Skip to main content
NCBI home page
Molecular Pathology : MP logoLink to Molecular Pathology : MP
. 1999 Dec;52(6):307–322. doi: 10.1136/mp.52.6.307

The Epstein-Barr virus and its association with human cancers.

K R Baumforth 1, L S Young 1, K J Flavell 1, C Constandinou 1, P G Murray 1
PMCID: PMC395716  PMID: 10748864

Abstract

The Epstein-Barr virus (EBV) has been linked to the development of a variety of human malignancies, including Burkitt's lymphoma, Hodgkin's disease, nasopharyngeal carcinoma, some T cell lymphomas, post-transplant lymphoproliferative disease, and more recently, certain cancers of the stomach and smooth muscle. This review summarizes these associations and in particular the role of the viral latent genes in the transformation process.

Full Text

The Full Text of this article is available as a PDF (320.2 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abbot S. D., Rowe M., Cadwallader K., Ricksten A., Gordon J., Wang F., Rymo L., Rickinson A. B. Epstein-Barr virus nuclear antigen 2 induces expression of the virus-encoded latent membrane protein. J Virol. 1990 May;64(5):2126–2134. doi: 10.1128/jvi.64.5.2126-2134.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Alexander F. E., Daniel C. P., Armstrong A. A., Clark D. A., Onions D. E., Cartwright R. A., Jarrett R. F. Case clustering, Epstein-Barr virus Reed-Sternberg cell status and herpes virus serology in Hodgkin's disease: results of a case-control study. Eur J Cancer. 1995;31A(9):1479–1486. doi: 10.1016/0959-8049(95)00117-2. [DOI] [PubMed] [Google Scholar]
  3. Alfieri C., Birkenbach M., Kieff E. Early events in Epstein-Barr virus infection of human B lymphocytes. Virology. 1991 Apr;181(2):595–608. doi: 10.1016/0042-6822(91)90893-g. [DOI] [PubMed] [Google Scholar]
  4. Anagnostopoulos I., Herbst H., Niedobitek G., Stein H. Demonstration of monoclonal EBV genomes in Hodgkin's disease and Ki-1-positive anaplastic large cell lymphoma by combined Southern blot and in situ hybridization. Blood. 1989 Aug 1;74(2):810–816. [PubMed] [Google Scholar]
  5. Armstrong A. A., Alexander F. E., Cartwright R., Angus B., Krajewski A. S., Wright D. H., Brown I., Lee F., Kane E., Jarrett R. F. Epstein-Barr virus and Hodgkin's disease: further evidence for the three disease hypothesis. Leukemia. 1998 Aug;12(8):1272–1276. doi: 10.1038/sj.leu.2401097. [DOI] [PubMed] [Google Scholar]
  6. Baichwal V. R., Sugden B. Transformation of Balb 3T3 cells by the BNLF-1 gene of Epstein-Barr virus. Oncogene. 1988 May;2(5):461–467. [PubMed] [Google Scholar]
  7. Barletta J. M., Kingma D. W., Ling Y., Charache P., Mann R. B., Ambinder R. F. Rapid in situ hybridization for the diagnosis of latent Epstein-Barr virus infection. Mol Cell Probes. 1993 Apr;7(2):105–109. doi: 10.1006/mcpr.1993.1014. [DOI] [PubMed] [Google Scholar]
  8. Bhat R. A., Thimmappaya B. Two small RNAs encoded by Epstein-Barr virus can functionally substitute for the virus-associated RNAs in the lytic growth of adenovirus 5. Proc Natl Acad Sci U S A. 1983 Aug;80(15):4789–4793. doi: 10.1073/pnas.80.15.4789. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Bonnet M., Guinebretiere J. M., Kremmer E., Grunewald V., Benhamou E., Contesso G., Joab I. Detection of Epstein-Barr virus in invasive breast cancers. J Natl Cancer Inst. 1999 Aug 18;91(16):1376–1381. doi: 10.1093/jnci/91.16.1376. [DOI] [PubMed] [Google Scholar]
  10. Borisch B., Finke J., Hennig I., Delacrétaz F., Schneider J., Heitz P. U., Laissue J. A. Distribution and localization of Epstein-Barr virus subtypes A and B in AIDS-related lymphomas and lymphatic tissue of HIV-positive patients. J Pathol. 1992 Oct;168(2):229–236. doi: 10.1002/path.1711680212. [DOI] [PubMed] [Google Scholar]
  11. Borisch B., Hennig I., Laeng R. H., Waelti E. R., Kraft R., Laissue J. Association of the subtype 2 of the Epstein-Barr virus with T-cell non-Hodgkin's lymphoma of the midline granuloma type. Blood. 1993 Aug 1;82(3):858–864. [PubMed] [Google Scholar]
  12. Bouzid M., Djennaoui D., Dubreuil J., Bouguermouh A., Ellouz D., Abdelwahab J., Decaussin G., Ooka T. Epstein-Barr virus genotypes in NPC biopsies from north Africa. Int J Cancer. 1994 Feb 15;56(4):468–473. doi: 10.1002/ijc.2910560403. [DOI] [PubMed] [Google Scholar]
  13. Boyle M. J., Sewell W. A., Sculley T. B., Apolloni A., Turner J. J., Swanson C. E., Penny R., Cooper D. A. Subtypes of Epstein-Barr virus in human immunodeficiency virus-associated non-Hodgkin lymphoma. Blood. 1991 Dec 1;78(11):3004–3011. [PubMed] [Google Scholar]
  14. Brielmeier M., Mautner J., Laux G., Hammerschmidt W. The latent membrane protein 2 gene of Epstein-Barr virus is important for efficient B cell immortalization. J Gen Virol. 1996 Nov;77(Pt 11):2807–2818. doi: 10.1099/0022-1317-77-11-2807. [DOI] [PubMed] [Google Scholar]
  15. Brink A. A., Dukers D. F., van den Brule A. J., Oudejans J. J., Middeldorp J. M., Meijer C. J., Jiwa M. 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):911–918. doi: 10.1136/jcp.50.11.911. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Brooks L. A., Lear A. L., Young L. S., Rickinson A. B. Transcripts from the Epstein-Barr virus BamHI A fragment are detectable in all three forms of virus latency. J Virol. 1993 Jun;67(6):3182–3190. doi: 10.1128/jvi.67.6.3182-3190.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Brooks L., Yao Q. Y., Rickinson A. B., Young L. S. Epstein-Barr virus latent gene transcription in nasopharyngeal carcinoma cells: coexpression of EBNA1, LMP1, and LMP2 transcripts. J Virol. 1992 May;66(5):2689–2697. doi: 10.1128/jvi.66.5.2689-2697.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Carbone A., Gloghini A., Zagonel V., Tirelli U. Expression of Epstein-Barr virus-encoded latent membrane protein 1 in nonendemic Burkitt's lymphomas. Blood. 1996 Feb 1;87(3):1202–1204. [PubMed] [Google Scholar]
  19. Carbone A., Tirelli U., Gloghini A., Volpe R., Boiocchi M. Human immunodeficiency virus-associated systemic lymphomas may be subdivided into two main groups according to Epstein-Barr viral latent gene expression. J Clin Oncol. 1993 Sep;11(9):1674–1681. doi: 10.1200/JCO.1993.11.9.1674. [DOI] [PubMed] [Google Scholar]
