GATA-1 genome-wide occupancy associates with distinct epigenetic profiles in mouse fetal liver erythropoiesis

Nucleic Acids Research

Volumn 41, Issue 9, 2013, Pages 4938-4948

  Papadopoulos, Giorgio L ^a,b   Karkoulia, Elena ^a,b   Tsamardinos, Ioannis ^b,c   Porcher, Catherine ^d   Ragoussis, Jiannis ^e   Bungert, Jörg ^f   Strouboulis, John ^a  

^a BIOMEDICAL SCIENCES RESEARCH CENTER ALEXANDER FLEMING   (Greece)

^b UNIVERSITY OF CRETE   (Greece)

^c INSTITUTE OF COMPUTER SCIENCE   (Greece)

^d UNIVERSITY OF OXFORD   (United Kingdom)

^e UNIVERSITY OF OXFORD   (United Kingdom)

^f UNIVERSITY OF FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H3; HISTONE H4; PROTEIN H3K27; PROTEIN H3K4; PROTEIN H4K16; TRANSCRIPTION FACTOR GATA 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL FRACTIONATION; CELL MATURATION; CHROMATIN STRUCTURE; DOWN REGULATION; EMBRYO; EPIGENETICS; ERYTHROBLAST; ERYTHROID CELL; ERYTHROPOIESIS; FETUS; FETUS LIVER; GENE CLUSTER; GENE EXPRESSION; GENE FUNCTION; GENE TARGETING; GENETIC ASSOCIATION; GENETIC VARIABILITY; HISTONE ACETYLATION; HISTONE MODIFICATION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RANDOM FOREST; UPREGULATION;

ANIMALS; CELLS, CULTURED; EPIGENESIS, GENETIC; ERYTHROID CELLS; ERYTHROPOIESIS; FETUS; GATA1 TRANSCRIPTION FACTOR; GENOME; HISTONES; LIVER; MICE;

EID: 84877296422     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt167     Document Type: Article

References (54)

