1887

Abstract

In the absence of the tegument protein pUL37, virion formation of pseudorabies virus (PrV) and herpes simplex virus type 1 (HSV-1) is severely impaired. Non-enveloped nucleocapsids accumulate in clusters in the cytoplasm, whereas only a few enveloped particles can be detected. Although a contribution of pUL37 to nuclear egress of HSV-1 has been suggested, the nuclear stages of morphogenesis are not impaired in PrV-ΔUL37-infected cells. Moreover, HSV-1 pUL37 has been described as essential for replication, whereas PrV is able to replicate productively without pUL37, although to lower titres than wild-type virus. Thus, there may be functional differences between the respective pUL37 proteins. This study compared the phenotypes of UL37-deleted PrV and HSV-1 in parallel assays, using a novel pUL37 deletion mutant of HSV-1 strain KOS, HSV-1ΔUL37[86–1035]. Aggregates of seemingly ‘naked’ nucleocapsids were present in the cytoplasm of African green monkey (Vero) or rabbit kidney (RK13) cells infected with HSV-1ΔUL37[86–1035] or PrV-ΔUL37. Nuclear retention of nucleocapsids was not observed in either virus. However, in contrast to PrV-ΔUL37, HSV-1ΔUL37[86–1035] was unable to replicate productively in, and to form plaques on, either Vero or RK13 cells. -complementation of respective deletion mutants with the heterologous pUL37 did not ensue. These data demonstrate that the conserved pUL37 in HSV-1 and PrV have similar but distinct functions.

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2009-07-01
2020-03-28
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References

