Epstein-Barr virus-encoded latent membrane protein 1 activates the JNK pathway through its extreme C terminus via a mechanism involving TRADD and TRAF2

Journal of Virology

Volumn 73, Issue 2, 1999, Pages 1023-1035

  Eliopoulos, Aristides G ^a   Blake, Sarah M S ^a   Floettmann, J Eike ^b   Rowe, Martin ^b   Young, Lawrence S ^a  

^a UNIVERSITY DEPARTMENT OF MEDICINE   (United Kingdom)

^b CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; LATENT MEMBRANE PROTEIN 1; STRESS ACTIVATED PROTEIN KINASE; TUMOR NECROSIS FACTOR RECEPTOR;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ENZYME ACTIVATION; EPSTEIN BARR VIRUS; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN INDUCTION; VIRUS GENE;

EID: 0032901776     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.73.2.1023-1035.1999     Document Type: Article

References (62)

1. Baichwal, V. R., and B. Sudgen. 1988. Transformation of Balb 3T3 cells by the BNLF1 gene of Epstein-Barr virus. Oncogene 2:461-467.
2. Brodeur, S. R., G. Cheng, D. Baltimore, and D. A. Thorley-Lawson. 1997. Localization of the major NF-κB -activating site and the sole TRAF3 binding site of LMP1 defines two distinct signaling motifs. J. Biol. Chem. 272:19777-19784.
3. Cao, Z., J. Xiong, M. Takeuchi, T. Kurama, and D. V. Goeddel. 1996. TRAF6 is a signal transducer for interleukin-1. Nature (London) 383:443-446.
4. Cheng, G., and D. Baltimore. 1996. TANK, a co-inducer with TRAF2 of TNF- and CD40L-mediated NF-κB activation. Genes Dev. 10:963-973.
5. Dawson, C. W., A. B. Rickinson, and L. S. Young. 1990. Epstein-Barr virus latent membrane protein inhibits human epithelial cell differentiation. Nature (London) 344:777-780.
6. Devergne, O., E. Hatzivassiliou, K. M. Izumi, K. M. Kaye, M. Kleijner, E. Kieff, and G. Mosialos. 1996. TRAF1, TRAF2 and TRAF3 effect NF-κB activation by an Epstein-Barr virus LMP1 domain important for B lymphocyte transformation. Mol. Cell. Biol. 16:7098-7108.
7. Eliopoulos, A. G., C. W. Dawson, G. Mosialos, J. E. Floettmann, M. Rowe, R. J. Armitage, J. Dawson, J. M. Zapata, D. J. Kerr, M. J. O. Wakelam, J. C. Reed, E. Kieff, and L. S. Young. 1996, CD40-induced growth inhibition in epithelial cells is mimicked by Epstein-Barr virus-encoded LMP1: involvement of TRAF3 as a common mediator. Oncogene 13:2243-2254.
8. Eliopoulos, A. G., and A. B. Rickinson. 1998. Epstein-Barr virus: LMP1 masquerades as an active receptor Curr. Biol. 8:R196-R198.
9. Eliopoulos, A. G., M. Stack, C. W. Dawson, K. M. Kaye, L. Hodgkin, S. Sihota, M. Rowe, and L. S. Young. 1997. Epstein-Barr virus-encoded LMP1 and CD40 mediate IL-6 production in epithelial cells via an NF-κB pathway involving TNF receptor-associated factors. Oncogene 14:2899-2916.
10. Eliopoulos, A. G., and L. S. 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.
11. Fahraeus, R., L. Rymo, J. S. Rhim, and G. Klein. 1990. Morphological transformation of human keratinocytes expressing the LMP1 gene of Epstein-Barr virus. Nature (London) 345:447-449.
12. Floettmann, J. E., A. G. Eliopoulos, M. Jones, L. S. Young, and M. Rowe. 1998. Epstein-Barr virus latent membrane protein-1 (LMP1) signaling is distinct from CD40 and involves physical cooperation of its C-terminus functional regions. Oncogene 17:2383-2393.
13. Floettmann, J. E., and M. Rowe. 1997. Epstein-Barr virus latent membrane protein-1 (LMP1) C-terminus activation region 2 (CTAR2) maps to the far C-terminus and requires oligomerization for NF-κB activation. Oncogene 15:1851-1858.
