Live-cell imaging reveals multiple interactions between epstein-barr virus nuclear antigen 1 and cellular chromatin during interphase and mitosis

Journal of Virology

Volumn 86, Issue 9, 2012, Pages 5314-5329

  Jourdan, Nathalie ^a,b,c   Jobart Malfait, Aude ^c,d   Reis, Gabriel Dos ^a,b,c   Quignon, Frédérique ^a,b,c   Piolot, Tristan ^c,d,e   Klein, Christophe ^a,b,c   Tramier, Marc ^c,d,f   Coppey Moisan, Maïté ^c,d   Marechal, Vincent ^a,b,c  

^a SORBONNE UNIVERSITÉ   (France)

^b CENTRE DE RECHERCHE DES CORDELIERS   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d INSTITUT JACQUES MONOD   (France)

^e INSTITUT CURIE   (France)

^f UNIVERSITÉ DE RENNES 1   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; EPSTEIN BARR VIRUS ANTIGEN 1; EPSTEIN BARR VIRUS NUCLEAR ANTIGEN 1 BINDING PROTEIN 2; HIGH MOBILITY GROUP B2 PROTEIN; UNCLASSIFIED DRUG;

ANALYTIC METHOD; ARTICLE; CELL NUCLEOPLASM; CELL NUCLEUS; CHROMATIN; CHROMOSOME; EPSTEIN BARR VIRUS; FLUORESCENCE RESONANCE ENERGY TRANSFER; HELA CELL; HUMAN; HUMAN CELL; IMAGING SYSTEM; INTERPHASE; LIVE CELL IMAGING; MITOSIS; NONHUMAN; NUCLEOLUS; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RAJI CELL; VIDEO MICROSCOPY; VIRUS CELL INTERACTION; YEAST DOUBLE HYBRID SCREENING;

CARRIER PROTEINS; CELL LINE; CELL NUCLEOLUS; CHROMATIN; EPSTEIN-BARR VIRUS NUCLEAR ANTIGENS; GENE EXPRESSION; HEPATOCYTES; HMGB2 PROTEIN; HUMANS; INTERPHASE; MITOSIS; PLASMIDS; PROTEIN BINDING; PROTEIN STABILITY; PROTEIN TRANSPORT;

HUMAN HERPESVIRUS 4;

EID: 84861309354     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.06303-11     Document Type: Article

References (75)

