Home LiteratureArticle Details
PMID: 19439479 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't

Features distinguishing Epstein-Barr virus infections of epithelial cells and B cells: viral genome expression, genome maintenance, and genome amplification.

Journal of virology ·Vol. 83 ·No. 15 ·2009-08-00 ·Pages 7749-60

Shannon-Lowe C, Adland E, Bell AI, Delecluse HJ, Rickinson AB, Rowe M

Abstract

Epstein-Barr virus (EBV) is associated with malignant diseases of lymphoid and epithelial cell origin. The tropism of EBV is due to B-cell-restricted expression of CD21, the major receptor molecule for the virus. However, efficient infection of CD21- epithelial cells can be achieved via transfer from EBV-coated B cells. We compare and contrast here the early events following in vitro infection of primary B cells and epithelial cells. Using sensitive, quantitative reverse transcription-PCR assays for several latent and lytic transcripts and two-color immunofluorescence staining to analyze expression at the single cell level, we confirmed and extended previous reports indicating that the two cell types support different patterns of transcription. Furthermore, whereas infection of B cells with one or two copies of EBV resulted in rapid amplification of the viral genome to >20 copies per cell, such amplification was not normally observed after infection of primary epithelial cells or undifferentiated epithelial lines. In epithelial cells, EBNA1 expression was detected in only ca. 40% of EBER+ cells, and the EBV genome was subsequently lost during prolonged culture. One exception was that infection of AGS, a gastric carcinoma line, resulted in maintenance of EBNA1 expression and amplification of the EBV episome. In contrast to B cells, where amplification of the EBV episome occurred even with a replication-defective BZLF1-knockout virus, amplification in AGS cells was dependent upon early lytic cycle gene expression. These data highlight the influence of the host cell on the outcome of EBV infection with regard to genome expression, amplification, and maintenance.