  1. Brack A. R., Dijkstra J. M., Granzow H., Klupp B. G., Mettenleiter T. C. 1999; Inhibition of virion maturation by simultaneous deletion of glycoproteins E, I, and M of pseudorabies virus. J Virol 73:5364–5372
    [Google Scholar]
  2. Chen D. H., Jiang H., Lee J., Liu F. Y., Zhou Z. H. 1999; Three-dimensional visualization of tegument/capsid interactions in the intact human cytomegalovirus. Virology 260:10–16 [CrossRef]
    [Google Scholar]
  3. Coller K. E., Lee J. I. H., Ueda A., Smith G. A. 2007; The capsid and tegument of the alphaherpesviruses are linked by an interaction between the UL25 and VP1/2 proteins. J Virol 81:11790–11797 [CrossRef]
    [Google Scholar]
  4. Desai P. J. 2000; A null mutation in the UL36 gene of herpes simplex virus type 1 results in accumulation of unenveloped DNA-filled capsids in the cytoplasm of infected cells. J Virol 74:11608–11618 [CrossRef]
    [Google Scholar]
  5. Desai P., Sexton G. L., McCaffery J. M., Person S. 2001; A null mutation in the gene encoding the herpes simplex virus type 1 UL37 polypeptide abrogates virus maturation. J Virol 75:10259–10271 [CrossRef]
    [Google Scholar]
  6. Farnsworth A., Goldsmith K., Johnson D. C. 2003; Herpes simplex virus glycoproteins gD and gE/gI serve essential but redundant functions during acquisition of the virion envelope in the cytoplasm. J Virol 77:8481–8494 [CrossRef]
    [Google Scholar]
  7. Farnsworth A., Wisner T. W., Johnson D. C. 2007; Cytoplasmic residues of herpes simplex virus glycoprotein gE required for secondary envelopment and binding of tegument proteins VP22 and UL11 to gE and gD. J Virol 81:319–331 [CrossRef]
    [Google Scholar]
  8. Fuchs W., Klupp B. G., Granzow H., Osterrieder N., Mettenleiter T. C. 2002a; The interacting UL31 and UL34 gene products of pseudorabies virus are involved in egress from the host-cell nucleus and represent components of primary enveloped but not mature virions. J Virol 76:364–378 [CrossRef]
    [Google Scholar]
  9. Fuchs W., Granzow H., Klupp B. G., Kopp M., Mettenleiter T. C. 2002b; The UL48 tegument protein of pseudorabies virus is critical for intracytoplasmic assembly of infectious virions. J Virol 76:6729–6742 [CrossRef]
    [Google Scholar]
  10. Fuchs W., Klupp B. G., Granzow H., Hengartner C., Brack A., Mundt A., Enquist L. W., Mettenleiter T. C. 2002c; Physical interaction between envelope glycoproteins E and M of pseudorabies virus and the major tegument protein UL49. J Virol 76:8208–8217 [CrossRef]
    [Google Scholar]
  11. Fuchs W., Klupp B. G., Granzow H., Mettenleiter T. C. 2004; Essential function of the pseudorabies virus UL36 gene product is independent of its interaction with the UL37 protein. J Virol 78:11879–11889 [CrossRef]
    [Google Scholar]
  12. Granzow H., Klupp B. G., Mettenleiter T. C. 2004; The pseudorabies virus US3 protein is a component of primary and of mature virions. J Virol 78:1314–1323 [CrossRef]
    [Google Scholar]
  13. Kaplan A. S., Vatter A. E. 1959; A comparison of herpes simplex and pseudorabies viruses. Virology 7:394–407 [CrossRef]
    [Google Scholar]
  14. Klupp B. G., Granzow H., Mundt E., Mettenleiter T. C. 2001; Pseudorabies virus UL37 gene product is involved in secondary envelopment. J Virol 75:8927–8936 [CrossRef]
    [Google Scholar]
  15. Klupp B. G., Fuchs W., Granzow H., Nixdorf R., Mettenleiter T. C. 2002; Pseudorabies virus UL36 tegument protein physically interacts with the UL37 protein. J Virol 76:3065–3071 [CrossRef]
    [Google Scholar]
  16. Kopp M., Granzow H., Fuchs W., Klupp B. G., Mettenleiter T. C. 2004; Simultaneous deletion of pseudorabies virus tegument protein UL11 and glycoprotein M severely impairs secondary envelopment. J Virol 78:3024–3034 [CrossRef]
    [Google Scholar]
  17. Krautwald M., Fuchs W., Klupp B. G., Mettenleiter T. C. 2009; Translocation of incoming pseudorabies virus capsids to the cell nucleus is delayed in the absence of tegument protein pUL37. J Virol 83:3389–3396 [CrossRef]
    [Google Scholar]
  18. Kuhn J., Leege T., Klupp B. G., Granzow H., Fuchs W., Mettenleiter T. C. 2008; Partial functional complementation of a pseudorabies virus UL25 deletion mutant by herpes simplex virus type 1 pUL25 indicates overlapping functions of alphaherpesvirus pUL25 proteins. J Virol 82:5725–5734 [CrossRef]
    [Google Scholar]
  19. Lake C. M., Hutt-Fletcher L. M. 2004; The Epstein–Barr virus BFRF1 and BFLF2 proteins interact and coexpression alters their cellular localization. Virology 320:99–106 [CrossRef]
    [Google Scholar]
  20. Leege T., Fuchs W., Granzow H., Kopp M., Klupp B. G., Mettenleiter T. C. 2009; Effects of simultaneous deletion of pUL11 and glycoprotein M on virion maturation of herpes simplex virus type 1. J Virol 83:896–907 [CrossRef]
    [Google Scholar]
  21. McGeoch D. J., Dalrymple M. A., Davison A. J., Dolan A., Frame M. C., McNab D., Perry L. J., Scott J. E., Taylor P. 1988; The complete DNA sequence of the long unique region in the genome of herpes simplex virus type 1. J Gen Virol 69:1531–1574 [CrossRef]
    [Google Scholar]
  22. McNabb D. S., Courtney R. J. 1992; Analysis of the UL36 open reading frame encoding the large tegument protein (ICP1/2) of herpes simplex virus type-1. J Virol 66:7581–7584
    [Google Scholar]
  23. Mettenleiter T. C. 2002; Herpesvirus assembly and egress. J Virol 76:1537–1547 [CrossRef]
    [Google Scholar]
  24. Mettenleiter T. C. 2006; Intriguing interplay between viral proteins during herpesvirus assembly or: the herpesvirus assembly puzzle. Vet Microbiol 113:163–169 [CrossRef]
    [Google Scholar]
  25. Mettenleiter T. C., Klupp B. G., Granzow H. 2006; Herpesvirus assembly: a tale of two membranes. Curr Opin Microbiol 9:423–429 [CrossRef]
    [Google Scholar]
  26. Nixdorf R., Klupp B. G., Karger A., Mettenleiter T. C. 2000; Effects of truncation of the carboxy terminus of pseudorabies virus glycoprotein B on infectivity. J Virol 74:7137–7145 [CrossRef]
    [Google Scholar]
  27. Reynolds A. E., Wills E. G., Roller R. J., Ryckman B. J., Baines J. D. 2002; Ultrastructural localization of the herpes simplex virus type 1 UL31, UL34, and US3 proteins suggests specific roles in primary envelopment and egress of nucleocapsids. J Virol 76:8939–8952 [CrossRef]
    [Google Scholar]
  28. Roberts A. P., Abaitua F., O'Hare P., McNab D., Rixon F. J., Pasdeloup D. 2009; Differing roles of inner tegument proteins pUL36 and pUL37 during entry of herpes simplex virus type 1. J Virol 83:105–116 [CrossRef]
    [Google Scholar]
  29. Sanchez V., Spector D. H. 2002; Virology: CMV makes a timely exit. Science 297:778–779 [CrossRef]
    [Google Scholar]
  30. Vittone V., Diefenbach E., Triffett D., Douglas M. W., Cunningham A. L., Diefenbach R. J. 2005; Determination of interactions between tegument proteins of herpes simplex virus type 1. J Virol 79:9566–9571 [CrossRef]
    [Google Scholar]
  31. Xia D., Srinivas S., Sato H., Pesnicak L., Straus S. E., Cohen J. I. 2003; Varicella-zoster virus open reading frame 21, which is expressed during latency, is essential for virus replication but dispensable for establishment of latency. J Virol 77:1211–1218 [CrossRef]
    [Google Scholar]
  32. Zhou Z. H., Chen D. H., Jakana J., Rixon F. J., Chiu W. 1999; Visualization of tegument–capsid interactions and DNA in intact herpes simplex virus type 1 virions. J Virol 73:3210–3218
    [Google Scholar]
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