Scl binds to primed enhancers in mesoderm to regulate hematopoietic and cardiac fate divergence

EMBO Journal

Volumn 34, Issue 6, 2015, Pages 759-777

  Org, Tõnis ^a   Duan, Dan ^a   Ferrari, Roberto ^a,b   Montel Hagen, Amelie ^a   Van Handel, Ben ^a   Kerényi, Marc A ^c   Sasidharan, Rajkumar ^a   Rubbi, Liudmilla ^a   Fujiwara, Yuko ^c   Pellegrini, Matteo ^a   Orkin, Stuart H ^c   Kurdistani, Siavash K ^a,b   Mikkola, Hanna K A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

cardiac specification; enhancer; hematopoiesis; mesoderm diversification; transcriptional regulation

Indexed keywords

FIBRINOGEN RECEPTOR; HAND1 PROTEIN; MYOCARDIN; POLYCOMB REPRESSIVE COMPLEX 2; PROTEIN; PROTEIN MYB; TRANSCRIPTION FACTOR GATA 1; TRANSCRIPTION FACTOR GATA 2; TRANSCRIPTION FACTOR GATA 3; TRANSCRIPTION FACTOR GATA 4; TRANSCRIPTION FACTOR GATA 6; TRANSCRIPTION FACTOR NKX2.5; TRANSCRIPTION FACTOR RUNX1; TRANSCRIPTION FACTOR TAL1; TRANSCRIPTION FACTOR TBX5; UNCLASSIFIED DRUG; VASCULAR ENDOTHELIAL CADHERIN; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; ONCOPROTEIN; TAL1 PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BINDING AFFINITY; BINDING SITE; BLOOD ANALYSIS; CELL ACTIVATION; CELL DIFFERENTIATION; CELL FATE; CELLS BY BODY ANATOMY; DEVELOPMENTAL STAGE; ENHANCER REGION; EPIGENETICS; GENE ACTIVATION; GENE REPRESSION; GENETIC VARIABILITY; HEART DEVELOPMENT; HEART MUSCLE CELL; HEMANGIOBLAST; HEMATOPOIETIC CELL; HEMATOPOIETIC STEM CELL; MESODERM; MOUSE; NONHUMAN; NUCLEAR REPROGRAMMING; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN MODIFICATION; REGENERATIVE MEDICINE; STEM CELL; BIOLOGICAL MODEL; CARDIAC MYOBLAST; CELL CULTURE; CHROMATIN IMMUNOPRECIPITATION; CYTOLOGY; EMBRYOLOGY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE LIBRARY; HUMAN; METABOLISM; MICROARRAY ANALYSIS; MOLECULAR GENETICS; PHYSIOLOGY; SEQUENCE ANALYSIS;

BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL DIFFERENTIATION; CELLS, CULTURED; CHROMATIN IMMUNOPRECIPITATION; ENHANCER ELEMENTS, GENETIC; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE LIBRARY; HEMATOPOIETIC STEM CELLS; HUMANS; MESODERM; MICROARRAY ANALYSIS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; MYOBLASTS, CARDIAC; PROTO-ONCOGENE PROTEINS; SEQUENCE ANALYSIS, RNA;

EID: 84924912759     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201490542     Document Type: Article

References (89)

1. Akalin A, Kormaksson M, Li S, Garrett-Bakelman FE, Figueroa ME, Melnick A, Mason CE, (2012) methylKit: a comprehensive R package for the analysis of genome-wide DNA methylation profiles. Genome Biol 13: R87
2. Amente S, Lania L, Majello B, (2013) The histone LSD1 demethylase in stemness and cancer transcription programs. Biochim Biophys Acta 1829: 981-986
3. Bertrand JY, Chi NC, Santoso B, Teng S, Stainier DYR, Traver D, (2010) Haematopoietic stem cells derive directly from aortic endothelium during development. Nature 464: 108-111
4. Blattler A, Farnham PJ, (2013) Cross-talk between site-specific transcription factors and DNA methylation states. J Biol Chem 288: 34287-34294
5. Blow MJ, McCulley DJ, Li Z, Zhang T, Akiyama JA, Holt A, Plajzer-Frick I, Shoukry M, Wright C, Chen F, Afzal V, Bristow J, Ren B, Black BL, Rubin EM, Visel A, Pennacchio LA, (2010) ChIP-Seq identification of weakly conserved heart enhancers. Nat Genet 42: 806-810
6. Boisset J-C, van Cappellen W, Andrieu-Soler C, Galjart N, Dzierzak E, Robin C, (2010) In vivo imaging of haematopoietic cells emerging from the mouse aortic endothelium. Nature 464: 116-120
