Skip to main content
Log in

Ultrastructure of differentiating cells during thymus histogenesis

A light and electron microscopic study of epithelial and lymphoid cell differentiation during thymus histogenesis in C57 black mice

  • Published:
Zeitschrift für Zellforschung und Mikroskopische Anatomie Aims and scope Submit manuscript

Summary

Thymus development was studied from twelve days after fertilization to four days post-partum. At twelve days, the endodermal bud consists of primitive undifferentiated cells containing a paucity of organelles separated from branchial mesenchyme by a fine fibrillar interface. Multivacuolar structures in the extracellular spaces or just within cell borders may represent a pathway for transfer of humoral substances.

At thirteen days, outgrowing processes of anlage cells disrupt the epithelial cords and free adjoining cells. Some of these round up and differentiate to conform to criteria identifying them as lymphocyte precursors. Transitional forms with some lymphoid characteristics were noted.

At fifteen days trabeculae carrying invasive blood vessels lobulate a now recognizable thymus. Several species of epithelial cells become distinguishable in the last quarter of gestation. Dendrite-like processes of stromal cells are crowded with vacuolar and lamellar membranous elements, mitochondria, ribosomes and innumerable small vesicles. Increasingly, many columnar cells of the medulla demonstrate pleomorphic inclusions resembling lysosomes, lipid droplets and secretion products.

These studies suggest that earliest thymocytes may originate by transformation of anlage epithelium and that the ultrastructure of many epithelial cells and the presence of endothelial pores places the thymus among organs active in synthesizing and secretory processes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Literature

  • Ackerman, G. A.: Cytochemistry of the lymphocytes. Phase microscope studies. In: The lymphocytes and lymphocytic tissue (J. W. Rebuck, ed.). New York: Paul B. Hoeber 1960.

    Google Scholar 

  • —: Electron microscopy of the bursa of Fabricius of the embryonic chick with particular reference to the lympho-epithelial nodules. J. Cell Biol. 13, 127–146 (1962).

    Google Scholar 

  • —, and R. A. Knouff: The epithelial origin of the lymphocyte in the thymus of the embryonic hamster. Anat. Rec. 152, 35–53 (1965).

    Google Scholar 

  • Archer, O., B. W. Papermaster, and R. A. Good: Thymectomy in rabbit and mouse: Consideration of time of lymphoid peripheralization. In: The thymus in immunobiology (R. A. Good and A. E. Gabrielsen, eds.). New York: Harper & Row. 1964.

    Google Scholar 

  • Auerbach, R.: Morphogenetic interactions in the development of the mouse thymus gland. Develop. Biol. 2, 271–284 (1960).

    Google Scholar 

  • —: Experimental analysis of the origin of cell types in the development of the mouse thymus. Develop. Biol. 3, 336–354 (1961).

    Google Scholar 

  • —: Developmental studies of mouse thymus and spleen. Nat. Cancer Inst. Monogr. 11, 23–33 (1963).

    Google Scholar 

  • Axelrad, A. A., and H. C. van der Gaag: Susceptibility to lymphoma induction by Gross's passage A virus in C3H/B mice of different ages. Relation to thymus cell multiplication and differentiation. J. nat. Cancer Inst. 28, 1065–1093 (1962).

    Google Scholar 

  • Baillif, R. N.: Thymic involution and regeneration in the albino rat following injection of acid colloidal substances. Amer. J. Anat. 84, 457–510 (1949).

    Google Scholar 

  • Beard, J.: The source of leukocytes and the true function of the thymus. Anat. Anz. 18, 550–573 (1900).

    Google Scholar 

  • —: The origin and histogenesis of the thymus in Raja batis. Zool. Jahrb., Abt. Anat. Ontog. 17. 403–480 (1903).

    Google Scholar 

  • Bell, E. T.: The development of the thymus. Amer. J. Anat. 5, 29–62 (1906).

    Google Scholar 

  • Biava, C.: Identification and structural forms of human particulate glycogen. Lab. Invest. 12, 1179–1197 (1963).

    Google Scholar 

  • Bloom, W.: Lymphocytes and monocytes. In: Handbook of haematology (H. Downey, ed.). New York: Paul B. Hoeber 1938.

    Google Scholar 

  • Clark jr., S. L.: The thymus in mice of strain 129 J studied with the electron microscope. Amer. J. Anat. 112, 1–34 (1963).

    Google Scholar 

  • —: Cytological evidence of secretion in the thymus. In: Ciba Foundation Symposium, “The thymus: Experimental and clinical studies” (G. E. W. Wolstenholme, and R. Porter, eds.). Boston: Little, Brown & Co. 1966.

