Integration of Elf-4 into stem/progenitor and erythroid regulatory networks through locus-wide chromatin studies coupled with in vivo functional validation

Molecular and Cellular Biology

Volumn 32, Issue 4, 2012, Pages 763-773

  Smith, Aileen M ^a   Calero Nieto, Fernando J ^a   Schütte, Judith ^a   Kinston, Sarah ^a   Timms, Richard T ^a   Wilson, Nicola K ^a   Hannah, Rebecca L ^a   Landry, Josette Renee ^a   Göttgens, Berthold ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ELF 4; TRANSCRIPTION FACTOR ERG; TRANSCRIPTION FACTOR FLI 1; TRANSCRIPTION FACTOR PU 1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CELL MATURATION; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; EMBRYO; ENDOTHELIUM CELL; ERYTHROID CELL; FETUS LIVER; GENE REGULATORY NETWORK; HEART; HEMATOPOIETIC STEM CELL; MICROARRAY ANALYSIS; MOUSE; MUTATION; NONHUMAN; PRIORITY JOURNAL; SEQUENCE ANALYSIS; STEM CELL; TRANSGENIC MOUSE; VITELLINE MEMBRANE; YOLK SAC;

ANIMALS; BASE SEQUENCE; CHROMATIN IMMUNOPRECIPITATION; CONSERVED SEQUENCE; DNA; DNA-BINDING PROTEINS; EMBRYONIC DEVELOPMENT; ENHANCER ELEMENTS, GENETIC; ERYTHROPOIESIS; GENE REGULATORY NETWORKS; HEMATOPOIESIS; HEMATOPOIETIC STEM CELLS; MICE; MICE, TRANSGENIC; MOLECULAR SEQUENCE DATA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROMOTER REGIONS, GENETIC; SEQUENCE HOMOLOGY, NUCLEIC ACID; TRANSCRIPTION FACTORS;

EID: 84863015813     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.05745-11     Document Type: Article

References (59)