7. Bresnick EH, Katsumura KR, Lee H-Y, Johnson KD, Perkins AS, (2012) Master regulatory GATA transcription factors: mechanistic principles and emerging links to hematologic malignancies. Nucleic Acids Res 40: 5819-5831
8. Calero-Nieto FJ, Ng FS, Wilson NK, Hannah R, Moignard V, Leal-Cervantes AI, Jimenez-Madrid I, Diamanti E, Wernisch L, Göttgens B, (2014) Key regulators control distinct transcriptional programmes in blood progenitor and mast cells. EMBO J 33: 1212-1226
9. Chen MJ, Yokomizo T, Zeigler BM, Dzierzak E, Speck NA, (2009) Runx1 is required for the endothelial to haematopoietic cell transition but not thereafter. Nature 457: 887-891
10. Chlon TM, Crispino JD, (2012) Combinatorial regulation of tissue specification by GATA and FOG factors. Development 139: 3905-3916
11. Chung YS, Zhang WJ, Arentson E, Kingsley PD, Palis J, Choi K, (2002) Lineage analysis of the hemangioblast as defined by FLK1 and SCL expression. Development 129: 5511-5520
12. Creemers EE, Sutherland LB, McAnally J, Richardson JA, Olson EN, (2006) Myocardin is a direct transcriptional target of Mef2, Tead and Foxo proteins during cardiovascular development. Development 133: 4245-4256
13. Creyghton MP, Cheng AW, Welstead GG, Kooistra T, Carey BW, Steine EJ, Hanna J, Lodato MA, Frampton GM, Sharp PA, Boyer LA, Young RA, Jaenisch R, (2010) Histone H3K27ac separates active from poised enhancers and predicts developmental state. Proc Natl Acad Sci USA 107: 21931-21936
14. Cui K, Zang C, Roh T-Y, Schones DE, Childs RW, Peng W, Zhao K, (2009) Chromatin signatures in multipotent human hematopoietic stem cells indicate the fate of bivalent genes during differentiation. Cell Stem Cell 4: 80-93
15. De Bruijn MF, Speck NA, Peeters MC, Dzierzak E, (2000) Definitive hematopoietic stem cells first develop within the major arterial regions of the mouse embryo. EMBO J 19: 2465-2474
16. De Pater E, Kaimakis P, Vink CS, Yokomizo T, Yamada-Inagawa T, van der Linden R, Kartalaei PS, Camper SA, Speck N, Dzierzak E, (2013) Gata2 is required for HSC generation and survival. J Exp Med 210: 2843-2850
17. Fehling HJ, Lacaud G, Kubo A, Kennedy M, Robertson S, Keller G, Kouskoff V, (2003) Tracking mesoderm induction and its specification to the hemangioblast during embryonic stem cell differentiation. Development 130: 4217-4227
18. Ferrari R, Su T, Li B, Bonora G, Oberai A, Chan Y, Sasidharan R, Berk AJ, Pellegrini M, Kurdistani SK, (2012) Reorganization of the host epigenome by a viral oncogene. Genome Res 22: 1212-1221
19. Fujiwara Y, Chang AN, Williams AM, Orkin SH, (2004) Functional overlap of GATA-1 and GATA-2 in primitive hematopoietic development. Blood 103: 583-585
20. Gao X, Johnson KD, Chang Y-I, Boyer ME, Dewey CN, Zhang J, Bresnick EH, (2013) Gata2 cis-element is required for hematopoietic stem cell generation in the mammalian embryo. J Exp Med 210: 2833-2842
21. Guo W, Fiziev P, Yan W, Cokus S, Sun X, Zhang MQ, Chen P-Y, Pellegrini M, (2013) BS-Seeker2: a versatile aligning pipeline for bisulfite sequencing data. BMC Genom 14: 774
22. Habibi E, Brinkman AB, Arand J, Kroeze LI, Kerstens HHD, Matarese F, Lepikhov K, Gut M, Brun-Heath I, Hubner NC, Benedetti R, Altucci L, Jansen JH, Walter J, Gut IG, Marks H, Stunnenberg HG, (2013) Whole-genome bisulfite sequencing of two distinct interconvertible DNA methylomes of mouse embryonic stem cells. Cell Stem Cell 13: 360-369
