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Modeling murine yolk sac hematopoiesis with embryonic stem cell culture systems |
Brandoch D. COOK( ) |
Department of Surgery, Weill Cornell Medical College, New York, NY 10065, USA |
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Abstract The onset of hematopoiesis in mammals is defined by generation of primitive erythrocytes and macrophage progenitors in embryonic yolk sac. Laboratories have met the challenge of transient and swiftly changing specification events from ventral mesoderm through multipotent progenitors and maturing lineage-restricted hematopoietic subtypes, by developing powerful in vitro experimental models to interrogate hematopoietic ontogeny. Most importantly, studies of differentiating embryonic stem cell derivatives in embryoid body and stromal coculture systems have identified crucial roles for transcription factor networks (e.g. Gata1, Runx1, Scl) and signaling pathways (e.g. BMP, VEGF, WNT) in controlling stem and progenitor cell output. These and other relevant pathways have pleiotropic biological effects, and are often associated with early embryonic lethality in knockout mice. Further refinement in subsequent studies has allowed conditional expression of key regulatory genes, and isolation of progenitors via cell surface markers (e.g. FLK1) and reporter-tagged constructs, with the purpose of measuring their primitive and definitive hematopoietic potential. These observations continue to inform attempts to direct the differentiation, and augment the expansion, of progenitors in human cell culture systems that may prove useful in cell replacement therapies for hematopoietic deficiencies. The purpose of this review is to survey the extant literature on the use of differentiating murine embryonic stem cells in culture to model the developmental process of yolk sac hematopoiesis.
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Keywords
hematopoietic
progenitors
embryonic
stem cells
differentiation
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Corresponding Author(s):
Brandoch D. COOK
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Just Accepted Date: 11 August 2014
Online First Date: 02 September 2014
Issue Date: 11 October 2014
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|
1 |
Baik J, Borges L, Magli A, Thatava T, Perlingeiro R C (2012). Effect of endoglin overexpression during embryoid body development. Exp Hematol, 40(10): 837–846
https://doi.org/10.1016/j.exphem.2012.06.007
pmid: 22728030
|
2 |
Bielinska M, Narita N, Heikinheimo M, Porter S B, Wilson D B (1996). Erythropoiesis and vasculogenesis in embryoid bodies lacking visceral yolk sac endoderm. Blood, 88(10): 3720–3730
pmid: 8916936
|
3 |
Boros K, Lacaud G, Kouskoff V (2011). The transcription factor Mxd4 controls the proliferation of the first blood precursors at?the onset of hematopoietic development in?vitro. Exp Hematol, 39(11): 1090–1100
https://doi.org/10.1016/j.exphem.2011.07.007
pmid: 21782766
|
4 |
Chan R J, Johnson S A, Li Y, Yoder M C, Feng G S (2003). A definitive role of Shp-2 tyrosine phosphatase in mediating embryonic stem cell differentiation and hematopoiesis. Blood, 102(6): 2074–2080
https://doi.org/10.1182/blood-2003-04-1171
pmid: 12791646
|
5 |
