In vivo repopulating activity emerges at the onset of hematopoietic specification during embryonic stem cell differentiation

Stem Cell Reports

Volumn 4, Issue 3, 2015, Pages 431-444

  Pearson, Stella ^a   Cuvertino, Sara ^a   Fleury, Maud ^a   Lacaud, Georges ^a   Kouskoff, Valerie ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVIN A; BONE MORPHOGENETIC PROTEIN 4; CYTOKINE; FIBROBLAST GROWTH FACTOR 2; VASCULOTROPIN; ACTIVIN; FIBROBLAST GROWTH FACTOR; GLYCOPROTEIN IIB; STEM CELL FACTOR RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL CLONING; CELL DIFFERENTIATION; CELL LINEAGE; CELL POPULATION; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; EMBRYONIC STEM CELL; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; IMMUNOPHENOTYPING; IN VITRO STUDY; IN VIVO STUDY; MALE; MESODERMAL CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; STEM CELL CULTURE; ANIMAL; CYTOLOGY; DRUG EFFECTS; GENETICS; METABOLISM; PHENOTYPE; STEM CELL TRANSPLANTATION; TRANSGENIC MOUSE;

ACTIVINS; ANIMALS; BONE MORPHOGENETIC PROTEIN 4; CELL DIFFERENTIATION; CYTOKINES; EMBRYONIC STEM CELLS; FIBROBLAST GROWTH FACTORS; HEMATOPOIESIS; HEMATOPOIETIC STEM CELLS; IMMUNOPHENOTYPING; MALE; MICE; MICE, TRANSGENIC; PHENOTYPE; PLATELET MEMBRANE GLYCOPROTEIN IIB; PROTO-ONCOGENE PROTEINS C-KIT; STEM CELL TRANSPLANTATION; VASCULAR ENDOTHELIAL GROWTH FACTORS;

EID: 84924593916     PISSN: 22136711     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.stemcr.2015.01.003     Document Type: Article

References (60)

