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EBV in T-/NK-Cell Tumorigenesis

  • Hiroshi Kimura
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1045)

Abstract

Epstein–Barr virus (EBV), which is associated with B-cell proliferative disorders, also transforms T- or natural killer (NK)-lineage cells and has been connected with various T- or NK (T/NK)-cell malignancies, such as extranodal NK/T-cell lymphoma-nasal type and aggressive NK-cell leukemia. Chronic active EBV (CAEBV) disease, which occurs most often in children and young adults in East Asia, is an EBV-associated T-/NK-cell lymphoproliferative disease. Patients with CAEBV often progress to overt lymphoma or leukemia over a long-term clinical course. EBV’s transforming capacity in B cells is well characterized, but the molecular pathogenesis of clonal expansion caused by EBV in T/NK cells has not yet been clarified. In the primary infection, EBV infects B cells and epithelial cells and may also infect some T/NK cells. In some individuals, because of poor presentation by specific human leukocyte antigens or the genetic background, EBV-infected T/NK cells evade host immunity and survive. Occasionally, with the help of viral oncogenes, EBV-associated T/NK lymphoproliferative diseases, such as CAEBV, may develop. The subsequent accumulation of genetic mutations and/or epigenetic modifications in driver genes, such as DDX3X and TP53, may lead to overt lymphoma and leukemia. Activation-induced cytidine deaminase and the APOBEC3 family, driven by EBV infection, may induce chromosomal recombination and somatic mutations.

Keywords

AID CAEBV Chronic active EBV disease DDX3X ENKL Extranodal NK/T-cell lymphoma-nasal type EBV-T/NK LPD Lymphomagenesis Lymphoproliferative disease 

References

  1. Alfieri C, Joncas JH (1987) Biomolecular analysis of a defective nontransforming Epstein-Barr virus (EBV) from a patient with chronic active EBV infection. J Virol 61:3306–3309PubMedPubMedCentralGoogle Scholar
  2. Anagnostopoulos I, Hummel M, Kreschel C, Stein H (1995) Morphology, immunophenotype, and distribution of latently and/or productively Epstein-Barr virus-infected cells in acute infectious mononucleosis: implications for the interindividual infection route of Epstein-Barr virus. Blood 85:744–750PubMedGoogle Scholar
  3. Aozasa K, Takakuwa T, Hongyo T, Yang WI (2008) Nasal NK/T-cell lymphoma: epidemiology and pathogenesis. Int J Hematol 87:110–117PubMedPubMedCentralCrossRefGoogle Scholar
  4. Borza CM, Hutt-Fletcher LM (2002) Alternate replication in B cells and epithelial cells switches tropism of Epstein-Barr virus. Nat Med 8:594–599PubMedCrossRefGoogle Scholar
  5. Chan JKC, Jaffe ES, Ralfkiaer E, Ko YH (2008a) Aggressive NK-cell leukaemia. In: Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, Thiele J (eds) WHO classification of tumours of haematopoietic and lymphoid tissues. WHO Press, LyonGoogle Scholar
  6. Chan JKC, Quintanilla-Martinez L, Ferry JA, Peh S-C (2008b) Extranodal NK/T-cell lymphoma, nasal type. In: Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, Thiele J (eds) WHO classification of tumours of haematopoietic and lymphoid tissues, 4th edn. WHO Press, LyonGoogle Scholar
  7. Chen CL, Sadler RH, Walling DM, Su IJ, Hsieh HC, Raab-Traub N (1993) Epstein-Barr virus (EBV) gene expression in EBV-positive peripheral T-cell lymphomas. J Virol 67:6303–6308PubMedPubMedCentralGoogle Scholar
  8. Cohen JI (2000) Epstein-Barr virus infection. N Engl J Med 343:481–492PubMedCrossRefGoogle Scholar
  9. Cohen JI, Kimura H, Nakamura S, Ko YH, Jaffe ES (2009) Epstein-Barr virus-associated lymphoproliferative disease in non-immunocompromised hosts: a status report and summary of an international meeting, 8–9 September 2008. Ann Oncol 20:1472–1482PubMedPubMedCentralCrossRefGoogle Scholar
