Pathobiology of Epstein-Barr virus-driven peripheral T-cell lymphomas

Seminars in Diagnostic Pathology

Volumn 28, Issue 3, 2011, Pages 234-244

  Piccaluga, Pier Paolo ^a   Gazzola, Anna ^a   Agostinelli, Claudio ^a   Bacci, Francesco ^a   Sabattini, Elena ^a   Pileri, Stefano A ^a  

^a UNIVERSITY OF BOLOGNA   (Italy)

Author keywords

EBV; Natural killer; Peripheral T cell lymphomas; T NK lymphoproliferative disorder

Indexed keywords

AGGRESSIVE NK CELL LEUKEMIA; ARTICLE; CANCER RADIOTHERAPY; EPSTEIN BARR VIRUS; HISTOPATHOLOGY; HUMAN; HYDROA VACCINIFORME LIKE LYMPHOMA; IMMUNOPHENOTYPING; LYMPHOCYTE TRANSFORMATION; LYMPHOPROLIFERATIVE DISEASE; MALIGNANT TRANSFORMATION; NATURAL KILLER CELL; NK T CELL LYMPHOMA; PERIPHERAL T CELL LYMPHOMA; PREVALENCE; PRIORITY JOURNAL; PROGNOSIS; T LYMPHOCYTE; VIRUS CARCINOGENESIS;

CELL TRANSFORMATION, NEOPLASTIC; EPSTEIN-BARR VIRUS INFECTIONS; HUMANS; LYMPHOMA, EXTRANODAL NK-T-CELL; LYMPHOMA, T-CELL, PERIPHERAL;

EID: 79960112753     PISSN: 07402570     EISSN: 19301111     Source Type: Journal    
DOI: 10.1053/j.semdp.2011.02.007     Document Type: Article

References (117)

1. Pagano J.S., Blaser M., Buendia M.A., et al. Infectious agents and cancer: criteria for a causal relation. Semin Cancer Biol 2004, 14:453-471.
2. De Falco G., Antonicelli G., Onnis A., et al. Role of EBV in microRNA dysregulation in Burkitt lymphoma. Semin Cancer Biol 2009, 19:401-406.
3. Leucci E., Onnis A., Cocco M., et al. B-cell differentiation in EBV-positive Burkitt lymphoma is impaired at posttranscriptional level by miRNA-altered expression. Int J Cancer 2011, 126:1316-1326.
4. Piccaluga P.P., De Falco G., Kustagi M., et al. Gene expression analysis uncovers similarity and differences among Burkitt lymphoma subtypes. Blood 18 January 2011, Epub ahead of print.
5. Tabanelli V., Agostinelli C., Sabattini E., et al. Systemic EBV+ T-cell lymphoproliferative disease of childhood in Western countries. A case report and review of literature. J Med Case Rep 2011, in press.
6. Pope J.H., Scott W., Moss D.J. Human lymphoid cell transformation by Epstein-Barr virus. Nat New Biol 1973, 246:140-141.
7. 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, 80:389-399.
8. Miller W.E., Cheshire J.L., Raab-Traub N. Interaction of tumor necrosis factor receptor-associated factor signaling proteins with the latent membrane protein 1 PXQXT motif is essential for induction of epidermal growth factor receptor expression. Mol Cell Biol 1998, 18:2835-2844.
9. Miller C.L., Lee J.H., Kieff E., et al. An integral membrane protein (LMP2) blocks reactivation of Epstein-Barr virus from latency following surface immunoglobulin crosslinking. Proc Natl Acad Sci U S A 1994, 91:772-776.
10. Quintanilla-Martinez L., Kimura H., Jaffe E.S. E.B.V-positive T-cell lymphoproliferative disorders of childhood. WHO Classification of Tumours of Haematopoietic and Lymphoid Tissues 2008, 278-280. IARC, Lyon. S. Swerdlow (Ed.).
