Epstein-Barr virus latent membrane protein-1 triggers AP-1 activity via the c-Jun N-terminal kinase cascade

EMBO Journal

Volumn 16, Issue 21, 1997, Pages 6478-6485

  Kieser, Arnd ^a   Kilger, Ellen ^a   Gires, Olivier ^a   Ueffing, Marius ^a   Kolch, Walter ^a   Hammerschmidt, Wolfgang ^a  

^a INSTITUTE OF EPIDEMIOLOGY   (Germany)

Author keywords

AP 1 transcription factor; c Jun N terminal kinase pathway; Epstein Barr virus; Latent membrane protein 1; Signal transduction

Indexed keywords

DIMER; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MEMBRANE PROTEIN; PROTEIN KINASE; TRANSCRIPTION FACTOR AP 1;

ALLELE; AMINO ACID SEQUENCE; ARTICLE; B LYMPHOCYTE; CARBOXY TERMINAL SEQUENCE; CELL TRANSFORMATION; CONTROLLED STUDY; DELETION MUTANT; EMBRYO; ENZYME ACTIVATION; EPSTEIN BARR VIRUS; FIBROBLAST; HUMAN; HUMAN CELL; ONCOGENE C JUN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION;

B-LYMPHOCYTES; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CELL TRANSFORMATION, VIRAL; CELLS, CULTURED; GENE EXPRESSION REGULATION, VIRAL; HERPESVIRUS 4, HUMAN; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; KIDNEY; MAP KINASE KINASE 4; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; MITOGEN-ACTIVATED PROTEIN KINASES; PROTEIN KINASES; PROTO-ONCOGENE PROTEINS C-JUN; SIGNAL TRANSDUCTION; TRANS-ACTIVATION (GENETICS); TRANSCRIPTION FACTOR AP-1; VIRAL MATRIX PROTEINS;

HUMAN HERPESVIRUS 4;

EID: 0030728946     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/16.21.6478     Document Type: Article

References (53)

