EBV latent membrane protein 1 is a negative regulator of TLR9

Journal of Immunology

Volumn 185, Issue 11, 2010, Pages 6439-6447

  Fathallah, Ikbal ^a   Parroche, Peggy ^a,b,c   Gruffat, Henri ^b,c   Zannetti, Claudia ^a,b,c   Johansson, Hanna ^a   Yue, Jiping ^a   Manet, Evelyn ^c,d   Tommasino, Massimo ^a   Sylla, Bakary S ^a   Hasan, Uzma A ^a,b,c  

^a INTERNATIONAL AGENCY FOR RESEARCH ON CANCER   (France)

^b INSERM U851   (United States)

^c Institut Federatif de Recherche Cardiovasculaire   (France)

^d CENTRE INTERNATIONAL DE RECHERCHE EN INFECTIOLOGIE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IMMUNOGLOBULIN G; INTERLEUKIN 6; LATENT MEMBRANE PROTEIN 1; LUCIFERASE; MESSENGER RNA; ONCOPROTEIN; TOLL LIKE RECEPTOR 9; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; CELL LINE; DEREGULATION; DOWN REGULATION; EPSTEIN BARR VIRUS; GENE DELETION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; INNATE IMMUNITY; LYMPHOBLASTOID CELL; PRIORITY JOURNAL; VIRUS INFECTION;

B-LYMPHOCYTES; CELL LINE; CELL LINE, TRANSFORMED; CELL LINE, TUMOR; DOWN-REGULATION; EPSTEIN-BARR VIRUS INFECTIONS; HERPESVIRUS 4, HUMAN; HUMANS; IMMUNE EVASION; IMMUNITY, INNATE; ONCOGENE PROTEINS, VIRAL; TOLL-LIKE RECEPTOR 9; TRANSCRIPTION, GENETIC; VIRAL MATRIX PROTEINS;

EID: 78650637968     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0903459     Document Type: Article

References (40)

