Hematopoietic transcriptional mechanisms: From locus-specific to genome-wide vantage points

Experimental Hematology

Volumn 42, Issue 8, 2014, Pages 618-629

  DeVilbiss, Andrew W ^a,b   Sanalkumar, Rajendran ^a,b   Johnson, Kirby D ^a,b   Keles, Sunduz ^b,c   Bresnick, Emery H ^a,b  

^a UNIVERSITY OF WISCONSIN   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ERYTHROID KRUPPEL LIKE FACTOR; KRUPPEL LIKE FACTOR; TRANSCRIPTION FACTOR GATA 1; TRANSCRIPTION FACTOR NF E2;

ANTIBODY DETECTION; BINDING AFFINITY; CATALYSIS; CELL CYCLE PROGRESSION; CELL DIFFERENTIATION; CHROMATIN IMMUNOPRECIPITATION; DNA DETERMINATION; ERYTHROPOIESIS; GENE LOCUS; GENE SEQUENCE; GENETIC ANALYSIS; GENETIC TRANSCRIPTION; HEMATOPOIESIS; HISTONE MODIFICATION; HUMAN; INTRON; MOLECULAR DYNAMICS; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CROSS LINKING; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; REPRODUCIBILITY; REVIEW; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION SITE; UPREGULATION;

CHROMATIN IMMUNOPRECIPITATION; GATA1 TRANSCRIPTION FACTOR; GENOME-WIDE ASSOCIATION STUDY; HEMATOPOIESIS; HUMANS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; SEQUENCE ANALYSIS, DNA; TRANSCRIPTION, GENETIC;

EID: 84905174592     PISSN: 0301472X     EISSN: 18732399     Source Type: Journal    
DOI: 10.1016/j.exphem.2014.05.004     Document Type: Review

References (164)

1. Ema H., Morita Y., Suda T. Heterogeneity and hierarchy of hematopoietic stem cells. Exp Hematol 2014, 42:74-82.e72.
2. Dzierzak E., Speck N.A. Of lineage and legacy: The development ofmammalian hematopoietic stem cells. Nat Immunol 2008, 9:129-136.
3. Orkin S.H., Zon L.I. Hematopoiesis: An evolving paradigm for stem cell biology. Cell 2008, 132:631-644.
4. Dedon P.C., Soults J.A., Allis C.D., Gorovsky M.A. A simplified formaldehyde fixation and immunoprecipitation technique for studying protein-DNA interactions. Anal Biochem 1991, 197:83-90.
5. Im H., Grass J.A., Johnson K.D., Boyer M.E., Wu J., Bresnick E.H. Measurement of protein-DNA interactions invivo by chromatin immunoprecipitation. Methods Mol Biol 2004, 284:129-146.
6. Sun L.V., Chen L., Greil F., et al. Protein-DNA interaction mapping using genomic tiling path microarrays in Drosophila. Proc Natl Acad Sci USA 2003, 100:9428-9433.
7. Weinmann A.S., Yan P.S., Oberley M.J., Huang T.H., Farnham P.J. Isolating human transcription factor targets by coupling chromatin immunoprecipitation and CpG island microarray analysis. Genes Dev 2002, 16:235-244.
8. Robertson G., Hirst M., Bainbridge M., et al. Genome-wide profiles of STAT1 DNA association using chromatin immunoprecipitation and massively parallel sequencing. Nat Methods 2007, 4:651-657.
9. Bailey T., Krajewski P., Ladunga I., et al. Practical guidelines for the comprehensive analysis of ChIP-seq data. PLoS Comput Biol 2013, 9:e1003326.
10. Landt S.G., Marinov G.K., Kundaje A., et al. ChIP-seq guidelines and practices of the ENCODE and modENCODE consortia. Genome Res 2012, 22:1813-1831.
11. Langmead B., Trapnell C., Pop M., Salzberg S.L. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 2009, 10:R25.
12. Li H., Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009, 25:1754-1760.
13. Chung D., Kuan P.F., Li B., et al. Discovering transcription factor binding sites in highly repetitive regions of genomes with multi-read analysis of ChIP-Seq data. PLoS Comput Biol 2011, 7:e1002111.
14. Newkirk D., Biesinger J., Chon A., Yokomori K., Xie X. AREM: Aligning short reads from ChIP-sequencing by expectation maximization. J Comput Biol 2011, 18:1495-1505.
