Epigenetic regulation of fetal globin gene expression in adult erythroid cells

Scarano, 1967, The heterogeneity of thymine methyl group origin in DNA pyrimidine isostichs of developing sea urchin embryos, Proc Natl Acad Sci U S A, 57, 1394, 10.1073/pnas.57.5.1394 Holliday, 1975, DNA modification mechanisms and gene activity during development, Science, 187, 226, 10.1126/science.1111098 Riggs, 1975, X inactivation, differentiation, and DNA methylation, Cytogenet Cell Genet, 14, 9, 10.1159/000130315 McGhee, 1979, Specific DNA methylation sites in the vicinity of the chicken beta-globin genes, Nature, 280, 419, 10.1038/280419a0 Razin, 1980, DNA methylation and gene function, Science, 210, 604, 10.1126/science.6254144 Shen, 1980, Tissue-specific DNA methylation in a cluster of rabbit beta-like globin genes, Proc Natl Acad Sci U S A, 77, 6634, 10.1073/pnas.77.11.6634 van der Ploeg, 1980, DNA methylation in the human gamma delta beta-globin locus in erythroid and nonerythroid tissues, Cell, 19, 947, 10.1016/0092-8674(80)90086-0 Jenuwein, 2001, Translating the histone code, Science, 293, 1074, 10.1126/science.1063127 Berger, 2002, Histone modifications in transcriptional regulation, Curr Opin Genet Dev, 12, 142, 10.1016/S0959-437X(02)00279-4 Britton, 2011, Breaking the histone code with quantitative mass spectrometry, Expert Rev Proteomics, 8, 631, 10.1586/epr.11.47 Zentner, 2013, Regulation of nucleosome dynamics by histone modifications, Nat Struct Mol Biol, 20, 259, 10.1038/nsmb.2470 Sankaran, 2009, Developmental and species-divergent globin switching are driven by BCL11A, Nature, 460, 1093, 10.1038/nature08243 Stamatoyannopoulos, 2005, Prospects for developing a molecular cure for thalassemia, Hematology, 10, 255, 10.1080/10245330512331390627 Porcu, 1997, The human beta globin locus introduced by YAC transfer exhibits a specific and reproducible pattern of developmental regulation in transgenic mice, Blood, 90, 4602, 10.1182/blood.V90.11.4602 Pope, 2000, Two-phase liquid culture system models normal human adult erythropoiesis at the molecular level, Eur J Haematol, 64, 292, 10.1034/j.1600-0609.2000.90032.x Fibach, 2005, Differentiation of human erythroid cells in culture, Curr Protoc Immunol, Chapter 22, 10.1002/0471142735.im22f07s69 DeSimone, 1978, Stimulation of fetal hemoglobin synthesis in baboons by hemolysis and hypoxia, Proc Natl Acad Sci U S A, 75, 2937, 10.1073/pnas.75.6.2937 Thein, 2007, Intergenic variants of HBS1L-MYB are responsible for a major quantitative trait locus on chromosome 6q23 influencing fetal hemoglobin levels in adults, Proc Natl Acad Sci U S A, 104, 11346, 10.1073/pnas.0611393104 Sankaran, 2008, Human fetal hemoglobin expression is regulated by the developmental stage-specific repressor BCL11A, Science, 322, 1839, 10.1126/science.1165409 Sankaran, 2011, A functional element necessary for fetal hemoglobin silencing, N Engl J Med, 365, 807, 10.1056/NEJMoa1103070 Yi, 2006, Sox6 directly silences epsilon globin expression in definitive erythropoiesis, PLoS Genet, 2, e14, 10.1371/journal.pgen.0020014 Xu, 2010, Transcriptional silencing of {gamma}-globin by BCL11A involves long-range interactions and cooperation with SOX6, Genes Dev, 24, 783, 10.1101/gad.1897310 Miller, 1993, A novel, erythroid cell-specific murine