LMP1 transmembrane domain 1 and 2 (TM1-2) FWLY mediates intermolecular interactions with TM3-6 to activate NF-κB

Journal of Virology

Volumn 80, Issue 21, 2006, Pages 10787-10793

  Soni, Vishal ^c   Yasui, Teruhito ^b   Cahir McFarland, Ellen ^c   Kieff, Elliott ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b OSAKA UNIVERSITY   (Japan)

^c NONE

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LATENT MEMBRANE PROTEIN 1; LATENT MEMBRANE PROTEIN 2; ONCOPROTEIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CYTOSOL; EPSTEIN BARR VIRUS; HUMAN; HUMAN CELL; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

AMINO ACID SEQUENCE; CELL LINE; HERPESVIRUS 4, HUMAN; HUMANS; MODELS, BIOLOGICAL; NF-KAPPA B; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; VIRAL MATRIX PROTEINS;

HUMAN HERPESVIRUS 4;

EID: 33750372538     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01214-06     Document Type: Article

References (60)

1. Albert, A. D., J. E. Young, and P. L. Yeagle. 1996. Rhodopsin-cholesterol interactions in bovine rod outer segment disk membranes. Biochim. Biophys. Acta 1285:47-55.
2. Anzenbacher, P., J. Hudecek, S. Vajda, V. Fidler, C. Larroque, and R. Lange. 1991. Nanosecond fluorescence of tryptophans in cytochrome P-450scc (CYP11A1): effect of substrate binding. Biochem. Biophys. Res. Commun. 181:1493-1499.
3. Ardila-Osorio, H., B. Clausse, Z. Mishal, J. Wiels, T. Tursz, and P. Bussen. 1999. Evidence of LMP1-TRAF3 interactions in glycosphingolipid-rich complexes of lymphoblastoid and nasopharyngeal carcinoma cells. Int. J. Cancer 81:645-649.
4. Brodeur, S. R., G. Cheng, D. Baltimore, and D. A. Thorley-Lawson. 1997. Localization of the major NF-KB-activating site and the sole TRAF3 binding site of LMP-1 defines two distinct signaling motifs. J. Biol. Chem. 272:19777-19784.
5. Cahir-McFarland, E., and E. Kieff. 2002. NF-κB inhibition in EBV-transformed lymphoblastoid cell lines. Recent Results Cancer Res. 159:44-48.
6. Cahir-McFarland, E. D., K. Carter, A. Rosenwald, J. M. Giltnane, S. E. Henrickson, L. M. Staudt, and E. Kieff. 2004. Role of NF-κB in cell survival and transcription of latent membrane protein 1-expressing or Epstein-Barr virus latency III-infected cells. J. Virol. 78:4108-4119.
7. Cahir-McFarland, E. D., D. M. Davidson, S. L. Schauer, J. Duong, and E. Kieff. 2000. NF-κB inhibition causes spontaneous apoptosis in Epstein-Barr virus-transformed lymphoblastoid cells. Proc. Natl. Acad. Sci. USA 97:6055-6060.
8. Chakrabarti, A. C., I. Clark-Lewis, and P. R. Cullis. 1994. Influence of charge, charge distribution, and hydrophobicity on the transport of short model peptides into liposomes in response to transmembrane pH gradients. Biochemistry 33:8479-8485.
9. Clausse, B., K. Fizazi, V. Walczak, C. Tetaud, J. Wiels, T. Tursz, and P. Busson. 1997. High concentration of the EBV latent membrane protein 1 in glycosphingolipid-rich complexes from both epithelial and lymphoid cells. Virology 228:285-293.
10. Coffin, W. F., III, T. R. Geiger, and J. M. Martin. 2003. Transmembrane domains 1 and 2 of the latent membrane protein 1 of Epstein-Barr virus contain a lipid raft targeting signal and play a critical role in cytostasis. J. Virol. 77:3749-3758.
11. Curran, J. A., F. S. Laverty, D. Campbell, J. Macdiarmid, and J. B. Wilson. 2001. Epstein-Barr virus encoded latent membrane protein-1 induces epithelial cell proliferation and sensitizes transgenic mice to chemical carcinogenesis. Cancer Res. 61:6730-6738.
12. 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.
13. 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.
14. Devergne, O., E. C. McFarland, G. Mosialos, K. M. Izumi, C. F. Ware, and E. Kieff. 1998. Role of the TRAF binding site and NF-κB activation in Epstein-Barr virus latent membrane protein 1-induced cell gene expression. J. Virol. 72:7900-7908.
15. 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.
16. Eliopoulos, A. G., N. J. Gallagher, S. M. Blake, C. W. Dawson, and L. S. Young. 1999. Activation of the p38 mitogen-activated protein kinase pathway by Epstein-Barr virus-encoded latent membrane protein 1 coregulates interleukin-6 and interleukin-8 production. J. Biol. Chem. 274:16085-16096.