1. Alcalay M, et al. 2003. Acute myeloid leukemia fusion proteins deregulate genes involved in stem cell maintenance and DNA repair. J. Clin. Invest. 112:1751-1761.
2. Athanasiou M, Mavrothalassitis G, Sun-Hoffman L, Blair DG. 2000. FLI-1 is a suppressor of erythroid differentiation in human hematopoietic cells. Leukemia 14:439-445.
3. Bartel FO, Higuchi T, Spyropoulos DD. 2000. Mouse models in the study of the Ets family of transcription factors. Oncogene 19:6443-6454.
4. Bee T, et al. 2009. The mouse Runx1 +23 hematopoietic stem cell enhancer confers hematopoietic specificity to both Runx1 promoters. Blood 113:5121-5124.
5. Blow MJ, et al. 2010. ChIP-Seq identification of weakly conserved heart enhancers. Nat. Genet. 42:806-810.
6. Calero-Nieto FJ, et al. 2010. Transcriptional regulation of Elf-1: locuswide analysis reveals four distinct promoters, a tissue-specific enhancer, control by PU.1 and the importance of Elf-1 downregulation for erythroid maturation. Nucleic Acids Res. 38:6363-6374.
7. Chapman MA, et al. 2004. Analysis of multiple genomic sequence align-ments: a web resource, online tools, and lessons learned from analysis of mammalian SCL loci. Genome Res. 14:313-318.
8. De Val S, et al. 2008. Combinatorial regulation of endothelial gene expression by Ets and Forkhead transcription factors. Cell 135:1053-1064.
9. Ernst J, et al. 2011. Mapping and analysis of chromatin state dynamics in nine human cell types. Nature 473:43-49.
10. Fukushima T, et al. 2003. The level of MEF but not ELF-1 correlates with FAB subtype of acute myeloid leukemia and is low in good prognosis cases. Leuk. Res. 27:387-392.
11. Garcon L, et al. 2005. Gfi-1B plays a critical role in terminal differentiation of normal and transformed erythroid progenitor cells. Blood 105: 1448-1455.
12. Gottgens B, et al. 1997. Transcription of the SCL gene in erythroid and CD34 positive primitive myeloid cells is controlled by a complex network of lineage-restricted chromatin-dependent and chromatin-independent regulatory elements. Oncogene 15:2419-2428.
13. Gottgens B, et al. 2002. Establishing the transcriptional programme for blood: the SCL stem cell enhancer is regulated by a multiprotein complex containing Ets and GATA factors. EMBO J. 21:3039-3050.
14. Hedvat CV, Yao J, Sokolic RA, Nimer SD. 2004. Myeloid ELF1-like factor is a potent activator of interleukin-8 expression in hematopoietic cells. J. Biol. Chem. 279:6395-6400.
15. Heintzman ND, et al. 2009. Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 459:108-112.
16. Heinz S, et al. 2010. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell 38:576-589.
17. Hubbard TJ, et al. 2009. ENSEMBL 2009. Nucleic Acids Res. 37:D690-D697.
18. Kai H, et al. 1999. Myeloid ELF-1-like factor up-regulates lysozyme transcription in epithelial cells. J. Biol. Chem. 274:20098-20102.
19. Kent WJ, et al. 2002. The human genome browser at UCSC. Genome Res. 12:996-1006.
20. Kim HG, et al. 2004. The ETS family transcription factor PU.1 is necessary for the maintenance of fetal liver hematopoietic stem cells. Blood 104:3894-3900.
21. Koga T, et al. 2005. Sp1-dependent regulation of myeloid Elf-1 like factor in human epithelial cells. FEBS Lett. 579:2811-2816.
22. Kruse EA, et al. 2009. Dual requirement for the ETS transcription factors Fli-1 and Erg in hematopoietic stem cells and the megakaryocyte lineage. Proc. Natl. Acad. Sci. U. S. A. 106:13814-13819.
23. Kuo YY, Chang ZF. 2007. GATA-1 and Gfi-1B interplay to regulate Bcl-xL transcription. Mol. Cell. Biol. 27:4261-4272.
24. Lacorazza HD, et al. 2002. The ETS protein MEF plays a critical role in perforin gene expression and the development of natural killer and NK-T cells. Immunity 17:437-449.
25. Lacorazza HD, et al. 2006. The transcription factor MEF/ELF4 regulates the quiescence of primitive hematopoietic cells. Cancer Cell 9:175-187.
26. Landry JR, et al. 2009. Expression of the leukemia oncogene Lmo2 is controlled by an array of tissue-specific elements dispersed over 100 kb and bound by Tal1/Lmo2, Ets, and Gata factors. Blood 113:5783-5792.
27. Landry JR, et al. 2005. Fli1, Elf1, and Ets1 regulate the proximal promoter of the LMO2 gene in endothelial cells. Blood 106:2680-2687.
28. 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.
29. Loughran SJ, et al. 2008. The transcription factor Erg is essential for definitive hematopoiesis and the function of adult hematopoietic stem cells. Nat. Immunol. 9:810-819.
30. Lund AH, et al. 2002. Genome-wide retroviral insertional tagging of genes involved in cancer in Cdkn2a-deficient mice. Nat. Genet. 32:160-165.
31. Maroulakou IG, Bowe DB. 2000. Expression and function of Ets transcription factors in mammalian development: a regulatory network. Oncogene 19:6432-6442.
