EBNA2 interferes with the germinal center phenotype by downregulating BCL6 and TCL1 in non-Hodgkin's lymphoma cells

Journal of Virology

Volumn 81, Issue 5, 2007, Pages 2274-2282

  Boccellato, Francesco ^a   Anastasiadou, Eleni ^a   Rosato, Paola ^a   Kempkes, Bettina ^b   Frati, Luigi ^a   Faggioni, Alberto ^a   Trivedi, Pankaj ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b INSTITUTE OF EPIDEMIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; HLA DR ANTIGEN; IMMUNOGLOBULIN M; LATENT MEMBRANE PROTEIN 1; LYMPHOCYTE MEMBRANE IMMUNOGLOBULIN; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; PROTEIN BCL 6; PROTEIN EBNA2; PROTEIN TCL1; TRANSACTIVATOR PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ARTICLE; B CELL LYMPHOMA; BURKITT LYMPHOMA; EPSTEIN BARR VIRUS; GENE REPRESSION; GENETIC TRANSFECTION; GERMINAL CENTER; HUMAN; HUMAN CELL; INFECTIOUS MONONUCLEOSIS; LARGE CELL LYMPHOMA; NONHODGKIN LYMPHOMA; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SOMATIC HYPERMUTATION; VIRUS LATENCY; VIRUS RECOMBINANT;

BASE SEQUENCE; BURKITT LYMPHOMA; CELL LINE, TUMOR; DNA, NEOPLASM; DNA-BINDING PROTEINS; DOWN-REGULATION; EPSTEIN-BARR VIRUS NUCLEAR ANTIGENS; GENE EXPRESSION; GENES, VIRAL; GERMINAL CENTER; HERPESVIRUS 4, HUMAN; HLA-DR ANTIGENS; HUMANS; IMMUNOGLOBULIN M; LYMPHOMA, B-CELL; LYMPHOMA, LARGE-CELL, DIFFUSE; LYMPHOMA, NON-HODGKIN; MODELS, BIOLOGICAL; PHENOTYPE; PROTO-ONCOGENE PROTEINS; TRANSFECTION; VIRAL MATRIX PROTEINS;

HUMAN HERPESVIRUS 4;

EID: 33847198276     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01822-06     Document Type: Article

References (54)

