Home LiteratureArticle Details
PMID: 16076866 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Rescue of "crippled" germinal center B cells from apoptosis by Epstein-Barr virus.

Blood ·Vol. 106 ·No. 13 ·2005-12-15 ·Pages 4339-44

Mancao C, Altmann M, Jungnickel B, Hammerschmidt W

Abstract

Epstein-Barr virus (EBV) is associated with B-cell lymphomas such as Hodgkin lymphoma, Burkitt lymphoma, and post-transplantation lymphoma, which originate from clonal germinal center (GC) B cells. During the process of somatic hypermutation, GC B cells can acquire deleterious or nonsense mutations in the heavy and light immunoglobulin genes. Such mutations abrogate the cell surface expression of the B-cell receptor (BCR), which results in the elimination of these nonfunctional B cells by immediate apoptosis. EBV encodes several latent genes, among them latent membrane protein 1 (LMP1) and LMP2A, which are regularly expressed in EBV-positive Hodgkin lymphoma and posttransplantation lymphomas. Since LMP1 and LMP2A mimic the function of 2 key receptors on B cells, CD40 and BCR, respectively, we wanted to learn whether EBV infection can rescue proapoptotic GC B cells with crippling mutations in the heavy chain immunoglobulin locus from apoptosis. We show here that BCR-negative GC B cells readily enter the cell cycle upon infection with EBV in vitro and yield clonal lymphoblastoid cell lines that are incapable of expressing a functional BCR because the rearranged and formerly functional heavy chain immunoglobulin alleles carry deleterious mutations. Our findings imply an important role for EBV in the process of lymphomagenesis in certain cases of Hodgkin lymphoma and posttransplantation lymphomas.

