Interaction of poxvirus intracellular mature virion proteins with the TPR domain of kinesin light chain in live infected cells revealed by two-photon-induced fluorescence resonance energy transfer fluorescence lifetime imaging microscopy

Journal of Virology

Volumn 84, Issue 24, 2010, Pages 12886-12894

  Jeshtadi, Ananya ^a   Burgos, Pierre ^b   Stubbs, Christopher D ^b   Parker, Anthony W ^b   King, Linda A ^a   Skinner, Michael A ^c   Botchway, Stanley W ^b  

^a OXFORD BROOKES UNIVERSITY   (United Kingdom)

^b Harwell Science and Innovation Campus   (United Kingdom)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

A36 PROTEIN; ENHANCED GREEN FLUORESCENT PROTEIN; KINESIN; MODIFIED VACCINIA VIRUS ANKARA 5T4 VACCINE; RECOMBINANT PROTEIN; RED FLUORESCENT PROTEIN; UNCLASSIFIED DRUG; VIRUS ENVELOPE PROTEIN;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; EMBRYO; FIBROBLAST; FLUORESCENCE MICROSCOPY; FLUORESCENCE RESONANCE ENERGY TRANSFER; FOWLPOX VIRUS; INTRACELLULAR TRANSPORT; LIGHT CHAIN; MOLECULAR IMAGING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; TETRATRICOPEPTIDE REPEAT; TWO HYBRID SYSTEM; VACCINIA VIRUS; VIRUS RECOMBINANT; WILD TYPE; YEAST;

ANIMALS; CHICK EMBRYO; FIBROBLASTS; FLUORESCENCE RESONANCE ENERGY TRANSFER; FLUORESCENT ANTIBODY TECHNIQUE; GREEN FLUORESCENT PROTEINS; HUMANS; LUMINESCENT PROTEINS; MICROSCOPY, FLUORESCENCE; MICROTUBULE-ASSOCIATED PROTEINS; PHOTONS; PLASMIDS; POXVIRIDAE; POXVIRIDAE INFECTIONS; VIRAL PROTEINS; VIRAL STRUCTURAL PROTEINS; VIRION;

AVIPOXVIRUS; FOWLPOX VIRUS; ORTHOPOXVIRUS; POXVIRIDAE; VACCINIA VIRUS; VACCINIA VIRUS ANKARA;

EID: 78649420245     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01395-10     Document Type: Article

References (60)