1. Alizadeh, A. A., M. B. Eisen, R. E. Davis, C. Ma, I. S. Lossos, A. Rosenwald, J. C. Boldrick, H. Sabet, T. Tran, X. Yu, J. I. Powell, L. Yang, G. E. Marti, T. Moore, J. Hudson, L. Lu, D. B. Lewis, R. Tibshirani, G. Sherlock, W. C. Chan, T. C. Greiner, D. D. Weisenburger, J. O. Armitage, R. Warnke, R. Levy, W. Wilson, M. R. Grever, J. C. Byrd, D. Botstein, P. O. Brown, and L. M. Staudt. 2000. Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling. Nature 403:503-511.
2. Altiok, E., J. Minarovits, L. F. Hu, B. Contreras-Brodin, G. Klein, and I. Ernberg. 1992. Host-cell-phenotype-dependent control of the BCR2/BWR1 promoter complex regulates the expression of Epstein-Barr virus nuclear antigens 2-6. Proc. Natl. Acad. Sci. USA 89:905-909.
3. Amini, R. M., M. Berglund, R., Rosenquist, A. Von Heideman, S. Lagercrantz, U. Thunberg, J. Bergh, C. Sundstrom, B. Glimelius, and G. Enblad. 2002. A novel B-cell line (U-2932) established from a patient with diffuse large B-cell lymphoma following Hodgkin lymphoma. Leukoc. Lymphoma 43:2179-2189.
4. Bereshchenko, O. R., W. Gu, and R. Dalla-Favera. 2002. Acetylation inactivates the transcriptional repressor BCL6. Nat. Genet. 32:606-613.
5. Brauninger, A., T. Spleker, A. Mottok, A. S. Baur, R. Kuppers, and M. L. Hansmann. 2003. Epstein-Barr virus (EBV)-positive lymphoproliferations in post-transplant patients show immunoglobulin V gene mutation patterns suggesting interference of EBV with normal B cell differentiation processes. Eur. J. Immunol. 33:1593-1602.
6. Brenner, C., R. Deplus, C. Didelot, A. Loriot, E. Vire, C. De Smet, A. Gutierrez, D. Danovi, D. Bernard, T. Boon, P. G. Pellici, B. Amati, T. Kouzarides, Y. de Launoit, L. Di Croce, and F. Fuks. 2005. Myc represses transcription through recruitment of DNA methyltransferase corepressor. EMBO J. 24:336-346.
7. Carbone, A., G. Gaidano, A. Gloghini, C. Pastore, G. Saglio, U. Tirelli, R. Dalla-Favera, and B. Falini. 1997. BCL-6 protein expression in AIDS-related non-Hodgkin's lymphomas: inverse relationship with Epstein-Barr virus-encoded latent membrane protein-1 expression. Am. J. Pathol. 150:155-165.
8. Cohen, J. I., F. Wang, J. Mannick, and E. Kieff. 1989. Epstein-Barr virus nuclear protein 2 is a key determinant of lymphocyte transformation. Proc. Natl. Acad. Sci. USA 86:9558-9562.
9. Cuomo, L., P. Trivedi, F. Wang, G. Winberg, G. Klein, and M. G. Masucci. 1990. Expression of the Epstein-Barr virus (EBV)-encoded membrane antigen (LMP) increases the stimulatory capacity of EBV-negative B lymphoma lines in allogeneic mixed lymphocyte cultures. Eur. J. Immunol. 20:2293-2299.
10. Dent, A. L., A. L. Shaffer, X. Yu, D. Allman, and L. M. Staudt. 1997. Control of inflammation, cytokine expression, and germinal center formation by BCL-6. Science 276:589-592.
11. Fahraeus, R., A. Jansson, A. Ricksten, A. Sjoblom, and L. Rymo. 1990. Epstein-Barr virus-encoded nuclear antigen 2 activates the viral latent membrane protein promoter by modulating the activity of a negative regulatory element. Proc. Natl. Acad. Sci. USA 87:7390-7394.
12. Hamilton-Dutoit, S. J., and G. Pallesen. 1992. A survey of Epstein-Barr virus gene expression in sporadic non-Hodgkin's lymphomas. Detection of Epstein-Barr virus in a subset of peripheral T-cell lymphomas. Am. J. Pathol. 140:1315-1325.
13. Harris, N. L., E. S. Jaffe, J. Diebold, G. Flandrin, H. K. Muller-Hermelink, and J. Vardiman. 2000. Lymphoma classification-from controversy to consensus: the R.E.A.L. and WHO Classification of lymphoid neoplasms. Ann. Oncol. 11:3-10.
14. Hayward, S. D. 2004. Viral interactions with the Notch pathway. Semin. Cancer Biol. 145:387-396.
15. Hoyer, K. K., S. W. French, D. E. Turner, M. T. Nguyen, M. Renard, C. S. Malone, S. Knoetig, C. F. Qi, T. T. Su, H. Cheroutre, R. Wall, D. J. Rawlings, H. C. Morse, and M. A. Teitell. 2002. Dysregulated TCL1 promotes multiple classes of mature B cell lymphoma. Proc. Natl. Acad. Sci. USA 99:14392-14397.
