Control of cell cycle entry and apoptosis in B lymphocytes infected by Epstein-Barr virus

Journal of Virology

Volumn 73, Issue 6, 1999, Pages 4678-4688

  Spender, Lindsay C ^a   Cannell, Emma J ^a,c   Hollyoake, Martine ^a   Wensing, Barbara ^a   Gawn, Jonathan M ^a   Brimmell, Matthew ^a   Packham, Graham ^a,b   Farrell, Paul J ^a,b  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b IMPERIAL COLLEGE SCHOOL OF MEDICINE   (United Kingdom)

^c INSTITUTE OF CANCER RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENT COMPONENT C3D RECEPTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN BCL 2;

APOPTOSIS; ARTICLE; B LYMPHOCYTE; CELL ACTIVATION; CELL CYCLE; CELL IMMORTALIZATION; EPSTEIN BARR VIRUS; GENE EXPRESSION SYSTEM; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; VIRUS INFECTION; VIRUS REPLICATION;

EID: 0032990331     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.73.6.4678-4688.1999     Document Type: Article

References (87)

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., G. J. Inman, D. H. Crawford, and P. J. Farrell. 1995. DNA damage in human B cells can induce apoptosis, proceeding from G1/S when p53 is transactivation competent and G2/M when it is transactivation defective. EMBO J. 14:4994-5005.
3. Ashkenazi, A., and V. Dixit. 1998. Death receptors: signaling and modulation. Science 281:1305-1308.
4. 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.
5. Beijersbergen, R. L., R. M. Kerkhoven, L. Zhu, L. Carlee, P. M. Voorhoeve, and R. Bernards. 1994. E2F-4, a new member of the E2F gene family, has oncogenic activity and associates with p107 in vivo. Genes Dev. 8:2680-2690.
6. Ben-Bassat, H., N. Goldblum, S. Mitrani, T. Goldblum, J. M. Yoffey, M. M. Cohen, Z. Bentwich, B. Ramot, E. Klein, and G. Klein. 1977. Establishment in continuous culture of a new type of lymphocyte from a "Burkitt like" malignant lymphoma (line D.G.-75). Int. J. Cancer 19:27-33.
7. Boise, L. H., M. Gonzalez-Garcia, C. E. Postema, L. Ding, T. Lindsten, L. A. Turka, X. Mao, G. Nunez, and C. B. Thompson. 1993. bcl-x, a bcl-2-related gene that functions as a dominant regulator of apoptotic cell death. Cell 74: 597-608.
8. Bonnefoy-Berard, N., L. Genestier, M. Flacher, and J. P. Revillard. 1994. The phosphoprotein phosphatase calcineurin controls calcium-dependent apoptosis in B cell lines. Eur. J. Immunol. 24:325-329.
9. Brimmell, M., R. Mendiola, J. Mangion, and G. Packham. 1998. BAX frameshift mutations in cell lines derived from human haemopoetic malignancies are associated with resistance to apoptosis and microsatellite instability. Oncogene 16:1803-1812.
10. Brodeur, S., G. Cheng, D. Baltimore, and D. Thorley-Lawson. 1997. Localization of the major NF-kappa B activating site and the sole TRAF3 binding site of LMP-1 defines two distinct signaling motifs. J. Biol. Chem. 272: 19777-19784.
11. Brooks, A., D. Shiffman, C. Chan, E. Brooks, and P. Milner. 1996. Functional analysis of the human cyclin D2 and D3 promoters. J. Biol. Chem. 271: 9090-9099.
12. Cannell, E., P. Farrell, and A. Sinclair. 1996. Epstein-Barr virus exploits the normal cell pathway to regulate Rb activity during the immortalisation of primary B cells. Oncogene 13:1413-1421.
13. Chittenden, T., E. A. Harrington, R. O'Connor, C. Flemington, R. J. Lutz, G. I. Evan, and B. C. Guild. 1995. Induction of apoptosis by the Bcl-2 homologue. Bak. Nature 374:733-736.