11. Straus S.E. The chronic mononucleosis syndrome. J Infect Dis 1988, 157:405-412.
12. Kimura H., Hoshino Y., Kanegane H., et al. Clinical and virologic characteristics of chronic active Epstein-Barr virus infection. Blood 2001, 98:280-286.
13. Kimura H., Morishima T., Kanegane H., et al. Prognostic factors for chronic active Epstein-Barr virus infection. J Infect Dis 2003, 187:527-533.
14. Suzuki K., Ohshima K., Karube K., 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.
15. Quintanilla-Martinez L., Kumar S., Fend F., et al. Fulminant EBV(+) T-cell lymphoproliferative disorder following acute/chronic EBV infection: a distinct clinicopathologic syndrome. Blood 2000, 96:443-451.
16. Chuang H.C., Lay J.D., Hsieh W.C., et al. Pathogenesis and mechanism of disease progression from hemophagocytic lymphohistiocytosis to Epstein-Barr virus-associated T-cell lymphoma: nuclear factor-kappa B pathway as a potential therapeutic target. Cancer Sci 2007, 98:1281-1287.
17. Chan J.K.C., Jaffe E.S., Ralfkiaer E. Aggressive NK-cell leukaemia. WHO Classification of Tumors of Hematopoietic and Lymphoid Tissues 2008, 276-277. IARC, Lyon. (ed 4). S. Swerdlow (Ed.).
18. Ruskova A., Thula R., Chan G. Aggressive natural killer-cell leukemia: report of five cases and review of the literature. Leuk Lymphoma 2004, 45:2427-2438.
19. Song S.Y., Kim W.S., Ko Y.H., et al. Aggressive natural killer cell leukemia: clinical features and treatment outcome. Haematologica 2002, 87:1343-1345.
20. Suzuki R., Suzumiya J., Nakamura S., et al. Aggressive natural killer-cell leukemia revisited: large granular lymphocyte leukemia of cytotoxic NK cells. Leukemia 2004, 18:763-770.
21. Imamura N., Kusunoki Y., Kawa-Ha K., et al. Aggressive natural killer cell leukaemia/lymphoma: report of four cases and review of the literature. Possible existence of a new clinical entity originating from the third lineage of lymphoid cells. Br J Hæmatol 1990, 75:49-59.
22. Kwong Y.L., Wong K.F., Chan L.C., et al. Large granular lymphocyte leukemia. A study of nine cases in a Chinese population. Am J Clin Pathol 1995, 103:76-81.
23. Oshimi K. Lymphoproliferative disorders of natural killer cells. Int J Hematol 1996, 63:279-290.
24. Chan J.K., Sin V.C., Wong K.F., et al. Nonnasal lymphoma expressing the natural killer cell marker CD56: a clinicopathologic study of 49 cases of an uncommon aggressive neoplasm. Blood 1997, 89:4501-4513.
25. Kwong Y.L., Chan A.C., Liang R., et al. CD56+ NK lymphomas: clinicopathological features and prognosis. Br J Haematol 1997, 97:821-829.
26. Chan J.K. Natural killer cell neoplasms. Anat Pathol 1998, 3:77-145.
27. Ryder J., Wang X., Bao L., et al. Aggressive natural killer cell leukemia: report of a Chinese series and review of the literature. Int J Hematol 2007, 85:18-25.
28. Ishihara S., Okada S., Wakiguchi H., et al. Clonal lymphoproliferation following chronic active Epstein-Barr virus infection and hypersensitivity to mosquito bites. Am J Hematol 1997, 54:276-281.
29. Ishihara S., Ohshima K., Tokura Y., et al. Hypersensitivity to mosquito bites conceals clonal lymphoproliferation of Epstein-Barr viral DNA-positive natural killer cells. Jpn J Cancer Res 1997, 88:82-87.
30. Hasserjian R.P., Harris N.L. NK-cell lymphomas and leukemias: a spectrum of tumors with variable manifestations and immunophenotype. Am J Clin Pathol 2007, 127:860-868.
