1887

Abstract

African swine fever virus (ASFV) is a large, enveloped DNA virus that assembles in perinuclear sites located close to the centrosome. It is reported here that the microtubule network becomes disorganized soon after the onset of viral DNA replication and formation of assembly sites. ASFV infection resulted in loss of -tubulin and pericentrin at the centrosome; this was due to protein relocalization, but not degradation. ASFV infection also inhibited the ability of the centrosome to nucleate microtubules. The reorganization of microtubules seen in ASFV-infected cells may therefore be mediated by -tubulin and pericentrin redistribution, and consequent disruption of centrosome assembly and function.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.80623-0
2005-03-01
2024-05-09
Loading full text...

Full text loading...

/deliver/fulltext/jgv/86/3/vir860589.html?itemId=/content/journal/jgv/10.1099/vir.0.80623-0&mimeType=html&fmt=ahah

References

  1. Abal M., Piel M., Bouckson-Castaing V., Mogensen M., Sibarita J.-B., Bornens M. 2002; Microtubule release from the centrosome in migrating cells. J Cell Biol 159:731–737 [CrossRef]
    [Google Scholar]
  2. Afonso C. L., Alcaraz C., Brun A., Sussman M. D., Onisk D. V., Escribano J. M., Rock D. L. 1992; Characterization of p30, a highly antigenic membrane and secreted protein of African swine fever virus. Virology 189:368–373 [CrossRef]
    [Google Scholar]
  3. Alonso C., Miskin J., Hernáez B., Fernandez-Zapatero P., Soto L., Cantó C., Rodríguez-Crespo I., Dixon L., Escribano J. M. 2001; African swine fever virus protein p54 interacts with the microtubular motor complex through direct binding to light-chain dynein. J Virol 75:9819–9827 [CrossRef]
    [Google Scholar]
  4. Andrés G., García-Escudero R., Viñuela E., Salas M. L., Rodríguez J. M. 2001; African swine fever virus structural protein pE120R is essential for virus transport from assembly sites to plasma membrane but not for infectivity. J Virol 75:6758–6768 [CrossRef]
    [Google Scholar]
  5. Avitabile E., Di Gaeta S., Torrisi M. R., Ward P. L., Roizman B., Campadelli-Fiume G. 1995; Redistribution of microtubules and Golgi apparatus in herpes simplex virus-infected cells and their role in viral exocytosis. J Virol 69:7472–7482
    [Google Scholar]
  6. Bornens M. 2002; Centrosome composition and microtubule anchoring mechanisms. Curr Opin Cell Biol 14:25–34 [CrossRef]
    [Google Scholar]
  7. Bystrevskaya V. B., Lobova T. V., Smirnov V. N., Makarova N. E., Kushch A. A. 1997; Centrosome injury in cells infected with human cytomegalovirus. J Struct Biol 120:52–60 [CrossRef]
    [Google Scholar]
  8. Carrascosa A. L., del Val M., Santarén J. F., Viñuela E. 1985; Purification and properties of African swine fever virus. J Virol 54:337–344
    [Google Scholar]
  9. Carvalho Z. G., De Matos A. P. A., Rodrigues-Pousada C. 1988; Association of African swine fever virus with the cytoskeleton. Virus Res 11:175–192 [CrossRef]
    [Google Scholar]
  10. Chabin-Brion K., Marceiller J., Perez F., Settegrana C., Drechou A., Durand G., Poüs C. 2001; The Golgi complex is a microtubule-organizing organelle. Mol Biol Cell 12:2047–2060 [CrossRef]
    [Google Scholar]
  11. Cobbold C., Wileman T. 1998; The major structural protein of African swine fever virus, p73, is packaged into large structures, indicative of viral capsid or matrix precursors, on the endoplasmic reticulum. J Virol 72:5215–5223
    [Google Scholar]
  12. Dammermann A., Desai A., Oegema K. 2003; The minus end in sight. Curr Biol 13:R614–R624 [CrossRef]
    [Google Scholar]
  13. Dictenberg J. B., Zimmerman W., Sparks C. A., Young A., Vidair C., Zheng Y., Carrington W., Fay F. S., Doxsey S. J. 1998; Pericentrin and γ -tubulin form a protein complex and are organized into a novel lattice at the centrosome. J Cell Biol 141:163–174 [CrossRef]