  10. Cohen JI, Jaffe ES, Dale JK, Pittaluga S, Heslop HE, Rooney CM, Gottschalk S, Bollard CM, Rao VK, Marques A, Burbelo PD, Turk SP, Fulton R, Wayne AS, Little RF, Cairo MS, El-Mallawany NK, Fowler D, Sportes C, Bishop MR, Wilson W, Straus SE (2011) Characterization and treatment of chronic active Epstein-Barr virus disease: a 28-year experience in the United States. Blood 117:5835–5849PubMedPubMedCentralCrossRefGoogle Scholar
  11. Coleman CB, Wohlford EM, Smith NA, King CA, Ritchie JA, Baresel PC, Kimura H, Rochford R (2015) Epstein-Barr virus type 2 latently infects T cells, inducing an atypical activation characterized by expression of lymphotactic cytokines. J Virol 89:2301–2312PubMedCrossRefGoogle Scholar
  12. Dobashi A, Tsuyama N, Asaka R, Togashi Y, Ueda K, Sakata S, Baba S, Sakamoto K, Hatake K, Takeuchi K (2016) Frequent BCOR aberrations in extranodal NK/T-Cell lymphoma, nasal type. Genes Chromosomes Cancer 55:460–471PubMedCrossRefGoogle Scholar
  13. Elenitoba-Johnson KS, Zarate-Osorno A, Meneses A, Krenacs L, Kingma DW, Raffeld M, Jaffe ES (1998) Cytotoxic granular protein expression, Epstein-Barr virus strain type, and latent membrane protein-1 oncogene deletions in nasal T-lymphocyte/natural killer cell lymphomas from Mexico. Mod Pathol 11:754–761PubMedGoogle Scholar
  14. Endo R, Yoshioka M, Ebihara T, Ishiguro N, Kikuta H, Kobayashi K (2004) Clonal expansion of multiphenotypic Epstein-Barr virus-infected lymphocytes in chronic active Epstein-Barr virus infection. Med Hypotheses 63:582–587PubMedCrossRefGoogle Scholar
  15. Epstein MA, Achong BG, Barr YM (1964) Virus particles in cultured lymphoblasts from Burkitt’s lymphoma. Lancet 1:702–703PubMedCrossRefGoogle Scholar
  16. Fischer E, Delibrias C, Kazatchkine MD (1991) Expression of CR2 (the C3dg/EBV receptor, CD21) on normal human peripheral blood T lymphocytes. J Immunol 146:865–869PubMedGoogle Scholar
  17. Fischer EM, Mouhoub A, Maillet F, Fremeaux-Bacchi V, Krief C, Gould H, Berrih-Aknin S, Kazatchkine MD (1999) Expression of CD21 is developmentally regulated during thymic maturation of human T lymphocytes. Int Immunol 11:1841–1849PubMedCrossRefGoogle Scholar
  18. Fox CP, Haigh TA, Taylor GS, Long HM, Lee SP, Shannon-Lowe C, O'connor S, Bollard CM, Iqbal J, Chan WC, Rickinson AB, Bell AI, Rowe M (2010) A novel latent membrane 2 transcript expressed in Epstein-Barr virus-positive NK- and T-cell lymphoproliferative disease encodes a target for cellular immunotherapy. Blood 116:3695–3704PubMedPubMedCentralCrossRefGoogle Scholar
  19. Fujiwara S, Ono Y (1995) Isolation of Epstein-Barr virus-infected clones of the human T-cell line MT-2: use of recombinant viruses with a positive selection marker. J Virol 69:3900–3903PubMedPubMedCentralGoogle Scholar
  20. Fujiwara S, Kimura H, Imadome K, Arai A, Kodama E, Morio T, Shimizu N, Wakiguchi H (2014) Current research on chronic active Epstein-Barr virus infection in Japan. Pediatr Int 56:159–166PubMedCrossRefGoogle Scholar
  21. Gotoh K, Ito Y, Shibata-Watanabe Y, Kawada J, Takahashi Y, Yagasaki H, Kojima S, Nishiyama Y, Kimura H (2008) Clinical and virological characteristics of 15 patients with chronic active Epstein-Barr virus infection treated with hematopoietic stem cell transplantation. Clin Infect Dis 46:1525–1534PubMedCrossRefGoogle Scholar
  22. Gru AA, Haverkos BH, Freud AG, Hastings J, Nowacki NB, Barrionuevo C, Vigil CE, Rochford R, Natkunam Y, Baiocchi RA, Porcu P (2015) The Epstein-Barr virus (EBV) in T cell and NK cell lymphomas: time for a reassessment. Curr Hematol Malig Rep 10:456–467PubMedPubMedCentralCrossRefGoogle Scholar
  23. Grywalska E, Rolinski J (2015) Epstein-Barr virus-associated lymphomas. Semin Oncol 42:291–303PubMedCrossRefGoogle Scholar
  24. Guo Y, Arakawa F, Miyoshi H, Niino D, Kawano R, Ohshima K (2014) Activated janus kinase 3 expression not by activating mutations identified in natural killer/T-cell lymphoma. Pathol Int 64(6):263PubMedCrossRefGoogle Scholar
  25. Harabuchi Y, Yamanaka N, Kataura A, Imai S, Kinoshita T, Mizuno F, Osato T (1990) Epstein-Barr virus in nasal T-cell lymphomas in patients with lethal midline granuloma. Lancet 335:128–130PubMedCrossRefGoogle Scholar