31. Ohno Y., Amakawa R., Fukuhara S., et al. Acute transformation of chronic large granular lymphocyte leukemia associated with additional chromosome abnormality. Cancer 1989, 64:63-67.
32. Oshimi K., Yamada O., Kaneko T., et al. Laboratory findings and clinical courses of 33 patients with granular lymphocyte-proliferative disorders. Leukemia 1993, 7:782-788.
33. Soler J., Bordes R., Ortuno F., et al. Aggressive natural killer cell leukaemia/lymphoma in two patients with lethal midline granuloma. Br J Hæmatol 1994, 86:659-662.
34. Nava V.E., Jaffe E.S. The pathology of NK-cell lymphomas and leukemias. Adv Anat Pathol 2005, 12:27-34.
35. Okuda T., Sakamoto S., Deguchi T., et al. Hemophagocytic syndrome associated with aggressive natural killer cell leukemia. Am J Hematol 1991, 38:321-323.
36. Mori N., Yamashita Y., Tsuzuki T., et al. Lymphomatous features of aggressive NK cell leukaemia/lymphoma with massive necrosis, haemophagocytosis and EB virus infection. Histopathology 2000, 37:363-371.
37. Kato K., Ohshima K., Ishihara S., et al. Elevated serum soluble Fas ligand in natural killer cell proliferative disorders. Br J Hæmatol 1998, 103:1164-1166.
38. Makishima H., Ito T., Momose K., et al. Chemokine system and tissue infiltration in aggressive NK-cell leukemia. Leuk Res 2007, 31:1237-1245.
39. Tanaka M., Suda T., Haze K., et al. Fas ligand in human serum. Nat Med 1996, 2:317-322.
40. Nakashima Y., Tagawa H., Suzuki R., et al. Genome-wide array-based comparative genomic hybridization of natural killer cell lymphoma/leukemia: different genomic alteration patterns of aggressive NK-cell leukemia and extranodal Nk/T-cell lymphoma, nasal type. Genes Chromosomes Cancer 2005, 44:247-255.
41. Kawa-Ha K., Ishihara S., Ninomiya T., et al. CD3-negative lymphoproliferative disease of granular lymphocytes containing Epstein-Barr viral DNA. J Clin Invest 1989, 84:51-55.
42. Hart D.N., Baker B.W., Inglis M.J., et al. Epstein-Barr viral DNA in acute large granular lymphocyte (natural killer) leukemic cells. Blood 1992, 79:2116-2123.
43. Su I.J., Chen R.L., Lin D.T., et al. Epstein-Barr virus (EBV) infects T lymphocytes in childhood EBV-associated hemophagocytic syndrome in Taiwan. Am J Pathol 1994, 144:1219-1225.
44. Kikuta H., Sakiyama Y., Matsumoto S., et al. Fatal Epstein-Barr virus-associated hemophagocytic syndrome. Blood 1993, 82:3259-3264.
45. Okano M., Matsumoto S., Osato T., et al. Severe chronic active Epstein-Barr virus infection syndrome. Clin Microbiol Rev 1991, 4:129-135.
46. Kasahara Y., Yachie A., Takei 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.
47. Jones J.F., Shurin S., Abramowsky C., et al. T-cell lymphomas containing Epstein-Barr viral DNA in patients with chronic Epstein-Barr virus infections. N Engl J Med 1988, 318:733-741.
48. Kanegane H., Bhatia K., Gutierrez M., et al. A syndrome of peripheral blood T-cell infection with Epstein-Barr virus (EBV) followed by EBV-positive T-cell lymphoma. Blood 1998, 91:2085-2091.
49. Went P., Agostinelli C., Gallamini A., et al. Marker expression in peripheral T-cell lymphoma: a proposed clinical-pathologic prognostic score. J Clin Oncol 2006, 24:2472-2479.
50. Chen J.S., Tzeng C.C., Tsao C.J., et al. Clonal karyotype abnormalities in EBV-associated hemophagocytic syndrome. Haematologica 1997, 82:572-576.
