Clinicopathological and prognostic significance of BCL2, BCL6, MYC, and IRF4 copy number gains and translocations in follicular lymphoma: a study by FISH analysis

References

• Swerdlow SH. WHO classification of tumours of haematopoietic and lymphoid tissues. Lyon: International Agency for Research on Cancer, WHO; 2017.
   Google Scholar
• Freedman A. Follicular lymphoma: 2018 update on diagnosis and management. Am J Hematol. 2018;93(2):296–305.
   PubMed Web of Science ®Google Scholar
• Friedberg JW, Taylor MD, Cerhan JR, et al. Follicular lymphoma in the United States: first report of the National LymphoCare Study. J Cin Oncol. 2009;27(8):1202–1208.
   PubMed Web of Science ®Google Scholar
• 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(9):1327–1334.
   PubMed Web of Science ®Google Scholar
• Choi SM, Betz BL, Perry AM. Follicular lymphoma diagnostic caveats and updates. Arch Pathol Lab Med. 2018;142(11):1330–1340.
   PubMed Web of Science ®Google Scholar
• Masir N, Jones M, Abdul-Rahman F, et al. Variation in BCL2 protein expression in follicular lymphomas without t(14;18) chromosomal translocations. Pathology. 2012;44(3):228–233. Apr
   PubMed Web of Science ®Google Scholar
• Espinet B, Bellosillo B, Melero C, et al. FISH is better than BIOMED-2 PCR to detect IgH/BCL2 translocation in follicular lymphoma at diagnosis using paraffin-embedded tissue sections. Leuk Res. 2008;32(5):737–742.
   PubMed Web of Science ®Google Scholar
• Ott G, Katzenberger T, Lohr A, et al. Cytomorphologic, immunohistochemical, and cytogenetic profiles of follicular lymphoma: 2 types of follicular lymphoma grade 3. Blood. 2002;99(10):3806–3812.
   PubMed Web of Science ®Google Scholar
• 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. Modern pathology: an official journal of the United States and Canadian Academy of Pathology. Mod Pathol. 2009;22(9):1251–1257.
   PubMed Web of Science ®Google Scholar
• Christie L, Kernohan N, Levison D, et al. C-MYC translocation in t(14;18) positive follicular lymphoma at presentation: an adverse prognostic indicator? Leuk Lymphoma. 2008;49(3):470–476.
   PubMed Web of Science ®Google Scholar
• Tagawa H, Karube K, Guo Y, et al. Trisomy 3 is a specific genomic aberration of t(14;18) negative follicular lymphoma. Leukemia. 2007;21(12):2549–2551.
   PubMed Web of Science ®Google Scholar
• 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(8):973–978.
   PubMed Web of Science ®Google Scholar
• Karube K, Guo Y, Suzumiya J, et al. CD10 − MUM1+ follicular lymphoma lacks BCL2 gene translocation and shows characteristic biologic and clinical features. Blood. 2007;109(7):3076–3079.
   PubMed Web of Science ®Google Scholar
• Nguyen L, Papenhausen P, Shao H. The role of c-MYC in B-cell lymphomas: diagnostic and molecular aspects. Genes. 2017;8(4):116.
   PubMed Web of Science ®Google Scholar
• 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(1):275–282.
   PubMed Web of Science ®Google Scholar
• Chang CM, Schroeder JC, Huang WY, et al. Non-Hodgkin lymphoma (NHL) subtypes defined by common translocations: utility of fluorescence in situ hybridization (FISH) in a case-control study. Leuk Res. 2010;34(2):190–195.
   PubMed Web of Science ®Google Scholar
• Quesada AE, Medeiros LJ, Desai PA, et al. Increased MYC copy number is an independent prognostic factor in patients with diffuse large B-cell lymphoma. Mod Pathol. 2017;30(12):1688–1697.
   PubMed Web of Science ®Google Scholar
• Kertowidjojo E, Sticco K, Ahmed T, et al. Copy number aberrations in B-cell lymphoma: a call for consideration in prognosis determination and therapy. Leuk Res Rep. 2019;11:38–40.
   PubMedGoogle Scholar
• Zamò A, Pischimarov J, Schlesner M, et al. Differences between BCL2-break positive and negative follicular lymphoma unraveled by whole-exome sequencing. Leukemia. 2018;32(3):685–693. Mar
   PubMed Web of Science ®Google Scholar
• Leich E, Salaverria I, Bea S, et al. Follicular lymphomas with and without translocation t(14;18) differ in gene expression profiles and genetic alterations. Blood. 2009;114(4):826–834.
   PubMed Web of Science ®Google Scholar
• Guo Y, Karube K, Kawano R, et al. Low-grade follicular lymphoma with t(14;18) presents a homogeneous disease entity otherwise the rest comprises minor groups of heterogeneous disease entities with Bcl2 amplification, Bcl6 translocation or other gene aberrances. Leukemia. 2005;19(6):1058–1063.