  20. Cen H., Breinig M. C., Atchison R. W., Ho M., McKnight J. L. Epstein-Barr virus transmission via the donor organs in solid organ transplantation: polymerase chain reaction and restriction fragment length polymorphism analysis of IR2, IR3, and IR4. J Virol. 1991 Feb;65(2):976–980. doi: 10.1128/jvi.65.2.976-980.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Cen H., Williams P. A., McWilliams H. P., Breinig M. C., Ho M., McKnight J. L. Evidence for restricted Epstein-Barr virus latent gene expression and anti-EBNA antibody response in solid organ transplant recipients with posttransplant lymphoproliferative disorders. Blood. 1993 Mar 1;81(5):1393–1403. [PubMed] [Google Scholar]
  22. Cesarman E., Chadburn A., Liu Y. F., Migliazza A., Dalla-Favera R., Knowles D. M. BCL-6 gene mutations in posttransplantation lymphoproliferative disorders predict response to therapy and clinical outcome. Blood. 1998 Oct 1;92(7):2294–2302. [PubMed] [Google Scholar]
  23. Cesarman E., Chang Y., Moore P. S., Said J. W., Knowles D. M. Kaposi's sarcoma-associated herpesvirus-like DNA sequences in AIDS-related body-cavity-based lymphomas. N Engl J Med. 1995 May 4;332(18):1186–1191. doi: 10.1056/NEJM199505043321802. [DOI] [PubMed] [Google Scholar]
  24. Chang K. L., Albújar P. F., Chen Y. Y., Johnson R. M., Weiss L. M. High prevalence of Epstein-Barr virus in the Reed-Sternberg cells of Hodgkin's disease occurring in Peru. Blood. 1993 Jan 15;81(2):496–501. [PubMed] [Google Scholar]
  25. Cheng G., Baltimore D. TANK, a co-inducer with TRAF2 of TNF- and CD 40L-mediated NF-kappaB activation. Genes Dev. 1996 Apr 15;10(8):963–973. doi: 10.1101/gad.10.8.963. [DOI] [PubMed] [Google Scholar]
  26. Cheung A., Kieff E. Long internal direct repeat in Epstein-Barr virus DNA. J Virol. 1982 Oct;44(1):286–294. doi: 10.1128/jvi.44.1.286-294.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Clarke P. A., Schwemmle M., Schickinger J., Hilse K., Clemens M. J. Binding of Epstein-Barr virus small RNA EBER-1 to the double-stranded RNA-activated protein kinase DAI. Nucleic Acids Res. 1991 Jan 25;19(2):243–248. doi: 10.1093/nar/19.2.243. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Cochet C., Martel-Renoir D., Grunewald V., Bosq J., Cochet G., Schwaab G., Bernaudin J. F., Joab I. Expression of the Epstein-Barr virus immediate early gene, BZLF1, in nasopharyngeal carcinoma tumor cells. Virology. 1993 Nov;197(1):358–365. doi: 10.1006/viro.1993.1597. [DOI] [PubMed] [Google Scholar]
  29. Crawford D. H., Thomas J. A., Janossy G., Sweny P., Fernando O. N., Moorhead J. F., Thompson J. H. Epstein Barr virus nuclear antigen positive lymphoma after cyclosporin A treatment in patient with renal allograft. Lancet. 1980 Jun 21;1(8182):1355–1356. doi: 10.1016/s0140-6736(80)91800-0. [DOI] [PubMed] [Google Scholar]
  30. Dawson C. W., Rickinson A. B., Young L. S. Epstein-Barr virus latent membrane protein inhibits human epithelial cell differentiation. Nature. 1990 Apr 19;344(6268):777–780. doi: 10.1038/344777a0. [DOI] [PubMed] [Google Scholar]
  31. Deacon E. M., Pallesen G., Niedobitek G., Crocker J., Brooks L., Rickinson A. B., Young L. S. Epstein-Barr virus and Hodgkin's disease: transcriptional analysis of virus latency in the malignant cells. J Exp Med. 1993 Feb 1;177(2):339–349. doi: 10.1084/jem.177.2.339. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Devergne O., Hatzivassiliou E., Izumi K. M., Kaye K. M., Kleijnen M. F., Kieff E., Mosialos G. 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):7098–7108. doi: 10.1128/mcb.16.12.7098. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Eliopoulos A. G., Blake S. M., Floettmann J. E., Rowe M., Young L. S. 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):1023–1035. doi: 10.1128/jvi.73.2.1023-1035.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Eliopoulos A. G., Gallagher N. J., Blake S. M., Dawson C. W., Young L. S. 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):16085–16096. doi: 10.1074/jbc.274.23.16085. [DOI] [PubMed] [Google Scholar]
  35. Eliopoulos A. G., Stack M., Dawson C. W., Kaye K. M., Hodgkin L., Sihota S., Rowe M., Young L. S. 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):2899–2916. doi: 10.1038/sj.onc.1201258. [DOI] [PubMed] [Google Scholar]
  36. Eliopoulos A. G., Young L. S. 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):1731–1742. doi: 10.1038/sj.onc.1201694. [DOI] [PubMed] [Google Scholar]
  37. Ernberg I., Andersson J. Acyclovir efficiently inhibits oropharyngeal excretion of Epstein-Barr virus in patients with acute infectious mononucleosis. J Gen Virol. 1986 Oct;67(Pt 10):2267–2272. doi: 10.1099/0022-1317-67-10-2267. [DOI] [PubMed] [Google Scholar]
  38. Flavell K., Constandinou C., Lowe D., Scott K., Newey C., Evans D., Dutton A., Simmons S., Smith R., Crocker J. Effect of material deprivation on Epstein-Barr virus infection in Hodgkin's disease in the West Midlands. Br J Cancer. 1999 May;80(3-4):604–608. doi: 10.1038/sj.bjc.6690398. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Floettmann J. E., Rowe M. 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):1851–1858. doi: 10.1038/sj.onc.1201359. [DOI] [PubMed] [Google Scholar]
  40. Fruehling S., Longnecker R. 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):241–251. doi: 10.1006/viro.1997.8690. [DOI] [PubMed] [Google Scholar]
  41. Fujii T., Kawai T., Saito K., Fukushima K., Hasegawa T., Tokunaga M., Yokoyama T. EBER-1 expression in thymic carcinoma. Acta Pathol Jpn. 1993 Mar;43(3):107–110. doi: 10.1111/j.1440-1827.1993.tb01118.x. [DOI] [PubMed] [Google Scholar]
  42. Fåhraeus R., Rymo L., Rhim J. S., Klein G. Morphological transformation of human keratinocytes expressing the LMP gene of Epstein-Barr virus. Nature. 1990 May 31;345(6274):447–449. doi: 10.1038/345447a0. [DOI] [PubMed] [Google Scholar]
  43. Gavioli R., Kurilla M. G., de Campos-Lima P. O., Wallace L. E., Dolcetti R., Murray R. J., Rickinson A. B., Masucci M. G. Multiple HLA A11-restricted cytotoxic T-lymphocyte epitopes of different immunogenicities in the Epstein-Barr virus-encoded nuclear antigen 4. J Virol. 1993 Mar;67(3):1572–1578. doi: 10.1128/jvi.67.3.1572-1578.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Gerber P., Lucas S., Nonoyama M., Perlin E., Goldstein L. I. Oral excretion of Epstein-Barr virus by healthy subjects and patients with infectious mononucleosis. Lancet. 1972 Nov 11;2(7785):988–989. doi: 10.1016/s0140-6736(72)92402-6. [DOI] [PubMed] [Google Scholar]
