Temporal specification of blood progenitors from mouse embryonic stem cells and induced pluripotent stem cells

Development

Volumn 137, Issue 17, 2010, Pages 2829-2839

  Irion, Stefan ^a   Clarke, Raedun L ^a   Luche, Hervé ^b   Kim, Injune ^c   Morrison, Sean J ^d   Fehling, Hans Joerg ^e   Keller, Gordon M ^a  

^a UNIVERSITY HEALTH NETWORK   (Canada)

^b CENTRE D IMMUNOLOGIE DE MARSEILLE LUMINY   (France)

^c Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

^d UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^e UNIVERSITY HOSPITAL ULM   (Germany)

Author keywords

AGM; Embryonic stem cells; Hematopoiesis; Induced pluripotent stem cell; Mouse; Sox17; Yolk sac

Indexed keywords

ACTIVIN A; BONE MORPHOGENETIC PROTEIN 4; FIBRINOGEN RECEPTOR; HEPATOCYTE NUCLEAR FACTOR 3BETA; HOX PROTEIN; TRANSCRIPTION FACTOR GATA 3; TRANSCRIPTION FACTOR RUNX1; TRANSCRIPTION FACTOR SOX1; TRANSCRIPTION FACTOR SOX17; TRANSCRIPTION FACTOR TAL1; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2; ACTIVIN; BMP4 PROTEIN, HUMAN; COMPLEMENT 1Q RECEPTOR; COMPLEMENT RECEPTOR; GLYCOPROTEIN IIB; HIGH MOBILITY GROUP B PROTEIN; HOMEODOMAIN PROTEIN; HOXB4 PROTEIN, MOUSE; MEMBRANE PROTEIN; RECOMBINANT PROTEIN; SOX17 PROTEIN, MOUSE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SOX; VASCULOTROPIN A; VEGFA PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; EMBRYONIC STEM CELL; FEMALE; HEMATOPOIESIS; HEMATOPOIETIC CELL; LYMPHOID CELL; MOUSE; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; STROMA CELL; T LYMPHOCYTE; YOLK SAC; ANIMAL; BIOLOGICAL MODEL; CELL LINE; CYTOLOGY; DRUG EFFECT; GENE EXPRESSION; GENETICS; HEMATOPOIETIC STEM CELL; LYMPHOPOIESIS; METABOLISM; PHYSIOLOGY; TIME;

MAMMALIA;

ACTIVINS; ANIMALS; BONE MORPHOGENETIC PROTEIN 4; CELL DIFFERENTIATION; CELL LINE; EMBRYONIC STEM CELLS; GENE EXPRESSION; HEMATOPOIESIS; HEMATOPOIETIC STEM CELLS; HMGB PROTEINS; HOMEODOMAIN PROTEINS; LYMPHOPOIESIS; MEMBRANE GLYCOPROTEINS; MICE; MODELS, BIOLOGICAL; PLATELET MEMBRANE GLYCOPROTEIN IIB; PLURIPOTENT STEM CELLS; RECEPTORS, COMPLEMENT; RECOMBINANT PROTEINS; SOXF TRANSCRIPTION FACTORS; TIME FACTORS; TRANSCRIPTION FACTORS; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 77956212581     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.042119     Document Type: Article

References (69)

