Expression of TCF3 target genes defines a subclass of diffuse large B-cell lymphoma characterized by up-regulation of MYC target genes and poor clinical outcome following R-CHOP therapy

References

• Swerdlow SH, Cook JR. As the world turns, evolving lymphoma classifications-past, present and future. Hum Pathol. 2020;95:55–77.
   PubMed Web of Science ®Google Scholar
• Morton LM, Wang SS, Devesa SS, et al. Lymphoma incidence patterns by WHO subtype in the United States, 1992–2001. Blood. 2006;107(1):265–276.
   PubMed Web of Science ®Google Scholar
• Crump M, Neelapu SS, Farooq U, et al. Outcomes in refractory diffuse large B-cell lymphoma: results from the international SCHOLAR-1 study. Blood. 2017;130(16):1800–1808.
   PubMed Web of Science ®Google Scholar
• Ziepert M, Hasenclever D, Kuhnt E, et al. Standard international prognostic index remains a valid predictor of outcome for patients with aggressive CD20+ B-cell lymphoma in the rituximab era. J Clin Oncol. 2010;28(14):2373–2380.
   PubMed Web of Science ®Google Scholar
• Sha C, Barrans S, Care MA, et al. Transferring genomics to the clinic: distinguishing burkitt and diffuse large B cell lymphomas. Genome Med. 2015;7(1):64.
   PubMedGoogle Scholar
• Alizadeh AA, Eisen MB, Davis RE, et al. Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling. Nature. 2000;403(6769):503–511.
   PubMed Web of Science ®Google Scholar
• Rosenwald A, Wright G, Chan WC, Lymphoma/Leukemia Molecular Profiling Project, et al. The use of molecular profiling to predict survival after chemotherapy for diffuse large-B-cell lymphoma. N Engl J Med. 2002;346(25):1937–1947.
   PubMed Web of Science ®Google Scholar
• Scott DW, Mottok A, Ennishi D, et al. Prognostic significance of diffuse large B-Cell lymphoma cell of origin determined by digital gene expression in formalin-fixed paraffin-embedded tissue biopsies. J Clin Oncol. 2015;33(26):2848–2856.
   PubMed Web of Science ®Google Scholar
• Shipp MA, Ross KN, Tamayo P, et al. Diffuse large B-cell lymphoma outcome prediction by gene-expression profiling and supervised machine learning. Nat Med. 2002;8(1):68–74.
   PubMed Web of Science ®Google Scholar
• Poulsen CB, Borup R, Nielsen FC, et al. Microarray-based classification of diffuse large B-cell lymphoma. Eur J Haematol. 2005;74(6):453–465.
   PubMed Web of Science ®Google Scholar
• Staiger AM, Ziepert M, Horn H, German High-Grade Lymphoma Study Group, et al. Clinical impact of the cell-of-Origin classification and the MYC/BCL2 dual expresser status in diffuse large B-cell lymphoma treated within prospective clinical trials of the German high-grade non-Hodgkin’s lymphoma study group. J Clin Oncol. 2017;35(22):2515–2526.
   PubMed Web of Science ®Google Scholar
• de Pooter RF, Kee BL. E proteins and the regulation of early lymphocyte development. Immunol Rev. 2010;238(1):93–109.
   PubMedGoogle Scholar
• Schmitz R, Ceribelli M, Pittaluga S, et al. Oncogenic mechanisms in Burkitt lymphoma. Cold Spring Harb Perspect Med. 2014;4:a014282.
   PubMed Web of Science ®Google Scholar
• Gebauer N, Bernard V, Feller AC, et al. ID3 mutations are recurrent events in double-hit B-cell lymphomas. Anticancer Res. 2013;33(11):4771–4778.
   PubMed Web of Science ®Google Scholar
• Chen L, Tyryshkin K, Moore A, et al. Objective quantification of BCL2 protein by multiplex immunofluorescence in routine biopsy samples of diffuse large B-cell lymphoma demonstrates associations with survival and BCL2 gene alterations. Leuk Lymphoma. 2020;61(6):1334–1344.
   PubMed Web of Science ®Google Scholar
• Scott DW, Wright GW, Williams PM, et al. Determining cell-of-origin subtypes of diffuse large B-cell lymphoma using gene expression in formalin-fixed paraffin-embedded tissue. Blood. 2014;123(8):1214–1217.