transcription factor that binds to the CACCC element and is related to the kruppel family of nuclear proteins, Mol Cell Biol, 13, 2776, 10.1128/MCB.13.5.2776 Wijgerde, 1996, The role of EKLF in human beta-globin gene competition, Genes Dev, 10, 2894, 10.1101/gad.10.22.2894 Zhou, 2006, Differential binding of erythroid krupple-like factor to embryonic/fetal globin gene promoters during development, J Biol Chem, 281, 16052, 10.1074/jbc.M601182200 Borg, 2010, Haploinsufficiency for the erythroid transcription factor KLF1 causes hereditary persistence of fetal hemoglobin, Nat Genet, 42, 801, 10.1038/ng.630 Zhou, 2010, KLF1 regulates BCL11A expression and gamma- to beta-globin gene switching, Nat Genet, 42, 742, 10.1038/ng.637 Jiang, 2006, cMYB is involved in the regulation of fetal hemoglobin production in adults, Blood, 108, 1077, 10.1182/blood-2006-01-008912 Lettre, 2008, DNA polymorphisms at the BCL11A, HBS1L-MYB, and beta-globin loci associate with fetal hemoglobin levels and pain crises in sickle cell disease, Proc Natl Acad Sci U S A, 105, 11869, 10.1073/pnas.0804799105 Sankaran, 2011, MicroRNA-15a and -16-1 act via MYB to elevate fetal hemoglobin expression in human trisomy 13, Proc Natl Acad Sci U S A, 108, 1519, 10.1073/pnas.1018384108 Harju-Baker, 2008, Silencing of Agamma-globin gene expression during adult definitive erythropoiesis mediated by GATA1-FOG1-Mi2 complex binding at the -566 GATA site, Mol Cell Biol, 28, 3101, 10.1128/MCB.01858-07 Miccio, 2010, NuRD mediates activating and repressive functions of GATA1 and FOG1 during blood development, EMBO J, 29, 442, 10.1038/emboj.2009.336 Miccio, 2010, Role of the GATA1/FOG1/NuRD pathway in the expression of human beta-like globin genes, Mol Cell Biol, 30, 3460, 10.1128/MCB.00001-10 Costa, 2012, Mi2beta is required for gamma-globin gene silencing: temporal assembly of a GATA1-FOG1-Mi2 repressor complex in beta-YAC transgenic mice, PLoS Genet, 8, e1003155, 10.1371/journal.pgen.1003155 Zhou, 2004, The role of p22 NF-E4 in human globin gene switching, J Biol Chem, 279, 26227, 10.1074/jbc.M402191200 Tanabe, 2007, Embryonic and fetal beta-globin gene repression by the orphan nuclear receptors, TR2 and TR4, EMBO J, 26, 2295, 10.1038/sj.emboj.7601676 Campbell, 2011, Forced TR2/TR4 expression in sickle cell disease mice confers enhanced fetal hemoglobin synthesis and alleviated disease phenotypes, Proc Natl Acad Sci U S A, 108, 18808, 10.1073/pnas.1104964108 Bank, 2006, Regulation of human fetal hemoglobin: new players, new complexities, Blood, 107, 435, 10.1182/blood-2005-05-2113 Sankaran, 2010, Advances in the understanding of haemoglobin switching, Br J Haematol, 149, 181, 10.1111/j.1365-2141.2010.08105.x Tate, 1993, Effects of DNA methylation on DNA-binding proteins and gene expression, Curr Opin Genet Dev, 3, 226, 10.1016/0959-437X(93)90027-M Pikaart, 1998, Loss of transcriptional activity of a transgene is accompanied by DNAmethylation and histone deacetylation and is prevented by insulators, Genes Dev, 12, 2852, 10.1101/gad.12.18.2852 DeSimone, 1982, 5-Azacytidine stimulates fetal hemoglobin synthesis in anemic baboons, Proc Natl Acad Sci U S A, 79, 4428, 10.1073/pnas.79.14.4428 Ley, 1982, 5-Azacytidine selectively increases gamma-globin synthesis in a patient with beta+ thalassemia, N