Epstein-Barr virus nuclear antigen 1 is a DNA binding protein with strong RNA-binding activity

Journal of General Virology

Volumn 85, Issue 10, 2004, Pages 2755-2765

  Lu, Chih Chung ^a   Wu, Chia Wei ^a   Chang, Shin C ^a   Chen, Tzu Yi ^a   Hu, Chwan Ren ^a   Yeh, Ming Yi ^a   Chen, Jen Yang ^a,b   Chen, Mei Ru ^a  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

CELL NUCLEUS ANTIGEN; DNA BINDING PROTEIN; POLYGUANYLIC ACID; POLYURIDYLIC ACID; RIBONUCLEOPROTEIN; RNA; SMALL NUCLEAR RNA; UNTRANSLATED RNA; VIRUS RNA; EBV ENCODED NUCLEAR ANTIGEN 1; EBV-ENCODED NUCLEAR ANTIGEN 1; EPSTEIN BARR VIRUS ANTIGEN; EPSTEIN BARR VIRUS ENCODED RNA 1; EPSTEIN-BARR VIRUS ENCODED RNA 1; RECOMBINANT PROTEIN;

ARTICLE; BINDING AFFINITY; BINDING COMPETITION; EPSTEIN BARR VIRUS; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION; GENE REPLICATION; HEPATITIS C VIRUS; IMMUNOPRECIPITATION; IN VITRO STUDY; MOLECULAR INTERACTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; RNA BINDING; RNA PROBE; RNA STRUCTURE; VIRUS GENOME; VIRUS INFECTION; CHEMISTRY; GENETICS; METABOLISM; SERODIAGNOSIS;

HEPATITIS C VIRUS; HUMAN HERPESVIRUS 4;

DNA-BINDING PROTEINS; EPSTEIN-BARR VIRUS NUCLEAR ANTIGENS; HEPACIVIRUS; PRECIPITIN TESTS; RECOMBINANT PROTEINS; RNA; RNA, VIRAL;

EID: 5444238400     PISSN: 00221317     EISSN: None     Source Type: Journal    
DOI: 10.1099/vir.0.80239-0     Document Type: Article

References (58)