1. Bertrand, J. Y., Giroux, S., Golub, R., Klaine, M., Jalil, A., Boucontet, L., Godin, I. and Cumano, A. (2005). Characterization of purified intraembryonic hematopoietic stem cells as a tool to define their site of origin. Proc. Natl. Acad. Sci. USA 102, 134-139. (Pubitemid 40094441)
2. Bertrand, J. Y., Chi, N. C., Santoso, B., Teng, S., Stainier, D. Y. and Traver, D. (2010). Haematopoietic stem cells derive directly from aortic endothelium during development. Nature 464, 108-111.
3. Boisset, J. C., van Cappellen, W., Andrieu-Soler, C., Galjart, N., Dzierzak, E. and Robin, C. (2010). In vivo imaging of haematopoietic cells emerging from the mouse aortic endothelium. Nature 464, 116-120.
4. Cho, S. K., Webber, T. D., Carlyle, J. R., Nakano, T., Lewis, S. M. and Zuniga-Pflucker, J. C. (1999). Functional characterization of B lymphocytes generated in vitro from embryonic stem cells. Proc. Natl. Acad. Sci. USA 96, 9797-9802.
5. Cho, S. K., Bourdeau, A., Letarte, M. and Zuniga-Pflucker, J. C. (2001). Expression and function of CD105 during the onset of hematopoiesis from Flk1(+) precursors. Blood 98, 3635-3642.
6. Choi, K., Kennedy, M., Kazarov, A., Papadimitriou, J. C. and Keller, G. (1998). A common precursor for hematopoietic and endothelial cells. Development 125, 725-732.
7. Conlon, F. L., Lyons, K. M., Takaesu, N., Barth, K. S., Kispert, A., Herrmann, B. and Robertson, E. J. (1994). A primary requirement for nodal in the formation and maintenance of the primitive streak in the mouse. Development 120, 1919-1928. (Pubitemid 24209725)
8. Cumano, A., Dieterlen-Lievre, F. and Godin, I. (1996). Lymphoid potential, probed before circulation in mouse, is restricted to caudal intraembryonic splanchnopleura. Cell 86, 907-916.
9. Cumano, A., Ferraz, J. C., Klaine, M., Di Santo, J. P. and Godin, I. (2001). Intraembryonic, but not yolk sac hematopoietic precursors, isolated before circulation, provide long-term multilineage reconstitution. Immunity 15, 477-485.
10. Davidson, A. J., Ernst, P., Wang, Y., Dekens, M. P., Kingsley, P. D., Palis, J., Korsmeyer, S. J., Daley, G. Q. and Zon, L. I. (2003). cdx4 mutants fail to specify blood progenitors and can be rescued by multiple hox genes. Nature 425, 300-306.
11. de Bruijn, M. F., Ma, X., Robin, C., Ottersbach, K., Sanchez, M. J. and Dzierzak, E. (2002). Hematopoietic stem cells localize to the endothelial cell layer in the midgestation mouse aorta. Immunity 16, 673-683.
12. Dieterlen-Lievre, F. (1975). On the origin of haemopoietic stem cells in the avian embryo: an experimental approach. J. Embryol. Exp. Morphol. 33, 607-619.
13. Ema, M., Takahashi, S. and Rossant, J. (2006). Deletion of the selection cassette, but not cis-acting elements, in targeted Flk1-lacZ allele reveals Flk1 Expression in multipotent mesodermal progenitors. Blood 107, 111-117.
14. Fehling, H. J., Lacaud, G., Kubo, A., Kennedy, M., Robertson, S., Keller, G. and Kouskoff, V. (2003). Tracking mesoderm induction and its specification to the hemangioblast during embryonic stem cell differentiation. Development 130, 4217-4227.
15. Gadue, P., Huber, T. L., Paddison, P. J. and Keller, G. M. (2006). Wnt and TGF-beta signaling are required for the induction of an in vitro model of primitive streak formation using embryonic stem cells. Proc. Natl. Acad. Sci. USA 103, 16806-16811.
16. Galic, Z., Kitchen, S. G., Kacena, A., Subramanian, A., Burke, B., Cortado, R. and Zack, J. A. (2006). T lineage differentiation from human embryonic stem cells. Proc. Natl. Acad. Sci. USA 103, 11742-11747.