Engl J Med, 307, 1469, 10.1056/NEJM198212093072401 Charache, 1983, Treatment of sickle cell anemia with 5-azacytidine results in increased fetal hemoglobin production and is associated with nonrandom hypomethylation of DNA around the gamma-delta-beta-globin gene complex, Proc Natl Acad Sci U S A, 80, 4842, 10.1073/pnas.80.15.4842 Lowrey, 1993, Brief report: treatment with azacitidine of patients with end-stage beta-thalassemia, N Engl J Med, 329, 845, 10.1056/NEJM199309163291205 Letvin, 1984, Augmentation of fetal-hemoglobin production in anemic monkeys by hydroxyurea, N Engl J Med, 310, 869, 10.1056/NEJM198404053101401 Papayannopoulou, 1984, Arabinosylcytosine induces fetal hemoglobin in baboons by perturbing erythroid cell differentiation kinetics, Science, 224, 617, 10.1126/science.6200940 Platt, 1984, Hydroxyurea enhances fetal hemoglobin production in sickle cell anemia, J Clin Invest, 74, 652, 10.1172/JCI111464 Torrealba-de Ron, 1984, Perturbations in the erythroid marrow progenitor cell pools may play a role in the augmentation of HbF by 5-azacytidine, Blood, 63, 201, 10.1182/blood.V63.1.201.201 Mabaera, 2008, Neither DNA hypomethylation nor changes in the kinetics of erythroid differentiation explain 5-azacytidine's ability to induce human fetal hemoglobin, Blood, 111, 411, 10.1182/blood-2007-06-093948 Lavelle, 2004, The molecular mechanism of fetal hemoglobin reactivation, Semin Hematol, 41, 3, 10.1053/j.seminhematol.2004.08.002 Goren, 2006, Fine tuning of globin gene expression by DNA methylation, PLoS ONE, 1, e46, 10.1371/journal.pone.0000046 Rupon, 2006, Methyl binding domain protein 2 mediates gamma-globin gene silencing in adult human betaYAC transgenic mice, Proc Natl Acad Sci U S A, 103, 6617, 10.1073/pnas.0509322103 Fathallah, 2007, Role of epigenetic modifications in normal globin gene regulation and butyrate-mediated induction of fetal hemoglobin, Blood, 110, 3391, 10.1182/blood-2007-02-076091 Chin, 2009, Transcriptional activation of the gamma-globin gene in baboons treated with decitabine and in cultured erythroid progenitor cells involves different mechanisms, Exp Hematol, 37, 1131, 10.1016/j.exphem.2009.06.007 Banzon, 2011, siDNMT1 increases gamma-globin expression in chemical inducer of dimerization (CID)-dependent mouse betaYAC bone marrow cells and in baboon erythroid progenitor cell cultures, Exp Hematol, 39, 26, 10.1016/j.exphem.2010.10.003 Olivieri, 2011, A pilot study of subcutaneous decitabine in beta-thalassemia intermedia, Blood, 118, 2708, 10.1182/blood-2011-03-341909 Hendrich, 1998, Identification and characterization of a family of mammalian methyl-CpG binding proteins, Mol Cell Biol, 18, 6538, 10.1128/MCB.18.11.6538 Kransdorf, 2006, MBD2 is a critical component of a methyl cytosine-binding protein complex isolated from primary erythroid cells, Blood, 108, 2836, 10.1182/blood-2006-04-016394 Gnanapragasam, 2011, p66Alpha-MBD2 coiled-coil interaction and recruitment of mi-2 are critical for globin gene silencing by the MBD2-NuRD complex, Proc Natl Acad Sci U S A, 108, 7487, 10.1073/pnas.1015341108 Hendrich, 2001, Closely related proteins MBD2 and MBD3 play distinctive but interacting roles in mouse development, Genes Dev, 15, 710, 10.1101/gad.194101 Ng, 1999, MBD2 is a transcriptional repressor belonging