1. Angel,P. and Karin,M. (1991) The role of Jun. Fos and the AP-I complex in cell-proliferation and transformation. Biochim. Biophys. Acta. 1072, 129-157.
2. Baichwal,V.R. and Sugden,B. (1988) Transformation of Balb 3T3 cells by the BNLF-1 gene of Epstein-Barr virus. Oncogene, 2, 461-467.
3. Baichwal,V.R. and Tjian,R. (1990) Control of c-Jun activity by interaction of a cell-specific inhibitor with regulatory domain delta: differences between v- and c-Jun. Cell, 63, 815-825.
4. Berberich,I., Shu,G., Siebelt,F., Woodgett,J.R., Kyriakis,J.M. and Clark,E.A. (1996) Cross-linking CD40 on B cells preferentially induces stress-activated protein kinases rather than mitogen-activated protein kinases. EMBO J., 15, 92-101.
5. Cohen,J.I., Wang,F. Mannick,J. and Kieff,E. (1989) Epstein-Barr virus nuclear protein 2 is a key determinant of lymphocyte transformation. Proc. Natl Acad. Sci. USA, 86, 9558-9562.
6. Cordier,M. et al. (1990) Stable transfection of Epstein-Barr virus (EBV) nuclear antigen 2 in lymphoma cells containing the EBV P3HR1 genome induces expression of B-cell activation molecules CD21 and CD23. J. Virol., 64, 1002-1013.
7. Derijard,B., Hibi,M., Wu,I.H., Barrett,T., Su,B., Deng,T., Karin,M. and Davis,R.J. (1994) JNK1: a protein kinase stimulated by UV light and Ha-Ras that binds and phosphorylates the c-Jun activation domain. Cell, 76, 1025-1037.
8. Deuschle,U., Meyer,W.K. and Thiesen,H.J. (1995) Tetracycline-reversible silencing of eukaryotic promoters. Mol. Cell. Biol., 15, 1907-1914.
9. Devergne,O., Hatzivassiliou,E., Izumi,K.M., Kaye,K.M., Kleijnen,M.F. Kieff,E. and Mosialos,G. (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.
10. Fahraeus,R., Jansson,A., Ricksten,A., Sjoeblom,A. and Rymo,L. (1990) Epstein-Barr virus-encoded nuclear antigen 2 activates the viral latent membrane protein promoter by modulating the activity of a negative regulatory element. Proc. Natl Acad. Sci. USA, 87, 7390-7394.
11. Farrell,P.J. (1995) Epstein-Barr virus immortalizing genes. Trends Microbiol., 3, 105-109.
12. Gires,O., Zimber-Strobl,U., Gonnella,R., Ueffing,M., Marschall,G., Zeidler,R., Pich,D. and Hammerschmidt,W. (1997) Latent membrane protein 1 of Epstein-Barr virus mimics a constitutively active receptor molecule. EMBO J., 16, 6131-6140.
13. Gossen,M., Bonin,A.L., and Bujard,H. (1993) Control of gene activity in higher eukaryotic cells by prokaryotic regulatory elements. Trends Biochem. Sci., 18, 471-415.
14. Grossman,S.R., Johannsen,E., Tong,X., Yalamanchili,K. and Kieff,E. (1994) The Epstein-Barr virus nuclear antigen 2 transactivator is directed to response elements by the J kappa recombination signal binding protein. Proc. Natl Acad. Sci. USA, 91, 7568-7572.
15. Hammarskjold,M.I., and Simurda,M.C. (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.
16. Hammerschmidt,W. and Sugden,B. (1989) Genetic analysis of immortalizing functions of Epstein-Barr virus in human B lymphocytes. Nature, 340, 393-397.
17. Henderson,S., Rowe,M., Gregory,C., Croom,C.D., Wang,F. and Longnecker,R. (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.
18. Henkel,T., Ling,P.D., Hayward,S.D. and Peterson,M.G. (1994) Mediation of Epstein-Barr virus EBNA2 transactivation by recombination signal-binding protein J kappa. Science, 265, 92-95.
19. Hibi,M., Lin,A., Smeal,T., Minden,A. and Karin,M. (1993) Identification of an oncoprotein- and UV-responsive protein kinase that binds and potentiates the c-Jun activation domain. Genes Dev., 7, 2135-2148.
20. Huen,D.S., Henderson,S.A., Croom-Cartrer,D. and Rowe,M. (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.
21. Karin,M. (1995) The regulation of AP-1 activity by mitogen-activated protein kinases. J. Biol. Chem., 270, 16483-16486.
22. Karin,M., Liu,Z. and Zandi,E. (1997) AP-1 function and regulation. Curr. Opin. Cell Biol. 9, 240-246.
23. Kaye,K.M., Izumi,K.M. and Kieff,E. (1993) Epstein-Barr virus latent membrane protein 1 is essential for B-lymphocyte growth transformation. Proc. Natl Acad. Sci. USA, 90, 9150-9154.
24. Kaye,K.M., Izumi,K.M., Mosialos,G. and Kieff,E. (1995) The Epstein-Barr virus LMPI 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.
25. Kempkes,B., Pich,D., Zeidler,R and Hammerschmidt,W. (1995a) Immortalization of human primary B-lymphocytes in vitro with DNA. Proc. Natl Acad. Sci. USA, 92, 5875-5879.
26. Kempkes,B., Spitkovsky,D., Jansen-Dürr,P., Ellwart,J.W., Delecluse, H.-J., Rottenberger,C., Kremmer,H., Bomkamm,G.W and Hammerschmidt,W. (1995b) B-cell proliferation and induction of early G1-regulating proteins by Epstem Barr virus mutants conditional for EBNA2. EMBO J., 14, 88-96.
27. Kieff,E. (1996) Epstein-Barr virus and its replication. In Fields,B.N., Knipe,D.M., Howley,P.M., Chanock,R.M., Monath,T.P., Melnick,J. L., Roizman,B. and Straus,S.F., (eds). Virology, Lippincott-Raven Publishers. Philadelphia, PA, pp. 2343-2396.
28. Kieser,A., Seitz,T., Adler,H.S., Coffer,P. Kremmer,E., Crespo,P., Gutkind,J.S., Henderson,D.W., Mushinski,J.F. Kolch,W. and Mischak,H. (1996) Protein kinase C-zeta reverts v-raf transformation of NIH-3T3 cells. Genes Dev., 10, 1455-1466.
