Deletion of the Scl +19 enhancer increases the blood stem cell compartment without affecting the formation of mature blood lineages

Experimental Hematology

Volumn 40, Issue 7, 2012, Pages

  Spensberger, Dominik ^a   Kotsopoulou, Ekaterini ^a   Ferreira, Rita ^a   Broccardo, Cyril ^a   Scott, Linda M ^a   Fourouclas, Nasios ^a   Ottersbach, Katrin ^a   Green, Anthony R ^a   Göttgens, Berthold ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE; MESSENGER RNA; TRANSCRIPTION FACTOR TAL1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE MARROW TRANSPLANTATION; CELL COUNT; CELL EXPANSION; CELL LINEAGE; CELL MATURATION; CELL SPECIFICITY; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; ENHANCER REGION; ERYTHROID PRECURSOR CELL; FETUS; FLOW CYTOMETRY; GENE; GENE DELETION; GENE LOCUS; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; LIVER CELL; MEGAKARYOCYTE; MOUSE; NONHUMAN; PHENOTYPE; POPULATION DYNAMICS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING; REGULATORY SEQUENCE; STEADY STATE; STEM CELL LEUKEMIA +19 ENHANCER GENE;

MUS;

EID: 84862573251     PISSN: 0301472X     EISSN: 18732399     Source Type: Journal    
DOI: 10.1016/j.exphem.2012.02.006     Document Type: Article

References (38)

