Low HOX gene expression in PML-RARα-positive leukemia results from suppressed histone demethylation

References

• Pui CH, Relling MV, Downing JR. Acute lymphoblastic leukemia. N Engl J Med. 2004 Apr 08;350(15):1535–1548. doi:10.1056/NEJMra023001.
   PubMed Web of Science ®Google Scholar
• Manno CS, Chew AJ, Hutchison S, et al. AAV-mediated factor IX gene transfer to skeletal muscle in patients with severe hemophilia B. Blood. 2003 Apr 15;101(8):2963–2972. doi:10.1182/blood-2002-10-3296.
   PubMed Web of Science ®Google Scholar
• Ferrucci PF, Grignani F, Pearson M, et al. Cell death induction by the acute promyelocytic leukemia-specific PML/RARalpha fusion protein. Proc Natl Acad Sci U S A. 1997 Sep 30;94(20):10901–10906. doi:10.1073/pnas.94.20.10901.
   PubMed Web of Science ®Google Scholar
• Collins SJ, Robertson KA, Mueller L. Retinoic acid-induced granulocytic differentiation of HL-60 myeloid leukemia cells is mediated directly through the retinoic acid receptor (RAR-alpha). Mol Cell Biol. 1990 May;10(5):2154–2163. doi:10.1128/MCB.10.5.2154.
   PubMed Web of Science ®Google Scholar
• Zhu J, Gianni M, Kopf E, et al. Retinoic acid induces proteasome-dependent degradation of retinoic acid receptor alpha (RARalpha) and oncogenic RARalpha fusion proteins. Proc Natl Acad Sci U S A. 1999 Dec 21;96(26):14807–14812. doi:10.1073/pnas.96.26.14807.
   PubMed Web of Science ®Google Scholar
• Nervi C, Ferrara FF, Fanelli M, et al. Caspases mediate retinoic acid-induced degradation of the acute promyelocytic leukemia PML/RARalpha fusion protein. Blood. 1998 Oct 01;92(7):2244–2251.
   PubMed Web of Science ®Google Scholar
• Degos L, Dombret H, Chomienne C, et al. All-trans-retinoic acid as a differentiating agent in the treatment of acute promyelocytic leukemia. Blood. 1995 May 15;85(10):2643–2653.
   PubMed Web of Science ®Google Scholar
• Ablain J, de The H. Revisiting the differentiation paradigm in acute promyelocytic leukemia. Blood. 2011 Jun 02;117(22):5795–5802. doi:10.1182/blood-2011-02-329367.
   PubMed Web of Science ®Google Scholar
• Grignani F, Ferrucci PF, Testa U, et al. The acute promyelocytic leukemia-specific PML-RAR alpha fusion protein inhibits differentiation and promotes survival of myeloid precursor cells. Cell. 1993 Aug 13;74(3):423–431. doi:10.1016/0092-8674(93)80044-F.
   PubMed Web of Science ®Google Scholar
• Vitaliano-Prunier A, Halftermeyer J, Ablain J, et al. Clearance of PML/RARA-bound promoters suffice to initiate APL differentiation. Blood. 2014 Dec 11;124(25):3772–3780. doi:10.1182/blood-2014-03-561852.
   PubMed Web of Science ®Google Scholar
• Imaizumi M, Suzuki H, Yoshinari M, et al. Mutations in the E-domain of RAR portion of the PML/RAR chimeric gene may confer clinical resistance to all-trans retinoic acid in acute promyelocytic leukemia. Blood. 1998 Jul 15;92(2):374–382.
   PubMed Web of Science ®Google Scholar
• Ding W, Li YP, Nobile LM, et al. Leukemic cellular retinoic acid resistance and missense mutations in the PML-RARalpha fusion gene after relapse of acute promyelocytic leukemia from treatment with all-trans retinoic acid and intensive chemotherapy. Blood. 1998 Aug 15;92(4):1172–1183.
   PubMed Web of Science ®Google Scholar
• Martens JH, Brinkman AB, Simmer F, et al. PML-RARalpha/RXR alters the epigenetic landscape in acute promyelocytic leukemia. Cancer Cell. 2010 Feb 17;17(2):173–185. doi:10.1016/j.ccr.2009.12.042.
   PubMed Web of Science ®Google Scholar
• Agger K, Cloos PA, Christensen J, et al. UTX and JMJD3 are histone H3K27 demethylases involved in HOX gene regulation and development. Nature. 2007 Oct 11;449(7163):731–734. doi:10.1038/nature06145.
   PubMed Web of Science ®Google Scholar
• Lee MG, Villa R, Trojer P, et al. Demethylation of H3K27 regulates polycomb recruitment and H2A ubiquitination. Science. 2007 Oct 19;318(5849):447–450. doi:10.1126/science.1149042.
