Home LiteratureArticle Details
PMID: 9351829 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

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

The EMBO journal ·Vol. 16 ·No. 21 ·1997-11-03 ·Pages 6478-85

Kieser A, Kilger E, Gires O, Ueffing M, Kolch W, Hammerschmidt W

Abstract

The Epstein-Barr virus latent membrane protein-1 (LMP-1) is an integral membrane protein which transforms fibroblasts and is essential for EBV-mediated B-cell immortalization. LMP-1 has been shown to trigger cellular NF-kappa B activity which, however, cannot fully explain the oncogenic potential of LMP-1. Here we show that LMP-1 induces the activity of the AP-1 transcription factor, a dimer of Jun/Jun or Jun/Fos proteins. LMP-1 effects on AP-1 are mediated through activation of the c-Jun N-terminal kinase (JNK) cascade, but not the extracellular signal-regulated kinase (Erk) pathway. Consequently, LMP-1 triggers the activity of the c-Jun N-terminal transactivation domain which is known to be activated upon JNK-mediated phosphorylation. Deletion analysis indicates that the 55 C-terminal amino acids of the LMP-1 molecule, but not its TRAF interaction domain, are essential for AP-1 activation. JNK-mediated transcriptional activation of AP-1 is the direct output of LMP-1-triggered signaling, as shown by an inducible LMP-1 mutant. Using a tetracycline-regulated LMP-1 allele, we demonstrate that JNK is also an effector of non-cytotoxic LMP-1 signaling in B cells, the physiological target cells of EBV. In summary, our data reveal a novel effector of LMP-1, the SEK/JNK/c-Jun/AP-1 pathway, which contributes to our understanding of the immortalizing and transforming potential of LMP-1.