  26. Hart DN, Baker BW, Inglis MJ, Nimmo JC, Starling GC, Deacon E, Rowe M, Beard ME (1992) Epstein-Barr viral DNA in acute large granular lymphocyte (natural killer) leukemic cells. Blood 79:2116–2123PubMedGoogle Scholar
  27. He B, Raab-Traub N, Casali P, Cerutti A (2003) EBV-encoded latent membrane protein 1 cooperates with BAFF/BLyS and APRIL to induce T cell-independent Ig heavy chain class switching. J Immunol 171:5215–5224PubMedPubMedCentralCrossRefGoogle Scholar
  28. Hildesheim A, Apple RJ, Chen CJ, Wang SS, Cheng YJ, Klitz W, Mack SJ, Chen IH, Hsu MM, Yang CS, Brinton LA, Levine PH, Erlich HA (2002) Association of HLA class I and II alleles and extended haplotypes with nasopharyngeal carcinoma in Taiwan. J Natl Cancer Inst 94:1780–1789PubMedCrossRefGoogle Scholar
  29. Honjo T, Muramatsu M, Fagarasan S (2004) AID: how does it aid antibody diversity? Immunity 20:659–668CrossRefGoogle Scholar
  30. Huang Y, De Reynies A, De Leval L, Ghazi B, Martin-Garcia N, Travert M, Bosq J, Briere J, Petit B, Thomas E, Coppo P, Marafioti T, Emile JF, Delfau-Larue MH, Schmitt C, Gaulard P (2010) Gene expression profiling identifies emerging oncogenic pathways operating in extranodal NK/T-cell lymphoma, nasal type. Blood 115:1226–1237PubMedPubMedCentralCrossRefGoogle Scholar
  31. Hudnall SD, Ge Y, Wei L, Yang NP, Wang HQ, Chen T (2005) Distribution and phenotype of Epstein-Barr virus-infected cells in human pharyngeal tonsils. Mod Pathol 18:519–527PubMedCrossRefGoogle Scholar
  32. Hutt-Fletcher LM (2007) Epstein-Barr virus entry. J Virol 81:7825–7832PubMedPubMedCentralCrossRefGoogle Scholar
  33. Ichigi Y, Naitoh K, Tokushima M, Haraoka S, Tagoh H, Kimoto M, Muraguchi A (1993) Generation of cells with morphological and antigenic properties of microglia from cloned EBV-transformed lymphoid progenitor cells derived from human fetal liver. Cell Immunol 149:193–207PubMedCrossRefGoogle Scholar
  34. Imadome K, Yajima M, Arai A, Nakazawa A, Kawano F, Ichikawa S, Shimizu N, Yamamoto N, Morio T, Ohga S, Nakamura H, Ito M, Miura O, Komano J, Fujiwara S (2011) Novel mouse xenograft models reveal a critical role of CD4+ T cells in the proliferation of EBV-infected T and NK cells. PLoS Pathog 7:e1002326PubMedPubMedCentralCrossRefGoogle Scholar
  35. Imai S, Sugiura M, Oikawa O, Koizumi S, Hirao M, Kimura H, Hayashibara H, Terai N, Tsutsumi H, Oda T, Chiba S, Osato T (1996) Epstein-Barr virus (EBV)-carrying and -expressing T-cell lines established from severe chronic active EBV infection. Blood 87:1446–1457PubMedGoogle Scholar
  36. Iqbal J, Kucuk C, Deleeuw RJ, Srivastava G, Tam W, Geng H, Klinkebiel D, Christman JK, Patel K, Cao K, Shen L, Dybkaer K, Tsui IF, Ali H, Shimizu N, Au WY, Lam WL, Chan WC (2009) Genomic analyses reveal global functional alterations that promote tumor growth and novel tumor suppressor genes in natural killer-cell malignancies. Leukemia 23:1139–1151PubMedCrossRefGoogle Scholar
  37. Ishihara S, Okada S, Wakiguchi H, Kurashige T, Hirai K, Kawa-Ha K (1997) Clonal lymphoproliferation following chronic active Epstein-Barr virus infection and hypersensitivity to mosquito bites. Am J Hematol 54:276–281PubMedCrossRefGoogle Scholar
  38. Ishikawa C, Nakachi S, Senba M, Sugai M, Mori N (2011) Activation of AID by human T-cell leukemia virus Tax oncoprotein and the possible role of its constitutive expression in ATL genesis. Carcinogenesis 32:110–119PubMedCrossRefGoogle Scholar
  39. Isobe Y, Sugimoto K, Yang L, Tamayose K, Egashira M, Kaneko T, Takada K, Oshimi K (2004) Epstein-Barr virus infection of human natural killer cell lines and peripheral blood natural killer cells. Cancer Res 64:2167–2174PubMedCrossRefGoogle Scholar
  40. Itakura O, Yamada S, Narita M, Kikuta H (1996) High prevalence of a 30-base pair deletion and single-base mutations within the carboxy terminal end of the LMP-1 oncogene of Epstein-Barr virus in the Japanese population. Oncogene 13:1549–1553PubMedGoogle Scholar
