Home LiteratureArticle Details
PMID: 9707608 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Epstein-Barr virus-transforming 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.

Sylla BS, Hung SC, Davidson DM, Hatzivassiliou E, Malinin NL, Wallach D, Gilmore TD, Kieff E, Mosialos G

Abstract

The Epstein-Barr virus oncoprotein latent infection membrane protein 1 (LMP1) is a constitutively aggregated pseudo-tumor necrosis factor receptor (TNFR) that activates transcription factor NF-kappaB through two sites in its C-terminal cytoplasmic domain. One site is similar to activated TNFRII in associating with TNFR-associated factors TRAF1 and TRAF2, and the second site is similar to TNFRI in associating with the TNFRI death domain interacting protein TRADD. TNFRI has been recently shown to activate NF-kappaB through association with TRADD, RIP, and TRAF2; activation of the NF-kappaB-inducing kinase (NIK); activation of the IkappaB alpha kinases (IKKalpha and IKKbeta); and phosphorylation of IkappaB alpha. IkappaB alpha phosphorylation on Ser-32 and Ser-36 is followed by its degradation and NF-kappaB activation. In this report, we show that NF-kappaB activation by LMP1 or by each of its effector sites is mediated by a pathway that includes NIK, IKKalpha, and IKKbeta. Dominant negative mutants of NIK, IKKalpha, or IKKbeta substantially inhibited NF-kappaB activation by LMP1 or by each of its effector sites.

