GFI1 and GFI1B control the loss of endothelial identity of hemogenic endothelium during hematopoietic commitment

Blood

Volumn 120, Issue 2, 2012, Pages 314-322

  Lancrin, Christophe ^a,b   Mazan, Milena ^a   Stefanska, Monika ^a   Patel, Rahima ^a   Lichtinger, Monika ^c   Costa, Guilherme ^a   Vargel, Özge ^b   Wilson, Nicola K ^d   Möröy, Tarik ^e   Bonifer, Constanze ^c   Göttgens, Berthold ^d   Kouskoff, Valerie ^a   Lacaud, Georges ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY EMBL   (Italy)

^c UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^e CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GFI1; TRANSCRIPTION FACTOR GFI1B; TRANSCRIPTION FACTOR RUNX1; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL STRUCTURE; CONTROLLED STUDY; DOWN REGULATION; EMBRYONAL TISSUE; FLOW CYTOMETRY; GENE EXPRESSION; HEMANGIOBLAST; HEMATOPOIESIS; MOUSE; NONHUMAN; PERIPHERAL BLOOD STEM CELL; PRIORITY JOURNAL; YOLK SAC;

EID: 84864073523     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2011-10-386094     Document Type: Article

References (50)

1. Medvinsky A, Rybtsov S, Taoudi S. Embryonic origin of the adult hematopoietic system: advances and questions. Development. 2011; 138(6):1017-1031.
2. Boisset JC, van Cappellen W, Andrieu-Soler C, Galjart N, Dzierzak E, Robin C. In vivo imaging of haematopoietic cells emerging from the mouse aortic endothelium. Nature. 2010;464(7285):116-120.
3. Chen MJ, Yokomizo T, Zeigler BM, Dzierzak E, Speck NA. Runx1 is required for the endothelial to haematopoietic cell transition but not thereafter. Nature. 2009;457(7231):887-891.
4. Zovein AC, Hofmann JJ, Lynch M, et al. Fate tracing reveals the endothelial origin of hematopoietic stem cells. Cell Stem Cell. 2008;3(6): 625-636.
5. Bertrand JY, Chi NC, Santoso B, Teng S, Stainier DY, Traver D. Haematopoietic stem cells derive directly from aortic endothelium during development. Nature. 2010;464(7285):108-111.
6. Kissa K, Herbomel P. Blood stem cells emerge from aortic endothelium by a novel type of cell transition. Nature. 2010;464(7285):112-115.
7. Choi K, Kennedy M, Kazarov A, Papadimitriou JC, Keller G. A common precursor for hematopoietic and endothelial cells. Development. 1998;125(4):725-732. (Pubitemid 28108096)
8. Huber TL, Kouskoff V, Fehling HJ, Palis J, Keller G. Haemangioblast commitment is initiated in the primitive streak of the mouse embryo. Nature. 2004;432(7017):625-630. (Pubitemid 39626269)
9. Lancrin C, Sroczynska P, Stephenson C, Allen T, Kouskoff V, Lacaud G. The haemangioblast generates haematopoietic cells through a haemogenic endothelium stage. Nature. 2009; 457(7231):892-895.
10. Eilken HM, Nishikawa S, Schroeder T. Continuous single-cell imaging of blood generation from haemogenic endothelium. Nature. 2009; 457(7231):896-900.
11. Tong B, Grimes HL, Yang TY, et al. The Gfi-1B proto-oncoprotein represses p21WAF1 and inhibits myeloid cell differentiation. Mol Cell Biol. 1998; 18(5):2462-2473. (Pubitemid 28183416)
12. Zweidler-Mckay PA, Grimes HL, Flubacher MM, Tsichlis PN. Gfi-1 encodes a nuclear zinc finger protein that binds DNA and functions as a transcriptional repressor. Mol Cell Biol. 1996;16(8): 4024-4034. (Pubitemid 26251201)
13. Grimes HL, Chan TO, Zweidler-McKay PA, Tong B, Tsichlis PN. The Gfi-1 proto-oncoprotein contains a novel transcriptional repressor domain, SNAG, and inhibits G1 arrest induced by interleukin-2 withdrawal. Mol Cell Biol. 1996; 16(11):6263-6272. (Pubitemid 26360986)
14. Khandanpour C, Sharif-Askari E, Vassen L, et al. Evidence that Growth factor independence 1b regulates dormancy and peripheral blood mobilization of hematopoietic stem cells. Blood. 2010; 116(24):5149-5161.
