Definitive hematopoietic stem cells first develop within the major arterial regions of the mouse embryo

EMBO Journal

Volumn 19, Issue 11, 2000, Pages 2465-2474

  De Bruijn, Marella F T R ^a   Speck, Nancy A ^b   Peeters, Marian C E ^a   Dzierzak, Elaine ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

AGM; AML1; Embryo; Runx1; Vitelline

Indexed keywords

ANIMAL TISSUE; AORTA; ARTERY; ARTICLE; CELL TRANSPLANTATION; EMBRYO; EMBRYO DEVELOPMENT; HEMATOPOIETIC STEM CELL; MOUSE; NONHUMAN; ORGAN CULTURE; PRIORITY JOURNAL; UMBILICAL ARTERY; UROGENITAL SYSTEM; YOLK SAC;

EID: 0034214284     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/19.11.2465     Document Type: Article

References (64)

1. Baldwin, H.S. et al. (1994) Platelet endothelial cell adhesion molecule-1 (PECAM-1/CD31): alternatively spliced, functionally distinct isoforms expressed during mammalian cardiovascular development. Development, 120, 2539-2553.
2. Bertwistle, D., Walmsley, M.E., Read, E.M., Pizzey, J.A. and Patient, R.K. (1996) GATA factors and the origins of adult and embryonic blood in Xenopus: responses to retinoic acid. Mech. Dev., 57, 199-214.
3. Brown, L., Rodaway, A., Schilling, T., Jowett, T., Ingham, P., Patient, R. and Sharrocks, A. (2000) Insights into early vasculogenesis revealed by expression of the ETS-domain transcription factor FLi-1 in wildtype and mutant zebrafish embryos. Mech. Dev., 90, 237-252.
4. Carmeliet, P. et al. (1996) Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature, 380, 435-439.
5. Chiquoine, A. (1954) The identification, origin and migration of the primordial germ cells in the mouse embryo. Anat. Rec., 118, 135-146.
6. 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.
7. de Bruijn, M.F.T.R., van Vianen, W., Ploemacher, R.E., Bakker-Woudenberg, I.A., Campbell, P.A., van Ewijk, W. and Leenen, P.J.M. (1998) Bone marrow cellular composition in Listeria monocytogenes infected mice detected using ER-MP12 and ER-MP20 antibodies: a flow cytometric alternative to differential counting. J. Immunol. Methods, 217, 27-39.
8. De Felici, M., Heasman, J., Wylie, C.C. and McLaren, A. (1986) Macrophages in the urogenital ridge of the mid-gestation mouse fetus. Cell. Differ., 18, 119-129.
9. Dieterlen-Lievre, F. (1998) Hematopoiesis: Progenitors and their genetic program. Curr. Biol., 8, R727-R730.
10. Dieterlen-Lievre, F. and Martin, C. (1981) Diffuse intraembryonic hemopoiesis in normal and chimeric avian development. Dev. Biol., 88, 180-191.
11. Drake, C.J., Brandt, S.J., Trusk, T.C. and Little, C.D. (1997) TAL1/SCL is expressed in endothelial progenitor cells/angioblasts and defines a dorsal-to-ventral gradient of vasculogenesis. Dev. Biol., 192, 17-30.
12. Dzierzak, E. and de Bruijn, M. (2000) Isolation and analysis of hematopoietic stem cells from mouse embryos. In Klug, C. and Jordan, C. (eds), Methods in Molecular Medicine: Hematopoietic Stem Cell Protocols. Humana Press, Totowa, NJ, in press.
13. Dzierzak, E. and Medvinsky, A. (1995) Mouse embryonic hematopoiesis. Trends Genet., 11, 359-366.
14. Dzierzak, E., Medvinsky, A. and de Bruijn, M. (1998) Qualitative and quantitative aspects of haemopoietic cell development in the mammalian embryo, Immunol. Today, 19, 228-236.
15. Ferrara, N., Carver-Moore, K., Chen, H., Dowd, M., Lu, L., O'Shea, K.S., Powell-Braxton, L., Hillan, K.J. and Moore, M.W. (1996) Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature, 380, 439-442.
16. Garcia-Porrero, J.A., Godin, I.E. and Dieterlen-Lievre, F. (1995) Potential intraembryonic hemogenic sites at pre-liver stages in the mouse. Anat. Embryol. (Berl.), 192, 425-435.
17. Garcia-Porrero, J.A., Manaia, A., Jimeno, J., Lasky, L.L., Dieterlen-Lievre, F. and Godin, I.E. (1998) Antigenic profiles of endothelial and hemopoietic lineages in murine intraembryonic hemogenic sites. Dev. Comp. Immunol., 22, 303-319.
18. Geissler, E.N., Ryan, M.A. and Housman, D.E. (1988) The dominant-white spotting (W) locus of the mouse encodes the c-kit protooncogene. Cell, 55, 185-192.
