1887

Journal of General Virology header logo

Volume 82, Issue 2

The UL14 protein of herpes simplex virus type 2 translocates the minor capsid protein VP26 and the DNA cleavage and packaging UL33 protein into the nucleus of coexpressing cells Free

Abstract

The herpes simplex virus type 2 (HSV-2) gene UL14 encodes a 32 kDa protein which is a minor component of the virion tegument and is expressed late in infection. The UL14 protein shows varied localization patterns in HSV-2-infected and singly expressing cells, suggesting the possibility that it is multifunctional. We have investigated the influence of the UL14 protein on the intracellular localization of capsid proteins and DNA cleavage and packaging proteins in coexpressing cells. VP26 is the minor capsid protein; it binds to hexons of the outer capsid shell and is predominantly cytoplasmic upon sole expression. We have found that VP26 coexpressed with the UL14 protein showed mutual and predominant relocation into the nucleus. At least seven viral genes encode proteins (UL6, UL15, UL17, UL25, UL28, UL32 and UL33) that are required for DNA cleavage and packaging. We have found that the UL33 protein, which was also cytoplasmic by sole expression, was relocated to the nucleus upon expression with the UL14 protein, which again seemed to be a result of mutual influence. Coexpression experiments also suggested the possibility of a mutual influence between the UL14 and UL17 proteins, and the UL17 protein and VP26. Our results suggest that the UL14 protein can influence the intracellular localization patterns of a number of proteins belonging to the capsid or the DNA encapsidation machinery.

  • Received:
  • Accepted:
  • Published Online:
© Microbiology Society
Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-82-2-321
2001-02-01
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/jgv/82/2/0820321a.html?itemId=/content/journal/jgv/10.1099/0022-1317-82-2-321&mimeType=html&fmt=ahah

