The bfl-1 gene is transcriptionally upregulated by the Epstein-Barr virus LMP1, and its expression promotes the survival of a Burkitt's lymphoma cell line

Journal of Virology

Volumn 74, Issue 14, 2000, Pages 6652-6658

  D'Souza, Brendan ^a   Rowe, Martin ^b   Walls, Dermot ^a  

^a DUBLIN CITY UNIVERSITY   (Ireland)

^b CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

LATENT MEMBRANE PROTEIN 1; MESSENGER RNA; PROTEIN BCL 2; PROTEIN P53; TETRACYCLINE; VIRUS PROTEIN;

APOPTOSIS; ARTICLE; BURKITT LYMPHOMA; CELL PROLIFERATION; CELL SURVIVAL; EPSTEIN BARR VIRUS; GENE CONTROL; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; VIRUS EXPRESSION;

APOPTOSIS; BLOTTING, NORTHERN; BURKITT LYMPHOMA; GENE EXPRESSION REGULATION, VIRAL; HERPESVIRUS 4, HUMAN; HUMANS; ONCOGENE PROTEINS, VIRAL; PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; RNA, MESSENGER; TUMOR CELLS, CULTURED; VIRAL MATRIX PROTEINS;

EID: 0033916788     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.74.14.6652-6658.2000     Document Type: Article

References (55)

