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Epstein-Barr virus-positive T/NK-cell lymphoproliferative disorders

  • Cai, Qingqing (Department of Medical Oncology, Sun Yat-sen University Cancer Center, State Key Laboratory of Oncology in South China, Collaborative Innovation Center of Cancer Medicine) ;
  • Chen, Kailin (Department of Medical Oncology, Sun Yat-sen University Cancer Center, State Key Laboratory of Oncology in South China, Collaborative Innovation Center of Cancer Medicine) ;
  • Young, Ken H (Department of Hematopathology, The University of Texas MD Anderson Cancer Center)
  • Received : 2014.09.30
  • Accepted : 2014.10.21
  • Published : 2015.01.31

Abstract

Epstein-Barr virus, a ubiquitous human herpesvirus, can induce both lytic and latent infections that result in a variety of human diseases, including lymphoproliferative disorders. The oncogenic potential of Epstein-Barr virus is related to its ability to infect and transform B lymphocytes into continuously proliferating lymphoblastoid cells. However, Epstein-Barr virus has also been implicated in the development of T/natural killer cell lymphoproliferative diseases. Epstein-Barr virus encodes a series of products that mimic several growth, transcription and anti-apoptotic factors, thus usurping control of pathways that regulate diverse homeostatic cellular functions and the microenvironment. However, the exact mechanism by which Epstein-Barr virus promotes oncogenesis and inflammatory lesion development remains unclear. Epstein-Barr virus-associated T/natural killer cell lymphoproliferative diseases often have overlapping clinical symptoms as well as histologic and immunophenotypic features because both lymphoid cell types derive from a common precursor. Accurate classification of Epstein-Barr virus-associated T/natural killer cell lymphoproliferative diseases is a prerequisite for appropriate clinical management. Currently, the treatment of most T/natural killer cell lymphoproliferative diseases is less than satisfactory. Novel and targeted therapies are strongly required to satisfy clinical demands. This review describes our current knowledge of the genetics, oncogenesis, biology, diagnosis and treatment of Epstein-Barr virus-associated T/natural killer cell lymphoproliferative diseases.

Keywords

References

  1. Vallejo AN, Davila E, Weyand CM, Goronzy JJ. Biology of T lymphocytes. Rheum Dis Clin North Am 2004; 30: 135-157. https://doi.org/10.1016/S0889-857X(03)00114-5
  2. Campbell KS, Hasegawa J. Natural killer cell biology: an update and future directions. J Allergy Clin Immunol 2013; 132: 536-544. https://doi.org/10.1016/j.jaci.2013.07.006
  3. Morice WG. The immunophenotypic attributes of NK cells and NK-cell lineage lymphoproliferative disorders. Am J Clin Pathol 2007; 127: 881-886. https://doi.org/10.1309/Q49CRJ030L22MHLF
  4. Lanier LL, Spits H, Phillips JH. The developmental relationship between NK cells and T cells. Immunol Today 1992; 13: 392-395. https://doi.org/10.1016/0167-5699(92)90087-N
  5. Delecluse HJ, Feederle R, O'Sullivan B, Taniere P. Epstein Barr virus-associated tumours: an update for the attention of the working pathologist. J Clin Pathol 2007; 60: 1358-1364.
  6. Rickinson AB. Co-infections, inflammation and oncogenesis: future directions for EBV research. Semin Cancer Biol 2014; 26: 99-115. https://doi.org/10.1016/j.semcancer.2014.04.004
  7. Parvaneh N, Filipovich AH, Borkhardt A. Primary immunodeficiencies predisposed to Epstein-Barr virus-driven haematological diseases. Br J Haematol 2013; 162: 573-586. https://doi.org/10.1111/bjh.12422
  8. Chang CM, Yu KJ, Mbulaiteye SM, Hildesheim A, Bhatia K. The extent of genetic diversity of Epstein-Barr virus and its geographic and disease patterns: a need for reappraisal. Virus Res 2009; 143: 209-221. https://doi.org/10.1016/j.virusres.2009.07.005
  9. Rickinson AB, Kieff E. Epstein-Barr virus. In: Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA, Roizman B, Straus SE (eds) Fields Virology, 5th edition. Lippincott Williams & Wilkins: Philadelphia, PA, USA, 2007, pp 2655-2700.
  10. Merlo A, Turrini R, Dolcetti R, Martorelli D, Muraro E, Comoli P et al. The interplay between Epstein-Barr virus and the immune system: a rationale for adoptive cell therapy of EBV-related disorders. Haematologica 2010; 95: 1769-1777. https://doi.org/10.3324/haematol.2010.023689
  11. Toczyski DP, Matera AG, Ward DC, Steitz JA. The Epstein-Barr virus (EBV) small RNA EBER1 binds and relocalizes ribosomal protein L22 in EBV-infected human B lymphocytes. Proc Natl Acad Sci USA 1994; 91: 3463-3467. https://doi.org/10.1073/pnas.91.8.3463
  12. Cesarman E. Gammaherpesviruses and lymphoproliferative disorders. Annu Rev Pathol 2014; 9: 349-372. https://doi.org/10.1146/annurev-pathol-012513-104656
  13. Petrara MR, Freguja R, Gianesin K, Zanchetta M, De Rossi A. Epstein-Barr virus-driven lymphomagenesis in the context of human immunodeficiency virus type 1 infection. Front Microbiol 2013; 4: 311.