MeSH Terms
Apoptosis B-Lymphocytes/immunology,metabolism,pathology Base Sequence Cells, Cultured Germinal Center/chemistry,immunology,pathology Herpesvirus 4, Human/physiology Humans Lymphoma/genetics,immunology,pathology,virology Molecular Sequence Data Sequence Alignment Sequence Homology, Nucleic Acid Somatic Hypermutation, Immunoglobulin/genetics
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Mancao Christoph
GSF-National Research Center for Environment and Health, Department of Gene Vectors, Marchioninistr 25, D-81377 Munich, Germany.
Altmann Markus
Jungnickel Berit
Hammerschmidt Wolfgang
References (44)
44 references, click to expand
  1. 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
  2. Transformation of BCR-deficient germinal-center B cells by EBV supports a major role of the virus in the pathogenesis of Hodgkin and posttransplantation lymphomas.
    Blood. 2005 Dec 15;106(13):4345-50 PMID: 16131568
  3. CD77: an antigen of germinal center B cells entering apoptosis.
    Eur J Immunol. 1991 May;21(5):1131-40 PMID: 1709864
  4. 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
  5. Epstein-Barr virus and Hodgkin's disease: transcriptional analysis of virus latency in the malignant cells.
    J Exp Med. 1993 Feb 1;177(2):339-49 PMID: 8381153
  6. 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
  7. Monoclonal antibodies directed against the Epstein-Barr virus-encoded nuclear antigen 1 (EBNA1): immunohistologic detection of EBNA1 in the malignant cells of Hodgkin's disease.
    Blood. 1994 Dec 1;84(11):3792-8 PMID: 7949135
  8. Antigen and Fc receptor signaling. The awesome power of the immunoreceptor tyrosine-based activation motif (ITAM).
    J Immunol. 1995 Oct 1;155(7):3281-5 PMID: 7561018
  9. Clonal selection and learning in the antibody system.
    Nature. 1996 Jun 27;381(6585):751-8 PMID: 8657279
  10. Hodgkin and Reed-Sternberg cells in Hodgkin's disease represent the outgrowth of a dominant tumor clone derived from (crippled) germinal center B cells.
    J Exp Med. 1996 Oct 1;184(4):1495-505 PMID: 8879220
  11. Epstein-Barr virus provides a new paradigm: a requirement for the immediate inhibition of apoptosis.
    PLoS Biol. 2005 Dec;3(12):e404 PMID: 16277553
  12. Rare occurrence of classical Hodgkin's disease as a T cell lymphoma.
    J Exp Med. 2000 Jan 17;191(2):387-94 PMID: 10637283
  13. Hodgkin and reed-sternberg cells represent an expansion of a single clone originating from a germinal center B-cell with functional immunoglobulin gene rearrangements but defective immunoglobulin transcription.
    Blood. 2000 Feb 15;95(4):1443-50 PMID: 10666223
  14. The expression pattern of Epstein-Barr virus latent genes in vivo is dependent upon the differentiation stage of the infected B cell.
    Immunity. 2000 Oct;13(4):497-506 PMID: 11070168
  15. Molecular biology of Hodgkin's lymphoma.
    Adv Cancer Res. 2002;84:277-312 PMID: 11883530
  16. The effects of the Epstein-Barr virus latent membrane protein 2A on B cell function.
    Int Rev Immunol. 2001;20(6):805-35 PMID: 11913951
  17. B-lymphocyte subpopulations are equally susceptible to Epstein-Barr virus infection, irrespective of immunoglobulin isotype expression.
    Immunology. 2003 Apr;108(4):427-30 PMID: 12667203
  18. B cells under influence: transformation of B cells by Epstein-Barr virus.
    Nat Rev Immunol. 2003 Oct;3(10):801-12 PMID: 14523386
  19. Part I: Hodgkin's lymphoma--molecular biology of Hodgkin and Reed-Sternberg cells.
    Lancet Oncol. 2004 Jan;5(1):11-8 PMID: 14700604
  20. B cell receptor signal strength determines B cell fate.
    Nat Immunol. 2004 Mar;5(3):317-27 PMID: 14758357
  21. Molecular single-cell PCR analysis of rearranged immunoglobulin genes as a tool to determine the clonal composition of normal and malignant human B cells.
    Methods Mol Biol. 2004;271:225-38 PMID: 15146124
  22. Unique CD40-mediated biological program in B cell activation requires both type 1 and type 2 NF-kappaB activation pathways.
    Proc Natl Acad Sci U S A. 2004 May 25;101(21):8108-13 PMID: 15148378
  23. Survival of resting mature B lymphocytes depends on BCR signaling via the Igalpha/beta heterodimer.
    Cell. 2004 Jun 11;117(6):787-800 PMID: 15186779
  24. Epstein-Barr virus sustains Burkitt's lymphomas and Hodgkin's disease.
    Trends Mol Med. 2004 Jul;10(7):331-6 PMID: 15242681
  25. Epstein-Barr virus transformation of human pre-B cells.
    J Exp Med. 1983 Aug 1;158(2):616-22 PMID: 6310019
  26. Epstein-Barr virus transforms precursor B cells even before immunoglobulin gene rearrangements.
    Nature. 1984 May 24-30;309(5966):369-72 PMID: 6328311
  27. Epstein-Barr virus-transformed human precursor B cell lines: altered growth phenotype of lines with germ-line or rearranged but nonexpressed heavy chain genes.
    Eur J Immunol. 1987 Aug;17(8):1199-207 PMID: 3040424
  28. Antigen receptor tail clue.
    Nature. 1989 Mar 30;338(6214):383-4 PMID: 2927501
  29. 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
  30. Mechanism of antigen-driven selection in germinal centres.
    Nature. 1989 Dec 21-28;342(6252):929-31 PMID: 2594086
  31. Long-term human B cell lines dependent on interleukin-4 and antibody to CD40.
    Science. 1991 Jan 4;251(4989):70-2 PMID: 1702555
  32. 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
  33. Germinal center founder cells display propensity for apoptosis before onset of somatic mutation.
    J Exp Med. 1997 Feb 3;185(3):563-71 PMID: 9053456
  34. Hodgkin and Reed-Sternberg cells in lymphocyte predominant Hodgkin disease represent clonal populations of germinal center-derived tumor B cells.
    Proc Natl Acad Sci U S A. 1997 Aug 19;94(17):9337-42 PMID: 9256483
  35. Immunohistochemical detection of the Epstein-Barr virus-encoded latent membrane protein 2A in Hodgkin's disease and infectious mononucleosis.
    Blood. 1997 Aug 15;90(4):1664-72 PMID: 9269787
  36. The immunoreceptor tyrosine-based activation motif of Epstein-Barr virus LMP2A is essential for blocking BCR-mediated signal transduction.
    Virology. 1997 Sep 1;235(2):241-51 PMID: 9281504
  37. 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
  38. Presence of Epstein-Barr virus latency type III at the single cell level in post-transplantation lymphoproliferative disorders and AIDS related lymphomas.
    J Clin Pathol. 1997 Nov;50(11):911-8 PMID: 9462239
  39. 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
  40. Propagation and recovery of intact, infectious Epstein-Barr virus from prokaryotic to human cells.
    Proc Natl Acad Sci U S A. 1998 Jul 7;95(14):8245-50 PMID: 9653172
  41. Epstein-Barr virus LMP2A drives B cell development and survival in the absence of normal B cell receptor signals.
    Immunity. 1998 Sep;9(3):405-11 PMID: 9768760
  42. Latent membrane protein 1 of Epstein-Barr virus coordinately regulates proliferation with control of apoptosis.
    Oncogene. 2005 Mar 3;24(10):1711-7 PMID: 15674340
  43. Epstein-Barr virus infection in vitro can rescue germinal center B cells with inactivated immunoglobulin genes.
    Blood. 2005 Dec 15;106(13):4249-52 PMID: 16123211
  44. Early events in Epstein-Barr virus infection of human B lymphocytes.
    Virology. 1991 Apr;181(2):595-608 PMID: 1849678
Article Info
Journal
Blood
Abbr.
Blood
ISSN
0006-4971
Published
2005-12-15
Epub
2005-00-02
Pages
4339-44
Language
English
Region
United States
NLM ID
7603509
PMCID
PMC1895254
Subset
IM
Grants
NCI NIH HHS · CA70723 · 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: product@genelibs.com