Double-hit B-cell lymphomas with BCL6 and MYC translocations are aggressive, frequently extranodal lymphomas distinct from BCL2 double-hit B-cell lymphomas

American Journal of Surgical Pathology

Volumn 37, Issue 3, 2013, Pages 323-332

  Pillai, Raju K ^a   Sathanoori, Malini ^a   Van Oss, Stephen Branden ^a   Swerdlow, Steven H ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

B cell lymphoma; BCL2; BCL6; Double hit lymphoma; MYC; unclassifiable

Indexed keywords

BCL6 PROTEIN, HUMAN; DNA BINDING PROTEIN;

AGED; ARTICLE; B CELL LYMPHOMA; FEMALE; FLOW CYTOMETRY; FLUORESCENCE IN SITU HYBRIDIZATION; GENE TRANSLOCATION; GENETICS; HUMAN; IMMUNOHISTOCHEMISTRY; IMMUNOPHENOTYPING; MALE; MIDDLE AGED; ONCOGENE MYC; PATHOLOGY; PHENOTYPE; PROTO ONCOGENE;

AGED; AGED, 80 AND OVER; DNA-BINDING PROTEINS; FEMALE; FLOW CYTOMETRY; GENES, BCL-2; GENES, MYC; HUMANS; IMMUNOHISTOCHEMISTRY; IMMUNOPHENOTYPING; IN SITU HYBRIDIZATION, FLUORESCENCE; LYMPHOMA, B-CELL; MALE; MIDDLE AGED; PHENOTYPE; TRANSLOCATION, GENETIC;

EID: 84873998338     PISSN: 01475185     EISSN: 15320979     Source Type: Journal    
DOI: 10.1097/PAS.0b013e31826cebad     Document Type: Article

References (58)

