EBNA3A association with RBP-Jκ down-regulates c-myc and Epstein-Barr virus-transformed lymphoblast growth

Journal of Virology

Volumn 77, Issue 2, 2003, Pages 999-1010

  Cooper, Andrew ^a   Johannsen, Eric ^a   Maruo, Seiji ^a   Cahir McFarland, Ellen ^a   Illanes, Diego ^a   Davidson, David ^a,b   Kieff, Elliott ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b GENZYME CORPORATION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; CELL NUCLEUS ANTIGEN; HYBRID PROTEIN; MYC PROTEIN; PROTEIN SUBUNIT; VIRUS ANTIGEN; VIRUS PROTEIN;

AMINO ACID SUBSTITUTION; APOPTOSIS; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CELL CYCLE; CELL PROLIFERATION; CONTROLLED STUDY; EPSTEIN BARR VIRUS; GENE OVEREXPRESSION; GENETIC TRANSCRIPTION; GENETICS; HUMAN; HUMAN CELL; MUTATION; NONHUMAN; NULL ALLELE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DETERMINATION; WILD TYPE;

B-LYMPHOCYTES; BASE SEQUENCE; CELL DIVISION; CELL LINE, TRANSFORMED; DNA PRIMERS; DNA-BINDING PROTEINS; DOWN-REGULATION; EPSTEIN-BARR VIRUS NUCLEAR ANTIGENS; GENES, MYC; HUMANS; IMMUNOGLOBULIN J RECOMBINATION SIGNAL SEQUENCE-BINDING PROTEIN; NUCLEAR PROTEINS; PROTEIN BINDING; S PHASE;

EID: 0037225594     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.77.2.999-1010.2003     Document Type: Article

References (85)

1. Alfieri, C., M. Birkenbach, and E. Kieff. 1991. Early events in Epstein-Barr virus infection of human B lymphocytes. Virology 181:595-608. (Erratum, 185:946.)
2. Allday, M. J., D. H. Crawford, and B. E. Griffin. 1989. Epstein-Barr virus latent gene expression during the initiation of B cell immortalization. J. Gen. Virol. 70:1755-1764.
3. Allman, D., J. A. Punt, D. J. Izon, J. C. Aster, and W. S. Pear. 2002. An invitation to T and more: Notch signaling in lymphopoiesis. Cell 109(Suppl.):S1-S11.
4. Aster, J. C., and W. S. Pear. 2001. Notch signaling in leukemia. Curr. Opin. Hematol. 8:237-244.
5. Bourillot, P. Y., L. Waltzer, A. Sergeant, and E. Manet. 1998. Transcriptional repression by the Epstein-Barr virus EBNA3A protein tethered to DNA does not require RBP-Jκ. J. Gen. Virol. 79:363-370.
6. Bresnick, E. H., J. Chu, H. M. Christensen, B. Lin, and J. Norton. 2000. Linking Notch signaling, chromatin remodeling, and T-cell leukemogenesis. J. Cell. Biochem. Suppl. 35:46-53.
7. Cahir-McFarland, E. D., D. M. Davidson, S. L. Schauer, J. Duong, and E. Kieff. 2000. NF-κB inhibition causes spontaneous apoptosis in Epstein-Barr virus-transformed lymphoblastoid cells. Proc. Natl. Acad. Sci. USA 97:6055-6060.
8. Chen, L., L. Smith, M. R. Johnson, K. Wang, R. B. Diasio, and J. B. Smith. 2000. Activation of protein kinase C induces nuclear translocation of RFX1 and down-regulates c-myc via an intron 1 X box in undifferentiated leukemia HL-60 cells. J. Biol. Chem. 275:32227-32233.
9. Cherney, B. W., K. Bhatia, and G. Tosato. 1994. A role for deregulated c-Myc expression in apoptosis of Epstein-Barr virus-immortalized B cells. Proc. Natl. Acad. Sci. USA 91:12967-12971.
10. Cludts, I., and P. J. Farrell. 1998. Multiple functions within the Epstein-Barr virus EBNA-3A protein. J. Virol. 72:1862-1869.