    Google Scholar 

  • Cooper, M. D., R. D. A. Peterson, M. A. South, and R. A. Good: The functions of the thymus system and the bursa system in the chicken. J. exp. Med. 123, 75–102 (1966).

    Google Scholar 

  • Deansley, R.: The structure and development of the thymus in fish, with special reference to Salmo fario. Quart. J. micr. Sci. 71, 113–146 (1927).

    Google Scholar 

  • Dustin, A. P.: Thymus et hématopoièse. Strasbourg méd. 85, 192–198 (1927).

    Google Scholar 

  • Fawcett, D. W.: Changes in the fine structure of the cytoplasmic organelles during differentiation. In: Developmental cytology (D. Rudnick, ed.). New York: Ronald Press 1959.

    Google Scholar 

  • —: Comparative observations on the fine structure of blood capillaries. In: The peripheral blood vessels (J. L. Orbison and D. E. Smith, eds.). Baltimore: Williams & Wilkins Co. 1963.

    Google Scholar 

  • Globerson, A., and M. Feldman: Role of the thymus in restoration of immune reactivity and lymphoid regeneration in irradiated mice. Transplant. 2, 212–227 (1964).

    Google Scholar 

  • Goldstein, A. L., F. D. Slater, and A. White: Preparation, assay and partial purification of a thymic lymphocytopoietic factor (Thymosin). Proc. nat. Acad. Sci. (Wash.) 56, 1010–1017 (1966).

    Google Scholar 

  • Good, R. A., A. P. Dalmasso, C. Martinez, O. K. Archer, J. C. Pierce, and B. W. Papermaster: The role of the thymus in development of immunological capacity in rabbits and mice. J. exp. Med. 116, 773–796 (1962).

    Google Scholar 

  • Granboulan, N.: Étude au microscope électronique des cellules de la lignée lymphocytaire normale. Rev. Hémat. 15, 52–71 (1960).

    Google Scholar 

  • Grobstein, C.: Kidney tubule induction in mouse metanephrogenic mesenchyme without cytoplasmic contact. J. exp. Zool. 135, 57–67 (1957).

    Google Scholar 

  • Hammar, J. A.: The new views as to the morphology of the thymus gland and their bearing on the problems of the thymus. Endocrinology 5, 731–760 (1921).

    Google Scholar 

  • Harland, J.: Early histogenesis of the thymus in the white rat. Anat. Rec. 77, 247–271 (1940).

    Google Scholar 

  • Hoshino, T.: The fine structure of ciliated vesicle-containing reticular cells in the mouse thymus. Exp. Cell Res. 27, 615–617 (1962).

    Google Scholar 

  • Izard, J.: Ultrastructure of the thymic reticulum in the guinea pig. Cytological aspects of the problem of thymic secretion. Anat. Rec. 155, 117–121 (1966).

    Google Scholar 

  • Kalmutz, J. E.: Antibody production in the opossum embryo. Nature (Lond.) 193, 851–853 (1962).

    Google Scholar 

  • Kindred, J. E.: A quantitative study of the hematopoietic organs of young albino rats. Amer. J. Anat. 71, 207–243 (1942).

    Google Scholar 

  • Kölliker, R. A. v.: Entwicklungsgeschichte des Menschen und der höheren Thiere, p. 815–880. Leipzig: Wilhelm Engelmann 1879.

    Google Scholar 

  • Kohnen, P., and L. Weiss: An electron microscopic study of thymic corpuscles in guinea pig and mouse. Anat. Rec. 148, 29–57 (1964).

    Google Scholar 

  • Law, L. W., T. B. Dunn, N. Trainin, and R. H. Levey: Studies of thymic function. In: The thymus (V. Defendi, and D. Metcalf, eds.). Wistar Inst. Monograph No 2. Philadelphia: Wistar Institute Press 1964.

    Google Scholar 

  • Low, F. N.: Electron microscopy of the lymphocyte. In: The lymphocyte and lymphocytic tissue (J. W. Rebuck, ed.). New York: Paul B. Hoeber 1960.

    Google Scholar 

  • Low, F. N., and J. A. Freeman: Electron microscope atlas of normal and leukemic human blood. New York: McGraw-Hill Book Co. 1958.

    Google Scholar 

  • Luft, J. H.: Improvements in epoxy resin embedding methods. J. biophys. biochem. Cytol. 9, 409–414 (1961).

    Google Scholar 

  • Marshall, A. H. E., and R. G. White: The immunological reactivity of the thymus. Brit. J. exp. Path. 42, 379–385 (1961).

    Google Scholar 

  • Maximow, A.: Untersuchungen über Blut und Bindegewebe II. Über die Histogenese der Thymus bei Säugetieren. Arch. micr. Anat. 74, 525–621 (1909).

