Follicular lymphoma, a B cell malignancy addicted to epigenetic mutations

References

• Czuczman MS, Weaver R, Alkuzweny B, Berlfein J, Grillo-Lopez AJ. Prolonged clinical and molecular remission in patients with low-grade or follicular non-Hodgkin's lymphoma treated with rituximab plus CHOP chemotherapy: 9-year follow-up. J Clin Oncol 2004; 22:4711-6; PMID:15483015; https://doi.org/10.1200/JCO.2004.04.020
   PubMed Web of Science ®Google Scholar
• Al-Tourah AJ, Gill KK, Chhanabhai M, Hoskins PJ, Klasa RJ, Savage KJ, Sehn LH, Shenkier TN, Gascoyne RD, Connors JM. Population-based analysis of incidence and outcome of transformed non-Hodgkin's lymphoma. J Clin Oncol 2008; 26:5165-9; PMID:18838711; https://doi.org/10.1200/JCO.2008.16.0283
   PubMed Web of Science ®Google Scholar
• Montoto S, Davies AJ, Matthews J, Calaminici M, Norton AJ, Amess J, Vinnicombe S, Waters R, Rohatiner AZ, Lister TA. Risk and clinical implications of transformation of follicular lymphoma to diffuse large B-cell lymphoma. J Clin Oncol 2007; 25:2426-33; PMID:17485708; https://doi.org/10.1200/JCO.2006.09.3260
   PubMed Web of Science ®Google Scholar
• Tsujimoto Y, Cossman J, Jaffe E, Croce CM. Involvement of the bcl-2 gene in human follicular lymphoma. Science 1985; 228:1440-3; PMID:3874430; https://doi.org/10.1126/science.3874430
   PubMed Web of Science ®Google Scholar
• Yunis JJ, Oken MM, Kaplan ME, Ensrud KM, Howe RR, Theologides A. Distinctive chromosomal abnormalities in histologic subtypes of non-Hodgkin's lymphoma. N Engl J Med 1982; 307:1231-6; PMID:7133054; https://doi.org/10.1056/NEJM198211113072002
   PubMed Web of Science ®Google Scholar
• Horsman DE, Gascoyne RD, Coupland RW, Coldman AJ, Adomat SA. Comparison of cytogenetic analysis, southern analysis, and polymerase chain reaction for the detection of t(14; 18) in follicular lymphoma. Am J Clin Pathol 1995; 103:472-8; PMID:7726146; https://doi.org/10.1093/ajcp/103.4.472
   PubMed Web of Science ®Google Scholar
• Weiss LM, Warnke RA, Sklar J, Cleary ML. Molecular analysis of the t(14;18) chromosomal translocation in malignant lymphomas. N Engl J Med 1987; 317:1185-9; PMID:3657890; https://doi.org/10.1056/NEJM198711053171904
   PubMed Web of Science ®Google Scholar
• Limpens J, Stad R, Vos C, de Vlaam C, de Jong D, van Ommen GJ, Schuuring E, Kluin PM. Lymphoma-associated translocation t(14;18) in blood B cells of normal individuals. Blood 1995; 85:2528-36. PMID:7727781.
   PubMed Web of Science ®Google Scholar
• Roulland S, Lebailly P, Lecluse Y, Heutte N, Nadel B, Gauduchon P. Long-term clonal persistence and evolution of t(14;18)-bearing B cells in healthy individuals. Leukemia 2006; 20:158-62; PMID:16307019; https://doi.org/10.1038/sj.leu.2404035
   PubMed Web of Science ®Google Scholar
• Horsman DE, Okamoto I, Ludkovski O, Le N, Harder L, Gesk S, Siebert R, Chhanabhai M, Sehn L, Connors JM, et al. Follicular lymphoma lacking the t(14;18)(q32;q21): identification of two disease subtypes. Br J Haematol 2003; 120:424-33; PMID:12580956; https://doi.org/10.1046/j.1365-2141.2003.04086.x
   PubMed Web of Science ®Google Scholar
• Kuppers R, Klein U, Hansmann ML, Rajewsky K. Cellular origin of human B-cell lymphomas. N Engl J Med 1999; 341:1520-9; PMID:10559454; https://doi.org/10.1056/NEJM199911113412007
   PubMed Web of Science ®Google Scholar
• Skibola CF, Berndt SI, Vijai J, Conde L, Wang Z, Yeager M, de Bakker PI, Birmann BM, Vajdic CM, Foo JN, et al. Genome-wide association study identifies five susceptibility loci for follicular lymphoma outside the HLA region. Am J Hum Genet 2014; 95:462-71; PMID:25279986; https://doi.org/10.1016/j.ajhg.2014.09.004
