An in vitro model of hemogenic endothelium commitment and hematopoietic production

Development (Cambridge)

Volumn 143, Issue 8, 2016, Pages 1302-1312

  Yvernogeau, Laurent ^a,b,c   Gautier, Rodolphe ^a,b   Khoury, Hanane ^a,b   Menegatti, Sara ^a,b,d   Schmidt, Melanie ^a,b   Gilles, Jean Francois ^a   Jaffredo, Thierry ^a,b  

^a SORBONNE UNIVERSITÉ   (France)

^b Sorbonne Universités   (France)

^c HUBRECHT INSTITUTE   (Netherlands)

^d UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Aorta; Avian; Endothelium; Hematopoiesis; Hemogenic endothelium; Quail

Indexed keywords

ANIMAL CELL; ANIMAL TISSUE; AORTA; ARTICLE; BLOOD CELL; CELL CULTURE; CELL TRANSFORMATION; COTURNIX JAPONICA; EMBRYO; ENDOTHELIAL TO HEMATOPOIETIC TRANSITION; ENDOTHELIUM CELL; HEMANGIOBLAST; IN VITRO STUDY; MESODERM; NONHUMAN; PRIORITY JOURNAL; SMOOTH MUSCLE CELL; ANIMAL; CELL ADHESION; CELL CULTURE TECHNIQUE; COTURNIX; CULTURE MEDIUM; CYTOLOGY; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; VASCULAR ENDOTHELIUM;

CULTURE MEDIUM; TRANSCRIPTOME;

ANIMALS; CELL ADHESION; CELL CULTURE TECHNIQUES; COTURNIX; CULTURE MEDIA; ENDOTHELIUM, VASCULAR; HEMANGIOBLASTS; HEMATOPOIESIS; HEMATOPOIETIC STEM CELLS; MESODERM; TRANSCRIPTOME;

EID: 84964270341     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.126714     Document Type: Article

References (48)