to the MeCP1 histone deacetylase complex, Nat Genet, 23, 58, 10.1038/12659 Feng, 2001, The MeCP1 complex represses transcription through preferential binding, remodeling, and deacetylating methylated nucleosomes, Genes Dev, 15, 827 Cramer, 2014, Probing the dynamic distribution of bound states for methylcytosine-binding domains on DNA, J Biol Chem, 289, 1294, 10.1074/jbc.M113.512236 Le Guezennec, 2006, MBD2/NuRD and MBD3/NuRD, two distinct complexes with different biochemical and functional properties, Mol Cell Biol, 26, 843, 10.1128/MCB.26.3.843-851.2006 Rank, 2010, Identification of a PRMT5-dependent repressor complex linked to silencing of human fetal globin gene expression, Blood, 116, 1585, 10.1182/blood-2009-10-251116 Amaya, 2013, Mi2beta-mediated silencing of the fetal gamma-globin gene in adult erythroid cells, Blood, 121, 3493, 10.1182/blood-2012-11-466227 Allfrey, 1964, Acetylation and methylation of histones and their possible role in the regulation of RNA synthesis, Proc Natl Acad Sci U S A, 51, 786, 10.1073/pnas.51.5.786 Vidali, 1978, Butyrate suppression of histone deacetylation leads to accumulation of multiacetylated forms of histones H3 and H4 and increased DNase I sensitivity of the associated DNA sequences, Proc Natl Acad Sci U S A, 75, 2239, 10.1073/pnas.75.5.2239 Marmorstein, 2001, Structure and function of histone acetyltransferases, Cell Mol Life Sci, 58, 693, 10.1007/PL00000893 Ginder, 1984, Activation of a chicken embryonic globin gene in adult erythroid cells by 5-azacytidine and sodium butyrate, Proc Natl Acad Sci U S A, 81, 3954, 10.1073/pnas.81.13.3954 Perrine, 1988, Butyrate infusions in the ovine fetus delay the biologic clock for globin gene switching, Proc Natl Acad Sci U S A, 85, 8540, 10.1073/pnas.85.22.8540 Boosalis, 2001, Short-chain fatty acid derivatives stimulate cell proliferation and induce STAT-5 activation, Blood, 97, 3259, 10.1182/blood.V97.10.3259 Witt, 2003, Induction of fetal hemoglobin expression by the histone deacetylase inhibitor apicidin, Blood, 101, 2001, 10.1182/blood-2002-08-2617 Sangerman, 2006, Mechanism for fetal hemoglobin induction by histone deacetylase inhibitors involves gamma-globin activation by CREB1 and ATF-2, Blood, 108, 3590, 10.1182/blood-2006-01-023713 Perrine, 1993, A short-term trial of butyrate to stimulate fetal-globin-gene expression in the beta-globin disorders, N Engl J Med, 328, 81, 10.1056/NEJM199301143280202 Perrine, 1994, Butyrate derivatives. new agents for stimulating fetal globin production in the beta-globin disorders, Am J Pediatr Hematol Oncol, 16, 67 Bradner, 2010, Chemical genetic strategy identifies histone deacetylase 1 (HDAC1) and HDAC2 as therapeutic targets in sickle cell disease, Proc Natl Acad Sci U S A, 107, 12617, 10.1073/pnas.1006774107 Lachner, 2002, The many faces of histone lysine methylation, Curr Opin Cell Biol, 14, 286, 10.1016/S0955-0674(02)00335-6 Wozniak, 2008, Epigenetic control of complex loci during erythropoiesis, Curr Top Dev Biol, 82, 55, 10.1016/S0070-2153(07)00003-8 Voigt, 2013, A double take on bivalent promoters, Genes Dev, 27, 1318, 10.1101/gad.219626.113 Zhao, 2009, PRMT5-mediated methylation of histone H4R3 recruits DNMT3A, coupling histone and DNA methylation in gene silencing, Nat Struct Mol Biol, 16, 304, 10.1038/nsmb.1568 