15. Kharchenko P.V., Tolstorukov M.Y., Park P.J. Design and analysis of ChIP-seq experiments for DNA-binding proteins. Nat Biotechnol 2008, 26:1351-1359.
16. Zhang Y., Liu T., Meyer C.A., et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol 2008, 9:R137.
17. Zeng X., Sanalkumar R., Bresnick E.H., Li H., Chang Q., Keles S. jMOSAiCS: Joint analysis of multiple ChIP-seq datasets. Genome Biol 2013, 14:R38.
18. Li Q., Brown J.B., Huang H., Bickel P.J. Measuring reproducibility of high-throughput experiments. Ann Appl Stat 2011, 5:1752-1779.
19. Bailey T.L., Boden M., Buske F.A., et al. MEME SUITE: Tools for motif discovery and searching. Nucleic Acids Res 2009, 37:W202-W208.
20. Lan X., Witt H., Katsumura K., et al. Integration of Hi-C and ChIP-seq data reveals distinct types of chromatin linkages. Nucleic Acids Res 2012, 40:7690-7704.
21. Dekker J., Rippe K., Dekker M., Kleckner N. Capturing chromosome conformation. Science 2002, 295:1306-1311.
22. Dekker J. The three 'C's of chromosome conformation capture: Controls, controls, controls. Nat Methods 2006, 3:17-21.
23. Evans T., Reitman M., Felsenfeld G. An erythrocyte-specific DNA-binding factor recognizes a regulatory sequence common to all chicken globin genes. Proc Natl Acad Sci USA 1988, 85:5976-5980.
24. Evans T., Felsenfeld G. The erythroid-specific transcription factor Eryf1: A new finger protein. Cell 1989, 58:877-885.
25. Tsai S.F., Martin D.I., Zon L.I., D'Andrea A.D., Wong G.G., Orkin S.H. Cloning of cDNA for the major DNA-binding protein of the erythroid lineage through expression in mammalian cells. Nature 1989, 339:446-451.
26. Yamamoto M., Ko L.J., Leonard M.W., Beug H., Orkin S.H., Engel J.D. Activity and tissue-specific expression of the transcription factor NF-E1 multigene family. Genes Dev 1990, 4:1650-1662.
27. Pevny L., Simon M.C., Robertson E., et al. Erythroid differentiation in chimaeric mice blocked by a targeted mutation in the gene for transcription factor GATA-1. Nature 1991, 349:257-260.
28. Simon M.C., Pevny L., Wiles M.V., Keller G., Costantini F., Orkin S.H. Rescue of erythroid development in gene targeted GATA-1- mouse embryonic stem cells. Nat Genet 1992, 1:92-98.
29. Fujiwara Y., Browne C.P., Cunniff K., Goff S.C., Orkin S.H. Arrested development of embryonic red cell precursors in mouse embryos lacking transcription factor GATA-1. Proc Natl Acad Sci USA 1996, 93:12355-12358.
30. Shivdasani R.A., Fujiwara Y., McDevitt M.A., Orkin S.H. A lineage-selective knockout establishes the critical role of transcription factor GATA-1 in mekagaryocyte growth and platelet development. EMBO J 1997, 16:3965-3973.
31. Yu C., Cantor A.B., Yang H., et al. Targeted deletion of a high-affinity GATA-binding site in the GATA-1 promoter leads to selective loss of the eosinophil lineage invivo. J Exp Med 2002, 195:1387-1395.
32. Migliaccio A.R., Rana R.A., Sanchez M., et al. GATA-1 as a regulator of mast cell differentiation revealed by the phenotype of the GATA-1low mouse mutant. J Exp Med 2003, 197:281-296.
33. Charron F., Nemer M. GATA transcription factors and cardiac development. Semin Cell Dev Biol 1999, 10:85-91.
34. Orkin S.H. GATA-binding transcription factors in hematopoietic cells. Blood 1992, 80:575-581.
35. Bresnick E.H., Katsumura K.R., Lee H.Y., Johnson K.D., Perkins A.S. Master regulatory GATA transcription factors: Mechanistic principles and emerging links to hematologic malignancies. Nucleic Acids Res 2012, 40:5819-5831.
36. Bresnick E.H., Lee H.Y., Fujiwara T., Johnson K.D., Keles S. GATA switches as developmental drivers. J Biol Chem 2010, 285:31087-31093.
37. Kumar M.S., Hancock D.C., Molina-Arcas M., et al. The GATA2 transcriptional network is requisite for RAS oncogene-driven non-small cell lung cancer. Cell 2012, 149:642-655.
