A key role for EZH2 in epigenetic silencing of HOX genes in mantle cell lymphoma

References

• Rosenwald A, Wright G, Wiestner A, Chan WC, Connors JM, Campo E, Gascoyne RD, Grogan TM, Muller-Hermelink HK, Smeland EB, et al. The proliferation gene expression signature is a quantitative integrator of oncogenic events that predicts survival in mantle cell lymphoma. Cancer Cell 2003; 3:185 - 97; http://dx.doi.org/10.1016/S1535-6108(03)00028-X; PMID: 12620412
   PubMed Web of Science ®Google Scholar
• van Kemenade FJ, Raaphorst FM, Blokzijl T, Fieret E, Hamer KM, Satijn DP, Otte AP, Meijer CJ. Coexpression of BMI-1 and EZH2 polycomb-group proteins is associated with cycling cells and degree of malignancy in B-cell non-Hodgkin lymphoma. Blood 2001; 97:3896 - 901; http://dx.doi.org/10.1182/blood.V97.12.3896; PMID: 11389032
   PubMed Web of Science ®Google Scholar
• Visser HP, Gunster MJ, Kluin-Nelemans HC, Manders EM, Raaphorst FM, Meijer CJ, Willemze R, Otte AP. The Polycomb group protein EZH2 is upregulated in proliferating, cultured human mantle cell lymphoma. Br J Haematol 2001; 112:950 - 8; http://dx.doi.org/10.1046/j.1365-2141.2001.02641.x; PMID: 11298590
   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; http://dx.doi.org/10.1038/nature11606; PMID: 23051747
   PubMed Web of Science ®Google Scholar
• Fiskus W, Wang Y, Sreekumar A, Buckley KM, Shi H, Jillella A, Ustun C, Rao R, Fernandez P, Chen J, et al. Combined epigenetic therapy with the histone methyltransferase EZH2 inhibitor 3-deazaneplanocin A and the histone deacetylase inhibitor panobinostat against human AML cells. Blood 2009; 114:2733 - 43; http://dx.doi.org/10.1182/blood-2009-03-213496; PMID: 19638619
   PubMed Web of Science ®Google Scholar
• Simon JA, Lange CA. Roles of the EZH2 histone methyltransferase in cancer epigenetics. Mutat Res 2008; 647:21 - 9; http://dx.doi.org/10.1016/j.mrfmmm.2008.07.010; PMID: 18723033
   PubMed Web of Science ®Google Scholar
• Viré E, Brenner C, Deplus R, Blanchon L, Fraga M, Didelot C, Morey L, Van Eynde A, Bernard D, Vanderwinden JM, et al. The Polycomb group protein EZH2 directly controls DNA methylation. Nature 2006; 439:871 - 4; http://dx.doi.org/10.1038/nature04431; PMID: 16357870
   PubMed Web of Science ®Google Scholar
• Halldórsdóttir AM, Kanduri M, Marincevic M, Mansouri L, Isaksson A, Göransson H, Axelsson T, Agarwal P, Jernberg-Wiklund H, Stamatopoulos K, et al. Mantle cell lymphoma displays a homogenous methylation profile: a comparative analysis with chronic lymphocytic leukemia. Am J Hematol 2012; 87:361 - 7; http://dx.doi.org/10.1002/ajh.23115; PMID: 22374828
   PubMed Web of Science ®Google Scholar
• Sauvageau G, Lansdorp PM, Eaves CJ, Hogge DE, Dragowska WH, Reid DS, Largman C, Lawrence HJ, Humphries RK. Differential expression of homeobox genes in functionally distinct CD34+ subpopulations of human bone marrow cells. Proc Natl Acad Sci U S A 1994; 91:12223 - 7; http://dx.doi.org/10.1073/pnas.91.25.12223; PMID: 7527557
   PubMed Web of Science ®Google Scholar
• Akam M. Hox and HOM: homologous gene clusters in insects and vertebrates. Cell 1989; 57:347 - 9; http://dx.doi.org/10.1016/0092-8674(89)90909-4; PMID: 2566382
   PubMed Web of Science ®Google Scholar