14. Chiu, V. K., C. M. Walsh, C. C. Liu, J. C. Reed, and W. R. Clark. 1995. Bcl-2 blocks degranulation but not fas-based cell-mediated cytotoxicity. J. Immunol. 154:2023-2032.
15. Cludts, I., and P. Farrell. 1998. Multiple functions within the Epstein-Barr virus EBNA-3A protein. J. Virol. 72:1862-1869.
16. Cory, S. 1995. Regulation of lymphocyte survival by the bcl-2 gene family. Annu. Rev. Immunol. 13:513-543.
17. Craig, R. W. 1995. The bcl-2 gene family. Semin. Cancer Biol. 6:35-43.
18. Debatin, K. M., and P. H. Krammer. 1995. Resistance to APO-1 (CD95) induced apoptosis in T-ALL is determined by a BCL-2 independent anti-apoptotic program. Leukemia 9:815-820.
19. Devergne, O., E. Hatzivassiliou, K. M. Izumi, K. M. Kaye, M. F. Kleijnen, E. Kieff, and G. Mosialos. 1996. Association of TRAF1, TRAF2, and TRAF3 with an Epstein-Barr virus LMP1 domain important for B-lymphocyte transformation: role in NF-κB activation. Mol. Cell. Biol. 16:7098-7108.
20. Eliopoulos, A., and L. Young. 1998. Activation of the cJun N-terminal kinase (JNK) pathway by the Epstein-Barr virus-encoded latent membrane protein 1 (LMP1). Oncogene 16:1731-1742.
21. Falk, M. H., B. C. Trauth, K. M. Debatin, C. Klas, C. D. Gregory, A. B. Rickinson, A. Calender, G. M. Lenoir, J. W. Ellwart, P. H. Krammer, and G. Bornkamm. 1992. Expression of the APO-1 antigen in Burkitt lymphoma cell lines correlates with a shift towards a lymphoblastoid phenotype. Blood 79: 3300-3306.
22. Farrell, P. 1995. Epstein-Barr virus immortalizing genes. Trends Microbiol. 3:105-109.
23. Farrell, P. 1998. Signal transduction from the Epstein-Barr virus LMP-1 transforming protein. Trends Microbiol. 6:175-177.
24. Farrow, S. N., J. H. White, I. Martinou, T. Raven, K. T. Pun, C. J. Grinham, J. C. Martinou, and R. Brown. 1995. Cloning of a bcl-2 homologue by interaction with adenovirus E1B 19K. Nature 374:731-733.
25. 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. Viral. 61:3870-3878.
26. 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.
27. 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.
28. 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.
29. Hollyoake, M., A. Stühler, P. J. Farrell, J. Gordon, and A. J. Sinclair. 1995. The normal cell cycle activation program is exploited during the infection of quiescent B lymphocytes by Epstein-Barr virus. Cancer Res. 55:4784-4787.
30. Itoh, N., Y. Tsujimoto, and S. Nagata. 1993. Effect of bcl-2 on Fas antigenmediated cell death. J. Immunol. 151:621-627.
31. Izumi, K., and E. Kieff. 1997. The EBV oncogene product LMP-1 engages the TRADD protein to mediate B lymphocyte growth transformation and activate NF-κB. Proc. Natl. Acad. Sci. USA 94:12592-12597.
32. Kelly, K., and K. A. Knox. 1995. Differential regulatory effects of cAMP-elevating agents on human normal and neoplastic B cell functional response following ligation of surface immunoglobulin and CD40. Cell. Immunol. 166: 93-102.
33. Kempkes, B., D. Spitkovsky, P. Jansen-Durr, J. W. Ellwart, E. Kremmer, H. J. Delecluse, C. Rottenberger, G. W. Bornkamm, and W. Hammerschmidt. 1995. B-cell proliferation and induction of early G1-regulating proteins by Epstein-Barr virus mutants conditional for EBNA2. EMBO J. 14: 88-96.
34. Kiefer, M. C., M. J. Brauer, V. C. Powers, J. J. Wu, S. R. Umansky, L. D. Tomei, and P. J. Barr. 1995. Modulation of apoptosis by the widely distributed Bcl-2 homologue Bak. Nature 374:736-739.