38. Kouros-Mehr H., Bechis S.K., Slorach E.M., et al. GATA-3 links tumor differentiation and dissemination in a luminal breast cancer model. Cancer Cell 2008, 13:141-152.
39. Forsberg E.C., Downs K.M., Christensen H.M., Im H., Nuzzi P.A., Bresnick E.H. Developmentally dynamic histone acetylation pattern of a tissue-specific chromatin domain. Proc Natl Acad Sci USA 2000, 97:14494-14499.
40. Hebbes T.R., Clayton A.L., Thorne A.W., Crane-Robinson C. Core histone hyperacetylation co-maps with generalized DNase I sensitivity in the chicken beta-globin chromosomal domain. EMBO J 1994, 13:1823-1830.
41. Johnson K.D., Grass J.A., Boyer M.E., et al. Cooperative activities of hematopoietic regulators recruit RNA polymerase II to a tissue-specific chromatin domain. Proc Natl Acad Sci USA 2002, 99:11760-11765.
42. Kiekhaefer C.M., Grass J.A., Johnson K.D., Boyer M.E., Bresnick E.H. Hematopoietic-specific activators establish an overlapping pattern of histone acetylation and methylation within a mammalian chromatin domain. Proc Natl Acad Sci USA 2002, 99:14309-14314.
43. Kiekhaefer C.M., Boyer M.E., Johnson K.D., Bresnick E.H. A WW domain-binding motif within the activation domain of the hematopoietic transcription factor NF-E2 is essential for establishment of a tissue-specific histone modification pattern. J Biol Chem 2004, 279:7456-7461.
44. Chung J.H., Whiteley M., Felsenfeld G. A 5' element of the chicken beta-globin domain serves as an insulator in human erythroid cells and protects against position effect in Drosophila. Cell 1993, 74:505-514.
45. Ohlsson R., Bartkuhn M., Renkawitz R. CTCF shapes chromatin by multiple mechanisms: The impact of 20 years of CTCF research on understanding the workings of chromatin. Chromosoma 2010, 119:351-360.
46. Forrester W.C., Takegawa S., Papayannopoulou T., Stamatoyannopoulos G., Groudine M. Evidence for a locus activation region: The formation of developmentally stable hypersensitive sites in globin-expressing hybrids. Nucleic Acids Res 1987, 15:10159-10177.
47. Grosveld F., van Assendelft G.B., Greaves D.R., Kollias G. Position-independent high-level expression of the human beta-globin gene in trangsenic mice. Cell 1987, 51:975-985.
48. Vakoc C.R., Letting D.L., Gheldof N., et al. Proximity among distant regulatory elements at the beta globin locus requires GATA-1 and FOG-1. Mol Cell 2005, 17:453-462.
49. Ragoczy T., Telling A., Sawado T., Groudine M., Kosak S.T. A genetic analysis of chromosome territory looping: diverse roles for distal regulatory elements. Chromosome Res 2003, 11:513-525.
50. Snow J.W., Trowbridge J.J., Johnson K.D., et al. Context-dependent function of "GATA switch" sites invivo. Blood 2011, 117:4769-4772.
51. Johnson K.D., Hsu A.P., Ryu M.J., et al. Cis-element mutated in GATA2-dependent immunodeficiency governs hematopoiesis and vascular integrity. J Clin Invest 2012, 122:3692-3704.
52. Gao X., Johnson K.D., Chang Y.I., et al. Gata2 cis-element is required for hematopoietic stem cell generation in the mammalian embryo. J Exp Med 2013, 210:2833-2842.
53. Snow J.W., Trowbridge J.J., Fujiwara T., et al. A single cis element maintains repression of the key developmental regulator Gata2. PLoS Genet 2010, 6:e1001103.
54. Horak C.E., Mahajan M.C., Luscombe N.M., Gerstein M., Weissman S.M., Snyder M. GATA-1 binding sites mapped in the beta-globin locus using mammalian chIp-chip analysis. Proc Natl Acad Sci USA 2002, 99:2924-2929.
55. Fujiwara T., O'Geen H., Keles S., et al. Discovering hematopoietic mechanisms through genome-wide analysis of GATA factor chromatin occupancy. Mol Cell 2009, 36:667-681.
56. Yu M., Riva L., Xie H., et al. Insights into GATA-1-mediated gene activation versus repression via genome-wide chromatin occupancy analysis. Mol Cell 2009, 36:682-695.