• Argiropoulos B, Humphries RK. Hox genes in hematopoiesis and leukemogenesis. Oncogene 2007; 26:6766 - 76; http://dx.doi.org/10.1038/sj.onc.1210760; PMID: 17934484
   PubMed Web of Science ®Google Scholar
• Eklund EA. The role of HOX genes in myeloid leukemogenesis. Curr Opin Hematol 2006; 13:67 - 73; http://dx.doi.org/10.1097/01.moh.0000208467.63861.d6; PMID: 16456371
   PubMed Web of Science ®Google Scholar
• Novak P, Jensen T, Oshiro MM, Wozniak RJ, Nouzova M, Watts GS, Klimecki WT, Kim C, Futscher BW. Epigenetic inactivation of the HOXA gene cluster in breast cancer. Cancer Res 2006; 66:10664 - 70; http://dx.doi.org/10.1158/0008-5472.CAN-06-2761; PMID: 17090521
   PubMed Web of Science ®Google Scholar
• Strathdee G, Sim A, Soutar R, Holyoake TL, Brown R. HOXA5 is targeted by cell-type-specific CpG island methylation in normal cells and during the development of acute myeloid leukaemia. Carcinogenesis 2007; 28:299 - 309; http://dx.doi.org/10.1093/carcin/bgl133; PMID: 16861263
   PubMed Web of Science ®Google Scholar
• Nagel S, Venturini L, Marquez VE, Meyer C, Kaufmann M, Scherr M, MacLeod RA, Drexler HG. Polycomb repressor complex 2 regulates HOXA9 and HOXA10, activating ID2 in NK/T-cell lines. Mol Cancer 2010; 9:151; http://dx.doi.org/10.1186/1476-4598-9-151; PMID: 20565746
   PubMed Web of Science ®Google Scholar
• Wu X, Gong Y, Yue J, Qiang B, Yuan J, Peng X. Cooperation between EZH2, NSPc1-mediated histone H2A ubiquitination and Dnmt1 in HOX gene silencing. Nucleic Acids Res 2008; 36:3590 - 9; http://dx.doi.org/10.1093/nar/gkn243; PMID: 18460542
   PubMed Web of Science ®Google Scholar
• Di Vinci A, Casciano I, Marasco E, Banelli B, Ravetti GL, Borzì L, Brigati C, Forlani A, Dorcaratto A, Allemanni G, et al. Quantitative methylation analysis of HOXA3, 7, 9, and 10 genes in glioma: association with tumor WHO grade and clinical outcome. J Cancer Res Clin Oncol 2012; 138:35 - 47; http://dx.doi.org/10.1007/s00432-011-1070-5; PMID: 21947269
   PubMed Web of Science ®Google Scholar
• Strathdee G, Holyoake TL, Sim A, Parker A, Oscier DG, Melo JV, Meyer S, Eden T, Dickinson AM, Mountford JC, et al. Inactivation of HOXA genes by hypermethylation in myeloid and lymphoid malignancy is frequent and associated with poor prognosis. Clin Cancer Res 2007; 13:5048 - 55; http://dx.doi.org/10.1158/1078-0432.CCR-07-0919; PMID: 17785556
   PubMed Web of Science ®Google Scholar
• Tsai KW, Hu LY, Wu CW, Li SC, Lai CH, Kao HW, Fang WL, Lin WC. Epigenetic regulation of miR-196b expression in gastric cancer. Genes Chromosomes Cancer 2010; 49:969 - 80; http://dx.doi.org/10.1002/gcc.20804; PMID: 20662076
   PubMed Web of Science ®Google Scholar
• Schotte D, Lange-Turenhout EA, Stumpel DJ, Stam RW, Buijs-Gladdines JG, Meijerink JP, Pieters R, Den Boer ML. Expression of miR-196b is not exclusively MLL-driven but is especially linked to activation of HOXA genes in pediatric acute lymphoblastic leukemia. Haematologica 2010; 95:1675 - 82; http://dx.doi.org/10.3324/haematol.2010.023481; PMID: 20494936
   PubMed Web of Science ®Google Scholar
• Hutter G, Scheubner M, Zimmermann Y, Kalla J, Katzenberger T, Hübler K, Roth S, Hiddemann W, Ott G, Dreyling M. Differential effect of epigenetic alterations and genomic deletions of CDK inhibitors [p16(INK4a), p15(INK4b), p14(ARF)] in mantle cell lymphoma. Genes Chromosomes Cancer 2006; 45:203 - 10; http://dx.doi.org/10.1002/gcc.20277; PMID: 16258956