He, 2013, Induction of human fetal hemoglobin expression by adenosine-2',3'-dialdehyde, J Transl Med, 11, 14, 10.1186/1479-5876-11-14 van Dijk, 2010, Fetal globin expression is regulated by friend of PRMT1, Blood, 116, 4349, 10.1182/blood-2010-03-274399 Li, 2010, H4R3 methylation facilitates beta-globin transcription by regulating histone acetyltransferase binding and H3 acetylation, Blood, 115, 2028, 10.1182/blood-2009-07-236059 Xu, 2013, Corepressor-dependent silencing of fetal hemoglobin expression by BCL11A, Proc Natl Acad Sci U S A, 110, 6518, 10.1073/pnas.1303976110 Cui, 2011, Nuclear receptors TR2 and TR4 recruit multiple epigenetic transcriptional corepressors that associate specifically with the embryonic beta-type globin promoters in differentiated adult erythroid cells, Mol Cell Biol, 31, 3298, 10.1128/MCB.05310-11 Shi, 2013, Lysine-specific demethylase 1 is a therapeutic target for fetal hemoglobin induction, Nat Med, 19, 291, 10.1038/nm.3101 Fuks, 2005, DNA methylation and histone modifications: teaming up to silence genes, Curr Opin Genet Dev, 15, 490, 10.1016/j.gde.2005.08.002 Johnson, 2007, The SRA methyl-cytosine-b inding domain links DNA and histone methylation, Curr Biol, 17, 379, 10.1016/j.cub.2007.01.009 Sarraf, 2004, Methyl-CpG binding protein MBD1 couples histone H3 methylation at lysine 9 by SETDB1 to DNA replication and chromatin assembly, Mol Cell, 15, 595, 10.1016/j.molcel.2004.06.043 Dodge, 2004, Histone H3-K9 methyltransferase ESET is essential for early development, Mol Cell Biol, 24, 2478, 10.1128/MCB.24.6.2478-2486.2004 Mutskov, 2002, The barrier function of an insulator couples high histone acetylation levels with specific protection of promoter DNA from methylation, Genes Dev, 16, 1540, 10.1101/gad.988502 Castel, 2013, RNA interference in the nucleus: roles for small RNAs in transcription, epigenetics and beyond, Nat Rev Genet, 14, 100, 10.1038/nrg3355 Lee, 2013, LIN28B-mediated expression of fetal hemoglobin and production of fetal-like erythrocytes from adult human erythroblasts ex vivo, Blood, 122, 1034, 10.1182/blood-2012-12-472308 Lulli, 2013, MicroRNA-486-3p regulates gamma-globin expression in human erythroid cells by directly modulating BCL11A, PLoS ONE, 8, e60436, 10.1371/journal.pone.0060436 Atweh, 2010, Pharmacologic induction of fetal hemoglobin production, Hematol Oncol Clin North Am, 24, 1131, 10.1016/j.hoc.2010.08.001 Fucharoen, 2013, A randomized phase I/II trial of HQK-1001, an oral fetal globin gene inducer, in beta-thalassaemia intermedia and HbE/beta-thalassaemia, Br J Haematol, 161, 587, 10.1111/bjh.12304 Moellering, 2009, Direct inhibition of the NOTCH transcription factor complex, Nature, 462, 182, 10.1038/nature08543 Cerchietti, 2010, A small-molecule inhibitor of BCL6 kills DLBCL cells in vitro and in vivo, Cancer Cell, 17, 400, 10.1016/j.ccr.2009.12.050 LaBelle, 2012, A stapled BIM peptide overcomes apoptotic resistance in hematologic cancers, J Clin Invest, 122, 2018, 10.1172/JCI46231 Kronke, 2014, Lenalidomide causes selective degradation of IKZF1 and IKZF3 in multiple myeloma cells, Science, 343, 301, 10.1126/science.1244851 Lu, 2014, The myeloma drug lenalidomide promotes the cereblon-dependent destruction of ikaros proteins, Science, 343, 305, 10.1126/science.1244917