Chanda B, Ditadi A, Iscove N N, Keller G (2013). Retinoic acid signaling is essential for embryonic hematopoietic stem cell development. Cell, 155(1): 215–227
https://doi.org/10.1016/j.cell.2013.08.055
pmid: 24074870
|
6 |
Cheng X, Huber T L, Chen V C, Gadue P, Keller G M (2008). Numb mediates the interaction between Wnt and Notch to modulate primitive erythropoietic specification from the hemangioblast. Development, 135(20): 3447–3458
https://doi.org/10.1242/dev.025916
pmid: 18799543
|
7 |
Clarke D, Vegiopoulos A, Crawford A, Mucenski M, Bonifer C, Frampton J (2000). In vitro differentiation of c-myb-/- ES cells reveals that the colony forming capacity of unilineage macrophage precursors and myeloid progenitor commitment are c-Myb independent. Oncogene, 19(30): 3343–3351
https://doi.org/10.1038/sj.onc.1203661
pmid: 10918591
|
8 |
Clarke R L, Yzaguirre A D, Yashiro-Ohtani Y, Bondue A, Blanpain C, Pear W S, Speck N A, Keller G (2013). The expression of Sox17 identifies and regulates haemogenic endothelium. Nat Cell Biol, 15(5): 502–510
https://doi.org/10.1038/ncb2724
pmid: 23604320
|
9 |
Cook B D, Evans T (2014). BMP signaling balances murine myeloid potential through SMAD-independent p38MAPK and NOTCH pathways. Blood, 124(3): 393–402
https://doi.org/10.1182/blood-2014-02-556993
pmid: 24894772
|
10 |
Cook B D, Liu S, Evans T (2011). Smad1 signaling restricts hematopoietic potential after promoting hemangioblast commitment. Blood, 117(24): 6489–6497
https://doi.org/10.1182/blood-2010-10-312389
pmid: 21515822
|
11 |
Dahl L, Richter K, H?gglund A C, Carlsson L (2008). Lhx2 expression promotes self-renewal of a distinct multipotential hematopoietic progenitor cell in embryonic stem cell-derived embryoid bodies. PLoS ONE, 3(4): e2025
https://doi.org/10.1371/journal.pone.0002025
pmid: 18431502
|
12 |
Doetschman T C, Eistetter H, Katz M, Schmidt W, Kemler R (1985). The in vitro development of blastocyst-derived embryonic stem cell lines: formation of visceral yolk sac, blood islands and myocardium. J Embryol Exp Morphol, 87: 27–45
pmid: 3897439
|
13 |
Era T, Izumi N, Hayashi M, Tada S, Nishikawa S, Nishikawa S (2008). Multiple mesoderm subsets give rise to endothelial cells, whereas hematopoietic cells are differentiated only from a restricted subset in embryonic stem cell differentiation culture. Stem Cells, 26(2): 401–411
https://doi.org/10.1634/stemcells.2006-0809
pmid: 17991917
|
14 |
Ferkowicz M J, Starr M, Xie X, Li W, Johnson S A, Shelley W C, Morrison P R, Yoder M C (2003). CD41 expression defines the onset of primitive and definitive hematopoiesis in the murine embryo. Development, 130(18): 4393–4403
https://doi.org/10.1242/dev.00632
pmid: 12900455
|
15 |
Fujimoto T T, Kohata S, Suzuki H, Miyazaki H, Fujimura K (2003). Production of functional platelets by differentiated embryonic stem (ES) cells in vitro. Blood, 102(12): 4044–4051
https://doi.org/10.1182/blood-2003-06-1773
pmid: 12920021
|
16 |
Gandillet A, Serrano A G, Pearson S, Lie-A-Ling M, Lacaud G, Kouskoff V (2009). Sox7-sustained expression alters the balance between proliferation and differentiation of hematopoietic progenitors at the onset of blood specification. Blood, 114(23): 4813–4822
https://doi.org/10.1182/blood-2009-06-226290
pmid: 19801444
|
17 |