15. van der Meer LT, Jansen JH, van der Reijden BA. Gfi1 and Gfi1b: key regulators of hematopoiesis. Leukemia. 2010;24(11):1834-1843.
16. Yucel R, Kosan C, Heyd F, Moroy T. Gfi1:green fluorescent protein knock-in mutant reveals differential expression and autoregulation of the growth factor independence 1 (Gfi1) gene during lymphocyte development. J Biol Chem. 2004; 279(39):40906-40917. (Pubitemid 39287690)
17. Karsunky H, Zeng H, Schmidt T, et al. Inflammatory reactions and severe neutropenia in mice lacking the transcriptional repressor Gfi1. Nat Genet. 2002;30(3):295-300.
18. Hock H, Hamblen MJ, Rooke HM, et al. Gfi-1 restricts proliferation and preserves functional integrity of haematopoietic stem cells. Nature. 2004;431(7011):1002-1007. (Pubitemid 39434423)
19. Zeng H, Yucel R, Kosan C, Klein-Hitpass L, Moroy T. Transcription factor Gfi1 regulates self-renewal and engraftment of hematopoietic stem cells. EMBO J. 2004;23(20):4116-4125. (Pubitemid 39472432)
20. Vassen L, Okayama T, Moroy T. Gfi1b:green fluorescent protein knock-in mice reveal a dynamic expression pattern of Gfi1b during hematopoiesis that is largely complementary to Gfi1. Blood. 2007;109(6):2356-2364. (Pubitemid 46425875)
21. Saleque S, Cameron S, Orkin SH. The zinc-finger proto-oncogene Gfi-1b is essential for development of the erythroid and megakaryocytic lineages. Genes Dev. 2002;16(3):301-306. (Pubitemid 34111410)
22. Anguita E, Villegas A, Iborra F, Hernandez A. GFI1B controls its own expression binding to multiple sites. Haematologica. 2010;95(1):36-46.
23. Doan LL, Porter SD, Duan Z, et al. Targeted transcriptional repression of Gfi1 by GFI1 and GFI1B in lymphoid cells. Nucleic Acids Res. 2004;32(8): 2508-2519. (Pubitemid 38854803)
24. Vassen L, Fiolka K, Mahlmann S, Moroy T. Direct transcriptional repression of the genes encoding the zinc-finger proteins Gfi1b and Gfi1 by Gfi1b. Nucleic Acids Res. 2005;33(3):987-998. (Pubitemid 41430519)
25. Wang Q, Stacy T, Binder M, Marin-Padilla M, Sharpe AH, Speck NA. Disruption of the Cbfa2 gene causes necrosis and hemorrhaging in the central nervous system and blocks definitive hematopoiesis. Proc Natl Acad Sci U S A. 1996; 93(8):3444-3449. (Pubitemid 26125639)
26. Sroczynska P, Lancrin C, Pearson S, Kouskoff V, Lacaud G. In vitro differentiation of mouse embryonic stem cells as a model of early hematopoietic development. Methods Mol Biol. 2009;538:317-334.
27. Lacaud G, Gore L, Kennedy M, et al. Runx1 is essential for hematopoietic commitment at the hemangioblast stage of development in vitro. Blood. 2002;100(2):458-466. (Pubitemid 34761107)
28. Lefevre P, Melnik S, Wilson N, Riggs AD, Bonifer C. Developmentally regulated recruitment of transcription factors and chromatin modification activities to chicken lysozyme cis-regulatory elements in vivo. Mol Cell Biol. 2003;23(12): 4386-4400. (Pubitemid 36666438)
29. Pearson S, Lancrin C, Lacaud G, Kouskoff V. The sequential expression of CD40 and Icam2 defines progressive steps in the formation of blood precursors from the mesoderm germ layer. Stem Cells. 2010;28(6):1089-1098.
30. Soneoka Y, Cannon PM, Ramsdale EE, et al. A transient three-plasmid expression system for the production of high titer retroviral vectors. Nucleic Acids Res. 1995;23(4):628-633.
31. Yokomizo T, Yamada-Inagawa T, Yzaguirre AD, Chen MJ, Speck NA, Dzierzak E. Whole-mount three-dimensional imaging of internally localized immunostained cells within mouse embryos. Nat Protoc. 2012;7(3):421-431.
32. Ferreras C, Lancrin C, Lie-A-Ling M, Kouskoff V, Lacaud G. Identification and characterization of a novel transcriptional target of RUNX1/AML1 at the onset of hematopoietic development. Blood. 2011;118(3):594-597.