1. Aiello, A. D. Delia, M. G. Borrello, D. Biassoni, R. Giardini, E. Fontanella, F. Pezzella, K. Pulford, M. Pierotti, and G. Della-Porta. 1992. Flow cytometric detection of the mitochondrial Bcl-2 protein in normal and neoplastic human lymphoid cells. Cytometry 13:502-509.
2. Akagi, T., E. Kondo, and T. Yoshino. 1994. Expression of Bcl-2 protein and Bcl-2 mRNA in normal and neoplastic lymphoid tissues. Leuk. Lymphoma 13:81-87.
3. Allday, M. J. 1996. Apoptosis and Epstein-Barr virus in B cells. Epstein-Barr Virus Rep. 3:55-65.
4. Baichwal, V. R., and B. Sugden. 1988. Transformation of Balb 3T3 cells by the BNLF-1 gene of Epstein-Barr virus. Oncogene 2:461-467.
5. Baker, S. J., and E. P. Reddy. 1996. Transducers of life and death: TNF receptor superfamily and associated proteins. Oncogene 12:1-9.
6. Brattsand, G., D. A. Cantrell, S. Ward, F. Ivars, and M. Gulberg. 1990. Signal transduction through the T-cell receptor-CD3 complex: evidence for heterogeneity in receptor coupling. J. Immunol. 144:3651-3658.
7. Chen, C.-Y. A., and A.-B. Shyu. 1995. AU-rich elements: characterisation and importance in mRNA degradation. Trends Biochem. Sci. 20:465-470.
8. Choi, S. S., I. C. Park, J. W. Yun, Y. C. Sung, S. I. Hong, and H. S. Shin. 1995. A novel Bcl-2 related gene, Bfl-1, is overexpressed in stomach cancer and preferentially expressed in bone marrow. Oncogene 11:1693-1698.
9. Chleq-Deschamps, C. M., D. P. LeBrun, P. Huie, D. P. Besnier, R. A. Warnke, R. K. Sibley, and M. L. Cleary. 1993. Topographical dissociation of Bcl-2 messenger RNA and protein expression in human lymphoid tissues. Blood 81:293-298.
10. D'Sa-Eipper, C., and G. Chinnadurai. 1998. Functional dissection of bfl-1, a bcl-2 homolog: anti-apoptosis, oncogene cooperation and cell proliferation activities. Oncogene 16:3105-3114.
11. D'Sa-Eipper, C., T. Subramanian, and G. Chinnadurai. 1996. bfl-1, a bcl-2 homologue, suppresses p53-induced apoptosis and exhibits potent cooperative transforming activity. Cancer Res. 56:3879-3882.
12. Farrell, P. 1995. Epstein-Barr virus immortalizing genes. Trends Microbiol. 3:105-109.
13. Finke, J., R. Fritzen, P. Ternes, P. Trivedi, K. J. Bross, W. Lange, R. Mertelsman, and G. Dolken. 1992. Expression of bcl-2 in Burkitt's lymphoma cell lines: induction by latent Epstein-Barr virus genes. Blood 80:459-469.
14. Floettmann, J. E., K. Ward, A. B. Rickinson, and M. Rowe. 1996. Cytostatic effect of Epstein-Barr virus latent membrane protein-1 analyzed using tetracydine-regulated expression in B cell lines. Virology 223:29-40.
15. Fries, K. L., W. E. Miller, and N. Raab-Traub. 1996. Epstein-Barr virus latent membrane protein 1 blocks p53-mediated apoptosis through the induction of the A20 gene. J. Virol. 70:8653-8659.
16. Gregory, C. D., M. Rowe, and A. B. Rickinson. 1990. Different Epstein-Barr virus-B cell interactions in phenotypically distinct clones of a Burkitt's lymphoma cell line. J. Gen. Virol. 71:1481-1495.
17. Gregory, C. D., C. Dive, S. Henderson, C. A. Smith, G. T. Williams, J. Gordon, and A. B. Rickinson. 1991. Activation of Epstein-Barr virus latent gene products protects human B cells from death by apoptosis. Nature 349: 612-614.
18. Harigai, M., T. Miyashita, M. Hanada, and J. C. Reed. 1996. A cis-acting element in the bcl-2 gene controls expression through translational mechanisms. Oncogene 12:1369-1374.
19. Henderson, S., M. Rowe, C. D. Gregory, D. Croom-Carter, F. Wang, R. Longnecker, E. Kieff, and A. B. Rickinson. 1991. Induction of bcl-2 expression by Epstein-Barr virus latent membrane protein 1 protects infected B cells from programmed cell death. Cell 65:1107-1115.
20. Hu, X., E. Yee, J. M. Harlan, F. Wong, and A. Karsan. 1998. Lipopolysaccharide induces the antiapoptotic molecules, A1 and A20, in microvascular endothelial cells. Blood 92:2759-2765.
