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

Journal of General Virology

Volumn 93, Issue 6, 2012, Pages 1328-1338

  Samad, Mohammad Abdus ^a,b   Komatsu, Tetsuro ^a   Okuwaki, Mitsuru ^a   Nagata, Kyosuke ^a  

^a UNIVERSITY OF TSUKUBA   (Japan)

^b ISLAMIC UNIVERSITY   (Bangladesh)

Author keywords

[No Author keywords available]

Indexed keywords

CORE PROTEIN; HISTONE; NUCLEOPHOSMIN; VIRUS DNA;

ADENOVIRUS; ADENOVIRUS INFECTION; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CHROMATIN STRUCTURE; CONTROLLED STUDY; GENE SILENCING; GENETIC ANALYSIS; GENETIC ASSOCIATION; IN VITRO STUDY; IN VIVO STUDY; LIFE CYCLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; VIRAL GENETICS; VIRUS GENOME; VIRUS REPLICATION; VIRUS TRANSCRIPTION;

ADENOVIRUS INFECTIONS, HUMAN; ADENOVIRUSES, HUMAN; GENE EXPRESSION REGULATION, VIRAL; HELA CELLS; HISTONES; HUMANS; NUCLEAR PROTEINS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; TRANSCRIPTION, GENETIC; VIRAL CORE PROTEINS; VIRUS REPLICATION;

ADENOVIRIDAE;

EID: 84861116425     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.036665-0     Document Type: Article

References (44)

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.
2. Anderson, C. W., Young, M. E. & Flint, S. J. (1989). Characterization of the adenovirus 2 virion protein, mu. Virology 172, 506-512.
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.
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.
5. Chatterjee, P. K., Vayda, M. E. & Flint, S. J. (1985). Interactions among the three adenovirus core proteins. J Virol 55, 379-386.
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.
7. Chen, J., Morral, N. & Engel, D. A. (2007). Transcription releases protein VII from adenovirus chromatin. Virology 369, 411-422.
8. Daniell, E., Groff, D. E. & Fedor, M. J. (1981). Adenovirus chromatin structure at different stages of infection. Mol Cell Biol 1, 1094-1105.
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.
10. Fedor, M. J. & Daniell, E. (1983). Ionic and nonionic interactions in adenoviral nucleoprotein complexes. J Virol 47, 370-375.
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.
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.
13. Haruki, H., Gyurcsik, B., Okuwaki, M. & Nagata, K. (2003). Ternary complex formation between DNA-adenovirus core protein VII and TAF-Ib/SET, an acidic molecular chaperone. FEBS Lett 555, 521-527.
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.
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.
16. Hingorani, K., Szebeni, A. & Olson, M. O. (2000). Mapping the functional domains of nucleolar protein B23. J Biol Chem 275, 24451-24457.
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.
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.
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.
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.
21. Levy, A. & Noll, M. (1981). Chromatin fine structure of active and repressed genes. Nature 289, 198-203.
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.
23. Matsumoto, K., Nagata, K., Ui, M. & Hanaoka, F. (1993). Template activating factor I, a novel host factor required to stimulate he adenovirus core DNA replication. J Biol Chem 268, 10582-10587.
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.
25. Matthews, D. A. (2001). Adenovirus protein V induces redistribution of nucleolin and B23 from nucleolus to cytoplasm. J Virol 75, 1031-1038.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
36. Savkur, R. S. & Olson, M. O. (1998). Preferential cleavage in preribosomal RNA by protein B23 endoribonuclease. Nucleic Acids Res 26, 4508-4515.
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.
38. Spector, D. J. (2007). Default assembly of early adenovirus chromatin. Virology 359, 116-125.
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.
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.
41. Tate, V. E. & Philipson, L. (1979). Parental adenovirus DNA accumulates in nucleosome-like structures in infected cells. Nucleic Acids Res 6, 2769-2785.
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.
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.
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.