19. Gering, M., Rodaway, A.R., Gottgens, B., Patient, R.K. and Green, A.R. (1998) The SCL gene specifies haemangioblast development from early mesoderm. EMBO J., 17, 4029-4045.
20. Godin, I., Garcia-Porrero, J.A., Dieterlen-Lievre, F. and Cumano, A. (1999) Stem cell emergence and hemopoietic activity are incompatible in mouse intraembryonic sites. J. Exp. Med., 190, 43-52.
21. Huang, H. and Auerbach, R. (1993) Identification and characterization of hematopoietic stem cells from the yolk sac of the early mouse embryo. Proc. Natl Acad. Sci. USA, 90, 10110-10114.
22. 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.
23. Kaufman, M. (1992) The Atlas of Mouse Development. Academic Press, London, UK.
24. Lakshmanan, G., Lieuw, K.H., Lim, K.C., Gu, Y., Grosveld, F., Engel, J.D. and Karis, A. (1999) Localization of distant urogenital system-, central nervous system- and endocardium-specific transcriptional regulatory elements in the GATA-3 locus. Mol. Cell. Biol., 19, 1558-1568.
25. Larsen, W. (1997) Human Embryology. Churchill Livingstone, New York, NY.
26. Lemischka, I.R. (1991) Clonal, in vivo behavior of the totipotent hematopoietic stem cell. Semin. Immunol., 3, 349-355.
27. Marshall, C.J., Moore, R.L., Thorogood, P., Brickell, P.M., Kinnon, C. and Thrasher, A.J. (1999) Detailed characterization of the human aortagonad-mesonephros region reveals morphological polarity resembling a hematopoietic stromal layer. Dev. Dyn., 215, 139-147.
28. Martineau, J., Nordqvist, K., Tilmann, C., Lovell-Badge, R. and Capel, B. (1997) Male-specific cell migration into the developing gonad. Curr. Biol., 7, 958-968.
29. McNagny, K.M., Pettersson, I., Rossi, F., Flamme, I., Shevchenko, A., Mann, M. and Graf, T. (1997) Thrombomucin, a novel cell surface protein that defines thrombocytes and multipotent hematopoietic progenitors. J. Cell Biol., 138, 1395-1407.
30. Medvinsky, A. and Dzierzak, E. (1996) Definitive hematopoiesis is autonomously initiated by the AGM region. Cell, 86, 897-906.
31. Medvinsky, A. and Dzierzak, E. (1999) Development of the hematopoietic stem cell: can we describe it? Blood, 94, 3613-3614.
32. Medvinsky, A.L., Gan, O.I., Semenova, M.L. and Samoylina, N.L. (1996) Development of day-8 colony-forming unit-spleen hematopoietic progenitors during early murine embryogenesis: spatial and temporal mapping. Blood, 87, 557-566.
33. Miles, C, Sanchez, M.-J., Sinclair, A. and Dzierzak, E. (1997) Expression of the Ly-6E.1 (Sca-1) transgene in adult hematopoietic stem cells and the developing mouse embryo. Development, 124, 537-547.
34. Moore, M.A. and Metcalf, D. (1970) Ontogeny of the haemopoietic system: yolk sac origin of in vivo and in vitro colony forming cells in the developing mouse embryo. Br. J. Haematol., 18, 279-296.
35. Muller, 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.
36. Nishikawa, S.I., Nishikawa, S., Kawamoto, H., Yoshida, H., Kizumoto, M., Kataoka, H. and Katsura, Y. (1998a) In vitro generation of lymphohematopoietic cells from endothelial cells purified from murine embryos. Immunity, 8, 761-769.
37. Nishikawa, S.-I., Nishikawa, S., Hirashima, M., Matsuyoshi, N. and Kodama, H. (1998b) Progressive lineage analysis by cell sorting and culture identifies FLK+VE-cadherin+ cells at a diverging point of endothelial and hemopoietic lineages. Development, 125, 1747-1757.
38. North, T., Gu, T.-L., Stacy, T., Wang, Q., Howard, L., Binder, M., Marin-Padilla, M. and Speck, N. (1999) Cbfa2 is required for the formation of intraaortic hematopoietic clusters. Development, 126, 2563-2575.
39. Ody, C., Vaigot, P., Quere, P., Imhof, B.A. and Corbel, C. (1999) Glycoprotein IIb-IIIa is expressed on avian multilineage hematopoietic progenitor cells. Blood, 93, 2898-2906.
40. Okuda, T., van Deursen, J., Hiebert, S.W., Grosveld, G. and Downing, J.R. (1996) AML 1, the target of multiple chromosomal translocations in human leukemia. is essential for normal fetal liver hematopoiesis. Cell, 84, 321-330.