Grigoriadis A E, Kennedy M, Bozec A, Brunton F, Stenbeck G, Park I H, Wagner E F, Keller G M (2010). Directed differentiation of hematopoietic precursors and functional osteoclasts from human ES and iPS cells. Blood, 115(14): 2769–2776
https://doi.org/10.1182/blood-2009-07-234690
pmid: 20065292
|
18 |
Hadland B K, Huppert S S, Kanungo J, Xue Y, Jiang R, Gridley T, Conlon R A, Cheng A M, Kopan R, Longmore G D (2004). A requirement for Notch1 distinguishes 2 phases of definitive hematopoiesis during development. Blood, 104(10): 3097–3105
https://doi.org/10.1182/blood-2004-03-1224
pmid: 15251982
|
19 |
Helgason C D, Sauvageau G, Lawrence H J, Largman C, Humphries R K (1996). Overexpression of HOXB4 enhances the hematopoietic potential of embryonic stem cells differentiated in vitro. Blood, 87(7): 2740–2749
pmid: 8639890
|
20 |
Hidaka M, Stanford W L, Bernstein A (1999). Conditional requirement for the Flk-1 receptor in the in vitro generation of early hematopoietic cells. Proc Natl Acad Sci USA, 96(13): 7370–7375
https://doi.org/10.1073/pnas.96.13.7370
pmid: 10377421
|
21 |
Irion S, Clarke R L, Luche H, Kim I, Morrison S J, Fehling H J, Keller G M (2010). Temporal specification of blood progenitors from mouse embryonic stem cells and induced pluripotent stem cells. Development, 137(17): 2829–2839
https://doi.org/10.1242/dev.042119
pmid: 20659975
|
22 |
Jackson M, Axton R A, Taylor A H, Wilson J A, Gordon-Keylock S A, Kokkaliaris K D, Brickman J M, Schulz H, Hummel O, Hubner N, Forrester L M (2012). HOXB4 can enhance the differentiation of embryonic stem cells by modulating the hematopoietic niche. Stem Cells, 30(2): 150–160
https://doi.org/10.1002/stem.782
pmid: 22084016
|
23 |
Johansson B M, Wiles M V (1995). Evidence for involvement of activin A and bone morphogenetic protein 4 in mammalian mesoderm and hematopoietic development. Mol Cell Biol, 15(1): 141–151
pmid: 7799920
|
24 |
Keller G, Kennedy M, Papayannopoulou T, Wiles M V (1993). Hematopoietic commitment during embryonic stem cell differentiation in culture. Mol Cell Biol, 13(1): 473–486
pmid: 8417345
|
25 |
Keller G, Wall C, Fong A Z, Hawley T S, Hawley R G (1998). Overexpression of HOX11 leads to the immortalization of embryonic precursors with both primitive and definitive hematopoietic potential. Blood, 92(3): 877–887
pmid: 9680355
|
26 |
Kennedy M, D’Souza S L, Lynch-Kattman M, Schwantz S, Keller G (2007). Development of the hemangioblast defines the onset of hematopoiesis in human ES cell differentiation cultures. Blood, 109(7): 2679–2687
pmid: 17148580
|
27 |
Kennedy M, Firpo M, Choi K, Wall C, Robertson S, Kabrun N, Keller G (1997). A common precursor for primitive erythropoiesis and definitive haematopoiesis. Nature, 386(6624): 488–493
https://doi.org/10.1038/386488a0
pmid: 9087406
|
28 |
Kingsley P D, Malik J, Fantauzzo K A, Palis J (2004). Yolk sac-derived primitive erythroblasts enucleate during mammalian embryogenesis. Blood, 104(1): 19–25
https://doi.org/10.1182/blood-2003-12-4162
pmid: 15031208
|
29 |
Kitajima K, Kojima M, Nakajima K, Kondo S, Hara T, Miyajima A, Takeuchi T (1999). Definitive but not primitive hematopoiesis is impaired in jumonji mutant mice. Blood, 93(1): 87–95
pmid: 9864150
|
30 |
