CD45lowc-Kithigh cells have hematopoietic properties in the mouse aorta-gonad-mesonephros region

Experimental Cell Research

Volumn 318, Issue 6, 2012, Pages 705-715

  Nobuhisa, Ikuo ^a,b   Yamasaki, Shoutarou ^b   Ramadan, Ahmed ^a,b   Taga, Tetsuya ^a,b  

^a TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^b KUMAMOTO UNIVERSITY   (Japan)

Author keywords

AGM; C Kit; CD45; Hematopoiesis; Mouse embryo

Indexed keywords

CD45 ANTIGEN; STEM CELL FACTOR;

AORTA; ARTICLE; CELL DIFFERENTIATION; CELL POPULATION; COCULTURE; COLONY FORMING CELL; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; GONAD; HEMATOPOIESIS; HEMATOPOIETIC CELL; IN VITRO STUDY; MESODERM; MESONEPHROS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STROMA CELL;

EID: 84857649065     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2012.01.017     Document Type: Article

References (36)

1. Ferkowicz M.J., Yoder M.C. Blood island formation: longstanding observations and modern interpretations. Exp. Hematol. 2005, 33:1041-1047.
2. de Bruijn M.F., Speck N.A., Peeters M.C., Dzierzak E. Definitive hematopoietic stem cells first develop within the major arterial regions of the mouse embryo. EMBO J. 2000, 19:2465-2474.
3. Medvinsky A., Dzierzak E. Definitive hematopoiesis is autonomously initiated by the AGM region. Cell 1996, 86:897-906.
4. Muller A.M., Medvinsky A., Strouboulis J., Grosveld F., Dzierzak E. Development of hematopoietic stem cell activity in the mouse embryo. Immunity 1994, 1:291-301.
5. Kumaravelu P., Hook L., Morrison A.M., Ure J., Zhao S., Zuyev S., Ansell J., Medvinsky A. Quantitative developmental anatomy of definitive haematopoietic stem cells/long-term repopulating units (HSC/RUs): role of the aorta-gonad-mesonephros (AGM) region and the yolk sac in colonisation of the mouse embryonic liver. Development 2002, 129:4891-4899.
6. Gekas C., Dieterlen-Lievre F., Orkin S.H., Mikkola H.K. The placenta is a niche for hematopoietic stem cells. Dev. Cell 2005, 8:365-375.
7. Ottersbach K., Dzierzak E. The murine placenta contains hematopoietic stem cells within the vascular labyrinth region. Dev. Cell 2005, 8:377-387.
8. Dzierzak E., Speck N.A. Of lineage and legacy: the development of mammalian hematopoietic stem cells. Nat. Immunol. 2008, 9:129-136.
9. Dzierzak E., Medvinsky A. The discovery of a source of adult hematopoietic cells in the embryo. Development 2008, 135:2343-2346.
10. Samokhvalov I.M., Samokhvalova N.I., Nishikawa S. Cell tracing shows the contribution of the yolk sac to adult haematopoiesis. Nature 2007, 446:1056-1061.
11. Rhodes K.E., Gekas C., Wang Y., Lux C.T., Francis C.S., Chan D.N., Conway S., Orkin S.H., Yoder M.C., Mikkola H.K. The emergence of hematopoietic stem cells is initiated in the placental vasculature in the absence of circulation. Cell Stem Cell 2008, 2:252-263.
12. Cumano A., Dieterlen-Lievre F., Godin I. Lymphoid potential, probed before circulation in mouse, is restricted to caudal intraembryonic splanchnopleura. Cell 1996, 86:907-916.
13. de Bruijn M.F., Ma X., Robin C., Ottersbach K., Sanchez M.J., Dzierzak E. Hematopoietic stem cells localize to the endothelial cell layer in the midgestation mouse aorta. Immunity 2002, 16:673-683.
14. Yokomizo T., Ogawa M., Osato M., Kanno T., Yoshida H., Fujimoto T., Fraser S., Nishikawa S., Okada H., Satake M., Noda T., Ito Y. Requirement of Runx1/AML1/PEBP2alphaB for the generation of haematopoietic cells from endothelial cells. Genes Cells 2001, 6:13-23.
15. North T.E., de Bruijn M.F., Stacy T., Talebian L., Lind E., Robin C., Binder M., Dzierzak E., Speck N.A. Runx1 expression marks long-term repopulating hematopoietic stem cells in the midgestation mouse embryo. Immunity 2002, 16:661-672.
16. Taoudi S., Gonneau C., Moore K., Sheridan J.M., Blackburn C.C., Taylor E., Medvinsky A. Extensive hematopoietic stem cell generation in the AGM region via maturation of VE-cadherin+CD45+ pre-definitive HSCs. Cell Stem Cell 2008, 3:99-108.
17. Bertrand J.Y., Giroux S., Golub R., Klaine M., Jalil A., Boucontet L., Godin I., Cumano A. Characterization of purified intraembryonic hematopoietic stem cells as a tool to define their site of origin. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:134-139.
