The role of Epstein-Barr virus in cancer

Expert Opinion on Biological Therapy

Volumn 6, Issue 11, 2006, Pages 1193-1205

  Patrie, Samuel B ^a   Farrell, Paul J ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Cancer; Epstein Barr virus; Lymphoma; PKR

Indexed keywords

ACQUIRED IMMUNE DEFICIENCY SYNDROME; B LYMPHOCYTE; BURKITT LYMPHOMA; CARCINOGENESIS; DISEASE ASSOCIATION; EPITHELIUM CELL; EPSTEIN BARR VIRUS; HODGKIN DISEASE; HUMAN; IMMUNE DEFICIENCY; LIFE CYCLE; LYMPHOCYTE DIFFERENTIATION; LYMPHOPROLIFERATIVE DISEASE; MEMORY CELL; NASOPHARYNX CARCINOMA; NONHUMAN; REVIEW; STOMACH CARCINOMA; TUMOR BIOPSY; TUMOR CELL; VIRUS ACTIVATION; VIRUS INFECTION; VIRUS REACTIVATION;

ANIMALS; GENE EXPRESSION PROFILING; HERPESVIRUS 4, HUMAN; HUMANS; IMMUNOTHERAPY, ACTIVE; NEOPLASMS;

HUMAN HERPESVIRUS 4;

EID: 33750839308     PISSN: 14712598     EISSN: None     Source Type: Journal    
DOI: 10.1517/14712598.6.11.1193     Document Type: Review

References (114)

1. SHANNON-LOWE CD, NEUHIERL B, BALDWIN G, RICKINSON AB, DELECLUSE HJ: Resting B cells as a transfer vehicle for Epstein-Barr virus infection of epithelial cells. Proc. Natl. Acad. Sci. USA (2006) 103(18):7065-7070.
2. YOUNG LS, RICKINSON AB: Epstein-Barr virus: 40 years on. Nat. Rev. Cancer (2004) 4(10):757-768.
3. THORLEY-LAWSON DA: EBV the prototypical human tumor virus-just how bad is it? J. Allergy Clin. Immunol. (2005) 116(2):251-261; quiz 262.
4. JAFFE ES, WILSON WH: Lymphomatoid granulomatosis: pathogenesis, pathology and clinical implications. Cancer Surv. (1997) 30:233-248.
5. VACHIE A, KANEGANE H, KASAHARAY: Epstein-Barr virus-associated T-/natural killer cell lymphoproliferative diseases. Semin. Hematol. (2003) 40(2):124-132.
6. GEORGESCU L, QUINN GC, SCHWARTZMAN S, PAGET SA: Lymphoma in patients with rheumatoid arthritis: association with the disease state or methotrexate treatment. Semin. Arthritis Rheum. (1997) 26(6):794-804.
7. VAN DEN BOSCH CA: Is endemic Burkitt's lymphoma an alliance between three infections and a tumour promoter? Lancet Oncol. (2004) 5(12):738-746.
8. CARBONE A, GLOGHINI A, GAIDANO G et al.: AIDS-related Burkitt's lymphoma. Morphologic and immunophenotypic study of biopsy specimens. Am. J. Clin. Pathol. (1995) 103(5):561-567.
9. O'CONOR GT, RAPPAPORT H, SMITH EB: Childhood lymphoma resembling 'Burkitt tumor' in the United States. Cancer (1965) 18:411-417.
10. WILDA M, BRUCH J, HARDER L et al.: Inactivation of the ARF-MDM-2-p53 pathway in sporadic Burkitt's lymphoma in children. Leukemia (2004) 18(3):584-588.
11. VAN DEN BOSCH C, HILLS M, KAZEMBE P, DZIWENI C, KADZAMIRA L: Time-space case clusters of Burkitt's lymphoma in Malawi. Leukemia (1993) 7(11):1875-1878.
12. OTIENO MW, REMICK SC, WHALEN C: Adult Burkitt's lymphoma in patients with and without human immunodeficiency virus infection in Kenya. Int. J. Cancer (2001) 92(5):687-691.