Klimchenko O, Mori M, Distefano A, Langlois T, Larbret F, Lecluse Y, Feraud O, Vainchenker W, Norol F, Debili N (2009). A common bipotent progenitor generates the erythroid and megakaryocyte lineages in embryonic stem cell-derived primitive hematopoiesis. Blood, 114(8): 1506–1517
https://doi.org/10.1182/blood-2008-09-178863
pmid: 19478046
|
31 |
Krause D S, Mucenski M L, Lawler A M, May W S (1998). CD34 expression by embryonic hematopoietic and endothelial cells does not require c-Myb. Exp Hematol, 26(11): 1086–1092
pmid: 9766450
|
32 |
Kyba M, Perlingeiro R C, Daley G Q (2002). HoxB4 confers definitive lymphoid-myeloid engraftment potential on embryonic stem cell and yolk sac hematopoietic progenitors. Cell, 109(1): 29–37
https://doi.org/10.1016/S0092-8674(02)00680-3
pmid: 11955444
|
33 |
Kyba M, Perlingeiro R C, Hoover R R, Lu C W, Pierce J, Daley G Q (2003). Enhanced hematopoietic differentiation of embryonic stem cells conditionally expressing Stat5. Proc Natl Acad Sci USA, 100(Suppl 1): 11904–11910
https://doi.org/10.1073/pnas.1734140100
pmid: 12930895
|
34 |
Lacaud G, Gore L, Kennedy M, Kouskoff V, Kingsley P, Hogan C, Carlsson L, Speck N, Palis J, Keller G (2002). Runx1 is essential for hematopoietic commitment at the hemangioblast stage of development in vitro. Blood, 100(2): 458–466
https://doi.org/10.1182/blood-2001-12-0321
pmid: 12091336
|
35 |
Laranjeiro R, Alcobia I, Neves H, Gomes A C, Saavedra P, Carvalho C C, Duarte A, Cidad?o A, Parreira L (2012). The notch ligand delta-like 4 regulates multiple stages of early hemato-vascular development. PLoS ONE, 7(4): e34553
https://doi.org/10.1371/journal.pone.0034553
pmid: 22514637
|
36 |
Lengerke C, McKinney-Freeman S, Naveiras O, Yates F, Wang Y, Bansal D, Daley G Q (2007). The cdx-hox pathway in hematopoietic stem cell formation from embryonic stem cells. Ann N Y Acad Sci, 1106(1): 197–208
https://doi.org/10.1196/annals.1392.006
pmid: 17303828
|
37 |
Li X, Xiong J W, Shelley C S, Park H, Arnaout M A (2006). The transcription factor ZBP-89 controls generation of the hematopoietic lineage in zebrafish and mouse embryonic stem cells. Development, 133(18): 3641–3650
https://doi.org/10.1242/dev.02540
pmid: 16914492
|
38 |
Lichanska A M, Browne C M, Henkel G W, Murphy K M, Ostrowski M C, McKercher S R, Maki R A, Hume D A (1999). Differentiation of the mononuclear phagocyte system during mouse embryogenesis: the role of transcription factor PU.1. Blood, 94(1): 127–138
pmid: 10381505
|
39 |
Liu B, Sun Y, Jiang F, Zhang S, Wu Y, Lan Y, Yang X, Mao N (2003). Disruption of Smad5 gene leads to enhanced proliferation of high-proliferative potential precursors during embryonic hematopoiesis. Blood, 101(1): 124–133
https://doi.org/10.1182/blood-2002-02-0398
pmid: 12393578
|
40 |
Lu L S, Wang S J, Auerbach R (1996). In vitro and in vivo differentiation into B cells, T cells, and myeloid cells of primitive yolk sac hematopoietic precursor cells expanded>100-fold by coculture with a clonal yolk sac endothelial cell line. Proc Natl Acad Sci USA, 93(25): 14782–14787
https://doi.org/10.1073/pnas.93.25.14782
pmid: 8962132
|
41 |
Lux C T, Yoshimoto M, McGrath K, Conway S J, Palis J, Yoder M C (2008). All primitive and definitive hematopoietic progenitor cells emerging before E10 in the mouse embryo are products of the yolk sac. Blood, 111(7): 3435–3438
https://doi.org/10.1182/blood-2007-08-107086
pmid: 17932251
|
42 |
