1887

Abstract

Identifying cellular genes that promote bovine herpesvirus-1 (BHV-1) productive infection is important, as BHV-1 is a significant bovine pathogen. Previous studies demonstrated that BHV-1 DNA is not very infectious unless cotransfected with a plasmid expressing bICP0, a viral protein that stimulates expression of all classes of viral promoters. Based on these and other studies, we hypothesize that the ability of bICP0 to interact with and modify the function of cellular proteins stimulates virus transcription. If this prediction is correct, cellular proteins that activate virus transcription could, in part, substitute for bICP0 functions. The adenovirus E1A gene and bICP0 encode proteins that are potent activators of viral gene expression, they do not specifically bind DNA and both proteins interact with chromatin-remodelling enzymes. Because of these functional similarities, E1A was tested initially to see if it could stimulate BHV-1 productive infection. E1A consistently stimulates BHV-1 productive infection, but not as efficiently as bICP0. The ability of E1A to bind Rb family members plays a role in stimulating productive infection, suggesting that E2F family members activate productive infection. E2F-4, but not E2F-1, E2F-2 or E2F-5, activates productive infection with similar efficiency as E1A. Next, E2F family members were examined for their ability to activate the BHV-1 immediate-early (IE) transcription unit 1 (IEtu1) promoter, as it regulates IE expression of bICP0 and bICP4. E2F-1 and E2F-2 strongly activate the IEtu1 promoter, but not a BHV-1 IEtu2 promoter or a herpes simplex virus type 1 ICP0 promoter construct. These studies suggest that E2F family members can stimulate BHV-1 productive infection.

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2003-04-01
2024-11-09
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References

  1. Advani S. J., Weichselbaum R. R., Roizman B. 2000; E2F proteins are posttranslationally modified concomitantly with a reduction in nuclear binding activity in cells infected with herpes simplex virus 1. J Virol 74:7842–7850
    [Google Scholar]
  2. Allen K. E., de la Luna S., Kerkhoven R. M., Bernards R., La Thangue N. B. 1997; Distinct mechanisms of nuclear accumulation regulate the functional consequence of E2F transcription factors. J Cell Sci 110:2819–2831
    [Google Scholar]
  3. Ambrosino C., Palmieri C., Puca A. 9 other authors 2002; Physical and functional interaction of HIV tat with E2F-4, a transcriptional regulator of mammalian cell cycle. J Biol Chem 272:31448–31458
    [Google Scholar]
  4. Blaho M., Aubert J. A. 2001; Modulation of apoptosis during herpes simplex virus infection in human cells. Microbes Infect 3:1–8
    [Google Scholar]
  5. Bowland S. L., Shewen P. E. 2000; Bovine respiratory disease: commercial vaccines currently available in Canada. Can Vet J 41:33–48
    [Google Scholar]
  6. 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]
  7. 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
    [Google Scholar]
  8. Cai W., Schaffer P. A. 1991; A cellular function can enhance gene expression and plating efficiency of a mutant defective in the gene for ICP0, a transactivating protein of herpes simplex virus type 1. J Virol 65:4078–4090
    [Google Scholar]
  9. 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. J Virol 63:1525–1530
    [Google Scholar]
  10. Chang Y. C., Nakajima H., Illenye S. 10 other authors 2000; Caspase-dependent apoptosis by ectopic expression of E2F-4. Oncogene 19:4713–4720
    [Google Scholar]
  11. Daksis J. I., Preston C. M. 1992; Herpes simplex virus immediate early gene expression in the absence of transinduction by Vmw65 varies during the cell cycle. Virology 189:196–202
    [Google Scholar]