   PubMed Web of Science ®Google Scholar
• Bouska A, McKeithan TW, Deffenbacher KE, et al. Genome-wide copy-number analyses reveal genomic abnormalities involved in transformation of follicular lymphoma. Blood. 2014;123(11):1681–1690.
   PubMed Web of Science ®Google Scholar
• Vaandrager JW, Schuuring E, Raap T, et al. Interphase FISH detection of BCL2 rearrangement in follicular lymphoma using breakpoint-flanking probes. Genes Chromosom Cancer. 2000;27(1):85–94.
   PubMed Web of Science ®Google Scholar
• Leich E, Hoster E, Wartenberg M, et al. Similar clinical features in follicular lymphomas with and without breaks in the BCL2 locus. Leukemia. 2016;30(4):854–860. Apr
   PubMed Web of Science ®Google Scholar
• Maeshima AM, Omatsu M, Nomoto J, et al. Diffuse large B-cell lymphoma after transformation from low-grade follicular lymphoma: morphological, immunohistochemical, and FISH analyses. Cancer Sci. 2008;99(9):1760–1768.
   PubMed Web of Science ®Google Scholar
• Masir N, Campbell LJ, Goff LK, et al. BCL2 protein expression in follicular lymphomas with t(14;18) chromosomal translocations. Br J Haematol. 2009;144(5):716–725.
   PubMed Web of Science ®Google Scholar
• Schraders M, de Jong D, Kluin P, et al. Lack of Bcl-2 expression in follicular lymphoma may be caused by mutations in the BCL2 gene or by absence of the t(14;18) translocation. J Pathol. 2005;205(3):329–335.
   PubMed Web of Science ®Google Scholar
• Horsman DE, Okamoto I, Ludkovski O, et al. Follicular lymphoma lacking the t(14;18)(q32;q21): identification of two disease subtypes. Br J Haematol. 2003;120(3):424–433. Feb
   PubMed Web of Science ®Google Scholar
• Katzenberger T, Ott G, Klein T, et al. Cytogenetic alterations affecting BCL6 are predominantly found in follicular lymphomas grade 3B with a diffuse large B-cell component. Am J Pathol. 2004;165(2):481–490.
   PubMed Web of Science ®Google Scholar
• 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(1):95–101.
   PubMed Web of Science ®Google Scholar
• Akasaka T, Lossos IS, Levy R. BCL6 gene translocation in follicular lymphoma: a harbinger of eventual transformation to diffuse aggressive lymphoma. Blood. 2003;102(4):1443–1448.
   PubMed Web of Science ®Google Scholar
• 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(11):4649–4655.
   PubMed Web of Science ®Google Scholar
• Aukema SM, van Pel R, Nagel I, et al. MYC expression and translocation analyses in low-grade and transformed follicular lymphoma. Histopathology. 2017;71(6):960–971.
   PubMed Web of Science ®Google Scholar
• Martinez-Climent JA, Alizadeh AA, Segraves R, et al. Transformation of follicular lymphoma to diffuse large cell lymphoma is associated with a heterogeneous set of DNA copy number and gene expression alterations. Blood. 2003;101(8):3109–3117.
   PubMed Web of Science ®Google Scholar
• Boonstra R, Bosga-Bouwer A, Mastik M, et al. Identification of chromosomal copy number changes associated with transformation of follicular lymphoma to diffuse large B-cell lymphoma. Hum Pathol. 2003;34(9):915–923.
   PubMed Web of Science ®Google Scholar
• Valera A, López-Guillermo A, Cardesa-Salzmann T, et al. MYC protein expression and genetic alterations have prognostic impact in patients with diffuse large B-cell lymphoma treated with immunochemotherapy. Haematologica. 2013;98(10):1554–1562. Oct
   PubMed Web of Science ®Google Scholar
• Li S, Seegmiller AC, Lin P, et al. B-cell lymphomas with concurrent MYC and BCL2 abnormalities other than translocations behave similarly to MYC/BCL2 double-hit lymphomas. Mod Pathol. 2015;28(2):208–217.
   PubMed Web of Science ®Google Scholar
• Willenbacher E, Willenbacher W, Weger R, et al. Patients with double/triple copy number gains on C-MYC, BCL2, and/or BCL6 treated with standard chemotherapy have a similarly poor prognosis than those with high-grade B cell lymphoma with C-MYC and BCL2 and/or BCL6 rearrangements: a single-center experience on a consecutive cohort of large B cell lymphomas. Ann Hematol. 2020;99(9):2125–2132.
   PubMed Web of Science ®Google Scholar
• Hoglund M, Sehn L, Connors JM, et al. Identification of cytogenetic subgroups and karyotypic pathways of clonal evolution in follicular lymphomas. Genes Chromosomes Cancer. 2004;39(3):195–204.
   PubMed Web of Science ®Google Scholar
• Horsman DE, Connors JM, Pantzar T, et al. Analysis of secondary chromosomal alterations in 165 cases of follicular lymphoma with t(14;18). Genes Chromosomes Cancer. 2001;30(4):375–382.
   PubMed Web of Science ®Google Scholar