  14. Roschewski M, Wilson WH. EBV-associated lymphomas in adults. Best Pract Res Clin Haematol 2012; 25: 75-89. https://doi.org/10.1016/j.beha.2012.01.005
  15. Young LS, Murray PG. Epstein-Barr virus and oncogenesis: from latent genes to tumours. Oncogene 2003; 22: 5108-5121. https://doi.org/10.1038/sj.onc.1206556
  16. Saha A, Robertson ES. Epstein-Barr virus-associated B-cell lymphomas: pathogenesis and clinical outcomes. Clin Cancer Res 2011; 17: 3056-3063. https://doi.org/10.1158/1078-0432.CCR-10-2578
  17. Chen J. Roles of the PI3K/Akt pathway in Epstein-Barr virus-induced cancers and therapeutic implications. World J Virol 2012; 1: 154-161. https://doi.org/10.5501/wjv.v1.i6.154
  18. Lee JW, Liu PF, Hsu LP, Chen PR, Chang CH, Shih WL. EBV LMP-1 negatively regulates expression and pro-apoptotic activity of Par-4 in nasopharyngeal carcinoma cells. Cancer Lett 2009; 279: 193-201. https://doi.org/10.1016/j.canlet.2009.01.037
  19. Vrzalikova K, Vockerodt M, Leonard S, Bell A, Wei W, Schrader A et al. Down-regulation of BLIMP1alpha by the EBV oncogene, LMP-1, disrupts the plasma cell differentiation program and prevents viral replication in B cells: implications for the pathogenesis of EBV-associated B-cell lymphomas. Blood 2011; 117: 5907-5917. https://doi.org/10.1182/blood-2010-09-307710
  20. Nourse JP, Jones K, Gandhi MK. Epstein-Barr virus-related post-transplant lymphoproliferative disorders: pathogenetic insights for targeted therapy. Am J Transplant 2011; 11: 888-895. https://doi.org/10.1111/j.1600-6143.2011.03499.x
  21. Seto E, Moosmann A, Gromminger S, Walz N, Grundhoff A, Hammerschmidt W. Micro RNAs of Epstein-Barr virus promote cell cycle progression and prevent apoptosis of primary human B cells. PLoS Pathog 2010; 6: e1001063. https://doi.org/10.1371/journal.ppat.1001063
  22. Hong GK, Kumar P, Wang L, Damania B, Gulley ML, Delecluse HJ et al. Epstein-Barr virus lytic infection is required for efficient production of the angiogenesis factor vascular endothelial growth factor in lymphoblastoid cell lines. J Virol 2005; 79: 13984-13992. https://doi.org/10.1128/JVI.79.22.13984-13992.2005
  23. Ma SD, Hegde S, Young KH, Sullivan R, Rajesh D, Zhou Y et al. A new model of Epstein-Barr virus infection reveals an important role for early lytic viral protein expression in the development of lymphomas. J Virol 2011; 85: 165-177. https://doi.org/10.1128/JVI.01512-10
  24. Burns DM, Crawford DH. Epstein-Barr virus-specific cytotoxic T-lymphocytes for adoptive immunotherapy of post-transplant lymphoproliferative disease. Blood Rev 2004; 18: 193-209. https://doi.org/10.1016/j.blre.2003.12.002
  25. Papadopoulos EB, Ladanyi M, Emanuel D, Mackinnon S, Boulad F, Carabasi MH et al. Infusions of donor leukocytes to treat Epstein-Barr virus-associated lymphoproliferative disorders after allogeneic bone marrow transplantation. N Engl J Med 1994; 330: 1185-1191. https://doi.org/10.1056/NEJM199404283301703
  26. Li J, Qian CN, Zeng YX. Regulatory T cells and EBV associated malignancies. Int Immunopharmacol 2009; 9: 590-592. https://doi.org/10.1016/j.intimp.2009.01.015
  27. Menasche G, Feldmann J, Fischer A, de Saint Basile G. Primary hemophagocytic syndromes point to a direct link between lymphocyte cytotoxicity and homeostasis. Immunol Rev 2005; 203: 165-179. https://doi.org/10.1111/j.0105-2896.2005.00224.x
  28. Karwacz K, Bricogne C, MacDonald D, Arce F, Bennett CL, Collins M et al. PD-L1 co-stimulation contributes to ligand-induced T cell receptor down-modulation on CD8+ T cells. EMBO Mol Med 2011; 3: 581-592. https://doi.org/10.1002/emmm.201100165
  29. Grivennikov SI, Greten FR, Karin M. Immunity, inflammation, and cancer. Cell 2010; 140: 883-899. https://doi.org/10.1016/j.cell.2010.01.025