1. Magnusdottir, E., Gillich, A., Grabole, N. and Surani, M.A. (2012) Combinatorial control of cell fate and reprogramming in the mammalian germline. Curr. Opin. Genet. Dev., 22, 466-474.
2. Dillon, N. (2012) Factor mediated gene priming in pluripotent stem cells sets the stage for lineage specification. Bioessays, 34, 194-204.
3. Furey, T.S. (2012) ChIP-seq and beyond: new and improved methodologies to detect and characterize protein-DNA interactions. Nat. Rev. Genet., 13, 840-852.
4. Tsiftsoglou, A.S., Vizirianakis, I.S. and Strouboulis, J. (2009) Erythropoiesis: model systems, molecular regulators, and developmental programs. IUBMB Life, 61, 800-830.
5. Socolovsky, M., Nam, H., Fleming, M.D., Haase, V.H., Brugnara, C. and Lodish, H.F. (2001) Ineffective erythropoiesis in Stat5a(-/-) 5b(-/-) mice due to decreased survival of early erythroblasts. Blood, 98, 3261-3273.
6. Gutierrez, L., Lindeboom, F., Ferreira, R., Drissen, R., Grosveld, F., Whyatt, D. and Philipsen, S. (2005) A hanging drop culture method to study terminal erythroid differentiation. Exp. Hematol., 33, 1083-1091.
7. Kina, T., Ikuta, K., Takayama, E., Wada, K., Majumdar, A.S., Weissman, I.L. and Katsura, Y. (2000) The monoclonal antibody TER-119 recognizes a molecule associated with glycophorin A and specifically marks the late stages of murine erythroid lineage. Br. J. Haematol., 109, 280-287.
8. Hattangadi, S.M., Wong, P., Zhang, L., Flygare, J. and Lodish, H.F. (2011) From stem cell to red cell: regulation of erythropoiesis at multiple levels by multiple proteins, RNAs, and chromatin modifications. Blood, 118, 6258-6268.
9. Welch, J.J., Watts, JA., Vakoc, C.R., Yao, Y., Wang, H., Hardison, R.C, Blobel, GA., Chodosh, LA. and Weiss, M.J. (2004) Global regulation of erythroid gene expression by transcription factor GATA-1. Blood, 104, 3136-3147.
10. Rodriguez, P., Bonte, E., Krijgsveld, J., Kolodziej, K.E., Guyot, B., Heck, A.J., Vyas, P., de Boer, E., Grosveld, F. and Strouboulis, J. (2005) GATA-1 forms distinct activating and repressive complexes in erythroid cells. EMBO J., 24, 2354-2366.
11. Ferreira, R., Ohneda, K., Yamamoto, M. and Philipsen, S. (2005) GATA1 function, a paradigm for transcription factors in hematopoiesis. Mol. Cell. Biol., 25, 1215-1227.
12. Crispino, J.D. (2005) GATA1 in normal and malignant hematopoiesis. Semin. Cell Dev. Biol., 16, 137-147.
13. Cantor, A.B. and Orkin, S.H. (2002) Transcriptional regulation of erythropoiesis: an affair involving multiple partners. Oncogene, 21, 3368-3376.
14. Letting, D.L., Rakowski, C, Weiss, M.J. and Blobel, GA. (2003) Formation of a tissue-specific histone acetylation pattern by the hematopoietic transcription factor GATA-1. Mol. Cell. Biol., 23, 1334-1340.
15. Steger, D.J., Lefterova, M.I., Ying, L., Stonestrom, A.J., Schupp, M., Zhuo, D., Vakoc, A.L., Kim, J.E., Chen, J., Lazar, MA. et al. (2008) DOT1L/KMT4 recruitment and H3K79 methylation are ubiquitously coupled with gene transcription in mammalian cells. Mol. Cell. Biol., 28, 2825-2839.
16. Yu, M., Riva, L., Xie, H., Schindler, Y., Moran, T.B., Cheng, Y., Yu, D., Hardison, R., Weiss, M.J., Orkin, S.H. et al. (2009) Insights into GATA-1-mediated gene activation versus repression via genome-wide chromatin occupancy analysis. Mol. Cell, 36, 682-695.
17. Heyworth, C, Pearson, S., May, G and Enver, T. (2002) Transcription factor-mediated lineage switching reveals plasticity in primary committed progenitor cells. EMBO J., 21, 3770-3781.
18. Graf, T. (2002) Differentiation plasticity of hematopoietic cells. Blood, 99, 3089-3101.
19. Iwasaki, H., Mizuno, S., Wells, R.A., Cantor, A.B., Watanabe, S. and Akashi, K. (2003) GATA-1 converts lymphoid and myelomonocytic progenitors into the megakaryocyte/erythrocyte lineages. Immunity, 19, 451-462.