1. Asahara, T., Bauters, C., Zheng, L. P., Takeshita, S., Bunting, S., Ferrara, N., Symes, J. F. and Isner, J. M. (1995). Synergistic effect of vascular endothelial growth factor and basic fibroblast growth factor on angiogenesis in vivo. Circulation 92, 365-371.
2. Bertrand, J. Y., Chi, N. C., Santoso, B., Teng, S., Stainier, D. Y. R. 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. Chen, M. J., Yokomizo, T., Zeigler, B. M., Dzierzak, E. and Speck, N. A. (2009). Runx1 is required for the endothelial to haematopoietic cell transition but not thereafter. Nature 457, 887-891.
5. 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.
6. Christ, B., Huang, R. and Scaal, M. (2007). Amniote somite derivatives. Dev. Dyn. 236, 2382-2396.
7. de Bruijn, M. F. T. R., 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.
8. De Val, S. and Black, B. L. (2009). Transcriptional control of endothelial cell development. Dev. Cell 16, 180-195.
9. Ditadi, A., Sturgeon, C. M., Tober, J., Awong, G., Kennedy, M., Yzaguirre, A. D., Azzola, L., Ng, E. S., Stanley, E. G., French, D. L. et al. (2015). Human definitive haemogenic endothelium and arterial vascular endothelium represent distinct lineages. Nat. Cell Biol. 17, 580-591.
10. Dzierzak, E. and Speck, N. A. (2008). Of lineage and legacy: the development of mammalian hematopoietic stem cells. Nat. Immunol. 9, 129-136.
11. Eilken, H. M., Nishikawa, S.-I. and Schroeder, T. (2009). Continuous single-cell imaging of blood generation from haemogenic endothelium. Nature 457, 896-900
12. Elefanty, A. G., Robb, L., Birner, R. and Begley, C. G. (1997). Hematopoietic-specific genes are not induced during in vitro differentiation of scl-null embryonic stem cells. Blood 90, 1435-1447.
13. Guo, R., Sakamoto, H., Sugiura, S. and Ogawa, M. (2007). Endothelial cell motility is compatible with junctional integrity. J. Cell. Physiol. 211, 327-335.
14. Hirashima, M., Ogawa, M., Nishikawa, S., Matsumura, K., Kawasaki, K., Shibuya, M. and Nishikawa, S.-I. (2003). A chemically defined culture of VEGFR2+ cells derived from embryonic stem cells reveals the role of VEGFR1 in tuning the threshold for VEGF in developing endothelial cells. Blood 101, 2261-2267.
15. Huang, G., Zhang, P., Hirai, H., Elf, S., Yan, X., Chen, Z., Koschmieder, S., Okuno, Y., Dayaram, T., Growney, J. D. et al. (2008). PU.1 is a major downstream target of AML1 (RUNX1) in adult mouse hematopoiesis. Nat. Genet. 40, 51-60.
16. Huber, T. L., Kouskoff, V., Fehling, H. J., Palis, J. and Keller, G. (2004). Haemangioblast commitment is initiated in the primitive streak of the mouse embryo. Nature 432, 625-630.
17. Jaffredo, T., Gautier, R., Eichmann, A. and Dieterlen-Lievre, F. (1998). Intraaortic hemopoietic cells are derived from endothelial cells during ontogeny. Development 125, 4575-4583.
18. Jaffredo, T., Bollerot, K., Sugiyama, D., Gautier, R. and Drevon, C. (2005a). Tracing the hemangioblast during embryogenesis: developmental relationships between endothelial and hematopoietic cells. Int. J. Dev. Biol. 49, 269-277
19. Jaffredo, T., Nottingham, W., Liddiard, K., Bollerot, K., Pouget, C. and de Bruijn, M. (2005b). From hemangioblast to hematopoietic stem cell: an endothelial connection? Exp. Hematol. 33, 1029-1040.
20. Kispert, A., Ortner, H., Cooke, J. and Herrmann, B. G. (1995). The chick Brachyury gene: developmental expression pattern and response to axial induction by localized activin. Dev. Biol. 168, 406-415.
21. Kissa, K. and Herbomel, P. (2010). Blood stem cells emerge from aortic endothelium by a novel type of cell transition. Nature 464, 112-115
22. Lam, E. Y. N., Hall, C. J., Crosier, P. S., Crosier, K. E. and Flores, M. V. (2010). Live imaging of Runx1 expression in the dorsal aorta tracks the emergence of blood progenitors from endothelial cells. Blood 116, 909-914.
23. Lamalice, L., Le Boeuf, F. and Huot, J. (2007). Endothelial cell migration during angiogenesis. Circ. Res. 100, 782-794.
24. Lancrin, C., Sroczynska, P., Stephenson, C., Allen, T., Kouskoff, V. and Lacaud, G. (2009). The haemangioblast generates haematopoietic cells through a haemogenic endothelium stage. Nature 457, 892-895.
25. Lancrin, C., Sroczynska, P., Serrano, A. G., Gandillet, A., Ferreras, C., Kouskoff, V. and Lacaud, G. (2010). Blood cell generation from the hemangioblast. J. Mol. Med. 88, 167-172.
26. Medvinsky, A., Rybtsov, S. and Taoudi, S. (2011). Embryonic origin of the adult hematopoietic system: advances and questions. Development 138, 1017-1031