  41. Ito Y, Kawamura Y, Iwata S, Kawada J, Yoshikawa T, Kimura H (2013a) Demonstration of type II latency in T lymphocytes of Epstein-Barr virus-associated hemophagocytic lymphohistiocytosis. Pediatr Blood Cancer 60:326–328PubMedCrossRefGoogle Scholar
  42. Ito Y, Suzuki R, Torii Y, Kawa K, Kikuta A, Kojima S, Kimura H (2013b) HLA-A*26 and HLA-B*52 are associated with a risk of developing EBV-associated T/NK lymphoproliferative disease. Blood e-Letter, bloodjournal_el; 8085Google Scholar
  43. Iwata S, Wada K, Tobita S, Gotoh K, Ito Y, Demachi-Okamura A, Shimizu N, Nishiyama Y, Kimura H (2010) Quantitative analysis of Epstein-Barr virus (EBV)-related gene expression in patients with chronic active EBV infection. J Gen Virol 91:42–50PubMedCrossRefGoogle Scholar
  44. Iwatsuki K, Xu Z, Takata M, Iguchi M, Ohtsuka M, Akiba H, Mitsuhashi Y, Takenoshita H, Sugiuchi R, Tagami H, Kaneko F (1999) The association of latent Epstein-Barr virus infection with hydroa vacciniforme. Br J Dermatol 140:715–721PubMedCrossRefGoogle Scholar
  45. Jiang L, Gu ZH, Yan ZX, Zhao X, Xie YY, Zhang ZG, Pan CM, Hu Y, Cai CP, Dong Y, Huang JY, Wang L, Shen Y, Meng G, Zhou JF, Hu JD, Wang JF, Liu YH, Yang LH, Zhang F, Wang JM, Wang Z, Peng ZG, Chen FY, Sun ZM, Ding H, Shi JM, Hou J, Yan JS, Shi JY, Xu L, Li Y, Lu J, Zheng Z, Xue W, Zhao WL, Chen Z, Chen SJ (2015) Exome sequencing identifies somatic mutations of DDX3X in natural killer/T-cell lymphoma. Nat Genet 47:1061–1066PubMedCrossRefGoogle Scholar
  46. Jones J, Shurin S, Abramowsky C, Tubbs R, Sciotto C, Wahl R, Sands J, Gottman D, Katz B, Sklar J (1988) T-cell lymphomas containing Epstein-Barr viral DNA in patients with chronic Epstein-Barr virus infections. N Engl J Med 318:733–741PubMedCrossRefGoogle Scholar
  47. Kanemitsu N, Isobe Y, Masuda A, Momose S, Higashi M, Tamaru JI, Sugimoto K, Komatsu N (2012) Expression of Epstein-Barr virus-encoded proteins in extranodal NK/T-cell lymphoma, nasal type (ENKL): differences in biological and clinical behaviors of LMP1-positive and -negative ENKL. Clin Cancer Res 18:2164–2172PubMedCrossRefGoogle Scholar
  48. Karube K, Nakagawa M, Tsuzuki S, Takeuchi I, Honma K, Nakashima Y, Shimizu N, Ko YH, Morishima Y, Ohshima K, Nakamura S, Seto M (2011) Identification of FOXO3 and PRDM1 as tumor-suppressor gene candidates in NK-cell neoplasms by genomic and functional analyses. Blood 118:3195–3204PubMedCrossRefGoogle Scholar
  49. Kasahara Y, Yachie A, Takei K, Kanegane C, Okada K, Ohta K, Seki H, Igarashi N, Maruhashi K, Katayama K, Katoh E, Terao G, Sakiyama Y, Koizumi S (2001) Differential cellular targets of Epstein-Barr virus (EBV) infection between acute EBV-associated hemophagocytic lymphohistiocytosis and chronic active EBV infection. Blood 98:1882–1888PubMedCrossRefGoogle Scholar
  50. Kawa K, Sawada A, Sato M, Okamura T, Sakata N, Kondo O, Kimoto T, Yamada K, Tokimasa S, Yasui M, Inoue M (2011) Excellent outcome of allogeneic hematopoietic SCT with reduced-intensity conditioning for the treatment of chronic active EBV infection. Bone Marrow Transplant 46:77–83PubMedCrossRefGoogle Scholar
  51. Kawaguchi H, Miyashita T, Herbst H, Niedobitek G, Asada M, Tsuchida M, Hanada R, Kinoshita A, Sakurai M, Kobayashi N, Et A (1993) Epstein-Barr virus-infected T lymphocytes in Epstein-Barr virus-associated hemophagocytic syndrome. J Clin Invest 92:1444–1450PubMedPubMedCentralCrossRefGoogle Scholar
  52. Kawa-Ha K, Ishihara S, Ninomiya T, Yumura-Yagi K, Hara J, Murayama F, Tawa A, Hirai K (1989) CD3-negative lymphoproliferative disease of granular lymphocytes containing Epstein-Barr viral DNA. J Clin Invest 84:51–55PubMedPubMedCentralCrossRefGoogle Scholar
  53. Kikuta H, Taguchi Y, Tomizawa K, Kojima K, Kawamura N, Ishizaka A, Sakiyama Y, Matsumoto S, Imai S, Kinoshita T, Et A (1988) Epstein-Barr virus genome-positive T lymphocytes in a boy with chronic active EBV infection associated with Kawasaki-like disease. Nature 333:455–457PubMedCrossRefGoogle Scholar