21. Jung-Ha, H., D. Kim, S.-B. Lee, S.-I. Hong, S.-Y. Park, J. Huh, C.-W. Kim, S.-S. Kim, Y. Lee, S. S. Choi, and H.-S. Shin. 1998. Expression of Bfl-1 in normal and tumour tissues: Bfl-1 overexpression in cancer is attributable to its preferential expression in infiltrating inflammatory cells. Hum. Pathol. 29: 723-728.
22. Karsan, A., E. Yee, K. Kaushansky, and J. M. Harlan. 1996. Cloning of a human Bcl-2 homologue: inflammatory cytokines induce human Al, in cultured endothelial cells. Blood 87:3089-3096.
23. Karsan, A., E. Yee, and J. M. Harlan. 1996. Endothelial cell death induced by tumour necrosis factor-α is inhibited by the Bcl-2 family member, Al. J. Biol. Chem. 271:27201-27204.
24. Kaye, K. M., K. M. Izumi, and E. Kieff. 1993. Epstein-Barr virus latent membrane protein 1 is essential for B-lymphocyte growth transformation. Proc. Natl. Acad. Sci. USA 90:9150-9154.
25. Keiff, E. 1996. Epstein-Barr virus and its replication, p. 2343-2396. In B. N. Fields, D. M. Knipe, P. Howley, R. M. Chanock, J. L. Melnick, T. P. Monath, B. Roizman, and S. E. Straus (ed.), Fields virology. Lippincott-Raven, Philadelphia, Pa.
26. Kenny, J. J., T. J. Knobloch, M. Augustus, K. C. Carter, C. A. Rosen, and J. C. Lang. 1997. GRS, a novel member of the Bcl-2 gene family, is highly expressed in multiple cancer cell lines and in normal leukocytes. Oncogene 14:997-1001.
27. Klein, G. 1994. Epstein-Barr virus strategy in normal and neoplastic B cells. Cell 77:791-793.
28. Laherty, C. D., H. M. Hu, A. W. Opipari, F. Wang, and V. M. Dixit. 1992. The Epstein-Barr virus LMP-1 gene product induces A20 zinc finger protein expression by activating nuclear factor-κB. J. Biol. Chem. 267:24157-24160.
29. Liljeholm, S., K. Hughes, T. Grundstorm, and P. Brodin. 1998. NF-kappaB only partially mediates Epstein-Barr virus latent membrane protein 1 activation of B cells. J. Gen. Virol. 79:2117-2125.
30. Lin, E. Y., A. Orlofsky, M. S. Berger, and M. B. Prystowsky. 1996. Characterization of Al, a novel hemopoietic-specific early-response gene with sequence similarity to bcl-2. J. Immunol. 151:1979-1988.
31. Liu, Y.-J., D. Y. Mason, G. D. Johnson, S. Abbot, C. D. Gregory, D. L. Hardie, J. Gordon, and I. C. M. MacLennan. 1991. Germinal center cells express Bcl-2 protein after activation by signals which prevent entry to apoptosis. Eur. J. Immunol. 21:1905-1910.
32. Maniatis, T., E. F. Fritsch, and J. Sambrook. 1982. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
33. Martin, J. M., D. Veis, S. J. Korsmeyer, and B. Sugden. 1993. Latent membrane protein of Epstein-Barr virus induces cellular phenotypes independently of expression of Bcl 2. J. Virol. 67:5269-5278.
34. Massuci, M. G., B. Contreras-Salazar, E. Ragnar, K. Falk, J. Minarovits, I. Ernberg, and G. Klein. 1989. 5-azacytidine upregulates the expression of Epstein-Barr virus nuclear antigen 2 (EBNA-2) through EBNA-6 and latent membrane protein in the Burkitt's lymphoma cell line Rael. J. Virol. 63: 3135-3141.
35. Miller, W. E., H. S. Earp, and N. Raab-Traub. 1995. The Epstein-Barr virus latent membrane protein 1 induces expression of epidermal growth factor receptor. J. Virol. 69:4390-4398.
36. Milner, A. E., G. D. Johnson, and C. D. Gregory. 1992. Prevention of programmed cell death in Burkitt lymphoma cell lines by bcl-2-dependent and -independent mechanisms. Int. J. Cancer 52:636-644.
37. Moreb, J. S., and M. Schweder. 1997. Human Al, a bcl-2-related gene, is induced in leukemic cells by cytokines as well as differentiating factors. Leukemia 11:998-1004.
38. Okan, I., Y. Wang, F. Chen, S. Imreh, G. Klein, and C. G. Wilman. 1995. The EBV-encoded LMP1 protein inhibits p53-triggered apoptosis but not growth arrest. Oncogene 11:1027-1031.
