Epstein–Barr virus-associated malignancies: pathobiology and emerging therapeutic options
Corey Smith and Rajiv KhannaCentre for Immunotherapy and Vaccine Development
Queensland Institute of Medical Research
Tumour Immunology Laboratory
Department of Immunology
300 Herston Road, Brisbane
Qld 4006, Australia
Tel: +61 7 3362 0385
Fax: +61 7 3845 3510
Email: rajiv.khanna@qimr.edu.au
Microbiology Australia 34(3) 120-124 https://doi.org/10.1071/MA13041
Published: 4 September 2013
Abstract
Epstein–Barr virus (EBV) was first identified in malignant Burkitt lymphoma cells in 1964. Since then, EBV has been associated with a number of other malignancies of either lymphocytic origin, including both B cell and NK/T cell cancers, or epithelial origin, predominantly nasopharyngeal and gastric cancers. While a complete understanding of the relationship between EBV-mediated cellular transformation and the oncogenic events that lead to uncontrolled malignant cell growth remains to be determined for a number of these cancers, it is clear in all of these settings that a breakdown in the immune surveillance of virally infected cells contributes to the survival of EBV-bearing malignant cells.
References
[1] Rickinson, A.B. et al. (1996) Epstein–Barr virus. In Fields Virology (Vol. 3), pp. 2397–2446, Philadelphia, Lippincott–Raven Publishers.[2] Rickinson, A.B. and Moss, D.J. (1997) Human cytotoxic T lymphocyte responses to Epstein–Barr virus infection. Annu. Rev. Immunol. 15, 405–431.
| Human cytotoxic T lymphocyte responses to Epstein–Barr virus infection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXisVCmtrc%3D&md5=89a536220f6497d4fe5f6a407a96a2b1CAS | 9143694PubMed |
[3] Thorley-Lawson, D.A. (2001) Epstein–Barr virus: exploiting the immune system. Nat. Rev. Immunol. 1, 75–82.
| Epstein–Barr virus: exploiting the immune system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlvF2qtb8%3D&md5=0ee4637828a32562ad99bf4b7d42dc87CAS | 11905817PubMed |
[4] Moss, P. and Rickinson, A. (2005) Cellular immunotherapy for viral infection after HSC transplantation. Nat. Rev. Immunol. 5, 9–20.
| Cellular immunotherapy for viral infection after HSC transplantation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXlvVOg&md5=876ed1005ac42986a8c584dbb7d44ecbCAS | 15630425PubMed |
[5] Rickinson, A.B. (1992) Introduction: viruses and human cancer. Semin. Cancer Biol. 3, 249–251.
| 1:STN:280:DyaK3s7itVGisA%3D%3D&md5=57a2c3fe2512ba63106bfaa41fb186daCAS | 1477330PubMed |
[6] Kieff, E. et al. (1996) Epstein–Barr virus and its replication. In Virology (Vol. 3), pp. 2343–2396, Philadelphia, Raven Press.
[7] Bollard, C.M. et al. (2012) T-cell therapy in the treatment of post-transplant lymphoproliferative disease. Nat. Rev. Clin. Oncol. 9, 510–519.
| T-cell therapy in the treatment of post-transplant lymphoproliferative disease.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1Kjs7zP&md5=f53de565415f6789d7d746d20cc8b07cCAS | 22801669PubMed |
[8] Young, L. et al. (1989) Expression of Epstein–Barr virus transformation-associated genes in tissues of patients with EBV lymphoproliferative disease. N. Engl. J. Med. 321, 1080–1085.
| Expression of Epstein–Barr virus transformation-associated genes in tissues of patients with EBV lymphoproliferative disease.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3c%2FhsV2rug%3D%3D&md5=6886e917c7ee95b6b1f1d786cb421e72CAS | 2552313PubMed |
[9] Razonable, R.R. and Paya, C.V. (2003) Herpesvirus infections in transplant recipients: current challenges in the clinical management of cytomegalovirus and Epstein–Barr virus infections. Herpes 10, 60–65.
| 14759337PubMed |
[10] Khanna, R. et al. (2001) Immunotherapeutic strategies for EBV-associated malignancies. Trends. Mol. Med. 7, 270–276.