35. Kieser, A., E. Kilger, O. Gires, M. Ueffing, W. Kolch, and W. Hammerschmidt. 1997. Epstein-Barr virus latent membrane protein-1 triggers AP-1 activity via the c-Jun N-terminal kinase cascade. EMBO J. 16:6478-6485.
36. Kilger, E., A. Kieser, M. Baumann, and W. Hammerschmidt. 1998. Epstein-Barr virus-mediated B-cell proliferation is dependent upon latent membrane protein I, which simulates an activated CD40 receptor. EMBO J. 17:1700-1709.
37. King, W., A. L. Thomas-Powell, N. Raab-Traub, M. Hawke, and E. Kieff. 1980. Epstein-Barr virus RNA. V. Viral RNA in a restringently infected, growth-transformed cell line. J. Virol. 36:506-518.
38. Klein, G., and L. Dombos. 1973. Relationship between the sensitivity of EBV-carrying lymphoblastoid lines to superinfection and the inducibility of the resident viral genome. Int. J. Cancer 11:327-337.
39. Krikos, A., C. Laherty, and V. Dixit. 1992. Transcriptional activation of the tumor necrosis factor inducible zinc finger protein A20 is mediated by κB elements. J. Biol. Chem. 267:17971-17976.
40. 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 nuclear factor kappa B. J. Biol. Chem. 267:24157-24160.
41. Lenoir, G., M. Vuillaume, and C. Bonnardel. 1985. The use of lymphomatous and lymphoblastoid cell lines in the study of Burkitt's lymphoma, p. 309-318. In G. Lenoir, G. O'Conor, and C. Olweny (ed.), Burkitt's lymphoma: a human cancer model. IARC Publications, Lyon, France.
42. Mann, K. P., D. Staunton, and D. A. Thorley-Lawson. 1985. Epstein-Barr virus-encoded protein found in plasma membrane in transformed cells. J. Virol. 55:710-720.
43. Meijerink, J. P., T. F. Smetsers, A. W. Sloetjes, E. H. Linders, and E. J. Mensink. 1995. Bax mutations in cell lines derived from hematological malignancies. Leukemia 9:1828-1832.
44. Memon, S. A., M. B. Moreno, D. Petrak, and C. M. Zacharchuk. 1995. Bcl-2 blocks glucocorticoid- but not Fas- or activation-induced apoptosis in a T cell hybridoma. J. Immunol. 155:4644-4652.
45. 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.
46. Moberg, K., M. Starz, and J. Lees. 1996. E2F-4 switches from p130 to p107 and pRb in response to cell cycle reentry. Mol. Cell. Biol. 16:1436-1449.
47. Moreno, M. B., S. A. Memon, and C. M. Zacharchuk. 1996. Apoptosis signaling pathways in normal T cells: differential activity of Bcl-2 and IL-1 beta-converting enzyme family protease inhibitors on glucocorticoid- and Fas-mediated cytotoxicity. J. Immunol. 157:3845-3849.
48. Mosialos, G., M. Birkenbach, R. Yalamanchili, T. VanArsdale, C. Ware, and E. Kieff. 1995. The Epstein-Barr virus transforming protein LMP1 engages signaling proteins for the tumor necrosis factor receptor family. Cell 80: 389-399.
49. Oltvai, Z. N., and S. J. Korsmeyer. 1994. Checkpoints of dueling dimers foil death wishes. Cell 79:189-192.
50. Oltrai, Z. N., C. L. Milliman, and S. J. Korsmeyer. 1993. Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell 74:609-619.
51. Opipari, A., M. Boguski, and V. Dixit. 1990. The A20 cDNA induced by tumor necrosis factor alpha encodes a novel type of zinc finger protein. J. Biol. Chem. 265:14705-14708.
52. Opipari, A., Jr., H. M. Hu, R. Yabkowitz, and V. M. Dixit 1992. The A20 zinc finger protein protects cells from tumor necrosis factor cytotoxicity. J. Biol. Chem. 267:12424-12427.
53. Owen-Schaub, L. B., R. Radinsky, E. Kruzel, K. Berry, and S. Yonehara. 1994. Anti-Fas on nonhematopoietic tumors: levels of Fas/APO-1 and bcl-2 are not predictive of biological responsiveness. Cancer Res. 54: 1580-1586.