1. Afonso, C. L., E. R. Tulman, G. Delhon, Z. Lu, G. J. Viljoen, D. B. Wallace, G. F. Kutish, and D. L. Rock. 2006. Genome of crocodilepox virus. J. Virol. 80:4978-4991.
2. Afonso, C. L., E. R. Tulman, Z. Lu, L. Zsak, G. F. Kutish, and D. L. Rock. 2000. The genome of fowlpox virus. J. Virol. 74:3815-3831.
3. Boulanger, D., P. Green, B. Jones, G. Henriquet, L. G. Hunt, S. M. Laidlaw, P. Monaghan, and M. A. Skinner. 2002. Identification and characterization of three immunodominant structural proteins of fowlpox virus. J. Virol. 76:9844-9855.
4. Boulanger, D., P. Green, T. Smith, C. P. Czerny, and M. A. Skinner. 1998. The 131-amino-acid repeat region of the essential 39-kilodalton core protein of fowlpox virus FP9, equivalent to vaccinia virus A4L protein, is nonessential and highly immunogenic. J. Virol. 72:170-179.
5. Boulanger, D., T. Smith, and M. A. Skinner. 2000. Morphogenesis and release of fowlpox virus. J. Gen. Virol. 81:675-687.
6. Breiman, A., and G. L. Smith. 2010. Vaccinia virus B5 protein affects the glycosylation, localization and stability of the A34 protein. J. Gen. Virol. 91:1823-1827.
7. Brown, M., Y. Zhang, S. Dermine, E. A. de Wynter, C. Hart, H. Kitchener, P. L. Stern, M. A. Skinner, and S. N. Stacey. 2000. Dendritic cells infected with recombinant fowlpox virus vectors are potent and long-acting stimulators of transgene-specific class I restricted T lymphocyte activity. Gene Ther. 7:1680-1689.
8. Bublot, M., N. Pritchard, J. S. Cruz, T. R. Mickle, P. Selleck, and D. E. Swayne. 2007. Efficacy of a fowlpox-vectored avian influenza H5 vaccine against Asian H5N1 highly pathogenic avian influenza virus challenge. Avian Dis. 51:498-500.
9. Chan, W. M., and B. M. Ward. 2010. There is an A33-dependent mechanism for the incorporation of B5-GFP into vaccinia virus extracellular enveloped virions. Virology 402:83-93.
10. Chen, Y., and A. Periasamy. 2004. Characterization of two-photon excitation fluorescence lifetime imaging microscopy for protein localization. Microsc. Res. Tech. 63:72-80.
11. Cudmore, S., P. Cossart, G. Griffiths, and M. Way. 1995. Actin-based motility of vaccinia virus. Nature 378:636-638.
12. da Fonseca, F. G., E. J. Wolffe, A. Weisberg, and B. Moss. 2000. Characterization of the vaccinia virus H3L envelope protein: topology and posttranslational membrane insertion via the C-terminal hydrophobic tail. J. Virol. 74:7508-7517.
13. Delhon, G., E. R. Tulman, C. L. Afonso, Z. Lu, A. de la Concha-Bermejillo, H. D. Lehmkuhl, M. E. Piccone, G. F. Kutish, and D. L. Rock. 2004. Genomes of the parapoxviruses ORF virus and bovine papular stomatitis virus. J. Virol. 78:168-177.
14. Dodding, M. P., T. P. Newsome, L. M. Collinson, C. Edwards, and M. Way. 2009. An E2-F12 complex is required for IEV morphogenesis during vaccinia infection. Cell Microbiol. 11:808-824.
15. Domi, A., A. S. Weisberg, and B. Moss. 2008. Vaccinia virus E2L null mutants exhibit a major reduction in extracellular virion formation and virus spread. J. Virol. 82:4215-4226. (Pubitemid 351563659)
16. Duncan, S. A., and G. L. Smith. 1992. Identification and characterization of an extracellular envelope glycoprotein affecting vaccinia virus egress. J. Virol. 66:1610-1621.
17. Engelstad, M., S. T. Howard, and G. L. Smith. 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.
18. Gindhart, J. G., Jr., and L. S. Goldstein. 1996. Tetratrico peptide repeats are present in the kinesin light chain. Trends Biochem. Sci. 21:52-53.
19. Hatano, Y., M. Yoshida, F. Uno, S. Yoshida, N. Osafune, K. Ono, M. Yamada, and S. Nii. 2001. Budding of fowlpox and pigeonpox viruses at the surface of infected cells. J. Electron Microsc. (Tokyo) 50:113-124.
20. Hautaniemi, M., N. Ueda, J. Tuimala, A. A. Mercer, J. Lahdenpera, and C. J. McInnes. 2010. The genome of Pseudocowpoxvirus: comparison of a reindeer isolate and a reference strain. J. Gen. Virol. 91:1560-1576.