  45. Gilligan K. J., Rajadurai P., Lin J. C., Busson P., Abdel-Hamid M., Prasad U., Tursz T., Raab-Traub N. Expression of the Epstein-Barr virus BamHI A fragment in nasopharyngeal carcinoma: evidence for a viral protein expressed in vivo. J Virol. 1991 Nov;65(11):6252–6259. doi: 10.1128/jvi.65.11.6252-6259.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Gires O., Kohlhuber F., Kilger E., Baumann M., Kieser A., Kaiser C., Zeidler R., Scheffer B., Ueffing M., Hammerschmidt W. Latent membrane protein 1 of Epstein-Barr virus interacts with JAK3 and activates STAT proteins. EMBO J. 1999 Jun 1;18(11):3064–3073. doi: 10.1093/emboj/18.11.3064. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Gires O., Zimber-Strobl U., Gonnella R., Ueffing M., Marschall G., Zeidler R., Pich D., Hammerschmidt W. Latent membrane protein 1 of Epstein-Barr virus mimics a constitutively active receptor molecule. EMBO J. 1997 Oct 15;16(20):6131–6140. doi: 10.1093/emboj/16.20.6131. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Given D., Yee D., Griem K., Kieff E. DNA of Epstein-Barr virus. V. Direct repeats of the ends of Epstein-Barr virus DNA. J Virol. 1979 Jun;30(3):852–862. doi: 10.1128/jvi.30.3.852-862.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Gratama J. W., Oosterveer M. A., Lepoutre J. M., van Rood J. J., Zwaan F. E., Vossen J. M., Kapsenberg J. G., Richel D., Klein G., Ernberg I. Serological and molecular studies of Epstein-Barr virus infection in allogeneic marrow graft recipients. Transplantation. 1990 Apr;49(4):725–730. doi: 10.1097/00007890-199004000-00014. [DOI] [PubMed] [Google Scholar]
  50. Gregory C. D., Dive C., Henderson S., Smith C. A., Williams G. T., Gordon J., Rickinson A. B. Activation of Epstein-Barr virus latent genes protects human B cells from death by apoptosis. Nature. 1991 Feb 14;349(6310):612–614. doi: 10.1038/349612a0. [DOI] [PubMed] [Google Scholar]
  51. Gregory C. D., Rowe M., Rickinson A. B. Different Epstein-Barr virus-B cell interactions in phenotypically distinct clones of a Burkitt's lymphoma cell line. J Gen Virol. 1990 Jul;71(Pt 7):1481–1495. doi: 10.1099/0022-1317-71-7-1481. [DOI] [PubMed] [Google Scholar]
  52. Grässer F. A., Murray P. G., Kremmer E., Klein K., Remberger K., Feiden W., Reynolds G., Niedobitek G., Young L. S., Mueller-Lantzsch N. 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):3792–3798. [PubMed] [Google Scholar]
  53. Gulley M. L., Pulitzer D. R., Eagan P. A., Schneider B. G. Epstein-Barr virus infection is an early event in gastric carcinogenesis and is independent of bcl-2 expression and p53 accumulation. Hum Pathol. 1996 Jan;27(1):20–27. doi: 10.1016/s0046-8177(96)90133-1. [DOI] [PubMed] [Google Scholar]
  54. Gutensohn N., Cole P. Epidemiology of Hodgkin's disease. Semin Oncol. 1980 Jun;7(2):92–102. [PubMed] [Google Scholar]
  55. Hatzivassiliou E., Miller W. E., Raab-Traub N., Kieff E., Mosialos G. 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):1116–1121. [PubMed] [Google Scholar]
  56. Hatzubai A., Anafi M., Masucci M. G., Dillner J., Lerner R. A., Klein G., Sulitzeanu D. Down-regulation of the EBV-encoded membrane protein (LMP) in Burkitt lymphomas. Int J Cancer. 1987 Sep 15;40(3):358–364. doi: 10.1002/ijc.2910400313. [DOI] [PubMed] [Google Scholar]
  57. Henderson A., Ripley S., Heller M., Kieff E. Chromosome site for Epstein-Barr virus DNA in a Burkitt tumor cell line and in lymphocytes growth-transformed in vitro. Proc Natl Acad Sci U S A. 1983 Apr;80(7):1987–1991. doi: 10.1073/pnas.80.7.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Henle G., Henle W., Diehl V. Relation of Burkitt's tumor-associated herpes-ytpe virus to infectious mononucleosis. Proc Natl Acad Sci U S A. 1968 Jan;59(1):94–101. doi: 10.1073/pnas.59.1.94. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Henle W., Henle G., Zajac B. A., Pearson G., Waubke R., Scriba M. Differential reactivity of human serums with early antigens induced by Epstein-Barr virus. Science. 1970 Jul 10;169(3941):188–190. doi: 10.1126/science.169.3941.188. [DOI] [PubMed] [Google Scholar]
  60. Herbst H., Niedobitek G., Kneba M., Hummel M., Finn T., Anagnostopoulos I., Bergholz M., Krieger G., Stein H. High incidence of Epstein-Barr virus genomes in Hodgkin's disease. Am J Pathol. 1990 Jul;137(1):13–18. [PMC free article] [PubMed] [Google Scholar]
  61. Heslop H. E., Brenner M. K., Rooney C. M. Donor T cells to treat EBV-associated lymphoma. N Engl J Med. 1994 Sep 8;331(10):679–680. doi: 10.1056/NEJM199409083311017. [DOI] [PubMed] [Google Scholar]
  62. Heslop H. E., Ng C. Y., Li C., Smith C. A., Loftin S. K., Krance R. A., Brenner M. K., Rooney C. M. Long-term restoration of immunity against Epstein-Barr virus infection by adoptive transfer of gene-modified virus-specific T lymphocytes. Nat Med. 1996 May;2(5):551–555. doi: 10.1038/nm0596-551. [DOI] [PubMed] [Google Scholar]
  63. Ho M., Miller G., Atchison R. W., Breinig M. K., Dummer J. S., Andiman W., Starzl T. E., Eastman R., Griffith B. P., Hardesty R. L. Epstein-Barr virus infections and DNA hybridization studies in posttransplantation lymphoma and lymphoproliferative lesions: the role of primary infection. J Infect Dis. 1985 Nov;152(5):876–886. doi: 10.1093/infdis/152.5.876. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Huen D. S., Henderson S. A., Croom-Carter D., Rowe M. 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):549–560. [PubMed] [Google Scholar]
  65. Imai S., Koizumi S., Sugiura M., Tokunaga M., Uemura Y., Yamamoto N., Tanaka S., Sato E., Osato T. Gastric carcinoma: monoclonal epithelial malignant cells expressing Epstein-Barr virus latent infection protein. Proc Natl Acad Sci U S A. 1994 Sep 13;91(19):9131–9135. doi: 10.1073/pnas.91.19.9131. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Israele V., Shirley P., Sixbey J. W. Excretion of the Epstein-Barr virus from the genital tract of men. J Infect Dis. 1991 Jun;163(6):1341–1343. doi: 10.1093/infdis/163.6.1341. [DOI] [PubMed] [Google Scholar]