54. Packham, G., M. Brimmell, and J. Cleveland. 1997. Mammalian cells express two differently localized Bag-1 isoforms generated by alternative translation initiation. Biochem. J. 328:808-813.
55. Packham, G., J. Lahti, B. Fee, J. Gawn, E. Coustan-Smith, D. Campana, L. Douglas, V. Kidd, S. Ghosh, and J. Cleveland. 1997. Fas activates NF-κB and induces apoptosis in T cell lines by signaling pathways distinct from those activated by TNF-α. Cell Death Differ. 4:130-139.
56. Pagano, M., S. Tarn, A. Theodoras, P. Beer-Romero, G. Sal, V. Chau, P. Yew, G. Draetta, and M. Rolfe. 1995. Role of the ubiquitin-proteasome pathway in regulating abundance of the cyclin dependent kinase inhibitor p27. Science 269:682-685.
57. Parker, G., R. Touitou, and M. Allday. Submitted for publication.
58. Pulvertaft, R 1965. A study of malignant tumours in Nigeria in short term tissue culture. J. Clin. Pathol. 18:261-273.
59. Reed, J. 1997. Double identity for proteins of the Bcl-2 family. Nature 387: 773-776.
60. Reed, J. C., T. Mijashita, S. Takayama, H. G. Wang, T. Sato, S. Krajewski, C. Aime-Sempe, S. Bodrug, S. Kitada, and M. Hanada. 1996. BCL-2 family proteins: regulators of cell death involved in the pathogenesis of cancer and resistance to therapy. J. Cell. Biochem. 60:23-32.
61. Reynolds, J. E., T. Yang, L. Qian, J. D. Jenkinson, P. Zhou, A. Eastman, and R. W. Craig. 1994. Mcl-1, a member of the Bcl-2 family, delays apoptosis induced by c-Myc overexpression in Chinese hamster ovary cells. Cancer Res. 54:6348-6352.
62. Rickinson, A. B., and E. Kieff. 1996. Epstein-Barr Virus, p. 2397-2446. In B. N. Fields, P. M. Knipe, and P. M. Howley (ed.), Fields virology. Lippincott-Raven, Philadelphia, Pa.
63. Rowe, M., D. T. Rowe, C. D. Gregory, L. S. Young, P. J. Farrell, H. Rupani, and A. B. Rickinson. 1987. Differences in B cell growth phenotype reflect novel patterns of Epstein-Barr virus latent gene expression in Burkitt's lymphoma cells. EMBO J. 6:2743-2751.
64. Saegusa, M., Y. Takano, M. Hashimura, Y. Shoji, and I. Okayasu. 1995. The possible role of bcl-2 expression in the progression of tumors of the ulerine cervix. Cancer 76:2297-2303.
65. Sandberg, M., W. Hammerschmidt, and B. Sugden. 1997. Characterization of LMP1's association with TRAF1, TRAF2, and TRAF3. J. Virol. 71: 4649-4656.
66. Sardet, C., L. LeCam, E. Fabrizio, and M. Vidal. 1997. E2Fs and the retinoblastoma protein family, p. 1-57. In M. Yaniv and J. Ghysdael (ed.), Oncogenes as transcriptional regulators. Birkhauser Verlag, Basel, Switzerland.
67. Sarma, V., Z. Lin, L. Clark, B. M. Rust, M. Tewari, R. J. Noelle, and V. M. Dixit. 1995. Activation of the B-cell surface receptor CD40 induces A20, a novel zinc finger protein that inhibits apoptosis. J. Biol. Chem. 270:12343-12346.
68. Sato, T., M. Hanada, S. Bodrug, S. Irie, N. Iwama, L. H. Boise, C. B. Thompson, E. Golemis, L. Fong, H. G. Wang, and J. C. Reed. 1994. Interactions among members of the Bcl-2 protein family analyzed with a yeast two-hybrid system. Proc. Natl. Acad. Sci. USA 91:9238-9242.