27. Newman, P. J., Berndt, M. C., Gorski, J., White, G. C., 2nd, Lyman, S., Paddock, C. and Muller, W. A. (1990). PECAM-1 (CD31) cloning and relation to adhesion molecules of the immunoglobulin gene superfamily. Science 247, 1219-1222
28. North, T. E., de Bruijn, M. F. T. R., 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.
29. Pardanaud, L. and Dieterlen-Lievre, F. (1999). Manipulation of the angiopoietic/ hemangiopoietic commitment in the avian embryo. Development 126, 617-627
30. Pardanaud, L., Altmann, C., Kitos, P., Dieterlen-Lievre, F. and Buck, C. A. (1987). Vasculogenesis in the early quail blastodisc as studied with a monoclonal antibody recognizing endothelial cells. Development 100, 339-349.
31. Pardanaud, L., Luton, D., Prigent, M., Bourcheix, L.-M., Catala, M. and Dieterlen-Lievre, F. (1996). Two distinct endothelial lineages in ontogeny, one of them related to hemopoiesis. Development 122, 1363-1371.
32. Pepper, M. S., Ferrara, N., Orci, L. and Montesano, R. (1992). Potent synergism between vascular endothelial growth factor and basic fibroblast growth factor in the induction of angiogenesis in vitro. Biochem. Biophys. Res. Commun. 189, 824-831.
33. Pouget, C., Gautier, R., Teillet, M.-A. and Jaffredo, T. (2006). Somite-derived cells replace ventral aortic hemangioblasts and provide aortic smooth muscle cells of the trunk. Development 133, 1013-1022.
34. Pourquie, O. (2003). Vertebrate somitogenesis: a novel paradigm for animal segmentation? Int. J. Dev. Biol. 47, 597-603.
35. Richard, C., Drevon, C., Canto, P.-Y., Villain, G., Bollerot, K., Lempereur, A., Teillet, M.-A., Vincent, C., Rossello Castillo, C., Torres, M. et al. (2013). Endothelio-mesenchymal interaction controls runx1 expression and modulates the notch pathway to initiate aortic hematopoiesis. Dev. Cell 24, 600-611.
36. Robertson, S. M., Kennedy, M., Shannon, J. M. and Keller, G. (2000). A transitional stage in the commitment of mesoderm to hematopoiesis requiring the transcription factor SCL/tal-1. Development 127, 2447-2459.
37. Seghezzi, G., Patel, S., Ren, C. J., Gualandris, A., Pintucci, G., Robbins, E. S., Shapiro, R. L., Galloway, A. C., Rifkin, D. B. and Mignatti, P. (1998). Fibroblast growth factor-2 (FGF-2) induces vascular endothelial growth factor (VEGF) expression in the endothelial cells of forming capillaries: an autocrine mechanism contributing to angiogenesis. J. Cell Biol. 141, 1659-1673.
38. Swiers, G., Baumann, C., O’Rourke, J., Giannoulatou, E., Taylor, S., Joshi, A., Moignard, V., Pina, C., Bee, T., Kokkaliaris, K. D. et al. (2013). Early dynamic fate changes in haemogenic endothelium characterized at the single-cell level. Nat. Commun. 4, 2924
39. Tavian, M., Coulombel, L., Luton, D., San Clemente, H., Dieterlen-Lievre, F. and Peault, B. (1996). Aorta-associated CD34+ hematopoietic cells in the early human embryo. Blood 87, 67-72.
40. Vogeli, K. M., Jin, S.-W., Martin, G. R. and Stainier, D. Y. R. (2006). A common progenitor for haematopoietic and endothelial lineages in the zebrafish gastrula. Nature 443, 337-339.
41. Wagner, D. D., Olmsted, J. B. and Marder, V. J. (1982). Immunolocalization of von Willebrand protein in Weibel-Palade bodies of human endothelial cells. J. Cell Biol. 95, 355-360.
42. Whelan, M. C. and Senger, D. R. (2003). Collagen I initiates endothelial cell morphogenesis by inducing actin polymerization through suppression of cyclic AMP and protein kinase A. J. Biol. Chem. 278, 327-334.
43. Wilkinson, D. G., Bhatt, S. and Herrmann, B. G. (1990). Expression pattern of the mouse T gene and its role in mesoderm formation. Nature 343, 657-659.
44. Wood, H. B., May, G., Healy, L., Enver, T. and Morriss-Kay, G. M. (1997). CD34 expression patterns during early mouse development are related to modes of blood vessel formation and reveal additional sites of hematopoiesis. Blood 90, 2300-2311.
45. Yokomizo, T. and Dzierzak, E. (2010). Three-dimensional cartography of hematopoietic clusters in the vasculature of whole mouse embryos. Development 137, 3651-3661.
46. Yvernogeau, L., Auda-Boucher, G. and Fontaine-Perus, J. (2012). Limb bud colonization by somite-derived angioblasts is a crucial step for myoblast emigration. Development 139, 277-287.
47. Zape, J. P. and Zovein, A. C. (2011). Hemogenic endothelium: origins, regulation, and implications for vascular biology. Semin. Cell Dev. Biol. 22, 1036-1047.
48. Zovein, A. C., Hofmann, J. J., Lynch, M., French, W. J., Turlo, K. A., Yang, Y., Becker, M. S., Zanetta, L., Dejana, E., Gasson, J. C. et al. (2008). Fate tracing reveals the endothelial origin of hematopoietic stem cells. Cell Stem Cell 3, 625-636