Genome-Wide Dna Methylation Drives Human Embryonic Stem Cell Erythropoiesis by Remodeling Gene Expression Dynamics

References

• Lu SJ , FengQ , ParkJSet al. Biologic properties and enucleation of red blood cells from human embryonic stem cells . Blood112 ( 12 ), 4475 – 4484 ( 2008 ).
   PubMed Web of Science ®Google Scholar
• Pryzhkova MV , PetersA , ZambidisET . Erythropoietic differentiation of a human embryonic stem cell line harbouring the sickle cell anaemia mutation . Reprod. Biomed. Online21 ( 2 ), 196 – 205 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Lu SJ , FengQ , CaballeroSet al. Generation of functional hemangioblasts from human embryonic stem cells . Nat. Methods4 ( 6 ), 501 – 509 ( 2007 ).
   PubMed Web of Science ®Google Scholar
• Bock C , BeermanI , LienWHet al. DNA methylation dynamics during in vivo differentiation of blood and skin stem cells . Mol. Cell47 ( 4 ), 633 – 647 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Hodges E , MolaroA , Dos SantosCOet al. Directional DNA methylation changes and complex intermediate states accompany lineage specificity in the adult hematopoietic compartment . Mol. Cell44 ( 1 ), 17 – 28 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Ji H , EhrlichLI , SeitaJet al. Comprehensive methylome map of lineage commitment from haematopoietic progenitors . Nature467 ( 7313 ), 338 – 342 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Shearstone JR , PopR , BockC , BoyleP , MeissnerA , SocolovskyM . Global DNA demethylation during mouse erythropoiesis in vivo . Science334 ( 6057 ), 799 – 802 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• De Goede OM , LavoiePM , RobinsonWP . Characterizing the hypomethylated DNA methylation profile of nucleated red blood cells from cord blood . Epigenomics8 ( 11 ), 1481 – 1494 ( 2016 ).
   PubMed Web of Science ®Google Scholar
• Farthing CR , FiczG , NgRKet al. Global mapping of DNA methylation in mouse promoters reveals epigenetic reprogramming of pluripotency genes . PLoS Genet.4 ( 6 ), e1000116 ( 2008 ).
   PubMed Web of Science ®Google Scholar
• Illingworth R , KerrA , DesousaDet al. A novel CpG island set identifies tissue-specific methylation at developmental gene loci . PLoS Biol.6 ( 1 ), e22 ( 2008 ).
   PubMed Web of Science ®Google Scholar
• Broske AM , VockentanzL , KharaziSet al. DNA methylation protects hematopoietic stem cell multipotency from myeloerythroid restriction . Nat. Genet.41 ( 11 ), 1207 – 1215 ( 2009 ).
   PubMed Web of Science ®Google Scholar
• Tadokoro Y , EmaH , OkanoM , LiE , NakauchiH . De novo DNA methyltransferase is essential for self-renewal, but not for differentiation, in hematopoietic stem cells . J. Exp. Med.204 ( 4 ), 715 – 722 ( 2007 ).
   PubMed Web of Science ®Google Scholar
• Yu Y , MoY , EbenezerDet al. High resolution methylome analysis reveals widespread functional hypomethylation during adult human erythropoiesis . J. Biol. Chem.288 ( 13 ), 8805 – 8814 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Futscher BW , OshiroMM , WozniakRJet al. Role for DNA methylation in the control of cell type specific maspin expression . Nat. Genet.31 ( 2 ), 175 – 179 ( 2002 ).
   PubMed Web of Science ®Google Scholar
• Li XY , ShenJZ , ShenSFet al. [Methylation status of IEX-1 gene promotor CpG island in malignant hematopoietic cell lines] . Zhongguo Shi Yan Xue Ye Xue Za Zhi19 ( 2 ), 473 – 476 ( 2011 ).
   PubMedGoogle Scholar
• Moen EL , StarkAL , ZhangW , DolanME , GodleyLA . The role of gene body cytosine modifications in MGMT expression and sensitivity to temozolomide . Mol. Cancer Ther.13 ( 5 ), 1334 – 1344 ( 2014 ).
   PubMed Web of Science ®Google Scholar
• Hong SJ , KangMI , OhJHet al. DNA methylation and expression patterns of key tissue-specific genes in adult stem cells and stomach tissues . J. Korean Med. Sci.24 ( 5 ), 918 – 929 ( 2009 ).