| Immunotherapeutic strategies for EBV-associated malignancies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXltVahu7c%3D&md5=f14d2c857968899cd7db7eb3f2ff29b8CAS | 11378517PubMed |
[11] Kuehnle, I. et al. (2000) CD20 monoclonal antibody (rituximab) for therapy of Epstein–Barr virus lymphoma after hemopoietic stem-cell transplantation. Blood 95, 1502–1505.
| 1:CAS:528:DC%2BD3cXhtFKitbc%3D&md5=b0b2d3a507c04f5420541aa70f9fbeb2CAS | 10666232PubMed |
[12] Rooney, C.M. et al. (1995) Use of gene-modified virus-specific T lymphocytes to control Epstein–Barr-virus-related lymphoproliferation. Lancet 345, 9–13.
| Use of gene-modified virus-specific T lymphocytes to control Epstein–Barr-virus-related lymphoproliferation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2M%2FpslOgsA%3D%3D&md5=700cbb8a0a6995f8e3357607a82377a4CAS | 7799740PubMed |
[13] Rooney, C.M. et al. (1998) Infusion of cytotoxic T cells for the prevention and treatment of Epstein–Barr virus-induced lymphoma in allogeneic transplant recipients. Blood 92, 1549–1555.
| 1:CAS:528:DyaK1cXls1Siu7w%3D&md5=ad77222e0572e741b38f7bfd403fa636CAS | 9716582PubMed |
[14] Heslop, H.E. et al . (2010) Long-term outcome of EBV-specific T-cell infusions to prevent or treat EBV-related lymphoproliferative disease in transplant recipients. Blood 115, 925–935.
| Long-term outcome of EBV-specific T-cell infusions to prevent or treat EBV-related lymphoproliferative disease in transplant recipients.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhvFOitr0%3D&md5=700eca907b91dd49d9c55e4348049daaCAS | 19880495PubMed |
[15] Khanna, R. et al. (1999) Activation and adoptive transfer of Epstein–Barr virus-specific cytotoxic T cells in solid organ transplant patients with posttransplant lymphoproliferative disease. Proc. Natl Acad. Sci. USA 96, 10391–10396.
| Activation and adoptive transfer of Epstein–Barr virus-specific cytotoxic T cells in solid organ transplant patients with posttransplant lymphoproliferative disease.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXlvFentL8%3D&md5=eb708ad3ef95545a0225e0f72b5aa5cfCAS | 10468618PubMed |
[16] Haque, T. et al. (2001) Complete regression of posttransplant lymphoproliferative disease using partially HLA-matched Epstein Barr virus-specific cytotoxic T cells. Transplantation 72, 1399–1402.
| Complete regression of posttransplant lymphoproliferative disease using partially HLA-matched Epstein Barr virus-specific cytotoxic T cells.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MnhtV2ntw%3D%3D&md5=efaac24c150f4820f1d4b1938d5009a0CAS | 11685111PubMed |
[17] Haque, T. et al. (2007) Allogeneic cytotoxic T-cell therapy for EBV-positive posttransplantation lymphoproliferative disease: results of a phase 2 multicenter clinical trial. Blood 110, 1123–1131.
| Allogeneic cytotoxic T-cell therapy for EBV-positive posttransplantation lymphoproliferative disease: results of a phase 2 multicenter clinical trial.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXptFKmu78%3D&md5=ad1949940f8b84cea2ffa9d818b57679CAS | 17468341PubMed |
[18] Haque, T. et al. (2002) Treatment of Epstein–Barr-virus-positive post-transplantation lymphoproliferative disease with partly HLA-matched allogeneic cytotoxic T cells. Lancet 360, 436–442.
| Treatment of Epstein–Barr-virus-positive post-transplantation lymphoproliferative disease with partly HLA-matched allogeneic cytotoxic T cells.Crossref | GoogleScholarGoogle Scholar | 12241714PubMed |
[19] Leen, A.M. et al. (2013) Multicenter study of banked third-party virus-specific T cells to treat severe viral infections after hematopoietic stem cell transplantation. Blood 121, 5113–5123.