1. Parkin, D. M., F. Bray, J. Ferlay, and P. Pisani. 2005. Global cancer statistics, 2002. CA Cancer J. Clin. 55:74-108.
2. Kieff, E. D., and A. B. Rickinson. 2007. Epstein-Barr virus and its replication. In Fields Virology, 5th Ed.. D. M. Knipe, and P. M. Howley, eds. Philadelphia: Lippincott Williams &Wilkins, p. 2603-2655.
3. Coffey, A. J., R. A. Brooksbank, O. Brandau, T. Oohashi, G. R. Howell, J. M. Bye, A. P. Cahn, J. Durham, P. Heath, P. Wray, et al. 1998. Host response to EBV infection in X-linked lymphoproliferative disease results from mutations in an SH2-domain encoding gene. Nat. Genet. 20:129-135.
4. Lamartine, J., K. E. Nichols, L. Yin, M. Krainer, F. Heitzmann, A. Bernard, S. Gaudi, G. M. Lenoir, J. L. Sullivan, J. E. Ikeda, et al. 1996. Physical map and cosmid contig encompassing a new interstitial deletion of the X-linked lymphoproliferative syndrome region. Eur. J. Hum. Genet. 4:342-351.
5. Purtilo, D. T., R. S. Strobach, M. Okano, and J. R. Davis. 1992. Epstein-Barr virus-associated lymphoproliferative disorders. Lab. Invest. 67:5-23.
6. 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. (Pubitemid 23306469)
7. Cahir McFarland, E. D., K. M. Izumi, and G. Mosialos. 1999. Epstein-barr virus transformation: involvement of latent membrane protein 1-mediated activation of NF-kappaB. Oncogene 18:6959-6964.
8. Eliopoulos, A. G., and L. S. Young. 2001. LMP1 structure and signal transduction. Semin. Cancer Biol. 11:435-444.
9. Mosialos, G., M. Birkenbach, R. Yalamanchili, T. Van Arsdale, 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.
10. Dawson, C. W., G. Tramountanis, A. G. Eliopoulos, and L. S. Young. 2003. Epstein-Barr virus latent membrane protein 1 (LMP1) activates the phosphatidylinositol 3-kinase/Akt pathway to promote cell survival and induce actin filament remodeling. J. Biol. Chem. 278:3694-3704.
11. Gires, O., F. Kohlhuber, E. Kilger, M. Baumann, A. Kieser, C. Kaiser, R. Zeidler, B. Scheffer, M. Ueffing, and W. Hammerschmidt. 1999. Latent membrane protein 1 of Epstein-Barr virus interacts with JAK3 and activates STAT proteins. EMBO J. 18:3064-3073.
12. 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-kappa B and cell surface phenotype via two effector regions in its carboxyterminal cytoplasmic domain. Oncogene 10:549-560.
13. Izumi, K. M., and E. D. Kieff. 1997. The Epstein-Barr virus oncogene product latent membrane protein 1 engages the tumor necrosis factor receptor-associated death domain protein to mediate B lymphocyte growth transformation and activate NF-kappaB. Proc. Natl. Acad. Sci. USA 94:12592-12597.
14. 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 virustransforming protein latent infection membrane protein 1 activates transcription factor NF-kappaB through a pathway that includes the NF-kappaB-inducing kinase and the IkappaB kinases IKKalpha and IKKbeta. Proc. Natl. Acad. Sci. USA 95:10106-10111.
15. Levitsky, V., and M. G. Masucci. 2002. Manipulation of immune responses by Epstein-Barr virus. Virus Res. 88:71-86.
16. Middeldorp, J. M., and D. M. Pegtel. 2008. Multiple roles of LMP1 in Epstein-Barr virus induced immune escape. Semin. Cancer Biol. 18:388-396.
17. 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.
18. Babcock, G. J., L. L. Decker, M. Volk, and D. A. Thorley-Lawson. 1998. EBV persistence in memory B cells in vivo. Immunity 9:395-404.
19. Takeda, K., and S. Akira. 2005. Toll-like receptors in innate immunity. Int. Immunol. 17:1-14.
20. Hornung, V., S. Rothenfusser, S. Britsch, A. Krug, B. Jahrsdörfer, T. Giese, S. Endres, and G. Hartmann. 2002. Quantitative expression of toll-like receptor 1-10 mRNA in cellular subsets of human peripheral blood mononuclear cells and sensitivity to CpG oligodeoxynucleotides. J. Immunol. 168:4531-4537.
21. Bowie, A. G., and I. R. Haga. 2005. The role of Toll-like receptors in the host response to viruses. Mol. Immunol. 42:859-867.