   PubMed Web of Science ®Google Scholar
• Lu SJ , HippJA , FengQ , HippJD , LanzaR , AtalaA . GeneChip analysis of human embryonic stem cell differentiation into hemangioblasts: an in silico dissection of mixed phenotypes . Genome Biol.8 ( 11 ), R240 ( 2007 ).
   PubMed Web of Science ®Google Scholar
• Feng S , JacobsenSE , ReikW . Epigenetic reprogramming in plant and animal development . Science330 ( 6004 ), 622 – 627 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Gu Y , LiuGH , PlongthongkumNet al. Global DNA methylation and transcriptional analyses of human ESC-derived cardiomyocytes . Protein & Cell5 ( 1 ), 59 – 68 ( 2014 ).
   PubMed Web of Science ®Google Scholar
• Wei D , LoekenMR . Increased DNA methyltransferase 3b (Dnmt3b)-mediated CpG island methylation stimulated by oxidative stress inhibits expression of a gene required for neural tube and neural crest development in diabetic pregnancy . Diabetes63 ( 10 ), 3512 – 3522 ( 2014 ).
   PubMed Web of Science ®Google Scholar
• Petell CJ , AlabdiL , HeM , San MiguelP , RoseR , GowherH . An epigenetic switch regulates de novo DNA methylation at a subset of pluripotency gene enhancers during embryonic stem cell differentiation . Nucleic Acids Res.44 ( 16 ), 7605 – 7617 ( 2016 ).
   PubMed Web of Science ®Google Scholar
• Sohni A , BartoccettiM , KhoueiryRet al. Dynamic switching of active promoter and enhancer domains regulates Tet1 and Tet2 expression during cell state transitions between pluripotency and differentiation . Mol. Cell. Biol.35 ( 6 ), 1026 – 1042 ( 2015 ).
   PubMed Web of Science ®Google Scholar
• Chasis JA , MohandasN . Erythroblastic islands: niches for erythropoiesis . Blood112 ( 3 ), 470 – 478 ( 2008 ).
   PubMed Web of Science ®Google Scholar
• Dzierzak E , PhilipsenS . Erythropoiesis: development and differentiation . Cold Spring Harb. Perspect. Med.3 ( 4 ), a011601 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Boisset JC , Van CappellenW , Andrieu-SolerC , GaljartN , DzierzakE , RobinC . In vivo imaging of haematopoietic cells emerging from the mouse aortic endothelium . Nature464 ( 7285 ), 116 – 120 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Fouse SD , ShenY , PellegriniMet al. Promoter CpG methylation contributes to ES cell gene regulation in parallel with Oct4/Nanog, PcG complex, and histone H3 K4/K27 trimethylation . Cell Stem Cell2 ( 2 ), 160 – 169 ( 2008 ).
   PubMed Web of Science ®Google Scholar
• Meissner A , MikkelsenTS , GuHet al. Genome-scale DNA methylation maps of pluripotent and differentiated cells . Nature454 ( 7205 ), 766 – 770 ( 2008 ).
   PubMed Web of Science ®Google Scholar
• Nagae G , IsagawaT , ShirakiNet al. Tissue-specific demethylation in CpG-poor promoters during cellular differentiation . Hum. Mol. Genet.20 ( 14 ), 2710 – 2721 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Jones PA . The DNA methylation paradox . Trends Genet.15 ( 1 ), 34 – 37 ( 1999 ).
   PubMed Web of Science ®Google Scholar
• Rauch TA , WuX , ZhongX , RiggsAD , PfeiferGP . A human B cell methylome at 100-base pair resolution . Proc. Natl Acad. Sci. USA106 ( 3 ), 671 – 678 ( 2009 ).
   PubMed Web of Science ®Google Scholar
• Hahn MA , WuXW , LiAX , HahnT , PfeiferGP . Relationship between gene body DNA methylation and intragenic H3K9me3 and H3K36me3 chromatin marks . PLoS ONE6 ( 4 ), e18844 ( 2011 ).
   Web of Science ®Google Scholar
• Miller JR , CartwrightEM , BrownleeGG , FedoroffNV , BrownDD . The nucleotide sequence of oocyte 5S DNA in Xenopus laevis. II. The GC-rich region . Cell13 ( 4 ), 717 – 725 ( 1978 ).
   PubMed Web of Science ®Google Scholar
• Mcmanus S , EbertA , SalvagiottoGet al. The transcription factor Pax5 regulates its target genes by recruiting chromatin-modifying proteins in committed B cells . EMBO J.30 ( 12 ), 2388 – 2404 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Richmond TD , ChohanM , BarberDL . Turning cells red: signal transduction mediated by erythropoietin . Trends Cell Biol.15 ( 3 ), 146 – 155 ( 2005 ).