   PubMed Web of Science ®Google Scholar
• Cheung KJ, Shah SP, Steidl C, Johnson N, Relander T, Telenius A, Lai B, Murphy KP, Lam W, Al-Tourah AJ, et al. Genome-wide profiling of follicular lymphoma by array comparative genomic hybridization reveals prognostically significant DNA copy number imbalances. Blood 2009; 113:137-48; PMID:18703704; https://doi.org/10.1182/blood-2008-02-140616
   PubMed Web of Science ®Google Scholar
• Horsman DE, Connors JM, Pantzar T, Gascoyne RD. Analysis of secondary chromosomal alterations in 165 cases of follicular lymphoma with t(14;18). Genes Chromosomes Cancer 2001; 30:375-82; PMID:11241790; https://doi.org/10.1002/gcc.1103
   PubMed Web of Science ®Google Scholar
• Johnson NA, Al-Tourah A, Brown CJ, Connors JM, Gascoyne RD, Horsman DE. Prognostic significance of secondary cytogenetic alterations in follicular lymphomas. Genes Chromosomes Cancer 2008; 47:1038-48; https://doi.org/10.1002/gcc.20606
   PubMed Web of Science ®Google Scholar
• Schwaenen C, Viardot A, Berger H, Barth TF, Bentink S, Dohner H, Enz M, Feller AC, Hansmann ML, Hummel M, et al. Microarray-based genomic profiling reveals novel genomic aberrations in follicular lymphoma which associate with patient survival and gene expression status. Genes Chromosomes Cancer 2009; 48:39-54; PMID:18828156; https://doi.org/10.1002/gcc.20617
   PubMed Web of Science ®Google Scholar
• Glas AM, Kersten MJ, Delahaye LJ, Witteveen AT, Kibbelaar RE, Velds A, Wessels LF, Joosten P, Kerkhoven RM, Bernards R, et al. Gene expression profiling in follicular lymphoma to assess clinical aggressiveness and to guide the choice of treatment. Blood 2005; 105:301-7; PMID:15345589; https://doi.org/10.1182/blood-2004-06-2298
   PubMed Web of Science ®Google Scholar
• Husson H, Carideo EG, Neuberg D, Schultze J, Munoz O, Marks PW, Donovan JW, Chillemi AC, O'Connell P, Freedman AS. Gene expression profiling of follicular lymphoma and normal germinal center B cells using cDNA arrays. Blood 2002; 99:282-9; PMID:11756183; https://doi.org/10.1182/blood.V99.1.282
   PubMed Web of Science ®Google Scholar
• Dave SS, Wright G, Tan B, Rosenwald A, Gascoyne RD, Chan WC, Fisher RI, Braziel RM, Rimsza LM, Grogan TM, et al. Prediction of survival in follicular lymphoma based on molecular features of tumor-infiltrating immune cells. N Engl J Med 2004; 351:2159-69; PMID:15548776; https://doi.org/10.1056/NEJMoa041869
   PubMed Web of Science ®Google Scholar
• Roehle A, Hoefig KP, Repsilber D, Thorns C, Ziepert M, Wesche KO, Thiere M, Loeffler M, Klapper W, Pfreundschuh M, et al. MicroRNA signatures characterize diffuse large B-cell lymphomas and follicular lymphomas. Br J Haematol 2008; 142:732-44; PMID:18537969; https://doi.org/10.1111/j.1365-2141.2008.07237.x
   PubMed Web of Science ®Google Scholar
• Wang W, Corrigan-Cummins M, Hudson J, Maric I, Simakova O, Neelapu SS, Kwak LW, Janik JE, Gause B, Jaffe ES, et al. MicroRNA profiling of follicular lymphoma identifies microRNAs related to cell proliferation and tumor response. Haematologica 2012; 97:586-94; PMID:22102710; https://doi.org/10.3324/haematol.2011.048132
   PubMed Web of Science ®Google Scholar
• Kridel R, Sehn LH, Gascoyne RD. Pathogenesis of follicular lymphoma. J Clin Invest 2012; 122:3424-31; PMID:23023713; https://doi.org/10.1172/JCI63186
   PubMed Web of Science ®Google Scholar
