1887

Abstract

Infection of cattle or bovine cells with bovine herpesvirus 1 (BHV-1) leads to increased apoptosis. Previous studies indicated that BHV-1 infected cell protein 0 (bICP0), the major transcriptional regulatory protein of BHV-1, is toxic in transiently transfected cells. Point mutations within the zinc RING finger of bICP0 reduced toxicity and eliminated the ability of bICP0 to activate viral gene expression. In mouse neuroblastoma cells (neuro-2A) and bovine turbinate cells, bICP0 activated caspase 3, a key regulatory protein in the apoptotic pathway. A pro-apoptotic gene (Bax), but not bICP0, induced caspase 3 cleavage and activation by 8 h after transfection of neuro-2A cells. Conversely, bICP0 or the N-terminal 356 aa of bICP0 did not induce caspase 3 cleavage in neuro-2A cells until 30 h after transfection, suggesting that bICP0 stimulates caspase 3 cleavage by an indirect mechanism. These studies indicate that the toxic functions of bICP0 correlate with caspase 3 cleavage and activation.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.80371-0
2004-12-01
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/jgv/85/12/vir853511.html?itemId=/content/journal/jgv/10.1099/vir.0.80371-0&mimeType=html&fmt=ahah

References

  1. Aubert M., Blaho J. A. 2001; Modulation of apoptosis during herpes simplex virus infection in human cells. Microbes Infect 3:859–866 [CrossRef]
    [Google Scholar]
  2. Best S. M., Shelton J. F., Pompey M., Wolfinbarger J. B., Bloom M. E. 2003; Caspase cleavage of the nonstructural protein NS1 mediates replication of Aleutian mink disease parvovirus. J Virol 77:5305–5312 [CrossRef]
    [Google Scholar]
  3. Boutell C., Everett R. D. 2003; The herpes simplex virus type 1 (HSV-1) regulatory protein ICP0 interacts with and ubiquitinates p53. J Biol Chem 278:36596–36602 [CrossRef]
    [Google Scholar]
  4. Boutell C., Sadis S., Everett R. D. 2002; Herpes simplex virus type 1 immediate-early protein ICP0 and its isolated RING finger domain act as ubiquitin E3 ligases in vitro. J Virol 76:841–850 [CrossRef]
    [Google Scholar]
  5. Bowles D. E., Holden V. R., Zhao Y., O'Callaghan D. J. 1997; The ICP0 protein of equine herpesvirus 1 is an early protein that independently transactivates expression of all classes of viral promoters. J Virol 71:4904–4914
    [Google Scholar]
  6. Bowles D. E., Kim S. K., O'Callaghan D. J. 2000; Characterization of the trans-activation properties of equine herpesvirus 1 EICP0 protein. J Virol 74:1200–1208 [CrossRef]
    [Google Scholar]
  7. Devireddy L. R., Jones C. J. 1999; Activation of caspases and p53 by bovine herpesvirus 1 infection results in programmed cell death and efficient virus release. J Virol 73:3778–3788
    [Google Scholar]
  8. Everett R. D. 1988; Analysis of the functional domains of herpes simplex virus type 1 immediate-early polypeptide Vmw110. J Mol Biol 202:87–96 [CrossRef]
    [Google Scholar]
  9. Everett R. D. 2000; ICP0, a regulator of herpes simplex virus during lytic and latent infection. Bioessays 22:761–770 [CrossRef]
    [Google Scholar]
  10. Everett R. D., Barlow P., Milner A., Luisi B., Orr A., Hope G., Lyon D. 1993; A novel arrangement of zinc-binding residues and secondary structure in the C3HC4 motif of an alpha herpes virus protein family. J Mol Biol 234:1038–1047 [CrossRef]
    [Google Scholar]
  11. Everett R., O'Hare P., O'Rourke D., Barlow P., Orr A. 1995; Point mutations in the herpes simplex virus type 1 Vmw110 RING finger helix affect activation of gene expression, viral growth, and interaction with PML-containing nuclear structures. J Virol 69:7339–7344
    [Google Scholar]
