215-4226.
55. Dodding MP, Newsome TP, Collinson LM, Edwards C, Way M (2009) An E2-F12 complex is required for IEV morphogenesis during vaccinia infection. Cell Microbiol.
56. Johnston SC, Ward BM (2009) Vaccinia virus protein F12 associates with intracellular enveloped virions through an interaction with A36. J Virol 83: 1708-1717.
57. Chakrabarti S, Sisler JR, Moss B (1997) Compact, synthetic, vaccinia virus early/late promoter for protein expression. Biotechniques 23: 1094-1097.
58. Law M, Hollinshead M, Lee HJ, Smith GL (2004) Yaba-like disease virus protein Y144R, a member of the complement control protein family, is present on enveloped virions that are associated with virus-induced actin tails. J Gen Virol 85: 1279-1290.
59. Carter GC, Law M, Hollinshead M, Smith GL (2005) Entry of the vaccinia virus intracellular mature virion and its interactions with glycosaminoglycans. J Gen Virol 86: 1279-1290.
60. Brady ST, Pfister KK, Bloom GS (1990) A monoclonal antibody against kinesin inhibits both anterograde and retrograde fast axonal transport in squid axoplasm. Proc Natl Acad Sci U S A 87: 1061-1065.
61. 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.
62. Araki Y, Kawano T, Taru H, Saito Y, Wada S, et al. (2007) The novel cargo Alcadein induces vesicle association of kinesin-1 motor components and activates axonal transport. Embo J 26: 1475-1486.
63. Ross JL, Ali MY, Warshaw DM (2008) Cargo transport: molecular motors navigate a complex cytoskeleton. Curr Opin Cell Biol 20: 41-47.
64. Hackney DD (2007) Jump-starting kinesin. J Cell Biol 176: 7-9.
65. Davies MV, Elroy-Stein O, Jagus R, Moss B, Kaufman RJ (1992) 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 66: 1943-1950.
66. Moore JB, Smith GL (1992) Steroid hormone synthesis by a vaccinia enzyme: a new type of virus virulence factor. EMBO J 11: 3490.
67. 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: 153-167.
68. Cooray S, Bahar MW, Abrescia NG, McVey CE, Bartlett NW, et al. (2007) Functional and structural studies of the vaccinia virus virulence factor N1 reveal a Bcl-2-like anti-apoptotic protein. J Gen Virol 88: 1656-1666.
69. Chen RA, Ryzhakov G, Cooray S, Randow F, Smith GL (2008) Inhibition of IkappaB kinase by vaccinia virus virulence factor B14. PLoS Pathog 4: e22. doi:10.1371/journal.ppat.0040022.
70. Graham SC, Bahar MW, Cooray S, Chen RA, Whalen DM, et al. (2008) Vaccinia virus proteins A52 and B14 Share a Bcl-2-like fold but have evolved to inhibit NF-kappaB rather than apoptosis. PLoS Pathog 4: e1000128. doi:10.1371/journal. ppat.1000128.
71. Cai D, Hoppe AD, Swanson JA, Verhey KJ (2007) Kinesin-1 structural organization and conformational changes revealed by FRET stoichiometry in live cells. J Cell Biol 176: 51-63.
72. 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.
73. Stenoien DL, Brady ST (1997) Immunochemical analysis of kinesin light chain function. Mol Biol Cell 8: 675-689.
74. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
75. Jeanmougin F, Thompson JD, Gouy M, Higgins DG, Gibson TJ (1998) Multiple sequence alignment with Clustal X. Trends Biochem Sci 23: 403-405.
76. Waterhouse AM, Procter JB, Martin DM, Clamp M, Barton GJ (2009) Jalview Version 2-a multiple sequence alignment editor and analysis workbench. Bioinformatics 25: 1189-1191.
77. Marti-Renom MA, Stuart AC, Fiser A, Sanchez R, Melo F, et al. (2000) Comparative protein structure modeling of genes and genomes. Annu Rev Biophys Biomol Struct 29: 291-325.
78. Laskowski RA, Moss DS, Thornton JM (1993) Main-chain bond lengths and bond angles in protein structures. J Mol Biol 231: 1049-1067.
79. Vriend G (1990) WHAT IF: a molecular modeling and drug design program. J Mol Graph 8: 52-56, 29.
80. Luthy R, Bowie JU, Eisenberg D (1992) Assessment of protein models with three-dimensional profiles. Nature 356: 83-85.