Dynamics of the epigenetic landscape during erythroid differentiation after GATA1 restoration

Genome Research

Volumn 21, Issue 10, 2011, Pages 1659-1671

  Wu, Weisheng ^a   Cheng, Yong ^a   Keller, Cheryl A ^a   Ernst, Jason ^b,c   Kumar, Swathi Ashok ^a   Mishra, Tejaswini ^a   Morrissey, Christapher ^a   Dorman, Christine M ^a   Chen, Kuan Bei ^a   Drautz, Daniela ^a   Giardine, Belinda ^a   Shibata, Yoichiro ^d   Song, Lingyun ^d   Pimkin, Max ^e   Crawford, Gregory E ^d   Furey, Terrence S ^f   Kellis, Manolis ^b,c   Miller, Webb ^a   Taylor, James ^g   Schuster, Stephan C ^a   Zhang, Yu ^a   Chiaromonte, Francesca ^a   Blobel, Gerd A ^e   Weiss, Mitchell J ^e   Hardison, Ross C ^a   more..

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^d DUKE UNIVERSITY   (United States)

^e CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^f UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^g EMORY UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEAR PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GATA 1;

ARTICLE; CELL DIFFERENTIATION; CHROMATIN STRUCTURE; EPIGENETICS; ERYTHROID CELL; GENE ACTIVATION; GENE CONTROL; GENE EXPRESSION PROFILING; GENE REPRESSION; GENETIC ASSOCIATION; HISTONE MODIFICATION; HUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; TRANSCRIPTION REGULATION;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL DIFFERENTIATION; CELL LINE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN IMMUNOPRECIPITATION; EPIGENESIS, GENETIC; ERYTHROPOIESIS; ESTRADIOL; GATA1 TRANSCRIPTION FACTOR; GATA2 TRANSCRIPTION FACTOR; GENE EXPRESSION PROFILING; GENE SILENCING; MICE; MULTIVARIATE ANALYSIS; PEPTIDE HYDROLASES; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS; RECEPTORS, ESTROGEN; RECOMBINANT PROTEINS; REGULATORY SEQUENCES, NUCLEIC ACID;

EID: 80053516108     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.125088.111     Document Type: Article

References (63)

