1887

Journal of General Virology header logo

Volume 83, Issue 12

The latency-related gene of bovine herpesvirus-1 can inhibit the ability of bICP0 to activate productive infection Free

Abstract

Transfection of bovine cells with bovine herpesvirus-1 genomic DNA yields low levels of infectious virus. Cotransfection with the bICP0 gene enhances productive infection and virus yield because bICP0 can activate viral gene expression. Since the latency-related (LR) gene overlaps and is antisense to bICP0, the effects of LR gene products on productive infection were tested. The intact LR gene inhibited productive infection in a dose-dependent fashion but LR protein expression was not required. Further studies indicated that LR gene sequences near the 3’ terminus of the LR RNA are necessary for inhibiting productive infection. When cotransfected with the bICP0 gene, the LR gene inhibited bICP0 RNA and protein expression in transiently transfected cells. Taken together, these results suggest that abundant LR RNA expression in sensory neurons is one factor that has the potential to inhibit productive infection and consequently promote the establishment and maintenance of latency.

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

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-83-12-2965
2002-12-01
2024-04-25
Loading full text...

Full text loading...

/deliver/fulltext/jgv/83/12/0832965a.html?itemId=/content/journal/jgv/10.1099/0022-1317-83-12-2965&mimeType=html&fmt=ahah