11. Coller, H. A., C. Grandori, P. Tamayo, T. Colbert, E. S. Lander, R. N. Eisenman, and T. R. Golub. 2000. Expression analysis with oligonucleotide microarrays reveals that MYC regulates genes involved in growth, cell cycle, signaling, and adhesion. Proc. Natl. Acad. Sci. USA 97:3260-3265.
12. Cordier, M., A. Calender, M. Billaud, U. Zimber, G. Rousselet, O. Pavlish, J. Banchereau, T. Tursz, G. Bornkamm, and G. M. Lenoir. 1990. Stable transfection of Epstein-Barr virus (EBV) nuclear antigen 2 in lymphoma cells containing the EBV P3HR1 genome induces expression of B-cell activation molecules CD21 and CD23. J. Virol. 64:1002-1013.
13. Dalbies-Tran, R., E. Stigger-Rosser, T. Dotson, and C. E. Sample. 2001. Amino acids of Epstein-Barr virus nuclear antigen 3A essential for repression of Jκ-mediated transcription and their evolutionary conservation. J. Virol. 75:90-99.
14. Dash, A. B., F. C. Orrico, and S. A. Ness. 1996. The EVES motif mediates both intermolecular and intramolecular regulation of c-Myb. Genes Dev. 10:1858-1869.
15. Ellisen, L. W., J. Bird, D. C. West, A. L. Soreng, T. C. Reynolds, S. D. Smith, and J. Sklar. 1991. TAN-1, the human homolog of the Drosophila notch gene, is broken by chromosomal translocations in T lymphoblastic neoplasms. Cell 66:649-661.
16. Evans, T. J., P. J. Farrell, and S. Swaminathan. 1996. Molecular genetic analysis of Epstein-Barr virus Cp promoter function. J. Virol. 70:1695-1705.
17. Feldman, B. J., T. Hampton, and M. L. Cleary. 2000. A carboxy-terminal deletion mutant of Notch1 accelerates lymphoid oncogenesis in E2A-PBX1 transgenic mice. Blood 96:1906-1913.
18. Feldman, B. J., T. R. Reid, and M. L. Cleary. 1997. Pim1 cooperates with E2a-Pbx1 to facilitate the progression of thymic lymphomas in transgenic mice. Oncogene 15:2735-2742.
19. Finke, J., M. Rowe, B. Kallin, I. Ernberg, A. Rosen, J. Dillner, and G. Klein. 1987. Monoclonal and polyclonal antibodies against Epstein-Barr virus nuclear antigen 5 (EBNA-5) detect multiple protein species in Burkitt's lymphoma and lymphoblastoid cell lines. J. Virol. 61:3870-3878.
20. Floettmann, J. E., K. Ward, A. B. Rickinson, and M. Rowe. 1996. Cytostatic effect of Epstein-Barr virus latent membrane protein-I analyzed using tetracycline-regulated expression in B cell lines. Virology 223:29-40.
21. Fuentes-Panana, E. M., and P. D. Ling. 1998. Characterization of the CBF2 binding site within the Epstein-Barr virus latency C promoter and its role in modulating EBNA2-mediated transactivation. J. Virol. 72:693-700.
22. Fuentes-Panana, E. M., R. Peng, G. Brewer, J. Tan, and P. D. Ling. 2000. Regulation of the Epstein-Barr virus C promoter by AUF1 and the cyclic AMP/protein kinase A signaling pathway. J. Virol 74:8166-8175.
23. Gilligan, K., H. Sato, P. Rajadurai, P. Busson, L. Young, A. Rickinson, T. Tursz, and N. Raab-Traub. 1990. Novel transcription from the Epstein-Barr virus terminal EcoRI fragment, DIJhet, in a nasopharyngeal carcinoma. J. Virol. 64:4948-4956.
24. Girard, L., Z. Hanna, N. Beaulieu, C. D. Hoemann, C. Simard, C. A. Kozak, and P. Jolicoeur. 1996. Frequent provirus insertional mutagenesis of Notchl in thymomas of MMTVD/myc transgenic mice suggests a collaboration of c-myc and Notchl for oncogenesis. Genes Dev. 10:1930-1944.