39. Opipari, A. W., H. M. Hu, R. Yabkovitz, and V. Dixit. 1992. The A20 zinc finger protein protects cells from tumour necrosis factor cytotoxicity. J. Biol. Chem. 267:12424-12427.
40. Park, I.-C., S. H. Lee, D. Y. Whang, W. S. Hong, S. S. Choi, H. S. Shin, T.-B. Choe, and S. I. Hong. 1997. Expression of a novel bcl-2 related gene, bfl-1, in various human cancers and cancer cell lines. Anticancer Res. 17:4619-4622.
41. Pezzella, F., A. G. D. Tse, J. L. Cordell, K. A. F. Pulford, K. C. Gatter, and D. Y. Mason. 1990. Expression of the bcl-2 oncogene protein is not specific for the 14:18 chromosomal translocation. Am. J. Pathol. 137:225-232.
42. Qu, L., and M. Rowe. 1992. Epstein-Barr virus latent gene expression in uncultured peripheral blood lymphocytes, J. Virol. 66:3715-3724.
43. Ramqvist T., K. P. Magnusson, Y. S. Wang, L. Szekely, G. Klein, and K. G. Wiman. 1993. Wild-type p53 induces apoptosis in a Burkitt lymphoma (BL) line that carries mutant p53. Oncogene 8:1495-1500.
44. Rowe, M., H. S. Evans, L. S. Young, K. Hennessy, E. Kieff, and A. B. Rickinson. 1987. Monoclonal antibodies to the latent membrane protein of Epstein-Barr virus reveal heterogeneity of the protein and inducible expression in virus-transformed cells. J. Gen. Virol. 68:1575-1586.
45. Rowe, M., R. Khanna, C. A. Jacob, V. Argaet, A. Kelly, S. Powis, M. Belich, D. Croom Carter, S. Lee, S. R. Burrows, J. Trowsdale, D. J. Moss, and A. B. Rickinson. 1995. Restoration of endogenous antigen processing in Burkitt's lymphoma cells by Epstein-Barr virus latent membrane protein-1: coordinate upregulation of peptide transporters and HLA-classI antigen expression. Eur. J. Immunol. 25:1374-1384.
46. Rowe, M., M. Peng-Pilon, D. S. Huen, R. Hardy, D. Croom-Carter, E. Lundgren, and A. B. Rickinson. 1994. Upregulation of bcl-2 by Epstein-Barr virus latent membrane protein LMP1: a B-cell-specific response that is delayed relative to NF-kappa B activation and to induction of cell surface markers. J. Virol. 68:5602-5612.
47. Rowe, M., C. M. Rooney, C. F. Edwards, G. M. Lenoir, and A. B. Rickinson. 1986. Epstein-Barr virus status and tumour cell phenotype in sporadic Burkitt's lymphoma. Int. J. Cancer 37:367-373.
48. Seto, M., U. Jaeger, R. D. Hockett, W. Graninger, S. Bennett, P. Goldman, and S. J. Korsmeyer. 1988. Alternative promoters and exons, somatic mutation and deregulation of the bcl-Ig fusion gene in lymphoma. EMBO J. 7: 123-131.
49. Silins, S. L., and T. B. Sculley. 1995. Burkitt's lymphoma cells are resistant to programmed cell death in the presence of the Epstein-Barr virus latent antigen EBNA-4. Int. J. Cancer 60:65-72.
50. Tewari, M., and V. M. Dixit. 1996. Recent advances in tumour necrosis factor and CD40 signaling. Current Opin. Genet. Dev. 6:39-44.
51. Tierney, R. J., N. Steven, L. S. Young, and A. B. Rickinson. 1994. Epstein-Barr virus latency in blood mononuclear cells: analysis of viral gene transcription during primary infection and in the carrier state. J. Virol. 68:7374-7385.
52. Wang, D., D. Leibowitz, and E. Kieff. 1985. An EBV membrane protein expressed in immortalised lymphocytes transforms established rodent cells. Cell 43:831-840.
53. Wang, S., M. Rowe, and E. Lundgren. 1996. Expression of the Epstein-Barr virus transforming protein LMP1 causes a rapid and transient stimulation of the bcl-2 homologue mcl-1 levels in B cell lines. Cancer Res. 56:4610-4613.
54. Young, R. L., and S. J. Korsmeyer. 1993. A negative regulatory element in the bcl-2 5′-untranslated region inhibits expression from an upstream promoter. Mol. Cell. Biol. 13:3686-3697.
55. Zong, W.-X., L. C. Edelstein, C. Chen, J. Bash, and C. Gelinas. 1999. The prosurvival Bcl-2 homolog Bfl-1/A1 is a direct transcriptional target of NF-κB that blocks TNF-α-induced apoptosis. Genes Dev. 13:382-387.