Martin R, Lahlil R, Damert A, Miquerol L, Nagy A, Keller G, Hoang T (2004). SCL interacts with VEGF to suppress apoptosis at the onset of hematopoiesis. Development, 131(3): 693–702
https://doi.org/10.1242/dev.00968
pmid: 14729577
|
43 |
McLeod D L, Shreeve M M, Axelrad A A (1974). Improved plasma culture system for production of erythrocytic colonies in vitro: quantitative assay method for CFU-E. Blood, 44(4): 517–534
pmid: 4137721
|
44 |
McReynolds L J, Gupta S, Figueroa M E, Mullins M C, Evans T (2007). Smad1 and Smad5 differentially regulate embryonic hematopoiesis. Blood, 110(12): 3881–3890
https://doi.org/10.1182/blood-2007-04-085753
pmid: 17761518
|
45 |
Miller J D, Stacy T, Liu P P, Speck N A (2001). Core-binding factor β (CBFβ), but not CBFbeta-smooth muscle myosin heavy chain, rescues definitive hematopoiesis in CBFβ-deficient embryonic stem cells. Blood, 97(8): 2248–2256
https://doi.org/10.1182/blood.V97.8.2248
pmid: 11290585
|
46 |
Nakano T, Kodama H, Honjo T (1996). In vitro development of primitive and definitive erythrocytes from different precursors. Science, 272(5262): 722–724
https://doi.org/10.1126/science.272.5262.722
pmid: 8614833
|
47 |
Nogueira M M, Mitjavila-Garcia M T, Le Pesteur F, Filippi M D, Vainchenker W, Dubart Kupperschmitt A, Sainteny F (2000). Regulation of Id gene expression during embryonic stem cell-derived hematopoietic differentiation. Biochem Biophys Res Commun, 276(2): 803–812
https://doi.org/10.1006/bbrc.2000.3543
pmid: 11027551
|
48 |
Nostro M C, Cheng X, Keller G M, Gadue P (2008). Wnt, activin, and BMP signaling regulate distinct stages in the developmental pathway from embryonic stem cells to blood. Cell Stem Cell, 2(1): 60–71
https://doi.org/10.1016/j.stem.2007.10.011
pmid: 18371422
|
49 |
Okuda T, van Deursen J, Hiebert S W, Grosveld G, Downing J R (1996). AML1, the target of multiple chromosomal translocations in human leukemia, is essential for normal fetal liver hematopoiesis. Cell, 84(2): 321–330
https://doi.org/10.1016/S0092-8674(00)80986-1
pmid: 8565077
|
50 |
Otani T, Inoue T, Tsuji-Takayama K, Ijiri Y, Nakamura S, Motoda R, Orita K (2005). Progenitor analysis of primitive erythropoiesis generated from in vitro culture of embryonic stem cells. Exp Hematol, 33(6): 632–640
https://doi.org/10.1016/j.exphem.2005.03.006
pmid: 15911087
|
51 |
Otani T, Nakamura S, Inoue T, Ijiri Y, Tsuji-Takayama K, Motoda R, Orita K (2004). Erythroblasts derived in vitro from embryonic stem cells in the presence of erythropoietin do not express the TER-119 antigen. Exp Hematol, 32(7): 607–613
https://doi.org/10.1016/j.exphem.2004.04.007
pmid: 15246156
|
52 |
Palis J, Robertson S, Kennedy M, Wall C, Keller G (1999). Development of erythroid and myeloid progenitors in the yolk sac and embryo proper of the mouse. Development, 126(22): 5073–5084
pmid: 10529424
|
53 |
Pearson S, Lancrin C, Lacaud G, Kouskoff V (2010). The sequential expression of CD40 and Icam2 defines progressive steps in the formation of blood precursors from the mesoderm germ layer. Stem Cells, 28(6): 1089–1098
https://doi.org/10.1002/stem.434
pmid: 20506544
|
54 |
Pereira C F, Chang B, Qiu J, Niu X, Papatsenko D, Hendry C E, Clark N R, Nomura-Kitabayashi A, Kovacic J C, Ma’ayan A, Schaniel C, Lemischka I R, Moore K (2013). Induction of a hemogenic program in mouse fibroblasts. Cell Stem Cell, 13(2): 205–218
