Interaction between basic residues of epstein-barr virus EBNA1 protein and cellular chromatin mediates viral plasmid maintenance

Journal of Biological Chemistry

Volumn 288, Issue 33, 2013, Pages 24189-24199

  Kanda, Teru ^a   Horikoshi, Naoki ^b   Murata, Takayuki ^a   Kawashima, Daisuke ^a   Sugimoto, Atsuko ^a   Narita, Yohei ^a   Kurumizaka, Hitoshi ^b   Tsurumi, Tatsuya ^a  

^a AICHI CANCER CENTER HOSPITAL   (Japan)

^b WASEDA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING DOMAIN; EPSTEIN-BARR VIRUS; INFECTED CELLS;

AMINO ACIDS; MAINTENANCE; VIRUSES;

CHROMOSOMES;

ARGININE; BETAINE; EPSTEIN BARR VIRUS ANTIGEN 1; GLYCINE; HYBRID PROTEIN;

AMINO ACID SUBSTITUTION; ARTICLE; CHROMATIN; CHROMOSOME BINDING DOMAIN; CONTROLLED STUDY; EPISOME; EPSTEIN BARR VIRUS; IN VITRO STUDY; MOLECULAR INTERACTION; MOLECULAR MODEL; MUTATIONAL ANALYSIS; NONHUMAN; NUCLEOSOME; PLASMID; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RESIDUE ANALYSIS;

AMINO ACID; CHROMOSOMES; CONFOCAL MICROSCOPY; DNA VIRUSES; EBNA1; EPISOME; EPSTEIN-BARR VIRUS; FLUORESCENCE; NUCLEOSOME; SITE-DIRECTED MUTAGENESIS;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; AMINO ACIDS, BASIC; CHROMATIN; CHROMOSOMES, HUMAN; EPSTEIN-BARR VIRUS NUCLEAR ANTIGENS; HELA CELLS; HERPESVIRUS 4, HUMAN; HUMANS; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; MUTATION; NUCLEOSOMES; PEPTIDES; PLASMIDS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS;

EID: 84882302748     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.491167     Document Type: Article

References (46)

