1887

Abstract

Affinity chromatography was used to identify cellular proteins that interact with the herpes simplex virus (HSV) tegument protein VP22. Among a small set of proteins that bind specifically to VP22, we identified TAF-I (template-activating factor I), a chromatin remodelling protein and close homologue of the histone chaperone protein NAP-1. TAF-I has been shown previously to promote more ordered transfer of histones to naked DNA through a direct interaction with histones. TAF-I, as a subunit of the INHAT (inhibitor of acetyltransferases) protein complex, also binds to histones and masks them from being substrates for the acetyltransferases p300 and PCAF. Using assays for TAF-I activity in chromatin assembly, we show that VP22 inhibits nucleosome deposition on DNA by binding to TAF-I. We also observed that VP22 binds non-specifically to DNA, an activity that is abolished by TAF-I. However, the presence of VP22 does not affect the property of INHAT in inhibiting the histone acetyltransferase activity of p300 or PCAF . We speculate that this interaction could be relevant to HSV DNA organization early in infection, for example, by interfering with nucleosomal deposition on the genome. Consistent with this possibility was the observation that overexpression of TAF-I in transfected cells interferes with the progression of HSV-1 infection.

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2003-09-01
2020-01-22
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References

  1. Adachi, Y., Pavlakis, G. N. & Copeland, T. D. ( 1994; ). Identification and characterization of SET, a nuclear phosphoprotein encoded by the translocation break point in acute undifferentiated leukemia. J Biol Chem 269, 2258–2262.
    [Google Scholar]
  2. Bulger, M. & Kadonaga, J. ( 1994; ). Biochemical reconstitution of chromatin with physiological nucleosome spacing. Methods Mol Genet 5, 241–262.
    [Google Scholar]
  3. Chang, L., Loranger, S. S., Mizzen, C., Ernst, S. G., Allis, C. D. & Annunziato, A. T. ( 1997; ). Histones in transit: cytosolic histone complexes and diacetylation of H4 during nucleosome assembly in human cells. Biochemistry 36, 469–480.[CrossRef]
    [Google Scholar]
  4. del Rio, T., Werner, H. C. & Enquist, L. W. ( 2002; ). The pseudorabies virus VP22 homologue (UL49) is dispensable for virus growth in vitro and has no effect on virulence and neuronal spread in rodents. J Virol 76, 774–782.[CrossRef]
    [Google Scholar]
  5. Deshmane, S. L. & Fraser, N. W. ( 1989; ). During latency, herpes simplex virus type 1 DNA is associated with nucleosomes in a chromatin structure. J Virol 63, 943–947.
    [Google Scholar]
  6. Dilber, M. S., Phelan, A., Aints, A., Mohamed, A. J., Elliott, G., Smith, C. I. & O'Hare, P. ( 1999; ). Intercellular delivery of thymidine kinase prodrug activating enzyme by the herpes simplex virus protein, VP22. Gene Ther 6, 12–21.[CrossRef]
    [Google Scholar]
  7. Dorange, F., Tischer, B. K., Vautherot, J. F. & Osterrieder, N. ( 2002; ). Characterization of Marek's disease virus serotype 1 (MDV-1) deletion mutants that lack UL46 to UL49 genes: MDV-1 UL49, encoding VP22, is indispensable for virus growth. J Virol 76, 1959–1970.[CrossRef]
    [Google Scholar]
  8. Elliott, G. & O'Hare, P. ( 1997; ). Intercellular trafficking and protein delivery by a herpesvirus structural protein. Cell 88, 223–233.[CrossRef]
    [Google Scholar]
  9. Elliott, G. & O'Hare, P. ( 1998; ). Herpes simplex virus type 1 tegument protein VP22 induces the stabilization and hyperacetylation of microtubules. J Virol 72, 6448–6455.
    [Google Scholar]
  10. Elliott, G. & O'Hare, P. ( 2000; ). Cytoplasm-to-nucleus translocation of a herpesvirus tegument protein during cell division. J Virol 74, 2131–2141.[CrossRef]
    [Google Scholar]
  11. Greaves, R. & O'Hare, P. ( 1989; ). Separation of requirements for protein–DNA complex assembly from those for functional activity in the herpes simplex virus regulatory protein Vmw65. J Virol 63, 1641–1650.