16. Hummel, M., I. Anagnostopoulos, P. Korbjuhn, and H. Stein. 1995. Epstein-Barr virus in B-cell non-Hodgkin's lymphomas: unexpected infection patterns and different infection incidence in low- and high-grade types. J. Pathol. 175:263-271.
17. Jochner, N., D. Eick, U. Zimber-Strobl, M. Pawlita, G. W. Bornkamm, and B. Kempkes. 1996. Epstein-Barr virus nuclear antigen 2 is a transcriptional suppressor of the immunoglobulin mu gene: implications for the expression of the translocated c-myc gene in Burkitt's lymphoma cells. EMBO J. 15:375-382.
18. Kelly, G., A. Bell, and A. B. Rickinson. 2002. Epstein-Barr virus-associated Burkitt lymphomagenesis selects for downregulation of the nuclear antigen EBNA2. Nat. Med. 8:1098-1104.
19. Kempkes, B., U. Zimber-Strobl, G. Eissner, M. Pawlita, M. Falk, W. Hammerschmidt, and G. W. Bornkamm. 1996. Epstein-Barr virus nuclear antigen 2 (EBNA2)-oestrogen receptor fusion proteins complement the EBNA2-deficient Epstein-Barr virus strain P3HR1 in transformation of primary B cells but suppress growth of human B cell lymphoma lines. J. Gen. Virol. 77:227-237.
20. Kiss, C., J. Nishikawa, K. Takada, P. Trivedi, G. Klein, and L. Szekely. 2003. T cell leukemia I oncogene expression depends on the presence of Epstein-Barr virus in the virus-carrying Burkitt lymphoma lines. Proc. Natl. Acad. Sci. USA 100:4813-4818.
21. Kurth, J., M. L. Hansmann, K. Rajewsky, and R. Kuppers. 2003. Epstein-Barr virus-infected B cells expanding in germinal centers of infectious mononucleosis patients do not participate in the germinal center reaction. Proc. Natl. Acad. Sci. USA 100:4730-4735.
22. Kusano, S., and N. Raab-Traub. 2001. An Epstein-Barr virus protein interacts with Notch. J. Virol. 75:384-395.
23. - cases in Japanese population. Jpn. J. Cancer Res. 91:1233-1240.
24. Laichalk, L. L., and D. A. Thorley-Lawson. 2005. Terminal differentiation into plasma cells initiates the replicative cycle of Epstein-Barr virus in vivo. J. Virol. 79:1296-1307.
25. Laine, J., G. Kunstle, T. Obata, M. Sha, and M. Noguchi. 2000. The protooncogene TCL1 is an Akt kinase coactivator. Mol. Cell 6:395-407.
26. Maier, S., M. Santak, A. Mantik, K. Grabusic, E. Kremmer, W. Hammerschmidt, and B. Kempkes. 2005. somatic knockout of CBF1 in a human B-cell line reveals that induction of CD21 and CCR7 by EBNA-2 is strictly CBF1 dependent and that downregulation of immunoglobulin M is partially CBF1 independent. J. Virol. 79:8784-8792.
27. 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.
28. Maruo, S., L. Yang, and K. Takada. 2001. Roles of Epstein-Barr virus glycoproteins gp350 and gp25 in the infection of human epithelial cells. J. Gen. Virol. 82:2373-2383.
29. Maurer, M., and E. von Stebut. 2004. Macrophage inflammatory protein-1. Int. J. Biochem. Cell. Biol. 36:1882-1886.
30. Panagopoulos, D., P. Victoratos, M. Alexiou, G. Kollias, and G. Mosialos. 2004. Comparative analysis of signal transduction by CD40 and the Epstein-Barr virus oncoprotein LMP1 in vivo. J. Virol. 78:13253-13261.
31. Pasqualucci, L., O. Bereschenko, H. Niu, U. Klein, K. Basso, R. Guglielmino, G. Cattoretti, and R. Dalla-Favera. 2003. Molecular pathogenesis of non Hodgkin's lymphoma: the role of Bcl-6. Leukoc. Lymphoma 44:5-12.
32. Phan, R. T., M. Saito, K. Basso, H. Niu, and R. Dalla-Favera. 2005. BCL6 interacts with the transcription factor Miz-1 to suppress the cyclin-dependent kinase inhibitor p21 and cell cycle arrest in germinal center B cells. Nat. Immunol. 6:1054-1060.
33. Piskurich, J. F., K. I. Lin, Y. Lin, Y. Wang, J. P. Ting, and K. Calame. 2000. BLIMP-1 mediates extinction of major histocompatibility class II transactivator expression in plasma cells. Nat. Immunol. 1:526-532.
34. 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.