• Morin RD, Johnson NA, Severson TM, Mungall AJ, An J, Goya R, Paul JE, Boyle M, Woolcock BW, Kuchenbauer F, et al. Somatic mutations altering EZH2 (Tyr641) in follicular and diffuse large B-cell lymphomas of germinal-center origin. Nat Genet 2010; 42:181-5; PMID:20081860; https://doi.org/10.1038/ng.518
   PubMed Web of Science ®Google Scholar
• Morin RD, Mendez-Lago M, Mungall AJ, Goya R, Mungall KL, Corbett RD, Johnson NA, Severson TM, Chiu R, Field M, et al. Frequent mutation of histone-modifying genes in non-Hodgkin lymphoma. Nature 2011; 476:298-303; PMID:21796119; https://doi.org/10.1038/nature10351
   PubMed Web of Science ®Google Scholar
• Okosun J, Bodor C, Wang J, Araf S, Yang CY, Pan C, Boller S, Cittaro D, Bozek M, Iqbal S, et al. Integrated genomic analysis identifies recurrent mutations and evolution patterns driving the initiation and progression of follicular lymphoma. Nat Genet 2014; 46:176-81; PMID:24362818; https://doi.org/10.1038/ng.2856
   PubMed Web of Science ®Google Scholar
• Pasqualucci L, Dominguez-Sola D, Chiarenza A, Fabbri G, Grunn A, Trifonov V, Kasper LH, Lerach S, Tang H, Ma J, et al. Inactivating mutations of acetyltransferase genes in B-cell lymphoma. Nature 2011; 471:189-95; PMID:21390126; https://doi.org/10.1038/nature09730
   PubMed Web of Science ®Google Scholar
• Pasqualucci L, Khiabanian H, Fangazio M, Vasishtha M, Messina M, Holmes AB, Ouillette P, Trifonov V, Rossi D, Tabbo F, et al. Genetics of follicular lymphoma transformation. Cell Reports 2014; 6:130-40; PMID:24388756; https://doi.org/10.1016/j.celrep.2013.12.027
   PubMed Web of Science ®Google Scholar
• Bodor C, Grossmann V, Popov N, Okosun J, O'Riain C, Tan K, Marzec J, Araf S, Wang J, Lee AM, et al. EZH2 mutations are frequent and represent an early event in follicular lymphoma. Blood 2013; 122:3165-8; PMID:24052547; https://doi.org/10.1182/blood-2013-04-496893
   PubMed Web of Science ®Google Scholar
• Bouska A, Zhang W, Gong Q, Iqbal J, Scuto A, Vose J, Ludvigsen M, Fu K, Weisenburger DD, Greiner TC, et al. Combined copy number and mutation analysis identifies oncogenic pathways associated with transformation of follicular lymphoma. Leukemia 2017; 31:83-91; PMID:27389057; https://doi.org/10.1038/leu.2016.175
   PubMed Web of Science ®Google Scholar
• Green MR, Gentles AJ, Nair RV, Irish JM, Kihira S, Liu CL, Kela I, Hopmans ES, Myklebust JH, Ji H, et al. Hierarchy in somatic mutations arising during genomic evolution and progression of follicular lymphoma. Blood 2013; 121:1604-11; PMID:23297126; https://doi.org/10.1182/blood-2012-09-457283
   PubMed Web of Science ®Google Scholar
• Li H, Kaminski MS, Li Y, Yildiz M, Ouillette P, Jones S, Fox H, Jacobi K, Saiya-Cork K, Bixby D, et al. Mutations in linker histone genes HIST1H1 B, C, D, and E; OCT2 (POU2F2); IRF8; and ARID1A underlying the pathogenesis of follicular lymphoma. Blood 2014; 123:1487-98; PMID:24435047; https://doi.org/10.1182/blood-2013-05-500264
   PubMed Web of Science ®Google Scholar
• Krysiak K, Gomez F, White BS, Matlock M, Miller CA, Trani L, Fronick CC, Fulton RS, Kreisel F, Cashen AF, et al. Recurrent somatic mutations affecting B-cell receptor signaling pathway genes in follicular lymphoma. Blood 2017; 129:473-83; PMID:28064239; https://doi.org/10.1182/blood-2016-07-729954
   PubMedGoogle Scholar
• Timp W, Feinberg AP. Cancer as a dysregulated epigenome allowing cellular growth advantage at the expense of the host. Nat Rev Cancer 2013; 13:497-510; PMID:23760024; https://doi.org/10.1038/nrc3486
   PubMed Web of Science ®Google Scholar