13. BURKITT D: A children's cancer dependent on climatic factors. Nature (1962) 194:232-234.
14. MOSS DJ, BURROWS SR, CASTELINO DJ et al. A comparison of Epstein-Barr virus-specific T-cell immunity in malaria-endemic and -nonendemic regions of Papua New Guinea. Int. J. Cancer (1983) 31(6):727-732.
15. LAM KM, SYED N, WHITTLE H, CRAWFORD DH: Circulating Epstein-Barr virus-carrying B cells in acute malaria. Lancet (1991) 337(8746):876-878.
16. IVERSEN U, IVERSEN OH, BLUMING AZ, ZIEGLER JL, KYALWASI S: Cell kinetics of African cases of Burkitt lymphoma. A preliminary report. Eur. J. Cancer (1972) 8(3):305-308.
17. GREGORY CD, DIVE C, HENDERSON S et al.: Activation of Epstein-Barr virus latent genes protects human B cells from death by apoptosis. Nature (1991) 349(6310):612-614.
18. KLEIN U, KLEIN G, EHLIN-HENRIKSSON B, RAJEWSKY K, KUPPERS R: Burkitt's lymphoma is a malignancy of mature B cells expressing somatically mutated V region genes. Mol. Med. (1995) 1(5):495-505.
19. CHAPMAN CJ, MOCKRIDGE CI, ROWE M, RICKINSON AB, STEVENSON FK: Analysis of VH genes used by neoplastic B cells in endemic Burkitt's lymphoma shows somatic hypermutation and intraclonal heterogeneity. Blood (1995) 85(8):2176-2181.
20. TAUB R, KIRSCH I, MORTON C et al.: Translocation of the c-myc gene into the immunoglobulin heavy chain locus in human Burkitt lymphoma and murine plasmacytoma cells. Proc. Natl. Acad. Sci. USA (1982) 79(24):7837-7841.
21. POLACK A, HORTNAGEL K, PAJIC A et al.: c-myc activation renders proliferation of Epstem-Barr virus (EBV)-transformed cells independent of EBV nuclear antigen 2 and latent membrane protein 1. Proc. Natl. Acad. Sci. USA (1996) 93(19):10411-10416.
22. LINDSTROM MS, KLANGBY U, WIMAN KG: p14ARF homozygous deletion or MDM2 overexpression in Burkitt lymphoma lines carrying wild type p53. Oncagene (2001) 20(17):2171-2177.
23. FARRELL PJ, ALLAN GJ, SHANAHAN F, VOUSDEN KH, CROOK T: p53 is frequently mutated in Burkitt's lymphoma cell lines. EMBO J. (1991) 10(10):2879-2887.
24. HEMANN MT, BRIC A, TERUYA-FELDSTEIN J et al.: Evasion of the p53 tumour surveillance network by tumour-derived MYC mutants. Nature (2005) 436(7052):807-811.
25. ROWE M, ROWE DT, GREGORY CD et al.: Differences in B cell growth phenotype reflect novel patterns of Epstein-Barr virus latent gene expression in Burkitt's lymphoma cells. EMBO J. (1987) 6(9):2743-2751.
26. KELLY G, BELL A, RICKINSON A: Epstein-Barr virus-associated Burkitt lymphomagenesis selects for downregulation of the nuclear antigen EBNA2. Nat. Med. (2002) 8(10):1098-1104.
27. XUE SA, LABRECQUE LG, LU QL et al.: Promiscuous expression of Epstein-Barr virus genes in Burkitt's lymphoma from the central African country Malawi. Int. J. Cancer (2002) 99(5):635-643.
28. HOCHBERG D, MIDDELDORP JM, CATALINA M et al.: Demonstration of the Burkitt's lymphoma Epstein-Barr virus phenotype in dividing latently infected memory cells in vivo. Proc. Natl. Acad. Sci. USA (2004) 101(1):239-244.
29. KELLY GL, MILNER AE, TIERNEY RJ et al.: Epstein-Barr virus nuclear antigen 2 (EBNA2) gene deletion is consistently linked with EBNA3A, -3B, and -3C expression in Burkitt's lymphoma cells and with increased resistance to apoptosis. J. Virol. (2005) 79(16):10709-10717.