51. Barrionuevo C., Anderson V.M., Zevallos-Giampietri E., et al. Hydroa-like cutaneous T-cell lymphoma: a clinicopathologic and molecular genetic study of 16 pediatric cases from Peru. Appl Immunohistochem Mol Morphol 2002, 10:7-14.
52. Cho K.H., Kim C.W., Heo D.S., et al. Epstein-Barr virus-associated peripheral T-cell lymphoma in adults with hydroa vacciniforme-like lesions. Clin Exp Dermatol 2001, 26:242-247.
53. Doeden K., Molina-Kirsch H., Perez E., et al. Hydroa-like lymphoma with CD56 expression. J Cutan Pathol 2008, 35:488-494.
54. Iwatsuki K., Xu Z., Ohtsuka M., et al. Cutaneous lymphoproliferative disorders associated with Epstein-Barr virus infection: a clinical overview. J Dermatol Sci 2000, 22:181-195.
55. Chen H.H., Hsiao C.H., Chiu H.C. Hydroa vacciniforme-like primary cutaneous CD8-positive T-cell lymphoma. Br J Dermatol 2002, 147:587-591.
56. Wu Y.H., Chen H.C., Hsiao P.F., et al. Hydroa vacciniforme-like Epstein-Barr virus-associated monoclonal T-lymphoproliferative disorder in a child. Int J Dermatol 2007, 46:1081-1086.
57. Nitta Y., Iwatsuki K., Kimura H., et al. Fatal natural killer cell lymphoma arising in a patient with a crop of Epstein-Barr virus-associated disorders. Eur J Dermatol 2005, 15:503-506.
58. Chan J.K.C., Quintanilla-Martinez L., Ferry J.A., et al. Extranodal NK/T-cell lymphoma nasal type. WHO Classification of Tumours of Haematopoietic and Lymphoid Tissues 2008, 285-288. IARC, Lyon. S. Swerdlow (Ed.).
59. Classification of malignant lymphomas in Japan: incidence of recently recognized entities. Lymphoma Study Group of Japanese Pathologists. Pathol Int 2000, 50:696-702. The World Health Organization.
60. Au W.Y., Ma S.Y., Chim C.S., et al. Clinicopathologic features and treatment outcome of mature T-cell and natural killer-cell lymphomas diagnosed according to the World Health Organization classification scheme: a single center experience of 10 years. Ann Oncol 2005, 16:206-214.
61. Quintanilla-Martinez L., Franklin J.L., Guerrero I., et al. Histological and immunophenotypic profile of nasal NK/T cell lymphomas from Peru: high prevalence of p53 overexpression. Hum Pathol 1999, 30:849-855.
62. Arber D.A., Weiss L.M., Albujar P.F., et al. Nasal lymphomas in Peru. High incidence of T-cell immunophenotype and Epstein-Barr virus infection. Am J Surg Pathol 1993, 17:392-399.
63. Chan J.K., Yip T.T., Tsang W.Y., et al. Detection of Epstein-Barr viral RNA in malignant lymphomas of the upper aerodigestive tract. Am J Surg Pathol 1994, 18:938-946.
64. Elenitoba-Johnson K.S., Zarate-Osorno A., Meneses A., et al. 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 1998, 11:754-761.
65. Kanavaros P., Lescs M.C., Briere J., et al. Nasal T-cell lymphoma: a clinicopathologic entity associated with peculiar phenotype and with Epstein-Barr virus. Blood 1993, 81:2688-2695.
66. Quintanilla-Martinez L., Fend F., Moguel L.R., 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.
67. van Gorp J., Weiping L., Jacobse K., et al. Epstein-Barr virus in nasal T-cell lymphomas (polymorphic reticulosis/midline malignant reticulosis) in western China. J Pathol 1994, 173:81-87.
68. Hummel M., Bentink S., Berger H., et al. A biologic definition of Burkitt's lymphoma from transcriptional and genomic profiling. N Engl J Med 2006, 354:2419-2430.