• Pastore A, Jurinovic V, Kridel R, Hoster E, Staiger AM, Szczepanowski M, Pott C, Kopp N, Murakami M, Horn H, et al. Integration of gene mutations in risk prognostication for patients receiving first-line immunochemotherapy for follicular lymphoma: a retrospective analysis of a prospective clinical trial and validation in a population-based registry. Lancet Oncol 2015; 16:1111-22; PMID:26256760; https://doi.org/10.1016/S1470-2045(15)00169-2
   PubMed Web of Science ®Google Scholar
• Lohr JG, Stojanov P, Lawrence MS, Auclair D, Chapuy B, Sougnez C, Cruz-Gordillo P, Knoechel B, Asmann YW, Slager SL, 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; 109:3879-84; PMID:22343534; https://doi.org/10.1073/pnas.1121343109
   PubMed Web of Science ®Google Scholar
• Pasqualucci L, Trifonov V, Fabbri G, Ma J, Rossi D, Chiarenza A, Wells VA, Grunn A, Messina M, Elliot O, et al. Analysis of the coding genome of diffuse large B-cell lymphoma. Nat Genet 2011; 43:830-7; PMID:21804550; https://doi.org/10.1038/ng.892
   PubMed Web of Science ®Google Scholar
• Love C, Sun Z, Jima D, Li G, Zhang J, Miles R, Richards KL, Dunphy CH, Choi WW, Srivastava G, et al. The genetic landscape of mutations in Burkitt lymphoma. Nat Genet 2012; 44:1321-5; PMID:23143597; https://doi.org/10.1038/ng.2468
   PubMed Web of Science ®Google Scholar
• Louissaint A, Jr., Schafernak KT, Geyer JT, Kovach AE, Ghandi M, Gratzinger D, Roth CG, Paxton CN, Kim S, Namgyal C, et al. Pediatric-type nodal follicular lymphoma: a biologically distinct lymphoma with frequent MAPK pathway mutations. Blood 2016; 128:1093-100; PMID:27325104; https://doi.org/10.1182/blood-2015-12-682591
   PubMed Web of Science ®Google Scholar
• Schmidt J, Gong S, Marafioti T, Mankel B, Gonzalez-Farre B, Balague O, Mozos A, Cabecadas J, van der Walt J, Hoehn D, et al. Genome-wide analysis of pediatric-type follicular lymphoma reveals low genetic complexity and recurrent alterations of TNFRSF14 gene. Blood 2016; 128:1101-11; PMID:27257180; https://doi.org/10.1182/blood-2016-03-703819
   PubMed Web of Science ®Google Scholar
• Weigert O, Weinstock DM. The evolving contribution of hematopoietic progenitor cells to lymphomagenesis. Blood 2012; 120:2553-61; PMID:22869790; https://doi.org/10.1182/blood-2012-05-414995
   PubMed Web of Science ®Google Scholar
• Martinez-Climent JA, Fontan L, Gascoyne RD, Siebert R, Prosper F. Lymphoma stem cells: enough evidence to support their existence? Haematologica 2010; 95:293-302; PMID:20139392; https://doi.org/10.3324/haematol.2009.013318
   PubMed Web of Science ®Google Scholar
• Okosun J, Montoto S, Fitzgibbon J. The routes for transformation of follicular lymphoma. Curr Opin Hematol 2016; 23:385-91; PMID:27135979; https://doi.org/10.1097/MOH.0000000000000255
   PubMed Web of Science ®Google Scholar
• Carlotti E, Wrench D, Matthews J, Iqbal S, Davies A, Norton A, Hart J, Lai R, Montoto S, Gribben JG, et al. Transformation of follicular lymphoma to diffuse large B-cell lymphoma may occur by divergent evolution from a common progenitor cell or by direct evolution from the follicular lymphoma clone. Blood 2009; 113:3553-7; PMID:19202129; https://doi.org/10.1182/blood-2008-08-174839
   PubMed Web of Science ®Google Scholar
• Weigert O, Kopp N, Lane AA, Yoda A, Dahlberg SE, Neuberg D, Bahar AY, Chapuy B, Kutok JL, Longtine JA, et al. Molecular ontogeny of donor-derived follicular lymphomas occurring after hematopoietic cell transplantation. Cancer discovery 2012; 2:47-55; PMID:22585168; https://doi.org/10.1158/2159-8290.CD-11-0208
   PubMed Web of Science ®Google Scholar