41. Perez-Aparicio, F.J., Carretero, A., Navarro, M. and Ruberte, J. (1998) The lack of genital ridge vascularization in the early chick embryo: implications in the migration of the primordial germ cells. Anat. Rec., 251, 398-405.
42. Petrenko, O., Beavis, A., Klaine, M., Kittappa, R., Godin, I. and Lemischka, I.R. (1999) The molecular characterization of the fetal stem cell marker AA4. Immunity, 10, 691-700.
43. Rich, I.N. (1995) Primordial germ cells are capable of producing cells of the hematopoietic system in vitro. Blood. 86, 463-472.
44. Robert, B., St. John, P.L. and Abrahamson, D.R. (1998) Direct visualization of renal vascular morphogenesis in Flk1 heterozygous mutant mice. Am. J. Physiol., 275, F164-172.
45. Rugh, R. (1990) The Mouse: Its Reproduction and Development. Oxford University Press, Oxford, UK.
46. Sabin, F.R. (1917) Origin and development of the primitive vessels of the chick and of the pig. Contrib. Embryol. Carnegie Inst., 226, 61-124.
47. Sanchez, M., Gottgens, B., Sinclair, A.M., Stanley, M., Begley, C.G., Hunter, S. and Green, A.R. (1999) An SCL 3′ enhancer targets developing endothelium together with embryonic and adult haematopoietic progenitors. Development, 126, 3891-3904.
48. Sanchez, 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.
49. Sato, T.N. et al. (1995) Distinct roles of the receptor tyrosine kinases Tie-1 and Tie-2 in blood vessel formation. Nature, 376, 70-74.
50. Shalaby, F., Rossant, J., Yamaguchi, T.P., Gertsenstein, M., Wu, X.F., Breitman, M.L. and Schuh, A.C. (1995) Failure of blood-island formation and vasculogenesis in Fik-1-deficient mice. Nature, 376, 62-66.
51. Shalaby, F., Ho, J., Stanford, W.L., Fischer, K.D., Schuh, A.C., Schwartz, L., Bernstein, A. and Rossant, J. (1997) A requirement for Flk1 in primitive and definitive hematopoiesis and vasculogenesis. Cell, 89, 981-990.
52. Spangrude, G.J., Smith, L., Uchida, N., Ikuta, K., Heimfeld, S., Friedman, J. and Weissman, I.L. (1991) Mouse hematopoietic stem cells. Blood, 78, 1395-1402.
53. Strouboulis, J., Dillon, N. and Grosveld, F. (1992) Developmental regulation of a complete 70-kb human β-globin locus in transgenic mice. Genes Dev., 6, 1857-1864.
54. Takakura, N., Huang, X.L., Naruse, T., Hamaguchi, I., Dumont, D.J., Yancopoulos, G.D. and Suda, T. (1998) Critical role of the TIE2 endotbelial receptor in the development of definitive hematopoiesis. Immunity, 9, 677-689.
55. + hematopoietic cells in the early human embryo. Blood, 87, 67-72.
56. Tavian, M., Hallais, M.F. and Peault, B. (1999) Emergence of intraembryonic hematopoietic precursors in the pre-liver human embryo. Development, 126, 793-803.
57. Turpen, J.B., Knudson, C.M. and Hoefen, P.S. (1981) The early ontogeny of hematopoietic cells studied by grafting cytogenetically labeled tissue anlagen: localization of a prospective stem cell compartment. Dev. Biol., 85, 99-112.
58. Walmsley, M.E., Guille, M.J., Bertwistle, D., Smith, J.C., Pizzey, J.A. and Patient, R.K. (1994) Negative control of Xenopus GATA-2 by activin and noggin with eventual expression in precursors of the ventral blood islands. Development, 120, 2519-2529.
59. Wang, Q., Stacy, T., Binder, M., Marin-Padilla, M., Sharpe, A.H. and Speck, N.A. (1996) Disruption of the Cbfa2 gene causes necrosis and hemorrhaging in the central nervous system and blocks definitive hematopoiesis. Proc. Natl Acad. Sci. USA, 93, 3444-3449.
60. 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.
61. 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.
62. Zettergren, L.D. (1982) Ontogeny and distribution of cells in B lineage in the American leopard frog. Rana pipiens. Dev. Comp. Immunol., 6, 311-320.
63. Zettergren, L.D. and Cutlan, R.T. (1992) Immunoglobulin-containing cells in chick embryo urogenital tissues: a new site for early B lineage cells in endothermic vertebrates. J. Exp. Zool., 262, 458-461.
64. Zhou, Y. et al. (1998) Rescue of the embryonic lethal hematopoietic defect reveals a critical role for GATA-2 in urogenital development. EMBO J., 17, 6689-6700.