MeSH Terms
B-Lymphocytes/metabolism Calcium-Calmodulin-Dependent Protein Kinases/analysis,physiology Cell Transformation, Viral/physiology Cells, Cultured Gene Expression Regulation, Viral Herpesvirus 4, Human/genetics,physiology 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/genetics,physiology Proto-Oncogene Proteins c-jun/chemistry Signal Transduction/physiology Transcription Factor AP-1/chemistry,metabolism Transcriptional Activation Viral Matrix Proteins/physiology
Chemicals
EBV-associated membrane antigen, Epstein-Barr virus Proto-Oncogene Proteins c-jun Transcription Factor AP-1 Viral Matrix Proteins Protein Kinases Calcium-Calmodulin-Dependent Protein Kinases JNK Mitogen-Activated Protein Kinases Mitogen-Activated Protein Kinase 1 Mitogen-Activated Protein Kinases MAP Kinase Kinase 4 MAP2K4 protein, human Mitogen-Activated Protein Kinase Kinases
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Kieser A
GSF-National Research Center for Environment and Health, Institute for Clinical Molecular Biology and Tumor Genetics, München, Germany.
Kilger E
Gires O
Ueffing M
Kolch W
Hammerschmidt W
References (52)
52 references, click to expand
  1. A vector that replicates as a plasmid and can be efficiently selected in B-lymphoblasts transformed by Epstein-Barr virus.
    Mol Cell Biol. 1985 Feb;5(2):410-3 PMID: 2983194
  2. Latent membrane protein 1 of Epstein-Barr virus mimics a constitutively active receptor molecule.
    EMBO J. 1997 Oct 15;16(20):6131-40 PMID: 9359753
  3. Orientation and patching of the latent infection membrane protein encoded by Epstein-Barr virus.
    J Virol. 1986 Apr;58(1):233-7 PMID: 3005654
  4. Transformation of Balb 3T3 cells by the BNLF-1 gene of Epstein-Barr virus.
    Oncogene. 1988 May;2(5):461-7 PMID: 2836780
  5. Genetic analysis of immortalizing functions of Epstein-Barr virus in human B lymphocytes.
    Nature. 1989 Aug 3;340(6232):393-7 PMID: 2547164
  6. Epstein-Barr virus nuclear protein 2 is a key determinant of lymphocyte transformation.
    Proc Natl Acad Sci U S A. 1989 Dec;86(23):9558-62 PMID: 2556717
  7. 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. 1990 Mar;64(3):1002-13 PMID: 2154588
  8. 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. 1990 May;64(5):2309-18 PMID: 2157887
  9. The level of c-fgr RNA is increased by EBNA-2, an Epstein-Barr virus gene required for B-cell immortalization.
    J Virol. 1990 Jun;64(6):2530-6 PMID: 2159528
  10. 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 U S A. 1990 Oct;87(19):7390-4 PMID: 2170976
  11. Control of c-Jun activity by interaction of a cell-specific inhibitor with regulatory domain delta: differences between v- and c-Jun.
    Cell. 1990 Nov 16;63(4):815-25 PMID: 2121368
  12. Induction of bcl-2 expression by Epstein-Barr virus latent membrane protein 1 protects infected B cells from programmed cell death.
    Cell. 1991 Jun 28;65(7):1107-15 PMID: 1648447
  13. The role of Jun, Fos and the AP-1 complex in cell-proliferation and transformation.
    Biochim Biophys Acta. 1991 Dec 10;1072(2-3):129-57 PMID: 1751545
  14. Epstein-Barr virus latent membrane protein transactivates the human immunodeficiency virus type 1 long terminal repeat through induction of NF-kappa B activity.
    J Virol. 1992 Nov;66(11):6496-501 PMID: 1404600
  15. The Epstein-Barr virus LMP1 gene product induces A20 zinc finger protein expression by activating nuclear factor kappa B.
    J Biol Chem. 1992 Dec 5;267(34):24157-60 PMID: 1332946
  16. All three domains of the Epstein-Barr virus-encoded latent membrane protein LMP-1 are required for transformation of rat-1 fibroblasts.
    J Virol. 1993 Mar;67(3):1638-46 PMID: 8382313
  17. Epstein-Barr virus nuclear proteins EBNA-3A and EBNA-3C are essential for B-lymphocyte growth transformation.
    J Virol. 1993 Apr;67(4):2014-25 PMID: 8445720
  18. cis-acting elements in the lytic origin of DNA replication of Epstein-Barr virus.
    J Virol. 1993 Jul;67(7):4237-45 PMID: 8389925
  19. Latent membrane protein of Epstein-Barr virus induces cellular phenotypes independently of expression of Bcl-2.
    J Virol. 1993 Sep;67(9):5269-78 PMID: 8394449
  20. Epstein-Barr virus latent membrane protein 1 is essential for B-lymphocyte growth transformation.
    Proc Natl Acad Sci U S A. 1993 Oct 1;90(19):9150-4 PMID: 8415670
  21. Identification of an oncoprotein- and UV-responsive protein kinase that binds and potentiates the c-Jun activation domain.
    Genes Dev. 1993 Nov;7(11):2135-48 PMID: 8224842
  22. Control of gene activity in higher eukaryotic cells by prokaryotic regulatory elements.
    Trends Biochem Sci. 1993 Dec;18(12):471-5 PMID: 8108860