  30. Balkwill FR, Mantovani A. Cancer-related inflammation: common themes and therapeutic opportunities. Semin Cancer Biol 2012; 22: 33-40. https://doi.org/10.1016/j.semcancer.2011.12.005
  31. Pittaluga S. Viral-associated lymphoid proliferations. Semin Diagn Pathol 2013; 30: 130-136. https://doi.org/10.1053/j.semdp.2012.08.009
  32. Terrin L, Dal Col J, Rampazzo E, Zancai P, Pedrotti M, Ammirabile G et al. Latent membrane protein 1 of Epstein-Barr virus activates the hTERT promoter and enhances telomerase activity in B lymphocytes. J Virol 2008; 82: 10175-10187. https://doi.org/10.1128/JVI.00321-08
  33. Terrin L, Dolcetti R, Corradini I, Indraccolo S, Dal Col J, Bertorelle R et al. hTERT inhibits the Epstein-Barr virus lytic cycle and promotes the proliferation of primary B lymphocytes: implications for EBV-driven lymphomagenesis. Int J Cancer 2007; 121: 576-587. https://doi.org/10.1002/ijc.22661
  34. Michelow P, Wright C, Pantanowitz L. A review of the cytomorphology of Epstein-Barr virus-associated malignancies. Acta Cytol 2012; 56: 1-14. https://doi.org/10.1159/000334235
  35. Gandhi MK. Epstein-Barr virus-associated lymphomas. Expert Rev Anti Infect Ther 2006; 4: 77-89. https://doi.org/10.1586/14787210.4.1.77
  36. Shah KM, Young LS. Epstein-Barr virus and carcinogenesis: beyond Burkitt's lymphoma. Clin Microbiol Infect 2009; 15: 982-988. https://doi.org/10.1111/j.1469-0691.2009.03033.x
  37. Cardenas-Mondragon MG, Carreon-Talavera R, Camorlinga-Ponce M, Gomez-Delgado A, Torres J, Fuentes-Panana EM. Epstein Barr virus and Helicobacter pylori co-infection are positively associated with severe gastritis in pediatric patients. PloS One 2013; 8: e62850. https://doi.org/10.1371/journal.pone.0062850
  38. McClain KL, Leach CT, Jenson HB, Joshi VV, Pollock BH, Parmley RT et al. Association of Epstein-Barr virus with leiomyosarcomas in children with AIDS. N Engl J Med 1995; 332: 12-18. https://doi.org/10.1056/NEJM199501053320103
  39. Gruhne B, Sompallae R, Marescotti D, Kamranvar SA, Gastaldello S, Masucci MG. The Epstein-Barr virus nuclear antigen-1 promotes genomic instability via induction of reactive oxygen species. Proc Natl Acad Sci U S A 2009; 106: 2313-2318. https://doi.org/10.1073/pnas.0810619106
  40. Gruhne B, Sompallae R, Masucci MG. Three Epstein-Barr virus latency proteins independently promote genomic instability by inducing DNA damage, inhibiting DNA repair and inactivating cell cycle checkpoints. Oncogene 2009; 28: 3997-4008. https://doi.org/10.1038/onc.2009.258
  41. Harabuchi Y, Takahara M, Kishibe K, Moriai S, Nagato T, Ishii H. Nasal natural killer (NK)/T-cell lymphoma: clinical, histological, virological, and genetic features. Int J Clin Oncol 2009; 14: 181-190. https://doi.org/10.1007/s10147-009-0882-7
  42. Hui AB, Lo KW, Teo PM, To KF, Huang DP. Genome wide detection of oncogene amplifications in nasopharyngeal carcinoma by array based comparative genomic hybridization. Int J Oncol 2002; 20: 467-473.
  43. Wong N, Hui AB, Fan B, Lo KW, Pang E, Leung SF et al. Molecular cytogenetic characterization of nasopharyngeal carcinoma cell lines and xenografts by comparative genomic hybridization and spectral karyotyping. Cancer Genet Cytogenet 2003; 140: 124-132. https://doi.org/10.1016/S0165-4608(02)00657-X
  44. Cesarman E. Gammaherpesvirus and lymphoproliferative disorders in immunocompromised patients. Cancer Lett 2011; 305: 163-174. https://doi.org/10.1016/j.canlet.2011.03.003
  45. Cesarman E, Chadburn A, Liu YF, Migliazza A, Dalla-Favera R, Knowles DM. BCL-6 gene mutations in posttransplantation lymphoproliferative disorders predict response to therapy and clinical outcome. Blood 1998; 92: 2294-2302.
