Epstein-Barr virus regulates c-MYC, apoptosis, and tumorigenicity in Burkitt lymphoma

Molecular and Cellular Biology

Volumn 19, Issue 3, 1999, Pages 1651-1660

  Ruf, Ingrid K ^a   Rhyne, Paul W ^a   Yang, Hui ^a   Borza, Corina M ^b   Hutt Fletcher, Lindsey M ^b   Cleveland, John L ^a,c   Sample, Jeffery T ^a,c  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^b UNIVERSITY OF MISSOURI KANSAS CITY   (United States)

^c UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOPTOSIS; ARTICLE; B LYMPHOCYTE; BURKITT LYMPHOMA; EPSTEIN BARR VIRUS; HUMAN; HUMAN CELL; ONCOGENE C MYC; PRIORITY JOURNAL; VIRUS CARCINOGENESIS; VIRUS CELL INTERACTION; VIRUS LATENCY;

DNA VIRUSES; HUMAN HERPESVIRUS 4;

EID: 0032980719     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.19.3.1651     Document Type: Article

References (61)

1. Adams, J. M., A. W. Harris, C. A. Pinkert, L. M. Corcoran, W. S. Alexander, S. Cory, R. D. Palmiter, and R. L. Brinster. 1985. The c-myc oncogene driven by immunoglobulin enhancers induces lymphoid malignancy in transgenic mice. Nature 318:533-538.
2. Arrand, J. R., and L. Rymo. 1982. Characterization of the major Epstein-Barr virus-specific RNA in Burkitt lymphoma-derived cells. J. Virol. 41:376-389.
3. Askew, D. S., R. A. Ashmun, B. C. Simmons, and J. L. Cleveland. 1991. Constitutive c-myc expression in an IL-3-dependent myeloid cell line suppresses cell-cycle arrest and accelerates apoptosis. Oncogene 6:1915-1922.
4. Borza, C. M., and L. M. Hutt-Fletcher. 1998. Epstein-Barr virus recombinant lacking expression of glycoprotein gp150 infects B cells normally but is enhanced for infection of the epithelial cells. J. Virol. 72:7577-7582.
5. Brooks, L., Q. Y. Yao, A. B. Rickinson, and L. S. Young. 1992. Epstein-Barr virus latent gene transcription in nasopharyngeal carcinoma cells: coexpression of EBNA1, LMP1, and LMP2 transcripts. J. Virol. 66:2689-2697.
6. Brooks, L. A., A. L. Lear, L. S. Young, and A. B. Rickinson. 1993. Transcripts from the Epstein-Barr virus BamHI A fragment are detectable in all three forms of virus latency. J. Virol. 67:3182-3190.
7. Chen, F., J. Z. Zou, L. di Renzo, G. Winberg, L. F. Hu, E. Klein, G. Klein, and I. Ernberg. 1995. A subpopulation of normal B cells latently infected with Epstein-Barr virus resembles Burkitt lymphoma cells in expressing EBNA-1 but not EBNA-2 or LMP-1. J. Virol. 69:3752-3758.
8. 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.
9. Chodosh, J., V. P. Holder, Y. Gan, A. Belgaumi, J. Sample, and J. W. Sixbey. 1998. Eradication of latent Epstein-Barr virus by hydroxyurea alters the growth-transformed cell phenotype. J. Infect. Dis. 177:1194-1201.
10. Clarke, P. A., M. Schwemmle, J. Schickinger, K. Hilse, and M. J. Clemens. 1991. Binding of Epstein-Barr virus small RNA EBER-1 to the double-stranded RNA-activated protein kinase DAI. Nucleic Acids Res. 19:243-248.
11. Deacon, E. M., G. Pallesen, G. Niedobitek, J. Crocker, L. Brooks, A. B. Rickinson, and L. S. Young. 1993. Epstein-Barr virus and Hodgkin's disease: transcriptional analysis of virus latency in the malignant cells. J. Exp. Med. 177:339-349.
12. Evan, G., C. S. Wyllie, C. S. Gilbert, H. Land, M. Brooks, T. Littlewood, C. Waters, and D. Hancock. 1992. Induction of apoptosis in fibroblasts by c-myc protein. Cell 69:119-128.
13. Evan, G. I., G. K. Lewis, G. Ramsay, and J. M. Bishop. 1985. Isolation of monoclonal antibodies specific for human c-myc proto-oncogene product. Mol. Cell. Biol. 5:3610-3616.
14. Fahraeus, R., H. Li-Fu, I. Ernberg, J. Finke, M. Rowe, G. Klein, K. Falk, E. Nilsson, M. Yadaf, P. Busson, T. Tursz, and B. Kallin. 1988. Expression of the Epstein-Barr virus genome in nasopharyngeal carcinoma. Int. J. Cancer 42:329-338.
15. Farrell, P. J., G. J. Allan, F. Shanathan, K. H. Vousden, and T. Crook. 1991. p53 is frequently mutated in Burkitt's lymphoma cell lines. EMBO J. 10: 2879-2887.