  12. Everett R. D., Meredith M., Orr A., Cross A., Kathoria M., Parkinson J. 1997; . A novel ubiquitin-specific protease is dynamically associated with the PML nuclear domain and binds to a herpesvirus regulatory protein [corrected and republished article originally printed in EMBO J 16, 566–577 (1997)]. EMBO J 16:1519–1530 [CrossRef]
    [Google Scholar]
  13. Everett R. D., Earnshaw W. C., Findlay J., Lomonte P. 1999a; Specific destruction of kinetochore protein CENP-C and disruption of cell division by herpes simplex virus immediate-early protein Vmw110. EMBO J 18:1526–1538 [CrossRef]
    [Google Scholar]
  14. Everett R. D., Lomonte P., Sternsdorf T., van Driel R., Orr A. 1999b; Cell cycle regulation of PML modification and ND10 composition. J Cell Sci 112:4581–4588
    [Google Scholar]
  15. Fraefel C., Zeng J., Choffat Y., Engels M., Schwyzer M., Ackermann M. 1994; Identification and zinc dependence of the bovine herpesvirus 1 transactivator protein BICP0. J Virol 68:3154–3162
    [Google Scholar]
  16. Hobbs W. E. II, DeLuca N. A. 1999; Perturbation of cell cycle progression and cellular gene expression as a function of herpes simplex virus ICP0. J Virol 73:8245–8255
    [Google Scholar]
  17. Hunsperger E. A., Wilcox C. L. 2003; Caspase-3-dependent reactivation of latent herpes simplex virus type 1 in sensory neuronal cultures. J Neurovirol 9:390–398 [CrossRef]
    [Google Scholar]
  18. Inman M., Zhang Y., Geiser V., Jones C. 2001; The zinc ring finger in the bICP0 protein encoded by bovine herpes virus-1 mediates toxicity and activates productive infection. J Gen Virol 82:483–492
    [Google Scholar]
  19. Jones C. 1998; Alphaherpesvirus latency: its role in disease and survival of the virus in nature. Adv Virus Res 51:81–133
    [Google Scholar]
  20. Jones C. 2003; Herpes simplex virus type 1 and bovine herpesvirus 1 latency. Clin Microbiol Rev 16:79–95 [CrossRef]
    [Google Scholar]
  21. Koppel R., Fraefel C., Vogt B., Bello L. J., Lawrence W. C., Schwyzer M. 1996; Recombinant bovine herpesvirus-1 (BHV-1) lacking transactivator protein BICP0 entails lack of glycoprotein C and severely reduced infectivity. Biol Chem 377:787–795
    [Google Scholar]
  22. Koppel R., Vogt B., Schwyzer M. 1997; Immediate-early protein BICP22 of bovine herpesvirus 1 trans-represses viral promoters of different kinetic classes and is itself regulated by BICP0 at transcriptional and posttranscriptional levels. Arch Virol 142:2447–2464 [CrossRef]
    [Google Scholar]
  23. Kruegger A., Baumann S., Krammer P. H., Kirchhoff S. 2001; FLICE-inhibitory proteins: regulators of death receptor-mediated apoptosis. Mol Cell Biol 21:8247–8254 [CrossRef]
    [Google Scholar]
  24. Lium E. K., Silverstein S. 1997; Mutational analysis of the herpes simplex virus type 1 ICP0 C3HC4 zinc ring finger reveals a requirement for ICP0 in the expression of the essential α 27 gene. J Virol 71:8602–8614
    [Google Scholar]
  25. Lium E. K., Panagiotidis C. A., Wen X., Silverstein S. J. 1998; The NH2 terminus of the herpes simplex virus type 1 regulatory protein ICP0 contains a promoter-specific transcription activation domain. J Virol 72:7785–7795
    [Google Scholar]
  26. Lovato L., Inman M., Henderson G., Doster A., Jones C. 2003; Infection of cattle with a bovine herpesvirus 1 (BHV-1) strain that contains a mutation in the latency-related gene leads to increased apoptosis in trigeminal ganglia during the transition from acute infection to latency. J Virol 77:4848–4857 [CrossRef]
    [Google Scholar]
  27. Maul G. G., Everett R. D. 1994; The nuclear location of PML, a cellular member of the C3HC4 zinc-binding domain protein family, is rearranged during herpes simplex virus infection by the C3HC4 viral protein ICP0. J Gen Virol 75:1223–1233 [CrossRef]
