Immunohistochemical and genomic profiles of diffuse large B-cell lymphomas: Implications for targeted EZH2 inhibitor therapy?

Oncotarget

Volumn 6, Issue 18, 2015, Pages 16712-16724

  Dubois, Sydney ^a   Mareschal, Sylvain ^a   Picquenot, Jean Michel ^a,b   Viailly, Pierre Julien ^a   Bohers, Elodie ^a   Cornic, Marie ^b   Bertrand, Philippe ^a   Veresezan, Elena Liana ^a,b   Ruminy, Philippe ^a   Maingonnat, Catherine ^a   Marchand, Vinciane ^a   Lanic, Hélène ^a,b   Penther, Dominique ^a   Bastard, Christian ^a   Tilly, Hervé ^a,b   Jardin, Fabrice ^a,b  

^a UNIVERSITY OF ROUEN   (France)

^b CENTRE HENRI BECQUEREL   (France)

Author keywords

Dlbcl; Ezh2; Immunohistochemistry; Methylation; Ngs

Indexed keywords

BLEOMYCIN; CYCLOPHOSPHAMIDE; CYTARABINE; DOXORUBICIN; ETOPOSIDE; IFOSFAMIDE; PREDNISONE; TRANSCRIPTION FACTOR EZH2; VINCRISTINE; VINDESINE; DNA BINDING PROTEIN; EZH2 PROTEIN, HUMAN; HISTONE; POLYCOMB REPRESSIVE COMPLEX 2;

ADOLESCENT; AGED; ARTICLE; FEMALE; GENE MUTATION; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; LARGE CELL LYMPHOMA; MAJOR CLINICAL STUDY; MALE; NEXT GENERATION SEQUENCING; PATHOGENESIS; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PROTEIN BLOOD LEVEL; PROTEIN TARGETING; UPREGULATION; VERY ELDERLY; ADULT; ANTAGONISTS AND INHIBITORS; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; LYMPHOMA, LARGE B-CELL, DIFFUSE; METABOLISM; METHYLATION; MIDDLE AGED; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; DNA-BINDING PROTEINS; ENHANCER OF ZESTE HOMOLOG 2 PROTEIN; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HISTONES; HUMANS; IMMUNOHISTOCHEMISTRY; LYMPHOMA, LARGE B-CELL, DIFFUSE; MALE; METHYLATION; MIDDLE AGED; POLYCOMB REPRESSIVE COMPLEX 2; YOUNG ADULT;

EID: 84937872378     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.3154     Document Type: Article

References (39)

1. Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, Thiele J, Vardiman JW. WHO classification of tumours of haematopoietic and lymphoid tissues. Lyon: IARC; 2008.
2. Alizadeh AA, Eisen MB, Davis RE, Ma C, Lossos IS, Rosenwald A, Boldrick JC, Sabet H, Tran T, Yu X, Powell JI, Yang L, Marti GE, et al. Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling. Nature. 2000; 403:503-11.
3. Wright G, Tan B, Rosenwald A, Hurt EH, Wiestner A, Staudt LM. A gene expression-based method to diagnose clinically distinct subgroups of diffuse large B cell lymphoma. Proc Natl Acad Sci U S A. 2003; 100:9991-6. [Internet] Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?art id=187912&tool=pmcentrez&rendertype=Abstract.
4. Margueron R, Reinberg D. The Polycomb complex PRC2 and its mark in life. Nature. 2011; 469:343-9. [cited 2014 Jul 9] [Internet] Available from: http://www.pubmedcentral. nih.gov/articlerender.fcgi?artid=3760771&tool=pmcentrez &rendertype=Abstract.
5. Viré E, Brenner C, Deplus R, Blanchon L, Fraga M, Didelot C, Morey L, Van Eynde A, Bernard D, Vanderwinden J-M, Bollen M, Esteller M, Di Croce L, et al. The Polycomb group protein EZH2 directly controls DNA methylation. Nature. 2006; 439:871-4. [cited 2014 Jul 10] [Internet] Available from: http://www.ncbi.nlm.nih. gov/pubmed/16357870.
6. Sneeringer CJ, Scott MP, Kuntz KW, Knutson SK, Pollock RM, Richon VM, Copeland RA. Coordinated activities of wild-type plus mutant EZH2 drive tumor-associated hypertrimethylation of lysine 27 on histone H3 (H3K27) in human B-cell lymphomas. Proc Natl Acad Sci U S A. 2010; 107:20980-5. [cited 2014 Jul 11] [Internet] Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid= 3000297&tool=pmcentrez&rendertype=Abstract.
7. Yap DB, Chu J, Berg T, Schapira M, Cheng S-WG, Moradian A, Morin RD, Mungall AJ, Meissner B, Boyle M, Marquez VE, Marra M a, Gascoyne RD, et al. Somatic mutations at EZH2 Y641 act dominantly through a mechanism of selectively altered PRC2 catalytic activity, to increase H3K27 trimethylation. Blood. 2011; 117:2451-9. [Internet] Available from: http://www.pubmedcentral.nih. gov/articlerender.fcgi?artid=3062411&tool=pmcentrez&re ndertype=Abstract.
8. McCabe MT, Ott HM, Ganji G, Korenchuk S, Thompson C, Van Aller GS, Liu Y, Graves AP, Della Pietra A, Diaz E, LaFrance L V, Mellinger M, Duquenne C, et al. EZH2 inhibition as a therapeutic strategy for lymphoma with EZH2-activating mutations. Nature. Nature Publishing Group. 2012; 492:108-12. [Internet] [cited 2013 Jan 29] Available from: http://www.ncbi.nlm.nih.gov/pubmed/23051747.
9. Knutson SK, Kawano S, Minoshima Y, Warholic NM, Huang K-C, Xiao Y, Kadowaki T, Uesugi M, Kuznetsov G, Kumar N, Wigle TJ, Klaus CR, Allain CJ, et al. Selective inhibition of EZH2 by EPZ-6438 leads to potent antitumor activity in EZH2-mutant non-hodgkin lymphoma. Mol Cancer Ther. 2014; 13:842-54. [Internet] Available from: http://www.ncbi.nlm.nih.gov/pubmed/24563539.
10. Qi W, Chan H, Teng L, Li L, Chuai S, Zhang R, Zeng J, Li M, Fan H. Selective inhibition of Ezh2 by a small molecule inhibitor blocks tumor cells proliferation. Proc Natl Acad Sci. 2012; 109:21360-5.
11. Copeland RA, Richon VM, Scott MD, Sneeringer CJ, Knutson SK, Pollock RM. US 8691507. 2014. [Internet] Available from: http://www.google.com/patents/US8691507?.
12. Holm K, Grabau D, Lövgren K, Aradottir S, Gruvberger-Saal S, Howlin J, Saal LH, Ethier SP, Bendahl P-O, Stål O, Malmström P, Fernö M, Rydén L, et al. Global H3K27 trimethylation and EZH2 abundance in breast tumor subtypes. Mol Oncol. 2012; [cited 2014 Jul 28]; 6:494-506. [Internet] Available from: http://www.ncbi.nlm.nih.gov/pubmed/22766277.
13. Bohers E, Mareschal S, Bouzelfen A, Marchand V, Ruminy P, Maingonnat C, Ménard A-L, Etancelin P, Bertrand P, Dubois S, Alcantara M, Bastard C, Tilly H, et al. Targetable activating mutations are very frequent in GCB and ABC diffuse large B-cell lymphoma. Genes Chromosome Cancer. 2014; 014 [cited 2013 Dec 19]; 53:144-53. [Internet] Available from: http://www.ncbi. nlm.nih.gov/pubmed/24327543.
14. Wang K, Li M, Hakonarson H. ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res. 2010; [cited 2014 Jul 15]; 38:e164. [Internet] Available from: http://www. pubmedcentral.nih.gov/articlerender.fcgi?artid=2938201& tool=pmcentrez&rendertype=Abstract.