https://doi.org/10.1016/j.stem.2013.05.024
pmid: 23770078
|
55 |
Perlingeiro R C, Kyba M, Bodie S, Daley G Q (2003). A role for thrombopoietin in hemangioblast development. Stem Cells, 21(3): 272–280
https://doi.org/10.1634/stemcells.21-3-272
pmid: 12743322
|
56 |
Perlingeiro R C, Kyba M, Daley G Q (2001). Clonal analysis of differentiating embryonic stem cells reveals a hematopoietic progenitor with primitive erythroid and adult lymphoid-myeloid potential. Development, 128(22): 4597–4604
pmid: 11714684
|
57 |
Pick M, Azzola L, Mossman A, Stanley E G, Elefanty A G (2007). Differentiation of human embryonic stem cells in serum-free medium reveals distinct roles for bone morphogenetic protein 4, vascular endothelial growth factor, stem cell factor, and fibroblast growth factor 2 in hematopoiesis. Stem Cells, 25(9): 2206–2214
https://doi.org/10.1634/stemcells.2006-0713
pmid: 17556598
|
58 |
Pineault N, Helgason C D, Lawrence H J, Humphries R K (2002). Differential expression of Hox, Meis1, and Pbx1 genes in primitive cells throughout murine hematopoietic ontogeny. Exp Hematol, 30(1): 49–57
https://doi.org/10.1016/S0301-472X(01)00757-3
pmid: 11823037
|
59 |
Robb L, Elwood N J, Elefanty A G, K?ntgen F, Li R, Barnett L D, Begley C G (1996). The scl gene product is required for the generation of all hematopoietic lineages in the adult mouse. EMBO J, 15(16): 4123–4129
pmid: 8861941
|
60 |
Robb L, Lyons I, Li R, Hartley L, K?ntgen F, Harvey R P, Metcalf D, Begley C G (1995). Absence of yolk sac hematopoiesis from mice with a targeted disruption of the scl gene. Proc Natl Acad Sci USA, 92(15): 7075–7079
https://doi.org/10.1073/pnas.92.15.7075
pmid: 7624372
|
61 |
Saleque S, Cameron S, Orkin S H (2002). The zinc-finger proto-oncogene Gfi-1b is essential for development of the erythroid and megakaryocytic lineages. Genes Dev, 16(3): 301–306
https://doi.org/10.1101/gad.959102
pmid: 11825872
|
62 |
Sandler V M, Lis R, Liu Y, Kedem A, James D, Elemento O, Butler J M, Scandura J M, Rafii S (2014). Reprogramming human endothelial cells to haematopoietic cells requires vascular induction. Nature, 511(7509): 312–318
https://doi.org/10.1038/nature13547
pmid: 25030167
|
63 |
Sauvageau G, Thorsteinsdottir U, Eaves C J, Lawrence H J, Largman C, Lansdorp P M, Humphries R K (1995). Overexpression of HOXB4 in hematopoietic cells causes the selective expansion of more primitive populations in vitro and in vivo. Genes Dev, 9(14): 1753–1765
https://doi.org/10.1101/gad.9.14.1753
pmid: 7622039
|
64 |
Shalaby F, Ho J, Stanford W L, Fischer K D, Schuh A C, Schwartz L, Bernstein A, Rossant J (1997). A requirement for Flk1 in primitive and definitive hematopoiesis and vasculogenesis. Cell, 89(6): 981–990
https://doi.org/10.1016/S0092-8674(00)80283-4
pmid: 9200616
|
65 |
Shivdasani R A, Mayer E L, Orkin S H (1995). Absence of blood formation in mice lacking the T-cell leukaemia oncoprotein tal-1/SCL. Nature, 373(6513): 432–434
https://doi.org/10.1038/373432a0
pmid: 7830794
|
66 |
Simon M C, Pevny L, Wiles M V, Keller G, Costantini F, Orkin S H (1992). Rescue of erythroid development in gene targeted GATA-1- mouse embryonic stem cells. Nat Genet, 1(2): 92–98
https://doi.org/10.1038/ng0592-92
pmid: 1302015
|
67 |
