The Notch ligand DLL4 specifically marks human hematoendothelial progenitors and regulates their hematopoietic fate

Leukemia

Volumn 29, Issue 8, 2015, Pages 1741-1753

  Ayllon V ^a   Bueno, C ^b   Ramos Mejia V ^a   Navarro Montero, O ^a   Prieto, C ^b   Real, P J ^a   Romero, T ^a   Garcia Leon M J ^c   Toribio, M L ^d   Bigas, A ^e   Menendez, P ^b  

^a UNIVERSITY OF GRANADA   (Spain)

^b UNIVERSITY OF BARCELONA   (Spain)

^c UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^d HOSPITAL DEL MAR   (Spain)

^e INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CD45 ANTIGEN; NOTCH RECEPTOR; PROTEIN; PROTEIN DLL4; TRANSCRIPTOME; UNCLASSIFIED DRUG; BIOLOGICAL MARKER; MEMBRANE PROTEIN; MESSENGER RNA; SIGNAL PEPTIDE;

ARTICLE; CELL DIFFERENTIATION; CLONOGENESIS; CONFOCAL MICROSCOPY; CONTROLLED STUDY; EMBRYO; EMBRYOID BODY; EMBRYONIC STEM CELL; ENDOTHELIAL PROGENITOR CELL; GENE EXPRESSION; HEMANGIOBLAST; HEMATOENDOTHELIAL PROGENITOR; HEMATOPOIESIS; HEMATOPOIETIC CELL; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA ANALYSIS; ANIMAL; CELL CULTURE; CELL PROLIFERATION; CYTOLOGY; ENDOTHELIUM; ENZYME IMMUNOASSAY; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; GENETICS; METABOLISM; MOUSE; NONOBESE DIABETIC MOUSE; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCID MOUSE;

ANIMALS; BIOLOGICAL MARKERS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; EMBRYOID BODIES; EMBRYONIC STEM CELLS; ENDOTHELIUM; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; HEMATOPOIESIS; HEMATOPOIETIC STEM CELLS; HUMANS; IMMUNOENZYME TECHNIQUES; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; MICE; MICE, INBRED NOD; MICE, SCID; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

EID: 84938952954     PISSN: 08876924     EISSN: 14765551     Source Type: Journal    
DOI: 10.1038/leu.2015.74     Document Type: Article

References (54)