1. Adams A. 1987. Replication of latent Epstein-Barr virus genomes in Raji cells. J. Virol. 61:1743-1746.
2. Agresti A, Lupo R, Bianchi ME, Muller S. 2003. HMGB1 interacts differentially with members of the Rel family of transcription factors. Biochem. Biophys. Res. Commun. 302:421-426.
3. Altmann M, et al. 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.
4. Ambinder RF, Shah WA, Rawlins DR, Hayward GS, Hayward SD. 1990. Definition of the sequence requirements for binding of the EBNA-1 protein to its palindromic target sites in Epstein-Barr virus DNA. J. Virol. 64:2369-2379.
5. Barbera AJ, et al. 2006. The nucleosomal surface as a docking station for Kaposi's sarcoma herpesvirus LANA. Science 311:856-861.
6. Baxter MK, McPhillips MG, Ozato K, McBride AA. 2005. The mitotic chromosome binding activity of the papillomavirus E2 protein correlates with interaction with the cellular chromosomal protein, Brd4. J. Virol. 79:4806-4818.
7. Biggiogera M, et al. 1989. Simultaneous immunoelectron microscopic visualization of protein B23 and C23 distribution in the HeLa cell nucleolus. J. Histochem. Cytochem. 37:1371-1374.
8. Boonyaratanakornkit V, et al. 1998. High-mobility group chromatin proteins 1 and 2 functionally interact with steroid hormone receptors to enhance their DNA binding in vitro and transcriptional activity in mammalian cells. Mol. Cell. Biol. 18:4471-4487.
9. Butteroni C, De Felici M, Scholer HR, Pesce M. 2000. Phage display screening reveals an association between germline-specific transcription factor Oct-4 and multiple cellular proteins. J. Mol. Biol. 304:529-540.
10. Canaan A, et al. 2009. EBNA1 regulates cellular gene expression by binding cellular promoters. Proc. Natl. Acad. Sci. U. S. A. 106:22421-22426.
11. Clegg RM, Holub O, Gohlke C. 2003. Fluorescence lifetime-resolved imaging: measuring lifetimes in an image. Methods Enzymol. 360:509-542.
12. Daikoku T, et al. 2004. In vivo dynamics of EBNA1-oriP interaction during latent and lytic replication of Epstein-Barr virus. J. Biol. Chem. 279:54817-54825.
13. Dhar SK, et al. 2001. Replication from oriP of Epstein-Barr virus requires human ORC and is inhibited by geminin. Cell 106:287-296.
14. Dresang LR, Vereide DT, Sugden B. 2009. Identifying sites bound by Epstein-Barr 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.
15. Förster T. 1946. Energiewanderung und fluorezenz. Naturwissenschaften 6:166-175.
16. Gardner JS, Chiu AL, Maki NE, Harris JF. 1985. A quantitative stability analysis of human monoclonal antibody production by heteromyeloma hybridomas, using an immunofluorescent technique. J. Immunol. Methods 85:335-346.
17. Gautier T, et al. 1994. Fate of specific nucleolar perichromosomal proteins during mitosis: cellular distribution and association with U3 snoRNA. Biol. Cell 82:81-93.
18. Grogan EA, et al. 1983. Two Epstein-Barr viral nuclear neoantigens distinguished by gene transfer, serology, and chromosome binding. Proc. Natl. Acad. Sci. U. S. A. 80:7650-7653.
19. Harrison S, Fisenne K, Hearing J. 1994. Sequence requirements of the Epstein-Barr virus latent origin of DNA replication. J. Virol. 68:1913-1925.
20. Hernandez-Verdun D, Gautier T. 1994. The chromosome periphery during mitosis. Bioessays 16:179-185.
21. Hiscox JA. 2002. The nucleolus: a gateway to viral infection? Arch. Virol. 147:1077-1089.
22. Hiscox JA. 2007. RNA viruses: hijacking the dynamic nucleolus. Nat. Rev. Microbiol. 5:119-127.
23. Jayaraman L, et al. 1998. High mobility group protein-1 (HMG-1) is a unique activator of p53. Genes Dev. 12:462-472.
24. Kanda T, Otter M, Wahl GM. 2001. Coupling of mitotic chromosome tethering and replication competence in Epstein-Barr virus-based plasmids. Mol. Cell. Biol. 21:3576-3588.
25. Kapoor P, Frappier L. 2005. Methods for measuring the replication and segregation of Epstein-Barr virus-based plasmids. Methods Mol. Biol. 292:247-266.