1. Botchan, M. (2004) Hitchhiking without covalent integration. Cell 117, 280-281
2. Calos, M. P. (1998) Stability without a centromere. Proc. Natl. Acad. Sci. U.S.A. 95, 4084-4085
3. Leight, E. R., and Sugden, B. (2000) EBNA-1. A protein pivotal to latent infection by Epstein-Barr virus. Rev. Med. Virol. 10, 83-100
4. Rawlins, D. R., Milman, G., Hayward, S. D., and Hayward, G. S. (1985) Sequence-specific DNA binding of the Epstein-Barr virus nuclear antigen (EBNA-1) to clustered sites in the plasmid maintenance region. Cell 42, 859-868
5. Reisman, D., Yates, J., and Sugden, B. (1985) A putative origin of replication of plasmids derived from Epstein-Barr virus is composed of two cisacting components. Mol. Cell. Biol. 5, 1822-1832
6. Ambinder, R. F., Mullen, M. A., Chang, Y. N., Hayward, G. S., and Hayward, S. D. (1991) Functional domains of Epstein-Barr virus nuclear antigen EBNA-1. J. Virol. 65, 1466-1478
7. Marechal, V., Dehee, A., Chikhi-Brachet, R., Piolot, T., Coppey-Moisan, M., and Nicolas, J. C. (1999) Mapping EBNA-1 domains involved in binding to metaphase chromosomes. J. Virol. 73, 4385-4392
8. Coppotelli, G., Mughal, N., and Masucci, M. G. (2013) The Gly-Ala repeat modulates the interaction of Epstein-Barr virus nuclear antigen-1 with cellular chromatin. Biochem. Biophys. Res. Commun. 431, 706-711
9. Hung, S. C., Kang, M. S., and Kieff, E. (2001) Maintenance of Epstein-Barr virus (EBV) oriP-based episomes requires EBV-encoded nuclear antigen-1 chromosome-binding domains, which can be replaced by highmobility group-I or histone H1. Proc. Natl. Acad. Sci. U.S.A. 98, 1865-1870
10. Sears, J., Ujihara, M., Wong, S., Ott, C., Middeldorp, J., and Aiyar, A. (2004) The amino terminus of Epstein-Barr Virus (EBV) nuclear antigen 1 contains AT hooks that facilitate the replication and partitioning of latent EBV genomes by tethering them to cellular chromosomes. J. Virol. 78, 11487-11505
11. Coppotelli, G., Mughal, N., Marescotti, D., and Masucci, M. G. (2011) High avidity binding to DNA protects ubiquitylated substrates from proteasomal degradation. J. Biol. Chem. 286, 19565-19575
12. Kanda, T., Otter, M., and Wahl, G. M. (2001) Coupling of mitotic chromosome tethering and replication competence in epstein-barr virusbased plasmids. Mol. Cell. Biol. 21, 3576-3588
13. Nayyar, V. K., Shire, K., and Frappier, L. (2009) Mitotic chromosome interactions of Epstein-Barr nuclear antigen 1 (EBNA1) and human EBNA1-binding protein 2 (EBP2). J. Cell Sci. 122, 4341-4350
14. Wu, H., Kapoor, P., and Frappier, L. (2002) Separation of the DNA replication, segregation, and transcriptional activation functions of Epstein-Barr nuclear antigen 1. J. Virol. 76, 2480-2490
15. Dresang, L. R., Vereide, D. T., and Sugden, B. (2009) Identifying sites bound by Epstein-Barr virus nuclear antigen 1 (EBNA1) in the human genome. Defining a position-weighted matrix to predict sites bound by EBNA1 in viral genomes. J. Virol. 83, 2930-2940
16. Van Scoy, S., Watakabe, I., Krainer, A. R., and Hearing, J. (2000) Human p32. A coactivator for Epstein-Barr virus nuclear antigen-1-mediated transcriptional activation and possible role in viral latent cycle DNA replication. Virology 275, 145-157
17. Wang, Y., Finan, J. E., Middeldorp, J. M., and Hayward, S. D. (1997) P32/ TAP, a cellular protein that interacts with EBNA-1 of Epstein-Barr virus. Virology 236, 18-29
18. Holowaty, M. N., Zeghouf, M., Wu, H., Tellam, J., Athanasopoulos, V., Greenblatt, J., and Frappier, L. (2003) Protein profiling with Epstein-Barr nuclear antigen-1 reveals an interaction with the herpesvirus-associated ubiquitin-specific protease HAUSP/USP7. J. Biol. Chem. 278, 29987-29994
19. Shire, K., Ceccarelli, D. F., Avolio-Hunter, T. M., and Frappier, L. (1999) EBP2, a human protein that interacts with sequences of the Epstein-Barr virus nuclear antigen 1 important for plasmid maintenance. J. Virol. 73, 2587-2595
20. Snudden, D. K., Hearing, J., Smith, P. R., Grässer, F. A., and Griffin, B. E. (1994) EBNA-1, the major nuclear antigen of Epstein-Barr virus, resembles 'RGG' RNA binding proteins. EMBO J. 13, 4840-4847
21. Norseen, J., Thomae, A., Sridharan, V., Aiyar, A., Schepers, A., and Lieberman, P. M. (2008) RNA-dependent recruitment of the origin recognition complex. EMBO J. 27, 3024-3035
22. Howden, S. E., Wardan, H., Voullaire, L., McLenachan, S., Williamson, R., Ioannou, P., and Vadolas, J. (2006) Chromatin-binding regions of EBNA1 protein facilitate the enhanced transfection of Epstein-Barr virus-based vectors. Hum. Gene Ther. 17, 833-844
