Summary
Hemopoiesis in the liver of 26 human embryos and fetuses at 26 days after ovulation to 30 weeks of gestation was studied by electron microscopy.
The development of hepatic hemopoiesis seems to be closely correlated with the histogenetic developmental course of the liver. In the earliest stage of hepatic hemopoiesis, undifferentiated mononuclear cells, i.e. presumptive hemopoietic stem cells and transitional cells to the immature erythroid cells, are found in the intercellular spaces of the hepatocytes. With the development of the fetus, erythroid cells increase in the hepatic parenchyma, whereas the stem cells become gradually reduced in number and cannot be detected in the later stages. These stem cells are exclusively observed in the extravascular spaces and are considered to be derived from the septum transversum.
The ultrastructure of hepatic erythroid cells is quite different from yolk sac-derived primitive erythroblasts and myeloid erythroblasts of the adult. Generally, hepatic erythroid cells show less discrepancy of nuclear and cytoplasmic maturation and free polyribosomes found in the cytoplasm are smaller in size and number than primitive erythroblasts. The particular cytoplasmic features found in primitive erythroblasts, and the microtubules characteristic of myeloid erythroblasts of the adult, are rarely observed in hepatic series.
The primitive and hepatic series of erythroid cells seem to be independent of each other and are considered to belong to different clones.
A small number of granulocytic and megakaryocytic cells are found from the earliest stages of hepatic hemopoiesis and their morphology seems to be different from that of the adult.
Kupffer’s stellate cells of the liver exist prior to the myeloid monoeytogenesis.
Similar content being viewed by others
References
Ackerman, G. A.: Ultrastructure and cytochemistry of the developing neutrophil. Lab. Invest.19, 290–302 (1968)
Aron, M.: Origine du sang dans le foie embryonnaire. C. R. Soc. Biol. (Paris)81, 362–364 (1921)
Bainton, D. F., Farquhar, M. G.: Origin of granules in polymorphonuclear leukocytes. Two types derived from opposite faces of the Golgi complex in developing granulocytes. J. Cell Biol.28, 277–301 (1966)
Barnes, D. W. H., Loutit, J. F.: Haemopoietic stem cells in the peripheral blood. Lancet1967 II, 1138–1141
Bekkum, D. W. van, Noord, M. J. van, Maat, B., Dicke, K. A.: Attempts at identification of hemopoietic stem cell in mouse. Blood38, 547–558 (1971)
Bessis, M.: Ultrastructure of normal and leukemic granulocytes. Proc. Int. Conf. on leukemia and lymphoma, p. 281–302. Philadelphia: Lea & Febiger 1968
Bessis, M., Breton-Gorius, J.: Ultrastructure du pro-érythroblaste. Nouv. Rev. franç. Hémat.1, 529–533 (1961)
Bessis, M., Thiéry, J. P.: Electron microscopy of human white blood cells and their stem cells. Int. Rev. Cytol.12, 199–241 (1961)
Bloom, W.: Embryogenesis of mammalian blood. In: Downey, H. (ed.), Handbook of hematology, vol. 2, p. 856–922. New York: Paul B. Hoeber 1938
Bloom, W., Bartelmez, G. W.: Haematopoiesis in young human embryos. Amer. J. Anat.67, 21–53 (1940)
Boyd, W. H.: Transformation of hepatic reticuloendothelial cells to erythroid cells by pars intermedia. Amer. J. Physiol.219, 1614–1619 (1970)
Capone, R. J., Weinreb, E. L., Chapman, G. B.: Electron microscope studies on normal human myeloid elements. Blood23, 300–320 (1964)
Cline, M. J., Moore, M. A. S.: Embryonic origin of the mouse macrophage. Blood39, 842–849 (1972)
Cole, R. J., Hunter, J., Paul, J.: Hormonal regulation of prenatal haemoglobin synthesis by erythropoietin. Brit. J. Haemat.14, 477–488 (1968)
Cole, R. J., Paul, J.: The effects of erythropoietin on haemsynthesis in mouse yolk sac and cultured foetal liver cells. J. Embryol. exp. Morph.15, 245–260 (1966)
Dicke, K. A., Noord, M. J. van, Bekkum, D. W. van: Attempts at morphological identification of hemopoietic stem cell in rodents and primates. Exp. Hemat.1, 36–45 (1973)
DuBois, A. M.: The embryonic liver. In: Rouiller, Ch. (ed.), The liver, vol. 1, p. 1–39. New York-London: Academic Press 1963
Dunn, C. D. R.: The differentiation of haemopoietic stem cells. Series Haematol.4, 4, 1–71 (1971)
Fukuda, T.: Paired cisternae, the characteristic feature of foetal cells. Experientia (Basel)28, 317–318 (1972a)
Fukuda, T.: Fetal hemopoiesis. Ph. D.-thesis, Postgraduate School of Science, Tohoku University (1972b)
Fukuda, T.: Undifferentiated mononuclear cell in human embryonic liver; presumptive hematopoietic stem cell. Virchows Arch. Abt. B14, 31–34 (1973a)
Fukuda, T.: Fetal hemopoiesis I. Electron microscopic studies on human yolk sac hemopoiesis. Virchows Arch. Abt. B14, 197–213 (1973b)