21. Herrero-Martinez, E., K. L. Roberts, M. Hollinshead, and G. L. Smith. 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.
22. Hollinshead, M., G. Rodger, H. Van Eijl, M. Law, R. Hollinshead, D. J. Vaux, and G. L. Smith. 2001. Vaccinia virus utilizes microtubules for movement to the cell surface. J. Cell Biol. 154:389-402.
23. Howard, A. R., T. G. Senkevich, and B. Moss. 2008. Vaccinia virus A26 and A27 proteins form a stable complex tethered to mature virions by association with the A17 transmembrane protein. J. Virol. 82:12384-12391.
24. Husain, M., A. S. Weisberg, and B. Moss. 2006. Existence of an operative pathway from the endoplasmic reticulum to the immature poxvirus membrane. Proc. Natl. Acad. Sci. U. S. A. 103:19506-19511.
25. Isaacs, S. N., E. J. Wolffe, L. G. Payne, and B. Moss. 1992. Characterization of a vaccinia virus-encoded 42-kilodalton class I membrane glycoprotein component of the extracellular virus envelope. J. Virol. 66:7217-7224.
26. Jeshtadi, A., G. Henriquet, S. M. Laidlaw, D. Hot, Y. Zhang, and M. A. Skinner. 2005. In vitro expression and analysis of secreted fowlpox virus CC chemokine-like proteins Fpv060, Fpv061, Fpv116 and Fpv121. Arch. Virol. 150:1745-1762.
27. Johnston, S. C., and B. M. Ward. 2009. Vaccinia virus protein F12 associates with intracellular enveloped virions through an interaction with A36. J. Virol. 83:1708-1717.
28. Laidlaw, S. M., and M. A. Skinner. 2004. Comparison of the genome sequence of FP9, an attenuated, tissue culture-adapted European strain of Fowlpox virus, with those of virulent American and European viruses. J. Gen. Virol. 85:305-322.
29. Lin, C. L., C. S. Chung, H. G. Heine, and W. Chang. 2000. 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. 74:3353-3365.
30. McKelvey, T. A., S. C. Andrews, S. E. Miller, C. A. Ray, and D. J. Pickup. 2002. Identification of the orthopoxvirus p4c gene, which encodes a structural protein that directs intracellular mature virus particles into A-type inclusions. J. Virol. 76:11216-11225.
31. Morgan, G. W., M. Hollinshead, B. J. Ferguson, B. J. Murphy, D. C. Carpentier, and G. L. Smith. 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.
32. Moss, B. 2006. Poxvirus entry and membrane fusion. Virology 344:48-54.
33. Osterrieder, A., C. M. Carvalho, M. Latijnhouwers, J. N. Johansen, C. Stubbs, S. Botchway, and C. Hawes. 2009. Fluorescence lifetime imaging of interactions between Golgi tethering factors and small GTPases in plants. Traffic 10:1034-1046.
34. Ploubidou, A., V. Moreau, K. Ashman, I. Reckmann, C. Gonzalez, and M. Way. 2000. Vaccinia virus infection disrupts microtubule organization and centrosome function. EMBO J. 19:3932-3944. (Pubitemid 30608533)
35. Rerks-Ngarm, S., P. Pitisuttithum, S. Nitayaphan, J. Kaewkungwal, J. Chiu, R. Paris, N. Premsri, C. Namwat, M. de Souza, E. Adams, M. Benenson, S. Gurunathan, J. Tartaglia, J. G. McNeil, D. P. Francis, D. Stablein, D. L. Birx, S. Chunsuttiwat, C. Khamboonruang, P. Thongcharoen, M. L. Robb, N. L. Michael, P. Kunasol, and J. H. Kim. 2009. Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand. N. Engl. J. Med. 361:2209-2220.
36. Rietdorf, J., A. Ploubidou, I. Reckmann, A. Holmstrom, F. Frischknecht, M. Zettl, T. Zimmermann, and M. Way. 2001. Kinesin-dependent movement on microtubules precedes actin-based motility of vaccinia virus. Nat. Cell Biol. 3:992-1000.
37. Roberts, K. L., and G. L. Smith. 2008. Vaccinia virus morphogenesis and dissemination. Trends Microbiol. 16:472-479.
38. Rodriguez, J. F., and M. Esteban. 1987. Mapping and nucleotide sequence of the vaccinia virus gene that encodes a 14-kilodalton fusion protein. J. Virol. 61:3550-3554.