   PubMed Web of Science ®Google Scholar
• Skvarova Kramarzova KFK, Mejstrikova E, Rejlova K, et al. Homeobox gene expression in acute myeloid leukemia is linked to typical underlying molecular aberrations. J Hematol Oncol. 2014;7:94. doi:10.1186/s13045-014-0094-0. PMID:25539595
   PubMed Web of Science ®Google Scholar
• Roche J, Zeng C, Baron A, et al. Hox expression in AML identifies a distinct subset of patients with intermediate cytogenetics. Leukemia. 2004 Jun;18(6):1059–1063. doi:10.1038/sj.leu.2403366.
   PubMed Web of Science ®Google Scholar
• Thompson A, Quinn MF, Grimwade D, et al. Global down-regulation of HOX gene expression in PML-RARalpha + acute promyelocytic leukemia identified by small-array real-time PCR. Blood. 2003 Feb 15;101(4):1558–1565. doi:10.1182/blood.V101.4.1558.
   PubMed Web of Science ®Google Scholar
• Kruidenier L, Chung CW, Cheng Z, et al. A selective jumonji H3K27 demethylase inhibitor modulates the proinflammatory macrophage response. Nature. 2012 Aug 16;488(7411):404–408. doi:10.1038/nature11262.
   PubMed Web of Science ®Google Scholar
• Azuara V, Perry P, Sauer S, et al. Chromatin signatures of pluripotent cell lines. Nat Cell Biol. 2006 May;8(5):532–538. doi:10.1038/ncb1403.
   PubMed Web of Science ®Google Scholar
• Bernstein BE, Mikkelsen TS, Xie X, et al. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell. 2006 Apr 21;125(2):315–326. doi:10.1016/j.cell.2006.02.041.
   PubMed Web of Science ®Google Scholar
• Tsumagari K, Baribault C, Terragni J, et al. DNA methylation and differentiation: HOX genes in muscle cells. Epigenetics Chromatin. 2013 Aug 02;6(1):25. doi:10.1186/1756-8935-6-25.
   PubMedGoogle Scholar
• Wei J, Zhai L, Xu J, et al. Role of Bmi1 in H2A ubiquitylation and Hox gene silencing. J Biol Chem. 2006 Aug 11;281(32):22537–22544. doi:10.1074/jbc.M600826200.
   PubMed Web of Science ®Google Scholar
• Beuchle D, Struhl G, Muller J. Polycomb group proteins and heritable silencing of Drosophila Hox genes. Development. 2001 Mar;128(6):993–1004.
   PubMed Web of Science ®Google Scholar
• Wang J, Mager J, Schnedier E, et al. The mouse PcG gene eed is required for Hox gene repression and extraembryonic development. Mamm Genome. 2002 Sep;13(9):493–503. doi:10.1007/s00335-002-2182-7.
   PubMed Web of Science ®Google Scholar
• Khan SN, Jankowska AM, Mahfouz R, et al. Multiple mechanisms deregulate EZH2 and histone H3 lysine 27 epigenetic changes in myeloid malignancies. Leukemia. 2013 Jun;27(6):1301–1309. doi:10.1038/leu.2013.80.
   PubMed Web of Science ®Google Scholar
• Milne TA, Briggs SD, Brock HW, et al. MLL targets SET domain methyltransferase activity to Hox gene promoters. Mol Cell. 2002 Nov;10(5):1107–1117. doi:10.1016/S1097-2765(02)00741-4.
   PubMed Web of Science ®Google Scholar
• Hanson RD, Hess JL, Yu BD, et al. Mammalian Trithorax and polycomb-group homologues are antagonistic regulators of homeotic development. Proc Natl Acad Sci U S A. 1999 Dec 07;96(25):14372–14377. doi:10.1073/pnas.96.25.14372.
   PubMed Web of Science ®Google Scholar
• Rocha-Viegas L, Villa R, Gutierrez A, et al. Role of UTX in retinoic acid receptor-mediated gene regulation in leukemia. Mol Cell Biol. 2014 Oct 01;34(19):3765–3775. doi:10.1128/MCB.00839-14.
   PubMed Web of Science ®Google Scholar
• Issaeva I, Zonis Y, Rozovskaia T, et al. Knockdown of ALR (MLL2) reveals ALR target genes and leads to alterations in cell adhesion and growth. Mol Cell Biol. 2007 Mar;27(5):1889–1903. doi:10.1128/MCB.01506-06.
   PubMed Web of Science ®Google Scholar
• He LZ, Tribioli C, Rivi R, et al. Acute leukemia with promyelocytic features in PML/RARalpha transgenic mice. Proc Natl Acad Sci U S A. 1997 May 13;94(10):5302–5307. doi:10.1073/pnas.94.10.5302.
   PubMed Web of Science ®Google Scholar
• Lin RJ, Nagy L, Inoue S, et al. Role of the histone deacetylase complex in acute promyelocytic leukaemia. Nature. 1998 Feb 19;391(6669):811–814. doi:10.1038/35895.
