The +37 kb Cebpa enhancer is critical for Cebpa myeloid gene expression and contains functional sites that bind SCL, GATA2, C/EBPα, PU.1, and additional Ets factors

PLoS ONE

Volumn 10, Issue 5, 2015, Pages

  Cooper, Stacy ^a   Guo, Hong ^a   Friedman, Alan D ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CCAAT ENHANCER BINDING PROTEIN ALPHA; CRISPR ASSOCIATED PROTEIN; GRANULOCYTE COLONY STIMULATING FACTOR; INTERLEUKIN 3; PROTEIN C MYB; PROTEIN MYB; TRANSCRIPTION FACTOR ERG; TRANSCRIPTION FACTOR ETS; TRANSCRIPTION FACTOR ETS 1; TRANSCRIPTION FACTOR FLI 1; TRANSCRIPTION FACTOR GATA; TRANSCRIPTION FACTOR GATA 2; TRANSCRIPTION FACTOR PU 1; TRANSCRIPTION FACTOR RUNX1; TRANSCRIPTION FACTOR TAL1; CCAAT ENHANCER BINDING PROTEIN; CEBPA PROTEIN, MOUSE; ONCOPROTEIN; PROTEIN BINDING; PROTO-ONCOGENE PROTEIN SPI-1; RUNX1 PROTEIN, HUMAN; TRANSACTIVATOR PROTEIN;

32DCL3 CELL LINE; ALLELE; AMINO ACID SEQUENCE; ARTICLE; BINDING AFFINITY; BINDING SITE; BONE MARROW CELL; CEBPA GENE; CELL LINE; CELL TRANSFORMATION; CONTROLLED STUDY; E BOX ELEMENT; ENHANCER REGION; GEL SHIFT ASSAY; GENE ACTIVITY; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE LOCUS; HEMATOPOIESIS; HISTONE MODIFICATION; HUMAN; INVESTIGATIVE PROCEDURES; NONHUMAN; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN INTERACTION; SIGNAL TRANSDUCTION; WILD TYPE; ANIMAL; GENETICS; METABOLISM; MOUSE; POINT MUTATION; REGULATORY SEQUENCE;

MURINAE; MUS MUSCULUS;

ANIMALS; CCAAT-ENHANCER-BINDING PROTEIN-ALPHA; CCAAT-ENHANCER-BINDING PROTEINS; CELL LINE; CORE BINDING FACTOR ALPHA 2 SUBUNIT; ENHANCER ELEMENTS, GENETIC; GATA2 TRANSCRIPTION FACTOR; HUMANS; MICE; POINT MUTATION; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-ETS; REGULATORY SEQUENCES, NUCLEIC ACID; TRANS-ACTIVATORS;

EID: 84929095239     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0126385     Document Type: Article

References (30)

