Summary
After about 12 days of gestation, fetal macrophages begin to appear in the subepidermal mesenchyme of rat fetuses. The macrophages are ultrastructurally characterized by cytoplasmic vacuoles, abundant polyribosomes and long filopodia. Immunocytologically, they possess Fc and complement (C3) receptors on the cell surface and are capable of immune phagocytosis, Latex or carbon phagocytosis, and glass adherence. From 15 days of gestation, lysosomal granules and miropinocytic vesicles gradually develop, together with an enlargement of Golgi complexes, whereas the number of polysomes and the number and size of cytoplasmic vacuoles are gradually reduced when gestation ends. Finally, the macrophages become amoeboid. Non-specific esterase and endogenous peroxidase activities are always absent in these macrophages. In culture experiments with cell suspensions prepared from the mesenchyme, fetal macrophages show a similar maturation process. Autoradiography with 3H-thymidine demonstrates a high proliferative capacity of the macrophages, particularly during the fetal stage.
Similar content being viewed by others
References
Andersen H (1962) Histochemical studies of the development of the human hip joints. Acta Anat 48:258–292
Andersen H (1964) Development, morphology and histochemistry of the early synovial tissue in human foetuses. Acta Anat 58:90–115
Andersen H, Mathiessen ME (1966) The histiocyte in human foetal tissues. Its morphology, cytochemistry, origin, function and fate. Z Zellforsch 72:193–211
Asano K, Imai Y, Kojima M (1969) Dynamics of subcutaneous connective tissue cells under stimulation, especially with reference to regeneration of histiocyte. Recent Advances in RES Research 9:107–130
Bainton DF (1980) Changes in peroxidase distribution within organelles of blood monocytes and peritoneal macrophages after surface adherence in vitro and in vivo. In: van Furth R (ed) Mononuclear phagocytes. Part 1. Functional aspects. Martinus Nijhoff Publishers, The Hague Boston London, pp 61–86
Ballard KJ, Holt SJ (1968) Cytological and cytochemical studies on cell death and digestion in the foetal rat foot: The role of macrophages and hydrolytic enzymes. J Cell Sci 3:245–262
Barka T, Anderson PJ (1965) Histochemistry, theory, practice and bibliography. Hoeber Medical Division, Harper & Row Publishers Inc. New York, Evanston and London, pp 238–242
Beelen RHJ, Veer vM, Fluitsma DM, Korn C, Hoefschmit ECM (1978) Identification of exudate-resident macrophages on the basis of peroxidase activity. J Reticuloendothel Soc 23:103–110
Beelen RHJ, Fluitsma DM, Meer JWM van der, Hoefschmit ECM (1980) Development of exudate-resident macrophages, on the basis of the pattern of peroxidase activity in vivo and in vitro. In: Furth R van (ed) Mononuclear phagocytes. Part II. Functional aspects. Martinus Nijhoff Publishers, The Hague Boston London, pp 78–112
Bodel PT, Nichols BA, Bainton DF (1977) Appearance of peroxidase reactivity within the rough endoplasmic reticulum of blood monocytes after surface adherence. J Exp Med 145:264–274
Bodel PT, Nichols BA, Bainton DF (1978) Differences in peroxidase localization of rabbit peritoneal macrophages after surface adherence. Am J Pathol 91:107–117
Breathnach AS (1978) Development and differentiation of dermal cells in man. J Invest Dermatol 71:2–8
Cline MJ (1975) Ontogeny of mononuclear phagocytes. In: Furth R van (ed) Mononuclear phagocytes in immunity, infection and pathology. Blackwell Scientific Publications, Oxford, pp 263–268
Cline MJ, Moore MAS (1972) Embryonic origin of the mouse macrophage. Blood 39:842–849
Daems WTh, Brederoo P (1973) Electron microscopical studies of the structure, phagocytic properties, and peroxidatic activity of resident and exudate peritoneal macrophages in the guinea pig. Z Zellforsch 144:247–297
Daems WTh, Rhee HJ van der (1980) Peroxidase and catalase in monocytes, macrophages, epithelioid cells and giant cells of the rat. In: Furth R van (ed) Mononuclear phagocytes. Martinus Nijhoff Publishers, The Hague, Boston London, pp 43–60
Daems WTh, Koerton HK, Soranzo MR (1976) Differences between monocyte-derived and tissue macrophages. In: Reichard SM, Escobar MR, Friedman H (eds) The reticuloendothelial system in health and disease: Functions and characteristics. Plenum Press, New York London, pp 27–40
Dawd DS, Hinchliffe JR (1971) Cell death in the ‘opaque patch’ in the central mesenchyme of the developing chick limb; a cytological, cytochemical and electron microscopic analysis. J Embryol Exp Morphol 26:401–424