| Multicenter study of banked third-party virus-specific T cells to treat severe viral infections after hematopoietic stem cell transplantation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtFSnt7fM&md5=d22b9634b7f385bfb8b45bc3f4429739CAS | 23610374PubMed |
[20] Bollard, C.M. et al. (2008) Immunotherapy targeting EBV-expressing lymphoproliferative diseases. Best Pract. Res. Clin. Haematol. 21, 405–420.
| Immunotherapy targeting EBV-expressing lymphoproliferative diseases.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFanurzP&md5=77633262283fa820cd8fb9ef5906ebbdCAS | 18790446PubMed |
[21] Gandhi, M.K. et al. (2004) Epstein–Barr virus‐associated Hodgkin’s lymphoma. Br. J. Haematol. 125, 267–281.
| Epstein–Barr virus‐associated Hodgkin’s lymphoma.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXkvFChsLo%3D&md5=8d53383a68d5b7f57427e69cd4d473e4CAS | 15086409PubMed |
[22] Ahmed, N. and Heslop, H.E. (2006) Viral lymphomagenesis. Curr. Opin. Hematol. 13, 254–259.
| Viral lymphomagenesis.Crossref | GoogleScholarGoogle Scholar | 16755222PubMed |
[23] Koduru, P.R.K. et al. (1993) Phenotypic and genotypic characterization of Hodgkins disease. Am. J. Hematol. 44, 117–124.
| Phenotypic and genotypic characterization of Hodgkins disease.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2c%2FptFarsg%3D%3D&md5=445d45a11e3cf733edc0742df51db5b7CAS |
[24] Gandhi, M.K. et al. (2007) Galectin-1 mediated suppression of Epstein–Barr virus-specific T-cell immunity in classic Hodgkin lymphoma. Blood 110, 1326–1329.
| Galectin-1 mediated suppression of Epstein–Barr virus-specific T-cell immunity in classic Hodgkin lymphoma.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXptFKls7g%3D&md5=ee887f366367d7857e7bb8ec5018c769CAS | 17438085PubMed |
[25] Gandhi, M.K. et al. (2006) Expression of LAG-3 by tumor-infiltrating lymphocytes is coincident with the suppression of latent membrane antigen-specific CD8+ T-cell function in Hodgkin lymphoma patients. Blood 108, 2280–2289.
| Expression of LAG-3 by tumor-infiltrating lymphocytes is coincident with the suppression of latent membrane antigen-specific CD8+ T-cell function in Hodgkin lymphoma patients.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVCgur7F&md5=dac7354c5a937ac4dc0efaf41dba2f4fCAS | 16757686PubMed |
[26] Smith, C. et al. (2009) Acquisition of polyfunctionality by Epstein–Barr virus-specific CD8+ T cells correlates with increased resistance to galectin-1-mediated suppression. J. Virol. 83, 6192–6198.
| Acquisition of polyfunctionality by Epstein–Barr virus-specific CD8+ T cells correlates with increased resistance to galectin-1-mediated suppression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXntFWqur4%3D&md5=bdb9a6c1bdc0d3ea4db679a6736d2e96CAS | 19357166PubMed |
[27] Poppema, S. and van den Berg, A. (2000) Interaction between host T cells and Reed–Sternberg cells in Hodgkin lymphomas. Semin. Cancer Biol. 10, 345–350.
| Interaction between host T cells and Reed–Sternberg cells in Hodgkin lymphomas.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3M7js1ejtQ%3D%3D&md5=a9e653e338cd698271075a8a49ae29b0CAS | 11100882PubMed |
[28] Rosdahl, N. et al. (1974) Hodgkin’s disease in patients with previous infectious mononucleosis: 30 years’ experience. BMJ 2, 253–256.
| Hodgkin’s disease in patients with previous infectious mononucleosis: 30 years’ experience.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE2c7mtVWktQ%3D%3D&md5=284a31f4e351216f071d9f6235c59ec6CAS | 4406463PubMed |
[29] Kanakry, J.A. and Ambinder, R.F. (2013) EBV-related lymphomas: new approaches to treatment. Curr. Treat. Options Oncol. 14, 224–236.
