Home LiteratureArticle Details
PMID: 11533177 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Epstein-Barr virus LMP-1 natural sequence variants differ in their potential to activate cellular signaling pathways.

Journal of virology ·Vol. 75 ·No. 19 ·2001-10-00 ·Pages 9129-41

Fielding CA, Sandvej K, Mehl A, Brennan P, Jones M, Rowe M

Abstract

The latent membrane protein 1 (LMP-1) oncogene of Epstein-Barr virus (EBV) is believed to contribute to the development of many EBV-associated tumors, and there is evidence that sequence variation can affect some functions of LMP-1. Most studies have been restricted to the prototype B95.8 LMP-1 gene and genes isolated from EBV of nasopharyngeal carcinoma (NPC) patients. Here, we analyzed the signaling functions of LMP-1 from a panel of nine EBV isolates, including representatives of four defined groups of European LMP-1 variants (groups A to D [K. Sandvej, J. W. Gratama, M. Munch, X. G. Zhou, R. L. Bolhuis, B. S. Andresen, N. Gregersen, and S. Hamilton-Dutoit, Blood 90:323-330, 1997]) and Chinese NPC-derived LMP-1. Chinese and group D variants activated the transcription factor NF-kappa B two- to threefold more efficiently than B95.8 LMP-1, while Chinese, group B, and group D variants similarly activated activator protein 1 (AP-1) transcription more efficiently than did B95.8 LMP-1. However, there were no amino acid substitutions in the core binding regions for tumor necrosis factor receptor-associated adapter proteins known to mediate NF-kappa B and AP-1 activation. In contrast, despite sequence variation in the proposed Janus kinase 3 binding region, STAT activation was remarkably constant among the panel of LMP-1 variants. Analysis of the induction of CD54 (intercellular adhesion molecule 1) protein expression by the LMP-1 variants showed differences that did not correlate with either NF-kappa B or AP-1. Therefore, while the defined sequence variant groups do correlate with LMP-1 function, the results highlight the fact that the relationship between sequence variation and signaling function is extremely complex. It appears unlikely that one particular amino acid substitution or deletion will define a disease-associated variant of LMP-1.

MeSH Terms
Amino Acid Sequence Genetic Variation Herpesvirus 4, Human/physiology Humans Jurkat Cells Molecular Sequence Data Signal Transduction Structure-Activity Relationship Viral Matrix Proteins/genetics Virus Replication/genetics
Chemicals
EBV-associated membrane antigen, Epstein-Barr virus Viral Matrix Proteins
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Fielding C A
Section of Infection and Immunity, Department of Medicine, University of Wales College of Medicine, Cardiff CF14 4XN, Wales, United Kingdom.
Sandvej K
Mehl A
Brennan P
Jones M
Rowe M
References (78)
78 references, click to expand
  1. High-level nuclear NF-kappa B and Oct-2 is a common feature of cultured Hodgkin/Reed-Sternberg cells.
    Blood. 1996 May 15;87(10):4340-7 PMID: 8639794
  2. Epstein-Barr virus latent membrane protein-1 oncogene deletions: correlations with malignancy in Epstein-Barr virus--associated lymphoproliferative disorders and malignant lymphomas.
    Blood. 1996 Jul 1;88(1):242-51 PMID: 8704180
  3. Constitutive activation of STAT proteins in primary lymphoid and myeloid leukemia cells and in Epstein-Barr virus (EBV)-related lymphoma cell lines.
    Blood. 1996 Aug 1;88(3):809-16 PMID: 8704235
  4. Expression of the Epstein Barr virus transforming protein LMP1 causes a rapid and transient stimulation of the Bcl-2 homologue Mcl-1 levels in B-cell lines.
    Cancer Res. 1996 Oct 15;56(20):4610-3 PMID: 8840972
  5. Analysis of Epstein-Barr virus gene polymorphisms in normal donors and in virus-associated tumors from different geographic locations.
    Blood. 1996 Nov 1;88(9):3491-501 PMID: 8896415
  6. Epstein-Barr virus latent membrane protein-1 (LMP1) signalling is distinct from CD40 and involves physical cooperation of its two C-terminus functional regions.
    Oncogene. 1998 Nov 5;17(18):2383-92 PMID: 9811470
  7. 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. 1999 Feb;73(2):1023-35 PMID: 9882303
  8. The molecular epidemiology and evolution of Epstein-Barr virus: sequence variation and genetic recombination in the latent membrane protein-1 gene.