26. Kapoor P, Lavoie BD, Frappier L. 2005. EBP2 plays a key role in Epstein- Barr virus mitotic segregation and is regulated by aurora family kinases. Mol. Cell. Biol. 25:4934-4945.
27. Kapoor P, Shire K, Frappier L. 2001. Reconstitution of Epstein-Barr virus-based plasmid partitioning in budding yeast. EMBO J. 20:222-230.
28. Kaschka-Dierich C, Falk L, Bjursell G, Adams A, Lindahl T. 1977. Human lymphoblastoid cell lines derived from individuals without lymphoproliferative disease contain the same latent forms of Epstein-Barr virus DNA as those found in tumor cells. Int. J. Cancer 20:173-180.
29. Krysan PJ, Haase SB, Calos MP. 1989. Isolation of human sequences that replicate autonomously in human cells. Mol. Cell. Biol. 9:1026-1033.
30. Lakowicz JR. 1980. Fluorescence spectroscopic investigations of the dynamic properties of proteins, membranes and nucleic acids. J. Biochem. Biophys. Methods 2:91-119.
31. Laurent B, et al. 2010. High-mobility group protein HMGB2 regulates human erythroid differentiation through trans-activation of GFI1B transcription. Blood 115:687-695.
32. Lee MA, Diamond ME, Yates JL. 1999. Genetic evidence that EBNA-1 is needed for efficient, stable latent infection by Epstein-Barr virus. J. Virol. 73:2974-2982.
33. Lee MC, et al. 2008. Ectopic EBP2 expression enhances cyclin E1 expression and induces chromosome instability in HEK293 stable clones. BMB Rep. 41:716-721.
34. Lindahl T, et al. 1976. Covalently closed circular duplex DNA of Epstein- Barr virus in a human lymphoid cell line. J. Mol. Biol. 102:511-530.
35. Lu F, et al. 2010. Genome-wide analysis of host-chromosome binding sites for Epstein-Barr virus nuclear antigen 1 (EBNA1). Virol. J. 7:262.
36. Marechal V, et al. 1999. Mapping EBNA-1 domains involved in binding to metaphase chromosomes. J. Virol. 73:4385-4392.
37. McPhillips MG, Ozato K, McBride AA. 2005. Interaction of bovine papillomavirus E2 protein with Brd4 stabilizes its association with chromatin. J. Virol. 79:8920-8932.
38. Middleton T, Sugden B. 1994. Retention of plasmid DNA in mammalian cells is enhanced by binding of the Epstein-Barr virus replication protein EBNA1. J. Virol. 68:4067-4071.
39. Miyashita EM, Yang B, Babcock GJ, Thorley-Lawson DA. 1997. Identification of the site of Epstein-Barr virus persistence in vivo as a resting B cell. J. Virol. 71:4882-4891.
40. Muller S, et al. 2001. New EMBO members' review: the double life of HMGB1 chromatin protein: architectural factor and extracellular signal. EMBO J. 20:4337-4340.
41. Nanbo A, Sugden A, Sugden B. 2007. The coupling of synthesis and partitioning of EBV's plasmid replicon is revealed in live cells. EMBO J. 26:4252-4262.
42. Nayyar VK, Shire K, 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.
43. Niederman JC, McCollum RW, Henle G, Henle W. 1968. Infectious mononucleosis: clinical manifestations in relation to EB virus antibodies. JAMA 203:205-209.
44. Norseen J, Johnson FB, Lieberman PM. 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.
45. Ochs R, Lischwe M, O'Leary P, Busch H. 1983. Localization of nucleolar phosphoproteins B23 and C23 during mitosis. Exp. Cell Res. 146:139-149.
46. Pallier C, et al. 2003. Association of chromatin proteins high mobility group box (HMGB) 1 andHMGB2with mitotic chromosomes. Mol. Biol. Cell 14:3414-3426.
47. Phair RD, Gorski SA, Misteli T. 2004. Measurement of dynamic protein binding to chromatin in vivo, using photobleaching microscopy. Methods Enzymol. 375:393-414.
48. Piolot T, Tramier M, Coppey M, Nicolas JC, Marechal V. 2001. Close but distinct regions of human herpesvirus 8 latency-associated nuclear antigen 1 are responsible for nuclear targeting and binding to human mitotic chromosomes. J. Virol. 75:3948-3959.
49. Poddar A, Reed SC, McPhillips MG, Spindler JE, McBride AA. 2009. The human papillomavirus type 8 E2 tethering protein targets the ribosomal DNA loci of host mitotic chromosomes. J. Virol. 83:640-650.