17. Galic, Z., Kitchen, S. G., Subramanian, A., Bristol, G., Marsden, M. D., Balamurugan, A., Kacena, A., Yang, O. and Zack, J. A. (2009). Generation of T lineage cells from human embryonic stem cells in a feeder free system. Stem Cells 27, 100-107.
18. Godin, I. E., Garcia-Porrero, J. A., Coutinho, A., Dieterlen-Lievre, F. and Marcos, M. A. (1993). Para-aortic splanchnopleura from early mouse embryos contains B1a cell progenitors. Nature 364, 67-70.
19. Irion, S., Nostro, M. C., Kattman, S. J. and Keller, G. M. (2009). Directed differentiation of pluripotent stem cells: from developmental biology to therapeutic applications. Cold Spring Harbor Symp. Quant. Biol. 73, 101-110.
20. Kabrun, N., Buhring, H. J., Choi, K., Ullrich, A., Risau, W. and Keller, G. (1997). Flk-1 expression defines a population of early embryonic hematopoietic precursors. Development 124, 2039-2048.
21. Kattman, S. J., Huber, T. L. and Keller, G. M. (2006). Multipotent Flk-1+ cardiovascular progenitor cells give rise to the cardiomyocyte, endothelial, and vascular smooth muscle lineages. Dev. Cell 11, 723-732.
22. Keller, G. (2005). Embryonic stem cell differentiation: emergence of a new era in biology and medicine. Genes Dev. 19, 1129-1155.
23. Kennedy, M., D'Souza, S. L., Lynch-Kattman, M., Schwantz, S. and Keller, G. (2007). Development of the hemangioblast defines the onset of hematopoiesis in human ES cell differentiation cultures. Blood 109, 2679-2687.
24. Kim, I., Saunders, T. L. and Morrison, S. J. (2007). Sox17 dependence distinguishes the transcriptional regulation of fetal from adult hematopoietic stem cells. Cell 130, 470-483.
25. Kissa, K. and Herbomel, P. (2010). Blood stem cells emerge from aortic endothelium by a novel type of cell transition. Nature 464, 112-115.
26. Kyba, M., Perlingeiro, R. C. and Daley, G. Q. (2002). HoxB4 confers definitive lymphoid-myeloid engraftment potential on embryonic stem cell and yolk sac hematopoietic progenitors. Cell 109, 29-37.
27. Ledran, M. H., Krassowska, A., Armstrong, L., Dimmick, I., Renstrom, J., Lang, R., Yung, S., Santibanez-Coref, M., Dzierzak, E., Stojkovic, M. et al. (2008). Efficient hematopoietic differentiation of human embryonic stem cells on stromal cells derived from hematopoietic niches. Cell Stem Cell 3, 85-98.
28. Lengerke, C., McKinney-Freeman, S., Naveiras, O., Yates, F., Wang, Y., Bansal, D. and Daley, G. Q. (2007). The Cdx-Hox pathway in hematopoietic stem cell formation from embryonic stem cells. Ann. NY Acad. Sci. 1106, 197-208.
29. Liao, W. P., Uetzmann, L., Burtscher, I. and Lickert, H. (2009). Generation of a mouse line expressing Sox17-driven cre recombinase with specific activity in arteries. Genesis 47, 476-483.
30. Liu, P., Wakamiya, M., Shea, M. J., Albrecht, U., Behringer, R. R. and Bradley, A. (1999). Requirement for Wnt3 in vertebrate axis formation. Nat. Genet. 22, 361-365. (Pubitemid 29369527)
31. Luche, H., Weber, O., Nageswara Rao, T., Blum, C. and Fehling, H. J. (2007). Faithful activation of an extra-bright red fluorescent protein in 'knock-in' cre-reporter mice ideally suited for lineage tracing studies. Eur. J. Immunol. 37, 43-53.
32. Lugus, J. J., Park, C., Ma, Y. D. and Choi, K. (2009). Both primitive and definitive blood cells are derived from Flk-1+ mesoderm. Blood 113, 563-566.
33. Matsui, T., Kanai-Azuma, M., Hara, K., Matoba, S., Hiramatsu, R., Kawakami, H., Kurohmaru, M., Koopman, P. and Kanai, Y. (2006). Redundant roles of Sox17 and Sox18 in postnatal angiogenesis in mice. J. Cell Sci. 119, 3513-3526.
34. McKinney-Freeman, S. L. and Daley, G. Q. (2007). Towards hematopoietic reconstitution from embryonic stem cells: a sanguine future. Curr. Opin. Hematol. 14, 343-347.