  12. Dallas P. B., Pacchione S., Wilsker D., Bowrin V., Kobayashi R., Moran E. 2000; The human SWI–SNF complex protein p270 is an ARID family member with non-sequence-specific DNA binding activity. Mol Cell Biol 20:3137–3146
    [Google Scholar]
  13. DeGregori J., Kowalik T., Nevins J. R. 1995; Cellular targets for activation by the E2F1 transcription factor include DNA synthesis- and G1/S-regulatory genes. Mol Cell Biol 15:4215–4224
    [Google Scholar]
  14. 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 Res 51:93–103
    [Google Scholar]
  15. Devireddy L. R., Jones C. J. 2000; Olf-1, a neuron-specific transcription factor, can activate the herpes simplex virus type 1-infected cell protein 0 promoter. J Biol Chem 275:77–81
    [Google Scholar]
  16. Ehmann G. L., Burnett H. A., Bachenheimer S. L. 2001; Pocket protein p130/Rb2 is required for efficient herpes simplex virus type 1 gene expression and viral replication. J Virol 75:7149–7160
    [Google Scholar]
  17. 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
    [Google Scholar]
  18. Everett R. D. 2000; ICP0, a regulator of herpes simplex virus during lytic and latent infection. Bioessays 22:761–770
    [Google Scholar]
  19. 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
    [Google Scholar]
  20. 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]
  21. 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. EMBO J 16:1519–1530
    [Google Scholar]
  22. 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
    [Google Scholar]
  23. 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]
  24. Flemington E. K. 2001; Herpesvirus lytic replication and the cell cycle: arresting new developments. J Virol 75:4475–4881
    [Google Scholar]
  25. 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]
  26. Geiser V., Inman M., Zhang Y., Jones C. 2002; The latency-related gene of bovine herpesvirus-1 can inhibit the ability of bICP0 to activate productive infection. J Gen Virol 83:2965–2971
    [Google Scholar]
  27. Griebel P. J., Qualtiere L., Davis W. C., Gee A., Bielefeldt Ohmann H., Lawman M. J., Babiuk L. A. 1987a; T lymphocyte population dynamics and function following a primary bovine herpesvirus type-1 infection. Viral Immunol 1:287–304
    [Google Scholar]
  28. 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 Immunol 1:267–286
    [Google Scholar]
  29. 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. J Gen Virol 71:369–377
    [Google Scholar]
  30. Harbour J. W., Dean D. C. 2000; The Rb/E2F pathway: expanding roles and emerging paradigms. Genes Dev 14:2393–2409
    [Google Scholar]
  31. Hariharan M. J., Nataraj C., Srikumaran S. 1993; Down regulation of murine MHC class I expression by bovine herpesvirus 1. Viral Immunol 6:273–284
    [Google Scholar]
  32. Helin K., Lees J. A., Vidal M., Dyson N., Harlow E., Fattaey A. 1992; A cDNA encoding a pRB-binding protein with properties of the transcription factor E2F. Cell 70:337–350
    [Google Scholar]
  33. Helin K., Wu C. L., Fattaey A. R., Lees J. A., Dynlacht B. D., Ngwu C., Harlow E. 1993; Heterodimerization of the transcription factors E2F-1 and DP-1 leads to cooperative trans-activation. Genes Dev 7:1850–1861
    [Google Scholar]
  34. Hilton M. J., Mounghane D., McLean T., Contractor N. V., O'Neil J., Carpenter K., Bachenheimer S. L. 1995; Induction by herpes simplex virus of free and heteromeric forms of E2F transcription factor. Virology 213:624–638
    [Google Scholar]
  35. Hinkley S., Hill A. B., Srikumaran S. 1998; Bovine herpesvirus-1 infection affects the peptide transport activity in bovine cells. Virus Res 53:91–96
    [Google Scholar]
  36. 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]
  37. 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. J Virol 75:8507–8515
    [Google Scholar]
  38. Inman M., Zhang Y., Geiser V., Jones C. 2001b; The zinc ring finger in the bICP0 protein encoded by bovine herpesvirus-1 mediates toxicity and activates productive infection. J Gen Virol 82:483–492