   PubMed Web of Science ®Google Scholar
• Kirito K , NakajimaK , WatanabeTet al. Identification of the human erythropoietin receptor region required for Stat1 and Stat3 activation . Blood99 ( 1 ), 102 – 110 ( 2002 ).
   PubMed Web of Science ®Google Scholar
• Cokic VP , BhattacharyaB , Beleslin-CokicBB , NoguchiCT , PuriRK , SchechterAN . JAK-STAT and AKT pathway-coupled genes in erythroid progenitor cells through ontogeny . J. Transl. Med.10 , 116 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Bausek N , ZeidlerMP . Galpha73B is a downstream effector of JAK/STAT signalling and a regulator of Rho1 in Drosophila haematopoiesis . J. Cell Sci.127 ( Pt 1 ), 101 – 110 ( 2014 ).
   PubMed Web of Science ®Google Scholar
• Furqan M , MukhiN , LeeB , LiuD . Dysregulation of JAK-STAT pathway in hematological malignancies and JAK inhibitors for clinical application . Biomarker Res.1 ( 1 ), 5 ( 2013 ).
   PubMedGoogle Scholar
• Porcher C , SwatW , RockwellK , FujiwaraY , AltFW , OrkinSh . The T cell leukemia oncoprotein SCL/tal-1 is essential for development of all hematopoietic lineages . Cell86 , 47 – 57 ( 1996 ).
   PubMed Web of Science ®Google Scholar
• Grass JA , BoyerME , PalS , WuJ , WeissMJ , BresnickEH . GATA-1-dependent transcriptional repression of GATA-2 via disruption of positive autoregulation and domain-wide chromatin remodeling . Proc. Natl Acad. Sci. USA100 ( 15 ), 8811 – 8816 ( 2003 ).
   PubMed Web of Science ®Google Scholar
• Okuda T , Van DeursenJ , HiebertSW , GrosveldG , DowningJR . AML1, the target of multiple chromosomal translocations in human leukemia, is essential for normal fetal liver hematopoiesis . Cell84 ( 2 ), 321 – 330 ( 1996 ).
   PubMed Web of Science ®Google Scholar
• Carotta S , WuL , NuttSL . Surprising new roles for PU.1 in the adaptive immune response . Immunol. Rev.238 ( 1 ), 63 – 75 ( 2010 ).
   PubMedGoogle Scholar
• Huang G , ZhangP , HiraiHet al. PU.1 is a major downstream target of AML1 (RUNX1) in adult mouse hematopoiesis . Nat. Genet.40 ( 1 ), 51 – 60 ( 2008 ).
   PubMed Web of Science ®Google Scholar
• Vinjamur DS , WadeKJ , MohamadSF , HaarJL , SawyerST , LloydJA . Kruppel-like transcription factors KLF1 and KLF2 have unique and coordinate roles in regulating embryonic erythroid precursor maturation . Haematologica99 ( 10 ), 1565 – 1573 ( 2014 ).
   PubMed Web of Science ®Google Scholar
• Inoue A , FujiwaraT , OkitsuYet al. Elucidation of the role of LMO2 in human erythroid cells . Exp. Hematol.41 ( 12 ), 1062 – 1076e1061 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Lu SJ , KelleyT , FengQet al. 3D microcarrier system for efficient differentiation of human pluripotent stem cells into hematopoietic cells without feeders and serum [corrected] . Regen. Med.8 ( 4 ), 413 – 424 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Nordlund J , BacklinCL , WahlbergPet al. Genome-wide signatures of differential DNA methylation in pediatric acute lymphoblastic leukemia . Genome Biol.14 ( 9 ), r105 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Sandoval J , HeynH , MoranSet al. Validation of a DNA methylation microarray for 450,000 CpG sites in the human genome . Epigenetics6 ( 6 ), 692 – 702 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Han H , YangX , PandiyanK , LiangG . Synergistic re-activation of epigenetically silenced genes by combinatorial inhibition of DNMTs and LSD1 in cancer cells . PLoS ONE8 ( 9 ), e75136 ( 2013 ).
   Web of Science ®Google Scholar
• The R Project for Statistical Computing . www.r-project.org
   Google Scholar
• KEGG PATHWAY Database . www.genome.jp/kegg/pathway.html
   Google Scholar
• The Li Lab. MethPrimer . www.urogene.org/cgi-bin/methprimer/methprimer.cgi
   Google Scholar