  46. Wensing B, Farrell PJ. Regulation of cell growth and death by Epstein-Barr virus. Microbes Infect 2000; 2: 77-84. https://doi.org/10.1016/S1286-4579(00)00282-3
  47. Capello D, Rossi D, Gaidano G. Post-transplant lymphoproliferative disorders: molecular basis of disease histogenesis and pathogenesis. Hematol Oncol 2005; 23: 61-67. https://doi.org/10.1002/hon.751
  48. Schuster V, Ott G, Seidenspinner S, Kreth HW. Common Epstein-Barr virus (EBV) type-1 variant strains in both malignant and benign EBV-associated disorders. Blood 1996; 87: 1579-1585.
  49. Taguchi A, Miyazaki M, Sakuragi S, Shinohara K, Kamei T, Inoue Y. Gamma/delta T cell lymphoma. Intern Med 2004; 43: 120-125. https://doi.org/10.2169/internalmedicine.43.120
  50. Volanakis EJ, Boothby MR, Sherr CJ. Epigenetic regulation of the Ink4a-Arf (Cdkn2a) tumor suppressor locus in the initiation and progression of Notch1-driven T cell acute lymphoblastic leukemia. Exp Hematol 2013; 41: 377-386. https://doi.org/10.1016/j.exphem.2012.11.006
  51. Fasseu M, Aplan PD, Chopin M, Boissel N, Bories JC, Soulier J et al. p16INK4A tumor suppressor gene expression and CD3epsilon deficiency but not pre-TCR deficiency inhibit TAL1-linked T-lineage leukemogenesis. Blood 2007; 110: 2610-2619. https://doi.org/10.1182/blood-2007-01-066209
  52. Tsellou E, Troungos C, Moschovi M, Athanasiadou-Piperopoulou F, Polychronopoulou S, Kosmidis H et al. Hypermethylation of CpG islands in the promoter region of the p15INK4B gene in childhood acute leukaemia. Eur J Cancer 2005; 41: 584-589. https://doi.org/10.1016/j.ejca.2004.12.010
  53. Maruo S, Zhao B, Johannsen E, Kieff E, Zou J, Takada K. Epstein-Barr virus nuclear antigens 3C and 3A maintain lymphoblastoid cell growth by repressing p16INK4A and p14ARF expression. Proc Natl Acad Sci USA 2011; 108: 1919-1924. https://doi.org/10.1073/pnas.1019599108
  54. Skalska L, White RE, Parker GA, Sinclair AJ, Paschos K, Allday MJ. Induction of p16(INK4a) is the major barrier to proliferation when Epstein-Barr virus (EBV) transforms primary B cells into lymphoblastoid cell lines. PLoS Pathog 2013; 9: e1003187. https://doi.org/10.1371/journal.ppat.1003187
  55. Campo E, Gaulard P, Zucca E, Jaffe ES, Harris NL, Diebold J et al. Report of the European Task Force on Lymphomas: workshop on peripheral T-cell lymphomas. Ann Oncol 1998; 9: 835-843. https://doi.org/10.1023/A:1008439620513
  56. Falini B, Pileri S, De Solas I, Martelli MF, Mason DY, Delsol G et al. Peripheral T-cell lymphoma associated with hemophagocytic syndrome. Blood 1990; 75: 434-444.
  57. Vose J, Armitage J, Weisenburger D. International peripheral T-cell and natural killer/T-cell lymphoma study: pathology findings and clinical outcomes. J Clin Oncol 2008; 26: 4124-4130. https://doi.org/10.1200/JCO.2008.16.4558
  58. Gallamini A, Stelitano C, Calvi R, Bellei M, Mattei D, Vitolo U et al. Peripheral T-cell lymphoma unspecified (PTCL-U): a new prognostic model from a retrospective multicentric clinical study. Blood 2004; 103: 2474-2479. https://doi.org/10.1182/blood-2003-09-3080
  59. Quintanilla-Martinez L, Fend F, Moguel LR, Spilove L, Beaty MW, Kingma DW et al. Peripheral T-cell lymphoma with Reed-Sternberg-like cells of B-cell phenotype and genotype associated with Epstein-Barr virus infection. Am J Surg Pathol 1999; 23: 1233-1240. https://doi.org/10.1097/00000478-199910000-00008
  60. Mendonca MC, Doi SQ, Glerum S, Sellitti DF. Increase of C-type natriuretic peptide expression by serum and platelet-derived growth factor-BB in human aortic smooth muscle cells is dependent on protein kinase C activation. Endocrinology 2006; 147: 4169-4178. https://doi.org/10.1210/en.2006-0239
  61. Went P, Agostinelli C, Gallamini A, Piccaluga PP, Ascani S, Sabattini E et al. Marker expression in peripheral T-cell lymphoma: a proposed clinical-pathologic prognostic score. J Clin Oncol 2006; 24: 2472-2479. https://doi.org/10.1200/JCO.2005.03.6327