15. Kumar P, HenikoffS, Ng PC. Predicting the effects of coding non-synonymous variants on protein function using the SIFT algorithm. Nat Protoc. 2009; [cited 2014 Jul 14]; 4:1073-81. [Internet] Available from: http://www.ncbi.nlm. nih.gov/pubmed/19561590.
16. Sehested J. A simple method for R banding of human chromosomes, showing a pH-dependent connection between R and G bands. Humangenetik. 1974; 21:55-8.
17. Foundation for Statistical Computing: R: A language and environment for statistical computing. Vienna, Austria. [Internet] Available from: http://www.r-project.org/.
18. Morin RD, Johnson NA, Severson TM, Mungall AJ, An J, Goya R, Paul JE, Boyle M, Woolcock BW, Kuchenbauer F, Yap D, Humphries RK, Griffith OL, et al. Somatic mutations altering EZH2 (Tyr641) in follicular and diffuse large B-cell lymphomas of germinal-center origin. Nat Genet. Nature Publishing Group. 2010; 42:181-5. [Internet] [cited 2013 Jan 29] Available from: http://www.pubmedcentral. nih.gov/articlerender.fcgi?artid=2850970&tool=pmcentrez &rendertype=Abstract.
19. Pasqualucci L, Trifonov V, Fabbri G, Ma J, Rossi D, Chiarenza A, Wells V a, Grunn A, Messina M, Elliot O, Chan J, Bhagat G, Chadburn A, et al. Analysis of the coding genome of diffuse large B-cell lymphoma. Nat Genet. Nature Publishing Group. 2011; 43:830-7. [cited 2013 Feb 5] [Internet] Available from: http://www.pubmedcentral. nih.gov/articlerender.fcgi?artid=3297422&tool=pmcen trez&rendertype=Abstract.
20. Ryan RJH, Nitta M, Borger D, Zukerberg LR, Ferry JA, Harris NL, Iafrate AJ, Bernstein BE, Sohani AR, Le LP. EZH2 codon 641 mutations are common in BCL2-rearranged germinal center B cell lymphomas. PLoS One. 2011; [cited 2014 May 6]; 6:e28585. [Internet] Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi ?artid=3237460&tool=pmcentrez&rendertype=Abstract.
21. Guo S, Chan JKC, Iqbal J, McKeithan T, Fu K, Meng B, Pan Y, Cheuk W, Luo D, Wang R, Zhang W, Greiner TC, Chan WC. EZH2 mutations in follicular lymphoma from different ethnic groups and associated gene expression alterations. Clin Cancer Res. 2014; [cited 2014 Jul 28]; 20:3078-86. [Internet] Available from: http://www.ncbi. nlm.nih.gov/pubmed/24634383.
22. Bohers E, Mareschal S, Bertrand P, Viailly PJ, Dubois S, Maingonnat C, Ruminy P, Tilly H, Jardin F. Activating somatic mutations in diffuse large B-cell lymphomas: lessons from next generation sequencing and key elements in the precision medicine era. Leuk Lymphoma. 2014; [cited 2014 Dec 4]; (May):1-10. [Internet] Available from: http://www.ncbi.nlm.nih.gov/pubmed/25130477.
23. Bödör C, Grossmann V. EZH2 mutations are frequent and represent an early event in follicular lymphoma. Blood. 2013; [cited 2014 Jul 31]; [cited 2014 Jul 31]; 122:3165-8. [Internet] Available from: http://bloodjournal.hematologylibrary. org/lookup/pmid?view=long&pmid=24052547.
24. Jiang Y, Redmond D, Nie K, Eng KW, Clozel T, Martin P, Tan LH, Melnick AM, Tam W, Elemento O. Deep sequencing reveals clonal evolution patterns and mutation events associated with relapse in B-cell lymphomas. Genome Biol. 2014; [cited 2014 Nov 18]; 15:432. [Internet] Available from: http://www.pubmedcentral.nih. gov/articlerender.fcgi?artid=4158101&tool=pmcentrez&r endertype=Abstract.
25. Lee HJ, Shin DH, Kim K Bin, Shin N, Park WY, Lee JH, Choi KU, Kim JY, Lee CH, Sol MY. Polycomb protein EZH2 expression in diffuse large B-cell lymphoma is associated with better prognosis in patients treated with rituximab, cyclophosphamide, doxorubicin, vincristine and prednisone. Leuk Lymphoma. 2014; [cited 2014 May 5]; 55:2056-63. [Internet] Available from: http://www.ncbi. nlm.nih.gov/pubmed/24304372.
26. Bodor C, O'Riain C, Wrench D, Matthews J, Iyengar S, Tayyib H, Calaminici M, Clear A, Iqbal S, Quentmeier H, Drexler H, Montoto S, Lister A, et al. EZH2 Y641 mutations in follicular lymphoma. Leukemia. 2011; 25:726-9.
27. Shen X, Liu Y, Hsu Y-J, Fujiwara Y, Kim J, Mao X, Yuan G-C, Orkin SH. EZH1 mediates methylation on histone H3 lysine 27 and complements EZH2 in maintaining stem cell identity and executing pluripotency. Mol Cell. 2008; [cited 2014 Jul 15]; 32:491-502. [Internet] Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi? artid=2630502&tool=pmcentrez&rendertype=Abstract.