   PubMed Web of Science ®Google Scholar
• Pinyol M, Hernandez L, Cazorla M, Balbín M, Jares P, Fernandez PL, Montserrat E, Cardesa A, Lopez-Otín C, Campo E. Deletions and loss of expression of p16INK4a and p21Waf1 genes are associated with aggressive variants of mantle cell lymphomas. Blood 1997; 89:272 - 80; PMID: 8978301
   PubMed Web of Science ®Google Scholar
• Reynolds PA, Sigaroudinia M, Zardo G, Wilson MB, Benton GM, Miller CJ, Hong C, Fridlyand J, Costello JF, Tlsty TD. Tumor suppressor p16INK4A regulates polycomb-mediated DNA hypermethylation in human mammary epithelial cells. J Biol Chem 2006; 281:24790 - 802; http://dx.doi.org/10.1074/jbc.M604175200; PMID: 16766534
   PubMed Web of Science ®Google Scholar
• Jadayel DM, Lukas J, Nacheva E, Bartkova J, Stranks G, De Schouwer PJ, et al. Potential role for concurrent abnormalities of the cyclin D1, p16CDKN2 and p15CDKN2B genes in certain B cell non-Hodgkin's lymphomas. Functional studies in a cell line (Granta 519). Leukemia: official journal of the Leukemia Society of America. Leukemia Research Fund, UK 1997; 11:64 - 72; http://dx.doi.org/10.1038/sj.leu.2400555
   PubMed Web of Science ®Google Scholar
• Acharyya S, Sharma SM, Cheng AS, Ladner KJ, He W, Kline W, Wang H, Ostrowski MC, Huang TH, Guttridge DC. TNF inhibits Notch-1 in skeletal muscle cells by Ezh2 and DNA methylation mediated repression: implications in duchenne muscular dystrophy. PLoS One 2010; 5:e12479; http://dx.doi.org/10.1371/journal.pone.0012479; PMID: 20814569
   PubMed Web of Science ®Google Scholar
• Kalushkova A, Fryknäs M, Lemaire M, Fristedt C, Agarwal P, Eriksson M, Deleu S, Atadja P, Osterborg A, Nilsson K, et al. Polycomb target genes are silenced in multiple myeloma. PLoS One 2010; 5:e11483; http://dx.doi.org/10.1371/journal.pone.0011483; PMID: 20634887
   PubMed Web of Science ®Google Scholar
• Béguelin 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; http://dx.doi.org/10.1016/j.ccr.2013.04.011; PMID: 23680150
   PubMed Web of Science ®Google Scholar
• Zhang X, Zhao X, Fiskus W, Lin J, Lwin T, Rao R, Zhang Y, Chan JC, Fu K, Marquez VE, et al. Coordinated silencing of MYC-mediated miR-29 by HDAC3 and EZH2 as a therapeutic target of histone modification in aggressive B-Cell lymphomas. Cancer Cell 2012; 22:506 - 23; http://dx.doi.org/10.1016/j.ccr.2012.09.003; PMID: 23079660
   PubMed Web of Science ®Google Scholar
• Hartmann E, Fernàndez V, Moreno V, Valls J, Hernández L, Bosch F, Abrisqueta P, Klapper W, Dreyling M, Hoster E, et al. Five-gene model to predict survival in mantle-cell lymphoma using frozen or formalin-fixed, paraffin-embedded tissue. J Clin Oncol 2008; 26:4966 - 72; http://dx.doi.org/10.1200/JCO.2007.12.0410; PMID: 18606985
   PubMed Web of Science ®Google Scholar
• Zhao JJ, Lin J, Lwin T, Yang H, Guo J, Kong W, Dessureault S, Moscinski LC, Rezania D, Dalton WS, et al. microRNA expression profile and identification of miR-29 as a prognostic marker and pathogenetic factor by targeting CDK6 in mantle cell lymphoma. Blood 2010; 115:2630 - 9; http://dx.doi.org/10.1182/blood-2009-09-243147; PMID: 20086245
   PubMed Web of Science ®Google Scholar