   PubMed Web of Science ®Google Scholar
• Grignani F, De Matteis S, Nervi C, et al. Fusion proteins of the retinoic acid receptor-alpha recruit histone deacetylase in promyelocytic leukaemia. Nature. 1998 Feb 19;391(6669):815–818. doi:10.1038/35901.
   PubMed Web of Science ®Google Scholar
• Di Croce L, Raker VA, Corsaro M, et al. Methyltransferase recruitment and DNA hypermethylation of target promoters by an oncogenic transcription factor. Science. 2002 Feb 08;295(5557):1079–1082. doi:10.1126/science.1065173.
   PubMed Web of Science ®Google Scholar
• Giampaolo A, Felli N, Diverio D, et al. Expression pattern of HOXB6 homeobox gene in myelomonocytic differentiation and acute myeloid leukemia. Leukemia. 2002 Jul;16(7):1293–1301. doi:10.1038/sj.leu.2402532.
   PubMed Web of Science ®Google Scholar
• Alharbi RA, Pettengell R, Pandha HS, et al. The role of HOX genes in normal hematopoiesis and acute leukemia. Leukemia. 2013 Apr;27(5):1000–1008. doi:10.1038/leu.2012.356.
   PubMed Web of Science ®Google Scholar
• Cole CB, Verdoni AM, Ketkar S, et al. PML-RARA requires DNA methyltransferase 3A to initiate acute promyelocytic leukemia. J Clin Invest. 2016 Jan;126(1):85–98. doi:10.1172/JCI82897.
   PubMed Web of Science ®Google Scholar
• Ntziachristos P, Tsirigos A, Welstead GG, et al. Contrasting roles of histone 3 lysine 27 demethylases in acute lymphoblastic leukaemia. Nature. 2014 Oct 23;514(7523):513–517. doi:10.1038/nature13605.
   PubMed Web of Science ®Google Scholar
• Lanotte M, Martin-Thouvenin V, Najman S, et al. NB4, a maturation inducible cell line with t(15;17) marker isolated from a human acute promyelocytic leukemia (M3). Blood. 1991 Mar 01;77(5):1080–1086.
   PubMed Web of Science ®Google Scholar
• Duprez E, Benoit G, Flexor M, et al. A mutated PML/RARA found in the retinoid maturation resistant NB4 subclone, NB4-R2, blocks RARA and wild-type PML/RARA transcriptional activities. Leukemia. 2000 Feb;14(2):255–261. doi:10.1038/sj.leu.2401683.
   PubMed Web of Science ®Google Scholar
• Rosenauer A, Raelson JV, Nervi C, et al. Alterations in expression, binding to ligand and DNA, and transcriptional activity of rearranged and wild-type retinoid receptors in retinoid-resistant acute promyelocytic leukemia cell lines. Blood. 1996 Oct 01;88(7):2671–2682.
   PubMed Web of Science ®Google Scholar
• Drabkin HA, Parsy C, Ferguson K, et al. Quantitative HOX expression in chromosomally defined subsets of acute myelogenous leukemia. Leukemia. 2002 Feb;16(2):186–195. doi:10.1038/sj.leu.2402354.
   PubMed Web of Science ®Google Scholar
• Starkova J, Zamostna B, Mejstrikova E, et al. HOX gene expression in phenotypic and genotypic subgroups and low HOXA gene expression as an adverse prognostic factor in pediatric ALL. Pediatr Blood Cancer. 2010 Dec 01;55(6):1072–1082. doi:10.1002/pbc.22749.
   PubMed Web of Science ®Google Scholar
• Das ND, Jung KH, Choi MR, et al. Gene networking and inflammatory pathway analysis in a JMJD3 knockdown human monocytic cell line. Cell Biochem Funct. 2012 Apr;30(3):224–232. doi:10.1002/cbf.1839.
   PubMed Web of Science ®Google Scholar
• Yang J, Fang X. [Expression of DNMT1, DNMT3a, and DNMT3b in eutopic endometrium]. Zhong Nan Da Xue Xue Bao Yi Xue Ban. 2012 Jan;37(1):94–99.
   PubMedGoogle Scholar
• Liu J, Mercher T, Scholl C, et al. A functional role for the histone demethylase UTX in normal and malignant hematopoietic cells. Exp Hematol. 2012 Jun;40(6):487–498. doi:10.1016/j.exphem.2012.01.017.
   PubMed Web of Science ®Google Scholar
• Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Meth. 2012 Mar 04;9(4):357–359. doi:10.1038/nmeth.1923.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Liu T, Meyer CA, et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 2008;9(9):R137. doi:10.1186/gb-2008-9-9-r137. PMID:18798982
   PubMed Web of Science ®Google Scholar
• Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics. 2010 Mar 15;26(6):841–842. doi:10.1093/bioinformatics/btq033.
   PubMed Web of Science ®Google Scholar