  62. Attygalle AD, Kyriakou C, Dupuis J, Grogg KL, Diss TC, Wotherspoon AC et al. Histologic evolution of angioimmunoblastic T-cell lymphoma in consecutive biopsies: clinical correlation and insights into natural history and disease progression. Am J Surg Pathol 2007; 31: 1077-1088. https://doi.org/10.1097/PAS.0b013e31802d68e9
  63. Dorfman DM, Brown JA, Shahsafaei A, Freeman GJ. Programmed death-1 (PD-1) is a marker of germinal center-associated T cells and angioimmunoblastic T-cell lymphoma. Am J Surg Pathol 2006; 30: 802-810. https://doi.org/10.1097/01.pas.0000209855.28282.ce
  64. Grogg KL, Attygalle AD, Macon WR, Remstein ED, Kurtin PJ, Dogan A. Expression of CXCL13, a chemokine highly upregulated in germinal center T-helper cells, distinguishes angioimmunoblastic T-cell lymphoma from peripheral T-cell lymphoma, unspecified. Mod Pathol 2006; 19: 1101-1107. https://doi.org/10.1038/modpathol.3800625
  65. Gisselbrecht C, Lepage E, Molina T, Quesnel B, Fillet G, Lederlin P et al. Shortened first-line high-dose chemotherapy for patients with poorprognosis aggressive lymphoma. J Clin Oncol 2002; 20: 2472-2479. https://doi.org/10.1200/JCO.2002.02.125
  66. Mounier N, Gisselbrecht C, Briere J, Haioun C, Feugier P, Offner F et al. Prognostic factors in patients with aggressive non-Hodgkin's lymphoma treated by front-line autotransplantation after complete remission: a cohort study by the Groupe d'Etude des Lymphomes de l'Adulte. J Clin Oncol 2004; 22: 2826-2834. https://doi.org/10.1200/JCO.2004.12.032
  67. Rudiger T, Weisenburger DD, Anderson JR, Armitage JO, Diebold J, MacLennan KA et al. Peripheral T-cell lymphoma (excluding anaplastic large-cell lymphoma): results from the Non-Hodgkin's Lymphoma Classification Project. Ann Oncol 2002; 13: 140-149. https://doi.org/10.1093/annonc/mdf033
  68. deLeval L, Gisselbrecht C, Gaulard P. Advances in the understanding and management of angioimmunoblastic T-cell lymphoma. Br J Haematol 2010; 148: 673-689. https://doi.org/10.1111/j.1365-2141.2009.08003.x
  69. Cho YU, Chi HS, Park CJ, Jang S, Seo EJ, Huh J. Distinct features of angioimmunoblastic T-cell lymphoma with bone marrow involvement. Am J Clin Pathol 2009; 131: 640-646. https://doi.org/10.1309/AJCPQXKCHQH4VAJ5
  70. Attygalle A, Al-Jehani R, Diss TC, Munson P, Liu H, Du MQ et al. Neoplastic T cells in angioimmunoblastic T-cell lymphoma express CD10. Blood 2002; 99: 627-633. https://doi.org/10.1182/blood.V99.2.627
  71. Patsouris E, Noel H, Lennert K. Angioimmunoblastic lymphadenopathy-type of T-cell lymphoma with a high content of epithelioid cells. Histopathology and comparison with lymphoepithelioid cell lymphoma. Am J Surg Pathol 1989; 13: 262-275.
  72. Willenbrock K, Renne C, Gaulard P, Hansmann ML. In angioimmunoblastic T-cell lymphoma, neoplastic T cells may be a minor cell population. A molecular single-cell and immunohistochemical study. Virchows Arch 2005; 446: 15-20. https://doi.org/10.1007/s00428-004-1114-1
  73. Foss FM, Zinzani PL, Vose JM, Gascoyne RD, Rosen ST, Tobinai K. Peripheral T-cell lymphoma. Blood 2011; 117: 6756-6767. https://doi.org/10.1182/blood-2010-05-231548
  74. Willenbrock K, Roers A, Seidl C, Wacker HH, Kuppers R, Hansmann ML. Analysis of T-cell subpopulations in T-cell non-Hodgkin's lymphoma of angioimmunoblastic lymphadenopathy with dysproteinemia type by single target gene amplification of T cell receptor- beta gene rearrangements. Am J Pathol 2001; 158: 1851-1857. https://doi.org/10.1016/S0002-9440(10)64141-7
  75. Karube K, Aoki R, Nomura Y, Yamamoto K, Shimizu K, Yoshida S et al. Usefulness of flow cytometry for differential diagnosis of precursor and peripheral T-cell and NK-cell lymphomas: analysis of 490 cases. Pathol Int 2008; 58: 89-97. https://doi.org/10.1111/j.1440-1827.2007.02195.x
  76. Attygalle AD, Chuang SS, Diss TC, Du MQ, Isaacson PG, Dogan A. Distinguishing angioimmunoblastic T-cell lymphoma from peripheral T-cell lymphoma, unspecified, using morphology, immunophenotype and molecular genetics. Histopathology 2007; 50: 498-508. https://doi.org/10.1111/j.1365-2559.2007.02632.x
