Home LiteratureArticle Details
PMID: 2157875 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Epstein-Barr virus nuclear antigen 2 induces expression of the virus-encoded latent membrane protein.

Journal of virology ·Vol. 64 ·No. 5 ·1990-05-00 ·Pages 2126-34

Abbot SD, Rowe M, Cadwallader K, Ricksten A, Gordon J, Wang F, Rymo L, Rickinson AB

Abstract

Infection of Epstein-Barr virus-negative human B-lymphoma cell lines with the fully transforming B95.8 Epstein-Barr virus strain was associated with complete virus latent gene expression and a change in the cell surface and growth phenotype toward that of in vitro-transformed lymphoblastoid cell lines. In contrast, the cells infected with the P3HR1 Epstein-Barr virus strain, a deletion mutant that cannot encode Epstein-Barr nuclear antigen 2 (EBNA2) or a full-length EBNA-LP, expressed EBNAs1, 3a, 3b, and 3c but were negative for the latent membrane protein (LMP) and showed no change in cellular phenotype. This suggests that EBNA2 and/or EBNA-LP may be required for subsequent expression of LMP in Epstein-Barr virus-infected B cells. Recombinant vectors capable of expressing the B95.8 EBNA2A protein were introduced by electroporation into two P3HR1-converted B-lymphoma cell lines, BL30/P3 and BL41/P3. In both cases, stable expression of EBNA2A was accompanied by activation of LMP expression from the resident P3HR1 genome; control transfectants that did not express the EBNA2A protein never showed induction of LMP. In further experiments, a recombinant vector capable of expressing the full-length B95.8 EBNA-LP was introduced into the same target lines. Strong EBNA-LP expression was consistently observed in the transfected clones but was never accompanied by induction of LMP. The EBNA2A gene transfectants expressing EBNA2A and LMP showed a dramatic change in cell surface and growth phenotype toward a pattern like that of lymphoblastoid cell lines; some but not all of these changes could be reproduced in the absence of EBNA2A by transfection of P3HR1-converted cell lines with a recombinant vector expressing LMP. These studies suggest that EBNA2 plays an important dual role in the process of B-cell activation to the lymphoblastoid phenotype; the protein can have a direct effect upon cellular gene expression and is also involved in activating the expression of a second virus-encoded effector protein, LMP.