30. KENNEDY G, KOMANO J, SUGDEN B: Epstein-Barr virus provides a survival factor to Burkitt's lymphomas. Proc. Natl. Acad. Sci. USA (2003) 100(24):14269-14274.
31. CAIX, SCHAFER A, LU S et al.: Epstein-Barr virus microRNAs are evolutionarily conserved and differentially expressed. PLoS Pathog. (2006) 2(3):e23.
32. PFEFFER S, ZAVOLAN M, GRASSER FA et al.: Identification of virus-encoded microRNAs. Nature (2004) 304:734-736.
33. KOMANO J, MARUO S, KUROZUMIK, ODA T, TAKADA K: Oncogenic role of Epstein-Barr virus-encoded RNAs in Burkitt's lymphoma cell line Akata. J Virol. (1999) 73(12):9827-9831.
34. YAMAMOTO N, TAKIZAWA T, IWANAGA Y, SHIMIZU N: Malignant transformation of B lymphoma cell line BJAB by Epstein-Barr virus-encoded small RNAs. FEBS Lett. (2000) 484(2):153-158.
35. RUF IK, RHYNE PW, YANG C, CLEVELAND JL, SAMPLE J: Epstein-Barr virus small RNAs potentiate tumourigenicity of Burkitt's lymphoma cells independently of an effect on apoptosis. J Virol (2000)74(21):10223-10228.
36. NANBO A, INOUE K, ADACHI-TAKASAWA K, TAKADA K: Epstein-Barr virus RNA confers resistance to interferon-alpha-induced apoptosis in Burkitt's lymphoma. EMBO J. (2002) 21(5):954-965.
37. DONZE O, DENG J, CURRAN J et al.: The protein kinase PKR: a molecular clock that sequentially activates survival and death programs. EMBO J. (2004) 23:564-571.
38. MEURS EF, GALABRU J, BARBER GN, KATZE MG, HOVANESSIAN AG: Tumor suppressor function of the interferon-induced double-stranded RNA-activated protein kinase. Proc. Natl. Acad. Sci. USA (1993) 90(1):232-236.
39. COULTAS L, STRASSER A: The role of the Bcl-2 protein family in cancer. Semin. Cancer Biol. (2003) 13(2):115-123.
40. KOMANO J, SUGIURA M, TAKADA K: Epstein-Barr virus contributes to the malignant phenotype and to apoptosis resistance in Burkitt's lymphoma cell line Akata. J. Virol. (1998) 72(11):9150-9156.
41. KOMANO J, TAKADA K: Role of bcl-2 in Epstein-Barr virus-induced malignant conversion of Burkitt's lymphoma cell line Akata. J. Virol. (2001) 75(3):1561-1564.
42. KITAGAWA N, GOTO M, KUROZUMI K et al.: Epstein-Barr virus-encoded poly(A)- RNA supports Burkitt's lymphoma growth through interleukin-10 induction. EMBO J. (2000) 19(4):6742-6750.
43. GANDHI MK, TELLAM JT, KHANNA R: Epstein-Barr virus-associated Hodgkin's lymphoma. Br. J. Haematol. (2004) 125(3):267-281.
44. KHAN G: Epstein-Barr virus, cytokines, and inflammation: a cocktail for the pathogenesis of Hodgkin's lymphoma? Exp. Hematol. (2006) 34(4):399-406.
45. GANDHI MK, LAMBLEY E, DURAISWAMY J et al.: Expression of LAG-3 by tumor-infiltrating lymphocytes is co-incident with the suppression of latent membrane antigen-specific CD8+ T-cell function in Hodgkin lymphoma patients. Blood (2006) 108(7):2280-2289.
46. JARRETT RF: Risk factors for Hodgkin's lymphoma by EBV status and significance of detection of EBV genomes in serum of patients with EBV-associated Hodgkin's lymphoma. Leuk. Lymphoma (2003) 44(Suppl. 3):S27-S32.
47. ALEXANDER FE, JARRETT RF, LAWRENCE D et al.: Risk factors for Hodgkin's disease by Epstein-Barr virus (EBV) status: prior infection by EBV and other agents. Br. J. Cancer (2000) 82(5):1117-1121.