  77. Rodriguez-Justo M, Attygalle AD, Munson P, Roncador G, Marafioti T, Piris MA. Angioimmunoblastic T-cell lymphoma with hyperplastic germinal centres: a neoplasia with origin in the outer zone of the germinal centre? Clinicopathological and immunohistochemical study of 10 cases with follicular T-cell markers. Mod Pathol 2009; 22: 753-761. https://doi.org/10.1038/modpathol.2009.12
  78. Grogg KL, Attygalle AD, Macon WR, Remstein ED, Kurtin PJ, Dogan A. Angioimmunoblastic T-cell lymphoma: a neoplasm of germinal-center T-helper cells? Blood 2005; 106: 1501-1502. https://doi.org/10.1182/blood-2005-03-1083
  79. Roncador G, Garcia Verdes-Montenegro JF, Tedoldi S, Paterson JC, Klapper W, Ballabio E et al. Expression of two markers of germinal center T cells (SAP and PD-1) in angioimmunoblastic T-cell lymphoma. Haematologica 2007; 92: 1059-1066. https://doi.org/10.3324/haematol.10864
  80. Krenacs L, Schaerli P, Kis G, Bagdi E. Phenotype of neoplastic cells in angioimmunoblastic T-cell lymphoma is consistent with activated follicular B helper T cells. Blood 2006; 108: 1110-1111. https://doi.org/10.1182/blood-2006-01-0394
  81. Marafioti T, Paterson JC, Ballabio E, Chott A, Natkunam Y, Rodriguez-Justo M et al. The inducible T-cell co-stimulator molecule is expressed on subsets of T cells and is a new marker of lymphomas of T follicular helper cell-derivation. Haematologica 2010; 95: 432-439. https://doi.org/10.3324/haematol.2009.010991
  82. Yuan CM, Vergilio JA, Zhao XF, Smith TK, Harris NL, Bagg A. CD10 and BCL6 expression in the diagnosis of angioimmunoblastic T-cell lymphoma: utility of detecting CD10+ T cells by flow cytometry. Hum Pathol 2005; 36: 784-791. https://doi.org/10.1016/j.humpath.2005.05.008
  83. Rodriguez Pinilla SM, Roncador G, Rodriguez-Peralto JL, Mollejo M, Garcia JF, Montes-Moreno S et al. Primary cutaneous CD4+ small/medium-sized pleomorphic T-cell lymphoma expresses follicular T-cell markers. Am J Surg Pathol 2009; 33: 81-90. https://doi.org/10.1097/PAS.0b013e31818e52fe
  84. Guo HQ, Huang GL, Guo CC, Pu XX, Lin TY. Diagnostic and prognostic value of circulating miR-221 for extranodal natural killer/T-cell lymphoma. Dis Markers 2010; 29: 251-258. https://doi.org/10.1155/2010/474692
  85. Oshimi K. Progress in understanding and managing natural killer-cell malignancies. Br J Haematol 2007; 139: 532-544. https://doi.org/10.1111/j.1365-2141.2007.06835.x
  86. Harabuchi Y, Imai S, Wakashima J, Hirao M, Kataura A, Osato T et al. Nasal T-cell lymphoma causally associated with Epstein-Barr virus: clinicopathologic, phenotypic, and genotypic studies. Cancer 1996; 77: 2137-2149. https://doi.org/10.1002/(SICI)1097-0142(19960515)77:10<2137::AID-CNCR27>3.0.CO;2-V
  87. Hirakawa S, Kuyama M, Takahashi S, Yamasaki O, Kanzaki H, Teshima T et al. Nasal and nasal-type natural killer/T-cell lymphoma. J Am Acad Dermatol 1999; 40: 268-272. https://doi.org/10.1016/S0190-9622(99)70204-5
  88. Harabuchi Y, Yamanaka N, Kataura A, Imai S, Kinoshita T, Mizuno F et al. Epstein-Barr virus in nasal T-cell lymphomas in patients with lethal midline granuloma. Lancet 1990; 335: 128-130. https://doi.org/10.1016/0140-6736(90)90002-M
  89. Takahashi N, Miura I, Chubachi A, Miura AB, Nakamura S. A clinicopathological study of 20 patients with T/natural killer (NK)-cell lymphoma-associated hemophagocytic syndrome with special reference to nasal and nasal-type NK/T-cell lymphoma. Int J Hematol 2001; 74: 303-308. https://doi.org/10.1007/BF02982065
  90. Liang R. Diagnosis and management of primary nasal lymphoma of T-cell or NK-cell origin. Clin Lymphoma 2000; 1: 33-37; discussion 38. https://doi.org/10.3816/CLM.2000.n.002
  91. Harris NL, Jaffe ES, Stein H, Banks PM, Chan JK, Cleary ML et al. A revised European-American classification of lymphoid neoplasms: a proposal from the International Lymphoma Study Group. Blood 1994; 84: 1361-1392.