  67. Izumi K. M., Kieff E. D. 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):12592–12597. doi: 10.1073/pnas.94.23.12592. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Jarrett R. F., Gallagher A., Jones D. B., Alexander F. E., Krajewski A. S., Kelsey A., Adams J., Angus B., Gledhill S., Wright D. H. Detection of Epstein-Barr virus genomes in Hodgkin's disease: relation to age. J Clin Pathol. 1991 Oct;44(10):844–848. doi: 10.1136/jcp.44.10.844. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Jiwa N. M., Oudejans J. J., Bai M. C., Van den Brule A. J., Horstman A., Vos W., Van der Valk P., Kluin P. M., Walboomers J. M., Meijer C. J. Expression of bcl-2 protein and transcription of the Epstein-Barr virus bcl-2 homologue BHRF-1 in Hodgkin's disease: implications for different pathogenic mechanisms. Histopathology. 1995 Jun;26(6):547–553. doi: 10.1111/j.1365-2559.1995.tb00273.x. [DOI] [PubMed] [Google Scholar]
  70. Junker A. K., Thomas E. E., Radcliffe A., Forsyth R. B., Davidson A. G., Rymo L. Epstein-Barr virus shedding in breast milk. Am J Med Sci. 1991 Oct;302(4):220–223. doi: 10.1097/00000441-199110000-00005. [DOI] [PubMed] [Google Scholar]
  71. Kaye K. M., Izumi K. M., Mosialos G., Kieff E. 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):675–683. doi: 10.1128/jvi.69.2.675-683.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Khanna R., Burrows S. R., Argaet V., Moss D. J. Endoplasmic reticulum signal sequence facilitated transport of peptide epitopes restores immunogenicity of an antigen processing defective tumour cell line. Int Immunol. 1994 Apr;6(4):639–645. doi: 10.1093/intimm/6.4.639. [DOI] [PubMed] [Google Scholar]
  73. Khanna R., Burrows S. R., Steigerwald-Mullen P. M., Thomson S. A., Kurilla M. G., Moss D. J. Isolation of cytotoxic T lymphocytes from healthy seropositive individuals specific for peptide epitopes from Epstein-Barr virus nuclear antigen 1: implications for viral persistence and tumor surveillance. Virology. 1995 Dec 20;214(2):633–637. doi: 10.1006/viro.1995.0076. [DOI] [PubMed] [Google Scholar]
  74. Knecht H., Bachmann E., Brousset P., Sandvej K., Nadal D., Bachmann F., Odermatt B. F., Delsol G., Pallesen G. 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):2937–2942. [PubMed] [Google Scholar]
  75. Knowles D. M., Cesarman E., Chadburn A., Frizzera G., Chen J., Rose E. A., Michler R. E. Correlative morphologic and molecular genetic analysis demonstrates three distinct categories of posttransplantation lymphoproliferative disorders. Blood. 1995 Jan 15;85(2):552–565. [PubMed] [Google Scholar]
  76. Laherty C. D., Hu H. M., Opipari A. W., Wang F., Dixit V. M. 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):24157–24160. [PubMed] [Google Scholar]
  77. Lam K. M., Syed N., Whittle H., Crawford D. H. Circulating Epstein-Barr virus-carrying B cells in acute malaria. Lancet. 1991 Apr 13;337(8746):876–878. doi: 10.1016/0140-6736(91)90203-2. [DOI] [PubMed] [Google Scholar]
  78. Le Roux A., Kerdiles B., Walls D., Dedieu J. F., Perricaudet M. The Epstein-Barr virus determined nuclear antigens EBNA-3A, -3B, and -3C repress EBNA-2-mediated transactivation of the viral terminal protein 1 gene promoter. Virology. 1994 Dec;205(2):596–602. doi: 10.1006/viro.1994.1687. [DOI] [PubMed] [Google Scholar]
  79. Lee S. P., Thomas W. A., Murray R. J., Khanim F., Kaur S., Young L. S., Rowe M., Kurilla M., Rickinson A. B. HLA A2.1-restricted cytotoxic T cells recognizing a range of Epstein-Barr virus isolates through a defined epitope in latent membrane protein LMP2. J Virol. 1993 Dec;67(12):7428–7435. doi: 10.1128/jvi.67.12.7428-7435.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  80. Leonard W. J., O'Shea J. J. Jaks and STATs: biological implications. Annu Rev Immunol. 1998;16:293–322. doi: 10.1146/annurev.immunol.16.1.293. [DOI] [PubMed] [Google Scholar]
  81. Lerner M. R., Andrews N. C., Miller G., Steitz J. A. Two small RNAs encoded by Epstein-Barr virus and complexed with protein are precipitated by antibodies from patients with systemic lupus erythematosus. Proc Natl Acad Sci U S A. 1981 Feb;78(2):805–809. doi: 10.1073/pnas.78.2.805. [DOI] [PMC free article] [PubMed] [Google Scholar]
  82. Levine P. H., Ablashi D. V., Berard C. W., Carbone P. P., Waggoner D. E., Malan L. Elevated antibody titers to Epstein-Barr virus in Hodgkin's disease. Cancer. 1971 Feb;27(2):416–421. doi: 10.1002/1097-0142(197102)27:2<416::aid-cncr2820270227>3.0.co;2-w. [DOI] [PubMed] [Google Scholar]
  83. Levitskaya J., Coram M., Levitsky V., Imreh S., Steigerwald-Mullen P. M., Klein G., Kurilla M. G., Masucci M. G. Inhibition of antigen processing by the internal repeat region of the Epstein-Barr virus nuclear antigen-1. Nature. 1995 Jun 22;375(6533):685–688. doi: 10.1038/375685a0. [DOI] [PubMed] [Google Scholar]
  84. Levitsky V., Zhang Q. J., Levitskaya J., Masucci M. G. The life span of major histocompatibility complex-peptide complexes influences the efficiency of presentation and immunogenicity of two class I-restricted cytotoxic T lymphocyte epitopes in the Epstein-Barr virus nuclear antigen 4. J Exp Med. 1996 Mar 1;183(3):915–926. doi: 10.1084/jem.183.3.915. [DOI] [PMC free article] [PubMed] [Google Scholar]
  85. Li S. N., Chang Y. S., Liu S. T. 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):2129–2135. [PubMed] [Google Scholar]
  86. Liebowitz D. Epstein-Barr virus and a cellular signaling pathway in lymphomas from immunosuppressed patients. N Engl J Med. 1998 May 14;338(20):1413–1421. doi: 10.1056/NEJM199805143382003. [DOI] [PubMed] [Google Scholar]
  87. Lombardi L., Newcomb E. W., Dalla-Favera R. Pathogenesis of Burkitt lymphoma: expression of an activated c-myc oncogene causes the tumorigenic conversion of EBV-infected human B lymphoblasts. Cell. 1987 Apr 24;49(2):161–170. doi: 10.1016/0092-8674(87)90556-3. [DOI] [PubMed] [Google Scholar]
  88. Longnecker R., Kieff E. A second Epstein-Barr virus membrane protein (LMP2) is expressed in latent infection and colocalizes with LMP1. J Virol. 1990 May;64(5):2319–2326. doi: 10.1128/jvi.64.5.2319-2326.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  89. Lung M. L., Chang G. C., Miller T. R., Wara W. M., Phillips T. L. Genotypic analysis of Epstein-Barr virus isolates associated with nasopharyngeal carcinoma in Chinese immigrants to the United States. Int J Cancer. 1994 Dec 15;59(6):743–746. doi: 10.1002/ijc.2910590605. [DOI] [PubMed] [Google Scholar]
  90. Lung M. L., Lam W. P., Chan K. H., Li S., Sham J., Choy D. Direct detection of Epstein-Barr virus in peripheral blood and comparison of Epstein-Barr virus genotypes present in direct specimens and lymphoblastoid cell lines established from nasopharyngeal carcinoma patients and healthy carriers in Hong Kong. Int J Cancer. 1992 Sep 9;52(2):174–177. doi: 10.1002/ijc.2910520203. [DOI] [PubMed] [Google Scholar]