48. JARRETT RF, KRAJEWSKI AS, ANGUS B et al.: The Scotland and Newcastle epidemiological study of Hodgkin's disease: impact of histopathological review and EBV status on incidence estimates. J. Clin. Pathol. (2003) 56(11):811-816.
49. BRAUNINGER A, HANSMANN ML, STRICKLER JG et al.: Identification of common germinal-center B-cell precursors in two patients with both Hodgkin's disease and non-Hodgkin's lymphoma. N. Engl. J. Med. (1999) 340(16):1239-1247.
50. BABCOCK GJ, THORLEY-LAWSON DA: Tonsillar memory B cells, latently infected with Epstein-Barr virus, express the restricted pattern of latent genes previously found only in Epstein-Barr virus-associated tumors. Proc. Natl. Acad. Sci. USA (2000) 97(22):12250-12255.
51. DUTTON A, REYNOLDS GM, DAWSON CW, YOUNG LS, MURRAY PG: Constitutive activation of phosphatidyl-inositide 3 kinase contributes to the survival of Hodgkin's lymphoma cells through a mechanism involving Akt kinase and mTOR. J. Pathol. (2005) 205(4):498-506.
52. BARGOU RC, EMMERICH F, KRAPPMANN D et al.: Constitutive nuclear factor-kappaB-RelA activation is required for proliferation and survival of Hodgkin's disease tumor cells. J. Clin. Invest. (1997) 100(12):2961-2969.
53. KULWICHIT W, EDWARDS RH, DAVENPORT EM et al.: Expression of the Epstein-Barr virus latent membrane protein 1 induces B cell lymphoma in transgenic mice. Proc. Natl. Acad. Sci. USA (1998) 95(20):11963-11968.
54. GIRES O, ZIMBER-STROBL U, GONNELLA R et al.: Latent membrane protein 1 of Epstein-Barr virus mimics a constitutively active receptor molecule. EMBO J. (1997) 16(20):6131-6140.
55. MOSIALOS G, BIRKENBACH M, YALAMANCHILI R et al.: The Epstein-Barr virus transforming protein LMP1 engages signaling proteins for the tumor necrosis factor receptor family. cell (1995)80(3):389-399.
56. ELIOPOULOS AG, CAAMANO JH, FLAVELL J et al.: Epstein-Barr virus-encoded latent infection membrane protein 1 regulates the processing of p100 NF-kappaB2 to p52 via an IKKgamma/NEMO-independent signalling pathway. Oncogene (2003) 22(48):7557-7569.
57. HUEN DS, HENDERSON SA, GROOM-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) 10(3):549-560.
58. GIRES O, KOHLHUBER F, KILGER E et al.: Latent membrane protein 1 of Epstein-Barr virus interacts with JAK3 and activates STAT proteins. EMBO J. (1999) 18(11):3064-3073.
59. LONGNECKER R, DRUKER B, ROBERTS TM, KIEFF E: An Epstein-Barr virus protein associated with cell growth transformation interacts with a tyrosine kinase. J Virol. (1991) 65(7):3681-3692.
60. BURKHARDT AL, BOLEN JB, KIEFF E, LONGNECKER R: An Epstein-Barr virus transformation-associated membrane protein interacts with src family tyrosine kinases. J. Virol. (1992) 66(8):5161-5167.
61. PORTIS T, LONGNECKER R: Epstein-Barr virus (EBV) LMP2A mediates B-lymphocyte survival through constitutive activation of the Ras/PI3K/Akt pathway. Oncogene (2004) 23(53):8619-8628.
62. PANOUSIS CG, ROWE DT: Epstein-Barr virus latent membrane protein 2 associates with and is a substrate for mitogen-activated protein kinase. J. Virol. (1997) 71(6):4752-4760.
63. DYKSTRA ML, LONGNECKER R, PIERCE SK: Epstein-Barr virus coopts lipid rafts to block the signaling and antigen transport functions of the BCR. Immunity (2001) 14(1):57-67.
64. MURRAY RJ, KURILLA MG, BROOKS JM et al.: Identification of target antigens for the human cytotoxic T cell response to Epstein-Barr virus (EBV): implications for the immune control of EBV-positive malignancies. J. Exp. Med. (1992) 176(1):157-168.