69. Medeiros L.J., Peiper S.C., Elwood L., et al. Angiocentric immunoproliferative lesions: a molecular analysis of eight cases. Hum Pathol 1991, 22:1150-1157.
70. Suzumiya J., Ohshima K., Takeshita M., et al. Nasal lymphomas in Japan: a high prevalence of Epstein-Barr virus type A and deletion within the latent membrane protein gene. Leuk Lymphoma 1999, 35:567-578.
71. Chiang A.K., Wong K.Y., Liang A.C., et al. Comparative analysis of Epstein-Barr virus gene polymorphisms in nasal T/NK-cell lymphomas and normal nasal tissues: implications on virus strain selection in malignancy. Int J Cancer 1999, 80:356-364.
72. Dirnhofer S., Angeles-Angeles A., Ortiz-Hidalgo C., et al. High prevalence of a 30-base pair deletion in the Epstein-Barr virus (EBV) latent membrane protein 1 gene and of strain type B EBV in Mexican classical Hodgkin's disease and reactive lymphoid tissue. Hum Pathol 1999, 30:781-787.
73. Kuo T.T., Shih L.Y., Tsang N.M., et al. NK/T cell lymphoma in Taiwan: a clinicopathologic study of 22 cases, with analysis of histologic subtypes, Epstein-Barr virus LMP-1 gene association, and treatment modalities. Int J Surg Pathol 2004, 12:375-387.
74. Tai Y.C., Kim L.H., Peh S.C. High frequency of EBV association and 30-bp deletion in the LMP-1 gene in CD56 lymphomas of the upper aerodigestive tract. Pathol Int 2004, 54:158-166.
75. Hoshida Y., Li T., Dong Z., et al. Lymphoproliferative disorders in renal transplant patients in Japan. Int J Cancer 2001, 91:869-875.
76. Kwong Y.L., Lam C.C., Chan T.M. Post-transplantation lymphoproliferative disease of natural killer cell lineage: a clinicopathological and molecular analysis. Br J Hæmatol 2000, 110:197-202.
77. Kern W.F., Spier C.M., Hanneman E.H., et al. Neural cell adhesion molecule-positive peripheral T-cell lymphoma: a rare variant with a propensity for unusual sites of involvement. Blood 1992, 79:2432-2437.
78. Petrella T., Delfau-Larue M.H., Caillot D., et al. Nasopharyngeal lymphomas: further evidence for a natural killer cell origin. Hum Pathol 1996, 27:827-833.
79. Tomita Y., Ohsawa M., Qiu K., et al. Epstein-Barr virus in lymphoproliferative diseases in the sino-nasal region: close association with CD56+ immunophenotype and polymorphic-reticulosis morphology. Int J Cancer 1997, 70:9-13.
80. Chim C.S., Ma E.S., Loong F., et al. Diagnostic cues for natural killer cell lymphoma: primary nodal presentation and the role of in situ hybridisation for Epstein-Barr virus encoded early small RNA in detecting occult bone marrow involvement. J Clin Pathol 2005, 58:443-445.
81. Kagami Y., Suzuki R., Taji H., et al. Nodal cytotoxic lymphoma spectrum: a clinicopathologic study of 66 patients. Am J Surg Pathol 1999, 23:1184-1200.
82. Saffer H., Wahed A., Rassidakis G.Z., et al. Clusterin expression in malignant lymphomas: a survey of 266 cases. Mod Pathol 2002, 15:1221-1226.
83. Wong K.F., Chan J.K., Cheung M.M., et al. Bone marrow involvement by nasal NK cell lymphoma at diagnosis is uncommon. Am J Clin Pathol 2001, 115:266-270.
84. Cheung M.M., Chan J.K., Lau W.H., et al. Primary non-Hodgkin's lymphoma of the nose and nasopharynx: clinical features, tumor immunophenotype, and treatment outcome in 113 patients. J Clin Oncol 1998, 16:70-77.