• Mar N, Digiuseppe JA, Dailey ME. Rubinstein-Taybi syndrome - a window into follicular lymphoma biology. Leukemia & lymphoma 2016; 57:2908-10; PMID:27086936; https://doi.org/10.3109/10428194.2016.1165816
   PubMed Web of Science ®Google Scholar
• Ortega-Molina A, Boss IW, Canela A, Pan H, Jiang Y, Zhao C, Jiang M, Hu D, Agirre X, Niesvizky I, et al. The histone lysine methyltransferase KMT2D sustains a gene expression program that represses B cell lymphoma development. Nat Med 2015; 21:1199-208; PMID:26366710; https://doi.org/10.1038/nm.3943
   PubMed Web of Science ®Google Scholar
• Zhang J, Dominguez-Sola D, Hussein S, Lee JE, Holmes AB, Bansal M, Vlasevska S, Mo T, Tang H, Basso K, et al. Disruption of KMT2D perturbs germinal center B cell development and promotes lymphomagenesis. Nat Med 2015; 21:1190-8; PMID:26366712; https://doi.org/10.1038/nm.3940
   PubMed Web of Science ®Google Scholar
• Bodor C, O'Riain C, Wrench D, Matthews J, Iyengar S, Tayyib H, Calaminici M, Clear A, Iqbal S, Quentmeier H, et al. EZH2 Y641 mutations in follicular lymphoma. Leukemia 2011; 25:726-9; PMID:21233829; https://doi.org/10.1038/leu.2010.311
   PubMed Web of Science ®Google Scholar
• Yap DB, Chu J, Berg T, Schapira M, Cheng SW, Moradian A, Morin RD, Mungall AJ, Meissner B, Boyle M, 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; PMID:21190999; https://doi.org/10.1182/blood-2010-11-321208
   PubMed Web of Science ®Google Scholar
• Beguelin W, Popovic R, Teater M, Jiang Y, Bunting KL, Rosen M, Shen H, Yang SN, Wang L, Ezponda T, et al. EZH2 is required for germinal center formation and somatic EZH2 mutations promote lymphoid transformation. Cancer Cell 2013; 23:677-92; PMID:23680150; https://doi.org/10.1016/j.ccr.2013.04.011
   PubMed Web of Science ®Google Scholar
• Caganova M, Carrisi C, Varano G, Mainoldi F, Zanardi F, Germain PL, George L, Alberghini F, Ferrarini L, Talukder AK, et al. Germinal center dysregulation by histone methyltransferase EZH2 promotes lymphomagenesis. J Clin Invest 2013; 123:5009-22; PMID:24200695; https://doi.org/10.1172/JCI70626
   PubMed Web of Science ®Google Scholar
• 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; 116:5247-55; PMID:20736451; https://doi.org/10.1182/blood-2010-04-280149
   PubMed Web of Science ®Google Scholar
• Green MR, Kihira S, Liu CL, Nair RV, Salari R, Gentles AJ, Irish J, Stehr H, Vicente-Duenas C, Romero-Camarero I, et al. Mutations in early follicular lymphoma progenitors are associated with suppressed antigen presentation. Proc Natl Acad Sci U S A 2015; 112:E1116-25; PMID:25713363; https://doi.org/10.1073/pnas.1501199112
   PubMed Web of Science ®Google Scholar
• Jiang Y, Ortega-Molina A, Geng H, Ying HY, Hatzi K, Parsa S, McNally D, Wang L, Doane AS, Agirre X, et al. CREBBP Inactivation Promotes the Development of HDAC3-Dependent Lymphomas. Cancer Discovery 2017; 7:38-53; PMID:27733359; https://doi.org/10.1158/2159-8290.CD-16-0975
   PubMed Web of Science ®Google Scholar
• Kretzmer H, Bernhart SH, Wang W, Haake A, Weniger MA, Bergmann AK, Betts MJ, Carrillo-de-Santa-Pau E, Doose G, Gutwein J, et al. DNA methylome analysis in Burkitt and follicular lymphomas identifies differentially methylated regions linked to somatic mutation and transcriptional control. Nat Genet 2015; 47:1316-25; PMID:26437030; https://doi.org/10.1038/ng.3413
   PubMed Web of Science ®Google Scholar
• Koues OI, Kowalewski RA, Chang LW, Pyfrom SC, Schmidt JA, Luo H, Sandoval LE, Hughes TB, Bednarski JJ, Cashen AF, et al. Enhancer sequence variants and transcription-factor deregulation synergize to construct pathogenic regulatory circuits in B-cell lymphoma. Immunity 2015; 42:186-98; PMID:25607463; https://doi.org/10.1016/j.immuni.2014.12.021