69. Sedlak, T. W., Z. N. Oltvai, E. Yang, K. Wang, L. H. Boise, C. B. Thompson, and S. J. Korsmeyer. 1995. Multiple Bcl-2 family members demonstrate selective dimerizations with Bax. Proc. Natl. Acad. Sci. USA 92:7834-7838.
70. Sheaff, R. J., M. Groudine, M. Gordon, J. M. Roberts, and B. E. Clurman. 1997. Cyclin E-CDK2 is a regulator of p27Kip1. Genes Dev. 11:1464-1478.
71. Shima, Y., N. Nishimoto, A. Ogata, Y. Fujii, K. Yoshizaki, and T. Kishimoto. 1995. Myeloma cells express Fas antigen/APO-1 (CD95) but only some are sensitive to anti-Fas antibody resulting in apoptosis. Blood 85:757-764.
72. Sinclair, A. J., and P. J. Farrell. 1995. Host cell requirements for efficient infection of quiescent primary B lymphocytes by Epstein-Barr virus. J. Virol. 69:5461-5468.
73. Sinclair, A. J., I. Palmero, G. Peters, and P. J. Farrell. 1994, EBNA-2 and EBNA-LP cooperate to cause G0 to G1 transition during immortalization of resting human B lymphocytes by Epstein-Barr virus. EMBO J. 13:3321-3328.
74. 1 cell state. Mol. Cell. Biol. 16:6965-6976.
75. Strobel, T., L. Swanson, S. Korsmeyer, and S. Cannistra. 1997. Radiation-induced apoptosis is not enhanced by expression of either p53 or BAX in SW626 ovarian cancer cells. Oncogene 14:2753-2758.
76. Sugano, N., W. Chen, M. Roberts, and N. Cooper. 1997. Epstein-Barr virus binding to CD21 activates the initial viral promoter via NF-kappa B induction. J. Exp. Med. 186:731-737.
77. 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.
78. Takayama, S., T. Sato, S. Krajewski, K. Kochel, S. Irie, J. A. Millan, and J. C. Reed. 1995. Cloning and functional analysis of BAG-1: a novel Bcl-2-binding protein with anti-cell death activity. Cell 80:279-284.
79. Vairo, G., D. Livingston, and D. Ginsberg. 1995. Functional interaction between E2F-4 and p130: evidence for distinct mechanisms underlying growth suppression by different retinoblastoma protein family members. Genes Dev. 9:869-881.
80. 0 to S phase transition in human primary B lymphocytes. J. Biol. Chem., in press.
81. Vlach, J., S. Hennecke, and B. Amati. 1997. Phosphorylation-dependent degradation of the cyclin-dependent kinase inhibitor p27. EMBO J. 16: 5334-5344.
82. Wang, H., R. J. Grand, A. E. Milner, R. J. Armitage, J. Gordon, and C. D. Gregory. 1996. Repression of apoptosis in human B-lymphoma cells by CD40-ligand and Bcl-2: relationship to the cell-cycle and role of the retinoblastoma protein. Oncogene 13:373-379.
83. Wilson, G., and G. Miller. 1979. Recovery of Epstein-Barr virus from non-producer neonatal human lymphoid cell transformants. Virology 95:351-358.
84. Yang, E., and S. J. Korsmeyer. 1996. Molecular thanatopsis: a discourse on the BCL2 family and cell death. Blood 88:386-401.
85. Yang, E., J. Zha, J. Jockel, L. H. Boise, C. B. Thompson, and S. J. Korsmeyer. 1995. Bad, a heterodimeric partner for Bcl-XL and Bcl-2, displaces Bax and promotes cell death. Cell 80:285-291.
86. Yin, X., Z. Oltvai, and S. Korsmeyer. 1994. BH1 and BH2 domains of Bcl-2 are required for inhibition of apoptosis and heterodimerization with Bax. Nature 369:321-323.
87. Zha, H., C. Aime-Sempe, T. Sato, and J. C. Reed. 1996. Proapoptotic protein Bax heterodimerizes with Bcl-2 and homodimerizes with Bax via a novel domain (BH3) distinct from BH1 and BH2, J. Biol. Chem. 271:7440-7444.