57. Cheng Y., Wu W., Kumar S.A., et al. Erythroid GATA1 function revealed by genome-wide analysis of transcription factor occupancy, histone modifications, and mRNA expression. Genome Res 2009, 19:2172-2184.
58. Ko L.J., Engel J.D. DNA-binding specificities of the GATA transcription factor family. Mol Cell Biol 1993, 13:4011-4022.
59. Merika M., Orkin S.H. DNA-binding specificity of GATA family transcription factors. Mol Cell Biol 1993, 13:3999-4010.
60. Katsumura K.R., DeVilbiss A.W., Pope N.J., Johnson K.D., Bresnick E.H. Transcriptional mechanisms underlying hemoglobin synthesis. Cold Spring Harbor Perspect Med 2013, 3:a015412.
61. Kang Y.A., Sanalkumar R., O'Geen H., et al. Autophagy driven by a master regulator of hematopoiesis. Mol Cell Biol 2012, 32:226-239.
62. Welch J.J., Watts J.A., Vakoc C.R., et al. Global regulation of erythroid gene expression by transcription factor GATA-1. Blood 2004, 104:3136-3147.
63. Crispino J.D., Lodish M.B., MacKay J.P., Orkin S.H. Use of altered specificity mutants to probe a specific protein-protein interaction in differentiation: The GATA-1:FOG complex. Mol Cell 1999, 3:219-228.
64. Tsang A.P., Visvader J.E., Turner C.A., et al. FOG, a multitype zinc finger protein, acts as a cofactor for transcription factor GATA-1 in erythroid and megakaryocytic differentiation. Cell 1997, 90:109-119.
65. Johnson K.D., Boyer M.E., Kang J.A., Wickrema A., Cantor A.B., Bresnick E.H. Friend of GATA-1-independent transcriptional repression: A novel mode of GATA-1 function. Blood 2007, 109:5230-5233.
66. DeVilbiss A.W., Boyer M.E., Bresnick E.H. Establishing a hematopoietic genetic network through locus-specific integration of chromatin regulators. Proc Natl Acad Sci USA 2013, 110:E3398-E3407.
67. Hong W., Nakazawa M., Chen Y.Y., et al. FOG-1 recruits the NuRD repressor complex to mediate transcriptional repression by GATA-1. EMBO J 2005, 24:67-78.
68. Miccio A., Wang Y., Hong W., et al. NuRD mediates activating and repressive functions of GATA-1 and FOG-1 during blood development. EMBO J 2010, 29:442-456.
69. Blobel G.A., Nakajima T., Eckner R., Montminy M., Orkin S.H. CREB-binding protein cooperates with transcription factor GATA-1 and is required for erythroid differentiation. Proc Natl Acad Sci USA 1998, 95:2061-2066.
70. Hung H.L., Lau J., Kim A.Y., Weiss M.J., Blobel G.A. CREB-binding protein acetylates hematopoietic transcription factor GATA-1 at functionally important sites. Mol Cell Biol 1999, 19:3496-3505.
71. Martowicz M.L., Grass J.A., Boyer M.E., Guend H., Bresnick E.H. Dynamic GATA factor interplay at a multi-component regulatory region of the GATA-2 locus. J Biol Chem 2005, 280:1724-1732.
72. Tripic T., Deng W., Cheng Y., et al. SCL and associated protein distinguish active from repressive GATA transcription factor complexes. Blood 2008, 113:2191-2201.
73. Mikkola H.K., Klintman J., Yang H., et al. Hematopoietic stem cells retain long-term repopulating activity and multipotency in the absence of stem-cell leukemia SCL/tal-1 gene. Nature 2003, 421:547-551.
74. Porcher C., Swat W., Rockwell K., Fujiwara Y., Alt F.W., Orkin S.H. The T cell leukemia oncoprotein SCL/tal-1 is essential for development of all hematopoietic lineages. Cell 1996, 86:47-57.
75. Hall M.A., Slater N.J., Salmon J.M., et al. Functional but abnormal adult erythropoiesis in the absence of the stem cell leukemia gene. Mol Cell Biol 2005, 25:6355-6362.
76. Palii C.G., Perez-Iratxeta C., Yao Z., et al. Differential genomic targeting of the transcription factor TAL1 in alternate haematopoietic lineages. EMBO J 2011, 30:494-509.
77. Gould K.A., Bresnick E.H. Sequence determinants of DNA binding by the hematopoietic helix-loop-helix transcription factor TAL1: Importance of sequences flanking the E-box core. Gene Expr 1998, 7:87-101.