References

  1. Ali M. A., Forghani B., Cantin E. M. 1996; Characterization of an essential HSV-1 protein encoded by the UL25 gene reported to be involved in virus penetration and capsid assembly. Virology 216:278–283
     [Google Scholar]
  2. al-Kobaisi M. F., Rixon F. J., McDougall I., Preston V. G. 1991; The herpes simplex virus UL33 gene product is required for the assembly of full capsids. Virology 180:380–388
     [Google Scholar]
  3. Baer R., Bankier A. T., Biggin M. D., Deininger P. L., Farrell P. J., Gibson T. J., Hatfull G., Hudson G. S., Satchwell S. C., Seguin C. others 1984; DNA sequence and expression of the B95-8 Epstein–Barr virus genome. Nature 310:207–211
     [Google Scholar]
  4. Baines J. D., Cunningham C., Nalwanga D., Davison A. 1997; The U(L)15 gene of herpes simplex virus type 1 contains within its second exon a novel open reading frame that is translated in frame with the U(L)15 gene product. Journal of Virology 71:2666–2673
     [Google Scholar]
  5. Chee M. S., Bankier A. T., Beck S., Bohni R., Brown C. M., Cerny R., Horsnell T., Hutchison C. A. III, Kouzarides T., Martignetti J. A. others 1990; Analysis of the protein-coding content of the sequence of human cytomegalovirus strain AD169. Current Topics in Microbiology and Immunology 154:125–169
     [Google Scholar]
  6. Cunningham C., Davison A. J., MacLean A. R., Taus N. S., Baines J. D. 2000; Herpes simplex virus type 1 gene UL14: phenotype of a null mutant and identification of the encoded protein. Journal of Virology 74:33–41
     [Google Scholar]
  7. Daikoku T., Shibata S., Goshima F., Oshima S., Tsurumi T., Yamada H., Yamashita Y., Nishiyama Y. 1997; Purification and characterization of the protein kinase encoded by the UL13 gene of herpes simplex virus type 2. Virology 235:82–93
     [Google Scholar]
  8. Desai P., DeLuca N. A., Person S. 1998; Herpes simplex virus type 1 VP26 is not essential for replication in cell culture but influences production of infectious virus in the nervous system of infected mice. Virology 247:115–124
     [Google Scholar]
  9. Dolan A., Jamieson F. E., Cunningham C., Barnett B. C., McGeoch D. J. 1998; The genome sequence of herpes simplex virus type 2. Journal of Virology 72:2010–2021
     [Google Scholar]
  10. Gibson W., Roizman B. 1972; Proteins specified by herpes simplex virus 8. Characterization and composition of multiple capsid forms of subtypes 1 and 2. Journal of Virology 10:1044–1052
     [Google Scholar]
  11. Gompels U. A., Nicholas J., Lawrence G., Jones M., Thomson B. J., Martin M. E., Efstathiou S., Craxton M., Macaulay H. A. 1995; The DNA sequence of human herpesvirus-6: structure, coding content, and genome evolution. Virology 209:29–51
     [Google Scholar]
  12. Goshima F., Watanabe D., Takakuwa H., Wada K., Daikoku T., Yamada M., Nishiyama Y. 2000; Herpes simplex virus UL17 protein is associated with B capsids and colocalizes with ICP35 and VP5 in infected cells. Archives of Virology 145:1–10
     [Google Scholar]
  13. Lamberti C., Weller S. K. 1996; The herpes simplex virus type 1 UL6 protein is essential for cleavage and packaging but not for genomic inversion. Virology 226:403–407
     [Google Scholar]
  14. Lamberti C., Weller S. K. 1998; The herpes simplex virus type 1 cleavage/packaging protein, UL32, is involved in efficient localization of capsids to replication compartments. Journal of Virology 72:2463–2473
     [Google Scholar]
  15. 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. Journal of General Virology 69:1531–1574
     [Google Scholar]
  16. McNab A. R., Desai P., Person S., Roof L. L., Thomse D. R., Newcomb W. W., Brown J. C., Homa F. L. 1998; The product of the herpes simplex virus type 1 UL25 gene is required for encapsidation but not for cleavage of replicated viral DNA. Journal of Virology 72:1060–1070
     [Google Scholar]
  17. Nicholson P., Addison C., Cross A. M., Kennard J., Preston V. G., Rixon F. J. 1994; Localization of the herpes simplex virus type 1 major capsid protein VP5 to the cell nucleus requires the abundant scaffolding protein VP22a. Journal of General Virology 75:1091–1099
     [Google Scholar]
  18. Patel A. H., MacLean J. B. 1995; The product of the UL6 gene of herpes simplex virus type 1 is associated with virus capsids. Virology 206:465–478
     [Google Scholar]
  19. Patel A. H., Rixon F. J., Cunningham C., Davison A. J. 1996; Isolation and characterization of herpes simplex virus type 1 mutants defective in the UL6 gene. Virology 217:111–123
     [Google Scholar]
  20. Perdue M. L., Cohen J. C., Randall C. C., O’Callaghan D. J. 1976; Biochemical studies of the maturation of herpesvirus nucleocapsid species. Virology 74:194–208
     [Google Scholar]
  21. Rixon F. J., Addison C., McGregor A., Macnab S. J., Nicholson P., Preston V. G., Tatman J. D. 1996; Multiple interactions control the intracellular localization of the herpes simplex virus type 1 capsid proteins. Journal of General Virology 77:2251–2260
     [Google Scholar]
  22. Roizman B. 1996; The function of herpes simplex virus genes: a primer for genetic engineering of novel vectors. Proceedings of the National Academy of Sciences, USA 93:11307–11312
     [Google Scholar]
  23. Roizman B., Sears A. E. 1996; Herpes simplex virus and their replication. In Fields Virology pp 1043–1107 Edited by Fields B. N., Knipe D. M., Howley P. M. Philadelphia: Lippincott–Raven;
     [Google Scholar]
  24. Salmon B., Baines J. D. 1998; Herpes simplex virus DNA cleavage and packaging: association of multiple forms of U(L)15-encoded proteins with B capsids requires at least the U(L)6, U(L)17, and U(L)28 genes. Journal of Virology 72:3045–3050
     [Google Scholar]
  25. Salmon B., Cunningham C., Davison A. J., Harris W. J., Baines J. D. 1998; The herpes simplex virus type 1 U(L)17 gene encodes virion tegument proteins that are required for cleavage and packaging of viral DNA. Journal of Virology 72:3779–3788
     [Google Scholar]
  26. Steven A. C., Spear P. G. 1997; Herpesvirus capsid assembly and envelopment. In Structural Biology of Viruses pp 312–351 Edited by Chiu W., Burnett R. M., Garcea R. New York: Oxford University Press;
     [Google Scholar]
  27. Tatman J. D., Preston V. G., Nicholson P., Elliott R. M., Rixon F. J. 1994; Assembly of herpes simplex virus type 1 capsids using a panel of recombinant baculoviruses. Journal of General Virology 75:1101–1113
     [Google Scholar]
  28. Taus N. S., Salmon B., Baines J. D. 1998; The herpes simplex virus 1 UL 17 gene is required for localization of capsids and major and minor capsid proteins to intranuclear sites where viral DNA is cleaved and packaged. Virology 252:115–125
     [Google Scholar]
  29. Tengelsen L. A., Pederson N. E., Shaver P. R., Wathen M. W., Homa F. L. 1993; Herpes simplex virus type 1 DNA cleavage and encapsidation require the product of the UL28 gene: isolation and characterization of two UL28 deletion mutants. Journal of Virology 67:3470–3480
     [Google Scholar]
  30. Thomsen D. R., Roof L. L., Homa F. L. 1995; Assembly of the herpes simplex virus capsid: requirement for the carboxyl-terminal twenty-five amino acids of the proteins encoded by the UL26 and UL26.5 genes. Journal of Virology 69:3690–3703
     [Google Scholar]
  31. Wada K., Goshima F., Takakuwa H., Yamada H., Daikoku T., Nishiyama Y. 1999; Identification and characterization of the UL14 gene product of herpes simplex virus type 2. Journal of General Virology 80:2423–2431
     [Google Scholar]
  32. Wingfield P. T., Stahl S. J., Thomsen D. R., Homa F. L., Booy F. P., Trus B. L., Steven A. C. 1997; Hexon-only binding of VP26 reflects differences between the hexon and penton conformations of VP5, the major capsid protein of herpes simplex virus. Journal of Virology 71:8955–8961
     [Google Scholar]
  33. Yu D., Sheaffer A. K., Tenney D. J., Weller S. K. 1997; Characterization of ICP6: lacZ insertion mutants of the UL15 gene of herpes simplex virus type 1 reveals the translation of two proteins. Journal of Virology 71:2656–2665
     [Google Scholar]
  34. 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. Journal of Virology 73:3210–3218
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-82-2-321
Loading
The UL14 protein of herpes simplex virus type 2 translocates the minor capsid protein VP26 and the DNA cleavage and packaging UL33 protein into the nucleus of coexpressing cells
J. Gen. Virol. 82, 321 (2001); https://doi.org/10.1099/0022-1317-82-2-321
/content/journal/jgv/10.1099/0022-1317-82-2-321
/content/journal/jgv/10.1099/0022-1317-82-2-321
Loading

Data & Media loading...

Most cited Most Cited RSS feed

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