MeSH Terms
B-Lymphocytes/virology Cell Line Cells, Cultured Epithelial Cells/virology Epstein-Barr Virus Infections/virology Gene Amplification Gene Expression Regulation, Viral Genome, Viral Herpesvirus 4, Human/genetics,physiology Humans Virus Internalization Virus Replication
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Shannon-Lowe Claire
CR-UK Institute for Cancer Studies, The University of Birmingham, Vincent Drive, Birmingham B15 2TT, United Kingdom.
Adland Emily
Bell Andrew I
Delecluse Henri-Jacques
Rickinson Alan B
Rowe Martin
References (67)
67 references, click to expand
  1. The amino terminus of Epstein-Barr Virus (EBV) nuclear antigen 1 contains AT hooks that facilitate the replication and partitioning of latent EBV genomes by tethering them to cellular chromosomes.
    J Virol. 2004 Nov;78(21):11487-505 PMID: 15479791
  2. Epstein-Barr virus (EBV) infection in infectious mononucleosis: virus latency, replication and phenotype of EBV-infected cells.
    J Pathol. 1997 Jun;182(2):151-9 PMID: 9274524
  3. The average number of molecules of Epstein-Barr nuclear antigen 1 per cell does not correlate with the average number of Epstein-Barr virus (EBV) DNA molecules per cell among different clones of EBV-immortalized cells.
    J Virol. 1990 May;64(5):2407-10 PMID: 2157896
  4. Epstein-Barr virus expression within keratinizing nasopharyngeal carcinoma.
    J Med Virol. 1998 Jul;55(3):227-33 PMID: 9624611
  5. The EBV nuclear antigen 1 (EBNA1) enhances B cell immortalization several thousandfold.
    Proc Natl Acad Sci U S A. 2003 Sep 16;100(19):10989-94 PMID: 12947043
  6. Distribution and phenotype of Epstein-Barr virus-infected cells in human pharyngeal tonsils.
    Mod Pathol. 2005 Apr;18(4):519-27 PMID: 15696119
  7. Persistent productive Epstein-Barr virus replication in normal epithelial cells in vivo.
    J Infect Dis. 2001 Dec 15;184(12):1499-507 PMID: 11740724
  8. Glycoprotein gp110 of Epstein-Barr virus determines viral tropism and efficiency of infection.
    Proc Natl Acad Sci U S A. 2002 Nov 12;99(23):15036-41 PMID: 12409611
  9. Epstein-Barr virus replication in oropharyngeal epithelial cells.
    N Engl J Med. 1984 May 10;310(19):1225-30 PMID: 6323983
  10. Transcription of the Epstein-Barr virus gene EBNA-1 from different promoters in nasopharyngeal carcinoma and B-lymphoblastoid cells.
    J Virol. 1992 Feb;66(2):706-14 PMID: 1370554
  11. Expression of proteins encoded by Epstein-Barr virus trans-activator genes depends on the differentiation of epithelial cells in oral hairy leukoplakia.
    Proc Natl Acad Sci U S A. 1991 Oct 1;88(19):8332-6 PMID: 1656439
  12. A complete set of overlapping cosmid clones of M-ABA virus derived from nasopharyngeal carcinoma and its similarity to other Epstein-Barr virus isolates.
    Gene. 1984 Mar;27(3):279-88 PMID: 6329907
  13. EBV persistence in memory B cells in vivo.
    Immunity. 1998 Sep;9(3):395-404 PMID: 9768759
  14. Monoclonal antibody against a 250,000-dalton glycoprotein of Epstein-Barr virus identifies a membrane antigen and a neutralizing antigen.
    Proc Natl Acad Sci U S A. 1980 May;77(5):2979-83 PMID: 6248876
  15. Expression of Epstein-Barr virus latent genes in oral epithelium: determinants of the pathogenesis of oral hairy leukoplakia.
    J Infect Dis. 2004 Jul 15;190(2):396-9 PMID: 15216478
  16. Epstein-Barr virus small RNAs potentiate tumorigenicity of Burkitt lymphoma cells independently of an effect on apoptosis.
    J Virol. 2000 Nov;74(21):10223-8 PMID: 11024153
  17. The Epstein-Barr virus lytic program is controlled by the co-operative functions of two transactivators.
    EMBO J. 2000 Jun 15;19(12):3080-9 PMID: 10856251
  18. Upregulation of bcl-2 by the Epstein-Barr virus latent membrane protein LMP1: a B-cell-specific response that is delayed relative to NF-kappa B activation and to induction of cell surface markers.
    J Virol. 1994 Sep;68(9):5602-12 PMID: 7520093
  19. Epstein-Barr virus-induced B-cell transformation: quantitating events from virus binding to cell outgrowth.
    J Gen Virol. 2005 Nov;86(Pt 11):3009-3019 PMID: 16227222
  20. Analysis of Epstein-Barr virus latent gene expression in endemic Burkitt's lymphoma and nasopharyngeal carcinoma tumour cells by using quantitative real-time PCR assays.
    J Gen Virol. 2006 Oct;87(Pt 10):2885-2890 PMID: 16963746
  21. Epstein-Barr virus (EBV) LMP2A mediates B-lymphocyte survival through constitutive activation of the Ras/PI3K/Akt pathway.
    Oncogene. 2004 Nov 11;23(53):8619-28 PMID: 15361852
  22. Epstein-Barr virus infection in oral hairy leukoplakia: virus replication in the absence of a detectable latent phase.
    J Gen Virol. 1991 Dec;72 ( Pt 12):3035-46 PMID: 1662695
  23. 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
  24. Epstein-Barr virus (EBV) gene expression in lymphoid B cells during acute infectious mononucleosis (IM) and clonality of the directly growing cell lines.
    Int J Cancer. 1997 May 2;71(3):345-9 PMID: 9139865
  25. Metaphase chromosome tethering is necessary for the DNA synthesis and maintenance of oriP plasmids but is insufficient for transcription activation by Epstein-Barr nuclear antigen 1.
    J Virol. 2003 Nov;77(21):11767-80 PMID: 14557661
  26. 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
  27. Expression of Epstein-Barr virus lytic gene BRLF1 in nasopharyngeal carcinoma: potential use in diagnosis.
    J Gen Virol. 2000 Oct;81(Pt 10):2417-2423 PMID: 10993929
  28. Latent membrane protein 1 is critical for efficient growth transformation of human B cells by epstein-barr virus.
    Cancer Res. 2003 Jun 1;63(11):2982-9 PMID: 12782607
  29. Multiple pathways for Epstein-Barr virus episome loss from nasopharyngeal carcinoma.
    Int J Cancer. 2008 Nov 1;123(9):2105-12 PMID: 18688856
  30. Resting B cells as a transfer vehicle for Epstein-Barr virus infection of epithelial cells.
    Proc Natl Acad Sci U S A. 2006 May 2;103(18):7065-70 PMID: 16606841