  54. Kim JH, Kim WS, Park C (2013) Epstein-Barr virus latent membrane protein 1 increases genomic instability through Egr-1-mediated up-regulation of activation-induced cytidine deaminase in B-cell lymphoma. Leuk Lymphoma 54:2035–2040PubMedCrossRefGoogle Scholar
  55. Kimura H (2006) Pathogenesis of chronic active Epstein-Barr virus infection: is this an infectious disease, lymphoproliferative disorder, or immunodeficiency? Rev Med Virol 16:251–261PubMedCrossRefGoogle Scholar
  56. Kimura H, Morishima T, Kanegane H, Ohga S, Hoshino Y, Maeda A, Imai S, Okano M, Morio T, Yokota S, Tsuchiya S, Yachie A, Imashuku S, Kawa K, Wakiguchi H (2003) Prognostic factors for chronic active Epstein-Barr virus infection. J Infect Dis 187:527–533PubMedCrossRefGoogle Scholar
  57. Kimura H, Hoshino Y, Hara S, Sugaya N, Kawada J, Shibata Y, Kojima S, Nagasaka T, Kuzushima K, Morishima T (2005) Differences between T cell-type and natural killer cell-type chronic active Epstein-Barr virus infection. J Infect Dis 191:531–539PubMedCrossRefGoogle Scholar
  58. Kimura H, Ito Y, Kawabe S, Gotoh K, Takahashi Y, Kojima S, Naoe T, Esaki S, Kikuta A, Sawada A, Kawa K, Ohshima K, Nakamura S (2012) EBV-associated T/NK-cell lymphoproliferative diseases in nonimmunocompromised hosts: prospective analysis of 108 cases. Blood 119:673–686PubMedCrossRefGoogle Scholar
  59. Kimura H, Kawada J, Ito Y (2013) Epstein-Barr virus-associated lymphoid malignancies: the expanding spectrum of hematopoietic neoplasms. Nagoya J Med Sci 75:169–179PubMedPubMedCentralGoogle Scholar
  60. Kimura H, Karube K, Ito Y, Hirano K, Suzuki M, Iwata S, Seto M (2014) Rare occurrence of JAK3 mutations in natural killer cell neoplasms in Japan. Leuk Lymphoma 55:962–963PubMedCrossRefGoogle Scholar
  61. Koo GC, Tan SY, Tang T, Poon SL, Allen GE, Tan L, Chong SC, Ong WS, Tay K, Tao M, Quek R, Loong S, Yeoh KW, Yap SP, Lee KA, Lim LC, Tan D, Goh C, Cutcutache I, Yu W, Ng CC, Rajasegaran V, Heng HL, Gan A, Ong CK, Rozen S, Tan P, Teh BT, Lim ST (2012) Janus kinase 3-activating mutations identified in natural killer/T-cell lymphoma. Cancer Discov 2(7):591PubMedCrossRefGoogle Scholar
  62. Li Z, Xia Y, Feng LN, Chen JR, Li HM, Cui J, Cai QQ, Sim KS, Nairismagi ML, Laurensia Y, Meah WY, Liu WS, Guo YM, Chen LZ, Feng QS, Pang CP, Chen LJ, Chew SH, Ebstein RP, Foo JN, Liu J, Ha J, Khoo LP, Chin ST, Zeng YX, Aung T, Chowbay B, Diong CP, Zhang F, Liu YH, Tang T, Tao M, Quek R, Mohamad F, Tan SY, Teh BT, Ng SB, Chng WJ, Ong CK, Okada Y, Raychaudhuri S, Lim ST, Tan W, Peng RJ, Khor CC, Bei JX (2016) Genetic risk of extranodal natural killer T-cell lymphoma: a genome-wide association study. Lancet Oncol 17:1240–1247PubMedCrossRefGoogle Scholar
  63. Li YY, Chung GT, Lui VW, To KF, Ma BB, Chow C, Woo JK, Yip KY, Seo J, Hui EP, Mak MK, Rusan M, Chau NG, Or YY, Law MH, Law PP, Liu ZW, Ngan HL, Hau PM, Verhoeft KR, Poon PH, Yoo SK, Shin JY, Lee SD, Lun SW, Jia L, Chan AW, Chan JY, Lai PB, Fung CY, Hung ST, Wang L, Chang AM, Chiosea SI, Hedberg ML, Tsao SW, Van Hasselt AC, Chan AT, Grandis JR, Hammerman PS, Lo KW (2017) Exome and genome sequencing of nasopharynx cancer identifies NF-kappaB pathway activating mutations. Nat Commun 8:14121PubMedPubMedCentralCrossRefGoogle Scholar
  64. Longnecker R, Kieff E, Cohen JI (2013) Epstein-Barr virus. In: Knipe DM, Howley PM (eds) Fields virology, 6th edn. Lippincott Williams & Willkins, PhiladelphiaGoogle Scholar
  65. Louie E, Henderson BE, Buell P, Jing JS, Menck HR, Pike MC (1977) Selected observations on the epidemiology of pharyngeal cancers. Natl Cancer Inst Monogr 47:129–133PubMedGoogle Scholar
  66. Nakamura M, Iwata S, Kimura H, Tokura Y (2011a) Elevated expression of activation-induced cytidine deaminase in T and NK cells from patients with chronic active Epstein-Barr virus infection. Eur J Dermatol 21:780–782PubMedGoogle Scholar
  67. Nakamura M, Sugita K, Sawada Y, Yoshiki R, Hino R, Tokura Y (2011b) High levels of activation-induced cytidine deaminase expression in adult T-cell leukaemia/lymphoma. Br J Dermatol 165:437–439PubMedCrossRefGoogle Scholar