1. Aukema SM, Siebert R, Schuuring E, et al. Double-hit B-cell lymphomas. Blood. 2011;117:2319-2331.
2. Klapper W, Stoecklein H, Zeynalova S, et al. Structural aberrations affecting the MYC locus indicate a poor prognosis independent of clinical risk factors in diffuse large B-cell lymphomas treated within randomized trials of the German High-Grade Non-Hodgkin's Lymphoma Study Group (DSHNHL). Leukemia. 2008;22:2226-2229.
3. Boerma EG, Siebert R, Kluin PM, et al. Translocations involving 8q24 in Burkitt lymphoma and other malignant lymphomas: a historical review of cytogenetics in the light of todays knowledge. Leukemia. 2009;23:225-234.
4. Iqbal J, Greiner TC, Patel K, et al. Distinctive patterns of BCL6 molecular alterations and their functional consequences in different subgroups of diffuse large B-cell lymphoma. Leukemia. 2007; 21:2332-2343.
5. Diaz-Alderete A, Doval A, Camacho F, et al. Frequency of BCL2 and BCL6 translocations in follicular lymphoma: relation with histological and clinical features. Leuk Lymphoma. 2008;49:95-101.
6. Gu K, Fu K, Jain S, et al. t(14;18)-negative follicular lymphomas are associated with a high frequency of BCL6 rearrangement at the alternative breakpoint region. Mod Pathol. 2009;22:1251-1257.
7. Kluin PM, Harris NL, Stein H, et al. B-cell lymphoma, unclassifiable, with features intermediate between diffuse large B-cell lymphoma and Burkitt lymphoma. In: Swerdlow SH, Campo E, Harris NL, et al, eds. WHO Classification of Tumors of Hematopoietic and Lymphoid Tissues. Lyon, France: IARC Press; 2008:265-266.
8. Johnson NA, Savage KJ, Ludkovski O, et al. Lymphomas with concurrent BCL2 and MYC translocations: the critical factors associated with survival. Blood. 2009;114:2273-2279.
9. Le Gouill S, Talmant P, Touzeau C, et al. The clinical presentation and prognosis of diffuse large B-cell lymphoma with t(14;18) and 8q24/c-MYC rearrangement. Haematologica. 2007;92:1335-1342.
10. Macpherson N, Lesack D, Klasa R, et al. Small noncleaved, non-Burkitt's (Burkit-Like) lymphoma: cytogenetics predict outcome and reflect clinical presentation. J Clin Oncol. 1999;17:1558-1567.
11. Niitsu N, Okamoto M, Miura I, et al. Clinical features and prognosis of de novo diffuse large B-cell lymphoma with t(14;18) and 8q24/c-MYC translocations. Leukemia. 2009;23:777-783.
12. Snuderl M, Kolman OK, Chen YB, et al. B-cell lymphomas with concurrent IGH-BCL2 and MYC rearrangements are aggressive neoplasms with clinical and pathologic features distinct from Burkitt lymphoma and diffuse large B-cell lymphoma. Am J Surg Pathol. 2010;34:327-340.
13. Tomita N, Tokunaka M, Nakamura N, et al. Clinicopathological features of lymphoma/leukemia patients carrying both BCL2 and MYC translocations. Haematologica. 2009;94:935-943.
14. Bertrand P. Bastard C, Maingonnat C, et al. Mapping of MYC breakpoints in 8q24 rearrangements involving non-immunoglobulin partners in B-cell lymphomas. Leukemia. 2007;21:515-523.
15. Kanungo A, Medeiros LJ, Abruzzo LV, et al. Lymphoid neoplasms associated with concurrent t(14;18) and 8q24/c-MYC translocation generally have a poor prognosis. Mod Pathol. 2006;19:25-33.
16. Lindsley RC, Lacasce AS. Biology of double-hit B-cell lymphomas. Curr Opin Hematol. 2012;19:299-304.
17. Li S, Lin P, Fayad LE, et al. B-cell lymphomas with MYC/8q24 rearrangements and IGH@BCL2/t(14;18)(q32;q21): an aggressive disease with heterogeneous histology, germinal center B-cell immunophenotype and poor outcome. Mod Pathol. 2012;25:145-156.
18. Wu D, Wood BL, Dorer R, et al. "Double-Hit" mature B-cell lymphomas show a common immunophenotype by flow cytometry that includes decreased CD20 expression. Am J Clin Pathol. 2010;134:258-265.
19. Basso K, Dalla-Favera R. Roles of BCL6 in normal and transformed germinal center B cells. Immunol Rev. 2012;247:172-183.
20. Mitelman F, Johansson B, Mertens F, eds. Mitelman Database of Chromosome Aberrations and Gene Fusions in Cancer. http://cgap.nci.nih.gov/chromosomes/ Mitelman. Accessed April 30, 2011.
21. Swerdlow SH, Campo E, Harris NL, et al. WHO Classification of Tumours of Hematopoietic and Lymphoid Tissues. Lyon, France: IARC Press; 2008.
22. Hans CP, Weisenburger DD, Greiner TC, et al. Confirmation of the molecular classification of diffuse large B-cell lymphoma by immunohistochemistry using a tissue microarray. Blood. 2004;103:275-282.
23. Cook JR, Sherer M, Craig FE, et al. t(14;18)(q32;q21) involving MALT1 and IGH genes in an extranodal diffuse large B-cell lymphoma. Hum Pathol. 2003;34:1212-1215.
24. Dewald GW, Ketterling RP, Wyatt WA, et al. Cytogenetic studies in neoplastic hematologic disorders. In: McClatchey KD, ed. Clinical Laboratory Medicine. Philadelphia: Lippincott Williams and Wilkins; 2002:658-685.
25. Seegmiller AC, Garcia R, Huang R, et al. Simple karyotype and bcl-6 expression predict a diagnosis of Burkitt lymphoma and better survival in IG-MYC rearranged high-grade B-cell lymphomas. Mod Pathol. 2010;23:909-920.
26. Aamot HV, Micci F, Holte H, et al. G-banding and molecular cytogenetic analyses of marginal zone lymphoma. Br J Haematol. 2005;130:890-901.
27. Ashihara E, Shimazaki C, Hirai H, et al. Human herpes virus 8-negative primary effusion lymphoma in a patient with a ventriculoperitoneal shunt tube. Int J Hematol. 2001;74:327-332.
28. Bernicot I, Douet-Guilbert N, Le Bris MJ, et al. Molecular cytogenetics of IGH rearrangements in non-Hodgkin B-cell lymphoma. Cytogenet Genome Res. 2007;118:345-352.