1. Scott LM, Civin CI, Rorth P, Friedman AD. A novel temporal expression pattern of three C/EBP family members in differentiating myelomonocytic cells. Blood 1992; 80: 1725-1735. PMID: 1391942
2. Iwasaki H, Mizuno S, Arinobu Y, Ozawa H, Mori Y, Shigematsu H, et al. The order of expression of transcription factors directs hierarchical specification of hematopoietic lineages. Genes Dev. 2006; 20: 3010-3021. PMID: 17079688
3. Ye M, Zhang H, Amabile G, Yang H, Staber PB, Zhang P, et al. C/EBPα controls acquisition and maintenance of adult haematopoietic stem cell quiescence. Nat Cell Biol. 2013; 15: 385-394. doi: 10.1038/ncb2698 PMID: 23502316
4. Hasemann MS, Lauridsen FK, Waage J, Jakobsen JS, Frank AK, Schuster MB, et al. C/EBPα is required for long-term self-renewal and lineage priming of hematopoietic stem cells and for the maintenance of epigenetic configurations in multipotent progenitors. PLoS Genet. 2014; 10: e1004079. doi: 10.1371/journal.pgen.1004079 PMID: 24415956
5. Zhang P, Iwasaki-Arai J, Iwasaki H, Fenyus ML, Dayaram T, Owens BM, et al. Enhancement of hematopoietic stem cell repopulating capacity and self-renewal in the absence of the transcription factor C/EBPα. Immunity 2004; 21: 853-863. PMID: 15589173
6. Ma O, Hong S, Guo H, Ghiaur G, Friedman AD. Granulopoiesis requires increased C/EBPα compared to monopoiesis, correlated with elevated Cebpa in immature G-CSF receptor versus M-CSF receptor expressing cells. PLoS One 2014; 9: e95784. doi: 10.1371/journal.pone.0095784 PMID: 24752325
7. Pabst T, Mueller BU, Zhang P, Radomska HS, Narravula S, Schnittger S, et al. Dominant-negative mutations of CEBPA, encoding CCAAT/enhancer binding protein-α (C/EBPα), in acute myeloid leukemia. Nat Genet. 2001; 27: 263-270. PMID: 11242107
8. Pabst T, Mueller BU, Harakawa N, Schoch C, Haferlach T, Behre G, et al. (2001) AML1-ETO downregulates the granulocytic differentiation factor C/EBPα in t(8;21) myeloid leukemia. Nat Med. 2001; 7: 444-451. PMID: 11283671
9. Friedman AD. C/EBPα in normal and malignant myelopoiesis. Int J Hematol. 2015; 101: 330-341. doi: 10.1007/s12185-015-1764-6 PMID: 25753223
10. Christy RJ, Kaestner KH, Geiman DE, Lane MD. CCAAT/enhancer binding protein gene promoter: binding of nuclear factors during differentiation of 3T3-L1 preadipocytes. Proc Natl Acad Sci USA 1991; 88: 2593-2597. PMID: 2006196
11. Guo H, Ma O, Speck NA, Friedman AD. Runx1 deletion or dominant inhibition reduces Cebpa transcription via conserved promoter and distal enhancer sites to favor monopoiesis over granulopoiesis. Blood 2012; 119: 4408-4418. doi: 10.1182/blood-2011-12-397091 PMID: 22451420
12. Guo H, Ma O, Friedman AD. The Cebpa +37 kb enhancer directs transgene expression to myeloid progenitors and to long-term hematopoietic stem cells. J Leuk Biol. 2014; 96: 419-426. doi: 10.1189/jlb.2AB0314-145R PMID: 24868087
13. Wilson NK, Foster SD, Wang X, Knezevic K, Schütte J, Kaimakis P, 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. doi: 10.1016/j.stem.2010.07.016 PMID: 20887958
14. Collins C, Wang J, Miao H, Bronstein J, Nawer H, Xu T, et al. C/EBPα is an essential collaborator in Hoxa9/Meis1-mediated leukemogenesis. Proc Natl Acad Sci USA 2014; 111: 9899-9904. doi: 10.1073/pnas.1402238111 PMID: 24958854
15. Valtieri M, Tweardy DJ, Caracciolo D, Johnson K, Mavilio F, Altmann S, et al. Cytokine-dependent granulocytic differentiation. Regulation of proliferative and differentiative responses in a murine progenitor cell line. J Immunol. 1987; 138: 3829-3835. PMID: 2438328
16. Suzow JG, Friedman AD. The murine myeloperoxidase promoter contains multiple functional elements - one element binds a cell type-restricted transcription factor, myeloid nuclear factor 1(MyNF1). Mol Cell Biol. 1993; 13: 2141-2151. PMID: 8384306
17. Oelgeschläger M, Nuchprayoon I, Lüscher B, Friedman AD C/EBP, c-Myb, and PU.1 cooperate to regulate the neutrophil elastase promoter. Mol Cell Biol. 1996; 16: 4717-4725. PMID: 8756629
18. Montague TG, Cruz JM, Gagnon JA, Church GM, Valen E. CHOPCHOP: a CRISPR/Cas9 and TALEN web tool for genome editing. Nucl Acids Res. 2014; 42: W401-W407. doi: 10.1093/nar/gku410 PMID: 24861617
19. Sharan SK, Thomason LC, Kuznetsov SG, Court DL. Recombineering: a homologous recombination-based method of genetic engineering. Nat Prot. 2009; 4: 206-223.
20. Britos-Bray M, Friedman AD. Core binding factor cannot synergistically activate the myeloperoxidase proximal enhancer in immature myeloid cells without c-Myb. Mol Cell Biol. 1997; 17: 5127-5135. PMID: 9271390
21. Smith LT, Hohaus S, Gonzalez DA, Dziennis SE, Tenen DG. PU.1 (Spi-1) and C/EBPα regulate the granulocyte colony-stimulating factor receptor promoter in myeloid cells. Blood 1996; 88: 1234-1247. PMID: 8695841
22. Goetz TL, Gu TL, Speck NA, Graves BJ. Auto-inhibition of Ets-1 is counteracted by DNA binding cooperativity with core-binding factor α2. Mol Cell Biol. 2000; 20: 81-90. PMID: 10594011
23. Lara-Astiaso D, Weiner A, Lorenzo-Vivas E, Zaretsky I, Jaitin DA, David E, et al. Chromatin state dynamics during blood formation. Science 2014; 345: 943-949. doi: 10.1126/science.1256271 PMID: 25103404
24. Cancer Genome Atlas Research Network (2013) Genomic and epigenomic landscapes of adult de novo acute myeloid leukemia. New Engl J Med. 2013; 368: 2059-2074. doi: 10.1056/NEJMoa1301689 PMID: 23634996
25. Ptasinska A, Assi SA, Mannari D, James SR, Williamson D, Dunne J, et al. Depletion of RUNX1/ETO in t(8;21) AML cells leads to genome-wide changes in chromatin structure and transcription factor binding. Leukemia 2012; 26:1829-1841. doi: 10.1038/leu.2012.49 PMID: 22343733
26. Zhao L, Glazov EA, Pattabiraman DR, Al-Owaidi F, Zhang P, Brown MA, et al. Integrated genome-wide chromatin occupancy and expression analyses identify key myeloid pro-differentiation transcription factors repressed by Myb. Nucl Acids Res. 2011; 39: 4664-4679. doi: 10.1093/nar/gkr024 PMID: 21317192
27. Klemsz MJ, McKercher SR, Celada A, Van Beveren C, Maki RA. The macrophage and B cell-specific transcription factor PU.1 is related to the ets oncogene. Cell 1990; 61: 113-124. PMID: 2180582
28. Alberich-Jordà M, Wouters B, Balastik M, Shapiro-Koss C, Zhang H, Di Ruscio A, et al. (2012) C/EBPγ deregulation results in differentiation arrest in acute myeloid leukemia. J Clin.Invest. 2012; 122: 4490-4504. doi: 10.1172/JCI65102 PMID: 23160200
29. Helboe L, Egebjerg J, Møller M, Thomsen C. Distribution and pharmacology of alanine-serine-cysteine transporter 1 (asc-1) in rodent brain. Eur J Neurosci. 2003; 18: 2227-2238. PMID: 14622183
30. Andersson R, Gebhard C, Miguel-Escalada I, Hoof I, Bornholdt J, Boyd M, et al. An atlas of active enhancers across human cell types and tissues. Nature 2014; 507:455-461. doi: 10.1038/nature12787 PMID: 24670763