Advanced search
Publication Cover
Epigenomics Volume 5, 2013 - Issue 4
Submit an article Journal homepage
2,874
Views
0
CrossRef citations to date
0
Altmetric
Review

Combating the Epigenome: Epigenetic Drugs Against Non-Hodgkin‘S Lymphoma

Melanie R Hassler1 Clinical Institute of Pathology, Medical University of Vienna, Waehringer Guertel 18–20, 1090Vienna, AustriaView further author information
,
Ana-Iris Schiefer1 Clinical Institute of Pathology, Medical University of Vienna, Waehringer Guertel 18–20, 1090Vienna, AustriaView further author information
&
Gerda Egger1 Clinical Institute of Pathology, Medical University of Vienna, Waehringer Guertel 18–20, 1090Vienna, AustriaCorrespondence[email protected]
View further author information
Pages 397-415 | Published online: 29 Jul 2013

References

  • Morton LM , WangSS, DevesaSS, HartgeP, WeisenburgerDD, LinetMS. Lymphoma incidence patterns by WHO subtype in the United States, 1992–2001. Blood107(1) , 265–276 (2006).
  • Harris NL , JaffeES, SteinH et al. A revised European–American classification of lymphoid neoplasms: a proposal from the International Lymphoma Study Group. Blood 84(5) , 1361–1392 (1994).
  • Swerdlow S , CampoE, HarrisN, AlE. World Health Organization Classification of Tumours of Haematopoietic and Lymphoid Tissues (4th Edition). International Agency for Research on Cancer Press, Lyon, France, 214–217 (2008).
  • Martin-Subero JI , Lopez-OtinC, CampoE. Genetic and epigenetic basis of chronic lymphocytic leukemia. Curr. Opin. Hematol.20(4) , 362–368 (2013).
  • Piccaluga PP , AgostinelliC, CalifanoA et al. Gene expression analysis of angioimmunoblastic lymphoma indicates derivation from T follicular helper cells and vascular endothelial growth factor deregulation. Cancer Res. 67(22) , 10703–10710 (2007).
  • Streubel B , VinatzerU, WillheimM, RadererM, ChottA. Novel t(5;9)(q33;q22) fuses ITK to SYK in unspecified peripheral T-cell lymphoma. Leukemia20(2) , 313–318 (2006).
  • Kohno T , YamadaY, AkamatsuN et al. Possible origin of adult T-cell leukemia/lymphoma cells from human T lymphotropic virus type-1-infected regulatory T cells. Cancer Sci. 96(8) , 527–533 (2005).
  • Beral V , PetermanT, BerkelmanR, JaffeH. AIDS-associated non-Hodgkin lymphoma. Lancet337(8745) , 805–809 (1991).
  • Canioni D , JabadoN, MacintyreE, PateyN, EmileJF, BrousseN. Lymphoproliferative disorders in children with primary immunodeficiencies: immunological status may be more predictive of the outcome than other criteria. Histopathology38(2) , 146–159 (2001).
  • Kassan SS , ThomasTL, MoutsopoulosHM et al. Increased risk of lymphoma in sicca syndrome. Ann. Intern. Med. 89(6) , 888–892 (1978).
  • Hamilton-Dutoit SJ , ReaD, RaphaelM et al. Epstein–Barr virus-latent gene expression and tumor cell phenotype in acquired immunodeficiency syndrome-related non-Hodgkin‘s lymphoma. Correlation of lymphoma phenotype with three distinct patterns of viral latency. Am. J. Pathol. 143(4) , 1072–1085 (1993).
  • Du MQ , BaconCM, IsaacsonPG. Kaposi sarcoma-associated herpesvirus/human herpesvirus 8 and lymphoproliferative disorders. J. Clin. Pathol.60(12) , 1350–1357 (2007).
  • Satou Y , YasunagaJ, YoshidaM, MatsuokaM. HTLV-I basic leucine zipper factor gene mRNA supports proliferation of adult T cell leukemia cells. Proc. Natl Acad. Sci. USA103(3) , 720–725 (2006).
  • Marcucci F , MeleA. Hepatitis viruses and non-Hodgkin lymphoma: epidemiology, mechanisms of tumorigenesis, and therapeutic opportunities. Blood117(6) , 1792–1798 (2011).
  • Guidoboni M , FerreriAJ, PonzoniM, DoglioniC, DolcettiR. Infectious agents in mucosa-associated lymphoid tissue-type lymphomas: pathogenic role and therapeutic perspectives. Clin. Lymphoma Myeloma6(4) , 289–300 (2006).
  • Carbone PP , KaplanHS, MusshoffK, SmithersDW, TubianaM. Report of the Committee on Hodgkin‘s Disease Staging Classification. Cancer Res.31(11) , 1860–1861 (1971).
  • Project TIN -HSLPF. A predictive model for aggressive non-Hodgkin‘s lymphoma. The International Non-Hodgkin‘s Lymphoma Prognostic Factors Project. N .Engl. J. Med.329(14) , 987–994 (1993).
  • Siebert R , RosenwaldA, StaudtLM, MorrisSW. Molecular features of B-cell lymphoma. Curr. Opin. Oncol.13(5) , 316–324 (2001).
  • Jares P , CampoE, PinyolM et al. Expression of retinoblastoma gene product (pRb) in mantle cell lymphomas. Correlation with cyclin D1 (PRAD1/CCND1) mRNA levels and proliferative activity. Am. J. Pathol. 148(5) , 1591–1600 (1996).
  • Quintanilla-Martinez L , Davies-HillT, FendF et al. Sequestration of p27Kip1 protein by cyclin D1 in typical and blastic variants of mantle cell lymphoma (MCL): implications for pathogenesis. Blood 101(8) , 3181–3187 (2003).
  • Carvajal-Cuenca A , SuaLF, SilvaNM et al. In situ mantle cell lymphoma: clinical implications of an incidental finding with indolent clinical behavior. Haematologica97(2) , 270–278 (2012).