Fukuda, T., Sato, H.: Desmosome, cilia, and peculiar structure of membranes in erythroblasts of human fetal liver. Virchows Arch. Abt. B7, 309–313 (1971)
Furth, R. van: The origin and turnover of promonocytes, monocytes and macrophages in normal mice. In: Furth, R. van (ed.), Mononuclear phagocytes, p. 151–165. Oxford: Blackwell 1970
Gilmour, J. R.: Normal haemopoiesis in intra-uterine and neonatal life. J. Path. Bact.52, 25–55 (1941)
Grasso, J. A.: Cytoplasmic microtubules in mammalian erythropoietic cells. Anat. Rec.156, 397–414 (1966)
Grasso, J. A., Swift, H., Ackerman, G. A.: Observations on the development of erythrocytes in mammalian fetal liver. J. Cell Biol.14, 235–254 (1962)
Howard, J. G.: The origin and immunological significance of Kupffer cells. In: Furth, R. van (ed.), Mononuclear phagocytes. p. 178–199 Oxford: Blackwell 1970
Ingram, V. M.: Embryonic red cell formation. Nature (Lond.)235, 338–339 (1972)
Ito, T., Nemoto, M.: Über die Kupffer’schen Sternzellen und die “Fettspeicherungszellen” (“fat-storing cells”) in der Blutkapillarenwand der menschlichen Leber. Folia anat. jap.24, 243–258 (1952)
Ito, T., Shibasaki, S.: Electron microscopic study on the hepatic sinusoidal wall and the fatstoring cells in the normal human liver. Arch. hist. jap.29, 137–192 (1968)
Karrier, H. E., Cox, J.: Electron microscopic observations on chick embryo liver. J. Ultrastruct. Res.5, 116–141 (1961)
Kay, H. E. M., Playfair, J. H. L., Wolfendale, M., Hopper, P. K.: Development of the thymus in the human foetus and its relation to immunological potential. Nature (Lond.)196, 238–240 (1962)
Krantz, S. B., Jacobson, L. O.: Erythropoietin and regulation of erythropoiesis. Chicago-London: Chicago Univ. Press 1970
Loutit, J.F.: Versatile haemopoietic stem cells. Brit. J. Haemat.15, 333–336 (1968)
Marks, P. A., Rifkind, R. A.: Protein synthesis, its control in erythropoiesis. Science175, 955–961 (1972)
Maximow, A.: Relation of blood cells to connective tissues and endothelium. Physiol. Rev.4, 533–563 (1924)
Maximow, A.: Bindegewebe und blutbildende Gewebe. In: Möllendorf, W. (Ed.), Handbuch der mikroskopischen Anatomie des Menschen, Bd. II/l, S. 232–583. Berlin: Springer 1927
Metcalf, D., Moore, M. A. S.: Haemopoietic cells. Amsterdam-London: North Holland 1971
Moore, M. A. S., Metcalf, D.: Ontogeny of the haemopoietic system: Yolk sac origin of in vivo and in vitro colony forming cells in the developing mouse embryo. Brit. J. Haemat.18, 279–296 (1970)
Murphy, M. J., Jr., Bertles, J. F., Gordon, A. S.: Identifying characteristics of the haematopoietic precursor cell. J. Cell Sci.9, 23–47 (1971)
Rifkind, R. A., Chui, D., Epler, H.: An ultrastructural study of early morphogenetic events during the establishment of fetal hepatic erythropoiesis. J. Cell Biol.40, 343–365 (1969)
Rubinstein, A. S., Trobaugh, F. E., Jr.: Ultrastructure of presumptive hematopoietic stem cells. Blood42, 61–80 (1973)
Seki, M.: Differentiation of hematopoietic cells. [Jap.]. Handbook of cytology vol. 7, (Ogawa, K., Oda, T., Kurosumi, K., Sugino, S., eds.), p. 185–219. Tokyo: Asakura 1971
Seno, S.: Critique of stem cell concept. [Jap.] Saishin-Igaku (Recent Medicine)28, 1664–1672 (1973)
Sorenson, G. D.: Hepatic hematocytopoiesis in the fetal rabbit: a light and electron microscopic study. Ann. N. Y. Acad. Sci.111, 45–69 (1963)
Tanaka, Y., Goodman, J. R.: Electron microscopy of human blood cells. New York-Evanston-San Francisco-London: Harper Row 1972
Thomas, D. B., Yoffey, J. M.: The origin of the hepatic hemocytoblasts. J. Anat. (Lond.)95, 605 (1961)
Thomas, D. B., Yoffey, J. M.: Human foetal haematopoiesis. II. Hepatic haematopoiesis in the human faetus. Brit. J. Haemat.10, 193–197 (1964)
Töndury, G., Kubik, S.: Zur Ontogenese des lymphatischen Systems. In: Handbuch der allgemeinen Pathologie, Bd. HI/6, Lymphgefäßsystem (Meessen, H., Hrsg.). S. 1–38 Berlin-Heidelberg-New York: Springer 1972
Yoffey, J. M.: The stem cell problem in the fetus. Israel J. med. Sci.7, 825–833 (1971)
Yoffey, J. M.: Haemopoietic stem cells. Ciba Foundation Symposium 13 (New Series). Amsterdam-London-New York: Elsevier-Excerpta Medica-North Holland 1973
Zamboni, L.: Electron microscopic studies of blood embryogenesis in humans. I. Ultrastructure of the fetal liver, II. The hemopoietic activity in the fetal liver. J. Ultrastruct. Res.12, 509–524, 525–541 (1965)
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Fukuda, T. Fetal hemopoiesis. Virchows Arch B Cell Pathol 16, 249–270 (1974). https://doi.org/10.1007/BF02894080
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF02894080