  68. Neves M, Marinho-Dias J, Ribeiro J, Sousa H (2017) Epstein-Barr virus strains and variations: geographic or disease-specific variants? J Med Virol 89:373–387PubMedCrossRefGoogle Scholar
  69. Niens M, Jarrett RF, Hepkema B, Nolte IM, Diepstra A, Platteel M, Kouprie N, Delury CP, Gallagher A, Visser L, Poppema S, Te Meerman GJ, Van Den Berg A (2007) HLA-A*02 is associated with a reduced risk and HLA-A*01 with an increased risk of developing EBV+ Hodgkin lymphoma. Blood 110:3310–3315PubMedCrossRefGoogle Scholar
  70. Ohga S, Ishimura M, Yoshimoto G, Miyamoto T, Takada H, Tanaka T, Ohshima K, Ogawa Y, Imadome K, Abe Y, Akashi K, Hara T (2011) Clonal origin of Epstein-Barr virus (EBV)-infected T/NK-cell subpopulations in EBV-positive T/NK-cell lymphoproliferative disorders of childhood. J Clin Virol 51:31–37PubMedCrossRefGoogle Scholar
  71. Ohshima K, Suzumiya J, Ohga S, Ohgami A, Kikuchi M (1997a) Integrated Epstein-Barr virus (EBV) and chromosomal abnormality in chronic active EBV infection. Int J Cancer 71:943–947PubMedCrossRefGoogle Scholar
  72. Ohshima K, Suzumiya J, Shimazaki K, Kato A, Tanaka T, Kanda M, Kikuchi M (1997b) Nasal T/NK cell lymphomas commonly express perforin and Fas ligand: important mediators of tissue damage. Histopathology 31:444–450PubMedCrossRefGoogle Scholar
  73. Ohshima K, Suzumiya J, Sugihara M, Nagafuchi S, Ohga S, Kikuchi M (1999) CD95 (Fas) ligand expression of Epstein-Barr virus (EBV)-infected lymphocytes: a possible mechanism of immune evasion in chronic active EBV infection. Pathol Int 49:9–13PubMedCrossRefGoogle Scholar
  74. Okano M, Kawa K, Kimura H, Yachie A, Wakiguchi H, Maeda A, Imai S, Ohga S, Kanegane H, Tsuchiya S, Morio T, Mori M, Yokota S, Imashuku S (2005) Proposed guidelines for diagnosing chronic active Epstein-Barr virus infection. Am J Hematol 80:64–69PubMedCrossRefGoogle Scholar
  75. Okazaki IM, Hiai H, Kakazu N, Yamada S, Muramatsu M, Kinoshita K, Honjo T (2003) Constitutive expression of AID leads to tumorigenesis. J Exp Med 197:1173–1181PubMedPubMedCentralCrossRefGoogle Scholar
  76. Osato T, Mizuno F, Imai S, Aya T, Koizumi S, Kinoshita T, Tokuda H, Ito Y, Hirai N, Hirota M et al (1987) African Burkitt’s lymphoma and an Epstein-Barr virus-enhancing plant Euphorbia tirucalli. Lancet 1:1257–1258PubMedCrossRefGoogle Scholar
  77. Panzer-Grumayer ER, Panzer S, Wolf M, Majdic O, Haas OA, Kersey JH (1993) Characterization of CD7+CD19+ lymphoid cells after Epstein-Barr virus transformation. J Immunol 151:92–99PubMedGoogle Scholar
  78. Paterson RL, Kelleher C, Amankonah TD, Streib JE, Xu JW, Jones JF, Gelfand EW (1995) Model of Epstein-Barr virus infection of human thymocytes: expression of viral genome and impact on cellular receptor expression in the T-lymphoblastic cell line, HPB-ALL. Blood 85:456–464PubMedGoogle Scholar
  79. Pileri SA, Weisenburger DD, Sng I, Jaffe ES (2008) Peripheral T-cell lymphoma, not otherwise specified. In: Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, Thiele J (eds) WHO classification of tumours of haematopoietic and lymphoid tissues, 4th edn. WHO Press, LyonGoogle Scholar
  80. Pugh TJ, Weeraratne SD, Archer TC, Pomeranz Krummel DA, Auclair D, Bochicchio J, Carneiro MO, Carter SL, Cibulskis K, Erlich RL, Greulich H, Lawrence MS, Lennon NJ, McKenna A, Meldrim J, Ramos AH, Ross MG, Russ C, Shefler E, Sivachenko A, Sogoloff B, Stojanov P, Tamayo P, Mesirov JP, Amani V, Teider N, Sengupta S, Francois JP, Northcott PA, Taylor MD, Yu F, Crabtree GR, Kautzman AG, Gabriel SB, Getz G, Jager N, Jones DT, Lichter P, Pfister SM, Roberts TM, Meyerson M, Pomeroy SL, Cho YJ (2012) Medulloblastoma exome sequencing uncovers subtype-specific somatic mutations. Nature 488:106–110PubMedPubMedCentralCrossRefGoogle Scholar
  81. Quintanilla-Martinez L, Kumar S, Fend F, Reyes E, Teruya-Feldstein J, Kingma DW, Sorbara L, Raffeld M, Straus SE, Jaffe ES (2000) Fulminant EBV(+) T-cell lymphoproliferative disorder following acute/chronic EBV infection: a distinct clinicopathologic syndrome. Blood 96:443–451PubMedGoogle Scholar