18. Taoudi S., Morrison A.M., Inoue H., Gribi R., Ure J., Medvinsky A. Progressive divergence of definitive haematopoietic stem cells from the endothelial compartment does not depend on contact with the foetal liver. Development 2005, 132:4179-4191.
19. Nobuhisa I., Ohtsu N., Okada S., Nakagata N., Taga T. Identification of a population of cells with hematopoietic stem cell properties in mouse aorta-gonad-mesonephros cultures. Exp. Cell Res. 2007, 313:965-974.
20. Ohtsu N., Nobuhisa I., Mochita M., Taga T. Inhibitory effects of homeodomain-interacting protein kinase 2 on the aorta-gonad-mesonephros hematopoiesis. Exp. Cell Res. 2007, 313:88-97.
21. Mukouyama Y., Hara T., Xu M., Tamura K., Donovan P.J., Kim H., Kogo H., Tsuji K., Nakahata T., Miyajima A. In vitro expansion of murine multipotential hematopoietic progenitors from the embryonic aorta-gonad-mesonephros region. Immunity 1998, 8:105-114.
22. Hashimoto K., Fujimoto T., Shimoda Y., Huang X., Sakamoto H., Ogawa M. Distinct hemogenic potential of endothelial cells and CD41+ cells in mouse embryos. Dev. Growth Differ. 2007, 49:287-300.
23. Matsuyoshi N., Toda K., Horiguchi Y., Tanaka T., Nakagawa S., Takeichi M., Imamura S. In vivo evidence of the critical role of cadherin-5 in murine vascular integrity. Proc. Assoc. Am. Physicians 1997, 109:362-371.
24. Kawasaki H., Mizuseki K., Nishikawa S., Kaneko S., Kuwana Y., Nakanishi S., Nishikawa S.I., Sasai Y. Induction of midbrain dopaminergic neurons from ES cells by stromal cell-derived inducing activity. Neuron 2000, 28:31-40.
25. Ploemacher R.E., van der Sluijs J.P., van Beurden C.A., Baert M.R., Chan P.L. Use of limiting-dilution type long-term marrow cultures in frequency analysis of marrow-repopulating and spleen colony-forming hematopoietic stem cells in the mouse. Blood 1991, 78:2527-2533.
26. Yang S., Graham J., Kahan J.W., Schwartz E.A., Gerritsen M.E. Functional roles for PECAM-1 (CD31) and VE-cadherin (CD144) in tube assembly and lumen formation in three-dimensional collagen gels. Am. J. Pathol. 1999, 155:887-895.
27. Goodell M.A., Brose K., Paradis G., Conner A.S., Mulligan R.C. Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J. Exp. Med. 1996, 183:1797-1806.
28. Goodell M.A., Rosenzweig M., Kim H., Marks D.F., DeMaria M., Paradis G., Grupp S.A., Sieff C.A., Mulligan R.C., Johnson R.P. Dye efflux studies suggest that hematopoietic stem cells expressing low or undetectable levels of CD34 antigen exist in multiple species. Nat. Med. 1997, 3:1337-1345.
29. Hirashima M., Kataoka H., Nishikawa S., Matsuyoshi N., Nishikawa S. Maturation of embryonic stem cells into endothelial cells in an in vitro model of vasculogenesis. Blood 1999, 93:1253-1263.
30. Nishikawa S.I., Nishikawa S., Hirashima M., Matsuyoshi N., Kodama H. Progressive lineage analysis by cell sorting and culture identifies FLK1+VE-cadherin+ cells at a diverging point of endothelial and hemopoietic lineages. Development 1998, 125:1747-1757.
31. Sakurai H., Era T., Jakt L.M., Okada M., Nakai S., Nishikawa S. In vitro modeling of paraxial and lateral mesoderm differentiation reveals early reversibility. Stem Cells 2006, 24:575-586.
32. Peeters M., Ottersbach K., Bollerot K., Orelio C., de Bruijn M., Wijgerde M., Dzierzak E. Ventral embryonic tissues and Hedgehog proteins induce early AGM hematopoietic stem cell development. Development 2009, 136:2613-2621.
33. Arai F., Hirao A., Ohmura M., Sato H., Matsuoka S., Takubo K., Ito K., Koh G.Y., Suda T. Tie2/angiopoietin-1 signaling regulates hematopoietic stem cell quiescence in the bone marrow niche. Cell 2004, 118:149-161.
34. Tamura H., Okamoto S., Iwatsuki K., Futamata Y., Tanaka K., Nakayama Y., Miyajima A., Hara T. In vivo differentiation of stem cells in the aorta-gonad-mesonephros region of mouse embryo and adult bone marrow. Exp. Hematol. 2002, 30:957-966.
35. Yokomizo T., Dzierzak E. Three-dimensional cartography of hematopoietic clusters in the vasculature of whole mouse embryos. Development 2010, 137:3651-3661.
36. Yamasaki S., Nobuhisa I., Ramadan A., Taga T. Identification of a yolk sac cell population with hematopoietic activity in veiw of CD45/c-Kit expression. Dev. Growth Differ. 2011, 53:870-877.