23. Harmston N, Lenhard B, (2013) Chromatin and epigenetic features of long-range gene regulation. Nucleic Acids Res 41: 7185-7199
24. He A, Gu F, Hu Y, Ma Q, Yi Ye L, Akiyama JA, Visel A, Pennacchio LA, Pu WT, (2014) Dynamic GATA4 enhancers shape the chromatin landscape central to heart development and disease. Nat Commun 5: 4907
25. Heintzman ND, Hon GC, Hawkins RD, Kheradpour P, Stark A, Harp LF, Ye Z, Lee LK, Stuart RK, Ching CW, Ching KA, Antosiewicz-Bourget JE, Liu H, Zhang X, Green RD, Lobanenkov VV, Stewart R, Thomson JA, Crawford GE, Kellis M, et al, (2009) Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 459: 108-112
26. Holtzinger A, Rosenfeld GE, Evans T, (2010) Gata4 directs development of cardiac-inducing endoderm from ES cells. Dev Biol 337: 63-73
27. Hon GC, Rajagopal N, Shen Y, McCleary DF, Yue F, Dang MD, Ren B, (2013) Epigenetic memory at embryonic enhancers identified in DNA methylation maps from adult mouse tissues. Nat Genet 45: 1198-1206
28. Hosoya T, Maillard I, Engel JD, (2010) From the cradle to the grave: activities of GATA-3 throughout T-cell development and differentiation. Immunol Rev 238: 110-125
29. Hu X, Li X, Valverde K, Fu X, Noguchi C, Qiu Y, Huang S, (2009a) LSD1-mediated epigenetic modification is required for TAL1 function and hematopoiesis. Proc Natl Acad Sci USA 106: 10141-10146
30. Hu X, Ybarra R, Qiu Y, Bungert J, Huang S, (2009b) Transcriptional regulation by TAL1: a link between epigenetic modifications and erythropoiesis. Epigenetics 4: 357-361
31. Huang DW, Sherman BT, Tan Q, Kir J, Liu D, Bryant D, Guo Y, Stephens R, Baseler MW, Lane HC, Lempicki RA, (2007) DAVID Bioinformatics Resources: expanded annotation database and novel algorithms to better extract biology from large gene lists. Nucleic Acids Res 35: W169-W175
32. Huang P, He Z, Ji S, Sun H, Xiang D, Liu C, Hu Y, Wang X, Hui L, (2011) Induction of functional hepatocyte-like cells from mouse fibroblasts by defined factors. Nature 475: 386-389
33. Huber TL, Kouskoff V, Fehling HJ, Palis J, Keller G, (2004) Haemangioblast commitment is initiated in the primitive streak of the mouse embryo. Nature 432: 625-630
34. Ieda M, Fu J-D, Delgado-Olguin P, Vedantham V, Hayashi Y, Bruneau BG, Srivastava D, (2010) Direct reprogramming of fibroblasts into functional cardiomyocytes by defined factors. Cell 142: 375-386
35. Iida M, Heike T, Yoshimoto M, Baba S, Doi H, Nakahata T, (2005) T Identification of cardiac stem cells with FLK1, CD31, and VE-cadherin expression during embryonic stem cell differentiation. FASEB J 19: 371-378
36. Ismailoglu I, Yeamans G, Daley GQ, Perlingeiro RCR, Kyba M, (2008) Mesodermal patterning activity of SCL. Exp Hematol 36: 1593-1603
37. Kassouf MT, Hughes JR, Taylor S, McGowan SJ, Soneji S, Green AL, Vyas P, Porcher C, (2010) Genome-wide identification of TAL1's functional targets: insights into its mechanisms of action in primary erythroid cells. Genome Res 20: 1064-1083
38. Kataoka H, Hayashi M, Nakagawa R, Tanaka Y, Izumi N, Nishikawa S, Jakt ML, Tarui H, Nishikawa S-I, (2011) Etv2/ER71 induces vascular mesoderm from Flk1+PDGFRα+ primitive mesoderm. Blood 118: 6975-6986
39. + cardiovascular progenitor cells give rise to the cardiomyocyte, endothelial, and vascular smooth muscle lineages. Dev Cell 11: 723-732
40. Kerenyi MA, Shao Z, Hsu Y-J, Guo G, Luc S, O'Brien K, Fujiwara Y, Peng C, Nguyen M, Orkin SH, (2013) Histone demethylase Lsd1 represses hematopoietic stem and progenitor cell signatures during blood cell maturation. Elife 2: e00633