| EBV-related lymphomas: new approaches to treatment.Crossref | GoogleScholarGoogle Scholar | 23549980PubMed |
[30] Kelly, K.M. et al. (2011) BEACOPP chemotherapy is a highly effective regimen in children and adolescents with high-risk Hodgkin lymphoma: a report from the Children’s Oncology Group. Blood 117, 2596–2603.
| BEACOPP chemotherapy is a highly effective regimen in children and adolescents with high-risk Hodgkin lymphoma: a report from the Children’s Oncology Group.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjsVWguro%3D&md5=8fc06af55ed51dce9bdc88323206d781CAS | 21079154PubMed |
[31] Gottschalk, S. et al. (2006) T cell therapies. Ernst Schering Found Symp Proc. , 69–82.
| 1:STN:280:DC%2BD2srislKktA%3D%3D&md5=a3cfb0c04bfc5f1100e55aeb7a8fbe67CAS | 17824182PubMed |
[32] Bollard, C.M. et al. (2006) Administration of latent membrane protein 2-specific cytotoxic T lymphocytes to patients with relapsed Epstein–Barr virus-positive lymphoma. Clin. Lymphoma Myeloma 6, 342–347.
| Administration of latent membrane protein 2-specific cytotoxic T lymphocytes to patients with relapsed Epstein–Barr virus-positive lymphoma.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XisFWktbc%3D&md5=5a27089829a7b3bc9ebc62869cc1efeeCAS | 16507214PubMed |
[33] Gottschalk, S. et al. (2005) Adoptive immunotherapy for EBV-associated malignancies. Leuk. Lymphoma 46, 1–10.
| Adoptive immunotherapy for EBV-associated malignancies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtFSntr3J&md5=b224fd899268216268dde48a5947e402CAS | 15621775PubMed |
[34] Bollard, C.M. et al. (2004) The generation and characterization of LMP2-specific CTLs for use as adoptive transfer from patients with relapsed EBV-positive Hodgkin disease. J. Immunother. 27, 317–327.
| The generation and characterization of LMP2-specific CTLs for use as adoptive transfer from patients with relapsed EBV-positive Hodgkin disease.Crossref | GoogleScholarGoogle Scholar | 15235393PubMed |
[35] Bollard, C.M. et al. (2004) Cytotoxic T lymphocyte therapy for Epstein–Barr virus+ Hodgkin’s disease. J. Exp. Med. 200, 1623–1633.
| Cytotoxic T lymphocyte therapy for Epstein–Barr virus+ Hodgkin’s disease.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtFGmurbI&md5=32f7f7903ad5424c42a641481533a6e6CAS | 15611290PubMed |
[36] Straathof, K.C. et al. (2003) Immunotherapy for Epstein–Barr virus-associated cancers in children. Oncologist 8, 83–98.
| Immunotherapy for Epstein–Barr virus-associated cancers in children.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhvVyqtr0%3D&md5=1e00b7370485ffb839c5df675c1a8e36CAS | 12604735PubMed |
[37] Smith, C. et al. (2006) Functional reversion of antigen-specific CD8+ T cells from patients with Hodgkin lymphoma following in vitro stimulation with recombinant polyepitope. J. Immunol. 177, 4897–4906.
| 1:CAS:528:DC%2BD28Xps1GnsLk%3D&md5=f8c327b8ded39d6142eaf06f93ae61e8CAS | 16982932PubMed |
[38] Heslop, H.E. (2005) Biology and treatment of Epstein–Barr virus-associated non-Hodgkin lymphomas. Hematology (Am Soc Hematol Educ Program) , 260–266.
| Biology and treatment of Epstein–Barr virus-associated non-Hodgkin lymphomas.Crossref | GoogleScholarGoogle Scholar | 16304390PubMed |
[39] Njie, R. et al. (2009) The effects of acute malaria on Epstein–Barr virus (EBV) load and EBV-specific T cell immunity in Gambian children. J. Infect. Dis. 199, 31–38.