• Xiao Y. Enhancer of zeste homolog 2: A potential target for tumor therapy. Int J Biochem Cell Biol 2011; 43:474 - 7; http://dx.doi.org/10.1016/j.biocel.2011.01.005; PMID: 21241820
   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
   PubMed Web of Science ®Google Scholar
• Fiskus W, Rao R, Balusu R, Ganguly S, Tao J, Sotomayor E, Mudunuru U, Smith JE, Hembruff SL, Atadja P, et al. Superior efficacy of a combined epigenetic therapy against human mantle cell lymphoma cells. Clin Cancer Res 2012; 18:6227 - 38; http://dx.doi.org/10.1158/1078-0432.CCR-12-0873; PMID: 22932665
   PubMed Web of Science ®Google Scholar
• Yu J, Yu J, Rhodes DR, Tomlins SA, Cao X, Chen G, Mehra R, Wang X, Ghosh D, Shah RB, et al. A polycomb repression signature in metastatic prostate cancer predicts cancer outcome. Cancer Res 2007; 67:10657 - 63; http://dx.doi.org/10.1158/0008-5472.CAN-07-2498; PMID: 18006806
   PubMed Web of Science ®Google Scholar
• Bracken AP, Pasini D, Capra M, Prosperini E, Colli E, Helin K. EZH2 is downstream of the pRB-E2F pathway, essential for proliferation and amplified in cancer. EMBO J 2003; 22:5323 - 35; http://dx.doi.org/10.1093/emboj/cdg542; PMID: 14532106
   PubMed Web of Science ®Google Scholar
• Varambally S, Dhanasekaran SM, Zhou M, Barrette TR, Kumar-Sinha C, Sanda MG, Ghosh D, Pienta KJ, Sewalt RG, Otte AP, et al. The polycomb group protein EZH2 is involved in progression of prostate cancer. Nature 2002; 419:624 - 9; http://dx.doi.org/10.1038/nature01075; PMID: 12374981
   PubMed Web of Science ®Google Scholar
• Hallek M, Cheson BD, Catovsky D, Caligaris-Cappio F, Dighiero G, Döhner H, Hillmen P, Keating MJ, Montserrat E, Rai KR, et al, International Workshop on Chronic Lymphocytic Leukemia. Guidelines for the diagnosis and treatment of chronic lymphocytic leukemia: a report from the International Workshop on Chronic Lymphocytic Leukemia updating the National Cancer Institute-Working Group 1996 guidelines. Blood 2008; 111:5446 - 56; http://dx.doi.org/10.1182/blood-2007-06-093906; PMID: 18216293
   PubMed Web of Science ®Google Scholar
• Rosén A, Bergh AC, Gogok P, Evaldsson C, Myhrinder AL, Hellqvist E, Rasul A, Björkholm M, Jansson M, Mansouri L, et al. Lymphoblastoid cell line with B1 cell characteristics established from a chronic lymphocytic leukemia clone by in vitro EBV infection. Oncoimmunology 2012; 1:18 - 27; http://dx.doi.org/10.4161/onci.1.1.18400; PMID: 22720208
   PubMed Web of Science ®Google Scholar
• Amin HM, McDonnell TJ, Medeiros LJ, Rassidakis GZ, Leventaki V, O’Connor SL, Keating MJ, Lai R. Characterization of 4 mantle cell lymphoma cell lines. Arch Pathol Lab Med 2003; 127:424 - 31; PMID: 12683869
   PubMed Web of Science ®Google Scholar
• Papakonstantinou NNS, Papadopoulos G, Hatzigeorgiou A, Anagnostopoulos A, Chlichlia A, Ghia P, Muzio M, Belessi C, Stamatopoulos K. Distinct profiles of miRNAs modulating immune signalling pathways in different subsets of chronic lymphocytic leukemia. 17th Congress of the European Haematology Association. Amsterdam, 2012.
   Google Scholar
• Kanduri M, Cahill N, Göransson H, Enström C, Ryan F, Isaksson A, Rosenquist R. Differential genome-wide array-based methylation profiles in prognostic subsets of chronic lymphocytic leukemia. Blood 2010; 115:296 - 305; http://dx.doi.org/10.1182/blood-2009-07-232868; PMID: 19897574
   PubMed Web of Science ®Google Scholar