Southwood C M, Downs K M, Bieker J J (1996). Erythroid Kruppel-like factor exhibits an early and sequentially localized pattern of expression during mammalian erythroid ontogeny. Dev Dyn, 20: 248–259
|
68 |
Stephenson J R, Axelrad A A, McLeod D L, Shreeve M M (1971). Induction of colonies of hemoglobin-synthesizing cells by erythropoietin in vitro. Proc Natl Acad Sci USA, 68(7): 1542–1546
https://doi.org/10.1073/pnas.68.7.1542
pmid: 4104431
|
69 |
Sturgeon C M, Chicha L, Ditadi A, Zhou Q, McGrath K E, Palis J, Hammond S M, Wang S, Olson E N, Keller G (2012). Primitive erythropoiesis is regulated by miR-126 via nonhematopoietic Vcam-1+ cells. Dev Cell, 23(1): 45–57
https://doi.org/10.1016/j.devcel.2012.05.021
pmid: 22749417
|
70 |
Sturgeon C M, Ditadi A, Awong G, Kennedy M, Keller G (2014). Wnt signaling controls the specification of definitive and primitive hematopoiesis from human pluripotent stem cells. Nat Biotechnol, 32(6): 554–561
https://doi.org/10.1038/nbt.2915
pmid: 24837661
|
71 |
Suwabe N, Takahashi S, Nakano T, Yamamoto M (1998). GATA-1 regulates growth and differentiation of definitive erythroid lineage cells during in vitro ES cell differentiation. Blood, 92(11): 4108–4118
pmid: 9834216
|
72 |
Tober J, Koniski A, McGrath K E, Vemishetti R, Emerson R, de Mesy-Bentley K K, Waugh R, Palis J (2007). The megakaryocyte lineage originates from hemangioblast precursors and is an integral component both of primitive and of definitive hematopoiesis. Blood, 109(4): 1433–1441
https://doi.org/10.1182/blood-2006-06-031898
pmid: 17062726
|
73 |
Tsai F Y, Keller G, Kuo F C, Weiss M, Chen J, Rosenblatt M, Alt F W, Orkin S H (1994). An early haematopoietic defect in mice lacking the transcription factor GATA-2. Nature, 371(6494): 221–226
https://doi.org/10.1038/371221a0
pmid: 8078582
|
74 |
Walker L, Carlson A, Tan-Pertel H T, Weinmaster G, Gasson J (2001). The notch receptor and its ligands are selectively expressed during hematopoietic development in the mouse. Stem Cells, 19(6): 543–552
https://doi.org/10.1634/stemcells.19-6-543
pmid: 11713346
|
75 |
Wang L, Li L, Menendez P, Cerdan C, Bhatia M (2005). Human embryonic stem cells maintained in the absence of mouse embryonic fibroblasts or conditioned media are capable of hematopoietic development. Blood, 105(12): 4598–4603
https://doi.org/10.1182/blood-2004-10-4065
pmid: 15718421
|
76 |
Wang L, Li L, Shojaei F, Levac K, Cerdan C, Menendez P, Martin T, Rouleau A, Bhatia M (2004). Endothelial and hematopoietic cell fate of human embryonic stem cells originates from primitive endothelium with hemangioblastic properties. Immunity, 21(1): 31–41
https://doi.org/10.1016/j.immuni.2004.06.006
pmid: 15345218
|
77 |
Wareing S, Eliades A, Lacaud G, Kouskoff V (2012). ETV2 expression marks blood and endothelium precursors, including hemogenic endothelium, at the onset of blood development. Dev Dyn, 241: 1454–1464
|
78 |
Warren A J, Colledge W H, Carlton M B, Evans M J, Smith A J, Rabbitts T H (1994). The oncogenic cysteine-rich LIM domain protein rbtn2 is essential for erythroid development. Cell, 78(1): 45–57
https://doi.org/10.1016/0092-8674(94)90571-1
pmid: 8033210
|
79 |
Weisel K C, Gao Y, Shieh J H, Moore M A (2006). Stromal cell lines from the aorta-gonado-mesonephros region are potent supporters of murine and human hematopoiesis. Exp Hematol, 34(11): 1505–1516