1. Anguita E, Hughes J, Heyworth C, Blobel GA, Wood WG, Higgs DR. 2004. Globin gene activation during haemopoiesis is driven by protein complexes nucleated by GATA-1 and GATA-2. EMBO J 23: 2841-2852. (Pubitemid 39013556)
2. Barton MC, Crowe AJ. 2001. Chromatin alteration, transcription and replication:What's the opening line to the story?Oncogene 20: 3094-3099. (Pubitemid 32553564)
3. Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B Methodol 57: 289-300.
4. Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J, Fry B, Meissner A, Wernig M, Plath K, et al. 2006. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125: 315-326.
5. The ENCODE Project Consortium. 2007. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 447: 799-816.
6. Boyle AP, Davis S, Shulha HP, Meltzer P, Margulies EH, Weng Z, Furey TS, Crawford GE. 2008a. High-resolution mapping and characterization of open chromatin across the genome. Cell 132: 311-322. (Pubitemid 351172431)
7. Boyle AP, Guinney J, Crawford GE, Furey TS. 2008b. F-Seq: a feature density estimator for high-throughput sequence tags. Bioinformatics 24: 2537-2538.
8. Chen KB, Zhang Y. 2010. A varying threshold method for ChIP peak-calling using multiple sources of information. Bioinformatics 26: i504-i510.
9. Cheng Y, King DC, Dore LC, Zhang X, Zhou Y, Zhang Y, Dorman C, Abebe D, Kumar SA, Chiaromonte F, et al. 2008. Transcriptional enhancement by GATA1-occupied DNA segments is strongly associated with evolutionary constraint on the binding site motif. Genome Res 18: 1896-1905.
10. Cheng Y, Wu W, Kumar SA, Yu D, Deng W, Tripic T, King DC, Chen KB, Zhang Y, Drautz D, et al. 2009. Erythroid GATA1 function revealed by genome-wide analysis of transcription factor occupancy, histone modifications, and mRNA expression. Genome Res 19: 2172-2184.
11. Davidson EH, Erwin DH. 2006. Gene regulatory networks and the evolution of animal body plans. Science 311: 796-800.
12. Ernst J, Kellis M. 2010. Discovery and characterization of chromatin states for systematic annotation of the human genome. Nat Biotechnol 28: 817-825.
13. Felsenfeld G, Groudine M. 2003. Controlling the double helix. Nature 421: 448-453. (Pubitemid 36157954)
14. Filion GJ, van Bemmel JG, Braunschweig U, Talhout W, Kind J, Ward LD, Brugman W, De Castro IJ, Kerkhoven RM, Bussemaker HJ, et al. 2010. Systematic protein location mapping reveals five principal chromatin types in Drosophila cells. Cell 143: 212-224.
15. Fujiwara T, O'Geen H, Keles S, Blahnik K, Linnemann AK, Kang YA, Choi K, Farnham PJ, Bresnick EH. 2009. Discovering hematopoietic mechanisms through genome-wide analysis of GATA factor chromatin occupancy. Mol Cell 36: 667-681.
16. Goldberg AD, Allis CD, Bernstein E. 2007. Epigenetics: a landscape takes shape. Cell 128: 635-638. (Pubitemid 46273578)
17. Grass JA, Boyer ME, Pal S, Wu J, Weiss MJ, Bresnick EH. 2003. GATA-1- dependent transcriptional repression of GATA-2 via disruption of positive autoregulation and domain-wide chromatin remodeling. Proc Natl Acad Sci 100: 8811-8816. (Pubitemid 36899180)
18. Gross D, Garrard W. 1988. Nuclease hypersensitive sites in chromatin. Annu Rev Biochem 57: 159-197.
19. Groudine M, Weintraub H. 1981. Activation of globin genes during chicken development. Cell 24: 393-401. (Pubitemid 11066823)
20. He HH, Meyer CA, Shin H, Bailey ST,Wei G,Wang Q, Zhang Y, Xu K, Ni M, Lupien M, et al. 2010. Nucleosome dynamics define transcriptional enhancers. Nat Genet 42: 343-347.
21. Heintzman ND, Stuart RK, Hon G, Fu Y, ChingCW, Hawkins RD, Barrera LO, van Calcar S, Qu C, Ching KA, et al. 2007. Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat Genet 39: 311-318. (Pubitemid 46328487)
22. Heinz S, Benner C, Spann N, Bertolino E, Lin YC, Laslo P, Cheng JX, Murre C, Singh H, Glass CK. 2010. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol Cell 38: 576-589.
23. Jing H, Vakoc CR, Ying L, Mandat S, Wang H, Zheng X, Blobel GA. 2008. Exchange of GATA factors mediates transitions in looped chromatin organization at a developmentally regulated gene locus. Mol Cell 29: 232-242. (Pubitemid 351172817)