MeSH Terms
Animals Binding Sites/genetics Cell Line Herpesvirus 4, Human/pathogenicity Humans I-kappa B Kinase In Vitro Techniques Mutation NF-kappa B/metabolism Phosphorylation Protein Serine-Threonine Kinases/genetics,metabolism Rabbits Reticulocytes/metabolism Signal Transduction Transfection Viral Matrix Proteins/genetics,metabolism
Chemicals
EBV-associated membrane antigen, Epstein-Barr virus NF-kappa B Viral Matrix Proteins Protein Serine-Threonine Kinases CHUK protein, human I-kappa B Kinase IKBKB protein, human IKBKE protein, human NF-kappa B kinase
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Sylla B S
Departments of Microbiology and Molecular Genetics and Medicine, Harvard Medical School and Brigham and Women's Hospital, 181 Longwood Avenue, Boston, MA, 02115, USA.
Hung S C
Davidson D M
Hatzivassiliou E
Malinin N L
Wallach D
Gilmore T D
Kieff E
Mosialos G
References (40)
40 references, click to expand
  1. 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-kappaB activation.
    Oncogene. 1997 Oct 9;15(15):1851-8 PMID: 9362452
  2. The TNF receptor 1-associated protein TRADD signals cell death and NF-kappa B activation.
    Cell. 1995 May 19;81(4):495-504 PMID: 7758105
  3. The truncated form of the Epstein-Barr virus latent-infection membrane protein expressed in virus replication does not transform rodent fibroblasts.
    J Virol. 1988 Jul;62(7):2337-46 PMID: 2836616
  4. The multiple membrane-spanning segments of the BNLF-1 oncogene from Epstein-Barr virus are required for transformation.
    Oncogene. 1989 Jan;4(1):67-74 PMID: 2536919
  5. Tumor necrosis factor receptor signaling. A dominant negative mutation suppresses the activation of the 55-kDa tumor necrosis factor receptor.
    J Biol Chem. 1992 Mar 5;267(7):4304-7 PMID: 1311304
  6. Phenotypes of Epstein-Barr virus LMP1 deletion mutants indicate transmembrane and amino-terminal cytoplasmic domains necessary for effects in B-lymphoma cells.
    J Virol. 1992 Jul;66(7):4612-6 PMID: 1318423
  7. 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
  8. 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
  9. Epstein-Barr virus recombinant molecular genetic analysis of the LMP1 amino-terminal cytoplasmic domain reveals a probable structural role, with no component essential for primary B-lymphocyte growth transformation.
    J Virol. 1994 Jul;68(7):4369-76 PMID: 8207810
  10. A novel family of putative signal transducers associated with the cytoplasmic domain of the 75 kDa tumor necrosis factor receptor.
    Cell. 1994 Aug 26;78(4):681-92 PMID: 8069916
  11. 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
  12. Targeted disruption of the p50 subunit of NF-kappa B leads to multifocal defects in immune responses.
    Cell. 1995 Jan 27;80(2):321-30 PMID: 7834752
  13. 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
  14. TRAF2-mediated activation of NF-kappa B by TNF receptor 2 and CD40.
    Science. 1995 Sep 8;269(5229):1424-7 PMID: 7544915
  15. Site-specific phosphorylation of IkappaBalpha by a novel ubiquitination-dependent protein kinase activity.
    Cell. 1996 Mar 22;84(6):853-62 PMID: 8601309
  16. TNF-dependent recruitment of the protein kinase RIP to the TNF receptor-1 signaling complex.
    Immunity. 1996 Apr;4(4):387-96 PMID: 8612133
  17. Tumor necrosis factor receptor associated factor 2 is a mediator of NF-kappa B activation by latent infection membrane protein 1, the Epstein-Barr virus transforming protein.
    Proc Natl Acad Sci U S A. 1996 Oct 1;93(20):11085-90 PMID: 8855313
  18. 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
  19. RIP mediates tumor necrosis factor receptor 1 activation of NF-kappaB but not Fas/APO-1-initiated apoptosis.
    EMBO J. 1996 Nov 15;15(22):6189-96 PMID: 8947041
  20. Epstein-Barr virus LMP1 induction of the epidermal growth factor receptor is mediated through a TRAF signaling pathway distinct from NF-kappaB activation.
    J Virol. 1997 Jan;71(1):586-94 PMID: 8985387
  21. MAP3K-related kinase involved in NF-kappaB induction by TNF, CD95 and IL-1.
    Nature. 1997 Feb 6;385(6616):540-4 PMID: 9020361
  22. The Epstein-Barr virus LMP1 amino acid sequence that engages tumor necrosis factor receptor associated factors is critical for primary B lymphocyte growth transformation.
    Proc Natl Acad Sci U S A. 1997 Feb 18;94(4):1447-52 PMID: 9037073
  23. MADD, a novel death domain protein that interacts with the type 1 tumor necrosis factor receptor and activates mitogen-activated protein kinase.
    J Biol Chem. 1997 May 2;272(18):12069-75 PMID: 9115275
  24. Identification and characterization of an IkappaB kinase.
    Cell. 1997 Jul 25;90(2):373-83 PMID: 9244310
  25. A cytokine-responsive IkappaB kinase that activates the transcription factor NF-kappaB.
    Nature. 1997 Aug 7;388(6642):548-54 PMID: 9252186
  26. The IkappaB kinase complex (IKK) contains two kinase subunits, IKKalpha and IKKbeta, necessary for IkappaB phosphorylation and NF-kappaB activation.
    Cell. 1997 Oct 17;91(2):243-52 PMID: 9346241
  27. IKK-1 and IKK-2: cytokine-activated IkappaB kinases essential for NF-kappaB activation.
    Science. 1997 Oct 31;278(5339):860-6 PMID: 9346484
  28. IkappaB kinase-beta: NF-kappaB activation and complex formation with IkappaB kinase-alpha and NIK.
    Science. 1997 Oct 31;278(5339):866-9 PMID: 9346485
  29. 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 U S A. 1997 Nov 11;94(23):12592-7 PMID: 9356494
  30. NF-kappaB activation: the I kappaB kinase revealed?
    Cell. 1997 Oct 31;91(3):299-302 PMID: 9363938
  31. Epstein-Barr virus latent membrane protein-1 triggers AP-1 activity via the c-Jun N-terminal kinase cascade.
    EMBO J. 1997 Nov 3;16(21):6478-85 PMID: 9351829
  32. The death domain kinase RIP mediates the TNF-induced NF-kappaB signal.
    Immunity. 1998 Mar;8(3):297-303 PMID: 9529147
  33. Differential regulation of IkappaB kinase alpha and beta by two upstream kinases, NF-kappaB-inducing kinase and mitogen-activated protein kinase/ERK kinase kinase-1.
    Proc Natl Acad Sci U S A. 1998 Mar 31;95(7):3537-42 PMID: 9520401
  34. NF-kappaB-inducing kinase activates IKK-alpha by phosphorylation of Ser-176.
    Proc Natl Acad Sci U S A. 1998 Mar 31;95(7):3792-7 PMID: 9520446
  35. A fusion of the EBV latent membrane protein-1 (LMP1) transmembrane domains to the CD40 cytoplasmic domain is similar to LMP1 in constitutive activation of epidermal growth factor receptor expression, nuclear factor-kappa B, and stress-activated protein kinase.
    J Immunol. 1998 Feb 1;160(3):1116-21 PMID: 9570524
  36. Activation of the cJun N-terminal kinase (JNK) pathway by the Epstein-Barr virus-encoded latent membrane protein 1 (LMP1).
    Oncogene. 1998 Apr 2;16(13):1731-42 PMID: 9582021
  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. Identification of a protein with homology to hsp90 that binds the type 1 tumor necrosis factor receptor.
    J Biol Chem. 1995 Feb 24;270(8):3574-81 PMID: 7876093
  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. 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
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
1998-08-18
Pages
10106-11
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC21469
Subset
IM
Grants
NCI NIH HHS · R01 CA047006 · United States
NCI NIH HHS · R35 CA047006 · United States
NCI NIH HHS · CA47006 · United States
NCI NIH HHS · CA71705 · United States
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]