References

  1. Ahmed M., Lock M., Miller C. G., Fraser N. W. 2002; Regions of the herpes simplex virus type 1 latency-associated transcript that protect cells from apoptosis in vitro and protect neuronal cells in vivo. Journal of Virology 76:717–729
     [Google Scholar]
  2. Bowland S. L., Shewen P. E. 2000; Bovine respiratory disease: commercial vaccines currently available in Canada. Canadian Veterninary Journal 41:33–48
     [Google Scholar]
  3. Bratanich A. C., Hanson N. D., Jones C. J. 1992; The latency-related gene of bovine herpesvirus 1 inhibits the activity of immediate-early transcription unit 1. Virology 191:988–991
     [Google Scholar]
  4. Bratty J., Chartrand P., Ferbeyre G., Cedergren R. 1993; The hammerhead RNA domain, a model ribozyme. Biochemica Biophysica Acta 1216:345–359
     [Google Scholar]
  5. Carter J. J., Weinberg A. D., Pollard A., Reeves R., Magnuson J. A., Magnuson N. S. 1989; Inhibition of T-lymphocyte mitogenic responses and effects on cell functions by bovine herpesvirus 1. Journal of Virology 63:1525–1530
     [Google Scholar]
  6. Ciacci-Zanella J., Stone M., Henderson G., Jones C. 1999; The latency-related gene of bovine herpesvirus 1 inhibits programmed cell death. Journal of Virology 73:9734–9740
     [Google Scholar]
  7. Clemens M. J., Elia A. 1997; The double-stranded RNA-dependent protein kinase PKR: structure and function. Journal of Interferon Cytokine Research 17:503–524
     [Google Scholar]
  8. Delhon G., Jones C. 1997; Identification of DNA sequences in the latency related promoter of bovine herpes virus type 1 which are bound by neuronal specific factors. Virus Research 51:93–103
     [Google Scholar]
  9. Devireddy L. R., Jones C. 1998; Alternative splicing of the latency-related transcript of bovine herpesvirus 1 yields RNAs containing unique open reading frames. Journal of Virology 72:7294–7301
     [Google Scholar]
  10. Griebel P. J., Qualtiere L., Davis W. C., Gee A., Bielefeldt D., Ohmann H., Lawman M. J., Babiuk L. A. 1987a; T lymphocyte population dynamics and function following a primary bovine herpesvirus type-1 infection. Viral Immunology 1:287–304
     [Google Scholar]
  11. Griebel P. J., Qualtiere L., Davis W. C., Lawman M. J., Babiuk L. A. 1987b; Bovine peripheral blood leukocyte subpopulation dynamics following a primary bovine herpesvirus-1 infection. Viral Immunology 1:267–286
     [Google Scholar]
  12. Griebel P. J., Ohmann H. B., Lawman M. J., Babiuk L. A. 1990; The interaction between bovine herpesvirus type 1 and activated bovine T lymphocytes. Journal of General Virology 71:369–377
     [Google Scholar]
  13. Hardwick J. M. 1998; Viral interference with apoptosis. Seminars in Cellular Developmental Biology 9:339–349
     [Google Scholar]
  14. Hariharan M. J., Nataraj C., Srikumaran S. 1993; Down regulation of murine MHC class I expression by bovine herpesvirus 1. Viral Immunology 6:273–284
     [Google Scholar]
  15. Hegde N. R., Lewin H. A., Duggan M. J., Stabel J. R., Srikumaran S. 1998; Development of a syngeneic bovine fibroblast cell line: implications for the study of bovine cytotoxic T lymphocytes. Viral Immunology 11:37–48
     [Google Scholar]
  16. Hinkley S., Hill A. B., Srikumaran S. 1998; Bovine herpesvirus-1 infection affects the peptide transport activity in bovine cells. Virus Research 53:91–96
     [Google Scholar]
  17. Hossain A., Schang L. M., Jones C. 1995; Identification of gene products encoded by the latency-related gene of bovine herpesvirus 1. Journal of Virology 69:5345–5352
     [Google Scholar]
  18. Hui E. K., Lo S. J. 1998; Does the latency associated transcript (LAT) of herpes simplex virus (HSV) function as a ribozyme during viral reactivation?. Virus Genes 16:147–148
     [Google Scholar]
  19. Inman M., Lovato L., Doster A., Jones C. 2001a; A mutation in the latency-related gene of bovine herpesvirus 1 leads to impaired ocular shedding in acutely infected calves. Journal of Virology 75:8507–8515
     [Google Scholar]
  20. Inman M., Perng G.-C., Henderson G., Ghiasi H., Nesburn A. B., Wechsler S. L., Jones C. 2001b; Region of herpes simplex virus type 1 latency-associated transcript sufficient for wild-type spontaneous reactivation promotes cell survival in tissue culture. Journal of Virology 75:3636–3646
     [Google Scholar]
  21. Inman M., Zhang Y., Geiser V., Jones C. 2001c; The zinc ring finger in the bICP0 protein encoded by bovine herpes virus-1 mediates toxicity and activates productive infection. Journal of General Virology 82:483–492
     [Google Scholar]
  22. Inman M., Lovato L., Doster A., Jones C. 2002; A mutation in the latency-related gene of bovine herpesvirus 1 distrupts the latency reactivation cycle in calves. Journal of Virology 76:6771–6779
     [Google Scholar]
  23. Jiang Y., Hossain A., Winkler M. T., Holt T., Doster A., Jones C. 1998; A protein encoded by the latency-related gene of bovine herpesvirus 1 is expressed in trigeminal ganglionic neurons of latently infected cattle and interacts with cyclin-dependent kinase 2 during productive infection. Journal of Virology 72:8133–8142
     [Google Scholar]
  24. Jones C. 1998; Alphaherpesvirus latency: its role in disease and survival of the virus in nature. Advances in Virus Research 51:81–133
     [Google Scholar]
  25. Jones C., Delhon G., Bratanich A., Kutish G., Rock D. 1990; Analysis of the transcriptional promoter which regulates the latency-related transcript of bovine herpesvirus 1. Journal of Virology 64:1164–1170