41. Kim J, Efe JA, Zhu S, Talantova M, Yuan X, Wang S, Lipton SA, Zhang K, Ding S, (2011) Direct reprogramming of mouse fibroblasts to neural progenitors. Proc Natl Acad Sci USA 108: 7838-7843
42. Kissa K, Herbomel P, (2010) Blood stem cells emerge from aortic endothelium by a novel type of cell transition. Nature 464: 112-115
43. Kowalczyk MS, Hughes JR, Garrick D, Lynch MD, Sharpe JA, Sloane-Stanley JA, McGowan SJ, De Gobbi M, Hosseini M, Vernimmen D, Brown JM, Gray NE, Collavin L, Gibbons RJ, Flint J, Taylor S, Buckle VJ, Milne TA, Wood WG, Higgs DR, (2012) Intragenic enhancers act as alternative promoters. Mol Cell 45: 447-458
44. Ku C-J, Hosoya T, Maillard I, Engel JD, (2012) GATA-3 regulates hematopoietic stem cell maintenance and cell-cycle entry. Blood 119: 2242-2251
45. Langmead B, Trapnell C, Pop M, Salzberg SL, (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25
46. Lee D, Park C, Lee H, Lugus JJ, Kim SH, Arentson E, Chung YS, Gomez G, Kyba M, Lin S, Janknecht R, Lim D-S, Choi K, (2008) ER71 acts downstream of BMP, Notch, and Wnt signaling in blood and vessel progenitor specification. Cell Stem Cell 2: 497-507
47. Li W, Ferkowicz MJ, Johnson SA, Shelley WC, Yoder MC, (2005) Endothelial cells in the early murine yolk sac give rise to CD41-expressing hematopoietic cells. Stem Cells Dev 14: 44-54
48. Li Y, Deng C, Hu X, Patel B, Fu X, Qiu Y, Brand M, Zhao K, Huang S, (2012) Dynamic interaction between TAL1 oncoprotein and LSD1 regulates TAL1 function in hematopoiesis and leukemogenesis. Oncogene 31: 5007-5018
49. Lichtinger M, Ingram R, Hannah R, Müller D, Clarke D, Assi SA, Lie-A-Ling M, Noailles L, Vijayabaskar MS, Wu M, Tenen DG, Westhead DR, Kouskoff V, Lacaud G, Göttgens B, Bonifer C, (2012) RUNX1 reshapes the epigenetic landscape at the onset of haematopoiesis. EMBO J 31: 4318-4333
50. Lien CL, Wu C, Mercer B, Webb R, Richardson JA, Olson EN, (1999) Control of early cardiac-specific transcription of Nk2-5 by a GATA-dependent enhancer. Development 126: 75-84
51. + hemangiogenic mesoderm by inhibiting cardiac mesoderm and Wnt signaling. Blood 119: 3295-3305
52. McLean CY, Bristor D, Hiller M, Clarke SL, Schaar BT, Lowe CB, Wenger AM, Bejerano G, (2010) GREAT improves functional interpretation of cis-regulatory regions. Nat Biotechnol 28: 495-501
53. Meissner A, Gnirke A, Bell GW, Ramsahoye B, Lander ES, Jaenisch R, (2005) Reduced representation bisulfite sequencing for comparative high-resolution DNA methylation analysis. Nucleic Acids Res 33: 5868-5877
54. Mikkola HKA, Fujiwara Y, Schlaeger TM, Traver D, Orkin SH, (2003) Expression of CD41 marks the initiation of definitive hematopoiesis in the mouse embryo. Blood 101: 508-516
55. North T, Gu TL, Stacy T, Wang Q, Howard L, Binder M, Marín-Padilla M, Speck NA, (1999) Cbfa2 is required for the formation of intra-aortic hematopoietic clusters. Development 126: 2563-2575
56. Nottingham WT, Jarratt A, Burgess M, Speck CL, Cheng J-F, Prabhakar S, Rubin EM, Li P-S, Sloane-Stanley J, Kong-A-San J, de Bruijn MFTR, (2007) Runx1-mediated hematopoietic stem-cell emergence is controlled by a Gata/Ets/SCL-regulated enhancer. Blood 110: 4188-4197
57. Oda M, Kumaki Y, Shigeta M, Jakt LM, Matsuoka C, Yamagiwa A, Niwa H, Okano M, (2013) DNA methylation restricts lineage-specific functions of transcription factor Gata4 during embryonic stem cell differentiation. PLoS Genet 9: e1003574