  • Jegalian AG , EberleFC, PackSD et al. Follicular lymphoma in situ: clinical implications and comparisons with partial involvement by follicular lymphoma. Blood 118(11) , 2976–2984 (2011).
  • Zhang Q , SiebertR, YanM et al. Inactivating mutations and overexpression of BCL10, a caspase recruitment domain-containing gene, in MALT lymphoma with t(1;14)(p22;q32). Nat. Genet. 22(1) , 63–68 (1999).
  • Zech L , HaglundU, NilssonK, KleinG. Characteristic chromosomal abnormalities in biopsies and lymphoid-cell lines from patients with Burkitt and non-Burkitt lymphomas. Int. J. Cancer17(1) , 47–56 (1976).
  • Alizadeh AA , EisenMB, DavisRE et al. Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling. Nature 403(6769) , 503–511 (2000).
  • Huang Y , De Reyniès A, De Leval L et al. Gene expression profiling identifies emerging oncogenic pathways operating in extranodal NK/T-cell lymphoma, nasal type. Blood115(6) , 1226–1237 (2010).
  • Piccaluga PP , AgostinelliC, CalifanoA et al. Gene expression analysis of peripheral T cell lymphoma, unspecified, reveals distinct profiles and new potential therapeutic targets. J. Clin. Invest. 117(3) , 823–834 (2007).
  • Bellan C , LazziS, De Falco G, Nyongo A, Giordano A, Leoncini L. Burkitt‘s lymphoma: new insights into molecular pathogenesis. J. Clin. Pathol.56(3) , 188–192 (2003).
  • Hagelkruys A , SawickaA, RennmayrM, SeiserC. The biology of HDAC in cancer: the nuclear and epigenetic components. Handb. Exp. Pharmacol.206 , 13–37 (2011).
  • Marquard L , PoulsenCB, GjerdrumLM et al. Histone deacetylase 1, 2, 6 and acetylated histone H4 in B- and T-cell lymphomas. Histopathology 54(6) , 688–698 (2009).
  • Marquard L , GjerdrumLM, ChristensenIJ, JensenPB, SehestedM, RalfkiaerE. Prognostic significance of the therapeutic targets histone deacetylase 1, 2, 6 and acetylated histone H4 in cutaneous T-cell lymphoma. Histopathology53(3) , 267–277 (2008).
  • Minucci S , PelicciPG. Retinoid receptors in health and disease: co-regulators and the chromatin connection. Semin. Cell Dev. Biol.10(2) , 215–225 (1999).
  • Pasqualucci L , BereschenkoO, NiuH et al. Molecular pathogenesis of non-Hodgkin‘s lymphoma: the role of Bcl-6. Leuk. Lymphoma 44(Suppl. 3) , S5–S12 (2003).
  • Zhang X , ChenX, LinJ et al. Myc represses miR-15a/miR-16–11 expression through recruitment of HDAC3 in mantle cell and other non-Hodgkin B-cell lymphomas. Oncogene 31(24) , 3002–3008 (2012).
  • Zhang X , ZhaoX, FiskusW 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 22(4) , 506–523 (2012).
  • Gupta M , HanJJ, StensonM, WellikL, WitzigTE. Regulation of STAT3 by histone deacetylase-3 in diffuse large B-cell lymphoma: implications for therapy. Leukemia26(6) , 1356–1364 (2012).
  • Bracken AP , HelinK. Polycomb group proteins: navigators of lineage pathways led astray in cancer. Nat. Rev. Cancer9(11) , 773–784 (2009).
  • Velichutina I , ShaknovichR, GengH et al. EZH2-mediated epigenetic silencing in germinal center B cells contributes to proliferation and lymphomagenesis. Blood 116(24) , 5247–5255 (2010).
  • van Galen JC , DukersDF, GirothC et al. Distinct expression patterns of polycomb oncoproteins and their binding partners during the germinal center reaction. Eur. J. Immunol. 34(7) , 1870–1881 (2004).
  • Morin RD , JohnsonNA, SeversonTM et al. Somatic mutations altering EZH2 (Tyr641) in follicular and diffuse large B-cell lymphomas of germinal-center origin. Nat. Genet. 42(2) , 181–185 (2010).
  • Love C , SunZ, JimaD et al. The genetic landscape of mutations in Burkitt lymphoma. Nat. Genet. 44(12) , 1321–1325 (2012).
  • Nikoloski G , LangemeijerSM, KuiperRP et al. Somatic mutations of the histone methyltransferase gene EZH2 in myelodysplastic syndromes. Nat. Genet. 42(8) , 665–667 (2010).
  • Visser HP , GunsterMJ, Kluin-NelemansHC et al. The polycomb group protein EZH2 is upregulated in proliferating, cultured human mantle cell lymphoma. Br. J. Haematol. 112(4) , 950–958 (2001).
  • Eckerle S , BruneV, DöringC et al. Gene expression profiling of isolated tumour cells from anaplastic large cell lymphomas: insights into its cellular origin, pathogenesis and relation to Hodgkin lymphoma. Leukemia 23(11) , 2129–2138 (2009).
  • Sasaki D , ImaizumiY, HasegawaH et al. Overexpression of Enhancer of zeste homolog 2 with trimethylation of lysine 27 on histone H3 in adult T-cell leukemia/lymphoma as a target for epigenetic therapy. Haematologica 96(5) , 712–719 (2011).
  • Majer CR , JinL, ScottMP et al. A687V EZH2 is a gain-of-function mutation found in lymphoma patients. FEBS Lett. 586(19) , 3448–3451 (2012).
  • McCabe MT , GravesAP, GanjiG et al. Mutation of A677 in histone methyltransferase EZH2 in human B-cell lymphoma promotes hypertrimethylation of histone H3 on lysine 27 (H3K27). Proc. Natl Acad. Sci. USA 109(8) , 2989–2994 (2012).