20. Wickrema, A. and Crispino, J.D. (2007) Erythroid and megakaryocytic transformation. Oncogene, 26, 6803-6815.
21. Bresnick, E.H., Lee, HY., Fujiwara, T., Johnson, K.D. and Keles, S. (2010) GATA switches as developmental drivers. J. Biol. Chem., 285, 31087-31093.
22. Nakajima, H. (2011) Role of transcription factors in differentiation and reprogramming of hematopoietic cells. Keio J. Med., 60, 47-55.
23. Soler, E., Andrieu-Soler, C, de Boer, E., Bryne, J.C, Thongjuea, S., Stadhouders, R., Palstra, R.J., Stevens, M., Kockx, C, van Ijcken, W. et al. (2010) The genome-wide dynamics of the binding of Ldb1 complexes during erythroid differentiation. Genes Dev., 24, 277-289.
24. Cheng, Y., Wu, W., Kumar, S.A., Yu, D., Deng, W., Tripic, T., King, D.C., Chen, K.B., 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.
25. Fujiwara, T., O'Geen, H., Keles, S., Blahnik, K., Linnemann, A.K., Kang, Y.A., Choi, K., Farnham, P.J. and Bresnick, E.H. (2009) Discovering hematopoietic mechanisms through genome-wide analysis of GATA factor chromatin occupancy. Mol. Cell, 36, 667-681.
26. Wontakal, S.N., Guo, X., Smith, C., MacCarthy, T., Bresnick, E.H., Bergman, A., Snyder, M.P., Weissman, S.M., Zheng, D. and Skoultchi, A.I. (2012) A core erythroid transcriptional network is repressed by a master regulator of myelo-lymphoid differentiation. Proc. Natl Acad. Sci. USA, 109, 3832-3837.
27. Dore, L.C., Chlon, T.M., Brown, C.D., White, K.P. and Crispino, J.D. (2012) Chromatin occupancy analysis reveals genome-wide GATA factor switching during hematopoiesis. Blood, 119, 3724-3733.
28. Chlon, T.M., Dore, L.C. and Crispino, J.D. (2012) Cofactor-mediated restriction of GATA-1 chromatin occupancy coordinates lineage-specific gene expression. Mol. Cell, 47, 608-621.
29. Tijssen, M.R., Cvejic, A., Joshi, A., Hannah, R.L., Ferreira, R., Forrai, A., Bellissimo, D.C., Oram, S.H., Smethurst, P.A., Wilson, N.K. et al. Genome-wide analysis of simultaneous GATA1/2, RUNX1, FLI1, and SCL binding in megakaryocytes identifies hematopoietic regulators. Dev. Cell, 20, 597-609.
30. Kassouf, M.T., Hughes, J.R., Taylor, S., McGowan, S.J., Soneji, S., Green, A.L., Vyas, P. and 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.
31. Tallack, M.R., Whitington, T., Yuen, W.S., Wainwright, E.N., Keys, J.R., Gardiner, B.B., Nourbakhsh, E., Cloonan, N., Grimmond, S.M., Bailey, T.L. et al. (2010) A global role for KLF1 in erythropoiesis revealed by ChIP-seq in primary erythroid cells. Genome Res., 20, 1052-1063.
32. Pilon, A.M., Ajay, S.S., Kumar, S.A., Steiner, L.A., Cherukuri, P.F., Wincovitch, S., Anderson, S.M., Mullikin, J.C., Gallagher, P.G., Hardison, R.C. et al. (2011) Genome-wide ChIP-Seq reveals a dramatic shift in the binding of the transcription factor erythroid Kruppel-like factor during erythrocyte differentiation. Blood, 118, e139-e148.
33. Wu, W., Cheng, Y., Keller, C.A., Ernst, J., Kumar, S.A., Mishra, T., Morrissey, C., Dorman, C.M., Chen, K.B., Drautz, D. et al. (2011) Dynamics of the epigenetic landscape during erythroid differentiation after GATA1 restoration. Genome Res., 21, 1659-1671.
34. von Lindern, M., Deiner, E.M., Dolznig, H., Parren-Van Amelsvoort, M., Hayman, M.J., Mullner, E.W. and Beug, H. (2001) Leukemic transformation of normal murine erythroid progenitors: v-and c-ErbB act through signaling pathways activated by the EpoR and c-Kit in stress erythropoiesis. Oncogene, 20, 3651-3664.
35. Schuh, A.H., Tipping, A.J., Clark, A.J., Hamlett, I., Guyot, B., Iborra, F.J., Rodriguez, P., Strouboulis, J., Enver, T., Vyas, P. et al. (2005) ETO-2 associates with SCL in erythroid cells and megakaryocytes and provides repressor functions in erythropoiesis. Mol. Cell. Biol., 25, 10235-10250.