25. Gordadze, A. V., R. Peng, J. Tan, G. Liu, R. Sutton, B. Kempkes, G. W. Bornkamm, and P. D. Ling. 2001. Notch11C partially replaces EBNA2 function in B cells immortalized by Epstein-Barr virus. J. Virol. 75:5899-5912.
26. Grana, X., J. Garriga, and X. Mayol. 1998. Role of the retinoblastoma protein family, pRB, p107 and p130 in the negative control of cell growth. Oncogene 17:3365-3383.
27. Grossman, S. R., E. Johannsen, X. Tong, R. Yalamanchili, and E. Kieff. 1994. The Epstein-Barr virus nuclear antigen 2 transactivator is directed to response elements by the Jκ recombination signal binding protein. Proc. Natl. Acad. Sci. USA 91:7568-7572.
28. Harada, S., and E. Kieff. 1997. Epstein-Barr virus nuclear protein LP stimulates EBNA-2 acidic domain-mediated transcriptional activation. J. Virol. 71:6611-6618.
29. Harada, S., R. Yalamanchili, and E. Kieff. 2001. Epstein-Barr virus nuclear protein 2 has at least two N-terminal domains that mediate self-association. J. Virol. 75:2482-2487.
30. Hatzivassiliou, E., P. Cardot, V. I. Zannis, and S. A. Mitsialis. 1997. Ultraspiracle, a Drosophila retinoic X receptor alpha homologue, can mobilize the human thyroid hormone receptor to transactivate a human promoter. Biochemistry 36:9221-9231.
31. Henderson, A., S. Ripley, M. Heller, and E. Kieff. 1983. Chromosome site for Epstein-Barr virus DNA in a Burkitt tumor cell line and in lymphocytes growth-transformed in vitro. Proc. Natl. Acad. Sci. USA 80:1987-1991.
32. Henkel, T., P. D. Ling, S. D. Hayward, and M. G. Peterson. 1994. Mediation of Epstein-Barr virus EBNA2 transactivation by recombination signal-binding protein J kappa. Science 265:92-95.
33. Hernandez, L., S. Hernandez, S. Bea, M. Pinyol, A. Ferrer, F. Bosch, A. Nadal, P. L. Fernandez, A. Palacin, E. Montserrat, and E. Campo. 1999. c-myc mRNA expression and genomic alterations in mantle cell lymphomas and other nodal non-Hodgkin's lymphomas. Leukemia 13:2087-2093.
34. Hoemann, C. D., N. Beaulieu, L. Girard, N. Rebai, and P. Jolicoeur. 2000. Two distinct Notchl mutant alleles are involved in the induction of T-cell leukemia in c-myc transgenic mice. Mol. Cell. Biol. 20:3831-3842.
35. Hsieh, J. J., S. Zhou, L. Chen, D. B. Young, and S. D. Hayward. 1999. CIR, a corepressor linking the DNA binding factor CBF1 to the histone deacetylase complex. Proc. Natl. Acad. Sci. USA 96:23-28.
36. Hubmann, R., J. D. Schwarzmeier, M. Shehata, M. Hilgarth, M. Duechler, M. Dettke, and R. Berger. 2002. Notch2 is involved in the overexpression of CD23 in B-cell chronic lymphocytic leukemia. Blood 99:3742-3747.
37. Hurley, E. A., L. D. Klaman, S. Agger, J. B. Lawrence, and D. A. Thorley-Lawson. 1991. The prototypical Epstein-Barr virus-transformed lymphoblastoid cell line IB4 is an unusual variant containing integrated but no episomal viral DNA. J. Virol. 65:3958-3963.
38. Johannsen, E., E. Koh, G. Mosialos, X. Tong, E. Kieff, and S. R. Grossman. 1995. Epstein-Barr virus nuclear protein 2 transactivation of the latent membrane protein 1 promoter is mediated by Jκ and PU.1. J. Virol. 69:253-262.