1. J.Y. Bertrand, N.C. Chi, B. Santoso, S. Teng, D.Y. Stainier, and D. Traver Haematopoietic stem cells derive directly from aortic endothelium during development Nature 464 2010 108 111
2. J.C. Boisset, W. van Cappellen, C. Andrieu-Soler, N. Galjart, E. Dzierzak, and C. Robin In vivo imaging of haematopoietic cells emerging from the mouse aortic endothelium Nature 464 2010 116 120
3. S. Bonde, A.M. Dowden, K.M. Chan, W.B. Tabayoyong, and N. Zavazava HOXB4 but not BMP4 confers self-renewal properties to ES-derived hematopoietic progenitor cells Transplantation 86 2008 1803 1809
4. C.E. Burns, D. Traver, E. Mayhall, J.L. Shepard, and L.I. Zon Hematopoietic stem cell fate is established by the Notch-Runx pathway Genes Dev. 19 2005 2331 2342
5. R.K. Burt, L. Verda, D.A. Kim, Y. Oyama, K. Luo, and C. Link Embryonic stem cells as an alternate marrow donor source: engraftment without graft-versus-host disease J. Exp. Med. 199 2004 895 904
6. A.E. Chen, M. Borowiak, R.I. Sherwood, A. Kweudjeu, and D.A. Melton Functional evaluation of ES cell-derived endodermal populations reveals differences between Nodal and Activin A-guided differentiation Development 140 2013 675 686
7. K. Choi, M. Kennedy, A. Kazarov, J.C. Papadimitriou, and G. Keller A common precursor for hematopoietic and endothelial cells Development 125 1998 725 732
8. K.D. Choi, M.A. Vodyanik, P.P. Togarrati, K. Suknuntha, A. Kumar, F. Samarjeet, M.D. Probasco, S. Tian, R. Stewart, J.A. Thomson, and I.I. Slukvin Identification of the hemogenic endothelial progenitor and its direct precursor in human pluripotent stem cell differentiation cultures Cell Rep. 2 2012 553 567
9. G. Costa, V. Kouskoff, and G. Lacaud Origin of blood cells and HSC production in the embryo Trends Immunol. 33 2012 215 223
10. T.C. Doetschman, H. Eistetter, M. Katz, W. Schmidt, and R. Kemler 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 1985 27 45
11. S. Doulatov, L.T. Vo, S.S. Chou, P.G. Kim, N. Arora, H. Li, B.K. Hadland, I.D. Bernstein, J.J. Collins, L.I. Zon, and G.Q. Daley Induction of multipotential hematopoietic progenitors from human pluripotent stem cells via respecification of lineage-restricted precursors Cell Stem Cell 13 2013 459 470
12. H.M. Eilken, S. Nishikawa, and T. Schroeder Continuous single-cell imaging of blood generation from haemogenic endothelium Nature 457 2009 896 900
13. M. Ema, T. Yokomizo, A. Wakamatsu, T. Terunuma, M. Yamamoto, and S. Takahashi Primitive erythropoiesis from mesodermal precursors expressing VE-cadherin, PECAM-1, Tie2, endoglin, and CD34 in the mouse embryo Blood 108 2006 4018 4024
14. H.J. Fehling, G. Lacaud, A. Kubo, M. Kennedy, S. Robertson, G. Keller, and V. Kouskoff Tracking mesoderm induction and its specification to the hemangioblast during embryonic stem cell differentiation Development 130 2003 4217 4227
15. M.J. Ferkowicz, M. Starr, X. Xie, W. Li, S.A. Johnson, W.C. Shelley, P.R. Morrison, and M.C. Yoder CD41 expression defines the onset of primitive and definitive hematopoiesis in the murine embryo Development 130 2003 4393 4403
16. L. Grabel Prospects for pluripotent stem cell therapies: into the clinic and back to the bench J. Cell. Biochem. 113 2012 381 387
17. N. Hole, G.J. Graham, U. Menzel, and J.D. Ansell A limited temporal window for the derivation of multilineage repopulating hematopoietic progenitors during embryonal stem cell differentiation in vitro Blood 88 1996 1266 1276
18. T.L. Huber, V. Kouskoff, H.J. Fehling, J. Palis, and G. Keller Haemangioblast commitment is initiated in the primitive streak of the mouse embryo Nature 432 2004 625 630
19. S. Irion, R.L. Clarke, H. Luche, I. Kim, S.J. Morrison, H.J. Fehling, and G.M. Keller Temporal specification of blood progenitors from mouse embryonic stem cells and induced pluripotent stem cells Development 137 2010 2829 2839
20. M.D. Kardel, and C.J. Eaves Modeling human hematopoietic cell development from pluripotent stem cells Exp. Hematol. 40 2012 601 611
21. G. Keller Embryonic stem cell differentiation: emergence of a new era in biology and medicine Genes Dev. 19 2005 1129 1155