MeSH Terms
Antigens, Viral/genetics B-Lymphocytes Burkitt Lymphoma Cell Division Cell Line Cell Nucleus/immunology Cell Transformation, Viral Clone Cells DNA, Viral/genetics Epstein-Barr Virus Nuclear Antigens Gene Expression Herpesvirus 4, Human/genetics,immunology Humans Membrane Proteins/genetics Plasmids Transfection
Chemicals
Antigens, Viral DNA, Viral Epstein-Barr Virus Nuclear Antigens Membrane Proteins
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Abbot S D
Department of Cancer Studies, Medical School, University of Birmingham, England.
Rowe M
Cadwallader K
Ricksten A
Gordon J
Wang F
Rymo L
Rickinson A B
References (40)
40 references, click to expand
  1. Early events in Epstein-Barr virus infection provide a model for B cell activation.
    J Exp Med. 1985 Jul 1;162(1):45-59 PMID: 2989413
  2. 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
  3. An EBV membrane protein expressed in immortalized lymphocytes transforms established rodent cells.
    Cell. 1985 Dec;43(3 Pt 2):831-40 PMID: 3000618
  4. Induction of Epstein-Barr virus nuclear antigens.
    J Virol. 1986 Jun;58(3):988-90 PMID: 3084809
  5. Nucleotide sequences of mRNAs encoding Epstein-Barr virus nuclear proteins: a probable transcriptional initiation site.
    Proc Natl Acad Sci U S A. 1986 Jul;83(14):5096-100 PMID: 3460083
  6. Control of human B-lymphocyte replication. II. Transforming Epstein-Barr virus exploits three distinct viral signals to undermine three separate control points in B-cell growth.
    Immunology. 1986 Aug;58(4):591-5 PMID: 2426189
  7. A human intercellular adhesion molecule (ICAM-1) distinct from LFA-1.
    J Immunol. 1986 Aug 15;137(4):1270-4 PMID: 3525675
  8. A bicistronic Epstein-Barr virus mRNA encodes two nuclear proteins in latently infected, growth-transformed lymphocytes.
    J Virol. 1987 Apr;61(4):945-54 PMID: 3029429
  9. Epstein-Barr virus nuclear antigen 2 specifically induces expression of the B-cell activation antigen CD23.
    Proc Natl Acad Sci U S A. 1987 May;84(10):3452-6 PMID: 3033649
  10. 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
  11. The activation antigen BLAST-2, when shed, is an autocrine BCGF for normal and transformed B cells.
    EMBO J. 1987 Jun;6(6):1637-42 PMID: 3038527
  12. Identification of sequences in Epstein-Barr virus DNA required for the expression of the second Epstein-Barr virus-determined nuclear antigen in COS-1 cells.
    J Gen Virol. 1987 Sep;68 ( Pt 9):2407-18 PMID: 2821180
  13. 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
  14. Monoclonal and polyclonal antibodies against Epstein-Barr virus nuclear antigen 5 (EBNA-5) detect multiple protein species in Burkitt's lymphoma and lymphoblastoid cell lines.
    J Virol. 1987 Dec;61(12):3870-8 PMID: 2824821
  15. Epstein-Barr virus (EBV) induces expression of B-cell activation markers on in vitro infection of EBV-negative B-lymphoma cells.
    Proc Natl Acad Sci U S A. 1987 Nov;84(22):8060-4 PMID: 2825176
  16. Different patterns of Epstein-Barr virus gene expression and of cytotoxic T-cell recognition in B-cell lines infected with transforming (B95.8) or nontransforming (P3HR1) virus strains.
    J Virol. 1988 Mar;62(3):894-901 PMID: 2828684
  17. Differences between laboratory strains of Epstein-Barr virus based on immortalization, abortive infection, and interference.
    Proc Natl Acad Sci U S A. 1974 Oct;71(10):4006-10 PMID: 4372601
  18. Monoclonal antibodies to Epstein-Barr virus-induced, transformation-associated cell surface antigens: binding patterns and effect upon virus-specific T-cell cytotoxicity.
    Int J Cancer. 1982 Apr 15;29(4):373-81 PMID: 6282762
  19. Deletion of the nontransforming Epstein-Barr virus strain P3HR-1 causes fusion of the large internal repeat to the DSL region.
    J Virol. 1982 Sep;43(3):952-68 PMID: 6292473
  20. Epstein-Barr virus DNA XII. A variable region of the Epstein-Barr virus genome is included in the P3HR-1 deletion.
    J Virol. 1982 Sep;43(3):979-86 PMID: 6292475
  21. Non-immortalizing P3J-HR-1 Epstein-Barr virus: a deletion mutant of its transforming parent, Jijoye.
    J Virol. 1982 Dec;44(3):834-44 PMID: 6294333
  22. Three distinct antigens associated with human T-lymphocyte-mediated cytolysis: LFA-1, LFA-2, and LFA-3.
    Proc Natl Acad Sci U S A. 1982 Dec;79(23):7489-93 PMID: 6984191
  23. Fading of immunofluorescence during microscopy: a study of the phenomenon and its remedy.
    J Immunol Methods. 1982 Dec 17;55(2):231-42 PMID: 6819318
  24. A human lymphocyte-associated antigen involved in cell-mediated lympholysis.
    Eur J Immunol. 1983 Mar;13(3):202-8 PMID: 6339253
  25. A cis-acting element from the Epstein-Barr viral genome that permits stable replication of recombinant plasmids in latently infected cells.
    Proc Natl Acad Sci U S A. 1984 Jun;81(12):3806-10 PMID: 6328526
  26. Immortalized B lymphocytes produce B-cell growth factor.
    Nature. 1984 Jul 12-18;310(5973):145-7 PMID: 6610833
  27. DNA sequence and expression of the B95-8 Epstein-Barr virus genome.
    Nature. 1984 Jul 19-25;310(5974):207-11 PMID: 6087149
  28. A membrane protein encoded by Epstein-Barr virus in latent growth-transforming infection.
    Proc Natl Acad Sci U S A. 1984 Nov;81(22):7207-11 PMID: 6095274
  29. Expression of a second Epstein-Barr virus-determined nuclear antigen in mouse cells after gene transfer with a cloned fragment of the viral genome.
    Proc Natl Acad Sci U S A. 1985 May;82(10):3435-9 PMID: 2987926
  30. Downregulation of cell adhesion molecules LFA-3 and ICAM-1 in Epstein-Barr virus-positive Burkitt's lymphoma underlies tumor cell escape from virus-specific T cell surveillance.
    J Exp Med. 1988 Jun 1;167(6):1811-24 PMID: 2898508
  31. A spliced Epstein-Barr virus gene expressed in immortalized lymphocytes is created by circularization of the linear viral genome.
    EMBO J. 1988 Mar;7(3):769-74 PMID: 2840285
  32. 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
  33. Two related Epstein-Barr virus membrane proteins are encoded by separate genes.
    J Virol. 1989 Feb;63(2):933-7 PMID: 2536113
  34. Altered growth phenotype of a Burkitt's lymphoma line following the introduction and stable expression of the EBNA 2A gene.
    Curr Top Microbiol Immunol. 1988;141:149-56 PMID: 3215047
  35. Distinction between Epstein-Barr virus type A (EBNA 2A) and type B (EBNA 2B) isolates extends to the EBNA 3 family of nuclear proteins.
    J Virol. 1989 Mar;63(3):1031-9 PMID: 2536817
  36. Influence of Burkitt's lymphoma and primary B cells on latent gene expression by the nonimmortalizing P3J-HR-1 strain of Epstein-Barr virus.
    J Virol. 1989 Apr;63(4):1531-9 PMID: 2538644
  37. Epstein-Barr virus latent gene expression during the initiation of B cell immortalization.
    J Gen Virol. 1989 Jul;70 ( Pt 7):1755-64 PMID: 2544663
  38. Genetic analysis of immortalizing functions of Epstein-Barr virus in human B lymphocytes.
    Nature. 1989 Aug 3;340(6232):393-7 PMID: 2547164
  39. 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
  40. Epstein-Barr virus-encoded protein found in plasma membranes of transformed cells.
    J Virol. 1985 Sep;55(3):710-20 PMID: 2991591
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
Published
1990-05-00
Pages
2126-34
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC249370
Subset
IM
Grants
Wellcome Trust · United Kingdom
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]