Immature hematopoietic stem cells undergo maturation in the fetal liver

Development (Cambridge)

Volumn 139, Issue 19, 2012, Pages 3521-3530

  Kieusseian, Aurelie ^a   de la Grange, Philippe Brunet ^b   Burlen Defranoux, Odile ^a   Godin, Isabelle ^c   Cumano, Ana ^a  

^a INSTITUT PASTEUR   (France)

^b Universite Paris Sud   (France)

^c INSERM   (France)

Author keywords

Fetal liver; Hematopoietic reconstitution; Hematopoietic stem cells; MHC class I

Indexed keywords

CD45 ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; STROMAL CELL DERIVED FACTOR 1; THROMBOPOIETIN;

ANIMAL CELL; ARTICLE; CELL CULTURE; CELL MATURATION; CONTROLLED STUDY; ENGRAFTMENT; FETUS; HEMATOPOIETIC STEM CELL; LIVER CELL; NONHUMAN; ORGAN CULTURE; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; DNA-BINDING PROTEINS; FEMALE; FETUS; HEMATOPOIESIS; HEMATOPOIETIC STEM CELLS; KILLER CELLS, NATURAL; LIVER; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PREGNANCY;

MUS;

EID: 84865850027     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.079210     Document Type: Article

References (32)

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.
2. Cardier, J. E. and Dempsey, J. (1998). Thrombopoietin and its receptor, c-mpl, are constitutively expressed by mouse liver endothelial cells: evidence of thrombopoietin as a growth factor for liver endothelial cells. Blood 91, 923-929.
3. Colucci, F., Soudais, C., Rosmaraki, E., Vanes, L., Tybulewicz, V. L. and Di Santo, J. P. (1999). Dissecting NK cell development using a novel alymphoid mouse model: investigating the role of the c-abl proto-oncogene in murine NK cell differentiation. J. Immunol. 162, 2761-2765.
4. 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.
5. 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.
6. Dussault, I. and Miller, S. C. (1995). Suppression of natural killer cell activity in infant mice occurs after target cell binding. Nat. Immun. 14, 35-43.
7. Godin, I., Dieterlen-Lièvre, F. and Cumano, A. (1995). Emergence of multipotent hemopoietic cells in the yolk sac and paraaortic splanchnopleura in mouse embryos, beginning at 8.5 days postcoitus. Proc. Natl. Acad. Sci. USA 92, 773-777.
8. Godin, I., Garcia-Porrero, J. A., Dieterlen-Lièvre, F. and Cumano, A. (1999). Stem cell emergence and hemopoietic activity are incompatible in mouse intraembryonic sites. J. Exp. Med. 190, 43-52.
9. Houssaint, E. (1981). Differentiation of the mouse hepatic primordium. II. Extrinsic origin of the haemopoietic cell line. Cell Differ. 10, 243-252.
10. Jaffe, L., Robertson, E. J. and Bikoff, E. K. (1991). Distinct patterns of expression of MHC class I and beta 2-microglobulin transcripts at early stages of mouse development. J. Immunol. 147, 2740-2749.
11. Kent, D. G., Copley, M. R., Benz, C., Wöhrer, S., Dykstra, B. J., Ma, E., Cheyne, J., Zhao, Y., Bowie, M. B., Zhao, Y. et al. (2009). Prospective isolation and molecular characterization of hematopoietic stem cells with durable self-renewal potential. Blood 113, 6342-6350.
12. Kiel, M. J., Yilmaz, O. H., Iwashita, T., Yilmaz, O. H., Terhorst, C. and Morrison, S. J. (2005). SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell 121, 1109-1121.
13. Kim, I., He, S., Yilmaz, O. H., Kiel, M. J. and Morrison, S. J. (2006). Enhanced purification of fetal liver hematopoietic stem cells using SLAM family receptors. Blood 108, 737-744.
14. Kimura, S., Roberts, A. W., Metcalf, D. and Alexander, W. S. (1998). Hematopoietic stem cell deficiencies in mice lacking c-Mpl, the receptor for thrombopoietin. Proc. Natl. Acad. Sci. USA 95, 1195-1200.
15. Lux, C. T., Yoshimoto, M., McGrath, K., Conway, S. J., Palis, J. and 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, 3435-3438.
16. Matsumoto, K., Isagawa, T., Nishimura, T., Ogaeri, T., Eto, K., Miyazaki, S., Miyazaki, J., Aburatani, H., Nakauchi, H. and Ema, H. (2009). Stepwise development of hematopoietic stem cells from embryonic stem cells', PLoS ONE 4, e4820.
17. Medvinsky, A. and Dzierzak, E. (1996). Definitive hematopoiesis is autonomously initiated by the AGM region. Cell 86, 897-906.
18. Medvinsky, A. L. and Dzierzak, E. A. (1998). Development of the definitive hematopoietic hierarchy in the mouse. Dev. Comp. Immunol. 22, 289-301.
19. Müller, A. M., Medvinsky, A., Strouboulis, J., Grosveld, F. and Dzierzak, E. (1994). Development of hematopoietic stem cell activity in the mouse embryo. Immunity 1, 291-301.
20. Palis, J., Robertson, 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.
21. Petit-Cocault, L., Volle-Challier, C., Fleury, M., Péault, B. and Souyri, M. (2007). Dual role of Mpl receptor during the establishment of definitive hematopoiesis. Development 134, 3031-3040.
22. Qian, H., Buza-Vidas, N., Hyland, C. D., Jensen, C. T., Antonchuk, J., Månsson, R., Thoren, L. A., Ekblom, M., Alexander, W. S. and Jacobsen, S. E. (2007). Critical role of thrombopoietin in maintaining adult quiescent hematopoietic stem cells. Cell Stem Cell 1, 671-684.
23. Rybtsov, S., Sobiesiak, M., Taoudi, S., Souilhol, C., Senserrich, J., Liakhovitskaia, A., Ivanovs, A., Frampton, J., Zhao, S. and Medvinsky, A. (2011). Hierarchical organization and early hematopoietic specification of the developing HSC lineage in the AGM region. J. Exp. Med. 208, 1305-1315.
24. 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.
25. Sánchez, M. J., Holmes, A., Miles, C. and Dzierzak, E. (1996). Characterization of the first definitive hematopoietic stem cells in the AGM and liver of the mouse embryo. Immunity 5, 513-525.
26. Shinkai, Y., Rathbun, G., Lam, K. P., Oltz, E. M., Stewart, V., Mendelsohn, M., Charron, J., Datta, M., Young, F., Stall, A. M. et al. (1992). RAG-2-deficient mice lack mature lymphocytes owing to inability to initiate V(D)J rearrangement. Cell 68, 855-867.
27. 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.
28. Weksberg, D. C., Chambers, S. M., Boles, N. C. and Goodell, M. A. (2008). CD150-side population cells represent a functionally distinct population of longterm hematopoietic stem cells. Blood 111, 2444-2451.
29. 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.
30. Yokota, T., Huang, J., Tavian, M., Nagai, Y., Hirose, J., Zúñiga-Pflücker, J. C., Péault, B. and Kincade, P. W. (2006). Tracing the first waves of lymphopoiesis in mice. Development 133, 2041-2051.
31. Yoshihara, H., Arai, F., Hosokawa, K., Hagiwara, T., Takubo, K., Nakamura, Y., Gomei, Y., Iwasaki, H., Matsuoka, S., Miyamoto, K. et al. (2007). Thrombopoietin/MPL signaling regulates hematopoietic stem cell quiescence and interaction with the osteoblastic niche. Cell Stem Cell 1, 685-697.
32. 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.