   PubMed Web of Science ®Google Scholar
• Schmitz R, Young RM, Ceribelli M, et al. Burkitt lymphoma pathogenesis and therapeutic targets from structural and functional genomics. Nature. 2012;490(7418):116–120.
   PubMed Web of Science ®Google Scholar
• Lenz G, Wright G, Dave SS, Lymphoma/Leukemia Molecular Profiling Project, et al. Stromal gene signatures in large-B-cell lymphomas. N Engl J Med. 2008;359(22):2313–2323.
   PubMed Web of Science ®Google Scholar
• Irizarry RA, Hobbs B, Collin F, et al. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics. 2003;4(2):249–264.
   PubMed Web of Science ®Google Scholar
• Gerolami J, Wong JJM, Zhang R, et al. A novel computational approach to identification of candidate biomarkers in high-dimensional molecular data. Diagnostics. 2022;12(8):1997.
   Web of Science ®Google Scholar
• Altman NS. An introduction to kernel and Nearest-Neighbor nonparametric regression. Am Statist. 1992;46:175–185.
   Web of Science ®Google Scholar
• Pellagatti A, Benner A, Mills KI, et al. Identification of gene expression-based prognostic markers in the hematopoietic stem cells of patients with myelodysplastic syndromes. J Clin Oncol. 2013;31(28):3557–3564.
   PubMed Web of Science ®Google Scholar
• Cull AH, Mahendru D, Snetsinger B, et al. Overexpression of arginase 1 is linked to DNMT3A and TET2 mutations in lower-grade myelodysplastic syndromes and chronic myelomonocytic leukemia. Leuk Res. 2018;65:5–13.
   PubMed Web of Science ®Google Scholar
• Cull AH, Rauh MJ. Success in bone marrow failure? Novel therapeutic directions based on the immune environment of myelodysplastic syndromes. J Leukoc Biol. 2017;102(2):209–219.
   PubMed Web of Science ®Google Scholar
• Reddy A, Zhang J, Davis NS, et al. Genetic and functional drivers of diffuse large B cell lymphoma. Cell. 2017;171(2):481–494.e15.
   PubMed Web of Science ®Google Scholar
• Wright G, Tan B, Rosenwald A, et al. A gene expression-based method to diagnose clinically distinct subgroups of diffuse large B cell lymphoma. Proc Natl Acad Sci USA. 2003;100(17):9991–9996.
   PubMed Web of Science ®Google Scholar
• Subramanian A, Tamayo P, Mootha VK, et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA. 2005;102(43):15545–15550.
   PubMed Web of Science ®Google Scholar
• Liberzon A, Birger C, Thorvaldsdottir H, et al. The molecular signatures database (MSigDB) hallmark gene set collection. Cell Syst. 2015;1(6):417–425.
   PubMed Web of Science ®Google Scholar
• Cheson BD, Pfistner B, Juweid ME, International Harmonization Project on Lymphoma, et al. Revised response criteria for malignant lymphoma. J Clin Oncol. 2007;25(5):579–586.
   PubMed Web of Science ®Google Scholar
• Ding BB, Yu JJ, Yu RY, et al. Constitutively activated STAT3 promotes cell proliferation and survival in the activated B-cell subtype of diffuse large B-cell lymphomas. Blood. 2008;111(3):1515–1523.
   PubMed Web of Science ®Google Scholar
• Sesques P, Johnson NA. Approach to the diagnosis and treatment of high-grade B-cell lymphomas with MYC and BCL2 and/or BCL6 rearrangements. Blood. 2017;129(3):280–288.
   PubMed Web of Science ®Google Scholar
• Pasqualucci L, Dalla-Favera R. Genetics of diffuse large B-cell lymphoma. Blood. 2018;131(21):2307–2319.
   PubMed Web of Science ®Google Scholar
• Chapuy B, Stewart C, Dunford AJ, et al. Molecular subtypes of diffuse large B cell lymphoma are associated with distinct pathogenic mechanisms and outcomes. Nat Med. 2018;24(5):679–690.
   PubMed Web of Science ®Google Scholar
• Carey CD, Gusenleitner D, Chapuy B, et al. Molecular classification of MYC-driven B-cell lymphomas by targeted gene expression profiling of fixed biopsy specimens. J Mol Diagn. 2015;17(1):19–30.