    Google Scholar 

  • Metcalf, D.: The thymic origin of the plasma-lymphocytosis-stimulating factor. Brit. J. Cancer 10, 442–457 (1956).

    Google Scholar 

  • Miller, J. F. A. P.: The immunological function of the thymus. Lancet 1961 II, 748–749.

  • —: The thymus and the development of immunologic responsiveness. Science 144, 1544–1550 (1964).

    Google Scholar 

  • Millonig, G.: Further observations on a phosphate buffer for osmium solutions in fixation. Fifth Int. Congress for Electron Microscopy (S. S. Breese, ed.). New York: Academic Press 1962.

    Google Scholar 

  • Osoba, D., and J. F. A. P. Miller: The lymphoid tissues and immune responses of neonatally thymectomized mice bearing thymus tissue in millipore diffusion chambers. J. exp. Med. 119, 177–194 (1964).

    Google Scholar 

  • Parrott, D. M. V., and J. East: Role of the thymus in neonatal life. Nature (Lond.) 195, 347–348 (1962).

    Google Scholar 

  • —, M. A. B. de Sousa, and J. East: Thymusdependent areas in the lymphoid organs of neonatally thymectomized mice. J. exp. Med. 123, 191–203 (1966).

    Google Scholar 

  • Reynolds, E. S.: The use of lead citrate at high pH as an electron opaque stain in electron microscopy. J. Cell Biol. 17, 208–212 (1963).

    Google Scholar 

  • Ruth, R. F.: Derivation of antibody producing cells from ectodermal and entodermal epithelia. Anat. Rec. 139, 270 (1961).

    Google Scholar 

  • Sabatini, D. D., K. G. Bensch, and R. J. Barrnett: Cytochemistry and electron microscopy. The preservation of cellular ultrastructure and enzymatic activity by aldehyde fixation. J. Cell Biol. 17, 19–58 (1963).

    Google Scholar 

  • Salkind, J.: Contributions histologiques à la biologie comparée du thymus. Arch. Zool. exp. gén. 55, 81 (1915).

    Google Scholar 

  • Sanel, F. T.: Effects of acute inanition and subsequent refeeding upon the thymi of weanling mice. An electron microscope study. (Abstr.). Anat. Rec. 148, 330–331 (1964).

    Google Scholar 

  • —, and W. M. Copenhaver: Histogenesis of mouse thymus studied with the light and electron microscopes. (Abstr.). Anat. Rec. 151, 410 (1965).

    Google Scholar 

  • Saunders Jr, J. W.: Death in embryonic systems. Science 154, 605–608 (1966).

    Google Scholar 

  • Ste. Marie, G., and C. P. Leblond: Cytologic features and cellular migration in the cortex and medulla of the thymus in the young rat. Blood 23, 275–299 (1964).

    Google Scholar 

  • Smith, C.: Studies on the thymus of the mammal. XIV. Histology and histochemistry of embryonic and early postnatal thymuses of C57/6 and AKR strain mice. Amer. J. Anat. 116, 611–629 (1965).

    Google Scholar 

  • Tanaka, H.: Mesenchymal and epithelial reticulum in lymph nodes and thymus of mice as revealed in the electron microscope. Ann. Rep. of the Inst. for Virus Res. Kyoto University 5, 146–169 (1962).

    Google Scholar 

  • Waksman, B. H., B. G. Arnason, and B. D. Jankovic: Role of the thymus in immune reactions in rats. III. Changes in the lymphid organs of thymectomized rats. J. exp. Med. 116, 187–206 (1962).

    Google Scholar 

  • Watson, M. L.: Staining of tissue sections for electron microscopy with heavy metals. J. biophys. biochem. Cytol. 4, 475–478 (1958).

    Google Scholar 

  • Weakley, B. S., D. I. Patt, and D. Shepro: Ultrastructure of the fetal thymus in the golden hamster. J. Morph. 115, 319–335 (1964).

    Google Scholar 

  • Weiss, L.: Electron microscopic observations on the vascular barrier in the cortex of the thymus of the mouse. Anat. Rec. 145, 413–438 (1963).

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

This study was supported by National Institutes of Health Grants 5 ROI-HE-06465 and 5 TI-GM-256.

The author wishes to express her appreciation to Professor W. M. Copenhaver for his valuable criticisms and encouragement during the course of this study and for his careful review of the manuscript. Indebtedness to Professor G. D. Pappas is also gratefully acknowledged.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sanel, F.T. Ultrastructure of differentiating cells during thymus histogenesis. Z. Zellforsch. 83, 8–29 (1967). https://doi.org/10.1007/BF00334735

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00334735

Keywords

Navigation