23. Jourdan, N., Jobart-Malfait, A., Dos Reis, G., Quignon, F., Piolot, T., Klein, C., Tramier, M., Coppey-Moisan, M., and Marechal, V. (2012) Live-cell imaging reveals multiple interactions between Epstein-Barr virus nuclear antigen 1 and cellular chromatin during interphase and mitosis. J. Virol. 86, 5314-5329
24. Norseen, J., Johnson, F. B., and Lieberman, P. M. (2009) Role for G-quadruplex RNA binding by Epstein-Barr virus nuclear antigen 1 in DNA replication and metaphase chromosome attachment. J. Virol. 83, 10336-10346
25. Aravind, L., and Landsman, D. (1998) AT-hook motifs identified in a wide variety of DNA-binding proteins. Nucleic Acids Res. 26, 4413-4421
26. Reeves, R., and Nissen, M. S. (1990) The A.T-DNA-binding domain of mammalian high mobility group I chromosomal proteins.Anovel peptide motif for recognizing DNA structure. J. Biol. Chem. 265, 8573-8582
27. Kanda, T., Sullivan, K. F., and Wahl, G. M. (1998) Histone-GFP fusion protein enables sensitive analysis of chromosome dynamics in living mammalian cells. Curr. Biol. 8, 377-385
28. Imai, Y., Matsushima, Y., Sugimura, T., and Terada, M. (1991) A simple and rapid method for generating a deletion by PCR. Nucleic Acids Res. 19, 2785
29. Zheng, L., Baumann, U., and Reymond, J. L. (2004) An efficient one-step site-directed and site-saturation mutagenesis protocol. Nucleic Acids Res. 32, e115
30. Kanda, T., Otter, M., and Wahl, G. M. (2001) Mitotic segregation of viral and cellular acentric extrachromosomal molecules by chromosome tethering. J. Cell Sci. 114, 49-58
31. Abe, A., Emi, N., Kanie, T., Imagama, S., Kuno, Y., Takahashi, M., Saito, H., and Naoe, T. (2004) Expression cloning of oligomerization-activated genes with cell-proliferating potency by pseudotype retrovirus vector. Biochem. Biophys. Res. Commun. 320, 920-926
32. Shimizu, N., Tanabe-Tochikura, A., Kuroiwa, Y., and Takada, K. (1994) Isolation of Epstein-Barr virus (EBV)-negative cell clones from the EBVpositive Burkitt's lymphoma (BL) line Akata. Malignant phenotypes of BL cells are dependent on EBV. J. Virol. 68, 6069-6073
33. Daikoku, T., Kudoh, A., Fujita, M., Sugaya, Y., Isomura, H., and Tsurumi, T. (2004) In vivo dynamics of EBNA1-oriP interaction during latent and lytic replication of Epstein-Barr virus. J. Biol. Chem. 279, 54817-54825
34. Yates, J. L., Camiolo, S. M., and Bashaw, J. M. (2000) The minimal replicator of Epstein-Barr virus oriP. J. Virol. 74, 4512-4522
35. Tachiwana, H., Kagawa, W., Shiga, T., Osakabe, A., Miya, Y., Saito, K., Hayashi-Takanaka, Y., Oda, T., Sato, M., Park, S. Y., Kimura, H., and Kurumizaka, H. (2011) Crystal structure of the human centromeric nucleosome containing CENP-A. Nature 476, 232-235
36. Tachiwana, H., Osakabe, A., Kimura, H., and Kurumizaka, H. (2008) Nucleosome formation with the testis-specific histone H3 variant, H3t, by human nucleosome assembly proteins in vitro. Nucleic Acids Res. 36, 2208-2218
37. Altmann, M., Pich, D., Ruiss, R., Wang, J., Sugden, B., and Hammerschmidt, W. (2006) Transcriptional activation by EBV nuclear antigen 1 is essential for the expression of EBV's transforming genes. Proc. Natl. Acad. Sci. U.S.A. 103, 14188-14193
38. Kennedy, G., and Sugden, B. (2003) EBNA-1, a bifunctional transcriptional activator. Mol. Cell. Biol. 23, 6901-6908
39. Singh, G., Aras, S., Zea, A. H., Koochekpour, S., and Aiyar, A. (2009) Optimal transactivation by Epstein-Barr nuclear antigen 1 requires the UR1 and ATH1 domains. J. Virol. 83, 4227-4235
40. Gotoh, E., Asakawa, Y., and Kosaka, H. (1995) Inhibition of protein serine/ threonine phosphatases directly induces premature chromosome condensation in mammalian somatic cells. Biomed. Res. 16, 63-68
41. Kirchmaier, A. L., and Sugden, B. (1997) Dominant-negative inhibitors of EBNA-1 of Epstein-Barr virus. J. Virol. 71, 1766-1775
42. Barbera, A. J., Chodaparambil, J. V., Kelley-Clarke, B., Joukov, V., Walter, J. C., Luger, K., and Kaye, K. M. (2006) The nucleosomal surface as a docking station for Kaposi's sarcoma herpesvirus LANA. Science 311, 856-861
43. Bischoff, F. R., and Ponstingl, H. (1991) Catalysis of guanine nucleotide exchange on Ran by the mitotic regulator RCC1. Nature 354, 80-82
44. Makde, R. D., England, J. R., Yennawar, H. P., and Tan, S. (2010) Structure of RCC1 chromatin factor bound to the nucleosome core particle. Nature 467, 562-566
45. Sekhar, V., Reed, S. C., and McBride, A. A. (2010) Interaction of the-papillomavirus E2 tethering protein with mitotic chromosomes. J. Virol. 84, 543-557
46. Harrer, M., Lührs, H., Bustin, M., Scheer, U., and Hock, R. (2004) Dynamic interaction of HMGA1a proteins with chromatin. J. Cell Sci. 117, 3459-3471