B23/nucleophosmin is involved in regulation of adenovirus chromatin structure at late infection stages, but not in virus replication and transcription Free

Abstract

B23/nucleophosmin has been identified as a stimulatory factor for replication of adenovirus DNA complexed with viral basic core proteins. In the present study, the function of B23 in the adenovirus life cycle was studied. It was found that both the expression of a decoy mutant derived from adenovirus core protein V that tightly associates with B23 and small interfering RNA-mediated depletion of B23 impeded the production of progeny virions. However, B23 depletion did not significantly affect the replication and transcription of the virus genome. Chromatin immunoprecipitation analyses revealed that B23 depletion significantly increased the association of viral DNA with viral core proteins and cellular histones. These results suggest that B23 is involved in the regulation of association and/or dissociation of core proteins and cellular histones with the virus genome. In addition, these results suggest that proper viral chromatin assembly, regulated in part by B23, is crucial for the maturation of infectious virus particles.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.036665-0
2012-06-01
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/jgv/93/6/1328.html?itemId=/content/journal/jgv/10.1099/vir.0.036665-0&mimeType=html&fmt=ahah

References

  1. Adachi Y., Copeland T. D., Hatanaka M., Oroszlan S. 1993; Nucleolar targeting signal of Rex protein of human T-cell leukemia virus type I specifically binds to nucleolar shuttle protein B-23. J Biol Chem 268:13930–13934[PubMed]
    [Google Scholar]
  2. Anderson C. W., Young M. E., Flint S. J. 1989; Characterization of the adenovirus 2 virion protein, mu. Virology 172:506–512 [View Article][PubMed]
    [Google Scholar]
  3. Black B. C., Center M. S. 1979; DNA-binding properties of the major core protein of adenovirus 2. Nucleic Acids Res 6:2339–2353 [View Article][PubMed]
    [Google Scholar]
  4. Brown D. T., Westphal M., Burlingham B. T., Winterhoff U., Doerfler W. 1975; Structure and composition of the adenovirus type 2 core. J Virol 16:366–387[PubMed]
    [Google Scholar]
  5. Chatterjee P. K., Vayda M. E., Flint S. J. 1985; Interactions among the three adenovirus core proteins. J Virol 55:379–386[PubMed]
    [Google Scholar]
  6. Chatterjee P. K., Vayda M. E., Flint S. J. 1986; Adenoviral protein VII packages intracellular viral DNA throughout the early phase of infection. EMBO J 5:1633–1644[PubMed]
    [Google Scholar]
  7. Chen J., Morral N., Engel D. A. 2007; Transcription releases protein VII from adenovirus chromatin. Virology 369:411–422 [View Article][PubMed]
    [Google Scholar]
  8. Daniell E., Groff D. E., Fedor M. J. 1981; Adenovirus chromatin structure at different stages of infection. Mol Cell Biol 1:1094–1105[PubMed]
    [Google Scholar]
  9. Déry C. V., Toth M., Brown M., Horvath J., Allaire S., Weber J. M. 1985; The structure of adenovirus chromatin in infected cells. J Gen Virol 66:2671–2684 [View Article][PubMed]
    [Google Scholar]
  10. Fedor M. J., Daniell E. 1983; Ionic and nonionic interactions in adenoviral nucleoprotein complexes. J Virol 47:370–375[PubMed]
    [Google Scholar]
  11. Greber U. F., Webster P., Weber J., Helenius A. 1996; The role of the adenovirus protease on virus entry into cells. EMBO J 15:1766–1777[PubMed]
    [Google Scholar]
  12. Gyurcsik B., Haruki H., Takahashi T., Mihara H., Nagata K. 2006; Binding modes of the precursor of adenovirus major core protein VII to DNA and template activating factor I: implication for the mechanism of remodeling of the adenovirus chromatin. Biochemistry 45:303–313 [View Article][PubMed]
    [Google Scholar]