58. Palencia-Desai S, Kohli V, Kang J, Chi NC, Black BL, Sumanas S, (2011) Vascular endothelial and endocardial progenitors differentiate as cardiomyocytes in the absence of Etsrp/Etv2 function. Development 138: 4721-4732
59. Pereira C-F, Chang B, Qiu J, Niu X, Papatsenko D, Hendry CE, Clark NR, Nomura-Kitabayashi A, Kovacic JC, Ma'ayan A, Schaniel C, Lemischka IR, Moore K, (2013) Induction of a hemogenic program in mouse fibroblasts. Cell Stem Cell 13: 205-218
60. Pimkin M, Kossenkov A V, Mishra T, Morrissey CS, Wu W, Keller CA, Blobel GA, Lee D, Beer MA, Hardison RC, Weiss MJ, (2014) Divergent functions of hematopoietic transcription factors in lineage priming and differentiation during erythro-megakaryopoiesis. Genome Res 24: 1932-1944
61. Pinello L, Xu J, Orkin SH, Yuan G-C, (2014) Analysis of chromatin-state plasticity identifies cell-type-specific regulators of H3K27me3 patterns. Proc Natl Acad Sci USA 111: E344-E353
62. Porcher C, Swat W, Rockwell K, Fujiwara Y, Alt FW, Orkin SH, (1996) The T cell leukemia oncoprotein SCL/tal-1 is essential for development of all hematopoietic lineages. Cell 86: 47-57
63. Rasmussen TL, Kweon J, Diekmann MA, Belema-Bedada F, Song Q, Bowlin K, Shi X, Ferdous A, Li T, Kyba M, Metzger JM, Koyano-Nakagawa N, Garry DJ, (2011) ER71 directs mesodermal fate decisions during embryogenesis. Development 138: 4801-4812
64. Ren X, Gomez GA, Zhang B, Lin S, (2010) Scl isoforms act downstream of etsrp to specify angioblasts and definitive hematopoietic stem cells. Blood 115: 5338-5346
65. Rhodes KE, Gekas C, Wang Y, Lux CT, Francis CS, Chan DN, Conway S, Orkin SH, Yoder MC, Mikkola HKA, (2008) The emergence of hematopoietic stem cells is initiated in the placental vasculature in the absence of circulation. Cell Stem Cell 2: 252-263
66. Schoenebeck JJ, Keegan BR, Yelon D, (2007) Vessel and blood specification override cardiac potential in anterior mesoderm. Dev Cell 13: 254-267
67. Soufi A, Donahue G, Zaret KS, (2012) Facilitators and impediments of the pluripotency reprogramming factors' initial engagement with the genome. Cell 151: 994-1004
68. Sumanas S, Gomez G, Zhao Y, Park C, Choi K, Lin S, (2008) Interplay among Etsrp/ER71, Scl, and Alk8 signaling controls endothelial and myeloid cell formation. Blood 111: 4500-4510
69. Takahashi S, Shimizu R, Suwabe N, Kuroha T, Yoh K, Ohta J, Nishimura S, Lim KC, Engel JD, Yamamoto M, (2000) GATA factor transgenes under GATA-1 locus control rescue germline GATA-1 mutant deficiencies. Blood 96: 910-916
70. Takahashi K, Yamanaka S, (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126: 663-676
71. Trapnell C, Pachter L, Salzberg SL, (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25: 1105-1111
72. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L, (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28: 511-515
73. Tripic T, Deng W, Cheng Y, Zhang Y, Vakoc CR, Gregory GD, Hardison RC, Blobel GA, (2009) SCL and associated proteins distinguish active from repressive GATA transcription factor complexes. Blood 113: 2191-2201
74. Van Handel B, Montel-Hagen A, Sasidharan R, Nakano H, Ferrari R, Boogerd CJ, Schredelseker J, Wang Y, Hunter S, Org T, Zhou J, Li X, Pellegrini M, Chen J-N, Orkin SH, Kurdistani SK, Evans SM, Nakano A, Mikkola HKA, (2012) Scl represses cardiomyogenesis in prospective hemogenic endothelium and endocardium. Cell 150: 590-605
75. Visel A, Minovitsky S, Dubchak I, Pennacchio LA, (2007) VISTA enhancer browser-a database of tissue-specific human enhancers. Nucleic Acids Res 35: D88-D92