39. Johannsen, E., C. L. Miller, S. R. Grossman, and E. Kieff. 1996. EBNA-2 and EBNA-3C extensively and mutually exclusively associate with RBPJκ in Epstein-Barr virus-transformed B lymphocytes. J. Virol. 70:4179-4183.
40. Kaiser, C., G. Laux, D. Eick, N. Jochner, G. W. Bornkamm, and B. Kempkes. 1999. The proto-oncogene c-myc is a direct target gene of Epstein-Barr virus nuclear antigen 2. J. Virol. 73:4481-4484.
41. Kang, M. S., S. C. Hung, and E. Kieff. 2001. Epstein-Barr virus nuclear antigen 1 activates transcription from episomal but not integrated DNA and does not alter lymphocyte growth. Proc. Natl. Acad. Sci. USA 98:15233-15238.
42. Kao, H. Y., P. Ordentlich, N. Koyano-Nakagawa, Z. Tang, M. Downes, C. R. Kintner, R. M. Evans, and T. Kadesch. 1998. A histone deacetylase corepressor complex regulates the Notch signal transduction pathway. Genes Dev. 12:2269-2277.
43. Kieff, E., and A. Rickinson. 2001. Epstein-Barr virus and its replication, p. 2511-2573. In D. M. Knipe, P. M. Howley, D. E. Griffin, R. A. Lamb, M. A. Martin, B. Roizman, and S. E. Straus (ed.), Fields Virology, 4th Ed. Lippincott Williams & Wilkins, Philadelphia, Pa.
44. Knutson, J. C. 1990. The level of c-fgr RNA is increased by EBNA-2, an Epstein-Barr virus gene required for B-cell immortalization. J. Virol. 64:2530-2536.
45. Krauer, K. G., N. Kienzle, D. B. Young, and T. B. Sculley. 1996. Epstein-Barr nuclear antigen-3 and -4 interact with RBP-2N, a major isoform of RBP-Jκ in B lymphocytes. Virology 226:346-353.
46. Le Roux, A., M. Berebbi, M. Moukaddem, M. Perricaudet, and I. Joab. 1993. Identification of a short amino acid sequence essential for efficient nuclear targeting of the Epstein-Barr virus nuclear antigen 3A. J. Virol. 67:1716-1720.
47. Le Roux, A., B. Kerdiles, D. Walls, J. F. Dedieu, and M. Perricaudet. 1994. The Epstein-Barr virus determined nuclear antigens EBNA-3A, -3B, and -3C repress EBNA-2-mediated transactivation of the viral terminal protein 1 gene promoter. Virology 205:596-602.
48. Leverson, J. D., P. J. Koskinen, F. C. Orrico, E. M. Rainio, K. J. Jalkanen, A. B. Dash, R. N. Eisenman, and S. A. Ness. 1998. Pim-1 kinase and p100 cooperate to enhance c-Myb activity. Mol. Cell 2:417-425.
49. Lin, J., E. Johannsen, E. Robertson, and E. Kieff. 2002. Epstein-Barr virus nuclear antigen 3C putative repression domain mediates coactivation of the LMP1 promoter with EBNA-2. J. Virol. 76:232-242.
50. Ling, P. D., and S. D. Hayward. 1995. Contribution of conserved amino acids in mediating the interaction between EBNA2 and CBF1/RBPJκ. J. Virol. 69:1944-1950.
51. Littlewood, T. D., D. C. Hancock, P. S. Danielian, M. G. Parker, and G. I. Evan. 1995. A modified oestrogen receptor ligand-binding domain as an improved switch for the regulation of heterologous proteins. Nucleic Acids Res. 23:1686-1690.
52. Makar, K. W., C. T. Pham, M. H. Dehoff, S. M. O'Connor, S. M. Jacobi, and V. M. Holers. 1998. An intronic silencer regulates B lymphocyte cell- and stage-specific expression of the human complement receptor type 2 (CR2, CD21) gene. J. Immunol. 160:1268-1278.
53. Mann, K. P., D. Staunton, and D. A. Thorley-Lawson. 1985. Epstein-Barr virus-encoded protein found in plasma membranes of transformed cells. J. Virol. 55:710-720.