50. Rawlins DR, Milman G, Hayward SD, Hayward GS. 1985. Sequencespecific DNA binding of the Epstein-Barr virus nuclear antigen (EBNA-1) to clustered sites in the plasmid maintenance region. Cell 42:859-868.
51. Ritzi M, et al. 2003. Complex protein-DNA dynamics at the latent origin of DNA replication of Epstein-Barr virus. J. Cell Sci. 116:3971-3984.
52. Sample J, Henson EB, Sample C. 1992. The Epstein-Barr virus nuclear protein 1 promoter active in type I latency is autoregulated. J. Virol. 66: 4654-4661.
53. Scherl A, et al. 2002. Functional proteomic analysis of human nucleolus. Mol. Biol. Cell 13:4100-4109
54. Sears J, et al. 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.
55. Shah KM, Young LS. 2009. Epstein-Barr virus and carcinogenesis: beyond Burkitt's lymphoma. Clin. Microbiol. Infect. 15:982-988.
56. Sheval EV, Polyakov VY. 2008. The peripheral chromosome scaffold, a novel structural component of mitotic chromosomes. Cell Biol. Int. 32: 708-712.
57. Shirakata M, Hirai K. 1998. Identification of minimal oriP of Epstein- Barr virus required for DNA replication. J. Biochem. 123:175-181.
58. Shire K, Ceccarelli DF, Avolio-Hunter TM, 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.
59. Soumpasis DM. 1983. Theoretical analysis of fluorescence photobleaching recovery experiments. Biophys. J. 41:95-97.
60. Stros M. 2010. HMGB proteins: interactions with DNA and chromatin. Biochim. Biophys. Acta 1799:101-113.
61. Stros M, Ozaki T, Bacikova A, Kageyama H, Nakagawara A. 2002. HMGB1 and HMGB2 cell-specifically downregulate the p53- and p73- dependent sequence-specific transactivation from the human Bax gene promoter. J. Biol. Chem. 277:7157-7164.
62. Thompson MP, Kurzrock R. 2004. Epstein-Barr virus and cancer. Clin. Cancer Res. 10:803-821.
63. Tramier M, et al. 2002. Picosecond-hetero-FRET microscopy to probe protein-protein interactions in live cells. Biophys. J. 83:3570-3577.
64. Tsujii R, et al. 2000. Ebp2p, yeast homologue of a human protein that interacts with Epstein-Barr virus nuclear antigen 1, is required for prerRNA processing and ribosomal subunit assembly. Genes Cells 5:543-553.
65. Van Hooser AA, Yuh P, Heald R. 2005. The perichromosomal layer. Chromosoma 114:377-388.
66. Wang Y, Finan JE, Middeldorp JM, Hayward SD. 1997. P32/TAP, a cellular protein that interacts with EBNA-1 of Epstein-Barr virus. Virology 236:18-29.
67. Wu H, Ceccarelli DF, Frappier L. 2000. The DNA segregation mechanism of Epstein-Barr virus nuclear antigen 1. EMBO Rep. 1:140-144.
68. Wu H, Kapoor P, Frappier L. 2002. Separation of the DNA replication, segregation, and transcriptional activation functions of Epstein-Barr nuclear antigen 1. J. Virol. 76:2480-2490.
69. Yates J, Warren N, Reisman D, Sugden B. 1984. A cis-Acting element from the Epstein-Barr viral genome that permits stable replication of recombinant plasmids in latently infected cells. Proc. Natl. Acad. Sci. U. S. A. 81:3806-3810.
70. Yates JL, Guan N. 1991. Epstein-Barr virus-derived plasmids replicate only once per cell cycle and are not amplified after entry into cells. J. Virol. 65:483-488.
71. Yates JL, Warren N, Sugden B. 1985. Stable replication of plasmids derived from Epstein-Barr virus in various mammalian cells. Nature 313: 812-815.
72. You J, Croyle JL, Nishimura A, Ozato K, Howley PM. 2004. Interaction of the bovine papillomavirus E2 protein with Brd4 tethers the viral DNA to host mitotic chromosomes. Cell 117:349-360.
73. Young LS, Rickinson AB. 2004. Epstein-Barr virus: 40 years on. Nat. Rev. Cancer 4:757-768.
74. Zappavigna V, Falciola L, Helmer-Citterich M, Mavilio F, Bianchi ME. 1996. HMG1 interacts with HOX proteins and enhances their DNA binding and transcriptional activation. EMBO J. 15:4981-4991.
75. Zwilling S, Konig H, Wirth T. 1995. High mobility group protein 2 functionally interacts with the POU domains of octamer transcription factors. EMBO J. 14:1198-1208.