    [Google Scholar]
  28. Maul G. G., Guldner H. H., Spivack J. G. 1993; Modification of discrete nuclear domains induced by herpes simplex virus type 1 immediate early gene 1 product (ICP0. J Gen Virol 74:2679–2690 [CrossRef]
    [Google Scholar]
  29. Nicholson D. W., Thornberry N. A. 1997; Caspases: killer proteases. Trends Biochem Sci 22:299–306 [CrossRef]
    [Google Scholar]
  30. Olmsted J. B., Carlson K., Klebe R., Ruddle F., Rosenbaum J. 1970; Isolation of microtubule protein from cultured mouse neuroblastoma cells. Proc Natl Acad Sci U S A 65:129–136 [CrossRef]
    [Google Scholar]
  31. Parkinson J., Everett R. D. 2000; Alphaherpesvirus proteins related to herpes simplex virus type 1 ICP0 affect cellular structures and proteins. J Virol 74:10006–10017 [CrossRef]
    [Google Scholar]
  32. Rock D. L., Beam S. L., Mayfield J. E. 1987a; Mapping bovine herpesvirus type 1 latency-related RNA in trigeminal ganglia of latently infected rabbits. J Virol 61:3827–3831
    [Google Scholar]
  33. Rock D. L., Nesburn A. B., Ghiasi H., Ong J., Lewis T. L., Lokensgard J. R., Wechsler S. L. 1987b; Detection of latency-related viral RNAs in trigeminal ganglia of rabbits latently infected with herpes simplex virus type 1. J Virol 61:3820–3826
    [Google Scholar]
  34. Schmitz I., Kirchhoff S., Krammer P. H. 2000; Regulation of death receptor-mediated apoptosis pathways. Int J Biochem Cell Biol 32:1123–1136 [CrossRef]
    [Google Scholar]
  35. Sperandio S., de Belle I., Bredesen D. E. 2000; An alternative, nonapoptotic form of programmed cell death. Proc Natl Acad Sci U S A 97:14376–14381 [CrossRef]
    [Google Scholar]
  36. Thornberry N. A., Rosen A., Nicholson D. W. 1997; Control of apoptosis by proteases. Adv Pharmacol 41:155–177
    [Google Scholar]
  37. Tikoo S. K., Campos M., Babiuk L. A. 1995; Bovine herpesvirus 1 (BHV-1): biology, pathogenesis, and control. Adv Virus Res 45:191–223
    [Google Scholar]
  38. Van Sant C., Hagglund R., Lopez P., Roizman B. 2001; The infected cell protein 0 of herpes simplex virus 1 dynamically interacts with proteasomes, binds and activates the cdc34 E2 ubiquitin-conjugating enzyme, and possesses in vitro E3 ubiquitin ligase activity. Proc Natl Acad Sci U S A 98:8815–8820 [CrossRef]
    [Google Scholar]
  39. Wang X. 2001; The expanding role of mitochondria in apoptosis. Genes Dev 15:2922–2933
    [Google Scholar]
  40. 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. J Virol 73:8657–8668
    [Google Scholar]
  41. Wirth U. V., Gunkel K., Engels M., Schwyzer M. 1989; Spatial and temporal distribution of bovine herpesvirus 1 transcripts. J Virol 63:4882–4889
    [Google Scholar]
  42. Wirth U. V., Vogt B., Schwyzer M. 1991; The three major immediate-early transcripts of bovine herpesvirus 1 arise from two divergent and spliced transcription units. J Virol 65:195–205
    [Google Scholar]
  43. Wirth U. V., Fraefel C., Vogt B., Vlcek C., Paces V., Schwyzer M. 1992; Immediate-early RNA 2.9 and early RNA 2.6 of bovine herpesvirus 1 are 3′ coterminal and encode a putative zinc finger transactivator protein. J Virol 66:2763–2772
    [Google Scholar]
  44. Wolf B. B., Green D. R. 1999; Suicidal tendencies: apoptotic cell death by caspase family proteinases. J Biol Chem 274:20049–20052 [CrossRef]
    [Google Scholar]
  45. Zhang Y., Jones C. 2001; The bovine herpesvirus 1 immediate-early protein (bICP0) associates with histone deacetylase 1 to activate transcription. J Virol 75:9571–9578 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.80371-0
Loading
/content/journal/jgv/10.1099/vir.0.80371-0
Loading

Data & Media loading...

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