  31. A positive autoregulatory loop of LMP1 expression and STAT activation in epithelial cells latently infected with Epstein-Barr virus.
    J Virol. 2003 Apr;77(7):4139-48 PMID: 12634372
  32. Identification of Epstein-Barr virus lytic activity in post-transplantation lymphoproliferative disease.
    Mod Pathol. 1996 Jun;9(6):621-30 PMID: 8782198
  33. Identification of a novel promoter located within the Bam HI Q region of the Epstein-Barr virus genome for the EBNA 1 gene.
    DNA Cell Biol. 1995 Sep;14(9):767-76 PMID: 7669254
  34. 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
  35. LMP1 of Epstein-Barr virus suppresses cellular senescence associated with the inhibition of p16INK4a expression.
    Oncogene. 2000 Apr 13;19(16):2002-13 PMID: 10803461
  36. Epstein-Barr virus latent membrane protein 1 blocks p53-mediated apoptosis through the induction of the A20 gene.
    J Virol. 1996 Dec;70(12):8653-9 PMID: 8970991
  37. Epstein-Barr virus infection in ex vivo tonsil epithelial cell cultures of asymptomatic carriers.
    J Virol. 2004 Nov;78(22):12613-24 PMID: 15507648
  38. Critical role of Epstein-Barr Virus (EBV)-encoded RNA in efficient EBV-induced B-lymphocyte growth transformation.
    J Virol. 2005 Apr;79(7):4298-307 PMID: 15767430
  39. The Epstein-Barr virus latency BamHI-Q promoter is positively regulated by STATs and Zta interference with JAK/STAT activation leads to loss of BamHI-Q promoter activity.
    Proc Natl Acad Sci U S A. 1999 Aug 3;96(16):9339-44 PMID: 10430944
  40. Synchronous and sequential activation of latently infected Epstein-Barr virus genomes.
    J Virol. 1989 Jan;63(1):445-9 PMID: 2462063
  41. Epstein-Barr virus infection and replication in a human epithelial cell system.
    Nature. 1992 Mar 26;356(6367):347-50 PMID: 1312681
  42. Transcriptional analysis of Epstein-Barr virus gene expression in EBV-positive gastric carcinoma: unique viral latency in the tumour cells.
    Br J Cancer. 1996 Aug;74(4):625-31 PMID: 8761381
  43. Latent Marek's disease virus can be activated from its chromosomally integrated state in herpesvirus-transformed lymphoma cells.
    EMBO J. 1993 Aug;12(8):3277-86 PMID: 8393785
  44. Elevated expression of ICAM1 (CD54) and minimal expression of LFA3 (CD58) in Epstein-Barr-virus-positive nasopharyngeal carcinoma cells.
    Int J Cancer. 1992 Apr 1;50(6):863-7 PMID: 1372880
  45. 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
  46. An Epstein-Barr virus-encoded microRNA targets PUMA to promote host cell survival.
    J Exp Med. 2008 Oct 27;205(11):2551-60 PMID: 18838543
  47. In vitro production of stable Epstein-Barr virus-positive epithelial cell clones which resemble the virus:cell interaction observed in nasopharyngeal carcinoma.
    Virology. 1996 Jan 1;215(1):40-50 PMID: 8553585
  48. Differentiation-associated expression of the Epstein-Barr virus BZLF1 transactivator protein in oral hairy leukoplakia.
    J Virol. 1991 Jun;65(6):2868-74 PMID: 1851858
  49. Cell-to-cell contact as an efficient mode of Epstein-Barr virus infection of diverse human epithelial cells.
    J Virol. 1998 May;72(5):4371-8 PMID: 9557727
  50. Expression of the Epstein-Barr virus immediate early gene, BZLF1, in nasopharyngeal carcinoma tumor cells.
    Virology. 1993 Nov;197(1):358-65 PMID: 8212572
  51. 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
  52. 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
  53. Epstein-Barr virus and carcinomas. Expression of the viral genome in an undifferentiated gastric carcinoma.
    Diagn Mol Pathol. 1992 Jun;1(2):103-8 PMID: 1342957
  54. Comparison of plasma Epstein-Barr virus (EBV) DNA levels and serum EBV immunoglobulin A/virus capsid antigen antibody titers in patients with nasopharyngeal carcinoma.
    Cancer. 2004 Mar 15;100(6):1162-70 PMID: 15022282
  55. Strict lymphotropism of Epstein-Barr virus during acute infectious mononucleosis in nonimmunocompromised individuals.
    Blood. 1997 Apr 15;89(8):2856-62 PMID: 9108405
  56. Epstein-Barr virus LMP1 blocks p16INK4a-RB pathway by promoting nuclear export of E2F4/5.
    J Cell Biol. 2003 Jul 21;162(2):173-83 PMID: 12860972
  57. Qualitative analysis of the expression of Epstein-Barr virus lytic genes in nasopharyngeal carcinoma biopsies.
    J Gen Virol. 1995 Jun;76 ( Pt 6):1401-8 PMID: 7782768
  58. 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
  59. Mapping EBNA-1 domains involved in binding to metaphase chromosomes.
    J Virol. 1999 May;73(5):4385-92 PMID: 10196336
  60. Hairy leukoplakia: an unusual combination of transforming and permissive Epstein-Barr virus infections.
    J Virol. 2000 Aug;74(16):7610-8 PMID: 10906215
  61. Detection of circular and linear herpesvirus DNA molecules in mammalian cells by gel electrophoresis.
    J Virol. 1984 Apr;50(1):248-54 PMID: 6321792
  62. Epstein-Barr virus latent membrane protein 2A is a B-cell receptor mimic and essential for B-cell survival.
    Blood. 2007 Nov 15;110(10):3715-21 PMID: 17682125
  63. 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
  64. The Epstein-Barr virus latent membrane protein 1 induces expression of the epidermal growth factor receptor.
    J Virol. 1995 Jul;69(7):4390-8 PMID: 7769701
  65. Epstein-Barr virus latent gene transcription in nasopharyngeal carcinoma cells: coexpression of EBNA1, LMP1, and LMP2 transcripts.
    J Virol. 1992 May;66(5):2689-97 PMID: 1313894
  66. 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
  67. Production of high-titer Epstein-Barr virus recombinants derived from Akata cells by using a bacterial artificial chromosome system.
    J Virol. 2004 Jul;78(13):7004-15 PMID: 15194777
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
1098-5514
Published
2009-08-00
Epub
2009-00-13
Pages
7749-60
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC2708605
Subset
IM
Grants
Worldwide Cancer Research · 07-0481 · United Kingdom
Cancer Research UK · 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: product@genelibs.com