Entry of the vaccinia virus intracellular mature virion and its interactions with glycosaminoglycans Free

Abstract

Vaccinia virus (VACV) produces two distinct enveloped virions, the intracellular mature virus (IMV) and the extracellular enveloped virus (EEV), but the entry mechanism of neither virion is understood. Here, the binding and entry of IMV particles have been investigated. The cell receptors for IMV are unknown, but it was proposed that IMV can bind to glycosaminoglycans (GAGs) on the cell surface and three IMV surface proteins have been implicated in this. In this study, the effect of soluble GAGs on IMV infectivity was reinvestigated and it was demonstrated that GAGs affected IMV infectivity partially in some cells, but not at all in others. Therefore, binding of IMV to GAGs is cell type-specific and not essential for IMV entry. By using electron microscopy, it is demonstrated that IMV from strains Western Reserve and modified virus Ankara enter cells by fusion with the plasma membrane. After an IMV particle bound to the cell, the IMV membrane fused with the plasma membrane and released the virus core into the cytoplasm. IMV surface antigen became incorporated into the plasma membrane and was not left outside the cell, as claimed in previous studies. Continuity between the IMV membrane and the plasma membrane was confirmed by tilt-series analysis to orientate membranes perpendicularly to the beam of the electron microscope. This analysis shows unequivocally that IMV is surrounded by a single lipid membrane and enters by fusion at the cell surface.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.80831-0
2005-05-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/jgv/86/5/vir861279.html?itemId=/content/journal/jgv/10.1099/vir.0.80831-0&mimeType=html&fmt=ahah