16. Fries, K. L., W. E. Miller, and N. Raab-Traub. 1996. Epstein-Barr virus latent membrane protein 1 blocks p53-mediated apoptosis through induction of the A20 gene. J. Virol. 70:8653-8659.
17. Fries, K. L., T. B. Sculley, J. Webster-Cyriaque, P. Rajadurai, R. H. Sadler, and N. Raab-Traub. 1997. Identification of a novel protein encoded by the BamHI A region of the Epstein-Barr virus. J. Virol. 71:2765-2771.
18. 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.
19. 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 genes protects human B cells from death by apoptosis. Nature 349:612-614.
20. Hann, S. R., and R. N. Eisenman. 1984. Proteins encoded by the human c-myc oncogene: differential expression in neoplastic cells. Mol. Cell. Biol. 4:2486-2497.
21. Henderson, S., M. Rowe, C. Gregory, D. Croom-Carter, F. Wang, R. Longnecker, E. Kieff, and A. 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.
22. Herbst, H., F. Dallenbach, M. Hummel, G. Niedobitek, S. Pileri, N. Muller-Lantzsch, and H. Stein. 1991. Epstein-Barr virus latent membrane protein expression in Hodgkin and Reed-Sternberg cells. Proc. Natl. Acad. Sci. USA 88:4766-4770.
23. Khanna, R., S. R. Burrows, M. G. Kurilla, C. A. Jacob, I. S. Misko, T. B. Sculley, E. Kieff, and D. J. Moss. 1992. Localization of Epstein-Barr virus cytotoxic T cell epitopes using recombinant vaccinia: implications for vaccine development. J. Exp. Med. 176:160-176.
24. Kieff, E. 1996. Epstein-Barr virus and its replication, p. 2343-2396. In B. N. Fields et al. (ed.), Fields virology, 3rd ed., vol 2. Raven Press, New York, N.Y.
25. Koromilas, A. E., S. Roy, G. N. Barber, M. G. Katze, and N. Sonenberg. 1992. Malignant transformation by a mutant of the IFN-inducible dsRNA-dependent protein kinase. Science 257:1685-1689.
26. Lacy, J., W. P. Summers, M. Watson, P. M. Glazer, and W. C. Summers. 1987. Amplification and deregulation of MYC following Epstein-Barr virus infection of a human B-cell line. Proc. Natl. Acad. Sci. USA 84:5838-5842.
27. Lacy, J., W. P. Summers, and W. C. Summers. 1989. Post-transcriptional mechanisms of deregulation of MYC following conversion of a human B cell line by Epstein-Barr virus. EMBO J. 8:1973-1980.
28. Laherty, C. D., H. M. Hu, A. W. Opipari, F. Wang, and V. M. Dixit. 1992. The Epstein-Barr virus LMP1 gene product induces A20 zinc finger protein expression by activating NF-κB. J. Biol. Chem. 267:24157-24160.
29. Magrath, I. 1990. The pathogenesis of Burkitt's lymphoma. Adv. Cancer. Res. 55:133-270.
30. 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.
31. Masucci, M., and I. Ernberg. 1994. Epstein-Barr virus: adaptation to a life within the immune system. Trends Microbiol. 2:125-130.
32. Meurs, E. F., J. Galabru, G. N. Barber, M. G. Katze, and A. G. Hovanessian. 1993. Tumor suppressor function of the interferon-induced double-stranded RNA-activated protein kinase. Proc. Natl. Acad. Sci. USA 90:232-236.
33. Miller, A. D., and G. Rosman. 1989. Improved retroviral vectors for gene transfer and expression. BioTechniques 7:980-990.
34. 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.
35. Milner, A. E., R. J. A. Grand, C. M. Waters, and C. D. Gregory. 1993. Apoptosis in Burkitt lymphoma cells is driven by c-myc. Oncogene 8:3385-3391.
36. Miyashita, E. M., B. Yang, K. M. C. Lam, D. H. Crawford, and D. A. Thorley-Lawson. 1995. A novel form of Epstein-Barr virus latency in normal B cells in vivo. Cell 80:593-601.
37. Miyashita, E. M., B. Yang, G. J. Babcock, and D. A. Thorley-Lawson. 1997. Identification of the site of Epstein-Barr virus persistence in vivo as a resting B cell. J. Virol. 71:4882-4891.
38. Murray, R., M. Kurilla, J. Brooks, W. Thomas, M. Rowe, E. Kieff, and A. Rickinson. 1992. Identification of target antigens for the human cytotoxic T cell response to Epstein-Barr virus (EBV): implications for the immune control of EBV positive malignancies. J. Exp. Med. 176:157-168.
39. Nonkwelo, C., E. B. D. Henson, and J. Sample. 1995. Characterization of the Epstein-Barr virus Fp promoter. Virology 206:183-195.