| The effects of acute malaria on Epstein–Barr virus (EBV) load and EBV-specific T cell immunity in Gambian children.Crossref | GoogleScholarGoogle Scholar | 19032105PubMed |
[40] Chattopadhyay, P.K. et al. (2013) Holoendemic malaria exposure is associated with altered Epstein–Barr virus-specific CD8(+) T-cell differentiation. J. Virol. 87, 1779–1788.
| Holoendemic malaria exposure is associated with altered Epstein–Barr virus-specific CD8(+) T-cell differentiation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXltV2itL0%3D&md5=ad3db2d2841e0bfb60896be1622ac8e1CAS | 23175378PubMed |
[41] Münz, C. et al. (2000) Human CD4(+) T lymphocytes consistently respond to the latent Epstein–Barr virus nuclear antigen EBNA1. J. Exp. Med. 191, 1649–1660.
| Human CD4(+) T lymphocytes consistently respond to the latent Epstein–Barr virus nuclear antigen EBNA1.Crossref | GoogleScholarGoogle Scholar | 10811859PubMed |
[42] Khanna, R. and Burrows, S.R. (2000) Role of cytotoxic T lymphocytes in Epstein–Barr virus-associated diseases. Annu. Rev. Microbiol. 54, 19–48.
| Role of cytotoxic T lymphocytes in Epstein–Barr virus-associated diseases.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXotFWrsrc%3D&md5=6eb6c377f365217cf00e30da6e92b27cCAS | 11018123PubMed |
[43] Moss, D.J. et al. (1999) Developing immunotherapeutic strategies for the control of Epstein–Barr virus-associated malignancies. J. Acquir. Immune. Defic. Syndr. 21, S80–S83.
| 1:CAS:528:DC%2BD3cXjtlKktbk%3D&md5=61a47019a3807bfb3224591ce0484663CAS | 10430223PubMed |
[44] Haluska, F.G. et al. (1986) The t(8; 14) chromosomal translocation occurring in B-cell malignancies results from mistakes in V-D-J joining. Nature 324, 158–161.
| The t(8; 14) chromosomal translocation occurring in B-cell malignancies results from mistakes in V-D-J joining.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXivVCjtg%3D%3D&md5=abf3905aeb5b991479eaefc3b36a6652CAS | 3097550PubMed |
[45] Razak, A.R. et al. (2010) Nasopharyngeal carcinoma: the next challenges. Eur. J. Cancer 46, 1967–1978.
| Nasopharyngeal carcinoma: the next challenges.Crossref | GoogleScholarGoogle Scholar | 20451372PubMed |
[46] Cho, W.C. (2007) Nasopharyngeal carcinoma: molecular biomarker discovery and progress. Mol. Cancer 6, 1.
| Nasopharyngeal carcinoma: molecular biomarker discovery and progress.Crossref | GoogleScholarGoogle Scholar | 17199893PubMed |
[47] Chan, A.T. et al. (2002) Nasopharyngeal carcinoma. Ann. Oncol. 13, 1007–1015.
| Nasopharyngeal carcinoma.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38vitFWgtg%3D%3D&md5=8c528d87fc489cf1c787f1d8786406eaCAS | 12176778PubMed |
[48] Raab-Traub, N. (2002) Epstein–Barr virus in the pathogenesis of NPC. Semin.Cancer Biol. 12, 431–441.
| Epstein–Barr virus in the pathogenesis of NPC.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xosl2gu7o%3D&md5=26786e326927f07b6442c3f76ec3e6aeCAS | 12450729PubMed |
[49] Bensouda, Y. et al. (2011) Treatment for metastatic nasopharyngeal carcinoma. Eur. Ann. Otorhinolaryngol. Head Neck Dis. 128, 79–85.
| Treatment for metastatic nasopharyngeal carcinoma.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3Mvls1eruw%3D%3D&md5=a68031c3795ee1d6d90e2a0ef02b9291CAS | 21177151PubMed |
[50] Smith, C. et al. (2012) Effective treatment of metastatic forms of Epstein–Barr virus-associated nasopharyngeal carcinoma with a novel adenovirus-based adoptive immunotherapy. Cancer Res. 72, 1116–1125.