  91. MacMahon E. M., Glass J. D., Hayward S. D., Mann R. B., Becker P. S., Charache P., McArthur J. C., Ambinder R. F. Epstein-Barr virus in AIDS-related primary central nervous system lymphoma. Lancet. 1991 Oct 19;338(8773):969–973. doi: 10.1016/0140-6736(91)91837-k. [DOI] [PubMed] [Google Scholar]
  92. Mannick J. B., Cohen J. I., Birkenbach M., Marchini A., Kieff E. The Epstein-Barr virus nuclear protein encoded by the leader of the EBNA RNAs is important in B-lymphocyte transformation. J Virol. 1991 Dec;65(12):6826–6837. doi: 10.1128/jvi.65.12.6826-6837.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  93. Mazeron M. C. Intérêt de la recherche des anticorps spécifiques du virus d'Epstein-Barr pour le diagnostic et la surveillance du carcinome indifférencié du nasopharynx. Bull Cancer Radiother. 1996;83(1):3–7. [PubMed] [Google Scholar]
  94. Miller C. L., Burkhardt A. L., Lee J. H., Stealey B., Longnecker R., Bolen J. B., Kieff E. Integral membrane protein 2 of Epstein-Barr virus regulates reactivation from latency through dominant negative effects on protein-tyrosine kinases. Immunity. 1995 Feb;2(2):155–166. doi: 10.1016/s1074-7613(95)80040-9. [DOI] [PubMed] [Google Scholar]
  95. Miller C. L., Lee J. H., Kieff E., Burkhardt A. L., Bolen J. B., Longnecker R. Epstein-Barr virus protein LMP2A regulates reactivation from latency by negatively regulating tyrosine kinases involved in sIg-mediated signal transduction. Infect Agents Dis. 1994 Apr-Jun;3(2-3):128–136. [PubMed] [Google Scholar]
  96. Misko I. S., Sculley T. B., Schmidt C., Moss D. J., Soszynski T., Burman K. Composite response of naive T cells to stimulation with the autologous lymphoblastoid cell line is mediated by CD4 cytotoxic T cell clones and includes an Epstein-Barr virus-specific component. Cell Immunol. 1991 Feb;132(2):295–307. doi: 10.1016/0008-8749(91)90029-b. [DOI] [PubMed] [Google Scholar]
  97. Mosialos G., Birkenbach M., Yalamanchili R., VanArsdale T., Ware C., Kieff E. The Epstein-Barr virus transforming protein LMP1 engages signaling proteins for the tumor necrosis factor receptor family. Cell. 1995 Feb 10;80(3):389–399. doi: 10.1016/0092-8674(95)90489-1. [DOI] [PubMed] [Google Scholar]
  98. Mosier D. E., Gulizia R. J., Baird S. M., Wilson D. B. Transfer of a functional human immune system to mice with severe combined immunodeficiency. Nature. 1988 Sep 15;335(6187):256–259. doi: 10.1038/335256a0. [DOI] [PubMed] [Google Scholar]
  99. Moss D. J., Burrows S. R., Khanna R., Misko I. S., Sculley T. B. Immune surveillance against Epstein-Barr virus. Semin Immunol. 1992 Apr;4(2):97–104. [PubMed] [Google Scholar]
  100. Moss D. J., Rickinson A. B., Pope J. H. Long-term T-cell-mediated immunity to Epstein-Barr virus in man. I. Complete regression of virus-induced transformation in cultures of seropositive donor leukocytes. Int J Cancer. 1978 Dec;22(6):662–668. doi: 10.1002/ijc.2910220604. [DOI] [PubMed] [Google Scholar]
  101. Moss D. J., Rickinson A. B., Pope J. H. Long-term T-cell-mediated immunity to Epstein-Barr virus in man. III. Activation of cytotoxic T cells in virus-infected leukocyte cultures. Int J Cancer. 1979 May 15;23(5):618–625. doi: 10.1002/ijc.2910230506. [DOI] [PubMed] [Google Scholar]
  102. Mueller N., Evans A., Harris N. L., Comstock G. W., Jellum E., Magnus K., Orentreich N., Polk B. F., Vogelman J. Hodgkin's disease and Epstein-Barr virus. Altered antibody pattern before diagnosis. N Engl J Med. 1989 Mar 16;320(11):689–695. doi: 10.1056/NEJM198903163201103. [DOI] [PubMed] [Google Scholar]
  103. Murray P. G., Constandinou C. M., Crocker J., Young L. S., Ambinder R. F. Analysis of major histocompatibility complex class I, TAP expression, and LMP2 epitope sequence in Epstein-Barr virus-positive Hodgkin's disease. Blood. 1998 Oct 1;92(7):2477–2483. [PubMed] [Google Scholar]
  104. Murray P. G., Niedobitek G., Kremmer E., Grässer F., Reynolds G. M., Cruchley A., Williams D. M., Müller-Lantzsch N., Young L. S. In situ detection of the Epstein-Barr virus-encoded nuclear antigen 1 in oral hairy leukoplakia and virus-associated carcinomas. J Pathol. 1996 Jan;178(1):44–47. doi: 10.1002/(SICI)1096-9896(199601)178:1<44::AID-PATH471>3.0.CO;2-0. [DOI] [PubMed] [Google Scholar]
  105. Murray P. G., Swinnen L. J., Constandinou C. M., Pyle J. M., Carr T. J., Hardwick J. M., Ambinder R. F. BCL-2 but not its Epstein-Barr virus-encoded homologue, BHRF1, is commonly expressed in posttransplantation lymphoproliferative disorders. Blood. 1996 Jan 15;87(2):706–711. [PubMed] [Google Scholar]
  106. Murray P. G., Young L. S., Rowe M., Crocker J. Immunohistochemical demonstration of the Epstein-Barr virus-encoded latent membrane protein in paraffin sections of Hodgkin's disease. J Pathol. 1992 Jan;166(1):1–5. doi: 10.1002/path.1711660102. [DOI] [PubMed] [Google Scholar]
  107. Nakagomi H., Dolcetti R., Bejarano M. T., Pisa P., Kiessling R., Masucci M. G. The Epstein-Barr virus latent membrane protein-1 (LMP1) induces interleukin-10 production in Burkitt lymphoma lines. Int J Cancer. 1994 Apr 15;57(2):240–244. doi: 10.1002/ijc.2910570218. [DOI] [PubMed] [Google Scholar]
  108. Nalesnik M. A., Jaffe R., Starzl T. E., Demetris A. J., Porter K., Burnham J. A., Makowka L., Ho M., Locker J. The pathology of posttransplant lymphoproliferative disorders occurring in the setting of cyclosporine A-prednisone immunosuppression. Am J Pathol. 1988 Oct;133(1):173–192. [PMC free article] [PubMed] [Google Scholar]
  109. Niedobitek G., Agathanggelou A., Rowe M., Jones E. L., Jones D. B., Turyaguma P., Oryema J., Wright D. H., Young L. S. Heterogeneous expression of Epstein-Barr virus latent proteins in endemic Burkitt's lymphoma. Blood. 1995 Jul 15;86(2):659–665. [PubMed] [Google Scholar]
  110. Niedobitek G., Hansmann M. L., Herbst H., Young L. S., Dienemann D., Hartmann C. A., Finn T., Pitteroff S., Welt A., Anagnostopoulos I. Epstein-Barr virus and carcinomas: undifferentiated carcinomas but not squamous cell carcinomas of the nasopharynx are regularly associated with the virus. J Pathol. 1991 Sep;165(1):17–24. doi: 10.1002/path.1711650105. [DOI] [PubMed] [Google Scholar]