54. Mannick, J. B., J. I. Cohen, M. Birkenbach, A. Marchini, and E. Kieff. 1991. The Epstein-Barr virus nuclear protein encoded by the leader of the EBNA RNAs is important in B-lymphocyte transformation. J. Virol. 65:6826-6837.
55. Matsuo, T., M. Heller, L. Petti, E. O'Shiro, and E. Kieff. 1984. Persistence of the entire Epstein-Barr virus genome integrated into human lymphocyte DNA. Science 226:1322-1325.
56. Maunders, M. J., L. Petti, and M. Rowe. 1994. Precipitation of the Epstein-Barr virus protein EBNA 2 by an EBNA 3c-specific monoclonal antibody. J. Gen. Virol. 75:769-778.
57. Pear, W. S., J. C. Aster, M. L. Scott, R. P. Hasserjian, B. Soffer, J. Sklar, and D. Baltimore. 1996. Exclusive development of T cell neoplasms in mice transplanted with bone marrow expressing activated Notch alleles. J. Exp. Med. 183:2283-2291.
58. Polack, A., K. Hortnagel, A. Pajic, B. Christoph, B. Baier, M. Falk, J. Mautner, C. Geltinger, G. W. Bornkamm, and B. Kempkes. 1996. c-myc activation renders proliferation of Epstein-Barr virus (EBV)-transformed cells independent of EBV nuclear antigen 2 and latent membrane protein 1. Proc. Natl. Acad. Sci. USA 93:10411-10416.
59. Puglielli, M. T., M. Woisetschlaeger, and S. H. Speck. 1996. oriP is essential for EBNA gene promoter activity in Epstein-Barr virus-immortalized lymphoblastoid cell lines. J. Virol. 70:5758-5768.
60. Reizis, B., and P. Leder. 2002. Direct induction of T lymphocyte-specific gene expression by the mammalian Notch signaling pathway. Genes Dev. 16:295-300.
61. Robertson, E. S., J. Lin, and E. Kieff. 1996. The amino-terminal domains of Epstein-Barr virus nuclear proteins 3A, 3B, and 3C interact with RBPJκ. J. Virol. 70:3068-3074.
62. Sadler, R. H., and N. Raab-Traub. 1995. Structural analyses of the Epstein-Barr virus BamHI A transcripts. J. Virol. 69:1132-1141.
63. Sjoblom, A., W. Yang, L. Palmqvist, A. Jansson, and L. Rymo. 1998. An ATF/CRE element mediates both EBNA2-dependent and EBNA2-independent activation of the Epstein-Barr virus LMP1 gene promoter. J. Virol. 72:1365-1376.
64. Smith, P. 2001. Epstein-Barr virus complementary strand transcripts (CSTs/BARTs) and cancer. Semin. Cancer Biol. 11:469-476.
65. Strobl, L. J., H. Hofelmayr, G. Marschall, M. Brielmeier, G. W. Bornkamm, and U. Zimber-Strobl. 2000. Activated Notch1 modulates gene expression in B cells similarly to Epstein-Barr viral nuclear antigen 2. J. Virol. 74:1727-1735.
66. Tomkinson, B., and E. Kieff. 1992. Use of second-site homologous recombination to demonstrate that Epstein-Barr virus nuclear protein 3B is not important for lymphocyte infection or growth transformation in vitro. J. Virol. 66:2893-2903.
67. Tomkinson, B., E. Robertson, and E. Kieff. 1993. Epstein-Barr virus nuclear proteins EBNA-3A and EBNA-3C are essential for B-lymphocyte growth transformation. J. Virol. 67:2014-2025.
68. Tong, X., R. Drapkin, D. Reinberg, and E. Kieff. 1995. The 62- and 80-kDa subunits of transcription factor IIH mediate the interaction with Epstein-Barr virus nuclear protein 2. Proc. Natl. Acad. Sci. USA 92:3259-3263.