| Effective treatment of metastatic forms of Epstein–Barr virus-associated nasopharyngeal carcinoma with a novel adenovirus-based adoptive immunotherapy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xjt1Wisrw%3D&md5=026d538092744dbfb38b82bdf333beabCAS | 22282657PubMed |
[51] Tse, E. and Kwong, Y.L. (2013) How I treat NK/T-cell lymphomas. Blood 121, 4997–5005.
| How I treat NK/T-cell lymphomas.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtVartL%2FF&md5=0eeb3c9aee3fb4037aece653b2503aedCAS | 23652805PubMed |
[52] Bugalia, A. et al. (2013) Immunomorphologic profile and Epstein–Barr virus status of a cohort of 35 cases of extranodal natural killer/T-cell lymphoma, nasal type of upper aerodigestive tract from a tertiary care center in South India. Leuk. Lymphoma 54, 1201–1207.
| Immunomorphologic profile and Epstein–Barr virus status of a cohort of 35 cases of extranodal natural killer/T-cell lymphoma, nasal type of upper aerodigestive tract from a tertiary care center in South India.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXns1ahu78%3D&md5=0c9964b85d27f3216a6fe057bb4c711eCAS | 23098105PubMed |
[53] Hildesheim, A. (2013) Invited commentary: Epstein–Barr virus-based screening for the early detection of nasopharyngeal carcinoma: a new frontier. Am. J. Epidemiol. 177, 251–253.
| Invited commentary: Epstein–Barr virus-based screening for the early detection of nasopharyngeal carcinoma: a new frontier.Crossref | GoogleScholarGoogle Scholar | 23255781PubMed |
[54] Lee, J.H. et al. (2009) Clinicopathological and molecular characteristics of Epstein–Barr virus-associated gastric carcinoma: a meta-analysis. J. Gastroenterol. Hepatol. 24, 354–365.
| Clinicopathological and molecular characteristics of Epstein–Barr virus-associated gastric carcinoma: a meta-analysis.Crossref | GoogleScholarGoogle Scholar | 19335785PubMed |
[55] Shah, K.M. and Young, L.S. (2009) Epstein–Barr virus and carcinogenesis: beyond Burkitt’s lymphoma. Clin. Microbiol. Infect. 15, 982–988.
| Epstein–Barr virus and carcinogenesis: beyond Burkitt’s lymphoma.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFChtbrM&md5=390a84bf0368e2ccb5837865273a0d28CAS | 19874382PubMed |
[56] Trimeche, M. et al. (2009) Prevalence and characteristics of Epstein–Barr virus-associated gastric carcinomas in Tunisia. Eur. J. Gastroenterol. Hepatol. 21, 1001–1007.
| Prevalence and characteristics of Epstein–Barr virus-associated gastric carcinomas in Tunisia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXps1Cjur4%3D&md5=f050f013863d11672245665a4513c996CAS | 19491698PubMed |
[57] Kim, D.N. et al. (2013) Characterization of naturally Epstein–Barr virus-infected gastric carcinoma cell line YCCEL1. J. Gen. Virol. 94, 497–506.
| Characterization of naturally Epstein–Barr virus-infected gastric carcinoma cell line YCCEL1.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXltVyqsrk%3D&md5=1308d13ef04b9ccaeed590ae2047d907CAS |
[58] Wang, Y. et al. (2010) Variations of Epstein–Barr virus nuclear antigen 1 gene in gastric carcinomas and nasopharyngeal carcinomas from Northern China. Virus Res. 147, 258–264.
| Variations of Epstein–Barr virus nuclear antigen 1 gene in gastric carcinomas and nasopharyngeal carcinomas from Northern China.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXpt1Wi&md5=be23ad8c58894ed3e67b0c923fce4b02CAS | 19941915PubMed |
[59] Saito, M. et al. (2013) Role of DNA methylation in the development of Epstein–Barr virus-associated gastric carcinoma. J. Med. Virol. 85, 121–127.
| Role of DNA methylation in the development of Epstein–Barr virus-associated gastric carcinoma.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhs1Kms73O&md5=3e497020045eacee5301a75fa1e056a5CAS | 23073987PubMed |