  • Yap DB , ChuJ, BergT et al. Somatic mutations at EZH2 Y641 act dominantly through a mechanism of selectively altered PRC2 catalytic activity, to increase H3K27 trimethylation. Blood 117(8) , 2451–2459 (2011).
  • Agger K , CloosPA, ChristensenJ et al. UTX and JMJD3 are histone H3K27 demethylases involved in HOX gene regulation and development. Nature 449(7163) , 731–734 (2007).
  • Lan F , BaylissPE, RinnJL et al. A histone H3 lysine 27 demethylase regulates animal posterior development. Nature 449(7163) , 689–694 (2007).
  • Lee MG , VillaR, TrojerP et al. Demethylation of H3K27 regulates polycomb recruitment and H2A ubiquitination. Science 318(5849) , 447–450 (2007).
  • McCabe MT , OttHM, GanjiG et al. EZH2 inhibition as a therapeutic strategy for lymphoma with EZH2-activating mutations. Nature 492(7427) , 108–112 (2012).
  • van Haaften G , DalglieshGL, DaviesH et al. Somatic mutations of the histone H3K27 demethylase gene UTX in human cancer. Nat. Genet. 41(5) , 521–523 (2009).
  • Morin RD , Mendez-LagoM, MungallAJ et al. Frequent mutation of histone-modifying genes in non-Hodgkin lymphoma. Nature 476(7360) , 298–303 (2011).
  • Pasqualucci L , TrifonovV, FabbriG et al. Analysis of the coding genome of diffuse large B-cell lymphoma. Nat. Genet. 43(9) , 830–837 (2011).
  • Lohr JG , StojanovP, LawrenceMS et al. Discovery and prioritization of somatic mutations in diffuse large B-cell lymphoma (DLBCL) by whole-exome sequencing. Proc. Natl Acad. Sci. USA 109(10) , 3879–3884 (2012).
  • Shilatifard A . Chromatin modifications by methylation and ubiquitination: implications in the regulation of gene expression. Annu. Rev. Biochem.75 , 243–269 (2006).
  • Issaeva I , ZonisY, RozovskaiaT et al. Knockdown of ALR (MLL2) reveals ALR target genes and leads to alterations in cell adhesion and growth. Mol. Cell. Biol. 27(5) , 1889–1903 (2007).
  • Yuan ZL , GuanYJ, ChatterjeeD, ChinYE. Stat3 dimerization regulated by reversible acetylation of a single lysine residue. Science307(5707) , 269–273 (2005).
  • Pasqualucci L , Dominguez-SolaD, ChiarenzaA et al. Inactivating mutations of acetyltransferase genes in B-cell lymphoma. Nature 471(7337) , 189–195 (2011).
  • Pasini D , MalatestaM, JungHR et al. Characterization of an antagonistic switch between histone H3 lysine 27 methylation and acetylation in the transcriptional regulation of polycomb group target genes. Nucleic Acids Res. 38(15) , 4958–4969 (2010).
  • Martín-Pérez D , SánchezE, MaestreL et al. Deregulated expression of the polycomb-group protein SUZ12 target genes characterizes mantle cell lymphoma. Am. J. Pathol. 177(2) , 930–942 (2010).
  • van Kemenade FJ , RaaphorstFM, BlokzijlT et al. 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 97(12) , 3896–3901 (2001).
  • Martín-Subero JI , KreuzM, BibikovaM et al. New insights into the biology and origin of mature aggressive B-cell lymphomas by combined epigenomic, genomic, and transcriptional profiling. Blood 113(11) , 2488–2497 (2009).
  • Widschwendter M , FieglH, EgleD et al. Epigenetic stem cell signature in cancer. Nat. Genet. 39(2) , 157–158 (2007).
  • Gal-Yam EN , EggerG, IniguezL et al. Frequent switching of polycomb repressive marks and DNA hypermethylation in the PC3 prostate cancer cell line. Proc. Natl Acad. Sci. USA 105(35) , 12979–12984 (2008).
  • Ehrich M , TurnerJ, GibbsP et al. Cytosine methylation profiling of cancer cell lines. Proc. Natl Acad. Sci. USA 105(12) , 4844–4849 (2008).
  • Challen GA , SunD, JeongM et al. Dnmt3a is essential for hematopoietic stem cell differentiation. Nat. Genet. 44(1) , 23–31 (2011).
  • Couronné L , BastardC, BernardOA. TET2 and DNMT3A mutations in human T-cell lymphoma. N .Engl. J. Med.366(1) , 95–96 (2012).
  • Shah MY , VasanthakumarA, BarnesNY et al. DNMT3B7, a truncated DNMT3B isoform expressed in human tumors, disrupts embryonic development and accelerates lymphomagenesis. Cancer Res. 70(14) , 5840–5850 (2010).
  • Vasanthakumar A , LeporeJB, ZegarekMH et al. Dnmt3b is a haploinsufficient tumor suppressor gene in Myc-induced lymphomagenesis. Blood121(11) , 2059–2063 (2013).
  • Amara K , ZiadiS, HachanaM, SoltaniN, KorbiS, TrimecheM. DNA methyltransferase DNMT3b protein overexpression as a prognostic factor in patients with diffuse large B-cell lymphomas. Cancer Sci.101(7) , 1722–1730 (2010).
  • Bröske AM , VockentanzL, KharaziS et al. DNA methylation protects hematopoietic stem cell multipotency from myeloerythroid restriction. Nat. Genet. 41(11) , 1207–1215 (2009).
  • Trowbridge JJ , SnowJW, KimJ, OrkinSH. DNA methyltransferase 1 is essential for and uniquely regulates hematopoietic stem and progenitor cells. Cell Stem Cell5(4) , 442–449 (2009).
  • Trowbridge JJ , SinhaAU, ZhuN, LiM, ArmstrongSA, OrkinSH. Haploinsufficiency of Dnmt1 impairs leukemia stem cell function through derepression of bivalent chromatin domains. Genes Dev.26(4) , 344–349 (2012).