    [Google Scholar]
  39. Inman M., Lovato L., Doster A., Jones C. 2002; A mutation in the latency-related gene of bovine herpesvirus 1 disrupts the latency reactivation cycle in calves. J Virol 76:6771–6779
    [Google Scholar]
  40. Jones C. 1998; Alphaherpesvirus latency: its role in disease and survival of the virus in nature. Adv Virus Res 51:81–133
    [Google Scholar]
  41. Jones C., Newby T. J., Holt T., Doster A., Stone M., Ciacci-Zanella J., Webster C. J., Jackwood M. W. 2000; Analysis of latency in cattle after inoculation with a temperature sensitive mutant of bovine herpesvirus 1 (RLB106). Vaccine 18:3185–3195
    [Google Scholar]
  42. Kaelin W. G. Jr, Krek W., Sellers W. R. other authors 1992; Expression cloning of a cDNA encoding a retinoblastoma-binding protein with E2F-like properties. Cell 70:351–364
    [Google Scholar]
  43. Kawaguchi Y., Bruni R., Roizman B. 1997a; Interaction of herpes simplex virus 1 α regulatory protein ICP0 with elongation factor 1δ: ICP0 affects translational machinery. J Virol 71:1019–1024
    [Google Scholar]
  44. Kawaguchi Y., Van Sant C., Roizman B. 1997b; Herpes simplex virus 1 α regulatory protein ICP0 interacts with and stabilizes the cell cycle regulator cyclin D3. J Virol 71:7328–7336
    [Google Scholar]
  45. 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]
  46. 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
    [Google Scholar]
  47. Lees-Miller S. P., Long M. C., Kilvert M. A., Lam V., Rice S. A., Spencer C. A. 1996; Attenuation of DNA-dependent protein kinase activity and its catalytic subunit by the herpes simplex virus type 1 transactivator ICP0. J Virol 70:7471–7477
    [Google Scholar]
  48. 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 α27 gene. J Virol 71:8602–8614
    [Google Scholar]
  49. 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]
  50. 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
    [Google Scholar]
  51. 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
    [Google Scholar]
  52. Misra V., Bratanich A. C., Carpenter D., O'Hare P. 1994; Protein and DNA elements involved in transactivation of the promoter of the bovine herpesvirus (BHV) 1 IE-1 transcription unit by the BHV α gene trans-inducing factor. J Virol 68:4898–4909
    [Google Scholar]
  53. Misra V., Walker S., Hayes S., O'Hare P. 1995; The bovine herpesvirus α gene trans-inducing factor activates transcription by mechanisms different from those of its herpes simplex virus type 1 counterpart VP16. J Virol 69:5209–5216
    [Google Scholar]
  54. 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 Immunol 10:21–34
    [Google Scholar]
  55. Nevins J. R., DeGregori J., Jakoi L., Leone G. 1997; Functional analysis of E2F transcription factor. Methods Enzymol 283:205–219
    [Google Scholar]
  56. Ohtani K., DeGregori J., Nevins J. R. 1995; Regulation of the cyclin E gene by transcription factor E2F1. Proc Natl Acad Sci U S A 92:12146–12150
    [Google Scholar]
  57. Olgiate J., Ehmann G. L., Vidyarthi S., Hilton M. J., Bachenheimer S. L. 1999; Herpes simplex virus induces intracellular redistribution of E2F4 and accumulation of E2F pocket protein complexes. Virology 258:257–270
    [Google Scholar]
  58. 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
    [Google Scholar]
  59. Parkinson J., Lees-Miller S. P., Everett R. D. 1999; Herpes simplex virus type 1 immediate-early protein vmw110 induces the proteasome-dependent degradation of the catalytic subunit of DNA-dependent protein kinase. J Virol 73:650–657
    [Google Scholar]
  60. Schang L. M., Phillips J., Schaffer P. A. 1998; Requirement for cellular cyclin-dependent kinases in herpes simplex virus replication and transcription. J Virol 72:5626–5637
    [Google Scholar]