  92. Mori N, Yatabe Y, Oka K, Kinoshita T, Kobayashi T, Ono T et al. Expression of perforin in nasal lymphoma. Additional evidence of its natural killer cell derivation. Am J Pathol 1996; 149: 699-705.
  93. Suzumiya J, Takeshita M, Kimura N, Kikuchi M, Uchida T, Hisano S et al. Expression of adult and fetal natural killer cell markers in sinonasal lymphomas. Blood 1994; 83: 2255-2260.
  94. Li CC, Tien HF, Tang JL, Yao M, Chen YC, Su IJ et al. Treatment outcome and pattern of failure in 77 patients with sinonasal natural killer/T-cell or T-cell lymphoma. Cancer 2004; 100: 366-375. https://doi.org/10.1002/cncr.11908
  95. Emile JF, Boulland ML, Haioun C, Kanavaros P, Petrella T, Delfau-Larue MH et al. CD5-CD56+ T-cell receptor silent peripheral T-cell lymphomas are natural killer cell lymphomas. Blood 1996; 87: 1466-1473.
  96. Suzuki R, Suzumiya J, Nakamura S, Aoki S, Notoya A, Ozaki S et al. Aggressive natural killer-cell leukemia revisited: large granular lymphocyte leukemia of cytotoxic NK cells. Leukemia 2004; 18: 763-770. https://doi.org/10.1038/sj.leu.2403262
  97. Ishida F, Ko YH, Kim WS, Suzumiya J, Isobe Y, Oshimi K et al. Aggressive natural killer cell leukemia: therapeutic potential of L-asparaginase and allogeneic hematopoietic stem cell transplantation. Cancer Sci 2012; 103: 1079-1083. https://doi.org/10.1111/j.1349-7006.2012.02251.x
  98. Ryder J, Wang X, Bao L, Gross SA, Hua F, Irons RD. Aggressive natural killer cell leukemia: report of a Chinese series and review of the literature. Int J Hematol 2007; 85: 18-25. https://doi.org/10.1532/IJH97.A10612
  99. Caligiuri MA. Human natural killer cells. Blood 2008; 112: 461-469. https://doi.org/10.1182/blood-2007-09-077438
  100. Lima M. Aggressive mature natural killer cell neoplasms: from epidemiology to diagnosis. Orphanet J Rare Dis 2013; 8: 95. https://doi.org/10.1186/1750-1172-8-95
  101. Kimura H, Ito Y, Kawabe S, Gotoh K, Takahashi Y, Kojima S et al. EBV-associated T/NK-cell lymphoproliferative diseases in nonimmunocompromised hosts: prospective analysis of 108 cases. Blood 2012; 119: 673-686. https://doi.org/10.1182/blood-2011-10-381921
  102. Kasahara Y, Yachie A, Takei K, Kanegane C, Okada K, Ohta K et al. Differential cellular targets of Epstein-Barr virus (EBV) infection between acute EBV-associated hemophagocytic lymphohistiocytosis and chronic active EBV infection. Blood 2001; 98: 1882-1888. https://doi.org/10.1182/blood.V98.6.1882
  103. Fox CP, Shannon-Lowe C, Gothard P, Kishore B, Neilson J, O'Connor N et al. Epstein-Barr virus-associated hemophagocytic lymphohistiocytosis in adults characterized by high viral genome load within circulating natural killer cells. Clin Infect Dis 2010; 51: 66-69. https://doi.org/10.1086/653424
  104. Su IJ, Lin DT, Hsieh HC, Lee SH, Chen J, Chen RL et al. Fatal primary Epstein-Barr virus infection masquerading as histiocytic medullary reticulosis in young children in Taiwan. Hematol Pathol 1990; 4: 189-195.
  105. Chen RL, Su IJ, Lin KH, Lee SH, Lin DT, Chuu WM et al. Fulminant childhood hemophagocytic syndrome mimicking histiocytic medullary reticulosis. An atypical form of Epstein-Barr virus infection. Am J Clin Pathol 1991; 96: 171-176. https://doi.org/10.1093/ajcp/96.2.171
  106. Suzuki K, Ohshima K, Karube K, Suzumiya J, Ohga S, Ishihara S et al. Clinicopathological states of Epstein-Barr virus-associated T/NK-cell lymphoproliferative disorders (severe chronic active EBV infection) of children and young adults. Int J Oncol 2004; 24: 1165-1174.
  107. Su IJ, Chen RL, Lin DT, Lin KS, Chen CC. Epstein-Barr virus (EBV) infects T lymphocytes in childhood EBV-associated hemophagocytic syndrome in Taiwan. Am J Pathol 1994; 144: 1219-1225.