24. John S, Sabo PJ, Johnson TA, Sung MH, Biddie SC, Lightman SL, Voss TC, Davis SR, Meltzer PS, Stamatoyannopoulos JA, et al. 2008. Interaction of the glucocorticoid receptor with the chromatin landscape. Mol Cell 29: 611-624. (Pubitemid 351374691)
25. John S, Sabo PJ, Thurman RE, Sung MH, Biddie SC, Johnson TA, Hager GL, Stamatoyannopoulos JA. 2011. Chromatin accessibility pre-determines glucocorticoid receptor binding patterns. Nat Genet 43: 264-268.
26. Kadam S, McAlpine GS, Phelan ML, Kingston RE, Jones KA, Emerson BM. 2000. Functional selectivity of recombinant mammalian SWI/SNF subunits. Genes Dev 14: 2441-2451.
27. Kassouf MT, Chagraoui H, Vyas P, Porcher C. 2008. Differential use of SCL/ TAL-1 DNA-binding domain in developmental hematopoiesis. Blood 112: 1056-1067.
28. 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.
29. Ko LJ, Engel JD. 1993. DNA-binding specificities of the GATA transcription factor family. Mol Cell Biol 13: 4011-4022. (Pubitemid 23187629)
30. Layon ME, Ackley CJ, West RJ, Lowrey CH. 2007. Expression of GATA-1 in a non-hematopoietic cell line induces beta-globin locus control region chromatin structure remodeling and an erythroid pattern of gene expression. J Mol Biol 366: 737-744. (Pubitemid 46175881)
31. Leonard M, Brice M, Engel JD, Papayannopoulou, T. 1993. Dynamics of GATA transcription factor expression during erythroid differentiation. Blood 82: 1071-1079. (Pubitemid 23253977)
32. Letting DL, Rakowski C, Weiss MJ, Blobel GA. 2003. Formation of a tissuespecific histone acetylation pattern by the hematopoietic transcription factor GATA-1. Mol Cell Biol 23: 1334-1340. (Pubitemid 36177041)
33. Martowicz ML, Grass JA, Boyer ME, Guend H, Bresnick EH. 2005. Dynamic GATA factor interplay at a multicomponent regulatory region of the GATA-2 locus. J Biol Chem 280: 1724-1732.
34. Muller J, Hart CM, Francis NJ, Vargas ML, Sengupta A, Wild B, Miller EL, O'Connor MB, Kingston RE, Simon JA. 2002. Histone methyltransferase activity of a Drosophila Polycomb group repressor complex. Cell 111: 197-208. (Pubitemid 35292440)
35. Munugalavadla V, Dore LC, Tan BL, Hong L, Vishnu M, Weiss MJ, Kapur R. 2005. Repression of c-kit and its downstream substrates by GATA-1 inhibits cell proliferation during erythroid maturation. Mol Cell Biol 25: 6747-6759. (Pubitemid 41023246)
36. Narlikar GJ, Fan HY, Kingston RE. 2002. Cooperation between complexes that regulate chromatin structure and transcription. Cell 108: 475-487. (Pubitemid 34260873)
37. Nichols KE, Crispino JD, Poncz M, White JG, Orkin SH, Maris JM, Weiss MJ. 2000. Familial dyserythropoietic anaemia and thrombocytopenia due to an inherited mutation in GATA1. Nat Genet 24: 266-270. (Pubitemid 30132195)
38. Pilon AM, Subramanian SA, Kumar SA, Steiner LA, Cherukuri P, Wincovitch S, Anderson SM, Mullikin J, Gallagher PG, Hardison R, et al. 2011. Genome-wide ChIP-seq reveals a dramatic shift in the binding of the transcription factor erythroid krupple-like factor (EKLF) during erythrocyte differentiation. Blood (in press).
39. Pop R, Shearstone JR, Shen Q, Liu Y, Hallstrom K, Koulnis M, Gribnau J, Socolovsky M. 2010. A key commitment step in erythropoiesis is synchronized with the cell cycle clock through mutual inhibition between PU.1 and S-phase progression. PLoS Biol 8: e1000484. doi: 10.1371/journal.pbio.1000484.
40. Porcher C, Liao EC, Fujiwara Y, Zon LI, Orkin SH. 1999. Specification of hematopoietic and vascular development by the bHLH transcription factor SCL without direct DNA binding. Development 126: 4603-4615.
41. Schotta G, Ebert A, Krauss V, Fischer A, Hoffmann J, Rea S, Jenuwein T, Dorn R, Reuter G. 2002. Central role of Drosophila SU(VAR)3-9 in histone H3- K9 methylation and heterochromatic gene silencing. EMBO J 21: 1121-1131. (Pubitemid 34206185)
42. Smale ST. 2010. Pioneer factors in embryonic stem cells and differentiation. Curr Opin Genet Dev 20: 519-526.
43. Soler E, Andrieu-Soler C, De Boer E, Bryne JC, Thongjuea S, Stadhouders R, Palstra RJ, Stevens M, Kockx C, van Ijcken W, et al. 2010. The genomewide dynamics of the binding of Ldb1 complexes during erythroid differentiation. Genes Dev 24: 277-289.