1. Costa G, Kouskoff V, Lacaud G. Origin of blood cells and HSC production in the embryo. Trends Immunol 2012; 33: 215-223.
2. Clapes T, Robin C. Embryonic development of hematopoietic stem cells: implications for clinical use. Regen Med 2012; 7: 349-368.
3. Islam MS, Ni Z, Kaufman DS. Use of human embryonic stem cells to understand hematopoiesis and hematopoietic stem cell niche. Curr Stem Cell Res Ther 2010; 5: 245-250.
4. Benedito R, Trindade A, Hirashima M, Henrique D, da Costa LL, Rossant J et al. Loss of Notch signalling induced by Dll4 causes arterial calibre reduction by increasing endothelial cell response to angiogenic stimuli. BMC Dev Biol 2008; 8: 117.
5. Corada M, Nyqvist D, Orsenigo F, Caprini A, Giampietro C, Taketo MM et al. The Wnt/beta-catenin pathway modulates vascular remodeling and specification by upregulating Dll4/Notch signaling. Dev Cell 2010; 18: 938-949.
6. Kim PG, Albacker CE, Lu YF, Jang IH, Lim Y, Heffner GC et al. Signaling axis involving Hedgehog, Notch, and Scl promotes the embryonic endothelial-to-hematopoietic transition. Proc Natl Acad Sci USA 2012; 110: E141-E150.
7. Yamamizu K, Matsunaga T, Uosaki H, Fukushima H, Katayama S, Hiraoka-Kanie M et al. Convergence of Notch and beta-catenin signaling induces arterial fate in vascular progenitors. J Cell Biol 2010; 189: 325-338.
8. 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: 116-120.
9. Tavian M, Peault B. Embryonic development of the human hematopoietic system. Int J Dev Biol 2005; 49: 243-250.
10. Ivanovs A, Rybtsov S, Anderson RA, Turner ML, Medvinsky A. Identification of the niche and phenotype of the first human hematopoietic stem cells. Stem Cell Rep 2014; 2: 449-456.
11. Kennedy M, D'Souza SL, Lynch-Kattman M, Schwantz S, Keller G. Development of the hemangioblast defines the onset of hematopoiesis in human ES cell differentiation cultures. Blood 2007; 109: 2679-2687.
12. Wang L, Li L, Shojaei F, Levac K, Cerdan C, Menendez P et al. Endothelial and hematopoietic cell fate of human embryonic stem cells originates from primitive endothelium with hemangioblastic properties. Immunity 2004; 21: 31-41.
13. Kumano K, Chiba S, Kunisato A, Sata M, Saito T, Nakagami-Yamaguchi E et al. Notch1 but not Notch2 is essential for generating hematopoietic stem cells from endothelial cells. Immunity 2003; 18: 699-711.
14. Robert-Moreno A, Espinosa L, de la Pompa JL, Bigas A. RBPjkappa-dependent Notch function regulates Gata2 and is essential for the formation of intra-embryonic hematopoietic cells. Development 2005; 132: 1117-1126.
15. Bertrand JY, Cisson JL, Stachura DL, Traver D. Notch signaling distinguishes 2 waves of definitive hematopoiesis in the zebrafish embryo. Blood 2010; 115: 2777-2783.
16. Yu X, Zou J, Ye Z, Hammond H, Chen G, Tokunaga A et al. Notch signaling activation in human embryonic stem cells is required for embryonic, but not trophoblastic, lineage commitment. Cell Stem Cell 2008; 2: 461-471.
17. Lee JB, Werbowetski-Ogilvie TE, Lee JH, McIntyre BA, Schnerch A, Hong SH et al. Notch-HES1 signaling axis controls hemato-endothelial fate decisions of human embyronic and induced pluripotent cells. Blood 2013; 122: 1162-1173.
18. Montes R, Ligero G, Sanchez L, Catalina P, de la Cueva T, Nieto A et al. Feeder-free maintenance of hESCs in mesenchymal stem cell-conditioned media: distinct requirements for TGF-beta and IGF-II. Cell Res 2009; 19: 698-709.
19. Ramos-Mejia V, Fernandez AF, Ayllon V, Real PJ, Bueno C, Anderson P et al. Maintenance of human embryonic stem cells in mesenchymal stem cell-conditioned media augments hematopoietic specification. Stem Cells Dev 2012; 21: 1549-1558.
20. Chadwick K, Wang L, Li L, Menendez P, Murdoch B, Rouleau A et al. Cytokines and BMP-4 promote hematopoietic differentiation of human embryonic stem cells. Blood 2003; 102: 906-915.
21. Ramos-Mejia V, Melen GJ, Sanchez L, Gutierrez-Aranda I, Ligero G, Cortes JL et al. Nodal/Activin signaling predicts human pluripotent stem cell lines prone to differentiate toward the hematopoietic lineage. Mol Ther 2010; 18: 2173-2181.
22. Vodyanik MA, Slukvin II. Hematoendothelial differentiation of human embryonic stem cells. Curr Protoc Cell Biol 2007; 23: Unit 23-Unit 26.
23. Real PJ, Ligero G, Ayllon V, Ramos-Mejia V, Bueno C, Gutierrez-Aranda I et al. SCL/TAL1 regulates hematopoietic specification from human embryonic stem cells. Mol Ther 2012; 20: 1443-1453.
24. Caolo V, van den Akker NM, Verbruggen S, Donners MM, Swennen G, Schulten H et al. Feed-forward signaling by membrane-bound ligand receptor circuit: the case of NOTCH DELTA-like 4 ligand in endothelial cells. J Biol Chem 2010; 285: 40681-40689.
25. Hayashi H, Kume T. Foxc transcription factors directly regulate Dll4 and Hey2 expression by interacting with the VEGF-Notch signaling pathways in endothelial cells. PLoS One 2008; 3: e2401.
26. Ruiz-Herguido C, Guiu J, D'Altri T, Ingles-Esteve J, Dzierzak E, Espinosa L et al. Hematopoietic stem cell development requires transient Wnt/beta-catenin activity. J Exp Med 2012; 209: 1457-1468.
27. Dando JS, Tavian M, Catelain C, Poirault S, Bennaceur-Griscelli A, Sainteny F et al. Notch/Delta4 interaction in human embryonic liver CD34+ CD38-cells: positive influence on BFU-E production and LTC-IC potential maintenance. Stem Cells 2005; 23: 550-560.