    [Google Scholar]
  14. Doxsey S. J., Stein P., Evans L., Calarco P. D., Kirschner M. 1994; Pericentrin, a highly conserved centrosome protein involved in microtubule organization. Cell 76:639–650 [CrossRef]
    [Google Scholar]
  15. Gilloteaux J., Nassiri M. R. 2000; Human bone marrow fibroblasts infected by cytomegalovirus: ultrastructural observations. J Submicrosc Cytol Pathol 32:17–45
    [Google Scholar]
  16. Harlow E., Lane D. 1988 Antibodies: a Laboratory Manual Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  17. Heath C. M., Windsor M., Wileman T. 2001; Aggresomes resemble sites specialized for virus assembly. J Cell Biol 153:449–456 [CrossRef]
    [Google Scholar]
  18. Jouvenet N., Monaghan P., Way M., Wileman T. 2004; Transport of African swine fever virus from assembly sites to the plasma membrane is dependent on microtubules and conventional kinesin. J Virol 78:7990–8001 [CrossRef]
    [Google Scholar]
  19. Kirschner M. W., Mitchison T. 1986; Microtubule dynamics. Nature 324:621 [CrossRef]
    [Google Scholar]
  20. Kotsakis A., Pomeranz L. E., Blouin A., Blaho J. A. 2001; Microtubule reorganization during herpes simplex virus type 1 infection facilitates the nuclear localization of VP22, a major virion tegument protein. J Virol 75:8697–8711 [CrossRef]
    [Google Scholar]
  21. McCrossan M., Windsor M., Ponnambalam S., Armstrong J., Wileman T. 2001; The trans Golgi network is lost from cells infected with African swine fever virus. J Virol 75:11755–11765 [CrossRef]
    [Google Scholar]
  22. Monaghan P., Cook H., Jackson T., Ryan M., Wileman T. 2004; The ultrastructure of the developing replication site in foot-and-mouth disease virus-infected BHK-38 cells. J Gen Virol 85:933–946 [CrossRef]
    [Google Scholar]
  23. Murti K. G., Goorha R. 1983; Interaction of frog virus-3 with the cytoskeleton. I. Altered organization of microtubules, intermediate filaments, and microfilaments. J Cell Biol 96:1248–1257 [CrossRef]
    [Google Scholar]
  24. Oakley B. R. 1992; γ -Tubulin: the microtubule organizer?. Trends Cell Biol 2:1–5 [CrossRef]
    [Google Scholar]
  25. Piperno G., LeDizet M., Chang X.-J. 1987; Microtubules containing acetylated α -tubulin in mammalian cells in culture. J Cell Biol 104:289–302 [CrossRef]
    [Google Scholar]
  26. Ploubidou A., Way M. 2001; Viral transport and the cytoskeleton. Curr Opin Cell Biol 13:97–105 [CrossRef]
    [Google Scholar]
  27. Ploubidou A., Moreau V., Ashman K., Reckmann I., González C., Way M. 2000; Vaccinia virus infection disrupts microtubule organization and centrosome function. EMBO J 19:3932–3944 [CrossRef]
    [Google Scholar]
  28. Quintyne N. J., Gill S. R., Eckley D. M., Crego C. L., Compton D. A., Schroer T. A. 1999; Dynactin is required for microtubule anchoring at centrosomes. J Cell Biol 147:321–334 [CrossRef]
    [Google Scholar]
  29. Rodríguez J. M., Salas M. L., Viñuela E. 1996; Intermediate class of mRNAs in African swine fever virus. J Virol 70:8584–8589
    [Google Scholar]
  30. Rouiller I., Brookes S. M., Hyatt A. D., Windsor M., Wileman T. 1998; African swine fever virus is wrapped by the endoplasmic reticulum. J Virol 72:2373–2387
    [Google Scholar]
  31. Young A., Dictenberg J. B., Purohit A., Tuft R., Doxsey S. J. 2000; Cytoplasmic dynein-mediated assembly of pericentrin and γ tubulin onto centrosomes. Mol Biol Cell 11:2047–2056 [CrossRef]
    [Google Scholar]
  32. Zimmerman W., Sparks C. A., Doxsey S. J. 1999; Amorphous no longer: the centrosome comes into focus. Curr Opin Cell Biol 11:122–128 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.80623-0
Loading
/content/journal/jgv/10.1099/vir.0.80623-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error