22. Finberg, R. W., J. P. Wang, and E. A. Kurt-Jones. 2007. Toll like receptors and viruses. Rev. Med. Virol. 17:35-43.
23. Pasare, C., and R. Medzhitov. 2005. Control of B-cell responses by Tolllike receptors. Nature 438:364-368.
24. Lund, J., A. Sato, S. Akira, R. Medzhitov, and A. Iwasaki. 2003. Toll-like receptor 9-mediated recognition of Herpes simplex virus-2 by plasmacytoid dendritic cells. J. Exp. Med. 198:513-520.
25. Lim, W. H., S. Kireta, G. R. Russ, and P. T. Coates. 2007. Human plasmacytoid dendritic cells regulate immune responses to Epstein-Barr virus (EBV) infection and delay EBV-related mortality in humanized NOD-SCID mice. Blood 109:1043-1050.
26. Guggemoos, S., D. Hangel, S. Hamm, A. Heit, S. Bauer, and H. Adler. 2008. TLR9 contributes to antiviral immunity during gammaherpesvirus infection. J. Immunol. 180:438-443.
27. Delecluse, H. J., D. Pich, T. Hilsendegen, C. Baum, and W. Hammerschmidt. 1999. A first-generation packaging cell line for Epstein-Barr virus-derived vectors. Proc. Natl. Acad. Sci. USA 96:5188-5193.
28. Dirmeier, U., B. Neuhierl, E. Kilger, G. Reisbach, M. L. Sandberg, and W. Hammerschmidt. 2003. Latent membrane protein 1 is critical for efficient growth transformation of human B cells by Epstein-Barr virus. Cancer Res. 63:2982-2989.
29. Caldeira, S., I. Zehbe, R. Accardi, I. Malanchi, W. Dong, M. Giarrè, E. M. de Villiers, R. Filotico, P. Boukamp, and M. Tommasino. 2003. The E6 and E7 proteins of the cutaneous human papillomavirus type 38 display transforming properties. J. Virol. 77:2195-2206.
30. Hasan, U. A., E. Bates, F. Takeshita, A. Biliato, R. Accardi, V. Bouvard, M. Mansour, I. Vincent, L. Gissmann, T. Iftner, et al. 2007. TLR9 expression and function is abolished by the cervical cancer-associated human papillomavirus type 16. J. Immunol. 178:3186-3197.
31. Takeshita, F., K. Suzuki, S. Sasaki, N. Ishii, D. M. Klinman, and K. J. Ishii. 2004. Transcriptional regulation of the human TLR9 gene. J. Immunol. 173:2552-2561.
32. Eliopoulos, A. G., S. M. Blake, J. E. Floettmann, M. Rowe, and L. S. Young. 1999. Epstein-Barr virus-encoded latent membrane protein 1 activates the JNK pathway through its extreme C terminus via a mechanism involving TRADD and TRAF2. J. Virol. 73:1023-1035.
33. Natoli, G., A. Costanzo, F. Guido, F. Moretti, A. Bernardo, V. L. Burgio, C. Agresti, and M. Levrero. 1998. Nuclear factor kB-independent cytoprotective pathways originating at tumor necrosis factor receptor-associated factor 2. J. Biol. Chem. 273:31262-31272.
34. Martin, H. J., J. M. Lee, D. Walls, and S. D. Hayward. 2007. Manipulation of the toll-like receptor 7 signaling pathway by Epstein-Barr virus. J. Virol. 81:9748-9758.
35. Iskra, S., M. Kalla, H. J. Delecluse, W. Hammerschmidt, and A. Moosmann. 2010. Toll-like receptor agonists synergistically increase proliferation and activation of B cells by epstein-barr virus. J. Virol. 84:3612-3623.
36. Ariza, M. E., R. Glaser, P. T. Kaumaya, C. Jones, and M. V. Williams. 2009. The EBV-encoded dUTPase activates NF-kappa B through the TLR2 and MyD88-dependent signaling pathway. J. Immunol. 182:851-859.
37. Sato, A., M. M. Linehan, and A. Iwasaki. 2006. Dual recognition of herpes simplex viruses by TLR2 and TLR9 in dendritic cells. Proc. Natl. Acad. Sci. USA 103:17343-17348.
38. Samanta, M., D. Iwakiri, T. Kanda, T. Imaizumi, and K. Takada. 2006. EB virusencoded RNAs are recognized by RIG-I and activate signaling to induce type I IFN. EMBO J. 25:4207-4214.
39. Iwakiri, D., L. Zhou, M. Samanta, M. Matsumoto, T. Ebihara, T. Seya, S. Imai, M. Fujieda, K. Kawa, and K. Takada. 2009. Epstein-Barr virus (EBV)-encoded small RNA is released from EBV-infected cells and activates signaling from Toll-like receptor 3. J. Exp. Med. 206:2091-2099.
40. Samanta, M., D. Iwakiri, and K. Takada. 2008. Epstein-Barr virus-encoded small RNA induces IL-10 through RIG-I-mediated IRF-3 signaling. Oncogene 27:4150-4160.