  • Egger G , LiangG, AparicioA, JonesPA. Epigenetics in human disease and prospects for epigenetic therapy. Nature429(6990) , 457–463 (2004).
  • Cheng JC , MatsenCB, GonzalesFA et al. Inhibition of DNA methylation and reactivation of silenced genes by zebularine. J. Natl Cancer Inst. 95(5) , 399–409 (2003).
  • Santi DV , GarrettCE, BarrPJ. On the mechanism of inhibition of DNA-cytosine methyltransferases by cytosine analogs. Cell33(1) , 9–10 (1983).
  • Santi DV , NormentA, GarrettCE. Covalent bond formation between a DNA-cytosine methyltransferase and DNA containing 5-azacytosine. Proc. Natl Acad. Sci. USA81(22) , 6993–6997 (1984).
  • Kantarjian HM , IssaJP. Decitabine dosing schedules. Semin. Hematol.42(3 Suppl. 2) , S17–S22 (2005).
  • Lee TT , KaronMR. Inhibition of protein synthesis in 5-azacytidine-treated HeLa cells. Biochem. Pharmacol.25(15) , 1737–1742 (1976).
  • Ogama Y , OuchidaM, YoshinoT et al. Prevalent hyper-methylation of the CDH13 gene promoter in malignant B cell lymphomas. Int. J. Oncol. 25(3) , 685–691 (2004).
  • Agrelo R , SetienF, EspadaJ et al. Inactivation of the lamin A/C gene by CpG island promoter hypermethylation in hematologic malignancies, and its association with poor survival in nodal diffuse large B-cell lymphoma. J. Clin. Oncol. 23(17) , 3940–3947 (2005).
  • Hassler MR , KlisaroskaA, KollmannK et al. Antineoplastic activity of the DNA methyltransferase inhibitor 5-aza-2´-deoxycytidine in anaplastic large cell lymphoma. Biochimie 94(11) , 2297–2307 (2012).
  • Han Y , AminHM, FrantzC et al. Restoration of shp1 expression by 5-AZA-2´-deoxycytidine is associated with downregulation of JAK3/STAT3 signaling in ALK-positive anaplastic large cell lymphoma. Leukemia 20(9) , 1602–1609 (2006).
  • Qin T , JelinekJ, SiJ, ShuJ, IssaJP. Mechanisms of resistance to 5-aza-2´-deoxycytidine in human cancer cell lines. Blood113(3) , 659–667 (2009).
  • Momparler RL . Pharmacology of 5-aza-2´-deoxycytidine (decitabine). Semin. Hematol.42(3 Suppl. 2) , S9–S16 (2005).
  • Samlowski WE , LeachmanSA, WadeM et al. Evaluation of a 7-day continuous intravenous infusion of decitabine: inhibition of promoter-specific and global genomic DNA methylation. J. Clin. Oncol. 23(17) , 3897–3905 (2005).
  • Karahoca M , MomparlerRL. Pharmacokinetic and pharmacodynamic analysis of 5-aza-2´-deoxycytidine (decitabine) in the design of its dose-schedule for cancer therapy. Clin. Epigenetics5(1) , 3 (2013).
  • Lavelle D , VaitkusK, LingY et al. Effects of tetrahydrouridine on pharmacokinetics and pharmacodynamics of oral decitabine. Blood 119(5) , 1240–1247 (2012).
  • Momparler RL , GoodmanJ. In vitro cytotoxic and biochemical effects of 5-aza-2´-deoxycytidine. Cancer Res.37(6) , 1636–1639 (1977).
  • Issa JP , Garcia-ManeroG, GilesFJ et al. Phase 1 study of low-dose prolonged exposure schedules of the hypomethylating agent 5-aza-2´-deoxycytidine (decitabine) in hematopoietic malignancies. Blood 103(5) , 1635–1640 (2004).
  • Kaminskas E , FarrellA, AbrahamS et al. Approval summary: azacitidine for treatment of myelodysplastic syndrome subtypes. Clin. Cancer Res. 11(10) , 3604–3608 (2005).
  • Blum KA , LiuZ, LucasDM et al. Phase I trial of low dose decitabine targeting DNA hypermethylation in patients with chronic lymphocytic leukaemia and non-Hodgkin lymphoma: dose-limiting myelosuppression without evidence of DNA hypomethylation. Br. J. Haematol. 150(2) , 189–195 (2010).
  • Stewart DJ , IssaJP, KurzrockR et al. Decitabine effect on tumor global DNA methylation and other parameters in a Phase I trial in refractory solid tumors and lymphomas. Clin. Cancer Res. 15(11) , 3881–3888 (2009).
  • Stathis A , HotteSJ, ChenEX et al. Phase I study of decitabine in combination with vorinostat in patients with advanced solid tumors and non-Hodgkin‘s lymphomas. Clin. Cancer Res. 17(6) , 1582–1590 (2011).
  • Cameron EE , BachmanKE, MyöhänenS, HermanJG, BaylinSB. Synergy of demethylation and histone deacetylase inhibition in the re-expression of genes silenced in cancer. Nat. Genet.21(1) , 103–107 (1999).
  • Minucci S , PelicciPG. Histone deacetylase inhibitors and the promise of epigenetic (and more) treatments for cancer. Nat. Rev. Cancer6(1) , 38–51 (2006).
  • Bradner JE , WestN, GrachanML et al. Chemical phylogenetics of histone deacetylases. Nat. Chem. Biol. 6(3) , 238–243 (2010).
  • Hu E , DulE, SungCM et al. Identification of novel isoform-selective inhibitors within class I histone deacetylases. J. Pharmacol. Exp. Ther. 307(2) , 720–728 (2003).
  • Vannini A , VolpariC, FilocamoG et al. Crystal structure of a eukaryotic zinc-dependent histone deacetylase, human HDAC8, complexed with a hydroxamic acid inhibitor. Proc. Natl Acad. Sci. USA 101(42) , 15064–15069 (2004).