14. Floettmann, J. E., K. Ward, A. B. Rickinson, and M. Rowe. 1996. Cytostatic effect of Epstein-Barr virus latent membrane protein-1 (LMP1) analysed using tetracycline-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 A20 gene. J. Virol. 70:8653-8659.
16. Gires, O., U. Zimber-Strobl, R. Gonella, M. Ueffing, G. Marschall, R. Zeidler, D. Pich, and W. Hammerschmidt. 1997. Latent Membrane Protein 1 of Epstein-Barr virus mimics a constitutively active receptor molecule. EMBO J. 16:6131-6140.
17. Gordon, J. 1995. CD40 and its ligand: central players in B lymphocyte survival, growth and differentiation. Blood Rev. 9:53-56.
18. Hammerschmidt, W., B. Sugden, and V. R. Baichwal. 1989. The transforming domain alone of the latent membrane protein of Epstein-Barr virus is toxic to cells when expressed at high levels. J. Virol. 63:2469-2475.
19. Hatzivassilliou, E., W. E. Miller, N. Raab-Traub, E. Kieff, and G. Mosialos. 1998. A fusion of the Epstein-Barr virus latent membrane protein 1 (LMP1) transmembrane domains to the CD40 cytoplasmic domain is similar to LMP1 in constitutive activation of epidermal growth factor expression. NF-κB and stress-activated protein kinase. J. Immunol. 160:1116-1121.
20. Henderson, S., M. Rowe, C. Gregory, D. Croom-Carter, F. Wang, R. Longnecker, E. Kieff, and A. B. Rickinson. 1991. Induction of bcl-2 expression by the Epstein-Barr-virus latent membrane protein-1 protects infected B-cells from programmed cell death. Cell 65:1107-1115.
21. Herrero, J. A., P. Mathew, and C. V. Paya. 1995. LMP1 activates NF-κB by targeting the inhibitory molecule IkBa. J. Virol. 69:2168-2174.
22. Hsu, H., J. Huang, H.-B. Shu, V. Baichwal, and D. V. Goeddel. 1996. TNF-dependent recruitment of the protein kinase RIP to the TNF receptor-1 signalling complex. Immunity 4:387-396.
23. Hsu, H., H.-B. Shu, M.-G. Pan, and D. V. Goeddel. 1996. TRADD-TRAF2 and TRADD-FADD interactions define two distinct TNF receptor 1 signal transduction pathways. Cell 84:299-308.
24. Hsu, H., J. Xiong, and D. V. Goeddel. 1995. The TNF receptor 1-associated protein TRADD signals cell death and NF-κB activation. Cell 81:495-504.
25. Huen, D. S., S. A. Henderson, D. Croom-Carter, and M. Rowe. 1995. The Epstein-Barr virus latent membrane protein 1 (LMP1) mediates activation of NF-κB and cell surface phenotype via two effector regions in its carboxy-terminal cytoplasmic domain. Oncogene 10:549-560.
26. Izumi, K. M., and E. D. Kieff. 1997. The Epstein-Barr virus oncogene product latent membrane protein 1 engages the tumour necrosis factor receptor-associated death domain protein to mediate B lymphocyte growth transformation and activate NF-κB. Proc. Natl. Acad. Sci. USA 94:12592-12597.
27. Jaattela, M., H. Mouritzen, F. Elling, and L. Bastholm. 1996. A20 zinc finger protein inhibits TNF and IL-1 signaling. J. Immunol. 156:1166-1173.
28. Jefferies, W. A., J. R. Green, and A. F. Williams. 1985. Authentic T-helper CD4-(W3/25) antigen on rat peritoneal-macrophages. J. Exp. Med. 162:117-127.
29. Kaye, K. M., O. Devergne, J. N. Harada, K. M. Izumi, R. Yalamanchili, E. Kieff, and G. Mosialos. 1996. Tumour necrosis factor receptor associated factor 2 is a mediator of NF-κB activation by latent infection membrane protein 1, the Epstein-Barr Virus transforming protein. Proc. Natl. Acad. Sci. USA 93:11085-11090.