1. Ali, N. & Siddiqui, A. (1997). The La antigen binds 5′ noncoding region of the hepatitis C virus RNA in the context of the initiator AUG codon and stimulates internal ribosome entry site-mediated translation. Proc Natl Acad Sci U S A 94, 2249-2254.
2. Ambinder, R. F., Shah, W. A., Rawlins, D. R., Hayward, G. S. & Hayward, S. D. (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.
3. Ambinder, R. F., Mullen, M. A., Chang, Y.-N., Hayward, G. S. & Hayward, S. D. (1991). Functional domains of Epstein-Barr virus nuclear antigen EBNA-1. J Virol 65, 1466-1478.
4. Attrill, H. L., Cumming, S. A., Clements, J. B. & Graham, S. V. (2002). The herpes simplex virus type 1 US11 protein binds the coterminal UL12, UL13, and UL14 RNAs and regulates UL13 expression in vivo. J Virol 76, 8090-8100.
5. Belsham, G. J., Sonenberg, N. & Svitkin, Y. V. (1995). The role of the La autoantigen in internal initiation. Curr Top Microbiol Immunol 203, 85-98.
6. Bochkarev, A., Barwell, J. A., Pfuetzner, R. A., Bochkareva, E., Frappier, L. & Edwards, A. M. (1996). Crystal structure of the DNA-binding domain of the Epstein-Barr virus origin binding protein, EBNA1, bound to DNA. Cell 84, 791-800.
7. Cassiday, L. A. & Maher, L. J., III (2002). Having it both ways: transcription factors that bind DNA and RNA. Nucleic Acids Res 30, 4118-4126.
8. Chang, Y., Tung, C.-H., Huang, Y.-T., Lu, J., Chen, J.-Y. & Tsai, C.-H. (1999). Requirement for cell-to-cell contact in Epstein-Barr virus infection of nasopharyngeal carcinoma cells and keratinocytes. J Virol 73, 8857-8866.
9. Chen, M.-R., Hsu, T.-Y., Chen, J.-Y. & Yang, C.-S. (1990). Molecular characterization of a cDNA clone encoding the Epstein-Barr virus (EBV) DNase. J Virol Methods 29, 127-141.
10. Chen, M.-R., Middeldorp, J. M. & Hayward, S. D. (1993). Separation of the complex DNA binding domain of EBNA-1 into DNA recognition and dimerization subdomains of novel structure. J Virol 67, 4875-4885.
11. Chen, M.-R., Zong, J. & Hayward, S. D. (1994). Delineation of a 16 amino acid sequence that forms a core DNA recognition motif in the Epstein-Barr virus EBNA-1 protein. Virology 205, 486-495.
12. Chen, M.-R., Yang, J.-F., Wu, C.-W., Middeldorp, J. M. & Chen, J.-Y. (1998). Physical association between the EBV protein EBNA-1 and P32/TAP/hyaluronectin. J Biomed Sci 5, 173-179.
13. Chen, M.-R., Tsai, C.-H., Wu, F.-F., Kan, S.-H., Yang, C.-S. & Chen, J.-Y. (1999). The major immunogenic epitopes of Epstein-Barr virus (EBV) nuclear antigen 1 are encoded by sequence domains which vary among nasopharyngeal carcinoma biopsies and EBV-associated cell lines. J Gen Virol 80, 447-455.
14. Chen, M.-R., Liu, M.-Y., Hsu, S.-M., Fong, C.-C., Chen, C.-J., Chen, I.-H., Hsu, M.-M., Yang, C.-S. & Chen, J.-Y. (2001 . Use of bacterially expressed EBNA-1 protein cloned from a nasopharyngeal carcinoma (NPC) biopsy as a screening test for NPC patients. J Med Virol 64, 51-57.
15. Cobianchi, F., Karpel, R. L., Williams, K. R., Notario, V. & Wilson, S. H. (1988). Mammalian heterogeneous nuclear ribonucleoprotein complex protein A1. Large-scale overproduction in Escherichia coli and cooperative binding to single-stranded nucleic acids. J Biol Chem 263, 1063-1071.
16. Fu, X-D. (1995). The superfamily of arginine/serine-rich splicing factors. RNA 1, 663-680.
17. Hearing, J. C. & Levine, A. J. (1985). The Epstein-Barr virus nuclear antigen (BamHI K antigen) is a single-stranded DNA binding phosphoprotein. Virology 145, 105-116.
18. Helbig, R. & Fackelmayer, F. O. (2003). Scaffold attachment factor A (SAF-A) is concentrated in inactive X chromosome territories through its RGG domain. Chromosoma 112, 173-182.
