Intra-aortic clusters undergo endothelial to hematopoietic phenotypic transition during early embryogenesis

PLoS ONE

Volumn 7, Issue 4, 2012, Pages

  Mizuochi, Chiyo ^a   Fraser, Stuart T ^b   Biasch, Katia ^c   Horio, Yuka ^a   Kikushige, Yoshikane ^d   Tani, Kenzaburo ^e   Akashi, Koichi ^d   Tavian, Manuela ^c   Sugiyama, Daisuke ^a  

^a KYUSHU UNIVERSITY   (Japan)

^b UNIVERSITY OF SYDNEY   (Australia)

^c INSERM   (France)

^d KYUSHU UNIVERSITY   (Japan)

^e KYUSHU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CD31 ANTIGEN; CD34 ANTIGEN; CD45 ANTIGEN; CELL MARKER; FIBRINOGEN RECEPTOR; MEMBRANE ANTIGEN; MESSENGER RNA; STEM CELL FACTOR; VASCULAR ENDOTHELIAL CADHERIN; BIOLOGICAL MARKER; LEUKOCYTE ANTIGEN;

ANIMAL CELL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; CD45 GENE; CELL AGGREGATION; CELL ASSAY; CELL JUNCTION; CELL KINETICS; CELL SEPARATION; CELL TRANSFORMATION; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; EMBRYO DEVELOPMENT; ENDOTHELIUM CELL; FEMALE; FLOW CYTOMETRY; GENE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; PHENOTYPIC VARIATION; PROTEIN EXPRESSION; UPREGULATION; ANIMAL; ANIMAL EMBRYO; AORTA; CELL DEDIFFERENTIATION; CYTOLOGY; GENE EXPRESSION; GENETICS; METABOLISM; PRENATAL DEVELOPMENT;

VERTEBRATA;

ANIMALS; ANTIGENS, CD; AORTA; BIOLOGICAL MARKERS; CELL DEDIFFERENTIATION; EMBRYO, MAMMALIAN; EMBRYONIC DEVELOPMENT; ENDOTHELIAL CELLS; FLOW CYTOMETRY; GENE EXPRESSION; HEMATOPOIETIC STEM CELLS; HUMANS; MICE;

EID: 84860458847     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0035763     Document Type: Article

References (42)