30. Kaye, K. M., K. M. Izumi, G. Mosialos, and E. Kieff. 1995. The Epstein-Barr virus LMP1 cytoplasmic carboxy terminus is essential for B-lymphocyte transformation: fibroblast cocultivation complements a critical function within the terminal 155 residues. J. Virol. 69:675-683.
31. Kieff, E. 1996. Epstein-Barr virus and its replication, p. 2343-2396. In B. C. Fields, D. M. Knipe, and P. M. Howley (ed.), Virology. Lippincott-Raven Press, New York, N. Y.
32. 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.
33. Kilger, E., A. Kieser, M. Baumann, and W. Hammerschmidt. 1998. EpsteinBarr virus-mediated B-cell proliferation is dependent upon latent membrane protein 1, which stimulates an activated CD40 receptor. EMBO J. 17:1700-1709.
34. Laherty, C. D., H. M. Hu, A. W. Opipari, F. Wang, and V. M. Dixit. 1992. The Epstein-Barr virus LMP-1 product induces A20 zinc finger protein expression by activating nuclear factor-B. J. Biol. Chem. 267:24157-24160.
35. Lee, S. Y., A. Reichlin, A. Santana, K. A. Sokol, M. C. Nussenzweig, and Y. Choi. 1997. TRAF2 is essential for JNK but not NF-κB activation and regulates lymphocyte proliferation and survival. Immunity 7:703-713.
36. Liu, Z., H. Hsu, D. V. Goeddel, and M. Karin. 1996. Dissection of TNF receptor 1 effector functions: JNK activation is not linked to apoptosis while NF-κB activation prevents cell death. Cell 87:565-576.
37. Lu, J. J.-Y., J.-Y. Chen, T.-Y. Hsu, W. C. Y. Yu, I.-J. Su, and C.-S. Yang. 1996. Induction of apoptosis in epithelial cells by Epstein-Barr virus latent membrane protein 1. J. Gen. Virol. 77:1883-1892.
38. Malinin, N. L., M. P. Boldin, A. V. Kovalenko, and D. Wallach. 1997. MAP3K-related kinase involved in NF-κB induction by TNF, CD95 and IL-1. Nature (London) 385:540-544.
39. Mercurio, F., H. Zhu, B. W. Murray, A. Shevchenko, B. L. Bennett, J. W. Li, D. B. Young, M. Barbosa, M. Mann, A. Manning, and A. Rao. 1997. IKK-1 and IKK-2: cytokine-activated IkB kinases essential for NF-κB activation. Science 278:860-866.
40. Miller, W. E., H. S. Earp, and N. Raab-Traub. 1995. The Epstein-Barr virus latent membrane protein-1 induces expression of the epidermal growth factor receptor. J. Virol. 69:4390-4398.
41. Mitchell, T., and B. Sudgen. 1995. Stimulation of NF-κB-mediated transcription by mutant derivatives of the latent membrane protein of Epstein-Barr virus. J. Virol. 69:2968-2976.
42. Moorthy, R. K., and D. A. Thorley-Lawson. 1993. All three domains of the Epstein-Barr virus-encoded latent membrane protein LMP1 are required for transformation of Rat-1 fibroblasts. J. Virol. 67:1638-1646.
43. Mosialos, G., M. Birkenbach, R. Yalamanchili, T. VanArsdale, C. Ware, and E. Kieff. 1995. The Epstein-Barr virus transforming protein LMP-1 engages signaling proteins for the tumour necrosis factor receptor family. Cell 80: 389-399.
44. Natoli, G., A. Costanzo, A. Ianni, D. J. Templeton, J. R. Woodgett, C. Balsano, and M. Levrerop. 1997. Activation of SAPK/JNK by TNF receptor 1 through a noncytotoxic TRAF2-dependent pathway. Science 275:200-203.
45. Peng, M., and E. Lundgren. 1992. Transient expression of the Epstein-Barr virus LMP1 gene in human primary B cells induces cellular activation and DNA synthesis. Oncogene 7:1775-1782.
46. Reinhard, C., B. Shamoon, V. Shyamala, and L. T. Williams. 1997. Tumour necrosis factor-α-induced activation of c-jun N-terminal kinase is mediated by TRAF2. EMBO J. 16:1080-1092.