  23. JNK1: a protein kinase stimulated by UV light and Ha-Ras that binds and phosphorylates the c-Jun activation domain.
    Cell. 1994 Mar 25;76(6):1025-37 PMID: 8137421
  24. JNK is involved in signal integration during costimulation of T lymphocytes.
    Cell. 1994 Jun 3;77(5):727-36 PMID: 8205621
  25. Epstein-Barr virus strategy in normal and neoplastic B cells.
    Cell. 1994 Jun 17;77(6):791-3 PMID: 8004668
  26. Oncogenic Ras activates c-Jun via a separate pathway from the activation of extracellular signal-regulated kinases.
    Proc Natl Acad Sci U S A. 1994 Jun 21;91(13):6030-4 PMID: 8016110
  27. Mediation of Epstein-Barr virus EBNA2 transactivation by recombination signal-binding protein J kappa.
    Science. 1994 Jul 1;265(5168):92-5 PMID: 8016657
  28. 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 U S A. 1994 Aug 2;91(16):7568-72 PMID: 8052621
  29. 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. 1994 Oct 17;13(20):4973-82 PMID: 7957063
  30. The Spi-1/PU.1 and Spi-B ets family transcription factors and the recombination signal binding protein RBP-J kappa interact with an Epstein-Barr virus nuclear antigen 2 responsive cis-element.
    EMBO J. 1994 Dec 1;13(23):5624-32 PMID: 7988559
  31. Differential activation of ERK and JNK mitogen-activated protein kinases by Raf-1 and MEKK.
    Science. 1994 Dec 9;266(5191):1719-23 PMID: 7992057
  32. Role of SAPK/ERK kinase-1 in the stress-activated pathway regulating transcription factor c-Jun.
    Nature. 1994 Dec 22-29;372(6508):794-8 PMID: 7997269
  33. Activation of stress-activated protein kinase by MEKK1 phosphorylation of its activator SEK1.
    Nature. 1994 Dec 22-29;372(6508):798-800 PMID: 7997270
  34. 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. 1995 Feb;69(2):675-83 PMID: 7815530
  35. B-cell proliferation and induction of early G1-regulating proteins by Epstein-Barr virus mutants conditional for EBNA2.
    EMBO J. 1995 Jan 3;14(1):88-96 PMID: 7828599
  36. 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 carboxy-terminal cytoplasmic domain.
    Oncogene. 1995 Feb 2;10(3):549-60 PMID: 7845680
  37. The Epstein-Barr virus transforming protein LMP1 engages signaling proteins for the tumor necrosis factor receptor family.
    Cell. 1995 Feb 10;80(3):389-99 PMID: 7859281
  38. Tetracycline-reversible silencing of eukaryotic promoters.
    Mol Cell Biol. 1995 Apr;15(4):1907-14 PMID: 7891684
  39. Stimulation of NF-kappa B-mediated transcription by mutant derivatives of the latent membrane protein of Epstein-Barr virus.
    J Virol. 1995 May;69(5):2968-76 PMID: 7707523
  40. Epstein-Barr virus immortalizing genes.
    Trends Microbiol. 1995 Mar;3(3):105-9 PMID: 7773587
  41. Immortalization of human primary B lymphocytes in vitro with DNA.
    Proc Natl Acad Sci U S A. 1995 Jun 20;92(13):5875-9 PMID: 7597045
  42. The regulation of AP-1 activity by mitogen-activated protein kinases.
    J Biol Chem. 1995 Jul 14;270(28):16483-6 PMID: 7622446
  43. Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis.
    Science. 1995 Nov 24;270(5240):1326-31 PMID: 7481820
  44. Cross-linking CD40 on B cells preferentially induces stress-activated protein kinases rather than mitogen-activated protein kinases.
    EMBO J. 1996 Jan 2;15(1):92-101 PMID: 8598210
  45. Protein kinase C-zeta reverts v-raf transformation of NIH-3T3 cells.
    Genes Dev. 1996 Jun 15;10(12):1455-66 PMID: 8666230
  46. Association of TRAF1, TRAF2, and TRAF3 with an Epstein-Barr virus LMP1 domain important for B-lymphocyte transformation: role in NF-kappaB activation.
    Mol Cell Biol. 1996 Dec;16(12):7098-108 PMID: 8943365
  47. Activation of JNK/SAPK pathway is not directly inhibitory for cell cycle progression in NIH3T3 cells.
    Oncogene. 1996 Dec 5;13(11):2421-30 PMID: 8957084
  48. Activation of SAPK/JNK by TNF receptor 1 through a noncytotoxic TRAF2-dependent pathway.
    Science. 1997 Jan 10;275(5297):200-3 PMID: 8985011
  49. 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. 1996 Dec 16;15(24):7070-8 PMID: 9003782
  50. AP-1 function and regulation.
    Curr Opin Cell Biol. 1997 Apr;9(2):240-6 PMID: 9069263
  51. Characterization of LMP-1's association with TRAF1, TRAF2, and TRAF3.
    J Virol. 1997 Jun;71(6):4649-56 PMID: 9151858
  52. An EBV membrane protein expressed in immortalized lymphocytes transforms established rodent cells.
    Cell. 1985 Dec;43(3 Pt 2):831-40 PMID: 3000618
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
1997-11-03
Pages
6478-85
Language
English
Region
England
NLM ID
8208664
PMCID
PMC1170253
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]