22. G. Keller, M. Kennedy, T. Papayannopoulou, and M.V. Wiles Hematopoietic commitment during embryonic stem cell differentiation in culture Mol. Cell. Biol. 13 1993 473 486
23. M. Kennedy, S.L. D'Souza, M. Lynch-Kattman, S. Schwantz, and G. Keller Development of the hemangioblast defines the onset of hematopoiesis in human ES cell differentiation cultures Blood 109 2007 2679 2687
24. M. Kennedy, G. Awong, C.M. Sturgeon, A. Ditadi, R. LaMotte-Mohs, J.C. Zúñiga-Pflücker, and G. Keller T lymphocyte potential marks the emergence of definitive hematopoietic progenitors in human pluripotent stem cell differentiation cultures Cell Rep. 2 2012 1722 1735
25. K. Kissa, and P. Herbomel Blood stem cells emerge from aortic endothelium by a novel type of cell transition Nature 464 2010 112 115
26. K. Kitajima, K. Minehata, K. Sakimura, T. Nakano, and T. Hara In vitro generation of HSC-like cells from murine ESCs/iPSCs by enforced expression of LIM-homeobox transcription factor Lhx2 Blood 117 2011 3748 3758
27. S. Kriks, J.W. Shim, J. Piao, Y.M. Ganat, D.R. Wakeman, Z. Xie, L. Carrillo-Reid, G. Auyeung, C. Antonacci, and A. Buch Dopamine neurons derived from human ES cells efficiently engraft in animal models of Parkinson's disease Nature 480 2011 547 551
28. M. Kyba, R.C. Perlingeiro, and G.Q. Daley HoxB4 confers definitive lymphoid-myeloid engraftment potential on embryonic stem cell and yolk sac hematopoietic progenitors Cell 109 2002 29 37
29. C. Lancrin, P. Sroczynska, C. Stephenson, T. Allen, V. Kouskoff, and G. Lacaud The haemangioblast generates haematopoietic cells through a haemogenic endothelium stage Nature 457 2009 892 895
30. C. Lancrin, P. Sroczynska, A.G. Serrano, A. Gandillet, C. Ferreras, V. Kouskoff, and G. Lacaud Blood cell generation from the hemangioblast J. Mol. Med. 88 2010 167 172
31. M.H. Ledran, A. Krassowska, L. Armstrong, I. Dimmick, J. Renström, R. Lang, S. Yung, M. Santibanez-Coref, E. Dzierzak, and M. Stojkovic Efficient hematopoietic differentiation of human embryonic stem cells on stromal cells derived from hematopoietic niches Cell Stem Cell 3 2008 85 98
32. D.A. Lesinski, N. Heinz, S. Pilat-Carotta, C. Rudolph, R. Jacobs, B. Schlegelberger, H. Klump, and B. Schiedlmeier Serum- and stromal cell-free hypoxic generation of embryonic stem cell-derived hematopoietic cells in vitro, capable of multilineage repopulation of immunocompetent mice Stem Cells Transl. Med. 1 2012 581 591
33. Y. Lin, M.C. Yoder, and M. Yoshimoto Lymphoid progenitor emergence in the murine embryo and yolk sac precedes stem cell detection Stem Cells Dev. 23 2014 1168 1177
34. R. Lis, S. Rafii, and D. James Wading through the waves of human embryonic hemogenesis Cell Cycle 12 2013 859 860
35. K. Matsumoto, T. Isagawa, T. Nishimura, T. Ogaeri, K. Eto, S. Miyazaki, J. Miyazaki, H. Aburatani, H. Nakauchi, and H. Ema Stepwise development of hematopoietic stem cells from embryonic stem cells PLoS ONE 4 2009 e4820
36. S.L. McKinney-Freeman, O. Naveiras, F. Yates, S. Loewer, M. Philitas, M. Curran, P.J. Park, and G.Q. Daley Surface antigen phenotypes of hematopoietic stem cells from embryos and murine embryonic stem cells Blood 114 2009 268 278
37. A. Medvinsky, and E. Dzierzak Definitive hematopoiesis is autonomously initiated by the AGM region Cell 86 1996 897 906
38. H.K. Mikkola, Y. Fujiwara, T.M. Schlaeger, D. Traver, and S.H. Orkin Expression of CD41 marks the initiation of definitive hematopoiesis in the mouse embryo Blood 101 2003 508 516
39. V. Moignard, S. Woodhouse, J. Fisher, and B. Göttgens Transcriptional hierarchies regulating early blood cell development Blood Cells Mol. Dis. 51 2013 239 247
40. E. Montecino-Rodriguez, and K. Dorshkind B-1 B cell development in the fetus and adult Immunity 36 2012 13 21
41. A.M. Müller, and E.A. Dzierzak ES cells have only a limited lymphopoietic potential after adoptive transfer into mouse recipients Development 118 1993 1343 1351
42. S.I. Nishikawa, S. Nishikawa, M. Hirashima, N. Matsuyoshi, and H. Kodama Progressive lineage analysis by cell sorting and culture identifies FLK1+VE-cadherin+ cells at a diverging point of endothelial and hemopoietic lineages Development 125 1998 1747 1757