47. Roberts, M. L., and N. R. Cooper. 1998. Activation of a Ras-MAPK-dependent pathway by Epstein-Barr virus latent membrane protein 1 is essential for cellular transformation. Virology. 240:93-99.
48. Rothe, M., V. Sarma, V. M. Dixit, and D. V. Goeddel. 1995. TRAF2-mediated activation of NF-κB by TNF receptor 2 and CD40. Science 269:1424-1427.
49. Rothe, M., J. Xiong, H.-B. Shu, K. Williamson, A. Goddard, and D. V. Goeddel. 1996. I-TRAF is a novel TRAF-interacting protein that regulates TRAF-mediated signal transduction. Proc. Natl. Acad. Sci. USA 93:8241-8246.
50. 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.
51. Rowe, M., M. Peng-Pilon, D. S. Huen, R. Hardy, D. Croom-Carter, E. Lundgren, and A. B. Rickinson. 1994. Up-regulation of bcl-2 by the Epstein-Barr virus latent membrane protein LMP1: a B-cell-specific response that is delayed relative to NF-κB activation and to induction of cell surface markers. J. Virol. 68:5602-5612.
52. Sakata, N., H. R. Patel, N. Terada, A. Aruffo, G. L. Johnson, and E. W. Gelfand. 1995. Selective activation of c-Jun kinase-activated protein kinase by CD40 on human B cells. J. Biol. Chem. 270:30823-30828.
53. Sandberg, M., W. Hammerschmidt, and B. Sudgen. 1997. Characterization of LMP1's association with TRAF1, TRAF2, and TRAF3. J. Virol. 71:4649-4656.
54. Shu, H.-B., M. Takeuchi, and D. V. Goeddel. 1996. The tumor necrosis factor receptor 2 signal transducers TRAF2 and c-IAP1 are components of the tumor necrosis factor receptor 1 signaling complex. Proc. Natl. Acad. Sci. USA 93:13973-13978.
55. Song, H. Y., C. H. Regnier, C. J. Kirschning, D. V. Goeddel, and M. Rothe. 1997. Tumour necrosis factor (TNF)-mediated kinase cascades: bifurcation of nuclear factor-kB and c-jun N-terminal kinase (JNK/SAPK) pathways at TNF receptor-associated factor 2. Proc. Natl. Acad. Sci. USA 94:9792-9796.
56. Song, H. Y., M. Rothe, and D. V. Goeddel. 1996. The tumour necrosis factor-inducible zinc finger protein A20 interacts with TRAF1/TRAF2 and inhibits NF-κB activation. Proc. Natl. Acad. Sci. USA 93:6721-6725.
57. Sylla, B. S., S. C. Hung, D. M. Davidson, E. Hatzivassiliou, N. L. Malinin, D. Wallach, T. D. Gilmore, E. Kieff, and G. Mosialos. 1998. Epstein-Barr virus-transforming protein latent infection membrane protein 1 activates transcription factor NF-κB through a pathway that includes the NF-κB-inducing kinase and the IκB kinases IKKα and IKKβ. Proc. Natl. Acad. Sci. USA 95:10106-10111.
58. Wang, D., D. Liebowitz, and E. Kieff. 1985. An EBV membrane protein expressed in immortalized lymphocytes transforms established rodent cells. Cell 43:831-840.
59. Woronicz, J. D., X. Gao, M. Rothe, and D. V. Goeddel. 1997 IκB kinase-β: NF-κB activation and complex formation with IkB kinase-a and NIK. Science 278:866-869.
60. Yeh, W.-C., A. Shahinian, D. Speiser, J. Kraunus, F. Billia, A. Wakeham, J. L. de la Pompa, D. Ferrick, B. Hum, N. Iscove, P. Ohashi, M. Rothe, D. V. Goeddel, and T. W. Mak. 1997. Early lethality, functional NF-κB activation and increased sensitivity to TNF-induced cell death in TRAF2-deficient mice. Immunity 7:715-725.
61. Young, L. S., C. W. Dawson, and A. G. Eliopoulos. 1997. Viruses and apoptosis. Br. Med. Bull. 53:509-521.
62. Young, L. S., and M. Rowe. 1992. Epstein-Barr virus, lymphomas and Hodgkin's disease. Semin. Cancer Biol. 3:273-284.