    J Infect Dis. 1999 Apr;179(4):763-74 PMID: 10068570
  9. Functional analysis of different LMP1 proteins isolated from Epstein-Barr virus-positive carriers.
    Virus Res. 1999 Mar;60(1):41-54 PMID: 10225273
  10. LMP1 signal transduction differs substantially from TNF receptor 1 signaling in the molecular functions of TRADD and TRAF2.
    EMBO J. 1999 May 4;18(9):2511-21 PMID: 10228165
  11. 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. 1999 Jun 4;274(23):16085-96 PMID: 10347160
  12. Latent membrane protein 1 of Epstein-Barr virus interacts with JAK3 and activates STAT proteins.
    EMBO J. 1999 Jun 1;18(11):3064-73 PMID: 10357818
  13. 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-kappaB activation.
    Mol Cell Biol. 1999 Aug;19(8):5759-67 PMID: 10409763
  14. Signature amino acid changes in latent membrane protein 1 distinguish Epstein-Barr virus strains.
    Virology. 1999 Aug 15;261(1):79-95 PMID: 10441557
  15. 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
  16. Constitutive nuclear factor-kappaB-RelA activation is required for proliferation and survival of Hodgkin's disease tumor cells.
    J Clin Invest. 1997 Dec 15;100(12):2961-9 PMID: 9399941
  17. Epstein-Barr virus-mediated B-cell proliferation is dependent upon latent membrane protein 1, which simulates an activated CD40 receptor.
    EMBO J. 1998 Mar 16;17(6):1700-9 PMID: 9501091
  18. The 30-base-pair deletion in Chinese variants of the Epstein-Barr virus LMP1 gene is not the major effector of functional differences between variant LMP1 genes in human lymphocytes.
    J Virol. 1998 May;72(5):4038-48 PMID: 9557692
  19. 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
  20. The NPC derived C15 LMP1 protein confers enhanced activation of NF-kappa B and induction of the EGFR in epithelial cells.
    Oncogene. 1998 Apr 9;16(14):1869-77 PMID: 9583684
  21. Role of the TRAF binding site and NF-kappaB activation in Epstein-Barr virus latent membrane protein 1-induced cell gene expression.
    J Virol. 1998 Oct;72(10):7900-8 PMID: 9733827
  22. The bfl-1 gene is transcriptionally upregulated by the Epstein-Barr virus LMP1, and its expression promotes the survival of a Burkitt's lymphoma cell line.
    J Virol. 2000 Jul;74(14):6652-8 PMID: 10864681
  23. Identification of functional differences between prototype Epstein-Barr virus-encoded LMP1 and a nasopharyngeal carcinoma-derived LMP1 in human epithelial cells.
    Virology. 2000 Jun 20;272(1):204-17 PMID: 10873763
  24. Degradation of the epstein-barr virus latent membrane protein 1 (LMP1) by the ubiquitin-proteasome pathway. Targeting via ubiquitination of the N-terminal residue.
    J Biol Chem. 2000 Aug 4;275(31):23491-9 PMID: 10807912
  25. Latent membrane protein 1 of Epstein-Barr virus inhibits as well as stimulates gene expression.
    J Virol. 2000 Oct;74(20):9755-61 PMID: 11000250
  26. Differences in the immunogenicity of latent membrane protein 1 (LMP1) encoded by Epstein-Barr virus genomes derived from LMP1-positive and -negative nasopharyngeal carcinoma.
    Cancer Res. 2000 Oct 1;60(19):5589-93 PMID: 11034108
  27. Analysis of the Epstein-Barr virus (EBV) latent membrane protein 1 (LMP-1) gene and promoter in Hodgkin's disease isolates: selection against EBV variants with mutations in the LMP-1 promoter ATF-1/CREB-1 binding site.
    Mol Pathol. 2000 Oct;53(5):280-8 PMID: 11091852
  28. Characterization of intercellular adhesion molecule-1 regulation by Epstein-Barr virus-encoded latent membrane protein-1 identifies pathways that cooperate with nuclear factor kappa B to activate transcription.
    J Biol Chem. 2001 Jan 12;276(2):984-92 PMID: 11034993
  29. Mechanism of action of a novel latent membrane protein-1 dominant negative.
    J Biol Chem. 2001 Jan 12;276(2):1195-203 PMID: 11031256
  30. Linkage between STAT regulation and Epstein-Barr virus gene expression in tumors.
    J Virol. 2001 Mar;75(6):2929-37 PMID: 11222718
  31. The transmembrane domains of the EBV-encoded latent membrane protein 1 (LMP1) variant CAO regulate enhanced signalling activity.