   PubMed Web of Science ®Google Scholar
• Solal-Celigny P, Roy P, Colombat P, White J, Armitage JO, Arranz-Saez R, Au WY, Bellei M, Brice P, Caballero D, et al. Follicular lymphoma international prognostic index. Blood 2004; 104:1258-65; PMID:15126323; https://doi.org/10.1182/blood-2003-12-4434
   PubMed Web of Science ®Google Scholar
• Buske C, Hoster E, Dreyling M, Hasford J, Unterhalt M, Hiddemann W. The Follicular Lymphoma International Prognostic Index (FLIPI) separates high-risk from intermediate- or low-risk patients with advanced-stage follicular lymphoma treated front-line with rituximab and the combination of cyclophosphamide, doxorubicin, vincristine, and prednisone (R-CHOP) with respect to treatment outcome. Blood 2006; 108:1504-8; PMID:16690968; https://doi.org/10.1182/blood-2006-01-013367
   PubMed Web of Science ®Google Scholar
• Knutson SK, Wigle TJ, Warholic NM, Sneeringer CJ, Allain CJ, Klaus CR, Sacks JD, Raimondi A, Majer CR, Song J, et al. A selective inhibitor of EZH2 blocks H3K27 methylation and kills mutant lymphoma cells. Nat Chem Biol 2012; 8:890-6. PMID:23023262; https://doi.org/10.1038/nchembio.1084
   PubMed Web of Science ®Google Scholar
• McCabe MT, Ott HM, Ganji G, Korenchuk S, Thompson C, Van Aller GS, Liu Y, Graves AP, Della Pietra A, 3rd Diaz E, et al. EZH2 inhibition as a therapeutic strategy for lymphoma with EZH2-activating mutations. Nature 2012; 492:108-12; PMID:23051747; https://doi.org/10.1038/nature11606
   PubMed Web of Science ®Google Scholar
• Verma SK, Tian X, LaFrance LV, Duquenne C, Suarez DP, Newlander KA, Romeril SP, Burgess JL, Grant SW, Brackley JA, et al. Identification of Potent, Selective, Cell-Active Inhibitors of the Histone Lysine Methyltransferase EZH2. ACS Medicinal Chem Lett 2012; 3:1091-6; PMID:24900432; https://doi.org/10.1021/ml3003346
   PubMed Web of Science ®Google Scholar
• Knutson SK, Warholic NM, Wigle TJ, Klaus CR, Allain CJ, Raimondi A, Porter Scott M, Chesworth R, Moyer MP, Copeland RA, et al. Durable tumor regression in genetically altered malignant rhabdoid tumors by inhibition of methyltransferase EZH2. Proc Natl Acad Sci U S A 2013; 110:7922-7; PMID:23620515; https://doi.org/10.1073/pnas.1303800110
   PubMed Web of Science ®Google Scholar
• Vaswani RG, Gehling VS, Dakin LA, Cook AS, Nasveschuk CG, Duplessis M, Iyer P, Balasubramanian S, Zhao F, Good AC, et al. Identification of (R)-N-((4-Methoxy-6-methyl-2-oxo-1,2-dihydropyridin-3-yl)methyl)-2-methyl-1-(1-(1 -(2,2,2-trifluoroethyl)piperidin-4-yl)ethyl)-1H-indole-3-carboxamide (CPI-1205), a Potent and Selective Inhibitor of Histone Methyltransferase EZH2, Suitable for Phase I Clinical Trials for B-Cell Lymphomas. J Medicinal Chem 2016; 59:9928-41; PMID:27739677; https://doi.org/10.1021/acs.jmedchem.6b01315
   PubMed Web of Science ®Google Scholar
• Kim KH, Roberts CW. Targeting EZH2 in cancer. Nat Med 2016; 22:128-34; PMID:26845405; https://doi.org/10.1038/nm.4036
   PubMed Web of Science ®Google Scholar
• Kim KH, Kim W, Howard TP, Vazquez F, Tsherniak A, Wu JN, Wang W, Haswell JR, Walensky LD, Hahn WC, et al. SWI/SNF-mutant cancers depend on catalytic and non-catalytic activity of EZH2. Nat Med 2015; 21:1491-6; PMID:26552009; https://doi.org/10.1038/nm.3968
   PubMed Web of Science ®Google Scholar