  13. Haruki H., Gyurcsik B., Okuwaki M., Nagata K. 2003; Ternary complex formation between DNA–adenovirus core protein VII and TAF-Iβ/SET, an acidic molecular chaperone. FEBS Lett 555:521–527 [View Article][PubMed]
    [Google Scholar]
  14. Haruki H., Okuwaki M., Miyagishi M., Taira K., Nagata K. 2006; Involvement of template-activating factor I/SET in transcription of adenovirus early genes as a positive-acting factor. J Virol 80:794–801 [View Article][PubMed]
    [Google Scholar]
  15. Hindley C. E., Davidson A. D., Matthews D. A. 2007; Relationship between adenovirus DNA replication proteins and nucleolar proteins B23.1 and B23.2. J Gen Virol 88:3244–3248 [View Article][PubMed]
    [Google Scholar]
  16. Hingorani K., Szebeni A., Olson M. O. 2000; Mapping the functional domains of nucleolar protein B23. J Biol Chem 275:24451–24457 [View Article][PubMed]
    [Google Scholar]
  17. Hisaoka M., Ueshima S., Murano K., Nagata K., Okuwaki M. 2010; Regulation of nucleolar chromatin by B23/nucleophosmin jointly depends upon its RNA binding activity and transcription factor UBF. Mol Cell Biol 30:4952–4964 [View Article][PubMed]
    [Google Scholar]
  18. Johnson J. S., Osheim Y. N., Xue Y., Emanuel M. R., Lewis P. W., Bankovich A., Beyer A. L., Engel D. A. 2004; Adenovirus protein VII condenses DNA, represses transcription, and associates with transcriptional activator E1A. J Virol 78:6459–6468 [View Article][PubMed]
    [Google Scholar]
  19. Kawase H., Okuwaki M., Miyaji M., Ohba R., Handa H., Ishimi Y., Fujii-Nakata T., Kikuchi A., Nagata K. 1996; NAP-I is a functional homologue of TAF-I that is required for replication and transcription of the adenovirus genome in a chromatin-like structure. Genes Cells 1:1045–1056 [View Article][PubMed]
    [Google Scholar]
  20. Komatsu T., Haruki H., Nagata K. 2011; Cellular and viral chromatin proteins are positive factors in the regulation of adenovirus gene expression. Nucleic Acids Res 39:889–901 [View Article][PubMed]
    [Google Scholar]
  21. Levy A., Noll M. 1981; Chromatin fine structure of active and repressed genes. Nature 289:198–203 [View Article][PubMed]
    [Google Scholar]
  22. Martin-Fernandez M., Longshaw S. V., Kirby I., Santis G., Tobin M. J., Clarke D. T., Jones G. R. 2004; Adenovirus type-5 entry and disassembly followed in living cells by FRET, fluorescence anisotropy, and FLIM. Biophys J 87:1316–1327 [View Article][PubMed]
    [Google Scholar]
  23. Matsumoto K., Nagata K., Ui M., Hanaoka F. 1993; Template activating factor I, a novel host factor required to stimulate the adenovirus core DNA replication. J Biol Chem 268:10582–10587[PubMed]
    [Google Scholar]
  24. Matsumoto K., Okuwaki M., Kawase H., Handa H., Hanaoka F., Nagata K. 1995; Stimulation of DNA transcription by the replication factor from the adenovirus genome in a chromatin-like structure. J Biol Chem 270:9645–9650 [View Article][PubMed]
    [Google Scholar]
  25. Matthews D. A. 2001; Adenovirus protein V induces redistribution of nucleolin and B23 from nucleolus to cytoplasm. J Virol 75:1031–1038 [View Article][PubMed]
    [Google Scholar]
  26. Murano K., Okuwaki M., Hisaoka M., Nagata K. 2008; Transcription regulation of the rRNA gene by a multifunctional nucleolar protein, B23/nucleophosmin, through its histone chaperone activity. Mol Cell Biol 28:3114–3126 [View Article][PubMed]
    [Google Scholar]
  27. 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 [View Article][PubMed]
    [Google Scholar]
  28. Nakanishi Y., Maeda K., Ohtsuki M., Hosokawa K., Natori S. 1986; In vitro transcription of a chromatin-like complex of major core protein VII and DNA of adenovirus serotype 2. Biochem Biophys Res Commun 136:86–93 [View Article][PubMed]
    [Google Scholar]