40. Packham, G., and J. L. Cleveland. 1995. c-Myc and apoptosis. Biochim. Biophys. Acta 1242:11-28.
41. Pallesen, G., S. J. Hamilton-Dutoit, M. Rowe, and L. S. Young. 1991. Expression of Epstein-Barr virus latent gene products in tumour cells of Hodgkin's disease. Lancet 337:320-322.
42. Qu, L., and D. T. Rowe. 1992. Epstein-Barr virus latent gene expression in uncultured peripheral blood lymphocytes. J. Virol. 66:3715-3724.
43. Rickinson, A. B., and E. Kieff. 1996. Epstein-Barr virus, p. 2397-2446. In B. N. Fields et al. (ed.), Fields virology, 3rd ed., vol. 2. Raven Press, New York, N.Y.
44. Robertson, E. S., B. Tomkinson, and E. Kieff. 1994. An Epstein-Barr virus with a 58-kilobase-pair deletion that includes BARF0 transforms B lymphocytes in vitro. J. Virol. 68:1449-1458.
45. Rooney, C. M., C. D. Gregory, M. Rowe, S. Finerty, C. Edwards, H. Rupani, and A. B. Rickinson. 1986. Endemic Burkitt's lymphoma: phenotypic analysis of tumor biopsy cells and of derived tumor cell lines. J. Natl. Cancer Inst. 77:681-687.
46. Rowe, D. T., M. Rowe, G. I. Evan, L. E. Wallace, P. J. Farrell, and A. B. Rickinson. 1986. Restricted expression of EBV latent genes and T-lymphocyte-detected membrane antigen in Burkitt's lymphoma cells. EMBO J. 5:2599-2607.
47. 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 the Epstein-Barr virus latent membrane protein LMP1: a B-cell-specific response that is delayed relative to NFκB activation and to induction of cell surface markers. J. Virol. 68:5602-5612.
48. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
49. Sample, J., and E. Kieff. 1990. Transcription of the Epstein-Barr virus genome during latency in growth-transformed lymphocytes. J. Virol. 64:1667-1674.
50. Sample, J., E. B. D. Henson, and C. Sample. 1992. The Epstein-Barr virus nuclear protein 1 promoter active in type I latency is autoregulated. J. Virol. 66:4654-4661.
51. Sharp, T. V., M. Schwemmle, I. Jeffrey, K. Laing, H. Mellor, C. G. Proud, K. Hilse, and M. J. Clemens. 1993. Comparative analysis of the regulation of the interferon-inducible protein kinase PKR by Epstein-Barr virus RNAs EBER-1 and EBER-2 and adenovirus VAI RNA. Nucleic Acids Res. 21: 4483-4490.
52. Shimizu, N., A. Tanabe-Tochikura, Y. Kuroiwa, and K. Takada. 1994. Isolation of Epstein-Barr virus (EBV)-negative cell clones from the EBV-positive Burkitt's lymphoma (BL) line Akata: malignant phenotypes of BL cells are dependent on EBV. J. Virol. 68:6069-6073.
53. Smith, P., and B. Griffin. 1991. Differential expression of Epstein-Barr viral transcripts for two proteins (TP1 and LMP) in lymphocyte and epithelial cells. Nucleic Acids Res. 19:2435-2440.
54. Swaminathan, S., B. Tomkinson, and E. Kieff. 1991. Recombinant Epstein-Barr virus with small RNA (EBERS) genes deleted transforms lymphocytes and replicates in vitro. Proc. Natl. Acad. Sci. USA 88:1546-1550.
55. Takada, K., and Y. Ono. 1989. Synchronous and sequential activation of latently infected Epstein-Barr virus genomes. J. Virol. 63:445-449.
56. Thorley-Lawson, D. A., E. M. Miyashita, and G. Khan. 1996. Epstein-Barr virus and the B cell: that's all it takes. Trends Microbiol. 4:204-208.
57. 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.
58. Toczyski, D. P., A. G. Matera, D. C. Ward, and J. A. Steitz. 1994. The Epstein-Barr virus (EBV) small RNA EBER1 binds and relocalizes ribosomal protein L22 in EBV-infected human B lymphocytes. Proc. Natl. Acad. Sci. USA 91:3463-3467.
59. Wilson, J. B., and A. J. Levine. 1992. The oncogenic potential of Epstein-Barr virus nuclear antigen 1 in transgenic mice. Curr. Top. Microbiol. Immunol. 182:325-384.
60. Wilson, J. B., J. L. Bell, and A. J. Levine. 1996. Expression of Epstein-Barr virus nuclear antigen-1 induces B cell neoplasia in transgenic mice. EMBO J. 15:3117-3126.
61. Young, L. S., C. W. Dawson, D. Clark, H. Rupani, P. Busson, T. Tursz, A. Johnson, and A. B. Rickinson. 1988. Epstein-Barr virus gene expression in nasopharyngeal carcinoma. J. Gen. Virol. 69:1051-1065.