17. 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.
18. Fennewald, S., V. van Santen, and E. Kieff. 1984. Nucleotide sequence of an mRNA transcribed in latent growth-transforming virus infection indicates that it may encode a membrane protein. J. Virol. 51:411-419.
19. 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 oligomerisation for NF-κB activation. Oncogene 15:1851-1858.
20. Franken, M., O. Devergne, M. Rosenzweig, B. Annis, E. Kieff, and F. Wang. 1996. Comparative analysis identifies conserved tumor necrosis factor receptor-associated factor 3 binding sites in the human and simian Epstein-Barr virus oncogene LMP1. J. Virol. 70:7819-7826.
21. Hammarskjold, M. L., and M. C. Simurda. 1992. Epstein-Barr virus latent membrane protein transactivates the human immunodeficiency virus type 1 long terminal repeat through induction of NF-κB activity. J. Virol. 66:6496-6501.
22. Hennessy, K., S. Fennewald, M. Hummel, T. Cole, and E. Kieff. 1984. A membrane protein encoded by Epstein-Barr virus in latent growth-transforming infection. Proc. Natl. Acad. Sci. USA 81:7207-7211.
23. Hessa, T., H. Kim, K. Bihlmaier, C. Lundin, J. Boekel, H. Andersson, I. Nilsson, S. H. White, and G. von Heijne. 2005. Recognition of transmembrane helices by the endoplasmic reticulum translocon. Nature 433:377-381.
24. Higuchi, M., K. M. Izumi, and E. Kieff. 2001. Epstein-Barr virus latent-infection membrane proteins are palmitoylated and raft-associated: protein 1 binds to the cytoskeleton through TNF receptor cytoplasmic factors. Proc. Natl. Acad. Sci. USA 98:4675-4680.
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., E. D. Cahir-McFarland, E. A. Riley, D. Rizzo, Y. Chen, and E. Kieff. 1999. The residues between the two transformation effector sites of Epstein-Barr virus latent membrane protein 1 are not critical for B-lymphocyte growth transformation. J. Virol. 73:9908-9916.
27. Izumi, K. M., E. D. Cahir-McFarland, A. T. Ting, E. A. Riley, B. Seed, and E. D. Kieff. 1999. The Epstein-Barr virus oncoprotein latent membrane protein 1 engages the tumor necrosis factor receptor-associated proteins TRADD and receptor-interacting protein (RIP) but does not induce apoptosis or require RIP for NF-κB activation. Mol. Cell. Biol. 19:5759-5767.
28. 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-κB. Proc. Natl. Acad. Sci. USA 94:12592-12597.
29. Jayasinghe, S., K. Hristova, and S. H. White. 2001. Energetics, stability, and prediction of transmembrane helices. J. Mol. Biol. 312:927-934.
30. Kaye, K. M., O. Devergne, J. N. Harada, K. M. Izumi, R. Yalamanchili, E. Kieff, and G. Mosialos. 1996. Tumor 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.
31. 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.
32. Kaykas, A., K. Worringer, and B. Sugden. 2002. LMP-1's transmembrane domains encode multiple functions required for LMP-1's efficient signaling. J. Virol. 76:11551-11560.
33. Kieff, E., and A. B. Rickinson. 2001. Epstein-Barr Virus and its replication, p. 2511-2574. In D. M. Knipe and P. M. Howley (ed.), Fields virology, 4th ed., vol. 2. Lippincott Williams and Wilkins, Philadelphia, Pa.
34. Kulwichit, W., R. H. Edwards, E. M. Davenport, J. F. Baskar, V. Godfrey, and N. Raab-Traub, 1998. Expression of the Epstein-Barr virus latent membrane protein 1 induces B cell lymphoma in transgenic mice. Proc. Natl. Acad. Sci. USA 95:11963-11968.
35. 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 κB. J. Biol. Chem. 267:24157-24160.
36. Li, J., P. C. Edwards, M. Burghammer, C. Villa, and G. F. Schertler. 2004. Structure of bovine rhodopsin in a trigonal crystal form. J. Mol. Biol. 343:1409-1438.
37. Liebowitz, D., and E. Kieff. 1989. Epstein-Barr virus latent membrane protein: induction of B-cell activation antigens and membrane patch formation does not require vimentin. J. Virol. 63:4051-4054.
38. Liebowitz, D., R. Kopan, E. Fuchs, J. Sample, and E. Kieff. 1987. An Epstein-Barr virus transforming protein associates with vimentin in lymphocytes. Mol. Cell. Biol. 7:2299-2308.
39. Liebowitz, D., J. Mannick, K. Takada, and E. Kieff. 1992. Phenotypes of Epstein-Barr virus LMP1 deletion mutants indicate transmembrane and amino-terminal cytoplasmic domains necessary for effects in B-lymphoma cells. J. Virol. 66:4612-4616.