    Virology. 2001 Apr 10;282(2):278-87 PMID: 11289810
  32. CD99 expression is positively regulated by Sp1 and is negatively regulated by Epstein-Barr virus latent membrane protein 1 through nuclear factor-kappaB.
    Blood. 2001 Jun 1;97(11):3596-604 PMID: 11369656
  33. Establishment in continuous culture of a new type of lymphocyte from a "Burkitt like" malignant lymphoma (line D.G.-75).
    Int J Cancer. 1977 Jan;19(1):27-33 PMID: 188769
  34. An EBV membrane protein expressed in immortalized lymphocytes transforms established rodent cells.
    Cell. 1985 Dec;43(3 Pt 2):831-40 PMID: 3000618
  35. Influence of the Epstein-Barr virus nuclear antigen EBNA 2 on the growth phenotype of virus-transformed B cells.
    J Virol. 1987 May;61(5):1310-7 PMID: 3033261
  36. Monoclonal antibodies to the latent membrane protein of Epstein-Barr virus reveal heterogeneity of the protein and inducible expression in virus-transformed cells.
    J Gen Virol. 1987 Jun;68 ( Pt 6):1575-86 PMID: 2438376
  37. Differences in B cell growth phenotype reflect novel patterns of Epstein-Barr virus latent gene expression in Burkitt's lymphoma cells.
    EMBO J. 1987 Sep;6(9):2743-51 PMID: 2824192
  38. Epstein-Barr virus gene expression in nasopharyngeal carcinoma.
    J Gen Virol. 1988 May;69 ( Pt 5):1051-65 PMID: 2836550
  39. Transformation of Balb 3T3 cells by the BNLF-1 gene of Epstein-Barr virus.
    Oncogene. 1988 May;2(5):461-7 PMID: 2836780
  40. Expression of Epstein-Barr virus-encoded proteins in nasopharyngeal carcinoma.
    Int J Cancer. 1988 Sep 15;42(3):329-38 PMID: 2843473
  41. Epstein-Barr virus latent infection membrane protein alters the human B-lymphocyte phenotype: deletion of the amino terminus abolishes activity.
    J Virol. 1988 Nov;62(11):4173-84 PMID: 2845129
  42. Expression of Epstein-Barr virus transformation-associated genes in tissues of patients with EBV lymphoproliferative disease.
    N Engl J Med. 1989 Oct 19;321(16):1080-5 PMID: 2552313
  43. Signal transduction through the T cell receptor-CD3 complex. Evidence for heterogeneity in receptor coupling.
    J Immunol. 1990 May 15;144(10):3651-8 PMID: 1970588
  44. Expression of the BNLF-1 oncogene of Epstein-Barr virus in the skin of transgenic mice induces hyperplasia and aberrant expression of keratin 6.
    Cell. 1990 Jun 29;61(7):1315-27 PMID: 1694724
  45. Expression of Epstein-Barr virus latent gene products in tumour cells of Hodgkin's disease.
    Lancet. 1991 Feb 9;337(8737):320-2 PMID: 1671232
  46. Epstein-Barr virus latent membrane protein expression in Hodgkin and Reed-Sternberg cells.
    Proc Natl Acad Sci U S A. 1991 Jun 1;88(11):4766-70 PMID: 1647016
  47. 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
  48. Isolation and sequencing of the Epstein-Barr virus BNLF-1 gene (LMP1) from a Chinese nasopharyngeal carcinoma.
    J Gen Virol. 1991 Oct;72 ( Pt 10):2399-409 PMID: 1681026
  49. Three pathways of Epstein-Barr virus gene activation from EBNA1-positive latency in B lymphocytes.
    J Virol. 1992 Jan;66(1):122-31 PMID: 1309242
  50. 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
  51. Cloning and characterization of the latent membrane protein (LMP) of a specific Epstein-Barr virus variant derived from the nasopharyngeal carcinoma in the Taiwanese population.
    Oncogene. 1992 Nov;7(11):2131-40 PMID: 1331932
  52. 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
  53. Clonability and tumorigenicity of human epithelial cells expressing the EBV encoded membrane protein LMP1.
    Oncogene. 1993 Jun;8(6):1575-83 PMID: 8389032
  54. Phosphatidylcholine hydrolysis activates NF-kappa B and increases human immunodeficiency virus replication in human monocytes and T lymphocytes.