  • Inoue S , MaiA, DyerMJ, CohenGM. Inhibition of histone deacetylase class I but not class II is critical for the sensitization of leukemic cells to tumor necrosis factor-related apoptosis-inducing ligand-induced apoptosis. Cancer Res.66(13) , 6785–6792 (2006).
  • Santo L , HideshimaT, KungAL et al. Preclinical activity, pharmacodynamic, and pharmacokinetic properties of a selective HDAC6 inhibitor, ACY-1215, in combination with bortezomib in multiple myeloma. Blood 119(11) , 2579–2589 (2012).
  • Fournel M , BonfilsC, HouY et al. MGCD0103, a novel isotype-selective histone deacetylase inhibitor, has broad spectrum antitumor activity in vitro and in vivo. Mol. Cancer Ther. 7(4) , 759–768 (2008).
  • Lin RJ , EganDA, EvansRM. Molecular genetics of acute promyelocytic leukemia. Trends Genet.15(5) , 179–184 (1999).
  • He LZ , TolentinoT, GraysonP et al. Histone deacetylase inhibitors induce remission in transgenic models of therapy-resistant acute promyelocytic leukemia. J. Clin. Invest. 108(9) , 1321–1330 (2001).
  • Kalac M , ScottoL, MarchiE et al. HDAC inhibitors and decitabine are highly synergistic and associated with unique gene-expression and epigenetic profiles in models of DLBCL. Blood 118(20) , 5506–5516 (2011).
  • Zhang C , RichonV, NiX, TalpurR, DuvicM. Selective induction of apoptosis by histone deacetylase inhibitor SAHA in cutaneous T-cell lymphoma cells: relevance to mechanism of therapeutic action. J. Invest. Dermatol.125(5) , 1045–1052 (2005).
  • Piekarz RL , RobeyRW, ZhanZ et al. T-cell lymphoma as a model for the use of histone deacetylase inhibitors in cancer therapy: impact of depsipeptide on molecular markers, therapeutic targets, and mechanisms of resistance. Blood 103(12) , 4636–4643 (2004).
  • Camphausen K , BurganW, CerraM et al. Enhanced radiation-induced cell killing and prolongation of gammaH2AX foci expression by the histone deacetylase inhibitor MS-275. Cancer Res. 64(1) , 316–321 (2004).
  • Munshi A , KurlandJF, NishikawaT et al. Histone deacetylase inhibitors radiosensitize human melanoma cells by suppressing DNA repair activity. Clin. Cancer Res. 11(13) , 4912–4922 (2005).
  • Richon VM , SandhoffTW, RifkindRA, MarksPA. Histone deacetylase inhibitor selectively induces p21WAF1 expression and gene-associated histone acetylation. Proc. Natl Acad. Sci. USA97(18) , 10014–10019 (2000).
  • Shao Y , GaoZ, MarksPA, JiangX. Apoptotic and autophagic cell death induced by histone deacetylase inhibitors. Proc. Natl Acad. Sci. USA101(52) , 18030–18035 (2004).
  • Insinga A , MonestiroliS, RonzoniS et al. Inhibitors of histone deacetylases induce tumor-selective apoptosis through activation of the death receptor pathway. Nat. Med. 11(1) , 71–76 (2005).
  • Nebbioso A , ClarkeN, VoltzE et al. Tumor-selective action of HDAC inhibitors involves TRAIL induction in acute myeloid leukemia cells. Nat. Med. 11(1) , 77–84 (2005).
  • Tang Y , ZhaoW, ChenY, ZhaoY, GuW. Acetylation is indispensable for p53 activation. Cell133(4) , 612–626 (2008).
  • Guan JS , HaggartySJ, GiacomettiE et al. HDAC2 negatively regulates memory formation and synaptic plasticity. Nature 459(7243) , 55–60 (2009).
  • Heideman MR , WiltingRH, YanoverE et al. Dosage-dependent tumor suppression by histone deacetylases 1 and 2 through regulation of c-Myc collaborating genes and p53 function. Blood 121(11) , 2038–2050 (2013).
  • Santoro F , BotrugnoOA, Dal Zuffo R et al. A dual role for HDAC1: oncosuppressor in tumorigenesis, oncogene in tumor maintenance. Blood121(17) , 3459–3468 (2013).
  • Dovey OM , FosterCT, ConteN et al. Histone deacetylase 1 and 2 are essential for normal T-cell development and genomic stability in mice. Blood 121(8) , 1335–1344 (2013).
  • Gloghini A , BuglioD, KhaskhelyNM et al. Expression of histone deacetylases in lymphoma: implication for the development of selective inhibitors. Br. J. Haematol. 147(4) , 515–525 (2009).
  • Balasubramanian S , RamosJ, LuoW, SirisawadM, VernerE, BuggyJJ. A novel histone deacetylase 8 (HDAC8)-specific inhibitor PCI-34051 induces apoptosis in T-cell lymphomas. Leukemia22(5) , 1026–1034 (2008).
  • Mann BS , JohnsonJR, CohenMH, JusticeR, PazdurR. FDA approval summary: vorinostat for treatment of advanced primary cutaneous T-cell lymphoma. Oncologist12(10) , 1247–1252 (2007).
  • Younes A , WedgwoodA, McLaughlinP et al. Treatment of relapsed or refractory lymphoma with the oral isotype-selective histone deacetylase inhibitor MGCD0103: interim results from a Phase II study. Blood 110(11), Abstract 2571 (2007).
  • Gore L , RothenbergML, O‘BryantCL et al. A Phase I and pharmacokinetic study of the oral histone deacetylase inhibitor, MS-275, in patients with refractory solid tumors and lymphomas. Clin. Cancer Res. 14(14) , 4517–4525 (2008).
  • Piekarz RL , FryeR, TurnerM et al. Phase II multi-institutional trial of the histone deacetylase inhibitor romidepsin as monotherapy for patients with cutaneous T-cell lymphoma. J. Clin. Oncol. 27(32) , 5410–5417 (2009).
  • Ryan QC , HeadleeD, AcharyaM et al. Phase I and pharmacokinetic study of MS-275, a histone deacetylase inhibitor, in patients with advanced and refractory solid tumors or lymphoma. J. Clin. Oncol. 23(17) , 3912–3922 (2005).
  • Kelly WK , O‘ConnorOA, KrugLM et al. Phase I study of an oral histone deacetylase inhibitor, suberoylanilide hydroxamic acid, in patients with advanced cancer. J. Clin. Oncol. 23(17) , 3923–3931 (2005).
  • Sandor V , BakkeS, RobeyRW et al. Phase I trial of the histone deacetylase inhibitor, depsipeptide (FR901228, NSC 630176), in patients with refractory neoplasms. Clin. Cancer Res. 8(3) , 718–728 (2002).
  • Garcia-Manero G , AssoulineS, CortesJ et al. Phase 1 study of the oral isotype specific histone deacetylase inhibitor MGCD0103 in leukemia. Blood 112(4) , 981–989 (2008).
  • Zain J . Role of histone deacetylase inhibitors in the treatment of lymphomas and multiple myeloma. Hematol. Oncol. Clin. North Am.26(3) , 671–704, ix (2012).
  • Bertino EM , OttersonGA. Romidepsin: a novel histone deacetylase inhibitor for cancer. Expert Opin. Investig. Drugs20(8) , 1151–1158 (2011).
  • Olsen EA , KimYH, KuzelTM et al. Phase IIb multicenter trial of vorinostat in patients with persistent, progressive, or treatment refractory cutaneous T-cell lymphoma. J. Clin. Oncol. 25(21) , 3109–3115 (2007).
  • Duvic M , TalpurR, NiX et al. Phase 2 trial of oral vorinostat (suberoylanilide hydroxamic acid, SAHA) for refractory cutaneous T-cell lymphoma (CTCL). Blood 109(1) , 31–39 (2007).
  • Kirschbaum M , FrankelP, PopplewellL 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. 29(9) , 1198–1203 (2011).
  • Crump M , CoiffierB, JacobsenED et al. Phase II trial of oral vorinostat (suberoylanilide hydroxamic acid) in relapsed diffuse large-B-cell lymphoma. Ann. Oncol. 19(5) , 964–969 (2008).
  • Whittaker SJ , DemierreMF, KimEJ et al. Final results from a multicenter, international, pivotal study of romidepsin in refractory cutaneous T-cell lymphoma. J. Clin. Oncol. 28(29) , 4485–4491 (2010).
  • Coiffier B , ProB, PrinceHM et al. Results from a pivotal, open-label, Phase II study of romidepsin in relapsed or refractory peripheral T-cell lymphoma after prior systemic therapy. J. Clin. Oncol. 30(6) , 631–636 (2012).
  • Piekarz RL , FryeR, PrinceHM et al. Phase 2 trial of romidepsin in patients with peripheral T-cell lymphoma. Blood 117(22) , 5827–5834 (2011).
  • Duvic M , BeckerJ, DalleS et al. Phase II trial of oral panobinostat (LBH589) in patients with refractory cutaneous T-cell lymphoma (CTCL). Blood 112(11), Abstract 1005 (2008).
  • Tan J , YangX, ZhuangL et al. Pharmacologic disruption of polycomb-repressive complex 2-mediated gene repression selectively induces apoptosis in cancer cells. Genes Dev. 21(9) , 1050–1063 (2007).
  • Miranda TB , CortezCC, YooCB et al. DZNep is a global histone methylation inhibitor that reactivates developmental genes not silenced by DNA methylation. Mol. Cancer Ther. 8(6) , 1579–1588 (2009).
  • Fiskus W , RaoR, BalusuR et al. Superior efficacy of a combined epigenetic therapy against human mantle cell lymphoma cells. Clin. Cancer Res. 18(22) , 6227–6238 (2012).
  • Greiner D , BonaldiT, EskelandR, RoemerE, ImhofA. Identification of a specific inhibitor of the histone methyltransferase SU(VAR)3–9. Nat. Chem. Biol.1(3) , 143–145 (2005).
  • Zheng W , IbáñezG, WuH et al. Sinefungin derivatives as inhibitors and structure probes of protein lysine methyltransferase SETD2. J. Am. Chem. Soc. 134(43) , 18004–18014 (2012).
  • Williams DE , DalisayDS, LiF et al. Nahuoic acid A produced by a Streptomyces sp. isolated from a marine sediment is a selective SAM-competitive inhibitor of the histone methyltransferase SETD8. Org. Lett. 15(2) , 414–417 (2013).
  • Kubicek S , O‘sullivanRJ, AugustEM et al. Reversal of H3K9me2 by a small-molecule inhibitor for the G9a histone methyltransferase. Mol. Cell. 25(3) , 473–481 (2007).
  • Knutson SK , WigleTJ, WarholicNM et al. A selective inhibitor of EZH2 blocks H3K27 methylation and kills mutant lymphoma cells. Nat. Chem. Biol. 8(11) , 890–896 (2012).
  • Filippakopoulos P , KnappS. The bromodomain interaction module. FEBS Lett.586(17) , 2692–2704 (2012).
  • Dhalluin C , CarlsonJE, ZengL, HeC, AggarwalAK, ZhouMM. Structure and ligand of a histone acetyltransferase bromodomain. Nature399(6735) , 491–496 (1999).
  • Mujtaba S , HeY, ZengL et al. Structural mechanism of the bromodomain of the coactivator CBP in p53 transcriptional activation. Mol. Cell. 13(2) , 251–263 (2004).
  • Fitzgerald KT , DiazMO. MLL2: a new mammalian member of the trx/MLL family of genes. Genomics59(2) , 187–192 (1999).
  • Shen W , XuC, HuangW et al. Solution structure of human Brg1 bromodomain and its specific binding to acetylated histone tails. Biochemistry 46(8) , 2100–2110 (2007).