References

  1. Appleyard G., Hapel A. J., Boulter E. A. 1971; An antigenic difference between intracellular and extracellular poxviruses. J Gen Virol 13:9–17 [CrossRef]
    [Google Scholar]
  2. Armstrong J. A., Metz D. H., Young M. R. 1973; The mode of entry of vaccinia virus into L cells. J Gen Virol 21:533–537 [CrossRef]
    [Google Scholar]
  3. Carter G. C., Rodger G., Murphy B. J., Law M., Krauss O., Hollinshead M., Smith G. L. 2003; Vaccinia virus cores are transported on microtubules. J Gen Virol 84:2443–2458 [CrossRef]
    [Google Scholar]
  4. Chang A., Metz D. H. 1976; Further investigations on the mode of entry of vaccinia virus into cells. J Gen Virol 32:275–282 [CrossRef]
    [Google Scholar]
  5. Chillakuru R. A., Ryu D. D., Yilma T. 1991; Propagation of recombinant vaccinia virus in HeLa cells: adsorption kinetics and replication in batch cultures. Biotechnol Prog 7:85–92 [CrossRef]
    [Google Scholar]
  6. Chung C.-S., Hsiao J.-C., Chang Y.-S., Chang W. 1998; A27L protein mediates vaccinia virus interaction with cell surface heparan sulfate. J Virol 72:1577–1585
    [Google Scholar]
  7. Dales S. 1963; The uptake and development of vaccinia virus in strain L cells followed with labeled viral deoxyribonucleic acid. J Cell Biol 18:51–72 [CrossRef]
    [Google Scholar]
  8. Dales S., Siminovitch L. 1961; The development of vaccinia virus in Earle's L strain cells as examined by electron microscopy. J Biophys Biochem Cytol 10:475–503 [CrossRef]
    [Google Scholar]
  9. Dales S., Kajioka R. 1964; The cycle of multiplication of vaccinia virus in Earle's strain L cells. I. Uptake and penetration. Virology 24:278–294 [CrossRef]
    [Google Scholar]
  10. Dales S., Mosbach E. H. 1968; Vaccinia as a model for membrane biogenesis. Virology 35:564–583 [CrossRef]
    [Google Scholar]
  11. Doms R. W., Blumenthal R., Moss B. 1990; Fusion of intra- and extracellular forms of vaccinia virus with the cell membrane. J Virol 64:4884–4892
    [Google Scholar]
  12. Gong S. C., Lai C. F., Esteban M. 1990; Vaccinia virus induces cell fusion at acid pH and this activity is mediated by the N-terminus of the 14-kDa virus envelope protein. Virology 178:81–91 [CrossRef]
    [Google Scholar]
  13. Granados R. R. 1973; Entry of an insect poxvirus by fusion of the virus envelope with the host cell membrane. Virology 52:305–309 [CrossRef]
    [Google Scholar]
  14. Griffiths G., Wepf R., Wendt T., Krijnse Locker J., Cyrklaff M., Roos N. 2001; Structure and assembly of intracellular mature vaccinia virus: isolated-particle analysis. J Virol 75:11034–11055 [CrossRef]
    [Google Scholar]
  15. Grimley P. M., Rosenblum E. N., Mims S. J., Moss B. 1970; Interruption by rifampin of an early stage in vaccinia virus morphogenesis: accumulation of membranes which are precursors of virus envelopes. J Virol 6:519–533
    [Google Scholar]
  16. Hollinshead M., Vanderplasschen A., Smith G. L., Vaux D. J. 1999; Vaccinia virus intracellular mature virions contain only one lipid membrane. J Virol 73:1503–1517
    [Google Scholar]
  17. Hsiao J.-C., Chung C.-S., Chang W. 1998; 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 72:8374–8379
    [Google Scholar]
  18. Hsiao J.-C., Chung C.-S., Chang W. 1999; Vaccinia virus envelope D8L protein binds to cell surface chondroitin sulfate and mediates the adsorption of intracellular mature virions to cells. J Virol 73:8750–8761
    [Google Scholar]
  19. Janeczko R. A., Rodriguez J. F., Esteban M. 1987; Studies on the mechanism of entry of vaccinia virus in animal cells. Arch Virol 92:135–150 [CrossRef]
    [Google Scholar]
  20. Kjellen L., Lindahl U. 1991; Proteoglycans: structures and interactions. Annu Rev Biochem 60:443–475 [CrossRef]
    [Google Scholar]
  21. Krijnse Locker J., Kuehn A., Schleich S., Rutter G., Hohenberg H., Wepf R., Griffiths G. 2000; Entry of the two infectious forms of vaccinia virus at the plasma membrane is signaling-dependent for the IMV but not the EEV. Mol Biol Cell 11:2497–2511 [CrossRef]
    [Google Scholar]
  22. Law M., Smith G. L. 2004; Studying the binding and entry of the intracellular and extracellular enveloped forms of vaccinia virus. Methods Mol Biol 269:187–204
    [Google Scholar]
  23. Lin C.-L., Chung C.-S., Heine H. G., Chang W. 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 [CrossRef]
    [Google Scholar]
  24. Moss B. 2001; Poxviridae : the viruses and their replication. In Fields Virology , 4th edn. pp  2849–2883 Edited by Knipe D. M., Howley P. M. Philadelphia, PA: Lippincott Williams & Wilkins;
    [Google Scholar]
  25. O'Doherty U., Swiggard W. J., Malim M. H. 2000; Human immunodeficiency virus type 1 spinoculation enhances infection through virus binding. J Virol 74:10074–10080 [CrossRef]
    [Google Scholar]
  26. Parkinson J. E., Smith G. L. 1994; Vaccinia virus gene A36R encodes a M r 43-50 K protein on the surface of extracellular enveloped virus. Virology 204:376–390 [CrossRef]
    [Google Scholar]
  27. Payne L. 1978; Polypeptide composition of extracellular enveloped vaccinia virus. J Virol 27:28–37
    [Google Scholar]
  28. Payne L. G., Norrby E. 1976; Presence of haemagglutinin in the envelope of extracellular vaccinia virus particles. J Gen Virol 32:63–72 [CrossRef]
    [Google Scholar]
  29. Payne L. G., Norrby E. 1978; Adsorption and penetration of enveloped and naked vaccinia virus particles. J Virol 27:19–27
    [Google Scholar]
  30. Risco C., Rodríguez J. R., López-Iglesias C., Carrascosa J. L., Esteban M., Rodríguez D. 2002; Endoplasmic reticulum-Golgi intermediate compartment membranes and vimentin filaments participate in vaccinia virus assembly. J Virol 76:1839–1855 [CrossRef]
    [Google Scholar]
  31. Rodger G., Smith G. L. 2002; Replacing the SCR domains of vaccinia virus protein B5R with EGFP causes a reduction in plaque size and actin tail formation but enveloped virions are still transported to the cell surface. J Gen Virol 83:323–332
    [Google Scholar]
  32. Rodriguez J. F., Smith G. L. 1990; IPTG-dependent vaccinia virus: identification of a virus protein enabling virion envelopment by Golgi membrane and egress. Nucleic Acids Res 18:5347–5351 [CrossRef]
    [Google Scholar]
  33. Rodriguez J. F., Paez E., Esteban M. 1987; A 14,000- M r envelope protein of vaccinia virus is involved in cell fusion and forms covalently linked trimers. J Virol 61:395–404
    [Google Scholar]
  34. Senkevich T. G., Ward B. M., Moss B. 2004a; Vaccinia virus entry into cells is dependent on a virion surface protein encoded by the A28L gene. J Virol 78:2357–2366 [CrossRef]
    [Google Scholar]
  35. Senkevich T. G., Ward B. M., Moss B. 2004b; 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 78:2348–2356 [CrossRef]
    [Google Scholar]
  36. Smith G. L., Vanderplasschen A., Law M. 2002; The formation and function of extracellular enveloped vaccinia virus. J Gen Virol 83:2915–2931
    [Google Scholar]
  37. Sodeik B., Krijnse-Locker J. 2002; Assembly of vaccinia virus revisited: de novo membrane synthesis or acquisition from the host?. Trends Microbiol 10:15–24 [CrossRef]
    [Google Scholar]
  38. Sodeik B., Doms R. W., Ericsson M., Hiller G., Machamer C. E., van't Hof W., van Meer G., Moss B., Griffiths G. 1993; Assembly of vaccinia virus: role of the intermediate compartment between the endoplasmic reticulum and the Golgi stacks. J Cell Biol 121:521–541 [CrossRef]
    [Google Scholar]
  39. Vanderplasschen A., Smith G. L. 1997; A novel virus binding assay using confocal microscopy: demonstration that the intracellular and extracellular vaccinia virions bind to different cellular receptors. J Virol 71:4032–4041
    [Google Scholar]
  40. Vanderplasschen A., Hollinshead M., Smith G. L. 1998; Intracellular and extracellular vaccinia virions enter cells by different mechanisms. J Gen Virol 79:877–887
    [Google Scholar]
  41. Vázquez M.-I., Esteban M. 1999; Identification of functional domains in the 14-kilodalton envelope protein (A27L) of vaccinia virus. J Virol 73:9098–9109
    [Google Scholar]
  42. Vázquez M.-I., Rivas G., Cregut D., Serrano L., Esteban M. 1998; The vaccinia virus 14-kilodalton (A27L) fusion protein forms a triple coiled-coil structure and interacts with the 21-kilodalton (A17L) virus membrane protein through a C-terminal α -helix. J Virol 72:10126–10137
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.80831-0
Loading
/content/journal/jgv/10.1099/vir.0.80831-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed