Epigenetic changes: A common theme in acute myelogenous leukemogenesis

Journal of Hematology and Oncology

Volumn 6, Issue 1, 2013, Pages

  Gutierrez, Soraya E ^a,b   Romero Oliva, Francisco A ^b  

^a UNIVERSITY OF CONCEPCIÓN   (Chile)

^b CENTRO DE ESTUDIOS CIENTÍFICOS CECS   (Chile)

Author keywords

[No Author keywords available]

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; ANACARDIC ACID; AZACITIDINE; BELINOSTAT; CURCUMIN; CYTARABINE; DACOGENE; DEPSIPEPTIDE; ENTINOSTAT; GIVINOSTAT; HISTONE DEACETYLASE INHIBITOR; IDARUBICIN; ITF 2375; MOCETINOSTAT; PANOBINOSTAT; PHENYLBUTYRATE; ROMIDEPSIN; TRAPOXIN B; TRICHOSTATIN A; UNCLASSIFIED DRUG; VALPROIC ACID; VORINOSTAT;

ACUTE GRANULOCYTIC LEUKEMIA; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; CANCER COMBINATION CHEMOTHERAPY; CANCER GROWTH; CANCER PROGNOSIS; CELL DEATH; CELLULAR DISTRIBUTION; CHROMATIN IMMUNOPRECIPITATION; CHROMOSOMAL INSTABILITY; CPG ISLAND; CUTANEOUS T CELL LYMPHOMA; DNA BINDING; DNA HISTONE INTERACTION; DNA METHYLATION; DNA REPLICATION; DNA SYNTHESIS; DRUG APPROVAL; DRUG TARGETING; ENZYME ACTIVITY; EPIGENETICS; G2 PHASE CELL CYCLE CHECKPOINT; GENE ACTIVATION; GENE CONTROL; GENE EXPRESSION; GENOMIC INSTABILITY; HISTONE ACETYLATION; HISTONE METHYLATION; HISTONE MODIFICATION; HUMAN; IN VITRO STUDY; LEUKEMOGENESIS; LOW DRUG DOSE; LUNG NON SMALL CELL CANCER; MYELODYSPLASTIC SYNDROME; NUCLEOSOME; PANCREAS CANCER; POINT MUTATION; PROTEIN PROCESSING; REVIEW; X CHROMOSOME INACTIVATION;

CELL DIFFERENTIATION; DNA METHYLATION; EPIGENOMICS; HUMANS; LEUKEMIA, MYELOID, ACUTE;

EID: 84881284204     PISSN: None     EISSN: 17568722     Source Type: Journal    
DOI: 10.1186/1756-8722-6-57     Document Type: Review

References (111)

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 4 2008
2. Remission rate and survival in acute myeloid leukemia: impact of selection and chemotherapy. Wahlin A, Hornsten P, Jonsson H, Eur J Haematol 1991 46 4 240 247 2015877
3. High-dose daunorubicin in older patients with acute myeloid leukemia. Lowenberg B, Ossenkoppele GJ, Van Putten W, Schouten HC, Graux C, Ferrant A, Sonneveld P, Maertens J, Jongen-Lavrencic M, Von Lilienfeld-Toal M, et al. N Engl J Med 2009 361 13 1235 1248 10.1056/NEJMoa0901409 19776405
4. Results of intensive chemotherapy in 998 patients age 65 years or older with acute myeloid leukemia or high-risk myelodysplastic syndrome: predictive prognostic models for outcome. Kantarjian H, O'Brien S, Cortes J, Giles F, Faderl S, Jabbour E, Garcia-Manero G, Wierda W, Pierce S, Shan J, et al. Cancer 2006 106 5 1090 1098 10.1002/cncr.21723 16435386
5. The structure of DNA in the nucleosome core. Richmond TJ, Davey CA, Nature 2003 423 6936 145 150 10.1038/nature01595 12736678
6. The role of chromatin during transcription. Li B, Carey M, Workman JL, Cell 2007 128 4 707 719 10.1016/j.cell.2007.01.015 17320508
7. The fundamental role of epigenetics in hematopoietic malignancies. Galm O, Herman JG, Baylin SB, Blood Rev 2006 20 1 1 13 10.1016/j.blre.2005.01.006 16426940
8. Leukaemogenesis: more than mutant genes. Chen J, Odenike O, Rowley JD, Nat Rev Cancer 2010 10 1 23 36 10.1038/nrc2765 20029422
9. DNA hypermethylation in somatic cells correlates with higher reprogramming efficiency. Barrero MJ, Berdasco M, Paramonov I, Bilic J, Vitaloni M, Esteller M, Izpisua Belmonte JC, Stem cells 2012 30 8 1696 1702 10.1002/stem.1138 22653871
10. Aberrant epigenetic landscape in cancer: how cellular identity goes awry. Berdasco M, Esteller M, Developmental cell 2010 19 5 698 711 10.1016/j.devcel.2010.10.005 21074720
11. Mutation in TET2 in myeloid cancers. Delhommeau F, Dupont S, Della Valle V, James C, Trannoy S, Masse A, Kosmider O, Le Couedic JP, Robert F, Alberdi A, et al. N Engl J Med 2009 360 22 2289 2301 10.1056/NEJMoa0810069 19474426
12. Concomitant analysis of EZH2 and ASXL1 mutations in myelofibrosis, chronic myelomonocytic leukemia and blast-phase myeloproliferative neoplasms. Abdel-Wahab O, Pardanani A, Patel J, Wadleigh M, Lasho T, Heguy A, Beran M, Gilliland DG, Levine RL, Tefferi A, Leukemia 2011 25 7 1200 1202 10.1038/leu.2011.58 21455215
13. DNMT3A mutational analysis in primary myelofibrosis, chronic myelomonocytic leukemia and advanced phases of myeloproliferative neoplasms. Abdel-Wahab O, Pardanani A, Rampal R, Lasho TL, Levine RL, Tefferi A, Leukemia 2011 25 7 1219 1220 10.1038/leu.2011.82 21519343
14. DNMT3A mutations in acute myeloid leukemia. Ley TJ, Ding L, Walter MJ, McLellan MD, Lamprecht T, Larson DE, Kandoth C, Payton JE, Baty J, Welch J, et al. N Engl J Med 2010 363 25 2424 2433 10.1056/NEJMoa1005143 21067377
15. MDS and secondary AML display unique patterns and abundance of aberrant DNA methylation. Figueroa ME, Skrabanek L, Li Y, Jiemjit A, Fandy TE, Paietta E, Fernandez H, Tallman MS, Greally JM, Carraway H, et al. Blood 2009 114 16 3448 3458 10.1182/blood-2009-01-200519 19652201
16. Aberrant DNA methylation is a dominant mechanism in MDS progression to AML. Jiang Y, Dunbar A, Gondek LP, Mohan S, Rataul M, O'Keefe C, Sekeres M, Saunthararajah Y, Maciejewski JP, Blood 2009 113 6 1315 1325 10.1182/blood-2008-06-163246 18832655
17. Impaired hydroxylation of 5-methylcytosine in myeloid cancers with mutant TET2. Ko M, Huang Y, Jankowska AM, Pape UJ, Tahiliani M, Bandukwala HS, An J, Lamperti ED, Koh KP, Ganetzky R, et al. Nature 2010 468 7325 839 843 10.1038/nature09586 21057493
18. ASXL1 mutations promote myeloid transformation through loss of PRC2-mediated gene repression. Abdel-Wahab O, Adli M, LaFave LM, Gao J, Hricik T, Shih AH, Pandey S, Patel JP, Chung YR, Koche R, et al. Cancer cell 2012 22 2 180 193 10.1016/j.ccr.2012.06.032 22897849
19. Somatic mutations altering EZH2 (Tyr641) in follicular and diffuse large B-cell lymphomas of germinal-center origin. Morin RD, Johnson NA, Severson TM, Mungall AJ, An J, Goya R, Paul JE, Boyle M, Woolcock BW, Kuchenbauer F, et al. Nature genetics 2010 42 2 181 185 10.1038/ng.518 20081860
20. JAK2 phosphorylates histone H3Y41 and excludes HP1alpha from chromatin. Dawson MA, Bannister AJ, Gottgens B, Foster SD, Bartke T, Green AR, Kouzarides T, Nature 2009 461 7265 819 822 10.1038/nature08448 19783980
21. Inactivating mutations of acetyltransferase genes in B-cell lymphoma. Pasqualucci L, Dominguez-Sola D, Chiarenza A, Fabbri G, Grunn A, Trifonov V, Kasper LH, Lerach S, Tang H, Ma J, et al. Nature 2011 471 7337 189 195 10.1038/nature09730 21390126
22. CREBBP mutations in relapsed acute lymphoblastic leukaemia. Mullighan CG, Zhang J, Kasper LH, Lerach S, Payne-Turner D, Phillips LA, Heatley SL, Holmfeldt L, Collins-Underwood JR, Ma J, et al. Nature 2011 471 7337 235 239 10.1038/nature09727 21390130
23. DNA methylation patterns and epigenetic memory. Bird A, Genes deve 2002 16 1 6 21 10.1101/gad.947102
24. DNA methylation: roles in mammalian development. Smith ZD, Meissner A, Nat Rev Genet 2013 14 3 204 220 23400093
25. An evaluation of new criteria for CpG islands in the human genome as gene markers. Wang Y, Leung FC, Bioinformatics 2004 20 7 1170 1177 10.1093/bioinformatics/bth059 14764558
26. Developmental programming of CpG island methylation profiles in the human genome. Straussman R, Nejman D, Roberts D, Steinfeld I, Blum B, Benvenisty N, Simon I, Yakhini Z, Cedar H, Nat Struct Biol 2009 16 5 564 571 10.1038/nsmb.1594
27. DNA methylation landscapes: provocative insights from epigenomics. Suzuki MM, Bird A, Nat Rev Genet 2008 9 6 465 476 10.1038/nrg2341 18463664
28. A genome-wide study of DNA methylation patterns and gene expression levels in multiple human and chimpanzee tissues. Pai AA, Bell JT, Marioni JC, Pritchard JK, Gilad Y, PLoS genetics 2011 7 2 1001316 10.1371/journal.pgen. 1001316 21383968
29. Divergent whole-genome methylation maps of human and chimpanzee brains reveal epigenetic basis of human regulatory evolution. Zeng J, Konopka G, Hunt BG, Preuss TM, Geschwind D, Yi SV, Am J Hum Genet 2012 91 3 455 465 10.1016/j.ajhg.2012.07.024 22922032
30. Genome-wide evolutionary analysis of eukaryotic DNA methylation. Zemach A, McDaniel IE, Silva P, Zilberman D, Science 2010 328 5980 916 919 10.1126/science.1186366 20395474
31. On the presence and role of human gene-body DNA methylation. Jjingo D, Conley AB, Yi SV, Lunyak VV, Jordan IK, Oncotarget 2012 3 4 462 474 22577155
32. CTCF-promoted RNA polymerase II pausing links DNA methylation to splicing. Shukla S, Kavak E, Gregory M, Imashimizu M, Shutinoski B, Kashlev M, Oberdoerffer P, Sandberg R, Oberdoerffer S, Nature 2011 479 7371 74 79 10.1038/nature10442 21964334
33. Effect of CpG methylation at different sequence context on acrolein- and BPDE-DNA binding and mutagenesis. Wang HT, Weng MW, Chen WC, Yobin M, Pan J, Chung FL, Wu XR, Rom W, Tang MS, Carcinogenesis 2013 34 1 220 227 10.1093/carcin/bgs323 23042304
34. Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription. Jones PL, Veenstra GJ, Wade PA, Vermaak D, Kass SU, Landsberger N, Strouboulis J, Wolffe AP, Nature genetics 1998 19 2 187 191 10.1038/561 9620779
35. Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nan X, Ng HH, Johnson CA, Laherty CD, Turner BM, Eisenman RN, Bird A, Nature 1998 393 6683 386 389 10.1038/30764 9620804
36. Targeting DNA methylation. Issa JP, Kantarjian HM, Clin Cancer Res 2009 15 12 3938 3946 10.1158/1078-0432.CCR-08-2783 19509174
37. Regulation of mammalian DNA methyltransferases: a route to new mechanisms. Denis H, Ndlovu MN, Fuks F, EMBO reports 2011 12 7 647 656 10.1038/embor.2011.110 21660058
38. DNA methylation in cancer development, diagnosis and therapy-multiple opportunities for genotoxic agents to act as methylome disruptors or remediators. Lewandowska J, Bartoszek A, Mutagenesis 2011 26 4 475 487 10.1093/mutage/ger019 21551264
39. Active DNA demethylation: many roads lead to Rome. Wu SC, Zhang Y, Nat Rev Mol Cell Biol 2010 11 9 607 620 10.1038/nrm2950 20683471
40. Epigenetic modifications and human pathologies: cancer and CVD. Duthie SJ, Proc Nutr Soc 2011 70 1 47 56 10.1017/S0029665110003952 21067630
41. DNA methylation and cancer. Jones PA, Oncogene 2002 21 35 5358 5360 10.1038/sj.onc.1205597 12154398
42. Pretreatment dietary intake is associated with tumor suppressor DNA methylation in head and neck squamous cell carcinomas. Colacino JA, Arthur AE, Dolinoy DC, Sartor MA, Duffy SA, Chepeha DB, Bradford CR, Walline HM, McHugh JB, D'Silva N, et al. Epigenetics 2012 7 8 883 891 10.4161/epi.21038 22722388
43. DNA methylation signatures identify biologically distinct subtypes in acute myeloid leukemia. Figueroa ME, Lugthart S, Li Y, Erpelinck-Verschueren C, Deng X, Christos PJ, Schifano E, Booth J, Van Putten W, Skrabanek L, et al. Cancer cell 2010 17 1 13 27 10.1016/j.ccr.2009.11.020 20060365
44. Recurring mutations found by sequencing an acute myeloid leukemia genome. Mardis ER, Ding L, Dooling DJ, Larson DE, McLellan MD, Chen K, Koboldt DC, Fulton RS, Delehaunty KD, McGrath SD, et al. N Engl J Med 2009 361 11 1058 1066 10.1056/NEJMoa0903840 19657110
45. IDH1 and IDH2 gene mutations identify novel molecular subsets within de novo cytogenetically normal acute myeloid leukemia: a Cancer and Leukemia Group B study. Marcucci G, Maharry K, Wu YZ, Radmacher MD, Mrozek K, Margeson D, Holland KB, Whitman SP, Becker H, Schwind S, et al. Asia Pac J Clin Oncol 2010 28 14 2348 2355
46. The common feature of leukemia-associated IDH1 and IDH2 mutations is a neomorphic enzyme activity converting alpha-ketoglutarate to 2-hydroxyglutarate. Ward PS, Patel J, Wise DR, Abdel-Wahab O, Bennett BD, Coller HA, Cross JR, Fantin VR, Hedvat CV, Perl AE, et al. Cancer cell 2010 17 3 225 234 10.1016/j.ccr.2010.01.020 20171147
47. Base-pair resolution DNA methylation sequencing reveals profoundly divergent epigenetic landscapes in acute myeloid leukemia. Akalin A, Garrett-Bakelman FE, Kormaksson M, Busuttil J, Zhang L, Khrebtukova I, Milne TA, Huang Y, Biswas D, Hess JL, et al. PLoS genetics 2012 8 6 1002781 10.1371/journal.pgen.1002781 22737091
48. Oncometabolite 2-hydroxyglutarate is a competitive inhibitor of alpha-ketoglutarate-dependent dioxygenases. Xu W, Yang H, Liu Y, Yang Y, Wang P, Kim SH, Ito S, Yang C, Wang P, Xiao MT, et al. Cancer cell 2011 19 1 17 30 10.1016/j.ccr.2010.12.014 21251613
49. Leukemic IDH1 and IDH2 mutations result in a hypermethylation phenotype, disrupt TET2 function, and impair hematopoietic differentiation. Figueroa ME, Abdel-Wahab O, Lu C, Ward PS, Patel J, Shih A, Li Y, Bhagwat N, Vasanthakumar A, Fernandez HF, et al. Cancer cell 2010 18 6 553 567 10.1016/j.ccr.2010.11.015 21130701
50. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Tahiliani M, Koh KP, Shen Y, Pastor WA, Bandukwala H, Brudno Y, Agarwal S, Iyer LM, Liu DR, Aravind L, et al. Science 2009 324 5929 930 935 10.1126/science.1170116 19372391
51. Tet-Mediated Formation of 5-Carboxylcytosine and Its Excision by TDG in Mammalian DNA. He Y-F, Li B-Z, Li Z, Liu P, Wang Y, Tang Q, Ding J, Jia Y, Chen Z, Li L, et al. Science 2011 333 6047 1303 1307 10.1126/science.1210944 21817016
52. Tet Proteins Can Convert 5-Methylcytosine to 5-Formylcytosine and 5-Carboxylcytosine. Ito S, Shen L, Dai Q, Wu SC, Collins LB, Swenberg JA, He C, Zhang Y, Science 2011 333 6047 1300 1303 10.1126/science.1210597 21778364
53. Thymine DNA glycosylase can rapidly excise 5-formylcytosine and 5-carboxylcytosine: potential implications for active demethylation of CpG sites. Maiti A, Drohat AC, J Biol Chem 2011 286 41 35334 35338 10.1074/jbc.C111.284620 21862836
54. Oxidative damage to methyl-CpG sequences inhibits the binding of the methyl-CpG binding domain (MBD) of methyl-CpG binding protein 2 (MeCP2). Valinluck V, Tsai HH, Rogstad DK, Burdzy A, Bird A, Sowers LC, Nucleic Acids Res 2004 32 14 4100 4108 10.1093/nar/gkh739 15302911
55. Mbd3/NURD complex regulates expression of 5-hydroxymethylcytosine marked genes in embryonic stem cells. Yildirim O, Li R, Hung JH, Chen PB, Dong X, Ee LS, Weng Z, Rando OJ, Fazzio TG, Cell 2011 147 7 1498 1510 10.1016/j.cell.2011. 11.054 22196727
56. Dynamic regulation of 5-hydroxymethylcytosine in mouse ES cells and during differentiation. Ficz G, Branco MR, Seisenberger S, Santos F, Krueger F, Hore TA, Marques CJ, Andrews S, Reik W, Nature 2011 473 7347 398 402 10.1038/nature10008 21460836
57. Base-resolution analysis of 5-hydroxymethylcytosine in the mammalian genome. Yu M, Hon GC, Szulwach KE, Song CX, Zhang L, Kim A, Li X, Dai Q, Shen Y, Park B, et al. Cell 2012 149 6 1368 1380 10.1016/j.cell.2012.04.027 22608086
58. Prognostic relevance of integrated genetic profiling in acute myeloid leukemia. Patel JP, Gonen M, Figueroa ME, Fernandez H, Sun Z, Racevskis J, Van Vlierberghe P, Dolgalev I, Thomas S, Aminova O, et al. N Engl J Med 2012 366 12 1079 1089 10.1056/NEJMoa1112304 22417203
59. IDH1 and IDH2 mutations are frequent genetic alterations in acute myeloid leukemia and confer adverse prognosis in cytogenetically normal acute myeloid leukemia with NPM1 mutation without FLT3 internal tandem duplication. Paschka P, Schlenk RF, Gaidzik VI, Habdank M, Kronke J, Bullinger L, Spath D, Kayser S, Zucknick M, Gotze K, et al. J Clin Oncol 2010 28 22 3636 3643 10.1200/JCO.2010.28.3762 20567020
60. The oncometabolite 2-hydroxyglutarate inhibits histone lysine demethylases. Chowdhury R, Yeoh KK, Tian YM, Hillringhaus L, Bagg EA, Rose NR, Leung IK, Li XS, Woon EC, Yang M, et al. EMBO reports 2011 12 5 463 469 10.1038/embor.2011.43 21460794
61. Transformation by the (R)-enantiomer of 2-hydroxyglutarate linked to EGLN activation. Koivunen P, Lee S, Duncan CG, Lopez G, Lu G, Ramkissoon S, Losman JA, Joensuu P, Bergmann U, Gross S, et al. Nature 2012 483 7390 484 488 10.1038/nature10898 22343896
62. (R)-2-hydroxyglutarate is sufficient to promote leukemogenesis and its effects are reversible. Losman JA, Looper RE, Koivunen P, Lee S, Schneider RK, McMahon C, Cowley GS, Root DE, Ebert BL, Kaelin WG Jr, Science 2013 339 6127 1621 1625 10.1126/science.1231677 23393090
63. Signals and combinatorial functions of histone modifications. Suganuma T, Workman JL, Annu Rev Biochem 2011 80 473 499 10.1146/annurev-biochem-061809- 175347 21529160
64. Nucleosome structural studies. Tan S, Davey CA, Curr Opin Struct Biol 2011 21 1 128 136 10.1016/j.sbi.2010.11.006 21176878
65. A method for genetically installing site-specific acetylation in recombinant histones defines the effects of H3 K56 acetylation. Neumann H, Hancock SM, Buning R, Routh A, Chapman L, Somers J, Owen-Hughes T, Van Noort J, Rhodes D, Chin JW, Molecular cell 2009 36 1 153 163 10.1016/j.molcel.2009.07.027 19818718