  • Filippakopoulos P , QiJ, PicaudS et al. Selective inhibition of BET bromodomains. Nature 468(7327) , 1067–1073 (2010).
  • Nicodeme E , JeffreyKL, SchaeferU et al. Suppression of inflammation by a synthetic histone mimic. Nature 468(7327) , 1119–1123 (2010).
  • Chung CW , CosteH, WhiteJH et al. Discovery and characterization of small molecule inhibitors of the BET family bromodomains. J. Med. Chem. 54(11) , 3827–3838 (2011).
  • Delmore JE , IssaGC, LemieuxME et al. BET bromodomain inhibition as a therapeutic strategy to target c-Myc. Cell 146(6) , 904–917 (2011).
  • Mertz JA , ConeryAR, BryantBM et al. Targeting MYC dependence in cancer by inhibiting BET bromodomains. Proc. Natl Acad. Sci. USA 108(40) , 16669–16674 (2011).
  • Momparler RL . Cancer epigenetics. Oncogene22(42) , 6479–6483 (2003).
  • Hiraga J , TomitaA, SugimotoT et al. Down-regulation of CD20 expression in B-cell lymphoma cells after treatment with rituximab-containing combination chemotherapies: its prevalence and clinical significance. Blood 113(20) , 4885–4893 (2009).
  • Shi W , HanX, YaoJ, YangJ, ShiY. Combined effect of histone deacetylase inhibitor suberoylanilide hydroxamic acid and anti-CD20 monoclonal antibody rituximab on mantle cell lymphoma cells apoptosis. Leukemia Res.36(6) , 749–755 (2012).
  • Ageberg M , RydstromK, RelanderT, DrottK. The histone deacetylase inhibitor valproic acid sensitizes diffuse large B-cell lymphoma cell lines to CHOP-induced cell death. Am. J. Transl. Res.5(2) , 170–183 (2013).
  • Dos Santos Ferreira AC , FernandesRA, KweeJK, KlumbCE. Histone deacetylase inhibitor potentiates chemotherapy-induced apoptosis through Bim upregulation in Burkitt‘s lymphoma cells. J. Cancer Res. Clin. Oncol.138(2) , 317–325 (2012).
  • Nagarajan RP , FouseSD, BellRJ, CostelloJF. Methods for cancer epigenome analysis. Adv. Exp. Med. Biol.754 , 313–338 (2013).
  • Clark SS , MclaughlinJ, TimmonsM et al. Expression of a distinctive BCR–ABL oncogene in Ph1-positive acute lymphocytic leukemia (ALL). Science 239(4841 Pt 1) , 775–777 (1988).
  • Carroll AJ , CristWM, ParmleyRT, RoperM, CooperMD, FinleyWH. Pre-B cell leukemia associated with chromosome translocation 1;19. Blood63(3) , 721–724 (1984).
  • Lillington DM , YoungBD, BergerR, MartineauM, MoormanAV, Secker-WalkerLM. The t(10;11)(p12;q23) translocation in acute leukaemia: a cytogenetic and clinical study of 20 patients. European 11q23 Workshop participants. Leukemia12(5) , 801–804 (1998).
  • Romana SP , Le Coniat M, Berger R. t(12;21): a new recurrent translocation in acute lymphoblastic leukemia. Genes Chromosomes Cancer9(3) , 186–191 (1994).
  • Gesk S , KlapperW, Martin-SuberoJI et al. A chromosomal translocation in cyclin D1-negative/cyclin D2-positive mantle cell lymphoma fuses the CCND2 gene to the IGK locus. Blood 108(3) , 1109–1110 (2006).
  • Horsman DE , OkamotoI, LudkovskiO et al. Follicular lymphoma lacking the t(14;18)(q32;q21): identification of two disease subtypes. Br. J. Haematol. 120(3) , 424–433 (2003).
  • Aarts WM , WillemzeR, BendeRJ, MeijerCJ, PalsST, Van Noesel CJ. VH gene analysis of primary cutaneous B-cell lymphomas: evidence for ongoing somatic hypermutation and isotype switching. Blood92(10) , 3857–3864 (1998).
  • Dohner H , StilgenbauerS, DohnerK, BentzM, LichterP. Chromosome aberrations in B-cell chronic lymphocytic leukemia: reassessment based on molecular cytogenetic analysis. J. Mol. Med. (Berl.)77(2) , 266–281 (1999).
  • Stilgenbauer S , LichterP, DohnerH. Genetic features of B-cell chronic lymphocytic leukemia. Rev. Clin. Exp. Hematol.4(1) , 48–72 (2000).
  • Akagi T , MotegiM, TamuraA et al. A novel gene, MALT1 at 18q21, is involved in t(11;18) (q21;q21) found in low-grade B-cell lymphoma of mucosa-associated lymphoid tissue. Oncogene 18(42) , 5785–5794 (1999).
  • Streubel B , LamprechtA, DierlammJ et al. T(14;18)(q32;q21) involving IGH and MALT1 is a frequent chromosomal aberration in MALT lymphoma. Blood 101(6) , 2335–2339 (2003).
  • Streubel B , VinatzerU, LamprechtA, RadererM, ChottA. T(3;14)(p14.1;q32) involving IGH and FOXP1 is a novel recurrent chromosomal aberration in MALT lymphoma. Leukemia19(4) , 652–658 (2005).
  • Martin-Subero JI , IbbotsonR, KlapperW et al. A comprehensive genetic and histopathologic analysis identifies two subgroups of B-cell malignancies carrying a t(14;19)(q32;q13) or variant BCL3-translocation. Leukemia 21(7) , 1532–1544 (2007).
  • Gazzo S , BaseggioL, CoignetL et al. Cytogenetic and molecular delineation of a region of chromosome 3q commonly gained in marginal zone B-cell lymphoma. Haematologica 88(1) , 31–38 (2003).