69. Tong, X., R. Drapkin, R. Yalamanchili, G. Mosialos, and E. Kieff. 1995. The Epstein-Barr virus nuclear protein 2 acidic domain forms a complex with a novel cellular coactivator that can interact with TFIIE. Mol. Cell. Biol. 15:4735-4744.
70. Tong, X., F. Wang, C. J. Thut, and E. Kieff. 1995. The Epstein-Barr virus nuclear protein 2 acidic domain can interact with TFIIB, TAF40, and RPA70 but not with TATA-binding protein. J. Virol 69:585-588.
71. Tsui, S., and W. H. Schubach. 1994. Epstein-Barr virus nuclear protein 2A forms oligomers in vitro and in vivo through a region required for B-cell transformation. J. Virol. 68:4287-4294.
72. Waltzer, L., M. Perricaudet, A. Sergeant, and E. Manet. 1996. Epstein-Barr virus EBNA3A and EBNA3C proteins both repress RBP-Jκ-EBNA2-activated transcription by inhibiting the binding of RBP-Jκ to DNA. J. Virol. 70:5909-5915.
73. Wang, F., H. Kikutani, S. F. Tsang, T. Kishimoto, and E. Kieff. 1991. Epstein-Barr virus nuclear protein 2 transactivates a cis-acting CD23 DNA element. J. Virol. 65:4101-4106.
74. Wang, F., S. F. Tsang, M. G. Kurilla, J. I. Cohen, and E. Kieff. 1990. Epstein-Barr virus nuclear antigen 2 transactivates latent membrane protein LMP1. J. Virol. 64:3407-3416.
75. Wang, L., S. R. Grossman, and E. Kieff. 2000. Epstein-Barr virus nuclear protein 2 interacts with p300, CBP, and PCAF histone acetyltransferases in activation of the LMP1 promoter. Proc. Natl. Acad. Sci. USA 97:430-435.
76. Woisetschlaeger, M., J. L. Strominger, and S. H. Speck. 1989. Mutually exclusive use of viral promoters in Epstein-Barr virus latently infected lymphocytes. Proc. Natl. Acad. Sci. USA 86:6498-6502.
77. Yalamanchili, R., X. Tong, S. Grossman, E. Johannsen, G. Mosialos, and E. Kieff. 1994. Genetic and biochemical evidence that EBNA 2 interaction with a 63-kDa cellular GTG-binding protein is essential for B lymphocyte growth transformation by EBV. Virology 204:634-641.
78. Youssoufian, H. 1998. Immunoaffinity purification of antibodies against GST fusion proteins. BioTechniques 24:198-200, 202.
79. Yu, B. W., I. Ichinose, M. A. Bonham, and M. Zajac-Kaye. 1993. Somatic mutations in c-myc intron I cluster in discrete domains that define protein binding sequences. J. Biol. Chem. 268:19586-19592.
80. Zabel, M. D., and J. H. Weis. 2001. Cell-specific regulation of the CD21 gene. Int. Immunopharmacol. 1:483-493.
81. Zajac-Kaye, M., E. P. Gelmann, and D. Levens. 1988. A point mutation in the c-myc locus of a Burkitt lymphoma abolishes binding of a nuclear protein. Science 240:1776-1780.
82. Zhao, B., D. R. Marshall, and C. E. Sample. 1996. A conserved domain of the Epstein-Barr virus nuclear antigens 3A and 3C binds to a discrete domain of Jκ. J. Virol. 70:4228-4236.
83. Zhao, B., and C. E. Sample. 2000. Epstein-Barr virus nuclear antigen 3C activates the latent membrane protein 1 promoter in the presence of Epstein-Barr virus nuclear antigen 2 through sequences encompassing an spi-1/Spi-B binding site. J. Virol. 74:5151-5160.
84. Zhou, S., M. Fujimuro, J. J. Hsieh, L. Chen, and S. D. Hayward. 2000. A role for SKIP in EBNA2 activation of CBF1-repressed promoters. J. Virol. 74:1939-1947.
85. Zhou, S., and S. D. Hayward. 2001. Nuclear localization of CBF1 is regulated by interactions with the SMRT corepressor complex. Mol. Cell. Biol. 21:6222-6232.