Abstract
In the course of a previous experimental study on the early development of the mouse embryo hemopoietic system, we found that, at the 10–25 pairs of somite stages, the para-aortic splanchnopleure contains hemopoietic progenitors. Trying to discover a structural basis for this potentiality, we have looked for cytological signs of hemopoiesis in the embryo proper between 8.5 and 12 days post-coitum, i.e. prior to full-blown fetal liver hemopoiesis. Two suggestive findings are reported: (1) intra-arterial hemopoietic cells aggregates are present in the omphalomesenteric and umbilical arteries and to a lesser degree in the dorsal aorta; (2) cells groups resembling yolk sac blood islands are observed in the mesentery. The intra-arterial aggregates are strikingly similar to the intra-aortic clusters of avian embryos. These cytological aspects provide the anatomical basis underlying recent functional data that revealed the hemogenic capacity of the para-aortic splanchnopleure.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Beaupain D, Martin C, Dieterlen-Lièvre F (1979) Are developmental hemoglobin changes related to the origin of stem cells and site of erythropoiesis ? Blood 53:212–225
Bechtold TE, Smith PB, Turpen JB (1992) Differential stem cell contribution to thymocyte succession during development of Xenopus laevis. J Immunol 148:2975–2982
Cumano A, Paige CJ (1992) Enrichment and characterization of uncommited B-cell precursors from fetal liver at day 12 of gestation. EMBO J 11:593–601
Cumano A, Paige CJ, Iscove NN, Brady G (1992) Bipotential precursors of B cells and macrophages in murine fetal liver. Nature 356:612–615
Dieterlen-Lièvre F (1975) On the origin of haematopoietic stem cells in avian embryos: an experimental approach. J Embryol Exp Morphol 33:607–619
Dieterlen-Lièvre F (1994) Hemopoiesis during avian ontogeny. Poult Sci Rev 5:273–305
Dieterlen-Lièvre F, Le Douarin N (1993) Developmental rules in the hematopoietic and immune systems of birds: how general are they? Semin Dev Biol 4:6325–6332
Dieterlen-Lièvre F, Martin C (1981) Diffuse intraembryonic hemopoiesis in normal and chimeric avian development. Dev Biol 88:180–191
Godin I, Garcia-Porrero JA, Coutinho A, Dieterlen-Lièvre F, Marcos MAR (1993) Paraaortic splanchnopleure from early mouse embryos contains B1a cell progenitors. Nature 364:67–69
Godin I, Dieterlen-Lièvre F, Cumano A (1995) Emergence of multipotent hematopoietic cells in the yolk sac and in the paraaortic splanchnopleura in mouse embryos, beginning at 8.5 dpc. Proc Natl Acad Sci USA 92:773–777
Haar JL, Ackerman A (1971) A phase and electron microscopic study of vasculogenesis and erythropoiesis in the yolk sac of the mouse. Anat Rec 170:199–224
Hamilton HL (1952) Lillie's development of the chick. Holt, New York
Houssaint E (1981) Differentiation of the mouse hepatic primordium. II. Extrinsic origin of the haemopoietic cell line. Cell Differ 10:243–252
Jordan CT, McKearn JP, Lemischka IR (1990) Cellular and developmental properties of fetal hematopoietic stem cells. Cell 61:953–963
Kaufman MH (1992) The atlas of mouse development. Harcourt Brace, Jovanovitch, Academic Press, San Diego
Lassila O, Martin C, Toivanen P, Dieterlen-Lièvre F (1982) Erythropoiesis and lymphopoiesis in the chick yolk-sac embryo chimeras: contribution of yolk sac and intraembryonic stem cells. Blood 59:377–381
Liu CP, Auerbach R (1991a) Ontogeny of murine T cells: thymusregulated development of T cell receptor-bearing cells derived from embryonic yolk sac. Eur J Immunol 21:1849–1855
Liu CP, Auerbach R (1991b) In vitro development of murine T cells from prethymic and preliver embryonic yolk sac hematopoietic stem cells. Development 113:1315–1323
Medvinsky AL, Samoylina NL, Muller AM, Dzierzak EA (1993) An early pre-liver intraembryonic source of CFU-S in the developing mouse. Nature 364:64–66
Metcalf D, Moore MAS (1971) Haematopoietic cells. In: Neuberger A, Tatum EL (eds) Frontiers in biology, vol 24. North Holland, Amsterdam, pp 550
Moore MAS, Metcalf D (1970) Ontogeny of the haematopoietic system: yolk sac origin of in vivo and in vitro colony forming cells in the developing mouse embryo. Br J Haematol 18:279–296
Muller AM, Medvinsky AL, Strouboulis J, Grosveld F, Dzierzak EA (1994) Development of hematopoietic stem cell activity in the mouse embryo. Immunity 1:291–301
Paige CJ, Kincade PW, Moore MAS, Lee G (1979) The fate of fetal and adult B-cell grafted into immunodeficient CBA/N mice. J Exp Med 150:548–563
Perah G, Feldman M (1976) In vitro activation of the in vivo colony forming unit of the mouse yolk sac. J Cell Physiol 91:193–200
Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208–212
Romanoff AL (1960) The avian embryo. MacMillan, New York
Rugh R (1990) The mouse: its reproduction and development, 2nd edn. Oxford Science Publications, Oxford
Sabin FR (1920) Studies on the origin of blood-vessels and of red blood-corpuscles as seen in the living blastoderm of chicks during the second day of incubation. Contrib Embryol Carnegie Inst 9:215–258
Smith RA, Glomski CA (1982) “Hemogenic endothelium” of the embryonic aorta: does it exist? Dev Comp Immunol 6:359–368
Takahashi K, Yamamura F, Naito M (1989) Differentiation, maturation, and proliferation of macrophages in the mouse yolk sac: a light-microscopic, enzyme-cytochemical, immunohistochemical, and ultrastructural study. J Leukoc Biol 45:87–96
Theiler K (1972) The house mouse: development and normal stages from fertilization to 4 weeks of age. Springer, Berlin Heidelberg New York
Toles JF, Chui DHK, Belbeck LW, Starr E, Barker JE (1989) Hemopoietic stem cells in murine embryonic yolk sac and peripheral blood. Proc Natl Acad Sci USA 86:7456–7459
Turpen JB, Knudson CM (1982) Ontogeny of hematopoietic cell in Rana pipiens: precursor cell migration during embryogenesis. Dev Biol 89:138–151
Turpen JB, Turpen CJ, Flajnik M (1979) Experimental analysis of hemopoietic cell development in the liver of larval Rana pipiens. Dev Biol 69:466–479
Weissman I, Papaioannou V, Gardner R (1978) Fetal hematopoietic origin of the adult hemolymphoid system. Cold Spring Harb Conf Cell Proliferation 5 Book A: 33–47
Wong PMC, Chung SW, Chui DHK, Eaves CJ (1986) Properties of the earliest clonogenic hemopoietic precursors to appear in the developing murine yolk sac. Proc Natl Acad Sci USA 83:3851–3854
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Garcia-Porrero, J.A., Godin, I.E. & Dieterlen-Lièvre, F. Potential intraembryonic hemogenic sites at pre-liver stages in the mouse. Anat Embryol 192, 425–435 (1995). https://doi.org/10.1007/BF00240375
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00240375