85. Wong K.F., Chan J.K., Ng C.S., et al. CD56 (NKH1)-positive hematolymphoid malignancies: an aggressive neoplasm featuring frequent cutaneous/mucosal involvement, cytoplasmic azurophilic granules, and angiocentricity. Hum Pathol 1992, 23:798-804.
86. Teruya-Feldstein J., Jaffe E.S., Burd P.R., et al. The role of Mig, the monokine induced by interferon-gamma, and IP-10, the interferon-gamma-inducible protein-10, in tissue necrosis and vascular damage associated with Epstein-Barr virus-positive lymphoproliferative disease. Blood 1997, 90:4099-4105.
87. Chan J.K., Tsang W.Y., Ng C.S. Clarification of CD3 immunoreactivity in nasal T/natural killer cell lymphomas: the neoplastic cells are often CD3 epsilon+. Blood 1996, 87:839-841.
88. Jaffe E.S. Nasal and nasal-type T/NK cell lymphoma: a unique form of lymphoma associated with the Epstein-Barr virus. Histopathology 1995, 27:581-583.
89. Jaffe E.S., Chan J.K., Su I.J., et al. Report of the Workshop on Nasal and Related Extranodal Angiocentric T/Natural Killer cell Lymphomas. Definitions, differential diagnosis, and epidemiology. Am J Surg Pathol 1996, 20:103-111.
90. Tsang W.Y., Chan J.K., Ng C.S., et al. Utility of a paraffin section-reactive CD56 antibody (123C3) for characterization and diagnosis of lymphomas. Am J Surg Pathol 1996, 20:202-210.
91. Ng C.S., Lo S.T., Chan J.K., et al. CD56+ putative natural killer cell lymphomas: production of cytolytic effectors and related proteins mediating tumor cell apoptosis?. Hum Pathol 1997, 28:1276-1282.
92. Ohshima K., Suzumiya J., Shimazaki K., et al. Nasal T/NK cell lymphomas commonly express perforin and Fas ligand: important mediators of tissue damage. Histopathology 1997, 31:444-450.
93. Ng S.B., Lai K.W., Murugaya S., et al. Nasal-type extranodal natural killer/T-cell lymphomas: a clinicopathologic and genotypic study of 42 cases in Singapore. Mod Pathol 2004, 17:1097-1107.
94. Ko Y.H., Ree H.J., Kim W.S., et al. Clinicopathologic and genotypic study of extranodal nasal-type natural killer/T-cell lymphoma and natural killer precursor lymphoma among Koreans. Cancer 2000, 89:2106-2116.
95. Siu L.L., Chan V., Chan J.K., et al. Consistent patterns of allelic loss in natural killer cell lymphoma. Am J Pathol 2000, 157:1803-1809.
96. Siu L.L., Wong K.F., Chan J.K., et al. Comparative genomic hybridization analysis of natural killer cell lymphoma/leukemia. Recognition of consistent patterns of genetic alterations. Am J Pathol 1999, 155:1419-1425.
97. Tien H.F., Su I.J., Tang J.L., et al. Clonal chromosomal abnormalities as direct evidence for clonality in nasal T/natural killer cell lymphomas. Br J Hæmatol 1997, 97:621-625.
98. Wong K.F., Zhang Y.M., Chan J.K. Cytogenetic abnormalities in natural killer cell lymphoma/leukaemia-is there a consistent pattern?. Leuk Lymphoma 1999, 34:241-250.
99. Siu L.L., Chan J.K., Wong K.F., et al. Specific patterns of gene methylation in natural killer cell lymphomas: p73 is consistently involved. Am J Pathol 2002, 160:59-66.
100. Hongyo T., Hoshida Y., Nakatsuka S., et al. p53, K-ras, c-kit and beta-catenin gene mutations in sinonasal NK/T-cell lymphoma in Korea and Japan. Oncol Rep 2005, 13:265-271.
101. Quintanilla-Martinez L., Kremer M., Keller G., et al. p53 mutations in nasal natural killer/T-cell lymphoma from Mexico: association with large cell morphology and advanced disease. Am J Pathol 2001, 159:2095-2105.