78. Wadman I.A., Osada H., Grutz G.G., et al. 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 1997, 16:3145-3157.
79. Kassouf M.T., Chagraoui H., Vyas P., Porcher C. Differential use of SCL/TAL-1 DNA-binding domain in developmental hematopoiesis. Blood 2008, 112:1056-1067.
80. Dorsett D. Distant liaisons: long-range enhancer-promoter interactions in Drosophila. Curr Opin Genet Dev 1999, 9:505-514.
81. Hacein-Bey-Abina S., Von Kalle C., Schmidt M., et al. LMO2-associated clonal T cell proliferation in two patients after gene therapy for SCID-X1. Science 2003, 302:415-419.
82. Mylona A., Andrieu-Soler C., Thongjuea S., et al. Genome-wide analysis shows that Ldb1 controls essential hematopoietic genes/pathways in mouse early development and reveals novel players in hematopoiesis. Blood 2013, 121:2902-2913.
83. Li L., Jothi R., Cui K., et al. Nuclear adaptor Ldb1 regulates a transcriptional program essential for the maintenance of hematopoietic stem cells. Nat Immunol 2011, 12:129-136.
84. Li L., Freudenberg J., Cui K., et al. Ldb1-nucleated transcription complexes function as primary mediators of global erythroid gene activation. Blood 2013, 121:4575-4585.
85. Li L., Lee J.Y., Gross J., Song S.H., Dean A., Love P.E. A requirement for Lim domain binding protein 1 in erythropoiesis. J Exp Med 2010, 207:2543-2550.
86. Love P.E., Warzecha C., Li L. Ldb1 complexes: The new master regulators of erythroid gene transcription. Trends Genet 2014, 30:1-9.
87. Miller I.J., Bieker J.J. 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 1993, 13:2776-2786.
88. Pilon A.M., Ajay S.S., Kumar S.A., et al. Genome-wide ChIP-Seq reveals a dramatic shift in the binding of the transcription factor erythroid Kruppel-like factor during erythrocyte differentiation. Blood 2011, 118:e139-e148.
89. Im H., Grass J.A., Johnson K.D., et al. Chromatin domain activation via GATA-1 utilization of a small subset of dispersed GATA motifs within a broad chromosomal region. Proc Natl Acad Sci USA 2005, 102:17065-17070.
90. Tallack M.R., Magor G.W., Dartigues B., et al. Novel roles for KLF1 in erythropoiesis revealed by mRNA-seq. Genome Res 2012, 22:2385-2398.
91. Tallack M.R., Whitington T., Yuen W.S., et al. A global role for KLF1 in erythropoiesis revealed by ChIP-seq in primary erythroid cells. Genome Res 2010, 20:1052-1063.
92. Tallack M.R., Keys J.R., Humbert P.O., Perkins A.C. EKLF/KLF1 controls cell cycle entry via direct regulation of E2f2. J Biol Chem 2009, 284:20966-20974.
93. Perkins A.C., Sharpe A.H., Orkin S.H. Lethal beta-thalassaemia in mice lacking the erythroid CACCC- transcription factor EKLF. Nature 1995, 375:318-322.
94. Pilon A.M., Arcasoy M.O., Dressman H.K., et al. Failure of terminal erythroid differentiation in EKLF-deficient mice is associated with cell cycle perturbation and reduced expression of E2F2. Mol Cell Biol 2008, 28:7394-7401.
95. Tsai F.Y., Keller G., Kuo F.C., et al. An early haematopoietic defect in mice lacking the transcription factor GATA-2. Nature 1994, 371:221-226.
96. Tsai F.-Y., Orkin S.H. Transcription factor GATA-2 is required for proliferation/survival of early hematopoietic cells and mast cell formation, but not for erythroid and myeloid terminal differentiation. Blood 1997, 89:3636-3643.
97. De Pater E., Kaimakis P., Vink C.S., et al. Gata2 is required for HSC generation and survival. J Exp Med 2013, 210:2843-2850.
98. Dorfman D.M., Wilson D.B., Bruns G.A., Orkin S.H. Human transcription factor GATA-2: Evidence for regulation of preproendothelin-1 gene expression in endothelial cells. J Biol Chem 1992, 267:1279-1285.
99. Hattangadi S.M., Wong P., Zhang L., Flygare J., Lodish H.F. From stem cell to red cell: Regulation of erythropoiesis at multiple levels by multiple proteins, RNAs, and chromatin modifications. Blood 2011, 118:6258-6268.