32. McDevitt MA, Fujiwara Y, Shivdasani RA, Orkin SH. 1997. An upstream, DNase I hypersensitive region of the hematopoietic-expressed transcription factor GATA-1 gene confers developmental specificity in transgenic mice. Proc. Natl. Acad. Sci. U. S. A. 94:7976-7981.
33. Melet F, Motro B, Rossi DJ, Zhang L, Bernstein A. 1996. Generation of a novel Fli-1 protein by gene targeting leads to a defect in thymus development and a delay in Friend virus-induced erythroleukemia. Mol. Cell. Biol. 16:2708-2718.
34. Mikkers H, et al. 2002. High-throughput retroviral tagging to identify components of specific signaling pathways in cancer. Nat. Genet. 32:153-159.
35. Miyazaki Y, et al. 2001. Cyclin A-dependent phosphorylation of the ETS-related protein, MEF, restricts its activity to the G1 phase of the cell cycle. J. Biol. Chem. 276:40528-40536.
36. Miyazaki Y, Sun X, Uchida H, Zhang J, Nimer S. 1996. MEF, a novel transcription factor with an Elf-1 like DNA binding domain but distinct transcriptional activating properties. Oncogene 13:1721-1729.
37. Moore SD, et al. 2006. ELF4 is fused to ERG in a case of acute myeloid leukemia with a t(X;21)(q25-26;q22). Leuk. Res. 30:1037-1042.
38. Ng CE, et al. 2010. A Runx1 intronic enhancer marks hemogenic endothelial cells and hematopoietic stem cells. Stem Cells 28:1869-1881.
39. North T, et al. 1999. Cbfa2 is required for the formation of intra-aortic hematopoietic clusters. Development 126:2563-2575.
40. Nottingham WT, et al. 2007. Runx1-mediated hematopoietic stem-cell emergence is controlled by a Gata/Ets/SCL-regulated enhancer. Blood 110:4188-4197.
41. Osawa M, et al. 2002. Erythroid expansion mediated by the Gfi-1B zinc finger protein: role in normal hematopoiesis. Blood 100:2769-2777.
42. Pekowska A, et al. 2011. H3K4 tri-methylation provides an epigenetic signature of active enhancers. EMBO J. 30:4198-4210.
43. Pimanda JE, et al. 2006. Endoglin expression in the endothelium is regulated by Fli-1, Erg, and Elf-1 acting on the promoter and a -8-kb enhancer. Blood 107:4737-4745.
44. Pimanda JE, et al. 2008. Endoglin expression in blood and endothelium is differentially regulated by modular assembly of the Ets/Gata hemangioblast code. Blood 112:4512-4522.
45. Pinto do O P, Kolterud A, Carlsson L. 1998. Expression of the LIMhomeobox gene LH2 generates immortalized steel factor-dependent multipotent hematopoietic precursors. EMBO J. 17:5744-5756.
46. Pruitt KD, Tatusova T, Maglott DR. 2007. NCBI reference sequences (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Res. 35:D61-D65.
47. Rao G, Rekhtman N, Cheng G, Krasikov T, Skoultchi AI. 1997. Deregulated expression of the PU.1 transcription factor blocks murine erythroleukemia cell terminal differentiation. Oncogene 14:123-131.
48. Rosenbloom KR, et al. 2010. ENCODE whole-genome data in the UCSC Genome Browser. Nucleic Acids Res. 38:D620-D625.
49. Saleque S, Cameron S, Orkin SH. 2002. The zinc-finger proto-oncogene Gfi-1b is essential for development of the erythroid and megakaryocytic lineages. Genes Dev. 16:301-306.
50. Sanchez M, et al. 1999. An SCL 3′ enhancer targets developing endothelium together with embryonic and adult haematopoietic progenitors. Development 126:3891-3904.
51. Seki Y, et al. 2002. The ETS transcription factor MEF is a candidate tumor suppressor gene on the X chromosome. Cancer Res. 62:6579-6586.
52. Sinclair AM, et al. 1999. Distinct 5′ SCL enhancers direct transcription to developing brain, spinal cord, and endothelium: neural expression is mediated by GATA factor binding sites. Dev. Biol. 209:128-142.
53. Spyropoulos DD, et al. 2000. Hemorrhage, impaired hematopoiesis, and lethality in mouse embryos carrying a targeted disruption of the Fli1 transcription factor. Mol. Cell. Biol. 20:5643-5652.
54. Vassen L, Okayama T, Moroy T. 2007. Gfi1b:green fluorescent protein knock-in mice reveal a dynamic expression pattern of Gfi1b during hematopoiesis that is largely complementary to Gfi1. Blood 109:2356-2364.
55. Wilson NK, et al. 2010. Combinatorial transcriptional control in blood stem/progenitor cells: genome-wide analysis of ten major transcriptional regulators. Cell Stem Cell 7:532-544.
56. Wilson NK, et al. 2010. Gfi1 expression is controlled by five distinct regulatory regions spread over 100 kilobases, with Scl/Tal1, Gata2, PU.1, Erg, Meis1, and Runx1 acting as upstream regulators in early hematopoietic cells. Mol. Cell. Biol. 30:3853-3863.
57. Wood AD, et al. 2009. ID1 promotes expansion and survival of primary erythroid cells and is a target of JAK2V617F-STAT5 signaling. Blood 114: 1820-1830.
58. Yamada T, Park CS, Mamonkin M, Lacorazza HD. 2009. Transcription factor ELF4 controls the proliferation and homing of CD8_T cells via the Kruppel-like factors KLF4 and KLF2. Nat. Immunol. 10:618-626.
59. 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.