  111. Niedobitek G., Herbst H., Young L. S., Rowe M., Dienemann D., Germer C., Stein H. Epstein-Barr virus and carcinomas. Expression of the viral genome in an undifferentiated gastric carcinoma. Diagn Mol Pathol. 1992 Jun;1(2):103–108. [PubMed] [Google Scholar]
  112. Niedobitek G., Kremmer E., Herbst H., Whitehead L., Dawson C. W., Niedobitek E., von Ostau C., Rooney N., Grässer F. A., Young L. S. 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):1664–1672. [PubMed] [Google Scholar]
  113. Niedobitek G., Young L. S., Sam C. K., Brooks L., Prasad U., Rickinson A. B. Expression of Epstein-Barr virus genes and of lymphocyte activation molecules in undifferentiated nasopharyngeal carcinomas. Am J Pathol. 1992 Apr;140(4):879–887. [PMC free article] [PubMed] [Google Scholar]
  114. Oudejans J. J., van den Brule A. J., Jiwa N. M., de Bruin P. C., Ossenkoppele G. J., van der Valk P., Walboomers J. M., Meijer C. J. BHRF1, the Epstein-Barr virus (EBV) homologue of the BCL-2 protooncogene, is transcribed in EBV-associated B-cell lymphomas and in reactive lymphocytes. Blood. 1995 Sep 1;86(5):1893–1902. [PubMed] [Google Scholar]
  115. Pallesen G., Hamilton-Dutoit S. J., Rowe M., Young L. S. Expression of Epstein-Barr virus latent gene products in tumour cells of Hodgkin's disease. Lancet. 1991 Feb 9;337(8737):320–322. doi: 10.1016/0140-6736(91)90943-j. [DOI] [PubMed] [Google Scholar]
  116. Pathmanathan R., Prasad U., Chandrika G., Sadler R., Flynn K., Raab-Traub N. Undifferentiated, nonkeratinizing, and squamous cell carcinoma of the nasopharynx. Variants of Epstein-Barr virus-infected neoplasia. Am J Pathol. 1995 Jun;146(6):1355–1367. [PMC free article] [PubMed] [Google Scholar]
  117. Polack A., Hörtnagel K., Pajic A., Christoph B., Baier B., Falk M., Mautner J., Geltinger C., Bornkamm G. W., Kempkes B. c-myc activation renders proliferation of Epstein-Barr virus (EBV)-transformed cells independent of EBV nuclear antigen 2 and latent membrane protein 1. Proc Natl Acad Sci U S A. 1996 Sep 17;93(19):10411–10416. doi: 10.1073/pnas.93.19.10411. [DOI] [PMC free article] [PubMed] [Google Scholar]
  118. Polack A., Hörtnagel K., Pajic A., Christoph B., Baier B., Falk M., Mautner J., Geltinger C., Bornkamm G. W., Kempkes B. c-myc activation renders proliferation of Epstein-Barr virus (EBV)-transformed cells independent of EBV nuclear antigen 2 and latent membrane protein 1. Proc Natl Acad Sci U S A. 1996 Sep 17;93(19):10411–10416. doi: 10.1073/pnas.93.19.10411. [DOI] [PMC free article] [PubMed] [Google Scholar]
  119. Qu L., Rowe D. T. Epstein-Barr virus latent gene expression in uncultured peripheral blood lymphocytes. J Virol. 1992 Jun;66(6):3715–3724. doi: 10.1128/jvi.66.6.3715-3724.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  120. Raab-Traub N., Flynn K., Pearson G., Huang A., Levine P., Lanier A., Pagano J. The differentiated form of nasopharyngeal carcinoma contains Epstein-Barr virus DNA. Int J Cancer. 1987 Jan 15;39(1):25–29. doi: 10.1002/ijc.2910390106. [DOI] [PubMed] [Google Scholar]
  121. Raab-Traub N., Flynn K. The structure of the termini of the Epstein-Barr virus as a marker of clonal cellular proliferation. Cell. 1986 Dec 26;47(6):883–889. doi: 10.1016/0092-8674(86)90803-2. [DOI] [PubMed] [Google Scholar]
  122. Raab-Traub N., Rajadurai P., Flynn K., Lanier A. P. Epstein-Barr virus infection in carcinoma of the salivary gland. J Virol. 1991 Dec;65(12):7032–7036. doi: 10.1128/jvi.65.12.7032-7036.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  123. Razzouk B. I., Srinivas S., Sample C. E., Singh V., Sixbey J. W. Epstein-Barr Virus DNA recombination and loss in sporadic Burkitt's lymphoma. J Infect Dis. 1996 Mar;173(3):529–535. doi: 10.1093/infdis/173.3.529. [DOI] [PubMed] [Google Scholar]
  124. Rickinson A. B. Epstein-Barr virus in action in vivo. N Engl J Med. 1998 May 14;338(20):1461–1463. doi: 10.1056/NEJM199805143382011. [DOI] [PubMed] [Google Scholar]
  125. Rooney C. M., Smith C. A., Ng C. Y., Loftin S., Li C., Krance R. A., Brenner M. K., Heslop H. E. Use of gene-modified virus-specific T lymphocytes to control Epstein-Barr-virus-related lymphoproliferation. Lancet. 1995 Jan 7;345(8941):9–13. doi: 10.1016/s0140-6736(95)91150-2. [DOI] [PubMed] [Google Scholar]
  126. Rousset F., Garcia E., Defrance T., Péronne C., Vezzio N., Hsu D. H., Kastelein R., Moore K. W., Banchereau J. Interleukin 10 is a potent growth and differentiation factor for activated human B lymphocytes. Proc Natl Acad Sci U S A. 1992 Mar 1;89(5):1890–1893. doi: 10.1073/pnas.89.5.1890. [DOI] [PMC free article] [PubMed] [Google Scholar]
  127. Rowe M., Rowe D. T., Gregory C. D., Young L. S., Farrell P. J., Rupani H., Rickinson A. B. 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):2743–2751. doi: 10.1002/j.1460-2075.1987.tb02568.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  128. Sam C. K., Brooks L. A., Niedobitek G., Young L. S., Prasad U., Rickinson A. B. Analysis of Epstein-Barr virus infection in nasopharyngeal biopsies from a group at high risk of nasopharyngeal carcinoma. Int J Cancer. 1993 Apr 1;53(6):957–962. doi: 10.1002/ijc.2910530616. [DOI] [PubMed] [Google Scholar]
  129. Sample J., Henson E. B., Sample C. The Epstein-Barr virus nuclear protein 1 promoter active in type I latency is autoregulated. J Virol. 1992 Aug;66(8):4654–4661. doi: 10.1128/jvi.66.8.4654-4661.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  130. Sandberg M., Hammerschmidt W., Sugden B. Characterization of LMP-1's association with TRAF1, TRAF2, and TRAF3. J Virol. 1997 Jun;71(6):4649–4656. doi: 10.1128/jvi.71.6.4649-4656.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  131. Selves J., Bibeau F., Brousset P., Meggetto F., Mazerolles C., Voigt J. J., Pradere B., Chiotasso P., Delsol G. Epstein-Barr virus latent and replicative gene expression in gastric carcinoma. Histopathology. 1996 Feb;28(2):121–127. doi: 10.1046/j.1365-2559.1996.287333.x. [DOI] [PubMed] [Google Scholar]
  132. Sheldon P. J., Hemsted E. H., Papamichail M., Holborow E. J. Thymic origin of atypical lymphoid cells in infectious mononucleosis. Lancet. 1973 May 26;1(7813):1153–1155. doi: 10.1016/s0140-6736(73)91148-3. [DOI] [PubMed] [Google Scholar]
  133. Shibata D., Weiss L. M. Epstein-Barr virus-associated gastric adenocarcinoma. Am J Pathol. 1992 Apr;140(4):769–774. [PMC free article] [PubMed] [Google Scholar]