65. MACMAHON EM, GLASS JD, HAYWARD SD et al.: Epstein-Barr virus in AIDS-related primary central nervous system lymphoma. Lancet (1991) 338(8773):969-973.
66. SAMOSZUK M, NGUYEN V, SHADAN FF, RAMZI E: Incidence of Epstein-Barr virus in AIDS-related lymphoma specimens. J Acquir. Immune Defic. Syndr. (1993) 6(8):913-918.
67. THOMAS JA, HOTCHIN NA, ALLDAY MJ et al.: Immunohistology of Epstein-Barr virus-associated antigens in B cell disorders from immunocompromised individuals. Transplantation (1990) 49(5):944-953.
68. WEISS LM, MOVAHED LA: In situ demonstration of Epstein-Barr viral genomes in viral-associated B cell lymphoproliferations. Am. J. Pathol. (1989) 134(3):651-659.
69. OUDEJANS JJ, JIWA M, VAN DEN BRULE AJ et al.: Detection of heterogeneous Epstein-Barr virus gene expression patterns within individual post-transplantation lymphoproliferative disorders. Am. J. Pathol. (1995) 147(4):923-933.
70. MURRAY PG, SWINNEN LJ, CONSTANDINOU CM et al.: BCL-2 but not its Epstein-Barr virus-encoded homologue, BHRF1, is commonly-expressed in posttransplantation lymphoproliferative disorders. Blood (1996) 87(2):706-711.
71. TIMMS JM, BELL A, FLAVELL JR et al: Target cells of Epstein-Barr-virus (EBV)-positive post-transplant lymphoproliferative disease: similarities to EBV-positive Hodgkin's lymphoma. Lancet (2003) 361(9353):217-223.
72. JOSEPH AM, BABCOCK GJ, THORLEY-LAWSON DA: Cells expressing the Epstein-Barr virus growth program are present in and restricted to the naive B-cell subset of healthy tonsils. J Virol. (2000) 74(21):9964-9971.
73. KAISER C, LAUX G, EICK D et al.: The proto-oncogene c-myc is a direct target gene of Epstein-Barr virus nuclear antigen 2. J. Virol. (1999) 73(5):4481-4484.
74. STROBL LJ, HOFELMAYR H, MARSCH ALL G et al.: Activated Notch 1 modulates gene expression in B cells similarly to Epstein-Barr viral nuclear antigen 2. J. Virol. (2000) 74(4):1727-1735.
75. CESARMAN E, CHADBURN A, LIU YF et al.: BCL-6 gene mutations in posttransplantation lymphoproliferative disorders predict response to therapy and clinical outcome. Blood (1998) 92(7):2294-2302.
76. BABCOCK GJ, HOCHBERG D, THORLEY-LAWSON AD: The expression pattern of Epstein-Barr virus latent genes in vivo is dependent upon the differentiation stage of the infected B cell. Immunity (2000) 13(4):497-506.
77. BURNS DM, CRAWFORD DH: Epstein-Barr virus-specific cytotoxic T-lymphocytes for adoptive immunotherapy of post-transplant lymphoproliferative disease. Blood Rev. (2004) 18(3):193-209.
78. FOSTER AE, ROONEY CM: Improving T cell therapy for cancer. Expert Opin. Biol. Ther. (2006) 6(3):215-229.
79. SAVOLDO B, GOSS JA, HAMMER MM et al.: Treatment of solid organ transplant recipients with autologous Epstein Barr virus-specific cytotoxic T lymphocytes (CTL). Blood (2006) (In Press).
80. NO AUTHORS LISTED: Cancer Incidence In Five Continents. Volume VIII. Parkin DM, Whelan SL, Ferlay J, Teppo L, Thomas DB (Eds), IARC Scientific Publications, Lyon, France (2002):1-781.
81. NIEDOBITEK G, YOUNG LS, SAMCK et al.: Expression of Epstein-Barr virus genes and of lymphocyte activation molecules in undifferentiated nasopharyngeal carcinomas. Am. J. Pathol. (1992) 140(4):879-887.