102. Shen L., Liang A.C., Lu L., et al. Frequent deletion of Fas gene sequences encoding death and transmembrane domains in nasal natural killer/T-cell lymphoma. Am J Pathol 2002, 161:2123-2131.
103. Huang Y., de Reynies A., de Leval L., et al. Gene expression profiling identifies emerging oncogenic pathways operating in extranodal NK/T-cell lymphoma, nasal type. Blood 2010, 115:1226-1237.
104. Piccaluga P.P., Agostinelli C., Zinzani P.L., et al. Expression of platelet-derived growth factor receptor alpha in peripheral T-cell lymphoma not otherwise specified. Lancet Oncol 2005, 6:440.
105. Piccaluga P.P., Agostinelli C., Califano A., et al. Gene expression analysis of peripheral T cell lymphoma, unspecified, reveals distinct profiles and new potential therapeutic targets. J Clin Invest 2007, 117:823-834.
106. Piccaluga P.P., Agostinelli C., Califano A., et al. Gene expression analysis of angioimmunoblastic lymphoma indicates derivation from T follicular helper cells and vascular endothelial growth factor deregulation. Cancer Res 2007, 67:10703-10710.
107. Au W.Y., Weisenburger D.D., Intragumtornchai T., et al. Clinical differences between nasal and extranasal natural killer/T-cell lymphoma: a study of 136 cases from the International Peripheral T-Cell Lymphoma Project. Blood 2009, 113:3931-3937.
108. Piccaluga P.P., Agostinelli C., Gazzola A., et al. Prognostic markers in peripheral T-cell lymphoma. Curr Hematol Malignancy Rep 2010, 5:222-228.
109. Chan J., Quintanilla-Martinez L., Ferry J., et al. Extranodal NK/T-cell lymphoma, nasal-type. WHO Classification of Tumors of Hematopoietic and Lymphoid Tissues 2008, 285. IARC, Lyon. (ed 4). S. Swerdlow (Ed.).
110. Barrionuevo C., Zaharia M., Martinez M.T., et al. Extranodal NK/T-cell lymphoma, nasal type: study of clinicopathologic and prognosis factors in a series of 78 cases from Peru. Appl Immunohistochem Mol Morphol 2007, 15:38-44.
111. Cheung M.M., Chan J.K., Lau W.H., et al. Early stage nasal NK/T-cell lymphoma: clinical outcome, prognostic factors, and the effect of treatment modality. Int J Radiat Oncol Biol Phys 2002, 54:182-190.
112. Au W.Y., Pang A., Choy C., et al. Quantification of circulating Epstein-Barr virus (EBV) DNA in the diagnosis and monitoring of natural killer cell and EBV-positive lymphomas in immunocompetent patients. Blood 2004, 104:243-249.
113. Chim C.S., Ma S.Y., Au W.Y., et al. Primary nasal natural killer cell lymphoma: long-term treatment outcome and relationship with the International Prognostic Index. Blood 2004, 103:216-221.
114. Huang W.T., Chang K.C., Huang G.C., et al. Bone marrow that is positive for Epstein-Barr virus encoded RNA-1 by in situ hybridization is related with a poor prognosis in patients with extranodal natural killer/T-cell lymphoma, nasal type. Haematologica 2005, 90:1063-1069.
115. Lee J., Suh C., Huh J., et al. Effect of positive bone marrow EBV in situ hybridization in staging and survival of localized extranodal natural killer/T-cell lymphoma, nasal-type. Clin Cancer Res 2007, 13:3250-3254.
116. Lee J., Suh C., Park Y.H., et al. Extranodal natural killer T-cell lymphoma, nasal-type: a prognostic model from a retrospective multicenter study. J Clin Oncol 2006, 24:612-618.
117. Suzuki R., Suzumiya J., Yamaguchi M., et al. Prognostic factors for mature natural killer (NK) cell neoplasms: aggressive NK cell leukemia and extranodal NK cell lymphoma, nasal type. Ann Oncol 2010, 21:1032-1040.