  • Sambani C , TrafalisDT, Mitsoulis-MentzikoffC et al. Clonal chromosome rearrangements in hairy cell leukemia: personal experience and review of literature. Cancer Genet. Cytogenet. 129(2) , 138–144 (2001).
  • Willis TG , DyerMJ. The role of immunoglobulin translocations in the pathogenesis of B-cell malignancies. Blood96(3) , 808–822 (2000).
  • Schop RF , KuehlWM, Van Wier SA et al. Waldenstrom macroglobulinemia neoplastic cells lack immunoglobulin heavy chain locus translocations but have frequent 6q deletions. Blood100(8) , 2996–3001 (2002).
  • Poulain S , RoumierC, DecambronA et al. MYD88 L265P mutation in Waldenstrom macroglobulinemia. Blood 121(22) , 4504–4511 (2013).
  • Ngo VN , YoungRM, SchmitzR et al. Oncogenically active MYD88 mutations in human lymphoma. Nature 470(7332) , 115–119 (2011).
  • Franke S , WlodarskaI, MaesB et al. Comparative genomic hybridization pattern distinguishes T-cell/histiocyte-rich B-cell lymphoma from nodular lymphocyte predominance Hodgkin‘s lymphoma. Am. J. Pathol. 161(5) , 1861–1867 (2002).
  • Hallermann C , KauneKM, GeskS et al. Molecular cytogenetic analysis of chromosomal breakpoints in the IGH, MYC, BCL6, and MALT1 gene loci in primary cutaneous B-cell lymphomas. J. Invest. Dermatol. 123(1) , 213–219 (2004).
  • Wessendorf S , BarthTF, ViardotA et al. Further delineation of chromosomal consensus regions in primary mediastinal B-cell lymphomas: an analysis of 37 tumor samples using high-resolution genomic profiling (array-CGH). Leukemia 21(12) , 2463–2469 (2007).
  • Gesk S , GascoyneRD, SchnitzerB et al. ALK-positive diffuse large B-cell lymphoma with ALK-Clathrin fusion belongs to the spectrum of pediatric lymphomas. Leukemia 19(10) , 1839–1840 (2005).
  • Schmitz R , YoungRM, CeribelliM et al. Burkitt lymphoma pathogenesis and therapeutic targets from structural and functional genomics. Nature 490(7418) , 116–120 (2012).
  • Graux C , CoolsJ, MichauxL, VandenbergheP, HagemeijerA. Cytogenetics and molecular genetics of T-cell acute lymphoblastic leukemia: from thymocyte to lymphoblast. Leukemia20(9) , 1496–1510 (2006).
  • Virgilio L , NarducciMG, IsobeM et al. Identification of the TCL1 gene involved in T-cell malignancies. Proc. Natl Acad. Sci. USA 91(26) , 12530–12534 (1994).
  • Stern MH , SoulierJ, RosenzwajgM et al. MTCP-1: a novel gene on the human chromosome Xq28 translocated to the T cell receptor alpha/delta locus in mature T cell proliferations. Oncogene 8(9) , 2475–2483 (1993).
  • Nakashima Y , TagawaH, SuzukiR et al. Genome-wide array-based comparative genomic hybridization of natural killer cell lymphoma/leukemia: different genomic alteration patterns of aggressive NK-cell leukemia and extranodal Nk/T-cell lymphoma, nasal type. Genes Chromosomes Cancer 44(3) , 247–255 (2005).
  • Przybylski GK , DikWA, WanzeckJ et al. Disruption of the BCL11B gene through inv(14)(q11.2q32.31) results in the expression of BCL11B–TRDC fusion transcripts and is associated with the absence of wild-type BCL11B transcripts in T-ALL. Leukemia 19(2) , 201–208 (2005).
  • Oshiro A , TagawaH, OhshimaK et al. Identification of subtype-specific genomic alterations in aggressive adult T-cell leukemia/lymphoma. Blood 107(11) , 4500–4507 (2006).
  • Siu LL , ChanV, ChanJK, WongKF, LiangR, KwongYL. Consistent patterns of allelic loss in natural killer cell lymphoma. Am. J. Pathol.157(6) , 1803–1809 (2000).
  • Zettl A , OttG, MakulikA et al. Chromosomal gains at 9q characterize enteropathy-type T-cell lymphoma. Am. J. Pathol. 161(5) , 1635–1645 (2002).
  • Wlodarska I , Martin-GarciaN, AchtenR et al. Fluorescence in situ hybridization study of chromosome 7 aberrations in hepatosplenic T-cell lymphoma: isochromosome 7q as a common abnormality accumulating in forms with features of cytologic progression. Genes Chromosomes Cancer 33(3) , 243–251 (2002).
  • Almire C , BertrandP, RuminyP et al. PVRL2 is translocated to the TRA@ locus in t(14;19)(q11;q13)-positive peripheral T-cell lymphomas. Genes Chromosomes Cancer 46(11) , 1011–1018 (2007).
  • Lepretre S , BuchonnetG, StamatoullasA et al. Chromosome abnormalities in peripheral T-cell lymphoma. Cancer Genet. Cytogenet. 117(1) , 71–79 (2000).
  • Morris SW , KirsteinMN, ValentineMB et al. Fusion of a kinase gene, ALK, to a nucleolar protein gene, NPM, in non-Hodgkin‘s lymphoma. Science 263(5151) , 1281–1284 (1994).
  • Batista DA , VonderheidEC, HawkinsA et al. Multicolor fluorescence in situ hybridization (SKY) in mycosis fungoides and Sezary syndrome: search for recurrent chromosome abnormalities. Genes Chromosomes Cancer 45(4) , 383–391 (2006).

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Order Reprints Request Corporate Permissions

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

Request Academic Permissions

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.

Related research

People also read lists articles that other readers of this article have read.

Recommended articles lists articles that we recommend and is powered by our AI driven recommendation engine.

Cited by lists all citing articles based on Crossref citations.
Articles with the Crossref icon will open in a new tab.