29. Dave BJ, Nelson M, Pickering DL, et al. Cytogenetic characterization of diffuse large cell lymphoma using multi-color fluorescence in situ hybridization. Cancer Genet Cytogenet. 2002;132:125-132.
30. Itoyama T, Nanjungud G, Chen W, et al.Molecular cytogenetic analysis of genomic instability at the 1q12-22 chromosomal site in B-cell non-Hodgkin lymphoma. Genes Chromosomes Cancer. 2002;35:318-328.
31. Kanda-Akano Y, Nomura K, Fujita Y, et al. Molecular-cytogenetic characterization of non-Hodgkin's lymphoma with double and cryptic translocations of the immunoglobulin heavy chain gene. Leuk Lymphoma. 2004;45:1559-1567.
32. Ladanyi M, Offit K, Jhanwar SC, et al. MYC rearrangement and translocations involving band 8q24 in diffuse large cell lymphomas. Blood. 1991;77:1057-1063.
33. Lai JL, Daudignon A, Kerckaert JP, et al. Translocation (3;13)(q27;q14): a nonrandom and probably secondary structural change in non-Hodgkin lymphomas. Cancer Genet Cytogenet. 1998;103:140-143.
34. Rubnitz JE, Abushullaih B, Kaste SC, et al. BCL6 rearrangement and mediastinal involvement in a case of B cell acute lymphoblastic leukemia. Leukemia. 1998;12:1163-1165.
35. Sandlund JT, Kastan MB, Kennedy W, et al. A subtle t(3;8) results in plausible juxtaposition of MYC and BCL6 in a child with Burkitt lymphoma/leukemia and ataxia-telangiectasia. Cancer Genet Cytogenet. 2006;168:69-72.
36. Sawyer JR, Lukacs JL, Munshi N, et al. Identification of new nonrandom translocations in multiple myeloma with multicolor spectral karyotyping. Blood. 1998;92:4269-4278.
37. Wang HY, Bossler AD, Schaffer A, et al. A novel t(3;8)(q27;q24.1) simultaneously involving both the BCL6 and MYC genes in a diffuse large B-cell lymphoma. Cancer Genet Cytogenet. 2007;172:45-53.
38. Daly P, Brito-Babapulle V, Lawlor E, et al. Variant translocation t(8;22) and abnormalities of chromosome 15(q22) and 17(q12-21) in a Burkitt's lymphoma/leukaemia with disseminated intravascular coagulation. Br J Haematol. 1986;64:561-569.
39. Katsura Y, Ohta I, Yoshida C, et al. Diffuse large B-cell lymphoma carrying both t(3; 7)(q27; p12) and t(8; 14)(q24; q32). Intern Med. 2011;50:905-908.
40. 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.
41. Dave SS, Fu K, Wright GW, et al. Molecular diagnosis of Burkitt's lymphoma. N Engl JMed. 2006;354:2431-2442.
42. Salaverria I, ZettlA, Bea S, et al.Chromosomal alterations detected by comparative genomic hybridization in subgroups of gene expressiondefined Burkitt's lymphoma. Haematologica. 2008;93:1327-1334.
43. Lin P, Dickason TJ, Fayad LE, et al. Prognostic value of MYC rearrangement in cases of B-cell lymphoma, unclassifiable, with features intermediate between diffuse large B-cell lymphoma and Burkitt lymphoma. Cancer. 2012;118:1566-1573.
44. Li JY, Xu W, Wu W, et al. The negative prognostic impact of derivative 9 deletions in patients who received hydroxyurea treatment for chronic myelogenous leukemia in the chronic phase. Onkologie. 2008;31:585-589.
45. Loong F, Chan AC, Ho BC, et al. Diffuse large B-cell lymphoma associated with chronic inflammation as an incidental finding and new clinical scenarios. Mod Pathol. 2010;23:493-501.
46. Tomita N. BCL2 and MYC dual-hit lymphoma/leukemia. J Clin Exp Hematop. 2011;51:7-12.
47. Karube K, Ying G, Tagawa H, et al. BCL6 gene amplification/3q27 gain is associated with unique clinicopathological characteristics among follicular lymphoma without BCL2 gene translocation. Mod Pathol. 2008;21:973-978.
48. Barrans S, Crouch S, Smith A, et al. Rearrangement of MYC is associated with poor prognosis in patients with diffuse large B-cell lymphoma treated in the era of rituximab. J Clin Oncol. 2010;28:3360-3365.
49. Durnick DK, Law ME, Maurer MJ, et al. Expression of LMO2 is associated with t(14;18)/IGH-BCL2 fusion but not BCL6 translocations in diffuse large B-cell lymphoma. Am J Clin Pathol. 2010;134:278-281.
50. Horn H, Schmelter C, Leich E, et al. Follicular lymphoma grade 3B is a distinct neoplasm according to cytogenetic and immunohistochemical profiles. Haematologica. 2011;96:1327-1334.
51. Renne C, Martin-Subero JI, Hansmann ML, et al. Molecular cytogenetic analyses of immunoglobulin loci in nodular lymphocyte predominant Hodgkin's lymphoma reveal a recurrent IGH-BCL6 juxtaposition. J Mol Diagn. 2005;7:352-356.
52. Salaverria I, Siebert R. Follicular lymphoma grade 3B. Best Pract Res Clin Haematol. 2011;24:111-119.
53. Wlodarska I, Nooyen P, Maes B, et al. Frequent occurrence of BCL6 rearrangements in nodular lymphocyte predominance Hodgkin lymphoma but not in classical Hodgkin lymphoma. Blood. 2003;101:706-710.
54. Ohno H. Pathogenetic and clinical implications of non-immunoglobulin; BCL6 translocations in B-cell non-Hodgkin's lymphoma. J Clin Exp Hematop. 2006;46:43-53.
55. Forbes SA, Bhamra G, Bamford S, et al. The Catalogue of Somatic Mutations in Cancer (COSMIC). Curr Protoc Hum Genet. 2008. Chapter 10: Unit 10 11.
56. Bosga-Bouwer AG, Haralambieva E, Booman M, et al. BCL6 alternative translocation breakpoint cluster region associated with follicular lymphoma grade 3B. Genes Chromosomes Cancer. 2005;44: 301-304.
57. Gollub W, Stassek B, Huckhagel T, et al. BCL6-translocations affect the phenotype of follicular lymphomas only in the absence of t(14;18)IgH/BCL2. Anticancer Res. 2009;29:4649-4655.
58. Bacher U, Haferlach T, Alpermann T, et al. Several lymphomaspecific genetic events in parallel can be found in mature B-cell neoplasms. Genes Chromosomes Cancer. 2011;50:43-50.