100. Weiss M.J., Keller G., Orkin S.H. Novel insights into erythroid development revealed through invitro differentiation of GATA-1 embryonic stem cells. Genes Dev 1994, 8:1184-1197.
101. Grass J.A., Boyer M.E., Pal S., Wu J., Weiss M.J., Bresnick E.H. GATA-1-dependent transcriptional repression of GATA-2 via disruption of positive autoregulation and domain-wide chromatin remodeling. Proc Natl Acad Sci USA 2003, 100:8811-8816.
102. Wozniak R.J., Keles S., Lugus J.J., et al. Molecular hallmarks of endogenous chromatin complexes containing master regulators of hematopoiesis. Mol Cell Biol 2008, 28:6681-6694.
103. Lugus J.J., Chung Y.S., Mills J.C., et al. GATA2 functions at multiple steps in hemangioblast development and differentiation. Development 2007, 134:393-405.
104. Dore L.C., Chlon T.M., Brown C.D., White K.P., Crispino J.D. Chromatin occupancy analysis reveals genome-wide GATA factor switching during hematopoiesis. Blood 2012, 119:3724-3733.
105. May G., Soneji S., Tipping A.J., et al. Dynamic analysis of gene expression and genome-wide transcription factor binding during lineage specification of multipotent progenitors. Cell Stem Cell 2013, 13:754-768.
106. Pal S., Cantor A.B., Johnson K.D., et al. Coregulator-dependent facilitation of chromatin occupancy by GATA-1. Proc Natl Acad Sci USA 2004, 101:980-985.
107. Sanalkumar R., Johnson K.D., Gao X., et al. Mechanism governing a stem cell-generating cis-regulatory element. Proc Natl Acad Sci USA 2014, 111:E1091-E1100.
108. Groschel S., Sanders M.A., Hoogenboezem R., et al. A single oncogenic enhancer rearrangement causes concomitant EVI1 and GATA2 deregulation in leukemia. Cell 2014, 157:369-381.
109. Yamazaki H., Suzuki M., Otsuki A., et al. A remote GATA2 hematopoietic enhancer drives leukemogenesis in inv(3)(q21;q26) by activating EVI1 expression. Cancer Cell 2014, 25:415-427.
110. Bender M.A., Roach J.N., Halow J., et al. Targeted deletion of 5'HS1 and 5'HS4 of the beta-globin locus control region reveals additive activity of the DNaseI hypersensitive sites. Blood 2001, 98:2022-2027.
111. Bender M.A., Bulger M., Close J., Groudine M. Beta-globin gene switching and DNaseI sensitivity of the endogenous beta-globin locus in mice do not require the locus control region. Mol Cell 2000, 5:387-393.
112. Hug B.A., Wesselschmidt R.L., Fiering S., et al. Analysis of mice containing a targeted deletion of beta-globin locus control region 5' hypersensitive site 3. Mol Cell Biol 1996, 16:2906-2912.
113. Fiering S., Epner E., Robinson K., et al. Targeted deletion of 5'HS2 of the murine beta-globin LCR reveals that it is not essential for proper regulation of the beta-globin locus. Genes Dev 1995, 9:2203-2213.
114. Bender M.A., Mehaffey M.G., Telling A., et al. Independent formation of DnaseI hypersensitive sites in the murine beta-globin locus control region. Blood 2000, 95:3600-3604.
115. Epner E., Reik A., Cimbora D., et al. The beta-globin LCR is not necessary for an open chromatin structure or developmentally regulated transcription of the native mouse beta-globin locus. Mol Cell 1998, 2:447-455.
116. Sung Y.H., Baek I.J., Kim D.H., et al. Knockout mice created by TALEN-mediated gene targeting. Nat Biotechnol 2013, 31:23-24.
117. Kim Y., Kweon J., Kim A., et al. A library of TAL effector nucleases spanning the human genome. Nat Biotechnol 2013, 31:251-258.
118. Cho S.W., Kim S., Kim J.M., Kim J.S. Targeted genome engineering in human cells with the Cas9 RNA-guided endonuclease. Nat Biotechnol 2013, 31:230-232.
119. Tijssen M.R., Cvejic A., Joshi A., et al. Genome-wide analysis of simultaneous GATA1/2, RUNX1, FLI1, and SCL binding in megakaryocytes identifies hematopoietic regulators. Dev Cell 2011, 20:597-609.