• Scott MT, Korfi K, Saffrey P, Hopcroft LE, Kinstrie R, Pellicano F, Guenther C, Gallipoli P, Cruz M, Dunn K, et al. Epigenetic Reprogramming Sensitizes CML Stem Cells to Combined EZH2 and Tyrosine Kinase Inhibition. Cancer discovery 2016; 6:1248-57; PMID:27630125; https://doi.org/10.1158/2159-8290.CD-16-0263
   PubMed Web of Science ®Google Scholar
• Xie H, Peng C, Huang J, Li BE, Kim W, Smith EC, Fujiwara Y, Qi J, Cheloni G, Das PP, et al. Chronic Myelogenous Leukemia- Initiating Cells Require Polycomb Group Protein EZH2. Cancer discovery 2016; 6:1237-47; PMID:27630126; https://doi.org/10.1158/2159-8290.CD-15-1439
   PubMed Web of Science ®Google Scholar
• Olsen EA, Kim YH, Kuzel TM, Pacheco TR, Foss FM, Parker S, Frankel SR, Chen C, Ricker JL, Arduino JM, et al. Phase IIb multicenter trial of vorinostat in patients with persistent, progressive, or treatment refractory cutaneous T-cell lymphoma. J Clin Oncol 2007; 25:3109-15; PMID:17577020; https://doi.org/10.1200/JCO.2006.10.2434
   PubMed Web of Science ®Google Scholar
• Ogura M, Ando K, Suzuki T, Ishizawa K, Oh SY, Itoh K, Yamamoto K, Au WY, Tien HF, Matsuno Y, et al. A multicentre phase II study of vorinostat in patients with relapsed or refractory indolent B-cell non-Hodgkin lymphoma and mantle cell lymphoma. Br J Haematol 2014; 165:768-76; PMID:24617454; https://doi.org/10.1111/bjh.12819
   PubMed Web of Science ®Google Scholar
• Kirschbaum M, Frankel P, Popplewell L, Zain J, Delioukina M, Pullarkat V, Matsuoka D, Pulone B, Rotter AJ, Espinoza-Delgado I, et al. Phase II study of vorinostat for treatment of relapsed or refractory indolent non-Hodgkin's lymphoma and mantle cell lymphoma. J Clin Oncol 2011; 29:1198-203; PMID:21300924; https://doi.org/10.1200/JCO.2010.32.1398
   PubMed Web of Science ®Google Scholar
• Assouline SE, Nielsen TH, Yu S, Alcaide M, Chong L, MacDonald D, Tosikyan A, Kukreti V, Kezouh A, Petrogiannis-Haliotis T, et al. Phase 2 study of panobinostat with or without rituximab in relapsed diffuse large B-cell lymphoma. Blood 2016; 128:185-94; PMID:27166360; https://doi.org/10.1182/blood-2016-02-699520
   PubMed Web of Science ®Google Scholar
• Bjornsson HT, Benjamin JS, Zhang L, Weissman J, Gerber EE, Chen YC, Vaurio RG, Potter MC, Hansen KD, Dietz HC. Histone deacetylase inhibition rescues structural and functional brain deficits in a mouse model of Kabuki syndrome. Sci Translational Med 2014; 6:256ra135; PMID:25273096; https://doi.org/10.1126/scitranslmed.3009278
   PubMed Web of Science ®Google Scholar
• Warrener R, Beamish H, Burgess A, Waterhouse NJ, Giles N, Fairlie D, Gabrielli B. Tumor cell-selective cytotoxicity by targeting cell cycle checkpoints. FASEB J 2003; 17:1550-2. PMID:12824307; https://doi.org/10.1096/fj.02-1003fje
   PubMed Web of Science ®Google Scholar
• Frew AJ, Johnstone RW, Bolden JE. Enhancing the apoptotic and therapeutic effects of HDAC inhibitors. Cancer Lett 2009; 280:125-33; PMID:19359091; https://doi.org/10.1016/j.canlet.2009.02.042
   PubMed Web of Science ®Google Scholar
• Scuto A, Kirschbaum M, Kowolik C, Kretzner L, Juhasz A, Atadja P, Pullarkat V, Bhatia R, Forman S, Yen Y, et al. The novel histone deacetylase inhibitor, LBH589, induces expression of DNA damage response genes and apoptosis in Ph- acute lymphoblastic leukemia cells. Blood 2008; 111:5093-100; PMID:18349321; https://doi.org/10.1182/blood-2007-10-117762
   PubMed Web of Science ®Google Scholar
• Ellis L, Hammers H, Pili R. Targeting tumor angiogenesis with histone deacetylase inhibitors. Cancer Lett 2009; 280:145-53; PMID:19111391; https://doi.org/10.1016/j.canlet.2008.11.012
   PubMed Web of Science ®Google Scholar