44. Steiner LA, Maksimova Y, Schulz V, Wong C, Raha D, Mahajan MC, Weissman SM, Gallagher PG. 2009. Chromatin architecture and transcription factor binding regulate expression of erythrocyte membrane protein genes. Mol Cell Biol 29: 5399-5412.
45. Tallack MR, Whitington T, Yuen WS, Wainwright EN, Keys JR, Gardiner BB, Nourbakhsh E, Cloonan N, Grimmond SM, Bailey TL, et al. 2010. A global role for KLF1 in erythropoiesis revealed by ChIP-seq in primary erythroid cells. Genome Res 20: 1052-1063.
46. 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.
47. Tsai FY, Keller GH, Kuo FC,Weiss M, Chen J, Rosenblatt M, Alt FW, Orkin SH. 1994. An early haematopoietic defect in mice lacking the transcription factor GATA-2. Nature 371: 221-226. (Pubitemid 24293019)
48. Vakoc CR, Letting DL, Gheldof N, Sawado T, Bender MA, Groudine M,Weiss MJ, Dekker J, Blobel GA. 2005. Proximity among distant regulatory elements at the beta-globin locus requires GATA-1 and FOG-1. Mol Cell 17: 453-462. (Pubitemid 40193315)
49. Wadman IA, Osada H, Grutz G, 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/NL1 proteins. EMBO J 16: 3145-3157. (Pubitemid 27234954)
50. Walsh JC, DeKoter RP, Lee HJ, Smith ED, Lancki DW, Gurish MF, Friend DS, Stevens RL, Anastasi J, Singh H. 2002. Cooperative and antagonistic interplay between PU.1 and GATA-2 in the specification of myeloid cell fates. Immunity 17: 665-676. (Pubitemid 35351511)
51. Wang H, Zhang Y, Cheng Y, Zhou Y, King DC, Taylor J, Chiaromonte F, Kasturi J, Petrykowska H, Gibb B, et al. 2006. Experimental validation of predicted mammalian erythroid cis-regulatory modules. Genome Res 16: 1480-1492. (Pubitemid 44878487)
52. Weiss MJ, Keller G, Orkin SH. 1994. Novel insights into erythroid development revealed through in vitro differentiation of GATA-1- embryonic stem cells. Genes Dev 8: 1184-1197. (Pubitemid 24163446)
53. Weiss MJ, Yu C, Orkin SH. 1997. Erythroid-cell-specific properties of transcription factor GATA-1 revealed by phenotypic rescue of a genetargeted cell line. Mol Cell Biol 17: 1642-1651. (Pubitemid 27097393)
54. Welch JJ, Watts JA, Vakoc CR, Yao Y, Wang H, Hardison RC, Blobel GA, Chodosh LA, Weiss MJ. 2004. Global regulation of erythroid gene expression by transcription factor GATA-1. Blood 104: 3136-3147. (Pubitemid 39507127)
55. Wilson NK, Miranda-Saavedra D, Kinston S, Bonadies N, Foster SD, Calero- Nieto F, Dawson MA, Donaldson IJ, Dumon S, Frampton J, et al. 2009. The transcriptional program controlled by the stem cell leukemia gene Scl/Tal1 during early embryonic hematopoietic development. Blood 113: 5456-5465.
56. Wilson NK, Foster SD, Wang X, Knezevic K, Schutte J, Kaimakis P, Chilarska PM, Kinston S, Ouwehand WH, Dzierzak E, et al. 2010. Combinatorial transcriptional control in blood stem/progenitor cells: genome-wide analysis of 10 major transcriptional regulators. Cell Stem Cell 7: 532-544.
57. Wold B, Myers RM. 2008. Sequence census methods for functional genomics. Nat Methods 5: 19-21.
58. Wozniak RJ, Keles S, Lugus JJ, Young KH, Boyer ME, Tran TM, Choi K, Bresnick EH. 2008. Molecular hallmarks of endogenous chromatin complexes containing master regulators of hematopoiesis. Mol Cell Biol 28: 6681-6694.
59. Yamamoto M, Ko LJ, Leonard MW, Beug H, Orkin SH, Engel JD. 1990. Activity and tissue-specific expression of the transcription factor NF-E1 multigene family. Genes Dev 4: 1650-1662.
60. Yu M, Riva L, Xie H, Schindler Y, Moran TB, Cheng Y, Yu D, Hardison R, Weiss MJ, Orkin SH, et al. 2009. Insights into GATA-1-mediated gene activation versus repression via genome-wide chromatin occupancy analysis. Mol Cell 36: 682-695.
61. Zhang J, Socolovsky M, Gross AW, Lodish HF. 2003. Role of Ras signaling in erythroid differentiation of mouse fetal liver cells: functional analysis by a flow cytometry-based novel culture system. Blood 102: 3938-3946. (Pubitemid 37486974)
62. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, Nussbaum C, Myers RM, Brown M, LiW, et al. 2008. Model-based analysis of ChIPSeq (MACS). Genome Biol 9: R137. doi: 10.1186/gb-2008-9-9-r137.
63. Zhang Y, Wu W, Cheng Y, King DC, Harris RS, Taylor J, Chiaromonte F, Hardison RC. 2009. Primary sequence and epigenetic determinants of in vivo occupancy of genomic DNA by GATA1. Nucleic Acids Res 37: 7024-7038.