120. Wilson N.K., Foster S.D., Wang X., et al. Combinatorial transcriptional control in blood stem/progenitor cells: Genome-wide analysis of ten major transcriptional regulators. Cell Stem Cell 2010, 7:532-544.
121. Beck D., Thoms J.A., Perera D., et al. Genome-wide analysis of transcriptional regulators in human HSPCs reveals a densely interconnected network of coding and noncoding genes. Blood 2013, 122:e12-e22.
122. Hollenhorst P.C., McIntosh L.P., Graves B.J. Genomic and biochemical insights into the specificity of ETS transcription factors. Annu Rev Biochem 2011, 80:437-471.
123. Linnemann A.K., O'Geen H., Keles S., Farnham P.J., Bresnick E.H. Genetic framework for GATA factor function in vascular biology. Proc Natl Acad Sci USA 2011, 108:13641-13646.
124. Hsu A.P., Sampaio E.P., Khan J., et al. Mutations in GATA2 are associated with the autosomal dominant and sporadic monocytopenia and mycobacterial infection (MonoMAC) syndrome. Blood 2011, 118:2653-2655.
125. Dickinson R.E., Griffin H., Bigley V., et al. Exome sequencing identifies GATA-2 mutation as the cause of dendritic cell, monocyte, B and NK lymphoid deficiency. Blood 2011, 118:2656-2658.
126. Hahn C.N., Chong C.E., Carmichael C.L., et al. Heritable GATA2 mutations associated with familial myelodysplastic syndrome and acute myeloid leukemia. Nat Genet 2011, 43:1012-1017.
127. Ostergaard P., Simpson M.A., Connell F.C., et al. Mutations in GATA2 cause primary lymphedema associated with a predisposition to acute myeloid leukemia (Emberger syndrome). Nat Genet 2011, 43:929-931.
128. Hsu A.P., Johnson K.D., Falcone E.L., et al. GATA2 haploinsufficiency caused by mutations in a conserved intronic element leads to MonoMAC syndrome. Blood 2013, 121:3830-3837. S3831-S3837.
129. Scott E.W., Simon M.C., Anastasi J., Singh H. Requirement of transcription factor PU.1 in the development of multiple hematopoietic lineages. Science 1994, 265:1573-1577.
130. Scott E.W., Fisher R.C., Olson M.C., Kehrli E.W., Simon M.C., Singh H. PU.1 functions in a cell-autonomous manner to control the differentiation of multipotential lymphoid-myeloid progenitors. Immunity 1997, 6:437-447.
131. Leddin M., Perrod C., Hoogenkamp M., et al. Two distinct auto-regulatory loops operate at the PU.1 locus in B cells and myeloid cells. Blood 2011, 117:2827-2838.
132. Heinz S., Benner C., Spann N., et al. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol Cell 2010, 38:576-589.
133. Stopka T., Amanatullah D.F., Papetti M., Skoultchi A.I. PU.1 inhibits the erythroid program by binding to GATA-1 on DNA and creating a repressive chromatin structure. EMBO J 2005, 24:3712-3723.
134. Zhang P.J., Zhang X., Iwama A., et al. PU.1 inhibits GATA-1 function and erythroid differentiation by blocking GATA-1 DNA binding. Blood 2000, 96:2641-2648.
135. Liu F., Kang I., Park C., et al. ER71 specifies Flk-1+ hemangiogenic mesoderm by inhibiting cardiac mesoderm and Wnt signaling. Blood 2012, 119:3295-3305.
136. Lee D., Park C., Lee H., et al. ER71 acts downstream of BMP, Notch, and Wnt signaling in blood and vessel progenitor specification. Cell Stem Cell 2008, 2:497-507.
137. Sumanas S., Gomez G., Zhao Y., Park C., Choi K., Lin S. Interplay among Etsrp/ER71, Scl, and Alk8 signaling controls endothelial and myeloid cell formation. Blood 2008, 111:4500-4510.
138. Rasmussen T.L., Kweon J., Diekmann M.A., et al. ER71 directs mesodermal fate decisions during embryogenesis. Development 2011, 138:4801-4812.
139. Jochum W., Passegue E., Wagner E.F. AP-1 in mouse development and tumorigenesis. Oncogene 2001, 20:2401-2412.
140. Kanki Y., Kohro T., Jiang S., et al. Epigenetically coordinated GATA2 binding is necessary for endothelium-specific endomucin expression. EMBO J 2011, 30:2582-2595.