1. Dzierzak E, Speck NA, (2008) Of lineage and legacy: the development of mammalian hematopoietic stem cells. Nat Immunol 9: 129-136.
2. Mikkola HK, Orkin SH, (2006) The journey of developing hematopoietic stem cells. Development 133: 3733-3744.
3. Godin I, Cumano A, (2002) The hare and the tortoise: an embryonic haematopoietic race. Nat Rev Immunol 2: 593-604.
4. Dieterlen-Lievre F, Pouget C, Bollerot K, Jaffredo T, (2006) Are intra-aortic hemopoietic cells derived from endothelial cells during ontogeny? Trends Cardiovasc Med 16: 128-139.
5. Jaffredo T, Bollerot K, Sugiyama D, Gautier R, Drevon C, (2005) Tracing the hemangioblast during embryogenesis: developmental relationships between endothelial and hematopoietic cells. Int J Dev Biol 49: 269-277.
6. Sugiyama D, Tsuji K, (2006) Definitive hematopoiesis from endothelial cells in the mouse embryo; a simple guide. Trends Cardiovasc Med 16: 45-49.
7. Medvinsky A, Dzierzak E, (1996) Definitive hematopoiesis is autonomously initiated by the AGM region. Cell 86: 897-906.
8. Taoudi S, Gonneau C, Moore K, Sheridan JM, Blackburn CC, et al. (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.
9. Rybtsov S, Sobiesiak M, Taoudi S, Souilhol C, Senserrich J, et al. (2011) Hierarchical organization and early hematopoietic specification of the developing HSC lineage in the AGM region. J Exp Med 208: 1305-1315.
10. McKinney-Freeman SL, Naveiras O, Yates F, Loewer S, Philitas M, et al. (2009) Surface antigen phenotypes of hematopoietic stem cells from embryos and murine embryonic stem cells. Blood 114: 268-278.
11. Yokomizo T, Dzierzak E, (2010) Three-dimensional cartography of hematopoietic clusters in the vasculature of whole mouse embryos. Development 137: 3651-3661.
12. Kumano K, Chiba S, Kunisato A, Sata M, Saito T, et al. (2003) Notch1 but not Notch2 is essential for generating hematopoietic stem cells from endothelial cells. Immunity 18: 699-711.
13. Yoder MC, Hiatt K, Dutt P, Mukherjee P, Bodine DM, et al. (1997) Characterization of definitive lymphohematopoietic stem cells in the day 9 murine yolk sac. Immunity 7: 335-344.
14. Garcia-Porrero JA, Godin IE, Dieterlen-Lievre F, (1995) Potential intraembryonic hemogenic sites at pre-liver stages in the mouse. Anat Embryol (Berl) 192: 425-435.
15. Garcia-Porrero JA, Manaia A, Jimeno J, Lasky LL, Dieterlen-Lievre F, et al. (1998) Antigenic profiles of endothelial and hemopoietic lineages in murine intraembryonic hemogenic sites. Dev Comp Immunol 22: 303-319.
16. Fraser ST, Ogawa M, Yokomizo T, Ito Y, Nishikawa S, (2003) Putative intermediate precursor between hematogenic endothelial cells and blood cells in the developing embryo. Dev Growth Differ 45: 63-75.
17. Jaffredo T, Gautier R, Eichmann A, Dieterlen-Lievre F, (1998) Intraaortic hemopoietic cells are derived from endothelial cells during ontogeny. Development 125: 4575-4583.
18. Sugiyama D, Ogawa M, Hirose I, Jaffredo T, Arai K, et al. (2003) Erythropoiesis from acetyl LDL incorporating endothelial cells at the preliver stage. Blood 101: 4733-4738.
19. Sugiyama D, Arai K, Tsuji K, (2005) Definitive hematopoiesis from acetyl LDL incorporating endothelial cells in the mouse embryo. Stem Cells Dev 14: 687-696.
20. Bertrand JY, Giroux S, Golub R, Klaine M, Jalil A, et al. (2005) Characterization of purified intraembryonic hematopoietic stem cells as a tool to define their site of origin. Proc Natl Acad Sci U S A 102: 134-139.
21. Zovein AC, Hofmann JJ, Lynch M, French WJ, Turlo KA, et al. (2008) Fate tracing reveals the endothelial origin of hematopoietic stem cells. Cell Stem Cell 3: 625-636.
22. Chen MJ, Yokomizo T, Zeigler BM, Dzierzak E, Speck NA, (2009) Runx1 is required for the endothelial to haematopoietic cell transition but not thereafter. Nature 457: 887-891.
23. Bertrand JY, Chi NC, Santoso B, Teng S, Stainier DY, et al. (2010) Haematopoietic stem cells derive directly from aortic endothelium during development. Nature 464: 108-111.
24. Kissa K, Herbomel P, (2010) Blood stem cells emerge from aortic endothelium by a novel type of cell transition. Nature 464: 112-115.
25. Boisset JC, van Cappellen W, Andrieu-Soler C, Galjart N, Dzierzak E, et al. (2010) In vivo imaging of haematopoietic cells emerging from the mouse aortic endothelium. Nature 464: 116-120.
26. Sasaki T, Mizuochi C, Horio Y, Nakao K, Akashi K, et al. (2010) Regulation of hematopoietic cell clusters in the placental niche through SCF/Kit signaling in embryonic mouse. Development 137: 3941-3952.
27. Mucenski ML, McLain K, Kier AB, Swerdlow SH, Schreiner CM, et al. (1991) A functional c-myb gene is required for normal murine fetal hepatic hematopoiesis. Cell 65: 677-689.
28. Okuda T, van Deursen J, Hiebert SW, Grosveld G, Downing JR, (1996) AML1, the target of multiple chromosomal translocations in human leukemia, is essential for normal fetal liver hematopoiesis. Cell 84: 321-330.
29. Wang Q, Stacy T, Binder M, Marin-Padilla M, Sharpe AH, et al. (1996) Disruption of the Cbfa2 gene causes necrosis and hemorrhaging in the central nervous system and blocks definitive hematopoiesis. Proc Natl Acad Sci U S A 93: 3444-3449.
30. North T, Gu TL, Stacy T, Wang Q, Howard L, et al. (1999) Cbfa2 is required for the formation of intra-aortic hematopoietic clusters. Development 126: 2563-2575.
31. Yuasa H, Oike Y, Iwama A, Nishikata I, Sugiyama D, et al. (2005) Oncogenic transcription factor Evi1 regulates hematopoietic stem cell proliferation through GATA-2 expression. EMBO J 24: 1976-1987.
32. Goyama S, Yamamoto G, Shimabe M, Sato T, Ichikawa M, et al. (2008) Evi-1 is a critical regulator for hematopoietic stem cells and transformed leukemic cells. Cell Stem Cell 3: 207-220.
33. Wood HB, May G, Healy L, Enver T, Morris-Kay GM, (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.
34. Takakura N, Huang XL, Naruse T, Hamaguchi I, Dumont DJ, et al. (1998) Critical role of the TIE2 endothelial cell receptor in the development of definitive hematopoiesis. Immunity 9: 677-686.
35. Theiler K, (1972) The house mouse: development and normal stages from fertilization to 4 weeks of age. Springer, Berlin Heidelberg New York.
36. Kishihara K, Penninger J, Wallace VA, Kundig TM, Kawai K, et al. (1993) Normal B lymphocyte development but impaired T cell maturation in CD45-exon6 protein tyrosine phosphatase-deficient mice. Cell 74: 143-156.
37. Byth KF, Conroy LA, Howlett S, Smith AJ, May J, et al. (1996) CD45-null transgenic mice reveal a positive regulatory role for CD45 in early thymocyte development, in the selection of CD4+CD8+ thymocytes, and B cell maturation. J Exp Med 183: 1707-1718.
38. Mee PJ, Turner M, Basson MA, Costello PS, Zamoyska R, et al. (1999) Greatly reduced efficiency of both positive and negative selection of thymocytes in CD45 tyrosine phosphatase-deficient mice. Eur J Immunol 29: 2923-2933.
39. North TE, de Bruijn MF, Stacy T, Talebian L, Lind E, et al. (2002) Runx1 expression marks long-term repopulating hematopoietic stem cells in the midgestation mouse embryo. Immunity 16: 661-672.
40. Matsubara A, Iwama A, Yamazaki S, Furuta C, Hirasawa R, et al. (2005) Endomucin, a CD34-like sialomucin, marks hematopoietic stem cells throughout development. J Exp Med 202: 1483-1492.
41. O'Rahilly R, Muller F, (1987) Development Stages in Human Embryos. Washington Carnegie Institution of Washington.
42. Tavian M, Peault B, (2005) The changing cellular environments of hematopoiesis in human development in utero. Exp Hematol 33: 1062-1069.