35. Rabson, M., L. Gradoville, L. Heston, and G. Miller. 1982. Non-immortalizing P3J-HR-1 Epstein-Barr virus: a deletion mutant of its transforming parent, Jijoye. J. Virol. 44:834-844.
36. Seoane, J., H. V. Le, and J. Massague. 2002. Myc suppression of the p21(Cip1) Cdk inhibitor influences the outcome of the p53 response to DNA damage. Nature 419:729-734.
37. Shaffer, A. L., X. Yu, Y. He, J. Boldrick, E. P. Chan, and L. M. Staudt. 2000. BCL-6 represses genes that function in lymphocyte differentiation, inflammation, and cell cycle control. Immunity 13:199-212.
38. Shen, R. R., D. O. Ferguson, M. Renard, K. K. Hoyer, U. Kim, X. Hao, F. W. Alt, R. G. Roeder, H. C Morse III, and M. A. Teitell. 2006. Dysregulated TCL1 requires the germinal center and genome instability for mature B-cell transformation. Blood 108:1991-1998.
39. Staege, M. S., S. P. Lee, T. Frisan, J. Mautner, S. Scholz, A. Pajic, A. B. Rickinson, M. G. Masucci, A. Polack, and G. W. Bornkamm. 2002. MYC overexpression imposes a nonimmunogenic phenotype on Epstein-Barr virus-infected B cells. Proc. Natl. Acad. Sci. USA 99:4550-4555.
40. Sudarsanam, P., and F. Winston. 2000. The Swi/Snf family nucleosome-remodeling complexes and transcriptional control. Trends Genet. 16:345-351.
41. Takada, K., K. Horinouchi, Y. Ono, T. Aya, T. Osato, M. Takahashi, and S. Hayasaka. 1991. An Epstein-Barr virus-producer line Akata: establishment of the cell line and analysis of viral DNA. Virus Genes 5:147-156.
42. Teitell, M. A. 2005. The TCL1 family of oncoproteins: co-activators of transformation. Nat. Rev. Cancer 5:640-648.
43. Tobollik, S., L. Meyer, M. Buettner, S. Klemmer, B. Kempkes, E. Kremmer, G. Niedobitek, and B. Jungnickel. 2006. Epstein-Barr-virus nuclear antigen 2 inhibits AID expression during EBV-driven B cell growth. Blood 108:3859-3864.
44. Thorley-Lawson, D. A. 2005. EBV the prototypical human tumor virus-just how bad is it? J. Allergy Clin. Immunol. 116:251-261.
45. Trivedi, P., Q. J. Zhang, F. Chen, J. Minarovits, M. Ekman, P. Biberfeld, G. Klein, and G. Winberg. 1995. Parallel existence of Epstein-Barr virus (EBV) positive and negative cells in a sporadic case of Burkitt lymphoma. Oncogene 11:505-510.
46. Uchida, J., T. Yasui, Y. Takaoka-Shichijo, M. Muraoka, W. Kulwichit, N. Raab-Traub, and H. Kikutani. 1999. Mimicry of CD40 signals by Epstein-Barr virus LMP1 in B lymphocyte responses. Science 286:300-303.
47. Wang, F., C. D. Gregory, M. Rowe, A. B. Rickinson, D. Wang, M. Birkenbach, H. Kikutani, T. Kishimoto, and E. Kieff. 1987. Epstein-Barr virus nuclear antigen 2 specifically induces expression of the B-cell activation antigen CD23. Proc. Natl. Acad. Sci. USA 84:3452-3456.
48. 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.
49. Wu, D. Y., A. Krumm, and W. H. Schubach. 2000. Promoter-specific targeting of human SWI-SNF complex by Epstein-Barr virus nuclear protein 2. J. Virol. 74:8893-8903.
50. Wu, D. Y., G. V. Kalpana, S. P. Goff, and W. H. Schubach. 1996. Epstein-Barr virus nuclear protein 2 (EBNA2) binds to a component of the human SNF-SWI complex, hSNF5/Ini1. J. Virol. 70:6020-6028.
51. Ye, B. H., P. H. Rao, R. S. Chaganti, and R. Dalla-Favera. 1993. Cloning of bcl-6, the locus involved in chromosome translocations affecting band 3q27 in B-cell lymphoma. Cancer Res. 53:2732-2735.
52. Ye, B. H., G. Cattoretti, Q. Shen, J. Zhang, N. Hawe, R. de Waard, C. Leung, M. Nouri-Shirazi, A. Orazi, R. S. Chaganti, P. Rothman, A. M. Stall, P. P. Pandolfi, and R. Dalla-Favera. 1997. The BCL-6 proto-oncogene controls germinal-centre formation and Th2-type inflammation. Nat. Genet. 16:161-170.
53. Yue, W., E. Gershburg, and J. S. Pagano. 2005. Hyperphosphorylation of EBNA2 by Epstein-Barr virus protein kinase suppresses transactivation of the LMP1 promoter. J. Virol. 79:5880-5885.
54. Zhou, G., and S. J. Ono. 2002. Transcriptional regulation of the BCL-6 gene: mechanistic dissection using mutant cell lines. Mol. Med. 8:645-654.