  82. Quintanilla-Martinez L, Kimura H, Jaffe ES (2008) EBV+ T-cell lymphoma of childhood. In: Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, Thiele J (eds) WHO classification of tumours of haematopoietic and lymphoid tissues, 4th edn. WHO Press, LyonGoogle Scholar
  83. Quintanilla-Martinez L, Ko YH, Kimura H, Jaffe ES (2017) EBV–positive T-cell and NK-cell lymphoproliferative diseases of childhood. In: Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, Thiele J (eds) WHO classification of tumours of haematopoietic and lymphoid tissues, revised 4th edn. WHO Press, LyonGoogle Scholar
  84. Robbiani DF, Bothmer A, Callen E, Reina-San-Martin B, Dorsett Y, Difilippantonio S, Bolland DJ, Chen HT, Corcoran AE, Nussenzweig A, Nussenzweig MC (2008) AID is required for the chromosomal breaks in c-myc that lead to c-myc/IgH translocations. Cell 135:1028–1038PubMedPubMedCentralCrossRefGoogle Scholar
  85. Schmitz R, Young RM, Ceribelli M, Jhavar S, Xiao W, Zhang M, Wright G, Shaffer AL, Hodson DJ, Buras E, Liu X, Powell J, Yang Y, Xu W, Zhao H, Kohlhammer H, Rosenwald A, Kluin P, Muller-Hermelink HK, Ott G, Gascoyne RD, Connors JM, Rimsza LM, Campo E, Jaffe ES, Delabie J, Smeland EB, Ogwang MD, Reynolds SJ, Fisher RI, Braziel RM, Tubbs RR, Cook JR, Weisenburger DD, Chan WC, Pittaluga S, Wilson W, Waldmann TA, Rowe M, Mbulaiteye SM, Rickinson AB, Staudt LM (2012) Burkitt lymphoma pathogenesis and therapeutic targets from structural and functional genomics. Nature 490:116–120PubMedPubMedCentralCrossRefGoogle Scholar
  86. Shibata Y, Hoshino Y, Hara S, Yagasaki H, Kojima S, Nishiyama Y, Morishima T, Kimura H (2006) Clonality analysis by sequence variation of the latent membrane protein 1 gene in patients with chronic active Epstein-Barr virus infection. J Med Virol 78:770–779PubMedCrossRefGoogle Scholar
  87. Shimizu N, Tanabe-Tochikura A, Kuroiwa Y, Takada K (1994) 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 68:6069–6073PubMedPubMedCentralGoogle Scholar
  88. Shumilov A, Tsai MH, Schlosser YT, Kratz AS, Bernhardt K, Fink S, Mizani T, Lin X, Jauch A, Mautner J, Kopp-Schneider A, Feederle R, Hoffmann I, Delecluse HJ (2017) Epstein-Barr virus particles induce centrosome amplification and chromosomal instability. Nat Commun 8:14257PubMedPubMedCentralCrossRefGoogle Scholar
  89. Straus SE, Tosato G, Armstrong G, Lawley T, Preble OT, Henle W, Davey R, Pearson G, Epstein J, Brus I, Et A (1985) Persisting illness and fatigue in adults with evidence of Epstein-Barr virus infection. Ann Intern Med 102:7–16PubMedCrossRefGoogle Scholar
  90. Sugimoto KJ, Shimada A, Wakabayashi M, Imai H, Sekiguchi Y, Nakamura N, Sawada T, Ota Y, Takeuchi K, Ito Y, Kimura H, Komatsu N, Noguchi M (2014) A probable identical Epstein-Barr virus clone-positive composite lymphoma with aggressive natural killer-cell leukemia and cytotoxic T-cell lymphoma. Int J Clin Exp Pathol 7:411–417PubMedGoogle Scholar
  91. Suspene R, Aynaud MM, Koch S, Pasdeloup D, Labetoulle M, Gaertner B, Vartanian JP, Meyerhans A, Wain-Hobson S (2011) Genetic editing of herpes simplex virus 1 and Epstein-Barr herpesvirus genomes by human APOBEC3 cytidine deaminases in culture and in vivo. J Virol 85:7594–7602PubMedPubMedCentralCrossRefGoogle Scholar
  92. Swerdlow SH, Campo E, Pileri SA, Harris NL, Stein H, Siebert R, Advani R, Ghielmini M, Salles GA, Zelenetz AD, Jaffe ES (2016) The 2016 revision of the World Health Organization classification of lymphoid neoplasms. Blood 127:2375–2390PubMedPubMedCentralCrossRefGoogle Scholar
  93. Tabiasco J, Vercellone A, Meggetto F, Hudrisier D, Brousset P, Fournie JJ (2003) Acquisition of viral receptor by NK cells through immunological synapse. J Immunol 170:5993–5998PubMedCrossRefGoogle Scholar