33. Wilson NK, Foster SD, 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(4): 532-544.
34. Wilson NK, Timms RT, Kinston SJ, et al. 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. 2010;30(15):3853-3863.
35. Telfer JC, Rothenberg EV. Expression and function of a stem cell promoter for the murine CBFalpha2 gene: distinct roles and regulation in natural killer and T cell development. Dev Biol. 2001; 229(2):363-382. (Pubitemid 32108698)
36. Hoogenkamp M, Lichtinger M, Krysinska H, et al. Early chromatin unfolding by RUNX1: a molecular explanation for differential requirements during specification versus maintenance of the hematopoietic gene expression program. Blood. 2009; 114(2):299-309.
37. Bristow CA, Shore P. Transcriptional regulation of the human MIP-1alpha promoter by RUNX1 and MOZ. Nucleic Acids Res. 2003;31(11):2735-2744. (Pubitemid 37448487)
38. Mucenski ML, McLain K, Kier AB, et al. A functional c-myb gene is required for normal murine fetal hepatic hematopoiesis. Cell. 1991;65(4): 677-689.
39. Sroczynska P, Lancrin C, Kouskoff V, Lacaud G. The differential activities of Runx1 promoters define milestones during embryonic hematopoiesis. Blood. 2009;114(26):5279-5289.
40. Okuda T, van Deursen J, Hiebert SW, Grosveld G, Downing JR. AML1, the target of multiple chromosomal translocations in human leukemia, is essential for normal fetal liver hematopoiesis. Cell. 1996;84(2):321-330. (Pubitemid 26042836)
41. Fiolka K, Hertzano R, Vassen L, et al. Gfi1 and Gfi1b act equivalently in haematopoiesis, but have distinct, non-overlapping functions in inner ear development. EMBO Rep. 2006;7(3):326-333.
42. Ji RP, Phoon CK, Aristizabal O, McGrath KE, Palis J, Turnbull DH. Onset of cardiac function during early mouse embryogenesis coincides with entry of primitive erythroblasts into the embryo proper. Circ Res. 2003;92(2):133-135. (Pubitemid 36254268)
43. McGrath KE, Koniski AD, Malik J, Palis J. Circulation is established in a stepwise pattern in the mammalian embryo. Blood. 2003;101(5):1669-1676. (Pubitemid 36237556)
44. Ma X, Robin C, Ottersbach K, Dzierzak E. The Ly-6A (Sca-1) GFP transgene is expressed in all adult mouse hematopoietic stem cells. Stem Cells. 2002;20(6):514-521. (Pubitemid 35463064)
45. Duan Z, Zarebski A, Montoya-Durango D, Grimes HL, Horwitz M. Gfi1 coordinates epigenetic repression of p21Cip/WAF1 by recruitment of histone lysine methyltransferase G9a and histone deacetylase 1. Mol Cell Biol. 2005;25(23): 10338-10351. (Pubitemid 41681959)
46. Montoya-Durango DE, Velu CS, Kazanjian A, et al. Ajuba functions as a histone deacetylase-dependent co-repressor for autoregulation of the growth factor-independent-1 transcription factor. J Biol Chem. 2008;283(46):32056- 32065.
47. Saleque S, Kim J, Rooke HM, Orkin SH. Epigenetic regulation of hematopoietic differentiation by Gfi-1 and Gfi-1b is mediated by the cofactors CoREST and LSD1. Mol Cell. 2007;27(4):562-572. (Pubitemid 47238633)
48. Lux CT, Yoshimoto M, McGrath K, Conway SJ, Palis J, Yoder MC. All primitive and definitive hematopoietic progenitor cells emerging before E10 in the mouse embryo are products of the yolk sac. Blood. 2008;111(7):3435-3438.
49. Ghiaur G, Ferkowicz MJ, Milsom MD, et al. Rac1 is essential for intraembryonic hematopoiesis and for the initial seeding of fetal liver with definitive hematopoietic progenitor cells. Blood. 2008; 111(7):3313-3321.
50. Koushik SV, Wang J, Rogers R, et al. Targeted inactivation of the sodium-calcium exchanger (Ncx1) results in the lack of a heartbeat and abnormal myofibrillar organization. FASEB J. 2001; 15(7):1209-1211.