82. RAAB-TRAUB N, FLYNN K: The structure of the termini of the Epstein-Barr virus as a marker of clonal cellular proliferation. Cell (1986) 47(6):883-889.
83. PATHMANATHAN R, PRASAD U, CHANDRIKA G et al.: Undifferentiated, nonkeratinizing, and squamous cell carcinoma of the nasopharynx. Variants of Epstein-Barr virus-infected neoplasia. Am J. Pathol. (1995) 146(6):1355-1367.
84. PATHMANATHAN R, PRASAD U, SADLER R, FLYNN K, RAAB-TRAUB N: Clonal proliferations of cells infected with Epstein-Barr virus in preinvasive lesions related to nasopharyngeal carcinoma. N. Engl J. Med. (1995) 333(11):693-698.
85. PAINE E, SCHEINMAN RI, BALDWIN AS JR, RAAB-TRAUB N: Expression of LMP1 in epithelial cells leads to the activation of a select subset of NF-kappa B/Rel family proteins. J. Virol (1995) 69(7):4572-4576.
86. THORNBURG NJ, PATHMANATHAN R, RAAB-TRAUB N: Activation of nuclear factor-kappaB p50 homodimer/Bcl-3 complexes in nasopharyngeal carcinoma. Cancer Res. (2003) 63(23):8293-8301.
87. MILLER WE, EARP HS, RAAB-TRAUB N: The Epstein-Barr virus latent membrane protein 1 induces expression of the epidermal growth factor receptor. J Virol. (1995) 69(7):4390-4398.
88. BUSSON P, ZHANG Q, GUILLON JM et al.: Elevated expression of ICAM1 (CD54) and minimal expression of LFA3 (CD58) in Epstein-Barr-virus-positive nasopharyngeal carcinoma cells. Int. J. Cancer (1992) 50(6):863-867.
89. YOSHIZAKIT, SATO H, FURUKAWA M, PAGANO JS: The expression of matrix metalloproteinase 9 is enhanced by Epstein-Barr virus latent membrane protein 1. Proc. Natl. Acad. Sci. USA (1998) 95(7):3621-3626.
90. TSAI CN, TSAI CL, TSE KP, CHANG HY, CHANG YS: The Epstein-Barr virus oncogene product, latent membrane protein 1, induces the downregulation of E-cadherin gene expression via activation of DNA methyltransferases. Proc. Natl. Acad. Sci. USA (2002) 99(15):10084-10089.
91. SCHOLLE F, BENDT KM, RAAB-TRAUB N: Epstein-Barr virus LMP2A transforms epithelial cells, inhibits cell differentiation, and activates Akt. J. Virol. (2000) 74(22):10681-10689.
92. MORRISON JA, KLINGELHUTZ AJ, RAAB-TRAUB N: Epstein-Barr virus latent membrane protein 2A activates beta-catenin signaling in epithelial cells. J. Virol. (2003) 77(22):12276-12284.
93. MORRISON JA, RAAB-TRAUB N: Roles of the ITAM and PY motifs of Epstein-Barr virus larent membrane protein 2A in the inhibition of epithelial cell differentiation and activation of (betal-catenin signaling. J. Virol. (2005) 79(4):2375-2382.
94. RAGOCZY T, MILLER G: Role of the Epstein-Barr virus RTA protein in activation of distinct classes of viral lytic cycle genes. J. Virol. (1999) 73(12):9858-9866.
95. DECAUSSIN G, SBIH-LAMMALI F, DE TURENNE-TESSIER M, BOUGUERMOUH A, OOKA T: Expression of BARF 1 gene encoded by Epstein-Barr virus in nasopharyngeal carcinoma biopsies. Cancer Res. (2000) 60(19):5584-5588.
96. LUO B, WANG Y, WANG XF et al.: Expression of Epstein-Barr virus genes in EBV-associated gastric carcinomas. World. J. Gastroenterol. (2005) 11(5):629-633.
97. STROCKBINE LD, COHEN JI, FARRAH T et al.: The Epstein-Barr virus BARF1 gene encodes a novel, soluble colony-stimulating factor-1 receptor. J. Virol. (1998) 72(5):4015-4021.