43. J. Palis, S. Robertson, M. Kennedy, C. Wall, and G. Keller Development of erythroid and myeloid progenitors in the yolk sac and embryo proper of the mouse Development 126 1999 5073 5084
44. S. Pearson, P. Sroczynska, G. Lacaud, and V. Kouskoff The stepwise specification of embryonic stem cells to hematopoietic fate is driven by sequential exposure to Bmp4, activin A, bFGF and VEGF Development 135 2008 1525 1535
45. S. Pearson, C. Lancrin, G. Lacaud, and V. Kouskoff The sequential expression of CD40 and Icam2 defines progressive steps in the formation of blood precursors from the mesoderm germ layer Stem Cells 28 2010 1089 1098
46. J.E. Pimanda, I.J. Donaldson, M.F. de Bruijn, S. Kinston, K. Knezevic, L. Huckle, S. Piltz, J.R. Landry, A.R. Green, D. Tannahill, and B. Göttgens The SCL transcriptional network and BMP signaling pathway interact to regulate RUNX1 activity Proc. Natl. Acad. Sci. USA 104 2007 840 845
47. A.J. Potocnik, H. Kohler, and K. Eichmann Hemato-lymphoid in vivo reconstitution potential of subpopulations derived from in vitro differentiated embryonic stem cells Proc. Natl. Acad. Sci. USA 94 1997 10295 10300
48. S. Rafii, C.C. Kloss, J.M. Butler, M. Ginsberg, E. Gars, R. Lis, Q. Zhan, P. Josipovic, B.S. Ding, and J. Xiang Human ESC-derived hemogenic endothelial cells undergo distinct waves of endothelial to hematopoietic transition Blood 121 2013 770 780
49. D. Ran, W.J. Shia, M.C. Lo, J.B. Fan, D.A. Knorr, P.I. Ferrell, Z. Ye, M. Yan, L. Cheng, D.S. Kaufman, and D.E. Zhang RUNX1a enhances hematopoietic lineage commitment from human embryonic stem cells and inducible pluripotent stem cells Blood 121 2013 2882 2890
50. C. Robin, K. Ottersbach, J.C. Boisset, A. Oziemlak, and E. Dzierzak CD41 is developmentally regulated and differentially expressed on mouse hematopoietic stem cells Blood 117 2011 5088 5091
51. S. Rybtsov, M. Sobiesiak, S. Taoudi, C. Souilhol, J. Senserrich, A. Liakhovitskaia, A. Ivanovs, J. Frampton, S. Zhao, and A. Medvinsky Hierarchical organization and early hematopoietic specification of the developing HSC lineage in the AGM region J. Exp. Med. 208 2011 1305 1315
52. Y. Shiba, S. Fernandes, W.Z. Zhu, D. Filice, V. Muskheli, J. Kim, N.J. Palpant, J. Gantz, K.W. Moyes, and H. Reinecke Human ES-cell-derived cardiomyocytes electrically couple and suppress arrhythmias in injured hearts Nature 489 2012 322 325
53. I.I. Slukvin Hematopoietic specification from human pluripotent stem cells: current advances and challenges toward de novo generation of hematopoietic stem cells Blood 122 2013 4035 4046
54. C.M. Sturgeon, A. Ditadi, R.L. Clarke, and G. Keller Defining the path to hematopoietic stem cells Nat. Biotechnol. 31 2013 416 418
55. L. Wang, L. Li, F. Shojaei, K. Levac, C. Cerdan, P. Menendez, T. Martin, A. Rouleau, and M. Bhatia Endothelial and hematopoietic cell fate of human embryonic stem cells originates from primitive endothelium with hemangioblastic properties Immunity 21 2004 31 41
56. L. Wang, P. Menendez, F. Shojaei, L. Li, F. Mazurier, J.E. Dick, C. Cerdan, K. Levac, and M. Bhatia Generation of hematopoietic repopulating cells from human embryonic stem cells independent of ectopic HOXB4 expression J. Exp. Med. 201 2005 1603 1614
57. Y. Wang, F. Yates, O. Naveiras, P. Ernst, and G.Q. Daley Embryonic stem cell-derived hematopoietic stem cells Proc. Natl. Acad. Sci. USA 102 2005 19081 19086
58. R. Yamamoto, Y. Morita, J. Ooehara, S. Hamanaka, M. Onodera, K.L. Rudolph, H. Ema, and H. Nakauchi Clonal analysis unveils self-renewing lineage-restricted progenitors generated directly from hematopoietic stem cells Cell 154 2013 1112 1126
59. L. Yang, M.H. Soonpaa, E.D. Adler, T.K. Roepke, S.J. Kattman, M. Kennedy, E. Henckaerts, K. Bonham, G.W. Abbott, and R.M. Linden Human cardiovascular progenitor cells develop from a KDR+ embryonic-stem-cell-derived population Nature 453 2008 524 528
60. A.C. Zovein, J.J. Hofmann, M. Lynch, W.J. French, K.A. Turlo, Y. Yang, M.S. Becker, L. Zanetta, E. Dejana, and J.C. Gasson Fate tracing reveals the endothelial origin of hematopoietic stem cells Cell Stem Cell 3 2008 625 636