  61. Schang L. M., Rosenberg A., Schaffer P. A. 1999; Transcription of herpes simplex virus immediate-early and early genes is inhibited by roscovitine, an inhibitor specific for cellular cyclin-dependent kinases. J Virol 73:2161–2172
    [Google Scholar]
  62. Schulze A., Zerfass K., Spitkovsky D., Middendorp S., Berges J., Helin K., Jansen-Durr P., Henglein B. 1995; Cell cycle regulation of the cyclin A gene promoter is mediated by a variant E2F site. Proc Natl Acad Sci U S A 92:11264–11268
    [Google Scholar]
  63. Schwyzer M., Wirth U. V., Vogt B., Fraefel C. 1994; BICP22 of bovine herpesvirus 1 is encoded by a spliced 1·7 kb RNA which exhibits immediate early and late transcription kinetics. J Gen Virol 75:1703–1711
    [Google Scholar]
  64. Shin E. K., Tevosian S. G., Yee A. S. 1996; The N-terminal region of E2F-1 is required for transcriptional activation of a new class of target promoter. J Biol Chem 271:12261–12268
    [Google Scholar]
  65. Stein R. W., Corrigan M., Yaciuk P., Whelan J., Moran E. 1990; Analysis of E1A-mediated growth regulation functions: binding of the 300-kilodalton cellular product correlates with E1A enhancer repression function and DNA synthesis-inducing activity. J Virol 64:4421–4427
    [Google Scholar]
  66. Tao Y., Kassatly R. F., Cress W. D., Horowitz J. M. 1997; Subunit composition determines E2F DNA-binding site specificity. Mol Cell Biol 17:6994–7007
    [Google Scholar]
  67. 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]
  68. Verona R., Moberg K., Estes S., Starz M., Vernon J. P., Lees J. A. 1997; E2F activity is regulated by cell cycle-dependent changes in subcellular localization. Mol Cell Biol 17:7268–7282
    [Google Scholar]
  69. Wang X. 2001; The expanding role of mitochondria in apoptosis. Genes Dev 152922–2933
    [Google Scholar]
  70. Wang H. G., Draetta G., Moran E. 1991; E1A induces phosphorylation of the retinoblastoma protein independently of direct physical association between the E1A and retinoblastoma products. Mol Cell Biol 11:4253–4265
    [Google Scholar]
  71. Wang H. G., Rikitake Y., Carter M. C., Yaciuk P., Abraham S. E., Zerler B., Moran E. 1993; Identification of specific adenovirus E1A N-terminal residues critical to the binding of cellular proteins and to the control of cell growth. J Virol 67:476–488
    [Google Scholar]
  72. Weintraub S. J., Prater C. A., Dean D. C. 1992; Retinoblastoma protein switches the E2F site from positive to negative element. Nature 358:259–261
    [Google Scholar]
  73. Wells J. M., Illenye S., Magae J., Wu C. L., Heintz N. H. 1997; Accumulation of E2F-4.DP-1 DNA binding complexes correlates with induction of dhfr gene expression during the G1 to S phase transition. J Biol Chem 272:4483–4492
    [Google Scholar]
  74. White E. 1998; Regulation of apoptosis by adenovirus E1A and E1B oncogenes. Semin Virol 8:505–513
    [Google Scholar]
  75. 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]
  76. 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]
  77. 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]
  78. 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]
  79. Yamada M., Sato N., Taniyama C., Ohtani K., Arai K., Masai H. 2002; A 63-base pair DNA segment containing an Sp1 site but not a canonical E2F site can confer growth-dependent and E2F-mediated transcriptional stimulation of the human ASK gene encoding the regulatory subunit for human Cdc7-related kinase. J Biol Chem 277:27668–27681
    [Google Scholar]
  80. Zerler B., Moran B., Maruyama K., Moomaw J., Grodzicker T., Ruley H. E. 1986; Adenovirus E1A coding sequences that enable ras and pmt oncogenes to transform cultured primary cells. Mol Cell Biol 6:887–899
    [Google Scholar]
  81. 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
    [Google Scholar]
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