39. Roper, R. L., L. G. Payne, and B. Moss. 1996. Extracellular vaccinia virus envelope glycoprotein encoded by the A33R gene. J. Virol. 70:3753-3762. (Pubitemid 26157355)
40. Sanderson, C. M., M. Hollinshead, and G. L. Smith. 2000. The vaccinia virus A27L protein is needed for the microtubule-dependent transport of intracellular mature virus particles. J. Gen. Virol. 81:47-58.
41. Sarov, I., and W. K. Joklik. 1973. Isolation and characterization of intermediates in vaccinia virus morphogenesis. Virology 52:223-233.
42. Scolari, S., S. Engel, N. Krebs, A. P. Plazzo, R. F. De Almeida, M. Prieto, M. Veit, and A. Herrmann. 2009. Lateral distribution of the transmembrane domain of influenza virus hemagglutinin revealed by time-resolved fluorescence imaging. J. Biol. Chem. 284:15708-15716.
43. Senkevich, T. G., E. V. Koonin, J. J. Bugert, G. Darai, and B. Moss. 1997. The genome of molluscum contagiosum virus: analysis and comparison with other poxviruses. Virology 233:19-42.
44. Shida, H., K. Tanabe, and S. Matsumoto. 1977. Mechanism of virus occlusion into A-type inclusion during poxvirus infection. Virology 76:217-233. (Pubitemid 8031109)
45. Skinner, M. A., S. M. Laidlaw, I. Eldaghayes, P. Kaiser, and M. G. Cottingham. 2005. Fowlpox virus as a recombinant vaccine vector for use in mammals and poultry. Expert Rev. Vaccines 4:63-76.
46. Smith, G. L., A. Vanderplasschen, and M. Law. 2002. The formation and function of extracellular enveloped vaccinia virus. J. Gen. Virol. 83:2915-2931.
47. Snippe, M., J. W. Borst, R. Goldbach, and R. Kormelink. 2005. The use of fluorescence microscopy to visualise homotypic interactions of tomato spotted wilt virus nucleocapsid protein in living cells. J. Virol. Methods 125:15-22. (Pubitemid 40298809)
48. Snippe, M., J. Willem Borst, R. Goldbach, and R. Kormelink. 2007. Tomato spotted wilt virus Gc and N proteins interact in vivo. Virology 357:115-123. (Pubitemid 44821296)
49. Sodeik, B., S. Cudmore, M. Ericsson, M. Esteban, E. G. Niles, and G. Griffiths. 1995. Assembly of vaccinia virus: incorporation of p14 and p32 into the membrane of the intracellular mature virus. J. Virol. 69:3560-3574.
50. Stubbs, C. D., S. W. Botchway, S. J. Slater, and A. W. Parker. 2005. The use of time-resolved fluorescence imaging in the study of protein kinase C localisation in cells. BMC Cell Biol. 6:22.
51. Suhling, K., P. M. French, and D. Phillips. 2005. Time-resolved fluorescence microscopy. Photochem. Photobiol. Sci. 4:13-22.
52. Tulman, E. R., C. L. Afonso, Z. Lu, L. Zsak, G. F. Kutish, and D. L. Rock. 2004. The genome of canarypox virus. J. Virol. 78:353-366.
53. Ulaeto, D., D. Grosenbach, and D. E. Hruby. 1996. The vaccinia virus 4c and A-type inclusion proteins are specific markers for the intracellular mature virus particle. J. Virol. 70:3372-3377.
54. Vale, R. D. 2003. The molecular motor toolbox for intracellular transport. Cell 112:467-480.
55. Vale, R. D., T. S. Reese, and M. P. Sheetz. 1985. Identification of a novel force-generating protein, kinesin, involved in microtubule-based motility. Cell 42:39-50.
56. van Eijl, H., M. Hollinshead, G. Rodger, W. H. Zhang, and G. L. Smith. 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.
57. van Eijl, H., M. Hollinshead, and G. L. Smith. 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.
58. Wallrabe, H., and A. Periasamy. 2005. Imaging protein molecules using FRET and FLIM microscopy. Curr. Opin. Biotechnol. 16:19-27.
59. Ward, B. M. 2005. Visualization and characterization of the intracellular movement of vaccinia virus intracellular mature virions. J. Virol. 79:4755-4763. (Pubitemid 40464226)
60. Ward, B. M., and B. Moss. 2004. Vaccinia virus A36R membrane protein provides a direct link between intracellular enveloped virions and the microtubule motor kinesin. J. Virol. 78:2486-2493.