28. Laranjeiro R, Alcobia I, Neves H, Gomes AC, Saavedra P, Carvalho CC et al. The Notch ligand delta-like 4 regulates multiple stages of early hemato-vascular development. PLoS One 2012; 7: e34553.
29. Suenobu S, Takakura N, Inada T, Yamada Y, Yuasa H, Zhang XQ et al. A role of EphB4 receptor and its ligand, ephrin-B2, in erythropoiesis. Biochem Biophys Res Commun 2002; 293: 1124-1131.
30. Chong DC, Koo Y, Xu K, Fu S, Cleaver O. Stepwise arteriovenous fate acquisition during mammalian vasculogenesis. Dev Dyn 2011; 240: 2153-2165.
31. Krebs LT, Xue Y, Norton CR, Shutter JR, Maguire M, Sundberg JP et al. Notch signaling is essential for vascular morphogenesis in mice. Genes Dev 2000; 14: 1343-1352.
32. Shutter JR, Scully S, Fan W, Richards WG, Kitajewski J, Deblandre GA et al. Dll4, a novel Notch ligand expressed in arterial endothelium. Genes Dev 2000; 14: 1313-1318.
33. Alcobia I, Gomes A, Saavedra P, Laranjeiro R, Oliveira S, Parreira L et al. Portrayal of the Notch system in embryonic stem cell-derived embryoid bodies. Cells Tissues Organs 2010; 193: 239-252.
34. Martinez JC, Muller MM, Turley H, Steers G, Choteau L, Li JL et al. Nuclear and membrane expression of the angiogenesis regulator delta-like ligand 4 (DLL4) in normal and malignant human tissues. Histopathology 2009; 54: 598-606.
35. McKinney-Freeman S, Cahan P, Li H, Lacadie SA, Huang HT, Curran M et al. The transcriptional landscape of hematopoietic stem cell ontogeny. Cell Stem Cell 2012; 11: 701-714.
36. Boisset JC, Clapes T, Van Der Linden R, Dzierzak E, Robin C. Integrin alphaIIb (CD41) plays a role in the maintenance of hematopoietic stem cell activity in the mouse embryonic aorta. Biol Open 2013; 2: 525-532.
37. Vodyanik MA, Thomson JA, Slukvin II. Leukosialin (CD43) defines hematopoietic progenitors in human embryonic stem cell differentiation cultures. Blood 2006; 108: 2095-2105.
38. Seo S, Fujita H, Nakano A, Kang M, Duarte A, Kume T. The forkhead transcription factors, Foxc1 and Foxc2, are required for arterial specification and lymphatic sprouting during vascular development. Dev Biol 2006; 294: 458-470.
39. Lancrin C, Sroczynska P, Stephenson C, Allen T, Kouskoff V, Lacaud G. The hae-mangioblast generates haematopoietic cells through a haemogenic endothelium stage. Nature 2009; 457: 892-895.
40. Zovein AC, Hofmann JJ, Lynch M, French WJ, Turlo KA, Yang Y et al. Fate tracing reveals the endothelial origin of hematopoietic stem cells. Cell Stem Cell 2008; 3: 625-636.
41. Rybtsov S, Sobiesiak M, Taoudi S, Souilhol C, Senserrich J, Liakhovitskaia A et al. Hierarchical organization and early hematopoietic specification of the developing HSC lineage in the AGM region. J Exp Med 2011; 208: 1305-1315.
42. Taoudi S, Gonneau C, Moore K, Sheridan JM, Blackburn CC, Taylor E et al. Extensive hematopoietic stem cell generation in the AGM region via maturation of VE-cadherin+CD45+ pre-definitive HSCs. Cell Stem Cell 2008; 3: 99-108.
43. Guiu J, Shimizu R, D'Altri T, Fraser ST, Hatakeyama J, Bresnick EH et al. Hes repressors are essential regulators of hematopoietic stem cell development downstream of Notch signaling. J Exp Med 2013; 210: 71-84.
44. Robert-Moreno A, Guiu J, Ruiz-Herguido C, Lopez ME, Ingles-Esteve J, Riera L et al. Impaired embryonic haematopoiesis yet normal arterial development in the absence of the Notch ligand Jagged1. EMBO J 2008; 27: 1886-1895.
45. Bigas A, D'Altri T, Espinosa L. The Notch pathway in hematopoietic stem cells. Curr Top Microbiol Immunol 2012; 360: 1-18.
46. 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: 108-111.
47. Swiers G, Rode C, Azzoni E, de Bruijn MF. A short history of hemogenic endo-thelium. Blood Cells Mol Dis 2013; 51: 206-212.
48. Duarte A, Hirashima M, Benedito R, Trindade A, Diniz P, Bekman E et al. Dosage-sensitive requirement for mouse Dll4 in artery development. Genes Dev 2004; 18: 2474-2478.
49. Krebs LT, Shutter JR, Tanigaki K, Honjo T, Stark KL, Gridley T. Haploinsufficient lethality and formation of arteriovenous malformations in Notch pathway mutants. Genes Dev 2004; 18: 2469-2473.
50. Hozumi K, Mailhos C, Negishi N, Hirano K, Yahata T, Ando K et al. Delta-like 4 is indispensable in thymic environment specific for T cell development. J Exp Med 2008; 205: 2507-2513.
51. Rafii S, Kloss CC, Butler JM, Ginsberg M, Gars E, Lis R et al. Human ESC-derived hemogenic endothelial cells undergo distinct waves of endothelial to hemato-poietic transition. Blood 2013; 121: 770-780.
52. Oberlin E, Fleury M, Clay D, Petit-Cocault L, Candelier JJ, Mennesson B et al. VE-cadherin expression allows identification of a new class of hematopoietic stem cells within human embryonic liver. Blood 2010; 116: 4444-4455.
53. Eilken HM, Nishikawa S, Schroeder T. Continuous single-cell imaging of blood generation from haemogenic endothelium. Nature 2009; 457: 896-900.
54. Grigorian M, Mandal L, Hakimi M, Ortiz I, Hartenstein V. The convergence of Notch and MAPK signaling specifies the blood progenitor fate in the Drosophila mesoderm. Dev Biol 2011; 353: 105-118.