  94. Takahashi E, Ohshima K, Kimura H, Hara K, Suzuki R, Kawa K, Eimoto T, Nakamura S (2011) Clinicopathological analysis of the age-related differences in patients with Epstein-Barr virus (EBV)-associated extranasal natural killer (NK)/T-cell lymphoma with reference to the relationship with aggressive NK cell leukaemia and chronic active EBV infection-associated lymphoproliferative disorders. Histopathology 59:660–671PubMedCrossRefGoogle Scholar
  95. Teo WL, Tan SY (2011) Loss of Epstein-Barr virus-encoded RNA expression in cutaneous dissemination of natural killer/T-cell lymphoma. J Clin Oncol 29:e342–e343PubMedCrossRefGoogle Scholar
  96. Thorley-Lawson DA, Gross A (2004) Persistence of the Epstein-Barr virus and the origins of associated lymphomas. N Engl J Med 350:1328–1337PubMedCrossRefGoogle Scholar
  97. Tsuchiyama J, Yoshino T, Mori M, Kondoh E, Oka T, Akagi T, Hiraki A, Nakayama H, Shibuya A, Ma Y, Kawabata T, Okada S, Harada M (1998) Characterization of a novel human natural killer-cell line (NK-YS) established from natural killer cell lymphoma/leukemia associated with Epstein-Barr virus infection. Blood 92:1374–1383PubMedGoogle Scholar
  98. Tsuge I, Morishima T, Morita M, Kimura H, Kuzushima K, Matsuoka H (1999) Characterization of Epstein-Barr virus (EBV)-infected natural killer (NK) cell proliferation in patients with severe mosquito allergy; establishment of an IL-2-dependent NK-like cell line. Clin Exp Immunol 115:385–392PubMedPubMedCentralCrossRefGoogle Scholar
  99. Tugizov SM, Berline JW, Palefsky JM (2003) Epstein-Barr virus infection of polarized tongue and nasopharyngeal epithelial cells. Nat Med 9:307–314PubMedCrossRefGoogle Scholar
  100. Van Prooyen N, Gold H, Andresen V, Schwartz O, Jones K, Ruscetti F, Lockett S, Gudla P, Venzon D, Franchini G (2010) Human T-cell leukemia virus type 1 p8 protein increases cellular conduits and virus transmission. Proc Natl Acad Sci U S A 107:20738–20743PubMedPubMedCentralCrossRefGoogle Scholar
  101. Weiss LM, Movahed LA, Warnke RA, Sklar J (1989) Detection of Epstein-Barr viral genomes in reed-Sternberg cells of Hodgkin’s disease. N Engl J Med 320:502–506PubMedCrossRefGoogle Scholar
  102. Xu JX, Hoshida Y, Yang WI, Inohara H, Kubo T, Kim GE, Yoon JH, Kojya S, Bandoh N, Harabuchi Y, Tsutsumi K, Koizuka I, Jia XS, Kirihata M, Tsukuma H, Aozasa K (2007) Life-style and environmental factors in the development of nasal NK/T-cell lymphoma: a case-control study in East Asia. Int J Cancer 120:406–410PubMedCrossRefGoogle Scholar
  103. Yamaguchi M, Takata K, Yoshino T, Ishizuka N, Oguchi M, Kobayashi Y, Isobe Y, Ishizawa K, Kubota N, Itoh K, Usui N, Miyazaki K, Wasada I, Nakamura S, Matsuno Y, Oshimi K, Kinoshita T, Tsukasaki K, Tobinai K (2014) Prognostic biomarkers in patients with localized natural killer/T-cell lymphoma treated with concurrent chemoradiotherapy. Cancer Sci 105:1435–1441PubMedPubMedCentralCrossRefGoogle Scholar
  104. Yoshioka M, Ishiguro N, Ishiko H, Ma X, Kikuta H, Kobayashi K (2001) Heterogeneous, restricted patterns of Epstein-Barr virus (EBV) latent gene expression in patients with chronic active EBV infection. J Gen Virol 82:2385–2392PubMedCrossRefGoogle Scholar
  105. Zhang Y, Nagata H, Ikeuchi T, Mukai H, Oyoshi MK, Demachi A, Morio T, Wakiguchi H, Kimura N, Shimizu N, Yamamoto K (2003) Common cytological and cytogenetic features of Epstein-Barr virus (EBV)-positive natural killer (NK) cells and cell lines derived from patients with nasal T/NK-cell lymphomas, chronic active EBV infection and hydroa vacciniforme-like eruptions. Br J Haematol 121:805–814PubMedCrossRefGoogle Scholar
  106. Zur Hausen H, Schulte-Holthausen H, Klein G, Henle W, Henle G, Clifford P, Santesson L (1970) EBV DNA in biopsies of Burkitt tumours and anaplastic carcinomas of the nasopharynx. Nature 228:1056–1058PubMedCrossRefGoogle Scholar

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© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  1. 1.Department of VirologyNagoya University Graduate School of MedicineNagoyaJapan

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