    J Virol. 1993 Nov;67(11):6596-604 PMID: 8411362
  55. Deletions within the LMP1 oncogene of Epstein-Barr virus are clustered in Hodgkin's disease and identical to those observed in nasopharyngeal carcinoma.
    Blood. 1993 Nov 15;82(10):2937-42 PMID: 8219183
  56. Epstein-Barr virus (EBV)-encoded membrane protein LMP1 from a nasopharyngeal carcinoma is non-immunogenic in a murine model system, in contrast to a B cell-derived homologue.
    Eur J Cancer. 1994;30A(1):84-8 PMID: 8142171
  57. Identification of potential hot spots in the carboxy-terminal part of the Epstein-Barr virus (EBV) BNLF-1 gene in both malignant and benign EBV-associated diseases: high frequency of a 30-bp deletion in Malaysian and Danish peripheral T-cell lymphomas.
    Blood. 1994 Dec 15;84(12):4053-60 PMID: 7994023
  58. Mutational hot spots within the carboxy terminal region of the LMP1 oncogene of Epstein-Barr virus are frequent in lymphoproliferative disorders.
    Oncogene. 1995 Feb 2;10(3):523-8 PMID: 7845677
  59. 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
  60. 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
  61. 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
  62. 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. 1999 Dec;73(12):9908-16 PMID: 10559303
  63. Latent membrane protein 1 associated signaling pathways are important in tumor cells of Epstein-Barr virus negative Hodgkin's disease.
    Oncogene. 1999 Nov 25;18(50):7161-7 PMID: 10597317
  64. Novel intertypic recombinants of epstein-barr virus in the chinese population.
    J Virol. 2000 Feb;74(3):1544-8 PMID: 10627567
  65. Inducible loss of NF-kappaB activity is associated with apoptosis and Bcl-2 down-regulation in Epstein-Barr virus-transformed B lymphocytes.
    Blood. 2000 Mar 15;95(6):2068-75 PMID: 10706876
  66. Involvement of two NF-kappa B binding elements in tumor necrosis factor alpha -, CD40-, and epstein-barr virus latent membrane protein 1-mediated induction of the cellular inhibitor of apoptosis protein 2 gene.
    J Biol Chem. 2000 Jun 16;275(24):18022-8 PMID: 10751398
  67. 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
  68. Characterization of LMP-1's association with TRAF1, TRAF2, and TRAF3.
    J Virol. 1997 Jun;71(6):4649-56 PMID: 9151858
  69. Epstein-Barr virus-encoded LMP1 and CD40 mediate IL-6 production in epithelial cells via an NF-kappaB pathway involving TNF receptor-associated factors.
    Oncogene. 1997 Jun 19;14(24):2899-916 PMID: 9205097
  70. Sequence analysis of the Epstein-Barr virus (EBV) latent membrane protein-1 gene and promoter region: identification of four variants among wild-type EBV isolates.
    Blood. 1997 Jul 1;90(1):323-30 PMID: 9207468
  71. Inhibition of in vitro proliferation of Epstein Barr Virus infected B cells by an antisense oligodeoxynucleotide targeted against EBV latent membrane protein LMP1.
    Oncogene. 1997 Jul 24;15(4):489-93 PMID: 9242386
  72. Localization of the major NF-kappaB-activating site and the sole TRAF3 binding site of LMP-1 defines two distinct signaling motifs.
    J Biol Chem. 1997 Aug 8;272(32):19777-84 PMID: 9242637
  73. 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
  74. 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
  75. 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
  76. Differences in the growth pattern and clinical course of EBV-LMP1 expressing and non-expressing nasopharyngeal carcinomas.
    Eur J Cancer. 1995;31A(5):658-60 PMID: 7640034
  77. Interleukin-2 activation of STAT5 requires the convergent action of tyrosine kinases and a serine/threonine kinase pathway distinct from the Raf1/ERK2 MAP kinase pathway.
    EMBO J. 1996 Apr 15;15(8):1902-13 PMID: 8617237
  78. Effect of a 10-amino acid deletion on the oncogenic activity of latent membrane protein 1 of Epstein-Barr virus.
    Oncogene. 1996 May 16;12(10):2129-35 PMID: 8668338
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
Published
2001-10-00
Pages
9129-41
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC114482
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: product@genelibs.com