40. Liebowitz, D., D. Wang, and E. Kieff. 1986. Orientation and patching of the latent infection membrane protein encoded by Epstein-Barr virus. J. Virol. 58:233-237.
41. 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.
42. Martin, J., and B. Sugden. 1991. The latent membrane protein oncoprotein resembles growth factor receptors in the properties of its turnover. Cell Growth Differ. 2:653-660.
43. Miller, W. E., J. L. Cheshire, A. S. Baldwin, Jr., and N. Raab-Traub. 1998. The NPC derived C15 LMP1 protein confers enhanced activation of NF-κB and induction of the EGFR in epithelial cells. Oncogene 16:1869-1877.
44. Miller, W. E., G. Mosialos, E. Kieff, and N. Raab-Traub. 1997. Epstein-Barr virus LMP1 induction of the epidermal growth factor receptor is mediated through a TRAF signaling pathway distinct from NF-κB activation. J. Virol. 71:586-594.
45. Mitchell, T., and B. Sugden. 1995. Stimulation of NF-κB-mediated transcription by mutant derivatives of the latent membrane protein of Epstein-Barr virus. J. Virol. 69:2968-2976.
46. 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.
47. Palczewski, K., T. Kumasaka, T. Hori, C. A. Behnke, H. Motoshima, B. A. Fox, I. Le Trong, D. C. Teller, T. Okada, R. E. Stenkamp, M. Yamamoto, and M. Miyano. 2000. Crystal structure of rhodopsin: a G protein-coupled receptor. Science 289:739-745.
48. Puls, A., A. G. Eliopoulos, C. D. Nobes, T. Bridges, L. S. Young, and A. Hall. 1999. Activation of the small GTPase Cdc42 by the inflammatory cytokines TNF-α and IL-1, and by the Epstein-Barr virus transforming protein LMP1. J. Cell Sci. 112(Pt. 17):2983-2992.
49. Rickinson, A. B., and E. Kieff. 2001. Epstein-Barr virus, p. 2575-2628. In D. M. Knipe and P. M. Howley (ed.), Fields virology, 4th ed., vol. 2. Lippincott Williams and Wilkins, Philadelphia, Pa.
50. Sandberg, M., W. Hammerschmidt, and B. Sugden. 1997. Characterization of LMP-1's association with TRAF1, TRAF2, and TRAF3. J. Virol. 71:4649-4656.
51. Shimada, Y., M. Maruya, S. Iwashita, and Y. Ohno-Iwashita. 2002. The C-terminal domain of perfringolysin O is an essential cholesterol-binding unit targeting to cholesterol-rich microdomains. Eur. J. Biochem. 269:6195-6203.
52. Ulmschneider, M. B., and M. S. Sansom. 2001. Amino acid distributions in integral membrane protein structures. Biochim. Biophys. Acta 1512:1-14.
53. Wan, J., L. Sun, J. W. Mendoza, Y. L. Chui, D. P. Huang, Z. J. Chen, N. Suzuki, S. Suzuki, W. C. Yen, S. Akira, K. Matsumoto, Z. G. Liu, and Z. Wu. 2004. Elucidation of the c-Jun N-terminal kinase pathway mediated by Estein-Barr virus-encoded latent membrane protein 1. Mol. Cell. Biol. 24:192-199.
54. Wang, D., D. Liebowitz, and E. Kieff. 1985. An EBV membrane protein expressed in immortalized lymphocytes transforms established rodent cells. Cell 43:831-840.
55. Wang, D., D. Liebowitz, F. Wang, C. Gregory, A. Rickinson, R. Larson, T. Springer, and E. Kieff. 1988. Epstein-Barr virus latent infection membrane protein alters the human B-lymphocyte phenotype: deletion of the amino terminus abolishes activity. J. Virol. 62:4173-4184.
56. Wang, F., C. Gregory, C. Sample, M. Rowe, D. Liebowitz, R. Murray, A. Rickinson, and E. Kieff. 1990. Epstein-Barr virus latent membrane protein (LMP1) and nuclear proteins 2 and 3C are effectors of phenotypic changes in B lymphocytes: EBNA-2 and LMP1 cooperatively induce CD23. J. Virol. 64:2309-2318.
57. Wimley, W. C., and S. H. White. 1996. Experimentally determined hydrophobicity scale for proteins at membrane interfaces. Nat. Struct. Biol. 3:842-848.
58. Yasui, T., M. Luftig, V. Soni, and E. Kieff. 2004. Latent infection membrane protein transmembrane FWLY is critical for intermolecular interaction, raft localization, and signaling. Proc. Natl. Acad. Sci. USA 101:278-283.
59. Yau, W. M., W. C., Wimley, K. Gawrisch, and S. H. White. 1998. The preference of tryptophan for membrane interfaces. Biochemistry 37:14713-14718.
60. Ye, H., Y. C. Park, M. Kreishman, E. Kieff, and H. Wu. 1999. The structural basis for the recognition of diverse receptor sequences by TRAF2. Mol. Cell 4:321-330.