36. Valouev, A., Johnson, D.S., Sundquist, A., Medina, C., Anton, E., Batzoglou, S., Myers, R.M. and Sidow, A. (2008) Genome-wide analysis of transcription factor binding sites based on ChIP-Seq data. Nat. Methods, 5, 829-834.
37. Guberman, J.M., Ai, J., Arnaiz, O., Baran, J., Blake, A., Baldock, R., Chelala, C., Croft, D., Cros, A., Cutts, R.J. et al. (2011) BioMart Central Portal: an open database network for the biological community. Database, 2011, bar041.
38. Barrett, T., Wilhite, S.E., Ledoux, P., Evangelista, C., Kim, I.F., Tomashevsky, M., Marshall, K.A., Phillippy, K.H., Sherman, P.M., Holko, M. et al. (2013) NCBI GEO: archive for functional genomics data sets-update. Nucleic Acids Res., 41, D991-D995.
39. Feng, J., Liu, T., Qin, B., Zhang, Y. and Liu, X.S. (2012) Identifying ChIP-seq enrichment using MACS. Nat. Protoc., 7, 1728-1740.
40. Martowicz, M.L., Grass, J.A., Boyer, M.E., Guend, H. and Bresnick, E.H. (2005) Dynamic GATA factor interplay at a multicomponent regulatory region of the GATA-2 locus. J. Biol. Chem., 280, 1724-1732.
41. Valverde-Garduno, V., Guyot, B., Anguita, E., Hamlett, I., Porcher, C. and Vyas, P. (2004) Differences in the chromatin structure and cis-element organization of the human and mouse GATA1 loci: implications for cis-element identification. Blood, 104, 3106-3116.
42. MacQuarrie, K.L., Fong, A.P., Morse, R.H. and Tapscott, S.J. (2011) Genome-wide transcription factor binding: beyond direct target regulation. Trends Genet., 27, 141-148.
43. Kerenyi, M.A. and Orkin, S.H. (2010) Networking erythropoiesis. J. Exp. Med., 207, 2537-2541.
44. Breiman, L. (2001) Random forests. Mach. Learn., 45, 5-32.
45. Wong, P., Hattangadi, S.M., Cheng, A.W., Frampton, G.M., Young, R.A. and Lodish, H.F. (2011) Gene induction and repression during terminal erythropoiesis are mediated by distinct epigenetic changes. Blood, 118, e128-e138.
46. Huang da, W., Sherman, B.T. and Lempicki, R.A. (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc., 4, 44-57.
47. Shearstone, J.R., Pop, R., Bock, C., Boyle, P., Meissner, A. and Socolovsky, M. (2011) Global DNA demethylation during mouse erythropoiesis in vivo. Science, 334, 799-802.
48. Kowalczyk, M.S., Hughes, J.R., Garrick, D., Lynch, M.D., Sharpe, J.A., Sloane-Stanley, J.A., McGowan, S.J., De Gobbi, M., Hosseini, M., Vernimmen, D. et al. (2012) Intragenic enhancers act as alternative promoters. Mol. Cell, 45, 447-458.
49. Blobel, G.A., Nakajima, T., Eckner, R., Montminy, M. and Orkin, S.H. (1998) CREB-binding protein cooperates with transcription factor GATA-1 and is required for erythroid differentiation. Proc. Natl Acad. Sci. USA, 95, 2061-2066.
50. Watamoto, K., Towatari, M., Ozawa, Y., Miyata, Y., Okamoto, M., Abe, A., Naoe, T. and Saito, H. (2003) Altered interaction of HDAC5 with GATA-1 during MEL cell differentiation. Oncogene, 22, 9176-9184.
51. Jin, Q., Yu, L.R., Wang, L., Zhang, Z., Kasper, L.H., Lee, J.E., Wang, C., Brindle, P.K., Dent, S.Y. and Ge, K. (2011) Distinct roles of GCN5/PCAF-mediated H3K9ac and CBP/p300-mediated H3K18/27ac in nuclear receptor transactivation. EMBO J., 30, 249-262.
52. Galvez, A.F., Huang, L., Magbanua, M.M., Dawson, K. and Rodriguez, R.L. (2011) Differential expression of thrombospondin (THBS1) in tumorigenic and nontumorigenic prostate epithelial cells in response to a chromatin-binding soy peptide. Nutr. Cancer, 63, 623-636.
53. Pekowska, A., Benoukraf, T., Ferrier, P. and Spicuglia, S. (2010) A unique H3K4me2 profile marks tissue-specific gene regulation. Genome Res., 20, 1493-1502.
54. Orford, K., Kharchenko, P., Lai, W., Dao, M.C., Worhunsky, D.J., Ferro, A., Janzen, V., Park, P.J. and Scadden, D.T. (2008) Differential H3K4 methylation identifies developmentally poised hematopoietic genes. Dev. Cell, 14, 798-809.