     [Google Scholar]
  26. Mador N., Goldenberg D., Cohen O., Panet A., Steiner I. 1998; Herpes simplex virus type 1 latency-associated transcripts suppress viral replication and reduce immediate-early gene mRNA levels in a neuronal cell line. Journal of Virology 72:5067–5075
     [Google Scholar]
  27. Maggioncalda J., Mehta A., Su Y. H., Fraser N. W., Block T. M. 1996; Correlation between herpes simplex virus type 1 rate of reactivation from latent infection and the number of infected neurons in trigeminal ganglia. Virology 225:72–81
     [Google Scholar]
  28. Nataraj C., Eidmann S., Hariharan M. J., Sur J. H., Perry G. A., Srikumaran S. 1997; Bovine herpesvirus 1 downregulates the expression of bovine MHC class I molecules. Viral Immunology 10:21–34
     [Google Scholar]
  29. Perng G.-C., Dunkel E. C., Geary P. A., Slanina S. M., Ghiasi H., Kaiwar R., Nesburn A. B., Wechsler S. L. 1994; The latency-associated transcript gene of herpes simplex virus type 1 (HSV-1) is required for efficient in vivo spontaneous reactivation of HSV-1 from latency. Journal of Virology 68:8045–8055
     [Google Scholar]
  30. Perng G.-C., Ghiasi H., Slanina S. M., Nesburn A. B., Wechsler S. L. 1996; The spontaneous reactivation function of the herpes simplex virus type 1 LAT gene resides completely within the first 1·5 kilobases of the 8·3-kilobase primary transcript. Journal of Virology 70:976–984
     [Google Scholar]
  31. Perng G.-C., Jones C., Ciacci-Zanella J., Stone M., Henderson G., Yukht A., Slanina S. M., Hofman F. M., Ghiasi H., Nesburn A. B., Wechsler S. L. 2000a; Virus-induced neuronal apoptosis blocked by the herpes simplex virus latency-associated transcript (LAT). Science 287:1500–1503
     [Google Scholar]
  32. Perng G.-C., Slanina S. M., Yukht A., Ghiasi H., Nesburn A. B., Wechsler S. L. 2000b; The latency-associated transcript gene enhances establishment of herpes simplex virus type 1 latency in rabbits. Journal of Virology 74:1885–1891
     [Google Scholar]
  33. Perng G.-C., Maguen B., Jin L., Mott K. R., Osorio N., Slanina S. M., Yukht A., Ghiasi H., Nesburn A. B., Inman M., Henderson G., Jones C., Wechsler S. L. 2002; A gene capable of blocking apoptosis can substitute for the herpes simplex virus type 1 latency-associated transcript gene and restore wild-type reactivation levels. Journal of Virology 76:1224–1235
     [Google Scholar]
  34. Player M. R., Torrence P. F. 1998; The 2-5A system: modulation of viral and cellular processes through acceleration of RNA degradation. Pharmacology Therapeutics 78:55–113
     [Google Scholar]
  35. Rock D. L., Beam S. L., Mayfield J. E. 1987; Mapping bovine herpesvirus type 1 latency-related RNA in trigeminal ganglia of latently infected rabbits. Journal of Virology 61:3827–3831
     [Google Scholar]
  36. Sawtell N. M. 1997; Comprehensive quantification of herpes simplex virus latency at the single-cell level. Journal of Virology 71:5423–5431
     [Google Scholar]
  37. Sawtell N. M., Thompson R. L. 1992; Herpes simplex virus type 1 latency-associated transcription unit promotes anatomical site-dependent establishment and reactivation from latency. Journal of Virology 66:2157–2169
     [Google Scholar]
  38. Schang L. M., Hossain A., Jones C. 1996; The latency-related gene of bovine herpesvirus 1 encodes a product which inhibits cell cycle progression. Journal of Virology 70:3807–3814
     [Google Scholar]
  39. Storz G. 2002; An expanding universe of noncoding RNAs. Science 296:1260–1263
     [Google Scholar]
  40. Thompson R. L., Sawtell N. M. 1997; The herpes simplex virus type 1 latency-associated transcript gene regulates the establishment of latency. Journal of Virology 71:5432–5440
     [Google Scholar]
  41. Thompson R. L., Sawtell N. M. 2001; Herpes simplex virus type 1 latency-associated transcript gene promotes neuronal survival. Journal of Virology 75:6660–6675
     [Google Scholar]
  42. Tikoo S. K., Campos M., Babiuk L. A. 1995; Bovine herpesvirus 1 (BHV-1): biology, pathogenesis, and control. Advances in Virus Research 45:191–223
     [Google Scholar]
  43. Wagner E. K., Bloom D. C. 1997; Experimental investigation of herpes simplex virus latency. Clinical Microbiology Reviews 10:419–443
     [Google Scholar]
  44. Winkler M. T., Doster A., Jones C. 1999; Bovine herpesvirus 1 can infect CD4+ T lymphocytes and induce programmed cell death during acute infection of cattle. Journal of Virology 73:8657–8668
     [Google Scholar]
  45. Winkler M. T., Doster A., Jones C. 2000; Persistence and reactivation of bovine herpesvirus 1 in the tonsils of latently infected calves. Journal of Virology 74:5337–5346
     [Google Scholar]
  46. Wirth U. V., Gunkel K., Engels M., Schwyzer M. 1989; Spatial and temporal distribution of bovine herpesvirus 1 transcripts. Journal of Virology 63:4882–4889
     [Google Scholar]
  47. Zhang Y., Jones C. 2001; The bovine herpesvirus 1 immediate-early protein (bICP0) associates with histone deacetylase 1 to activate transcription. Journal of Virology 75:9571–9578
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-83-12-2965
Loading
The latency-related gene of bovine herpesvirus-1 can inhibit the ability of bICP0 to activate productive infection
J. Gen. Virol. 83, 2965 (2002); https://doi.org/10.1099/0022-1317-83-12-2965
/content/journal/jgv/10.1099/0022-1317-83-12-2965
/content/journal/jgv/10.1099/0022-1317-83-12-2965
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