    [Google Scholar]
  12. Haarr, L. & Skulstad, S. ( 1994; ). The herpes simplex virus type 1 particle: structure and molecular functions. APMIS 102, 321–346.[CrossRef]
    [Google Scholar]
  13. Ishimi, Y. & Kikuchi, A. ( 1991; ). Identification and molecular cloning of yeast homolog of nucleosome assembly protein I which facilitates nucleosome assembly in vitro. J Biol Chem 266, 7025–7029.
    [Google Scholar]
  14. Ishimi, Y., Kojima, M., Yamada, M. & Hanaoka, F. ( 1987; ). Binding mode of nucleosome-assembly protein (AP-I) and histones. Eur J Biochem 162, 19–24.[CrossRef]
    [Google Scholar]
  15. Kraemer, D., Wozniak, R. W., Blobel, G. & Radu, A. ( 1994; ). The human CAN protein, a putative oncogene product associated with myeloid leukemogenesis, is a nuclear pore complex protein that faces the cytoplasm. Proc Natl Acad Sci U S A 91, 1519–1523.[CrossRef]
    [Google Scholar]
  16. Kwong, A. D. & Frenkel, N. ( 1989; ). The herpes simplex virus virion host shutoff function. J Virol 63, 4834–4839.
    [Google Scholar]
  17. Leinbach, S. S. & Summers, W. C. ( 1980; ). The structure of herpes simplex virus type 1 DNA as probed by micrococcal nuclease digestion. J Gen Virol 51, 45–59.[CrossRef]
    [Google Scholar]
  18. Leslie, J., Rixon, F. J. & McLauchlan, J. ( 1996; ). Overexpression of the herpes simplex virus type 1 tegument protein VP22 increases its incorporation into virus particles. Virology 220, 60–68.[CrossRef]
    [Google Scholar]
  19. Liang, X., Chow, B., Li, Y., Raggo, C., Yoo, D., Attah-Poku, S. & Babiuk, L. A. ( 1995; ). Characterization of bovine herpesvirus 1 UL49 homolog gene and product: bovine herpesvirus 1 UL49 homolog is dispensable for virus growth. J Virol 69, 3863–3867.
    [Google Scholar]
  20. Matsumoto, K., Nagata, K., Okuwaki, M. & Tsujimoto, M. ( 1999; ). Histone- and chromatin-binding activity of template activating factor-I. FEBS Lett 463, 285–288.[CrossRef]
    [Google Scholar]
  21. McQuibban, G. A., Commisso-Cappelli, C. N. & Lewis, P. N. ( 1998; ). Assembly, remodeling, and histone binding capabilities of yeast nucleosome assembly protein 1. J Biol Chem 273, 6582–6590.[CrossRef]
    [Google Scholar]
  22. Mencinger, M., Panagopoulos, I., Contreras, J. A., Mitelman, F. & Aman, P. ( 1998; ). Expression analysis and chromosomal mapping of a novel human gene, APRIL, encoding an acidic protein rich in leucines. Biochim Biophys Acta 1395, 176–180.[CrossRef]
    [Google Scholar]
  23. Miyaji-Yamaguchi, M., Okuwaki, M. & Nagata, K. ( 1999; ). Coiled-coil structure-mediated dimerization of template activating factor-I is critical for its chromatin remodeling activity. J Mol Biol 290, 547–557.[CrossRef]
    [Google Scholar]
  24. Morrison, E. E., Stevenson, A. J., Wang, Y. F. & Meredith, D. M. ( 1998; ). Differences in the intracellular localization and fate of herpes simplex virus tegument proteins early in the infection of Vero cells. J Gen Virol 79, 2517–2528.
    [Google Scholar]
  25. Muggeridge, M. I. & Fraser, N. W. ( 1986; ). Chromosomal organization of the herpes simplex virus genome during acute infection of the mouse central nervous system. J Virol 59, 764–767.