28. Sahasrabuddhe A, Chen X, Chung F, Velusamy T, Lim MS, Elenitoba-Johnson KSJ. Oncogenic Y641 mutations in EZH2 prevent Jak2/β-TrCP-mediated degradation. Oncogene. Nature Publishing Group. 2014; [cited 2014 Oct 1];(August 2013) 1-10. [Internet] Available from: http://www.ncbi.nlm.nih.gov/pubmed/24469040.
29. Rizzardi AE, Johnson AT, Vogel RI, Pambuccian SE, Henriksen J, Skubitz AP, Metzger GJ, Schmechel SC. Quantitative comparison of immunohistochemical staining measured by digital image analysis versus pathologist visual scoring. Diagn Pathol. 2012; 7:42. [Internet] Available from: http://www.pubmedcentral.nih.gov/articlerender. fcgi?artid=3379953&tool=pmcentrez&renderty pe=Abstract.
30. Lohr JG, Stojanov P, Lawrence MS, Auclair D, Chapuy B, Sougnez C, Cruz-Gordillo P, Knoechel B, Asmann YW, Slager SL, Novak AJ, Dogan A, Ansell SM, et al. Discovery and prioritization of somatic mutations in diffuse large B-cell lymphoma (DLBCL) by whole-exome sequencing. Proc Natl Acad Sci U S A. 2012; [cited 2014 Oct 4]; 109:3879-84. [Internet] Available from: http://www. pubmedcentral.nih.gov/articlerender.fcgi?artid=3309757& tool=pmcentrez&rendertype=Abstract.
31. Morin RD, Mungall K, Pleasance E, Mungall AJ, Goya R, HuffRD, Scott DW, Ding J, Roth A, Chiu R, Corbett RD, Chan FC, Mendez-lago M, et al. Mutational and structural analysis of diffuse large B-cell lymphoma using wholegenome sequencing. Blood. 2013; 122:1256-66.
32. Turner CA, Mack DH, Davis MM. Pillars article: Blimp-1, a novel zinc finger-containing protein that can drive the maturation of B lymphocytes into immunoglobulin-secreting cells. 1994. J Immunol. 2010; 185:5-14. [Internet] Available from: http://www.ncbi.nlm.nih.gov/pubmed/20562267.
33. Velichutina I, Shaknovich R, Geng H, Johnson NA, Gascoyne RD, Melnick AM, Elemento O. EZH2-mediated epigenetic silencing in germinal center B cells contributes to proliferation and lymphomagenesis. Blood. 2010; [cited 2014 Oct 28]; 116:5247-55. [Internet] Available from: http://bloodjournal.hematologylibrary.org/content/116/24/5247.short.
34. Béguelin W, Popovic R, Teater M, Jiang Y. EZH2 is required for germinal center formation and somatic EZH2 mutations promote lymphoid transformation. Cancer Cell. 2013; 23:677-92. [Internet] Available from: http://www. sciencedirect.com/science/article/pii/S1535610813001797.
35. Zhao X, Lwin T, Zhang X, Huang a, Wang J, Marquez VE, Chen-Kiang S, Dalton WS, Sotomayor E, Tao J. Disruption of the MYC-miRNA-EZH2 loop to suppress aggressive B-cell lymphoma survival and clonogenicity. Leukemia. 2013; [cited 2014 Sep 4]; 27:2341-50. [Internet] Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi? artid=4015113&tool=pmcentrez&rendertype=Abstract.
36. Sander S, Bullinger L, Klapproth K, Fiedler K, Kestler HA, Barth TFE, Möller P, Stilgenbauer S, Pollack JR, Wirth T. MYC stimulates EZH2 expression by repression of its negative regulator miR-26a. Blood. 2008; [cited 2014 Sep 4]; 112:4202-12. [Internet] Available from: http://bloodjournal. hematologylibrary.org/content/112/10/4202.short.
37. Berg T, Thoene S, Yap D, Wee T, Schoeler N, Roste P, Lim E, Bilenky M, Mungall AJ, Oellerich T, Lee S, Lai CK, Umlandt P, et al. A transgenic mouse model demonstrating the oncogenic role of mutations in the polycomb-group gene EZH2 in lymphomagenesis. Blood. 2014; 123:3914-25. [Internet] Available from: http://bloodjournal.hematologylibrary. org/content/early/2014/05/06/blood-2012-12-473439.short.
38. Mareschal S, Lanic H, Ruminy P, Bastard C, Tilly H, Jardin F. The proportion of activated B-cell like subtype among de novo diffuse large B-cell lymphoma increases with age. Haematologica. 2011; [cited 2014 Oct 15]; 96:1888-90. [Internet] Available from: http://www.haematologica. org/content/96/12/1888.
39. Klapper W, Kreuz M, Kohler C, Burkhardt B, Szczepanowski M, Salaverria I, Hummel M, Loeffler M, Pillizzery S, Woessmann W, Schwänen C, Trümper L, Wessendorf S, et al. Patient age at diagnosis is associated with the molecular characteristics of diffuse large B-cell lymphoma. Blood. 2012; [cited 2014 Sep 1]; 119:1882-7. [Internet] Available from: http://bloodjournal.hematologylibrary. org/content/119/8/1882.short.