  134. Shibata D., Weiss L. M., Nathwani B. N., Brynes R. K., Levine A. M. Epstein-Barr virus in benign lymph node biopsies from individuals infected with the human immunodeficiency virus is associated with concurrent or subsequent development of non-Hodgkin's lymphoma. Blood. 1991 Apr 1;77(7):1527–1533. [PubMed] [Google Scholar]
  135. Shimizu N., Tanabe-Tochikura A., Kuroiwa Y., Takada K. Isolation of Epstein-Barr virus (EBV)-negative cell clones from the EBV-positive Burkitt's lymphoma (BL) line Akata: malignant phenotypes of BL cells are dependent on EBV. J Virol. 1994 Sep;68(9):6069–6073. doi: 10.1128/jvi.68.9.6069-6073.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  136. Shiramizu B., Barriga F., Neequaye J., Jafri A., Dalla-Favera R., Neri A., Guttierez M., Levine P., Magrath I. Patterns of chromosomal breakpoint locations in Burkitt's lymphoma: relevance to geography and Epstein-Barr virus association. Blood. 1991 Apr 1;77(7):1516–1526. [PubMed] [Google Scholar]
  137. Sinclair A. J., Palmero I., Peters G., Farrell P. J. EBNA-2 and EBNA-LP cooperate to cause G0 to G1 transition during immortalization of resting human B lymphocytes by Epstein-Barr virus. EMBO J. 1994 Jul 15;13(14):3321–3328. doi: 10.1002/j.1460-2075.1994.tb06634.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  138. Sing A. P., Ambinder R. F., Hong D. J., Jensen M., Batten W., Petersdorf E., Greenberg P. D. Isolation of Epstein-Barr virus (EBV)-specific cytotoxic T lymphocytes that lyse Reed-Sternberg cells: implications for immune-mediated therapy of EBV+ Hodgkin's disease. Blood. 1997 Mar 15;89(6):1978–1986. [PubMed] [Google Scholar]
  139. Sixbey J. W., Lemon S. M., Pagano J. S. A second site for Epstein-Barr virus shedding: the uterine cervix. Lancet. 1986 Nov 15;2(8516):1122–1124. doi: 10.1016/s0140-6736(86)90531-3. [DOI] [PubMed] [Google Scholar]
  140. Sixbey J. W., Nedrud J. G., Raab-Traub N., Hanes R. A., Pagano J. S. Epstein-Barr virus replication in oropharyngeal epithelial cells. N Engl J Med. 1984 May 10;310(19):1225–1230. doi: 10.1056/NEJM198405103101905. [DOI] [PubMed] [Google Scholar]
  141. Sixbey J. W., Shirley P., Chesney P. J., Buntin D. M., Resnick L. Detection of a second widespread strain of Epstein-Barr virus. Lancet. 1989 Sep 30;2(8666):761–765. doi: 10.1016/s0140-6736(89)90829-5. [DOI] [PubMed] [Google Scholar]
  142. Staal S. P., Ambinder R., Beschorner W. E., Hayward G. S., Mann R. A survey of Epstein-Barr virus DNA in lymphoid tissue. Frequent detection in Hodgkin's disease. Am J Clin Pathol. 1989 Jan;91(1):1–5. doi: 10.1093/ajcp/91.1.1. [DOI] [PubMed] [Google Scholar]
  143. Sugawara Y., Mizugaki Y., Uchida T., Torii T., Imai S., Makuuchi M., Takada K. Detection of Epstein-Barr virus (EBV) in hepatocellular carcinoma tissue: a novel EBV latency characterized by the absence of EBV-encoded small RNA expression. Virology. 1999 Apr 10;256(2):196–202. doi: 10.1006/viro.1999.9619. [DOI] [PubMed] [Google Scholar]
  144. Swaminathan S., Tomkinson B., Kieff E. Recombinant Epstein-Barr virus with small RNA (EBER) genes deleted transforms lymphocytes and replicates in vitro. Proc Natl Acad Sci U S A. 1991 Feb 15;88(4):1546–1550. doi: 10.1073/pnas.88.4.1546. [DOI] [PMC free article] [PubMed] [Google Scholar]
  145. Szekely L., Selivanova G., Magnusson K. P., Klein G., Wiman K. G. EBNA-5, an Epstein-Barr virus-encoded nuclear antigen, binds to the retinoblastoma and p53 proteins. Proc Natl Acad Sci U S A. 1993 Jun 15;90(12):5455–5459. doi: 10.1073/pnas.90.12.5455. [DOI] [PMC free article] [PubMed] [Google Scholar]
  146. Tierney R. J., Steven N., Young L. S., Rickinson A. B. Epstein-Barr virus latency in blood mononuclear cells: analysis of viral gene transcription during primary infection and in the carrier state. J Virol. 1994 Nov;68(11):7374–7385. doi: 10.1128/jvi.68.11.7374-7385.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  147. Toczyski D. P., Matera A. G., Ward D. C., Steitz J. A. The Epstein-Barr virus (EBV) small RNA EBER1 binds and relocalizes ribosomal protein L22 in EBV-infected human B lymphocytes. Proc Natl Acad Sci U S A. 1994 Apr 12;91(8):3463–3467. doi: 10.1073/pnas.91.8.3463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  148. Tomkinson B., Kieff E. Use of second-site homologous recombination to demonstrate that Epstein-Barr virus nuclear protein 3B is not important for lymphocyte infection or growth transformation in vitro. J Virol. 1992 May;66(5):2893–2903. doi: 10.1128/jvi.66.5.2893-2903.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  149. Tomkinson B., Robertson E., Kieff E. Epstein-Barr virus nuclear proteins EBNA-3A and EBNA-3C are essential for B-lymphocyte growth transformation. J Virol. 1993 Apr;67(4):2014–2025. doi: 10.1128/jvi.67.4.2014-2025.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  150. Tosato G., Blaese R. M. Epstein-Barr virus infection and immunoregulation in man. Adv Immunol. 1985;37:99–149. doi: 10.1016/s0065-2776(08)60339-9. [DOI] [PubMed] [Google Scholar]
  151. Trivedi P., Masucci M. G., Winberg G., Klein G. The epstein-Barr-virus-encoded membrane protein LMP but not the nuclear antigen EBNA-1 induces rejection of transfected murine mammary carcinoma cells. Int J Cancer. 1991 Jul 9;48(5):794–800. doi: 10.1002/ijc.2910480527. [DOI] [PubMed] [Google Scholar]
  152. Uccini S., Monardo F., Stoppacciaro A., Gradilone A., Aglianò A. M., Faggioni A., Manzari V., Vago L., Costanzi G., Ruco L. P. High frequency of Epstein-Barr virus genome detection in Hodgkin's disease of HIV-positive patients. Int J Cancer. 1990 Oct 15;46(4):581–585. doi: 10.1002/ijc.2910460405. [DOI] [PubMed] [Google Scholar]
  153. Wang D., Liebowitz D., Kieff E. An EBV membrane protein expressed in immortalized lymphocytes transforms established rodent cells. Cell. 1985 Dec;43(3 Pt 2):831–840. doi: 10.1016/0092-8674(85)90256-9. [DOI] [PubMed] [Google Scholar]
  154. Wang F., Gregory C. D., Rowe M., Rickinson A. B., Wang D., Birkenbach M., Kikutani H., Kishimoto T., Kieff E. 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):3452–3456. doi: 10.1073/pnas.84.10.3452. [DOI] [PMC free article] [PubMed] [Google Scholar]