19. Holcik, M. & Korneluk, R. G. (2000). Functional characterization of the X-linked inhibitor of apoptosis (XIAP) internal ribosome entry site element: role of La autoantigen in XIAP translation. Mol Cell Biol 20, 4648-4657.
20. Huber, M. D., Dworet, J. H., Shire, K., Frappier, L. & McAlear, M. A. (2000). The budding yeast homolog of the human EBNA1-binding protein 2 (Ebp2p) is an essential nucleolar protein required for pre-rRNA processing. J Biol Chem 275, 28764-28773.
21. Kapoor, P. & Frappier, L. (2003). EBNA1 partitions Epstein-Barr virus plasmids in yeast cells by attaching to human EBNA1-binding protein 2 on mitotic chromosomes. J Virol 77, 6946-6956.
22. Kieff, E. (1996). Epstein-Barr virus and its replication. In Fields Virology, 3rd edn, pp. 2343-2396. Edited by B. N. Fields, D. M. Knipe & P. M. Howley. Philadelphia, PA: Lippincott-Raven.
23. Kienzle, N., Young, D. B., Liaskou, D., Buck, M., Greco, S. & Sculley, T. B. (1999). Intron retention may regulate expression of Epstein-Barr virus nuclear antigen 3 family genes. J Virol 73 1195-1204.
24. Kiledjian, M. & Dreyfuss, G. (1992). Primary structure and binding activity of the hnRNP U protein: binding RNA through RGG box. EMBO J 11, 2655-2664.
25. Krainer, A. R., Conway, G. C. & Kozak, D. (1990). Purification and characterization of pre-mRNA splicing factor SF2 from HeLa cells. Genes Dev 4, 1158-1171.
26. Kube, D., Vockerodt, M., Weber, O. & 8 other authors (1999). Expression of Epstein-Barr virus nuclear antigen 1 is associated with enhanced expression of CD25 in the Hodgkin cell line L428. J Virol 73, 1630-1636.
27. Lerga, A., Hallier, M., Delva, L., Orvain, C., Gallais, I., Marie, J. & Moreau-Gachelin, F. (2001). Identification of an RNA binding specificity for the potential splicing factor TLS. J Biol Chem 276, 6807-6816.
28. Li, C., Ai, L.-S., Lin, C.-H., Hsieh, M., Li, Y.-C. & Li, S.-Y. (1998). Protein N-arginine methylation in adenosine dialdehyde-treated lymphoblastoid cells. Arch Biochem Biophys 351, 53-59.
29. Mackey, D., Middleton, T. & Sugden, B. (1995). Multiple regions within EBNA1 can link DNAs. J Virol 69, 6199-6208.
30. Manley, J. L. & Tacke, R. (1996). SR proteins and splicing control. Genes Dev 10, 1569-1579.
31. Maraia, R. J. & Intine, R. V. A. (2001). Recognition of nascent RNA by the human La antigen: conserved and divergent features of structure and function. Mol Cell Biol 21, 367-379.
32. Marechal, V., Dehee, A., Chikhi-Brachet, R., Piolot, T., Coppey-Moisan, M. & Nicolas, J.-C. (1999). Mapping EBNA-1 domains involved in binding to metaphase chromosomes. J Virol 73, 4385-4392.
33. Mears, W. E. & Rice, S. A. (1996). The RGG box motif of the herpes simplex virus ICP27 protein mediates an RNA-binding activity and determines in vivo methylation. J Virol 70, 7445-7453.
34. Middleton, T. & Sugden, B. (1992). EBNA1 can link the enhancer element to the initiator element of the Epstein-Barr virus plasmid origin of DNA replication. J Virol 66, 489-495.
35. Miller, M. M. & Read, L. K. (2003). Trypanosoma brucei: functions of RBP16 cold shock and RGG domains in macromolecular interactions. Exp Parasitol 105, 140-148.
36. Niranjanakumari, S., Lasda, E., Brazas, R. & Garcia-Blanco, M. A. (2002). Reversible cross-linking combined with immunoprecipitation to study RNA-protein interactions in vivo. Methods 26, 182-190.
37. Pannone, B. K., Xue, D. & Wolin, S. L. (1998). A role for the yeast La protein in U6 snRNP assembly: evidence that the La protein is a molecular chaperone for RNA polymerase III transcripts. EMBO J 17, 7442-7453.
38. Petersen-Mahrt, S. K., Estmer, C., Öhrmalm, C., Matthews, D. A., Russell, W. C. & Akusjärvi, G. (1999). The splicing factor-associated protein, p32, regulates RNA splicing by inhibiting ASF/SF2 RNA binding and phosphorylation. EMBO J 18 1014-1024.