  108. Quintanilla-Martinez L, Ridaura C, Nagl F, Saez-de-Ocariz M, Duran-McKinster C, Ruiz-Maldonado R et al. Hydroa vacciniforme-like lymphoma: a chronic EBV+ lymphoproliferative disorder with risk to develop a systemic lymphoma. Blood 2013; 122: 3101-3110. https://doi.org/10.1182/blood-2013-05-502203
  109. Iwatsuki K, Xu Z, Takata M, Iguchi M, Ohtsuka M, Akiba H et al. The association of latent Epstein-Barr virus infection with hydroa vacciniforme. Br J Dermatol 1999; 140: 715-721. https://doi.org/10.1046/j.1365-2133.1999.02777.x
  110. Cho KH, Lee SH, Kim CW, Jeon YK, Kwon IH, Cho YJ et al. Epstein-Barr virus-associated lymphoproliferative lesions presenting as a hydroa vacciniforme-like eruption: an analysis of six cases. Br J Dermatol 2004; 151: 372-380. https://doi.org/10.1111/j.1365-2133.2004.06038.x
  111. Kimura H, Hoshino Y, Kanegane H, Tsuge I, Okamura T, Kawa K et al. Clinical and virologic characteristics of chronic active Epstein-Barr virus infection. Blood 2001; 98: 280-286. https://doi.org/10.1182/blood.V98.2.280
  112. Cohen JI, Kimura H, Nakamura S, Ko YH, Jaffe ES. 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 2009; 20: 1472-1482. https://doi.org/10.1093/annonc/mdp064
  113. Ishihara S, Yabuta R, Tokura Y, Ohshima K, Tagawa S. Hypersensitivity to mosquito bites is not an allergic disease, but an Epstein-Barr virus-associated lymphoproliferative disease. Int J Hematol 2000; 72: 223-228.
  114. Tokura Y, Ishihara S, Tagawa S, Seo N, Ohshima K, Takigawa M. Hypersensitivity to mosquito bites as the primary clinical manifestation of a juvenile type of Epstein-Barr virus-associated natural killer cell leukemia/lymphoma. J Am Acad Dermatol 2001; 45: 569-578. https://doi.org/10.1067/mjd.2001.114751
  115. Kawa K, Okamura T, Yagi K, Takeuchi M, Nakayama M, Inoue M. Mosquito allergy and Epstein-Barr virus-associated T/natural killer-cell lymphoproliferative disease. Blood 2001; 98: 3173-3174. https://doi.org/10.1182/blood.V98.10.3173
  116. Henter JI, Horne A, Arico M, Egeler RM, Filipovich AH, Imashuku S et al. HLH-2004: Diagnostic and therapeutic guidelines for hemophagocytic lymphohistiocytosis. Pediatr Blood Cancer 2007; 48: 124-131. https://doi.org/10.1002/pbc.21039
  117. Ahn JS, Rew SY, Shin MG, Kim HR, Yang DH, Cho D et al. Clinical significance of clonality and Epstein-Barr virus infection in adult patients with hemophagocytic lymphohistiocytosis. Am J Hematol 2010; 85: 719-722. https://doi.org/10.1002/ajh.21795
  118. Lau LG, Tan LK, Salto-Tellez M, Koay ES, Liu TC. T-cell post-transplant lymphoproliferative disorder after hematopoietic stem cell transplantation: another case and a review of the literature. Bone Marrow Transplant 2004; 34: 821-822. https://doi.org/10.1038/sj.bmt.1704677
  119. Tiede C, Maecker-Kolhoff B, Klein C, Kreipe H, Hussein K. Risk factors and prognosis in T-cell posttransplantation lymphoproliferative diseases: reevaluation of 163 cases. Transplantation 2013; 95: 479-488. https://doi.org/10.1097/TP.0b013e3182762e07
  120. Green M, Michaels MG. Epstein-Barr virus infection and posttransplant lymphoproliferative disorder. Am J Transplant. 2013; 13 (Suppl 3): 41-54; quiz 54. https://doi.org/10.1111/ajt.12004
  121. Kawa K. Diagnosis and treatment of Epstein-Barr virus-associated natural killer cell lymphoproliferative disease. Int J Hematol 2003; 78: 24-31. https://doi.org/10.1007/BF02983236
  122. Bollard CM, Rooney CM, Heslop HE. T-cell therapy in the treatment of post-transplant lymphoproliferative disease. Nat Rev Clin Oncol 2012; 9: 510-519. https://doi.org/10.1038/nrclinonc.2012.111
  123. Hatton O, Martinez OM, Esquivel CO. Emerging therapeutic strategies for Epstein-Barr virus+ post-transplant lymphoproliferative disorder. Pediatr Transplant 2012; 16: 220-229. https://doi.org/10.1111/j.1399-3046.2012.01656.x

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