35. Medvinsky, A. and Dzierzak, E. (1996). Definitive hematopoiesis is autonomously initiated by the AGM region. Cell 86, 897-906.
36. Medvinsky, A. L., Samoylina, N. L., Muller, A. M. and Dzierzak, E. A. (1993). An early pre-liver intraembryonic source of CFU-S in the developing mouse. Nature 364, 64-67.
37. Medvinsky, A. L., Gan, O. I., Semenova, M. L. and Samoylina, N. L. (1996). Development of day-8 colony-forming unit-spleen hematopoietic progenitors during early murine embryogenesis: spatial and temporal mapping. Blood 87, 557-566.
38. Murry, C. E. and Keller, G. (2008). Differentiation of embryonic stem cells to clinically relevant populations: lessons from embryonic development. Cell 132, 661-680.
39. Nakano, T., Kodama, H. and Honjo, T. (1994). Generation of lymphohematopoietic cells from embryonic stem cells in culture. Science 265, 1098-1101.
40. Narayan, A. D., Chase, J. L., Lewis, R. L., Tian, X., Kaufman, D. S., Thomson, J. A. and Zanjani, E. D. (2006). Human embryonic stem cell-derived hematopoietic cells are capable of engrafting primary as well as secondary fetal sheep recipients. Blood 107, 2180-2183.
41. Ng, E. S., Azzola, L., Sourris, K., Robb, L., Stanley, E. G. and Elefanty, A. G. (2005). The primitive streak gene Mixl1 is required for efficient haematopoiesis and BMP4-induced ventral mesoderm patterning in differentiating ES cells. Development 132, 873-884.
42. North, T. E., de Bruijn, M. F., Stacy, T., Talebian, L., Lind, E., Robin, C., Binder, M., Dzierzak, E. and Speck, N. A. (2002). Runx1 expression marks long-term repopulating hematopoietic stem cells in the midgestation mouse embryo. Immunity 16, 661-672.
43. Nostro, M. C., Cheng, X., Keller, G. M. and 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, 60-71.
44. Palis, J., Roberston, S., Kennedy, M., Wall, C. and Keller, G. (1999). Development of erythroid and myeloid progenitors in the yolk sac and embryo proper of the mouse. Development 126, 5073-5084.
45. Pandolfi, P. P., Roth, M. E., Karis, A., Leonard, M. W., Dzierzak, E., Grosveld, F. G., Engel, J. D. and Lindenbaum, M. H. (1995). Targeted disruption of the GATA3 gene causes severe abnormalities in the nervous system and in fetal liver haematopoiesis. Nat. Genet. 11, 40-44.
46. Parameswaran, M. and Tam, P. P. (1995). Regionalisation of cell fate and morphogenetic movement of the mesoderm during mouse gastrulation. Dev. Genet. 17, 16-28.
47. Park, C., Afrikanova, I., Chung, Y. S., Zhang, W. J., Arentson, E., Fong Gh, G., Rosendahl, A. and Choi, K. (2004). A hierarchical order of factors in the generation of FLK1- and SCL-expressing hematopoietic and endothelial progenitors from embryonic stem cells. Development 131, 2749-2762.
48. Pearson, S., Sroczynska, P., Lacaud, G. and Kouskoff, V. (2008). The stepwise specification of embryonic stem cells to hematopoietic fate is driven by sequential exposure to Bmp4, Activin A, bFGF and VEGF. Development 135, 1525-1535. (Pubitemid 351753642)
49. Petrenko, O., Beavis, A., Klaine, M., Kittappa, R., Godin, I. and Lemischka, I. R. (1999). The molecular characterization of the fetal stem cell marker AA4. Immunity 10, 691-700.
50. Robb, L., Elwood, N. J., Elefanty, A. G., Köntgen, F., Li, R., Barnett, L. D. and Begley, C. G. (1996). The scl gene product is required for the generation of all hematopoietic lineages in the adult mouse. EMBO J. 15, 4123-4129.
51. Rubin, L. L. (2008). Stem cells and drug discovery: the beginning of a new era? Cell 132, 549-552.
52. Russell, E. S. (1979). Hereditary anemias of the mouse: a review for geneticists. Adv. Genet. 20, 357-459.