39. Polvino-Bodnar, M., Kiso, J. & Schaffer, P. A. (1988). Mutational analysis of Epstein-Barr virus nuclear antigen 1 (EBNA 1). Nucleic Acids Res 16, 3415-3435.
40. Ramos, A., Hollingworth, D. & Pastore, A. (2003). G-quartet-dependent recognition between the FMRP RGG box and RNA. RNA 9, 1198-1207.
41. Rawlins, D. R., Milman, G., Hayward, S. D. & 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.
42. Sandri-Goldin, R. M. (1998). ICP27 mediates HSV RNA export by shuttling through a leucine-rich nuclear export signal and binding viral intronless RNAs through an RGG motif. Genes Dev 12 868-879.
43. Shah, W. A., Ambinder, R. F., Hayward, G. S. & Hayward, S. D. (1992). Binding of EBNA-1 to DNA creates a protease-resistant domain that encompasses the DNA recognition and dimerization functions. J Virol 66, 3355-3362.
44. Shire, K., Ceccarelli, D. F. J., Avolio-Hunter, T. M. & 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.
45. Snudden, D. K., Hearing, J., Smith, P. R., Grasser, F. A. & Griffin, B. E. (1994). EBNA-1, the major nuclear antigen of Epstein-Barr virus, resembles 'RGG' RNA binding proteins. EMBO J 13, 4840-4847.
46. Srinivas, S. K. & Sixbey, J. W. (1995). Epstein-Barr virus induction of recombinase-activating genes RAG1 and RAG2. J Virol 69, 8155-8158.
47. Sugawara, Y., Makuuchi, M., Kato, N., Shimotohno, K. & Takada, K. (1999a). Enhancement of hepatitis C virus replication by Epstein-Barr virus-encoded nuclear antigen 1. EMBO J 18, 5755-5760.
48. Sugawara, Y., Mizugaki, Y., Uchida, T., Torii, T., Imai, S., Makuuchi, M. & Takada, K. (1999b). Detection of Epstein-Barr virus (EBV) in hepatocellular carcinoma tissue: a novel EBV latency characterized by the absence of EBV-encoded small RNA expression. Virology 256, 196-202.
49. Swanson, M. S. & Dreyfuss, G. (1988). Classification and purification of proteins of heterogeneous nuclear ribonucleoprotein particles by RNA-binding specificities. Mol Cell Biol 8, 2237-2241.
50. Vanhamme, L., Perez-Morga, D., Marchal, C. & 8 other authors (1998). Trypanosoma brucei TBRGG1, a mitochondrial oligo(U)-binding protein that co-localizes with an in vitro RNA editing activity. J Biol Chem 273, 21825-21833.
51. Van Horn, D. J., Yoo, C. J., Xue, D., Shi, H. & Wolin, S. L. (1997). The La protein in Schizosaccharomyces pombe: a conserved yet dispensable phosphoprotein that functions in tRNA maturation. RNA 3, 1434-1443.
52. Van Scoy, S., Watakabe, I., Krainer, A. R. & 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.
53. Wang, Y., Finan, J. E., Middeldorp, J. M. & Hayward, S. D. (1997). P32/TAP, a cellular protein that interacts with EBNA-1 of Epstein-Barr virus. Virology 236, 18-29.
54. Yang, T.-H., Tsai, W.-H., Lee, Y.-M., Lei, H.-Y., Lai, M.-Y., Chen, D.-S., Yeh, N.-H. & Lee, S.-C. (1994). Purification and characterization of nucleolin and its identification as a transcription repressor. Mol Cell Biol 14, 6068-6074.
55. Yates, J. L. & Camiolo, S. M. (1988). Dissection of DNA replication and enhancer activation functions of Epstein-Barr virus nuclear antigen 1. Cancer Cells 6, 197-205.
56. Yen, J.-H., Chang, S. C., Hu, C.-R., Chu, S.-C., Lin, S.-S., Hsieh, Y.-S. & Chang, M.-F. (1995). Cellular proteins specifically bind to the 5′-noncoding region of hepatitis C virus RNA. Virology 208, 723-732.
57. Zetterberg, H., Jansson, A., Rymo, L., Chen, F., Karlsson, A., Klein, G. & Brodin, B. (2002). The Epstein-Barr virus ZEBRA protein activates transcription from the early lytic F promoter by binding to a promoter-proximal AP-1-like site. J Gen Virol 83 2007-2014.
58. Zuker, M. (2003). Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31, 3406-3415.