29. Klein,G. (1994) Epstein-Barr virus strategy in normal and neoplastic B cells. Cell, 77, 791-793.
30. Knutson,J.C. (1990) The level of c-fgr RNA is increased by EBNA-2, an Epstein-Barr virus gene required for B-cell immortalization. J. Virol., 64, 2530-2536.
31. Laherty,C.D., Hu,H.M., Opipari,A.W., Wang,F. and Dixit,V.M (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.
32. Laux,G., Adam,B., Strobl,L.J. and Moreau-Gachelin,F. (1994) The Spi-1/PU, 1 and Spi-B ets family transcription factors and the recombination signal binding protein RBP-J kjppa interact with an Epstein-Barr virus nuclear antigen 2 responsive cis-element. EMBO J., 13, 5624-5632.
33. Liebowitz,D., Wang,D. and Kieff,E. (1986) Orientation and patching of the latent infection membrane protein encoded by Epstein-Barr virus. J. Virol., 58, 233-237.
34. Martin,J.M., Veis,D., Korsmeyer,S.J. and Sugden,B. (1993) Latent membrane protein of Epstein- Barr virus induces cellular phenotypes independently of expression of Bcl-2. J. Virol., 67, 5269-5275.
35. Minden,A., Lin,A., McMahon,M., Lange-Carter,C., Deijard,B., Davis,R.J., Johnson,G.L. and Karin,M. (1994) Differential activation of ERK and JNK mitogen-activated protein kinases by Raf-1 and MEKK. Science, 266, 1719-1723.
36. Mitchell,T. and Sugden,B. (1995) Stimulation of NF-κB-mediated transcription by mutant derivatives of the latent membrane protein of Epstein-Barr virus. J. Virol., 69, 2968-2976.
37. Moorthy,R.K. and Thorley-Lawson,D.A. (1993) All three domains of the Epstein-Barr virus-encoded latent membrane protein LMP-1 are required for transformation of rat-1 fibroblasts. J. Virol., 67, 1638-1646.
38. Mosialos.G., Birkenbach,M., Yalamanchili,R., VanArsdale,T., Ware,C. and Kieff,E. (1995) The Epstein-Barr virus transforming protein LMP1 engages signaling proteins for the tumor necrosis factor receptor family. Cell, 80, 389-399
39. Natoli,G., Costanzo,A., Ianni,A., Templeton,D.J., Woodgett,J.R., Balsano,C. and Levrero,M. (1997) Activation of SAPK/JNK by TNF receptor 1 through a non-cytotoxic TRAF2-dependent pathway. Science, 275, 200-203.
40. Sanchez,I., Hughes,R.T., Mayer,B.J., Yee,K., Woodgett,J.R., Avruch,J., Kyriakis,J.M. and Zon,L.I. (1994) Role of SAPK/KRK kinase-1 in the stress-activated pathway regulating transcription factor c-Jun. Nature, 372, 794-798.
41. Sandberg,M., Hammerschimdt,W. and Sugden,B. (1997) Characterization ot LMP-1's association with TRAF1, TRAF2, and TRAF3. J. Virol., 71, 4649-4656.
42. Schepers,A., Pich,D., Mankertz,J. and Hammerschmidt,W. (1993) Cisacting elements in the lytic origin of DNA replication of Epstein Barr virus J. Virol., 67, 4237-4245.
43. Shu,J., Hitomi,M. and Stacey,O. (1996) Activation of JNK/SAPK pathway is not directly inhibitory for cell cycle progression in NIH3T3 cells. Oncogene, 13, 2421-2430.
44. Su,B., Jacinto,E., Hibi,M., Kallunki,T., Karin,M and Ben-Neriah,Y. (1994) JNK is involved in signal integration during costimulation of T lymphocytes. Cell. 77, 727-736.
45. Sugden,B., Marsh,K. and Yates,J. (1985) A vector that replicates as a plasmid and can he efficiently selected in B-lymphohlasts transformed by Epstein-Barr virus. Mol. Cell Biol., 5, 410-413.
46. Tomkinson,B., Robertson,E. and Kieff,E. (1993) Epstein-Barr virus nuclear proteins EBNA-3A and EBNA-3C are essential for B-lymphocyte growth transformation. J. Virol., 67, 2014-2025.
47. Wang,D., Liebowitz,D. and Kieff,E. (1985) An EBV membrane protein expressed in immortalized lymphocytes transforms established rodent cells. Cell, 43, 831-840.
48. Wang,F., Gregory,C., Sample,C., Rowe,M., Liebowitz,D., Murray,R., Rickinson,A. and Kieff,E. (1990) Epstein-Barr virus latent membrane prnlein (LMP1) and nuclear proteins 2 and 3C are effectors of phenotypic changes in B lymphocytes: EBNA-2 and LMPI cooperatively induce CD23. J. Virol., 64, 2309-2318.
49. Wesiwick,J.K., Cox,A.D., Der,C.J., Cobb,M.H., Hibi,M., Karin,M. and Brenner,D.A. (1994) Oncogenic Ras activates c-Jun via a separate pathway from the activation of extracellular signal-regulated kinases. Proc. Natl Acad. Sci. USA, 91, 6030-6034.
50. Xia,Z., Dickens,M., Raingeaud,J., Davis,R.J. and Greenberg,M.E. (1995) Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science, 270, 1326-1331.
51. Yan,M., Dai,T. Deak,J.C., Kyriakis,J.M., Zon,L.I., Woodgett,J.R. and Templeton,D.J. (1994) Activation of stress-activated protein kinase by MEKK1 phosphorylation ot its activator SEK1. Nature, 372, 798-800.
52. Zimber-Strobl,U., Kempkes,B., Marschall,g., Zeidler,R., Van Kooten,C., Banchereau,J., Bornkamm,G.W. and Hammerschmidt,W. (1996) Epstein-Barr virus latent membrane protein (LMP1) is not sufficient to maintain proliferation of B-cells but both it and activated CD40 can prolong their survival. EMBO J., 15, 7070-7078.
53. Zimber-Strobl,U., Strohl,L.J., Meitinger,C., Hinrichs,R., Sukai,T. Hurukawa,T., Honjo,T. and Bornkamm,G.W. (1994) Epstein Barr virus nuclear antigen 2 exerts its transactivating function through interaction with recombination signal binding protein RBP-J kappa, the homologue of Drosophila Suppressor of Hairless. EMBO J., 13, 4973-4982.