Deimann W, Fahimi HD (1979) The appearance of transitional forms between monocytes and Kupffer cells in the liver of rats treated with glucan. J Exp Med 149:883–897
Fukuda T (1973) Fetal hemopoiesis. I. Electron microscopic studies on human yolk sac hematopoiesis. Virchows Arch Abt B Zell Path 14:197–213
Furth R van (1980) Cells of the mononuclear phagocyte system. Nomenclature in terms of sites and conditions. In: Furth R van (ed) Mononuclear phagocytes. Part I. Functional aspects. Martinus Nijhoff Publishers, The Hague, Boston London, pp 1–30
Furth R van (1981) Development of mononuclear phagocytes. In: Förster O, Landy M (eds) Heterogeneity of mononuclear phagocytes. Academic Press, London New York Toronto Sydney San Francisco, pp 3–10
Furth R van, Cohn ZA, Hirch JG, Humphrey JH, Spector WG, Langevoort HL (1972) The mononuclear phagocyte system: a new classification of macrophages, monocytes and their precursor cell. Bull WHO 46:845–852
Furth R van, Langevoort HL, Schaberg A (1975) Mononuclear phagocytes in human pathology — proposal for an approach to improve classification. In: Furth R van (ed) Mononuclear phagocytes in immunity, infection and pathology. Blackwell Scientific Publications, Oxford London Edinburgh Melborne, pp 1–15
Furth R van, Diesselhoff-den Dulk MMC, Raeburn JA, Zwet ThL van, Crofton R, OudAlblas AB van (1980) Characteristics, origin and kinetics of human and murine mononuclear phagocytes. In: Furth R van (ed) Mononuclear phagocytes. Part I. Functional aspects. Martinus Nijhoff Publishers, The Hague, Boston London, pp 279–298
Graham RC, Karnovsky MJ (1966) The early stages of absorption of injected horseradish peroxidase in the proximal tubules of mouse kidney. Ultrastructural cytochemistry by a new technique. J Histochem Cytochem 14:291–302
Hoyes AD (1969) The human foetal yolk sac. An ultrastructural study of four specimens. Z Zellforsch 99:469–490
Jacoby F (1965) Macrophages. In: Wilmer EN (ed) ells and tissues in culture; methods, biology and pathology. Vol. 2, New York, Academic Press, pp 1–93
Johnson GR, Jones RO (1973) Differentiation of the mammalian hepatic primordium in vitro. I. Morphogenesis and the onset of hematopoiesis. J Embryol Exp Morphol 30:83–96
Kojima M (1976) Macrophages, reticuloendothelial system and mononuclear system. Recent Advances in RES Research 16:1–25
Naito M (1975) Electron microscopical study on the origin of Kupffer cells. Recent Advances in RES Research 15:67–82
Naito M, Wisse E (1977) Observations on the fine structure and cytochemistry of sinusoidal cells in fetal and neonatal rat liver. In: Wisse E, Knook DL (eds) Kupffer cells and other sinusoidal cells. Elsevier, Amsterdam, pp 497–505
Naito M, Oka K, Sato T, Hamajima M, Kojima M (1979) Ultrastructural and cytochemical changes of monocytes in vivo and in vitro. Recent Advances in RES Research 18:66–82
Naito M, Takahasi K, Takahashi H, Kojima M (1982) Ontogenetic development of Kupffer cells. In: Knook DL, Wisse E (eds) Sinusoidal liver cells. Elsevier Biochemical Press, Amsterdam, pp 155–164
Oka K, Miyasaki M, Kojima M (1982) An electron microscopical study on peroxidase activity of rabbit monocytes, resident and exudate macrophages. Acta Pathol Jpn 32:445–460
Pino RM, Bankston PW (1979) The development of the sinusoids of fetal rat liver: Localization of endogenous peroxidase in fetal Kupffer cells. J Histochem Cytochem 27:643–652
Sakuma H, Kasajima T, Imai Y, Kojima M (1981) An electron microscopic study on the reticuloendothelial cells in the lymph nodes. Acta Pathol Jpn 31:449–472
Takahashi K, Sakuma H, Naito M, Yaginuma Y, Takahasi H, Asano S, Hojo H, Kojima M (1980) Cytological characters, transformation, and ontogenesis of dermal histiocytes and fibroblasts of rats. Acta Pathol Jpn 30:743–766
Watanabe K, Sasadaira H, Komatsu N, Izumi S, Ozawa A, Ohnishi N (1980) Enzyme histochemical properties of macrophages under various conditions. In: Abstract of a Naito Foundation Symposium on Biological Defense Mechanisms (II). The Naito Foundation, Tokyo, pp 1–2
Wisse E (1974) Observations on the fine structure and peroxidase cytochemistry of normal rat liver Kupffer cells. J Ultrastruct Res 46:393–426
Author information
Authors and Affiliations
Additional information
Supported by Grant-in-Aid for Cancer Research from the Ministry of Education, Science and Culture, Japan (No. 401057)
Rights and permissions
About this article
Cite this article
Takahashi, K., Takahashi, H., Naito, M. et al. Ultrastructural and functional development of macrophages in the dermal tissue of rat fetuses. Cell Tissue Res. 232, 539–552 (1983). https://doi.org/10.1007/BF00216427
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00216427