53. Samokhvalov, I. M., Samokhvalova, N. I. and Nishikawa, S. (2007). Cell tracing shows the contribution of the yolk sac to adult haematopoiesis. Nature 446, 1056-1061.
54. Schmitt, T. M. and Zuniga-Pflucker, J. C. (2002). Induction of T cell development from hematopoietic progenitor cells by delta-like-1 in vitro. Immunity 17, 749-756.
55. Schmitt, T. M., de Pooter, R. F., Gronski, M. A., Cho, S. K., Ohashi, P. S. and Zuniga-Pflucker, J. C. (2004). Induction of T cell development and establishment of T cell competence from embryonic stem cells differentiated in vitro. Nat. Immunol. 5, 410-417.
56. Shalaby, F., Ho, J., Stanford, W. L., Fischer, K. D., Schuh, A. C., Schwartz, L., Bernstein, A. and Rossant, J. (1997). A requirement for Flk1 in primitive and definitive hematopoiesis and vasculogenesis. Cell 89, 981-990.
57. Stadtfeld, M., Maherali, N., Breault, D. T. and Hochedlinger, K. (2008). Defining molecular cornerstones during fibroblast to iPS cell reprogramming in mouse. Cell Stem Cell 2, 230-240.
58. Tabatabaei-Zavareh, N., Vlasova, A., Greenwood, C. P. and Takei, F. (2007). Characterization of developmental pathway of natural killer cells from embryonic stem cells in vitro. PLoS ONE 2, e232.
59. Taoudi, S., Gonneau, C., Moore, K., Sheridan, J. M., Blackburn, C. C., Taylor, E. and Medvinsky, A. (2008). Extensive hematopoietic stem cell generation in the AGM region via maturation of VE-cadherin+CD45+ pre-definitive HSCs. Cell Stem Cell 3, 99-108.
60. Tian, X., Woll, P. S., Morris, J. K., Linehan, J. L. and Kaufman, D. S. (2006). Hematopoietic engraftment of human embryonic stem cell-derived cells is regulated by recipient innate immunity. Stem Cells 24, 1370-1380. (Pubitemid 44464705)
61. Timmermans, F., Velghe, I., Vanwalleghem, L., De Smedt, M., Van Coppernolle, S., Taghon, T., Moore, H. D., Leclercq, G., Langerak, A. W., Kerre, T. et al. (2009). Generation of T cells from human embryonic stem cell-derived hematopoietic zones. J. Immunol. 182, 6879-6888.
62. Vodyanik, M. A., Bork, J. A., Thomson, J. A. and Slukvin, I. I. (2005). Human embryonic stem cell-derived CD34+ cells: efficient production in the coculture with OP9 stromal cells and analysis of lymphohematopoietic potential. Blood 105, 617-626.
63. Wang, L., Li, L., Shojaei, F., Levac, K., Cerdan, C., Menendez, P., Martin, T., Rouleau, A. and Bhatia, M. (2004). Endothelial and hematopoietic cell fate of human embryonic stem cells originates from primitive endothelium with hemangioblastic properties. Immunity 21, 31-41.
64. Wang, L., Menendez, P., Cerdan, C. and Bhatia, M. (2005a). Hematopoietic development from human embryonic stem cell lines. Exp. Hematol. 33, 987-996.
65. Wang, Q., Stacy, T., Binder, M., Marin-Padilla, M., Sharpe, A. H. and Speck, N. A. (1996). Disruption of the Cbfa2 gene causes necrosis and hemorrhaging in the central nervous system and blocks definitive hematopoiesis. Proc. Natl. Acad. Sci. USA 93, 3444-3449.
66. Wang, Y., Yates, F., Naveiras, O., Ernst, P. and Daley, G. Q. (2005b). Embryonic stem cell-derived hematopoietic stem cells. Proc. Natl. Acad. Sci. USA 102, 19081-19086.
67. Winnier, G., Blessing, M., Labosky, P. A. and Hogan, B. L. (1995). Bone morphogenetic protein-4 is required for mesoderm formation and patterning in the mouse. Genes Dev. 9, 2105-2116.
68. Yamane, T., Hosen, N., Yamazaki, H. and Weissman, I. L. (2009). Expression of AA4.1 marks lymphohematopoietic progenitors in early mouse development. Proc. Natl. Acad. Sci. USA 106, 8953-8958.
69. Yoder, M. C., Hiatt, K., Dutt, P., Mukherjee, P., Bodine, D. M. and Orlic, D. (1997). Characterization of definitive lymphohematopoietic stem cells in the day 9 murine yolk sac. Immunity 7, 335-344. (Pubitemid 27446008)