1. Bloor A.J., Sanchez M.J., Green A.R., Gottgens B. The role of the stem cell leukemia (SCL) gene in hematopoietic and endothelial lineage specification. J Hematother Stem Cell Res 2002, 11:195-206.
2. Begley C.G., Aplan P.D., Davey M.P., et al. Chromosomal translocation in a human leukemic stem-cell line disrupts the T-cell antigen receptor delta-chain diversity region and results in a previously unreported fusion transcript. Proc Natl Acad Sci U S A 1989, 86:2031-2035.
3. Begley C.G., Green A.R. The SCL gene: from case report to critical hematopoietic regulator. Blood 1999, 93:2760-2770.
4. Elefanty A.G., Begley C.G., Metcalf D., Barnett L., Kontgen F., Robb L. Characterization of hematopoietic progenitor cells that express the transcription factor SCL, using a lacZ "knock-in" strategy. Proc Natl Acad Sci U S A 1998, 95:11897-11902.
5. Elefanty A.G., Begley C.G., Hartley L., Papaevangeliou B., Robb L. SCL expression in the mouse embryo detected with a targeted lacZ reporter gene demonstrates its localization to hematopoietic, vascular, and neural tissues. Blood 1999, 94:3754-3763.
6. Robb L., Elwood N.J., Elefanty A.G., et al. The scl gene product is required for the generation of all hematopoietic lineages in the adult mouse. EMBO J 1996, 15:4123-4129.
7. 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.
8. Robb L., Lyons I., Li R., et al. Absence of yolk sac hematopoiesis from mice with a targeted disruption of the scl gene. Proc Natl Acad Sci U S A 1995, 92:7075-7079.
9. Shivdasani R.A., Mayer E.L., Orkin S.H. Absence of blood formation in mice lacking the T-cell leukaemia oncoprotein tal-1/SCL. Nature 1995, 373:432-434.
10. Hall M.A., Curtis D.J., Metcalf D., et al. The critical regulator of embryonic hematopoiesis, SCL, is vital in the adult for megakaryopoiesis, erythropoiesis, and lineage choice in CFU-S12. Proc Natl Acad Sci U S A 2003, 100:992-997.
11. Mikkola H.K., Klintman J., Yang H., et al. Haematopoietic stem cells retain long-term repopulating activity and multipotency in the absence of stem-cell leukaemia SCL/tal-1 gene. Nature 2003, 421:547-551.
12. Curtis D.J., Hall M.A., Van Stekelenburg L.J., Robb L., Jane S.M., Begley C.G. SCL is required for normal function of short-term repopulating hematopoietic stem cells. Blood 2004, 103:3342-3348.
13. Brunet de la Grange P., Armstrong F., Duval V., et al. Low SCL/TAL1 expression reveals its major role in adult hematopoietic myeloid progenitors and stem cells. Blood 2006, 108:2998-3004.
14. Delabesse E., Ogilvy S., Chapman M.A., Piltz S.G., Gottgens B., Green A.R. Transcriptional regulation of the SCL locus: identification of an enhancer that targets the primitive erythroid lineage in vivo. Mol Cell Biol 2005, 25:5215-5225.
15. Gottgens B., Barton L.M., Gilbert J.G., et al. Analysis of vertebrate SCL loci identifies conserved enhancers. Nat Biotechnol 2000, 18:181-186.
16. Gottgens B., Broccardo C., Sanchez M.J., et al. The scl +18/19 stem cell enhancer is not required for hematopoiesis: identification of a 5' bifunctional hematopoietic-endothelial enhancer bound by Fli-1 and Elf-1. Mol Cell Biol 2004, 24:1870-1883.
17. Sanchez M., Gottgens B., Sinclair A.M., et al. An SCL 3' enhancer targets developing endothelium together with embryonic and adult haematopoietic progenitors. Development 1999, 126:3891-3904.
18. Sinclair A.M., Gottgens B., Barton L.M., et al. Distinct 5' SCL enhancers direct transcription to developing brain, spinal cord, and endothelium: neural expression is mediated by GATA factor binding sites. Dev Biol 1999, 209:128-142.
19. Sanchez M.J., Bockamp E.O., Miller J., Gambardella L., Green A.R. Selective rescue of early haematopoietic progenitors in Scl(-/-) mice by expressing Scl under the control of a stem cell enhancer. Development 2001, 128:4815-4827.
20. Gottgens B., Ferreira R., Sanchez M.J., et al. cis-Regulatory remodeling of the SCL locus during vertebrate evolution. Mol Cell Biol 2010, 30:5741-5751.
21. Salmon J.M., Slater N.J., Hall M.A., et al. Aberrant mast-cell differentiation in mice lacking the stem-cell leukemia gene. Blood 2007, 110:3573-3581.
22. Yang L., Bryder D., Adolfsson J., et al. Identification of Lin(-)Sca1(+)kit(+)CD34(+)Flt3- short-term hematopoietic stem cells capable of rapidly reconstituting and rescuing myeloablated transplant recipients. Blood 2005, 105:2717-2723.
23. Ogilvy S., Ferreira R., Piltz S.G., Bowen J.M., Gottgens B., Green A.R. The SCL +40 enhancer targets the midbrain together with primitive and definitive hematopoiesis and is regulated by SCL and GATA proteins. Mol Cell Biol 2007, 27:7206-7219.
24. Gottgens B., Nastos A., Kinston S., et al. Establishing the transcriptional programme for blood: the SCL stem cell enhancer is regulated by a multiprotein complex containing Ets and GATA factors. EMBO J 2002, 21:3039-3050.
25. Silberstein L., Sanchez M.J., Socolovsky M., et al. Transgenic analysis of the stem cell leukemia +19 stem cell enhancer in adult and embryonic hematopoietic and endothelial cells. Stem Cells 2005, 23:1378-1388.
26. Bender M.A., Byron R., Ragoczy T., Telling A., Bulger M., Groudine M. Flanking HS-62.5 and 3' HS1, and regions upstream of the LCR, are not required for beta-globin transcription. Blood 2006, 108:1395-1401.
27. 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.
28. 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.
29. Anguita E., Sharpe J.A., Sloane-Stanley J.A., Tufarelli C., Higgs D.R., Wood W.G. Deletion of the mouse alpha-globin regulatory element (HS -26) has an unexpectedly mild phenotype. Blood 2002, 100:3450-3456.
30. Ahituv N., Zhu Y., Visel A., et al. Deletion of ultraconserved elements yields viable mice. PLoS Biol 2007, 5:e234.
31. Snow J.W., Trowbridge J.J., Johnson K.D., et al. Context-dependent function of "GATA switch" sites in vivo. Blood 2011, 117:4769-4772.
32. 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.
33. 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.
34. Murrell A.M., Bockamp E.O., Gottgens B., et al. Discordant regulation of SCL/TAL-1 mRNA and protein during erythroid differentiation. Oncogene 1995, 11:131-139.
35. Bockamp E.O., McLaughlin F., Murrell A.M., et al. Lineage-restricted regulation of the murine SCL/TAL-1 promoter. Blood 1995, 86:1502-1514.
36. Begley C.G. The SCL transcription factor and differential regulation of macrophage differentiation by LIF, OSM and IL-6. Stem Cells 1994, 12(suppl 1):143-149. discussion 149-151.
37. Calkhoven C.F., Muller C., Martin R., et al. Translational control of SCL-isoform expression in hematopoietic lineage choice. Genes Dev 2003, 17:959-964.
38. Tang T., Arbiser J.L., Brandt S.J. Phosphorylation by mitogen-activated protein kinase mediates the hypoxia-induced turnover of the TAL1/SCL transcription factor in endothelial cells. J Biol Chem 2002, 277:18365-18372.