98. WEI MX, OOKA T: A transforming function of the BARF1 gene encoded by Epstein-Barr virus. EMBO J. (1989) 8(10):2897-2903.
99. WEI MX, DE TURENNE-TESSIER M, DECAUSSIN G, BENET G, OOKA T: Establishment of a monkey kidney epithelial cell line with the BARF 1 open reading frame from Epstein-Barr virus. Oncogene (1997) 14(25):3073-3081.
100. SHENG W, DECAUSSIN G, LIGOUT A, TAKADA K, OOKA T: Malignant transformation of Epstein-Barr virus-negative Akata cells by introduction of the BARF1 gene carried by Epstein-Barr virus. J Virol. (2003) 77(6):3859-3865.
101. SALL A, CASERTA S, JOLICOEUR P et al.: Mitogenic activity of Epstein-Barr virus-encoded BARF1 protein. Oncogene (2004) 23(28):4938-4944.
102. SHIBATA D, WEISS LM: Epstein-Barr virus-associated gastric adenocarcinoma. Am. J. Pathol. (1992) 140(4):769-774.
103. IMAI S, KOIZUMI S, SUGIURA M et al.: Gastric carcinoma: monoclonal epithelial malignant cells expressing Epstein-Barr virus latent infection protein. Proc. Natl. Acad. Sci. USA (1994) 91(19):9131-9135.
104. SUGIURA M, IMAI S, TOKUNAGA M et al.: Transcriptional analysis of Epstein-Barr virus gene expression in EBV-positive gastric carcinoma: unique viral latency in the tumour cells. Br. J. Cancer (1996)74(4):625-631.
105. WONG HL, WANG X, CHANG RC et al.: Stable expression of EBERs in immortalized nasopharyngeal epithelial cells confers resistance to apoptotic stress. Mol. Carcinog. (2005) 44:92-101.
106. NANBO A, YOSHIYAMA H, TAKADA K: Epstein-Barr virus-encoded poly(A)-RNA confers resistance to apoptosis mediated through Fas by blocking the PKR pathway in human epithelial intestine 407 cells. J. Virol. (2005) 79(19):12280-12285.
107. GIL J, ESTEBAN M: The interferon-induced protein kinase (PKR), triggers apoptosis through FADD-mediated activation of caspase 8 in a manner independent of Fas and TNF-alpha receptors. Oncogene (2000) 19(32):3665-3674.
108. GIL J, GARCIA MA, ESTEBAN M: Caspase 9 activation by the dsRNA-dependent protein kinase, PKR: molecular mechanism and relevance. FEBS Lett. (2002) 529(2-3):249-255.
109. BALACHANDRAN S, KIM CN, YEH WC et al.: Activation of the dsRNA-dependent protein kinase, PKR, induces apoptosis through FADD-mediated death signaling. EMBO J. (1998) 17(23):6888-6902.
110. IWAKIRI D, EIZURU Y, TOKUNAGA M, TAKADA K: Autocrine growth of Epstein-Barr virus-positive gastric carcinoma cells mediated by an Epstein-Barr virus-encoded small RNA. Cancer Res. (2003) 63:7062-7067.
111. IWAKIRI D, SHEEN T, CHEN J, HUANG DP, TAKADA K: Epstein-Barr Virus-encoded small RNA induces insulin-like growth factor 1 and supports growth of nasopharyngeal carcinoma-derived cell lines. Oncogene (2005) 24:1767-1773.
112. GANDHI MK, LAMBLEY E, BURROWS J et al.: Plasma Epstein-Barr virus (EBV) DNA is a biomarker for EBV-positive Hodgkin's lymphoma. Clin. Cancer Res. (2006) 12(2):460-464.
113. LIN JC, WANG WY, CHEN KY et al.: Quantification of plasma Epstein-Barr virus DNA in patients with advanced nasopharyngeal carcinoma. N. Engl. J. Med. (2004) 350(24):2461-2470.
114. BOLLARD CM, AGUILAR L, STRAATHOF KC et al.: Cytotoxic T lymphocyte therapy for Epstein-Barr virus+ Hodgkin's disease. J. Exp. Med. (2004) 200(12):1623-1633.