  155. Wang F., Gregory C., Sample C., Rowe M., Liebowitz D., Murray R., Rickinson A., Kieff E. 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):2309–2318. doi: 10.1128/jvi.64.5.2309-2318.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  156. Wang F., Tsang S. F., Kurilla M. G., Cohen J. I., Kieff E. Epstein-Barr virus nuclear antigen 2 transactivates latent membrane protein LMP1. J Virol. 1990 Jul;64(7):3407–3416. doi: 10.1128/jvi.64.7.3407-3416.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  157. Weinberg E., Hoisington S., Eastman A. Y., Rice D. K., Malfetano J., Ross J. S. Uterine cervical lymphoepithelial-like carcinoma. Absence of Epstein-Barr virus genomes. Am J Clin Pathol. 1993 Feb;99(2):195–199. doi: 10.1093/ajcp/99.2.195. [DOI] [PubMed] [Google Scholar]
  158. Weinreb M., Day P. J., Niggli F., Green E. K., Nyong'o A. O., Othieno-Abinya N. A., Riyat M. S., Raafat F., Mann J. R. The consistent association between Epstein-Barr virus and Hodgkin's disease in children in Kenya. Blood. 1996 May 1;87(9):3828–3836. [PubMed] [Google Scholar]
  159. Weiss L. M., Movahed L. A., Butler A. E., Swanson S. A., Frierson H. F., Jr, Cooper P. H., Colby T. V., Mills S. E. Analysis of lymphoepithelioma and lymphoepithelioma-like carcinomas for Epstein-Barr viral genomes by in situ hybridization. Am J Surg Pathol. 1989 Aug;13(8):625–631. doi: 10.1097/00000478-198908000-00001. [DOI] [PubMed] [Google Scholar]
  160. Weiss L. M., Strickler J. G., Warnke R. A., Purtilo D. T., Sklar J. Epstein-Barr viral DNA in tissues of Hodgkin's disease. Am J Pathol. 1987 Oct;129(1):86–91. [PMC free article] [PubMed] [Google Scholar]
  161. Weiss L. M., Strickler J. G., Warnke R. A., Purtilo D. T., Sklar J. Epstein-Barr viral DNA in tissues of Hodgkin's disease. Am J Pathol. 1987 Oct;129(1):86–91. [PMC free article] [PubMed] [Google Scholar]
  162. Wilson J. B., Bell J. L., Levine A. J. Expression of Epstein-Barr virus nuclear antigen-1 induces B cell neoplasia in transgenic mice. EMBO J. 1996 Jun 17;15(12):3117–3126. [PMC free article] [PubMed] [Google Scholar]
  163. Wilson J. B., Weinberg W., Johnson R., Yuspa S., Levine A. J. 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):1315–1327. doi: 10.1016/0092-8674(90)90695-b. [DOI] [PubMed] [Google Scholar]
  164. Witherspoon R. P., Fisher L. D., Schoch G., Martin P., Sullivan K. M., Sanders J., Deeg H. J., Doney K., Thomas D., Storb R. Secondary cancers after bone marrow transplantation for leukemia or aplastic anemia. N Engl J Med. 1989 Sep 21;321(12):784–789. doi: 10.1056/NEJM198909213211203. [DOI] [PubMed] [Google Scholar]
  165. Wu T. C., Mann R. B., Charache P., Hayward S. D., Staal S., Lambe B. C., Ambinder R. F. Detection of EBV gene expression in Reed-Sternberg cells of Hodgkin's disease. Int J Cancer. 1990 Nov 15;46(5):801–804. doi: 10.1002/ijc.2910460509. [DOI] [PubMed] [Google Scholar]
  166. Yao Q. Y., Ogan P., Rowe M., Wood M., Rickinson A. B. Epstein-Barr virus-infected B cells persist in the circulation of acyclovir-treated virus carriers. Int J Cancer. 1989 Jan 15;43(1):67–71. doi: 10.1002/ijc.2910430115. [DOI] [PubMed] [Google Scholar]
  167. Yeung W. M., Zong Y. S., Chiu C. T., Chan K. H., Sham J. S., Choy D. T., Ng M. H. Epstein-Barr virus carriage by nasopharyngeal carcinoma in situ. Int J Cancer. 1993 Mar 12;53(5):746–750. doi: 10.1002/ijc.2910530507. [DOI] [PubMed] [Google Scholar]
  168. Young L. S., Dawson C. W., Clark D., Rupani H., Busson P., Tursz T., Johnson A., Rickinson A. B. Epstein-Barr virus gene expression in nasopharyngeal carcinoma. J Gen Virol. 1988 May;69(Pt 5):1051–1065. doi: 10.1099/0022-1317-69-5-1051. [DOI] [PubMed] [Google Scholar]
  169. Young L. S., Yao Q. Y., Rooney C. M., Sculley T. B., Moss D. J., Rupani H., Laux G., Bornkamm G. W., Rickinson A. B. New type B isolates of Epstein-Barr virus from Burkitt's lymphoma and from normal individuals in endemic areas. J Gen Virol. 1987 Nov;68(Pt 11):2853–2862. doi: 10.1099/0022-1317-68-11-2853. [DOI] [PubMed] [Google Scholar]
  170. Young L., Alfieri C., Hennessy K., Evans H., O'Hara C., Anderson K. C., Ritz J., Shapiro R. S., Rickinson A., Kieff E. 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):1080–1085. doi: 10.1056/NEJM198910193211604. [DOI] [PubMed] [Google Scholar]
  171. Zheng X., Yan L., Nilsson B., Eklund G., Drettner B. Epstein-Barr virus infection, salted fish and nasopharyngeal carcinoma. A case-control study in southern China. Acta Oncol. 1994;33(8):867–872. doi: 10.3109/02841869409098448. [DOI] [PubMed] [Google Scholar]
  172. Zimber-Strobl U., Suentzenich K. O., Laux G., Eick D., Cordier M., Calender A., Billaud M., Lenoir G. M., Bornkamm G. W. Epstein-Barr virus nuclear antigen 2 activates transcription of the terminal protein gene. J Virol. 1991 Jan;65(1):415–423. doi: 10.1128/jvi.65.1.415-423.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  173. Zutter M. M., Martin P. J., Sale G. E., Shulman H. M., Fisher L., Thomas E. D., Durnam D. M. Epstein-Barr virus lymphoproliferation after bone marrow transplantation. Blood. 1988 Aug;72(2):520–529. [PubMed] [Google Scholar]
  174. d'Amore F., Johansen P., Houmand A., Weisenburger D. D., Mortensen L. S. Epstein-Barr virus genome in non-Hodgkin's lymphomas occurring in immunocompetent patients: highest prevalence in nonlymphoblastic T-cell lymphoma and correlation with a poor prognosis. Danish Lymphoma Study Group, LYFO. Blood. 1996 Feb 1;87(3):1045–1055. [PubMed] [Google Scholar]
  175. de Campos-Lima P. O., Gavioli R., Zhang Q. J., Wallace L. E., Dolcetti R., Rowe M., Rickinson A. B., Masucci M. G. HLA-A11 epitope loss isolates of Epstein-Barr virus from a highly A11+ population. Science. 1993 Apr 2;260(5104):98–100. doi: 10.1126/science.7682013. [DOI] [PubMed] [Google Scholar]
  176. de Campos-Lima P. O., Levitsky V., Brooks J., Lee S. P., Hu L. F., Rickinson A. B., Masucci M. G. T cell responses and virus evolution: loss of HLA A11-restricted CTL epitopes in Epstein-Barr virus isolates from highly A11-positive populations by selective mutation of anchor residues. J Exp Med. 1994 Apr 1;179(4):1297–1305. doi: 10.1084/jem.179.4.1297. [DOI] [PMC free article] [PubMed] [Google Scholar]
  177. de Campos-Lima P. O., Torsteinsdóttir S., Cuomo L., Klein G., Sulitzeanu D., Masucci M. G. Antigen processing and presentation by EBV-carrying cell lines: cell-phenotype dependence and influence of the EBV-encoded LMP1. Int J Cancer. 1993 Mar 12;53(5):856–862. doi: 10.1002/ijc.2910530525. [DOI] [PubMed] [Google Scholar]

Articles from Molecular Pathology are provided here courtesy of BMJ Publishing Group

RESOURCES