  29. Nakano M. Y., Boucke K., Suomalainen M., Stidwill R. P., Greber U. F. 2000; The first step of adenovirus type 2 disassembly occurs at the cell surface, independently of endocytosis and escape to the cytosol. J Virol 74:7085–7095 [View Article][PubMed]
    [Google Scholar]
  30. Okuda M., Horn H. F., Tarapore P., Tokuyama Y., Smulian A. G., Chan P.-K., Knudsen E. S., Hofmann I. A., Snyder J. D.other authors 2000; Nucleophosmin/B23 is a target of CDK2/cyclin E in centrosome duplication. Cell 103:127–140 [View Article][PubMed]
    [Google Scholar]
  31. Okuwaki M., Iwamatsu A., Tsujimoto M., Nagata K. 2001a; Identification of nucleophosmin/B23, an acidic nucleolar protein, as a stimulatory factor for in vitro replication of adenovirus DNA complexed with viral basic core proteins. J Mol Biol 311:41–55 [View Article][PubMed]
    [Google Scholar]
  32. Okuwaki M., Matsumoto K., Tsujimoto M., Nagata K. 2001b; Function of nucleophosmin/B23, a nucleolar acidic protein, as a histone chaperone. FEBS Lett 506:272–276 [View Article][PubMed]
    [Google Scholar]
  33. Okuwaki M., Tsujimoto M., Nagata K. 2002; The RNA binding activity of a ribosome biogenesis factor, nucleophosmin/B23, is modulated by phosphorylation with a cell cycle-dependent kinase and by association with its subtype. Mol Biol Cell 13:2016–2030 [View Article][PubMed]
    [Google Scholar]
  34. Okuwaki M., Kato K., Shimahara H., Tate S., Nagata K. 2005; Assembly and disassembly of nucleosome core particles containing histone variants by human nucleosome assembly protein I. Mol Cell Biol 25:10639–10651 [View Article][PubMed]
    [Google Scholar]
  35. Samad M. A., Okuwaki M., Haruki H., Nagata K. 2007; Physical and functional interaction between a nucleolar protein nucleophosmin/B23 and adenovirus basic core proteins. FEBS Lett 581:3283–3288 [View Article][PubMed]
    [Google Scholar]
  36. Savkur R. S., Olson M. O. 1998; Preferential cleavage in pre-ribosomal RNA by protein B23 endoribonuclease. Nucleic Acids Res 26:4508–4515 [View Article][PubMed]
    [Google Scholar]
  37. Sergeant A., Tigges M. A., Raskas H. J. 1979; Nucleosome-like structural subunits of intranuclear parental adenovirus type 2 DNA. J Virol 29:888–898[PubMed]
    [Google Scholar]
  38. Spector D. J. 2007; Default assembly of early adenovirus chromatin. Virology 359:116–125 [View Article][PubMed]
    [Google Scholar]
  39. Sung M. T., Lischwe M. A., Richards J. C., Hosokawa K. 1977; Adenovirus chromatin I. Isolation and characterization of the major core protein VII and precursor Pro-VII. J Biol Chem 252:4981–4987[PubMed]
    [Google Scholar]
  40. Sung M. T., Cao T. M., Coleman R. T., Budelier K. A. 1983; Gene and protein sequences of adenovirus protein VII, a hybrid basic chromosomal protein. Proc Natl Acad Sci U S A 80:2902–2906 [View Article][PubMed]
    [Google Scholar]
  41. Tate V. E., Philipson L. 1979; Parental adenovirus DNA accumulates in nucleosome-like structures in infected cells. Nucleic Acids Res 6:2769–2785 [View Article][PubMed]
    [Google Scholar]
  42. Trotman L. C., Mosberger N., Fornerod M., Stidwill R. P., Greber U. F. 2001; Import of adenovirus DNA involves the nuclear pore complex receptor CAN/Nup214 and histone H1. Nat Cell Biol 3:1092–1100 [View Article][PubMed]
    [Google Scholar]
  43. Xue Y., Johnson J. S., Ornelles D. A., Lieberman J., Engel D. A. 2005; Adenovirus protein VII functions throughout early phase and interacts with cellular proteins SET and pp32. J Virol 79:2474–2483 [View Article][PubMed]
    [Google Scholar]
  44. Yu Y., Maggi L. B. Jr, Brady S. N., Apicelli A. J., Dai M. S., Lu H., Weber J. D. 2006; Nucleophosmin is essential for ribosomal protein L5 nuclear export. Mol Cell Biol 26:3798–3809 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.036665-0
Loading
/content/journal/jgv/10.1099/vir.0.036665-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited Most Cited RSS feed