141. Lichtinger M., Ingram R., Hannah R., et al. RUNX1 reshapes the epigenetic landscape at the onset of haematopoiesis. EMBO J 2012, 31:4318-4333.
142. Miyamoto T., Iwasaki H., Reizis B., et al. Myeloid or lymphoid promiscuity as a critical step in hematopoietic lineage commitment. Dev Cell 2002, 3:137-147.
143. Akashi K. Lineage promiscuity and plasticity in hematopoietic development. Ann NY Acad Sci 2005, 1044:125-131.
144. Hu M., Krause D., Greaves M., et al. Multilineage gene expression precedes commitment in the hemopoietic system. Genes Dev 1997, 11:774-785.
145. Cirillo L.A., Zaret K.S. An early developmental transcription factor complex that is more stable on nucleosome core particles than on free DNA. Mol Cell 1999, 4:961-969.
146. Bresnick E.H., Martowicz M.L., Pal S., Johnson K.D. Developmental control via GATA factor interplay at chromatin domains. J Cell Physiol 2005, 205:1-9.
147. Kadauke S., Udugama M.I., Pawlicki J.M., et al. Tissue-specific mitotic bookmarking by hematopoietic transcription factor GATA1. Cell 2012, 150:725-737.
148. Mouse E.C., Stamatoyannopoulos J.A., Snyder M., et al. An encyclopedia of mouse DNA elements (Mouse ENCODE). Genome Biol 2012, 13:418.
149. Gerstein M.B., Kundaje A., Hariharan M., et al. Architecture of the human regulatory network derived from ENCODE data. Nature 2012, 489:91-100.
150. Ruau D., Ng F.S., Wilson N.K., et al. Building an ENCODE-style data compendium on a shoestring. Nat Methods 2013, 10:926.
151. Hannah R., Joshi A., Wilson N.K., Kinston S., Gottgens B. A compendium of genome-wide hematopoietic transcription factor maps supports the identification of gene regulatory control mechanisms. Exp Hematol 2011, 39:531-541.
152. Chacon D., Beck D., Perera D., Wong J.W., Pimanda J.E. BloodChIP: a database of comparative genome-wide transcription factor binding profiles in human blood cells. Nucleic Acids Res 2014, 42:D172-D177.
153. Shankaranarayanan P., Mendoza-Parra M.A., Walia M., et al. Single-tube linear DNA amplification (LinDA) for robust ChIP-seq. Nat Methods 2011, 8:565-567.
154. Adli M., Bernstein B.E. Whole-genome chromatin profiling from limited numbers of cells using nano-ChIP-seq. Nat Protocols 2011, 6:1656-1668.
155. Gilfillan G.D., Hughes T., Sheng Y., et al. Limitations and possibilities of low cell number ChIP-seq. BMC Genomics 2012, 13:645.
156. Moignard V., Macaulay I.C., Swiers G., et al. Characterization of transcriptional networks in blood stem and progenitor cells using high-throughput single-cell gene expression analysis. Nat Cell Biol 2013, 15:363-372.
157. Novershtern N., Subramanian A., Lawton L.N., et al. Densely interconnected transcriptional circuits control cell states in human hematopoiesis. Cell 2011, 144:296-309.
158. Forsberg E.C., Bresnick E.H. Histone acetylation beyond promoters: long-range acetylation patterns in the chromatin world. Bioessays 2001, 23:820-830.
159. Wu C.T., Morris J.R. Transvection and other homology effects. Curr Opin Genet Dev 1999, 9:237-246.
160. Krivega I., Dean A. Enhancer and promoter interactions-long distance calls. Curr Opin Genet Dev 2012, 22:79-85.
161. Dekker J., Marti-Renom M.A., Mirny L.A. Exploring the three-dimensional organization of genomes: Interpreting chromatin interaction data. Nat Rev Genet 2013, 14:390-403.
162. Horike S., Cai S., Miyano M., Cheng J.F., Kohwi-Shigematsu T. Loss of silent-chromatin looping and impaired imprinting of DLX5 in Rett syndrome. Nat Genet 2005, 37:31-40.
163. Handoko L., Xu H., Li G., et al. CTCF-mediated functional chromatin interactome in pluripotent cells. Nat Genet 2011, 43:630-638.
164. Fullwood M.J., Wei C.L., Liu E.T., Ruan Y. Next-generation DNA sequencing of paired-end tags (PET) for transcriptome and genome analyses. Genome Res 2009, 19:521-532.