https://doi.org/10.1016/j.exphem.2006.06.013
pmid: 17046570
|
80 |
Weiss M J, Keller G, Orkin S H (1994). Novel insights into erythroid development revealed through in vitro differentiation of GATA-1 embryonic stem cells. Genes Dev, 8(10): 1184–1197
https://doi.org/10.1101/gad.8.10.1184
pmid: 7926723
|
81 |
Wiles M V, Johansson B M (1997). Analysis of factors controlling primary germ layer formation and early hematopoiesis using embryonic stem cell in vitro differentiation. Leukemia, 11(Suppl 3): 454–456
pmid: 9209423
|
82 |
Wiles M V, Keller G (1991). Multiple hematopoietic lineages develop from embryonic stem (ES) cells in culture. Development, 111(2): 259–267
pmid: 1893864
|
83 |
Wu H, Liu X, Jaenisch R, Lodish H F (1995). Generation of committed erythroid BFU-E and CFU-E progenitors does not require erythropoietin or the erythropoietin receptor. Cell, 83(1): 59–67
https://doi.org/10.1016/0092-8674(95)90234-1
pmid: 7553874
|
84 |
Zafonte B T, Liu S, Lynch-Kattman M, Torregroza I, Benvenuto L, Kennedy M, Keller G, Evans T (2007). Smad1 expands the hemangioblast population within a limited developmental window. Blood, 109(2): 516–523
https://doi.org/10.1182/blood-2006-02-004564
pmid: 16990609
|
85 |
Zambidis E T, Peault B, Park T S, Bunz F, Civin C I (2005). Hematopoietic differentiation of human embryonic stem cells progresses through sequential hematoendothelial, primitive, and definitive stages resembling human yolk sac development. Blood, 106(3): 860–870
https://doi.org/10.1182/blood-2004-11-4522
pmid: 15831705
|
86 |
Zhang H, Nieves J L, Fraser S T, Isern J, Douvaras P, Papatsenko D, D’Souza S L, Lemischka I R, Dyer M A, Baron M H (2014). Expression of podocalyxin separates the hematopoietic and vascular potentials of mouse embryonic stem cell-derived mesoderm. Stem Cells, 32(1): 191–203
https://doi.org/10.1002/stem.1536
pmid: 24022884
|
87 |
Zhang L, Magli A, Catanese J, Xu Z, Kyba M, Perlingeiro R C (2011). Modulation of TGF-β signaling by endoglin in murine hemangioblast development and primitive hematopoiesis. Blood, 118(1): 88–97
https://doi.org/10.1182/blood-2010-12-325019
pmid: 21602526
|
88 |
Zhang W J, Park C, Arentson E, Choi K (2005). Modulation of hematopoietic and endothelial cell differentiation from mouse embryonic stem cells by different culture conditions. Blood, 105(1): 111–114
https://doi.org/10.1182/blood-2004-04-1306
pmid: 15231577
|
89 |
Zheng J, Kitajima K, Sakai E, Kimura T, Minegishi N, Yamamoto M, Nakano T (2006). Differential effects of GATA-1 on proliferation and differentiation of erythroid lineage cells. Blood, 107(2): 520–527
https://doi.org/10.1182/blood-2005-04-1385
pmid: 16174764
|
90 |
Zou G M, Chan R J, Shelley W C, Yoder M C (2006). Reduction of Shp-2 expression by small interfering RNA reduces murine embryonic stem cell-derived in vitro hematopoietic differentiation. Stem Cells, 24(3): 587–594
https://doi.org/10.1634/stemcells.2005-0272
pmid: 16269528
|
91 |
Zou G M, Luo M H, Reed A, Kelley M R, Yoder M C (2007). Ape1 regulates hematopoietic differentiation of embryonic stem cells through its redox functional domain. Blood, 109(5): 1917–1922
https://doi.org/10.1182/blood-2006-08-044172
pmid: 17053053
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