• Maeda T, Towatari M, Kosugi H, Saito H. Up-regulation of costimulatory/adhesion molecules by histone deacetylase inhibitors in acute myeloid leukemia cells. Blood 2000; 96:3847-56. PMID:11090069
   PubMed Web of Science ®Google Scholar
• Harris WJ, Huang X, Lynch JT, Spencer GJ, Hitchin JR, Li Y, Ciceri F, Blaser JG, Greystoke BF, Jordan AM, et al. The histone demethylase KDM1A sustains the oncogenic potential of MLL-AF9 leukemia stem cells. Cancer Cell 2012; 21:473-87; PMID:22464800; https://doi.org/10.1016/j.ccr.2012.03.014
   PubMed Web of Science ®Google Scholar
• Maes T, Tirapu I, Mascaro C, Ortega A, Estiarte A, Valls N, Castro-Palomino J, Arjol CB, Kurz G. Preclinical characterization of a potent and selective inhibitor of the histone demethylase KDM1A for MLL leukemia. J Clin Oncol 2013; 31:1; PMID:23129739; https://doi.org/10.1200/JCO.2012.44.8589
   PubMed Web of Science ®Google Scholar
• Mohammad H, Smitheman K, Van Aller G, Cusan M, Kamat S, Liu Y, Johnson N, Hann C, Armstrong S, Kruger R. Novel anti-tumor activity of targeted LSD1 inhibition by GSK2879552. Eur J Cancer 2014; 50:72; https://doi.org/10.1016/S0959-8049(14)70338-7
   Web of Science ®Google Scholar
• Hancock RL, Dunne K, Walport LJ, Flashman E, Kawamura A. Epigenetic regulation by histone demethylases in hypoxia. Epigenomics 2015; 7:791-811; PMID:25832587; https://doi.org/10.2217/epi.15.24
   PubMed Web of Science ®Google Scholar
• Maes T, Carceller E, Salas J, Ortega A, Buesa C. Advances in the development of histone lysine demethylase inhibitors. Curr Opin Pharmacol 2015; 23:52-60; PMID:26057211; https://doi.org/10.1016/j.coph.2015.05.009
   PubMed Web of Science ®Google Scholar
• Vinogradova M, Gehling VS, Gustafson A, Arora S, Tindell CA, Wilson C, Williamson KE, Guler GD, Gangurde P, Manieri W, et al. An inhibitor of KDM5 demethylases reduces survival of drug-tolerant cancer cells. Nat Chem Biol 2016; 12:531-8; PMID:27214401; https://doi.org/10.1038/nchembio.2085
   PubMed Web of Science ®Google Scholar
• Horton JR, Liu X, Gale M, Wu L, Shanks JR, Zhang X, Webber PJ, Bell JS, Kales SC, Mott BT, et al. Structural Basis for KDM5A Histone Lysine Demethylase Inhibition by Diverse Compounds. Cell Chem Biol 2016; 23:769-81; PMID:27427228; https://doi.org/10.1016/j.chembiol.2016.06.006
   PubMed Web of Science ®Google Scholar
• Chen R, Frankel P, Popplewell L, Siddiqi T, Ruel N, Rotter A, Thomas SH, Mott M, Nathwani N, Htut M, et al. A phase II study of vorinostat and rituximab for treatment of newly diagnosed and relapsed/refractory indolent non-Hodgkin lymphoma. Haematologica 2015; 100:357-62; PMID:25596263; https://doi.org/10.3324/haematol.2014.117473
   PubMed Web of Science ®Google Scholar
• Evens AM, Balasubramanian S, Vose JM, Harb W, Gordon LI, Langdon R, Sprague J, Sirisawad M, Mani C, Yue J, et al. A Phase I/II Multicenter, Open-Label Study of the Oral Histone Deacetylase Inhibitor Abexinostat in Relapsed/Refractory Lymphoma. Clin Cancer Res 2016; 22:1059-66; PMID:26482040; https://doi.org/10.1158/1078-0432.CCR-15-0624
   PubMed Web of Science ®Google Scholar
• Younes A, Berdeja JG, Patel MR, Flinn I, Gerecitano JF, Neelapu SS, Kelly KR, Copeland AR, Akins A, Clancy MS, et al. Safety, tolerability, and preliminary activity of CUDC-907, a first-in-class, oral, dual inhibitor of HDAC and PI3K, in patients with relapsed or refractory lymphoma or multiple myeloma: an open-label, dose-escalation, phase 1 trial. Lancet Oncol 2016; 17:622-31; PMID:27049457; https://doi.org/10.1016/S1470-2045(15)00584-7
   PubMed Web of Science ®Google Scholar