    [Google Scholar]
  26. Nagata, K., Kawase, H., Handa, H., Yano, K., Yamasaki, M., Ishimi, Y., Okuda, A., Kikuchi, A. & Matsumoto, K. ( 1995; ). Replication factor encoded by a putative oncogene, set, associated with myeloid leukemogenesis. Proc Natl Acad Sci U S A 92, 4279–4283.[CrossRef]
    [Google Scholar]
  27. Nagata, K., Saito, S., Okuwaki, M., Kawase, H., Furuya, A., Kusano, A., Hanai, N., Okuda, A. & Kikuchi, A. ( 1998; ). Cellular localization and expression of template-activating factor I in different cell types. Exp Cell Res 240, 274–281.[CrossRef]
    [Google Scholar]
  28. Normand, N., van Leeuwen, H. & O'Hare, P. ( 2001; ). Particle formation by a conserved domain of the herpes simplex virus protein VP22 facilitating protein and nucleic acid delivery. J Biol Chem 276, 15042–15050.[CrossRef]
    [Google Scholar]
  29. O'Hare, P. ( 1993; ). The virion transactivator of herpes simplex virus. Semin Virol 4, 145–155.[CrossRef]
    [Google Scholar]
  30. Okuwaki, M. & Nagata, K. ( 1998; ). Template activating factor-I remodels the chromatin structure and stimulates transcription from the chromatin template. J Biol Chem 273, 34511–34518.[CrossRef]
    [Google Scholar]
  31. Pomeranz, L. E. & Blaho, J. A. ( 1999; ). Modified VP22 localizes to the cell nucleus during synchronized herpes simplex virus type 1 infection. J Virol 73, 6769–6781.
    [Google Scholar]
  32. Poot, R. A., Dellaire, G., Hulsmann, B. B., Grimaldi, M. A., Corona, D. F., Becker, P. B., Bickmore, W. A. & Varga-Weisz, P. D. ( 2000; ). HuCHRAC, a human ISWI chromatin remodelling complex contains hACF1 and two novel histone-fold proteins. EMBO J 19, 3377–3387.[CrossRef]
    [Google Scholar]
  33. Ren, X., Harms, J. S. & Splitter, G. A. ( 2001; ). Bovine herpesvirus 1 tegument protein VP22 interacts with histones, and the carboxyl terminus of VP22 is required for nuclear localization. J Virol 75, 8251–8258.[CrossRef]
    [Google Scholar]
  34. Seo, S. B., McNamara, P., Heo, S., Turner, A., Lane, W. S. & Chakravarti, D. ( 2001; ). Regulation of histone acetylation and transcription by INHAT, a human cellular complex containing the set oncoprotein. Cell 104, 119–130.[CrossRef]
    [Google Scholar]
  35. Seo, S. B., Macfarlan, T., McNamara, P., Hong, R., Mukai, Y., Heo, S. & Chakravarti, D. ( 2002; ). Regulation of histone acetylation and transcription by nuclear protein pp32, a subunit of the INHAT complex. J Biol Chem 277, 14005–14010.[CrossRef]
    [Google Scholar]
  36. Simon, R. H. & Felsenfeld, G. ( 1979; ). A new procedure for purifying histone pairs H2A+H2B and H3+H4 from chromatin using hydroxylapatite. Nucleic Acids Res 6, 689–696.[CrossRef]
    [Google Scholar]
  37. Smibert, C. A., Johnson, D. C. & Smiley, J. R. ( 1992; ). Identification and characterization of the virion-induced host shutoff product of herpes simplex virus gene UL41. J Gen Virol 73, 467–470.[CrossRef]
    [Google Scholar]
  38. van Leeuwen, H., Elliott, G. & O'Hare, P. ( 2002; ). Evidence of a role for nonmuscle myosin II in herpes simplex virus type 1 egress. J Virol 76, 3471–3481.[CrossRef]
    [Google Scholar]
  39. von Lindern, M., van Baal, S., Wiegant, J., Raap, A., Hagemeijer, A. & Grosveld, G. ( 1992; ). CAN, a putative oncogene associated with myeloid leukemogenesis, may be activated by fusion of its 3′ half to different genes: characterization of the SET gene. Mol Cell Biol 12, 3346–3355.
    [Google Scholar]
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