76. Visel A, Blow MJ, Li Z, Zhang T, Akiyama JA, Holt A, Plajzer-Frick I, Shoukry M, Wright C, Chen F, Afzal V, Ren B, Rubin EM, Pennacchio LA, (2009) ChIP-seq accurately predicts tissue-specific activity of enhancers. Nature 457: 854-858
77. Wadman IA, Osada H, Grütz GG, Agulnick AD, Westphal H, Forster A, Rabbitts TH, (1997) The LIM-only protein Lmo2 is a bridging molecule assembling an erythroid, DNA-binding complex which includes the TAL1, E47, GATA-1 and Ldb1/NLI proteins. EMBO J 16: 3145-3157
78. Wamstad JA, Alexander JM, Truty RM, Shrikumar A, Li F, Eilertson KE, Ding H, Wylie JN, Pico AR, Capra JA, Erwin G, Kattman SJ, Keller GM, Srivastava D, Levine SS, Pollard KS, Holloway AK, Boyer LA, Bruneau BG, (2012) Dynamic and coordinated epigenetic regulation of developmental transitions in the cardiac lineage. Cell 151: 206-220
79. Wareing S, Mazan A, Pearson S, Göttgens B, Lacaud G, Kouskoff V, (2012) The Flk1-Cre-mediated deletion of ETV2 defines its narrow temporal requirement during embryonic hematopoietic development. Stem Cells 30: 1521-1531
80. Whyte WA, Bilodeau S, Orlando DA, Hoke HA, Frampton GM, Foster CT, Cowley SM, Young RA, (2012) Enhancer decommissioning by LSD1 during embryonic stem cell differentiation. Nature 482: 221-225
81. Wilson NK, Foster SD, Wang X, Knezevic K, Schütte J, Kaimakis P, Chilarska PM, Kinston S, Ouwehand WH, Dzierzak E, Pimanda JE, de Bruijn MFTR, Göttgens B, (2010) Combinatorial transcriptional control in blood stem/progenitor cells: genome-wide analysis of ten major transcriptional regulators. Cell Stem Cell 7: 532-544
82. Wozniak RJ, Boyer ME, Grass JA, Lee Y, Bresnick EH, (2007) Context-dependent GATA factor function: combinatorial requirements for transcriptional control in hematopoietic and endothelial cells. J Biol Chem 282: 14665-14674
83. Wu W, Morrissey CS, Keller CA, Mishra T, Pimkin M, Blobel GA, Weiss MJ, Hardison RC, (2014) Dynamic shifts in occupancy by TAL1 are guided by GATA factors and drive large-scale reprogramming of gene expression during hematopoiesis. Genome Res 24: 1945-1962
84. Xu J, Shao Z, Glass K, Bauer DE, Pinello L, Van Handel B, Hou S, Stamatoyannopoulos JA, Mikkola HKA, Yuan G-C, Orkin SH, (2012) Combinatorial assembly of developmental stage-specific enhancers controls gene expression programs during human erythropoiesis. Dev Cell 23: 796-811
85. Yoshimoto M, Montecino-Rodriguez E, Ferkowicz MJ, Porayette P, Shelley WC, Conway SJ, Dorshkind K, Yoder MC, (2011) Embryonic day 9 yolk sac and intra-embryonic hemogenic endothelium independently generate a B-1 and marginal zone progenitor lacking B-2 potential. Proc Natl Acad Sci USA 108: 1468-1473
86. Yu M, Riva L, Xie H, Schindler Y, Moran TB, Cheng Y, Yu D, Hardison R, Weiss MJ, Orkin SH, Bernstein BE, Fraenkel E, Cantor AB, (2009) Insights into GATA-1-mediated gene activation versus repression via genome-wide chromatin occupancy analysis. Mol Cell 36: 682-695
87. Zentner GE, Tesar PJ, Scacheri PC, (2011) Epigenetic signatures distinguish multiple classes of enhancers with distinct cellular functions. Genome Res 21: 1273-1283
88. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, Nusbaum C, Myers RM, Brown M, Li W, Liu XS, (2008) Model-based analysis of ChIP-Seq (MACS). Genome Biol 9: R137
89. Zovein AC, Hofmann JJ, Lynch M, French WJ, Turlo KA, Yang Y, Becker MS, Zanetta L, Dejana E, Gasson JC, Tallquist MD, Iruela-Arispe ML, (2008) Fate tracing reveals the endothelial origin of hematopoietic stem cells. Cell Stem Cell 3: 625-636