66. Differential expression of histone deacetylases HDAC1, 2 and 3 in human breast cancer-overexpression of HDAC2 and HDAC3 is associated with clinicopathological indicators of disease progression. Muller BM, Jana L, Kasajima A, Lehmann A, Prinzler J, Budczies J, Winzer KJ, Dietel M, Weichert W, Denkert C, BMC cancer 2013 13 1 215 10.1186/1471-2407-13-215 23627572
67. Bromodomains as therapeutic targets in cancer. Barbieri I, Cannizzaro E, Dawson MA, Brief Funct Genomic 2013 12 3 219 230 10.1093/bfgp/elt007
68. Targeting specific HATs for neurodegenerative disease treatment: translating basic biology to therapeutic possibilities. Pirooznia SK, Elefant F, Front cellular neuroscience 2013 7 30
69. Translating the histone code. Jenuwein T, Allis CD, Science 2001 293 5532 1074 1080 10.1126/science.1063127 11498575
70. OPERating ON Chromatin, a Colorful Language where Context Matters. Gardner KE, Allis CD, Strahl BD, J Mol Biol 2011 409 1 36 46 10.1016/j.jmb.2011.01.040 21272588
71. Chromatin modifying activity of leukaemia associated fusion proteins. Di Croce L, Hum Mol Genet 2005 1 77 84
72. Chromatin remodeling and cancer, Part I: Covalent histone modifications. Wang GG, Allis CD, Chi P, Trends Mol Med 2007 13 9 363 372 10.1016/j.molmed. 2007.07.003 17822958
73. Histone deacetylases: a common molecular target for differentiation treatment of acute myeloid leukemias? Minucci S, Nervi C, Lo Coco F, Pelicci PG, Oncogene 2001 20 24 3110 3115 10.1038/sj.onc.1204336 11420727
74. Increased HDAC1 deposition at hematopoietic promoters in AML and its association with patient survival. Tickenbrock L, Klein HU, Trento C, Hascher A, Gollner S, Baumer N, Kuss R, Agrawal S, Bug G, Serve H, et al. Leukemia research 2011 35 5 620 625 10.1016/j.leukres.2010.11.006 21176959
75. Histone acetylation and disease. Timmermann S, Lehrmann H, Polesskaya A, Harel-Bellan A, Cell Mol Life Sci 2001 58 5-6 728 736 11437234
76. ETO, fusion partner in t(8;21) acute myeloid leukemia, represses transcription by interaction with the human N-CoR/mSin3/HDAC1 complex. Wang J, Hoshino T, Redner RL, Kajigaya S, Liu JM, Proc Natl Acad Sci USA 1998 95 18 10860 10865 10.1073/pnas.95.18.10860 9724795
77. Role of the histone deacetylase complex in acute promyelocytic leukaemia. Lin RJ, Nagy L, Inoue S, Shao W, Miller WH Jr, Evans RM, Nature 1998 391 6669 811 814 10.1038/35895 9486654
78. HDAC isoenzyme expression is deregulated in chronic lymphocytic leukemia B-cells and has a complex prognostic significance. Van Damme M, Crompot E, Meuleman N, Mineur P, Bron D, Lagneaux L, Stamatopoulos B, Epigenetics 2012 7 12 1403 1412 10.4161/epi.22674 23108383
79. Altered Hox expression and segmental identity in Mll-mutant mice. Yu BD, Hess JL, Horning SE, Brown GA, Korsmeyer SJ, Nature 1995 378 6556 505 508 10.1038/378505a0 7477409
80. Growth disturbance in fetal liver hematopoiesis of Mll-mutant mice. Yagi H, Deguchi K, Aono A, Tani Y, Kishimoto T, Komori T, Blood 1998 92 1 108 117 9639506
81. Truncation of the Mll gene in exon 5 by gene targeting leads to early preimplantation lethality of homozygous embryos. Ayton P, Sneddon SF, Palmer DB, Rosewell IR, Owen MJ, Young B, Presley R, Subramanian V, Genesis 2001 30 4 201 212 10.1002/gene.1066 11536426
82. Identification of a gene, MLL, that spans the breakpoint in 11q23 translocations associated with human leukemias. Ziemin-vanderPoel S, McCabe NR, Gill HJ, Espinosa R, Patel Y III, Harden A, Rubinelli P, Smith SD, LeBeau MM, Rowley JD, et al. Proc Natl Acad Sci USA 1991 88 23 10735 10739 10.1073/pnas.88.23.10735 1720549
83. MLL targets SET domain methyltransferase activity to Hox gene promoters. Milne TA, Briggs SD, Brock HW, Martin ME, Gibbs D, Allis CD, Hess JL, Molecular cell 2002 10 5 1107 1117 10.1016/S1097-2765(02)00741-4 12453418
84. Mixed lineage leukemia: a structure-function perspective of the MLL1 protein. Cosgrove MS, Patel A, The FEBS journal 2010 277 8 1832 1842 10.1111/j.1742-4658.2010.07609.x 20236310
85. MLL translocations, histone modifications and leukaemia stem-cell development. Krivtsov AV, Armstrong SA, Nat Rev Cancer 2007 7 11 823 833 10.1038/nrc2253 17957188
86. Mechanisms of leukemogenesis by MLL fusion proteins. Marschalek R, Br J Haematol 2011 152 2 141 154 10.1111/j.1365-2141.2010.08459.x 21118195
87. Chromatin-related properties of CBP fused to MLL generate a myelodysplastic-like syndrome that evolves into myeloid leukemia. Lavau C, Du C, Thirman M, Zeleznik-Le N, EMBO J 2000 19 17 4655 4664 10.1093/emboj/19.17.4655 10970858
88. The mll-AF9 gene fusion in mice controls myeloproliferation and specifies acute myeloid leukaemogenesis. Dobson CL, Warren AJ, Pannell R, Forster A, Lavenir I, Corral J, Smith AJ, Rabbitts TH, EMBO J 1999 18 13 3564 3574 10.1093/emboj/18.13.3564 10393173
89. The AF10 leucine zipper is required for leukemic transformation of myeloid progenitors by MLL-AF10. DiMartino JF, Ayton PM, Chen EH, Naftzger CC, Young BD, Cleary ML, Blood 2002 99 10 3780 3785 10.1182/blood.V99.10.3780 11986236
90. hDOT1L links histone methylation to leukemogenesis. Okada Y, Feng Q, Lin Y, Jiang Q, Li Y, Coffield VM, Su L, Xu G, Zhang Y, Cell 2005 121 2 167 178 10.1016/j.cell.2005.02.020 15851025
91. Mechanisms of transcriptional repression by histone lysine methylation. Hublitz P, Albert M, Peters AH, Int J Dev Biol 2009 53 2-3 335 354 19412890
92. DOT1L, the H3K79 methyltransferase, is required for MLL-AF9-mediated leukemogenesis. Nguyen AT, Taranova O, He J, Zhang Y, Blood 2011 117 25 6912 6922 10.1182/blood-2011-02-334359 21521783
93. MLL-AF9 and MLL-ENL alter the dynamic association of transcriptional regulators with genes critical for leukemia. Monroe SC, Jo SY, Sanders DS, Basrur V, Elenitoba-Johnson KS, Slany RK, Hess JL, Exp Hematol 2011 39 1 77-86 71-75 20854876
94. Leukaemic transformation by CALM-AF10 involves upregulation of Hoxa5 by hDOT1L. Okada Y, Jiang Q, Lemieux M, Jeannotte L, Su L, Zhang Y, Nat Cell Biol 2006 8 9 1017 1024 10.1038/ncb1464 16921363
95. KDM2b/JHDM1b, an H3K36me2-specific demethylase, is required for initiation and maintenance of acute myeloid leukemia. He J, Nguyen AT, Zhang Y, Blood 2011 117 14 3869 3880 10.1182/blood-2010-10-312736 21310926
96. Randomized controlled trial of azacitidine in patients with the myelodysplastic syndrome: a study of the cancer and leukemia group B. Silverman LR, Demakos EP, Peterson BL, Kornblith AB, Holland JC, Odchimar-Reissig R, Stone RM, Nelson D, Powell BL, DeCastro CM, et al. Int J Clin Oncol 2002 20 10 2429 2440 10.1200/JCO.2002.04.117
97. Decitabine improves patient outcomes in myelodysplastic syndromes: results of a phase III randomized study. Kantarjian H, Issa JP, Rosenfeld CS, Bennett JM, Albitar M, DiPersio J, Klimek V, Slack J, De Castro C, Ravandi F, et al. Cancer 2006 106 8 1794 1803 10.1002/cncr.21792 16532500
98. Phase I study of 5-aza-2′-deoxycytidine in combination with valproic acid in non-small-cell lung cancer. Chu BF, Karpenko MJ, Liu Z, Aimiuwu J, Villalona-Calero MA, Chan KK, Grever MR, Otterson GA, Cancer Chemother Pharmacol 2013 71 1 115 121 10.1007/s00280-012-1986-8 23053268
99. Targeting the MAGE A3 antigen in pancreatic cancer. Cogdill AP, Frederick DT, Cooper ZA, Garber HR, Ferrone CR, Fiedler A, Rosenberg L, Thayer SP, Warshaw AL, Wargo JA, Surgery 2012 152 3 Suppl 1 13 18 22770803
100. 5-Aza-cytidine is a potent inhibitor of DNA methyltransferase 3a and induces apoptosis in HCT-116 colon cancer cells via Gadd45- and p53-dependent mechanisms. Schneider-Stock R, Diab-Assef M, Rohrbeck A, Foltzer-Jourdainne C, Boltze C, Hartig R, Schonfeld P, Roessner A, Gali-Muhtasib H, J Pharmacol Exp Ther 2005 312 2 525 536 15547111
101. Epigenetic modifications as therapeutic targets. Kelly TK, De Carvalho DD, Jones PA, Nature biotechnology 2010 28 10 1069 1078 10.1038/nbt.1678 20944599
102. Cancer DNA methylation: molecular mechanisms and clinical implications. McCabe MT, Brandes JC, Vertino PM, Clin Cancer Res 2009 15 12 3927 3937 10.1158/1078-0432.CCR-08-2784 19509173
103. 5-Azacytidine and 5-aza-2′-deoxycytidine as inhibitors of DNA methylation: mechanistic studies and their implications for cancer therapy. Christman JK, Oncogene 2002 21 35 5483 5495 10.1038/sj.onc.1205699 12154409
104. Concise drug review: azacitidine and decitabine. Derissen EJ, Beijnen JH, Schellens JH, Oncologist 2013 18 5 619 624 10.1634/theoncologist.2012-0465 23671007
105. Clinical studies of histone deacetylase inhibitors. Prince HM, Bishton MJ, Harrison SJ, Clin Cancer Res 2009 15 12 3958 3969 10.1158/1078-0432.CCR-08- 2785 19509172
106. The Rpd3/Hda1 family of lysine deacetylases: from bacteria and yeast to mice and men. Yang X-J, Seto E, Nat Rev Mol Cell Biol 2008 9 3 206 218 10.1038/nrm2346 18292778
107. The therapeutic uses of chromatin-modifying agents. Mai A, Expert Opin Ther Targets 2007 11 6 835 851 10.1517/14728222.11.6.835 17504020
108. Histone deacetylase inhibitors in the treatment of hematological malignancies and solid tumors. Federico M, Bagella L, J Biomed Biotechnol 2011 2011 475641 21188171
109. Curcumin, a novel p300/CREB-binding protein-specific inhibitor of acetyltransferase, represses the acetylation of histone/nonhistone proteins and histone acetyltransferase-dependent chromatin transcription. Balasubramanyam K, Varier RA, Altaf M, Swaminathan V, Siddappa NB, Ranga U, Kundu TK, J Biol Chem 2004 279 49 51163 51171 10.1074/jbc.M409024200 15383533
110. Polyisoprenylated benzophenone, garcinol, a natural histone acetyltransferase inhibitor, represses chromatin transcription and alters global gene expression. Balasubramanyam K, Altaf M, Varier RA, Swaminathan V, Ravindran A, Sadhale PP, Kundu TK, J Biol Chem 2004 279 32 33716 33726 10.1074/jbc.M402839200 15155757
111. Inhibition of histone acetyltransferase activity by anacardic acid sensitizes tumor cells to ionizing radiation. Sun Y, Jiang X, Chen S, Price BD, FEBS Lett 2006 580 18 4353 4356 10.1016/j.febslet.2006.06.092 16844118