   PubMed Web of Science ®Google Scholar
• Dominguez-Sola D, Victora GD, Ying CY, et al. The proto-oncogene MYC is required for selection in the germinal center and cyclic reentry. Nat Immunol. 2012;13(11):1083–1091.
   PubMed Web of Science ®Google Scholar
• Green MR, Vicente-Dueñas C, Romero-Camarero I, et al. Transient expression of Bcl6 is sufficient for oncogenic function and induction of mature B-cell lymphoma. Nat Commun. 2014;5:3904.
   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
• Blenk S, Engelmann J, Weniger M, et al. Germinal center B cell-like (GCB) and activated B cell-like (ABC) type of diffuse large B cell lymphoma (DLBCL): analysis of molecular predictors, signatures, cell cycle state and patient survival. Cancer Inform. 2007;3:399–420.
   PubMedGoogle Scholar
• Bret C, Klein B, Moreaux J. Gene expression-based risk score in diffuse large B-cell lymphoma. Oncotarget. 2012;3(12):1700–1710.
   PubMedGoogle Scholar
• Lossos IS, Czerwinski DK, Alizadeh AA, et al. Prediction of survival in diffuse large-B-cell lymphoma based on the expression of six genes. N Engl J Med. 2004;350(18):1828–1837.
   PubMed Web of Science ®Google Scholar
• Akhmedov M, Galbusera L, Montemanny R, et al. 2018. A prize-collecting steiner tree application for signature selection to stratify diffuse large B-cell lymphoma subtypes. In bioRxiv. Cold Spring Harbor Laboratory.
   Google Scholar
• Mundt F, Merrien M, Nygren L, et al. Expression of GNAZ, encoding the Gα(z) protein, predicts survival in mantle cell lymphoma. Br J Haematol. 2019;185(4):708–712.
   PubMed Web of Science ®Google Scholar
• Jeong MH, Park SY, Lee SH, et al. EPB41L5 mediates TGFβ-Induced metastasis of gastric cancer. Clin Cancer Res. 2019;25(12):3617–3629.
   PubMed Web of Science ®Google Scholar
• Otsuka Y, Sato H, Oikawa T, et al. High expression of EPB41L5, an integral component of the Arf6-driven mesenchymal program, correlates with poor prognosis of squamous cell carcinoma of the tongue. Cell Commun Signal. 2016;14(1):28.
   PubMedGoogle Scholar
• Haldrup J, Strand SH, Cieza-Borrella C, et al. FRMD6 has tumor suppressor functions in prostate cancer. Oncogene. 2021;40(4):763–776.
   PubMed Web of Science ®Google Scholar
• Amini RM, Ljungström V, Abdulla M, et al. Clonal hematopoiesis in patients with high-grade B-cell lymphoma is associated with inferior outcome. Am J Hematol. 2020;95(10):E287–E289.
   PubMed Web of Science ®Google Scholar
• Dozzo M, Zaja F, Volpetti S, et al. Two cases of concomitant diffuse large B-cell lymphoma and myelodysplastic syndrome. Am J Hematol. 2014;89(10):1011–1013.
   PubMed Web of Science ®Google Scholar
• Riihijärvi S, Fiskvik I, Taskinen M, et al. Prognostic influence of macrophages in patients with diffuse large B-cell lymphoma: a correlative study from a Nordic phase II trial. Haematologica. 2015;100(2):238–245.
   PubMed Web of Science ®Google Scholar
• Nam SJ, Go H, Paik JH, et al. An increase of M2 macrophages predicts poor prognosis in patients with diffuse large B-cell lymphoma treated with rituximab, cyclophosphamide, doxorubicin, vincristine and prednisone. Leuk Lymphoma. 2014;55(11):2466–2476.
   PubMed Web of Science ®Google Scholar
• Ochi Y, Hiramoto N, Yoshizato T, et al. Clonally related diffuse large B-cell lymphoma and interdigitating dendritic cell sarcoma sharing MYC translocation. Haematologica. 2018;103(11):e553–e556.
   PubMed Web of Science ®Google Scholar
• Rapino F, Robles EF, Richter-Larrea JA, et al. C/EBPα induces highly efficient macrophage transdifferentiation of B lymphoma and leukemia cell lines and impairs their tumorigenicity. Cell Rep. 2013;3(4):1153–1163.
   PubMed Web of Science ®Google Scholar