Summary
The kinetics of the effects of acute administration and of multiple injections of TSH on the ultrastructure of the thyroid of the dog were studied. The results are correlated with data obtained by light microscopy and by biochemical study of the tissue. The response to TSH is more delayed in the dog than in the rat; it is characterized by interfollicular and intrafollicular heterogeneity: only after 3 hours do all thyroid cells demonstrate signs of stimulation. The stimulation of each thyroid cell results in three overlapping stages: colloid phagocytosis, colloid digestion and morphological changes suggesting increased biosynthetic activity. The former effects are concomitant with the effects of TSH on the secretory process in vivo and the metabolic activation of thyroid slices in vitro; the latter effect parallels an increased RNA content of the tissue. Thyroids stimulated for 3 and 6 days by TSH exhibit marked hyperplasia and cellular hypertrophy. The colloid is scant and no colloid droplets are evident. After three days of TSH administration, numerous intracellular spaces, containing colloid are observed.
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Bauer, W. C., Meyer, J. S.: Origin and fate of colloid droplets of the thyroid gland. Lab. Invest. 14, 1795–1808 (1965).
Burton, K.: A study of the conditions and mechanism of the diphenylamine reaction for the coloumetric estimation of deoxyribonucleic acid. Biochem. J. 62, 315–323 (1956).
Creek, R. D.: Effect of thyrotropin on the weight, protein, ribonucleic acids, and the radioactive phosphorus uptake of chick thyroids. Endocrinology 76, 1124–1133 (1965).
Dempsey, E. W., Peterson, R. R.: Electron microscopic observations on the thyroid glands of normal, hypophysectomized, cold exposed and thiouracil-treated rat. Endocrinology 56, 46–58 (1955).
Dumont, J. E.: Le métabolisme du glucose dans le tissu thyroïdien et sa régulation par l'hormone thyréotrope. Ann. Soc. roy. Sc. Méd. Natur. Brux. 18, 111–241 (1965).
—, Rocmans, P.: In vivo effects of thyrotropin on the metabolism of the thyroid gland. J. Physiol. (Lond.) 174, 26–45 (1964a).
- - Effects of TSH in isolated thyroid preparations and in the whole dog. Proceed. 2nd Intern. Congr. Endocr., p. 81–86. Ser. 83: Excerpta Medica 1964b.
—, Tondeur-Montenez, T.: Action de l'hormone thyréotrope sur le métabolisme énergétique du tissu thyroïdien. III — Evaluation au moyen du (14C) glucose des voies du métabolisme du glucose dans le tissu thyroïdien de chien. Biochim. biophys. Acta (Amst.) 111, 258–272 (1965).
Ekholm, R., Smeds, S.: On dense bodies and droplets in the follicular cells of the guinea pig thyroid. J. Ultrastruct. Res. 16, 71–82 (1966).
Fabre, M., Marescaux, J.: Structure et ultrastructure d'auto et d'homo-greffons thyroïdiens intratesticulaires chez le cobaye thyroïdectomisé. Z. Zellforsch. 84, 328–341 (1968).
Fiala, S., Sproul, E. E., Fiala, A. E.: Regulation by anterior pituitary hormones of nucleic acids in dependent endocrine glands. Proc. Soc. exp. Biol. (N. Y.) 94, 517–520 (1957).
Fleck, A., Begg, D.: The estimation of ribonucleic acid using ultraviolet absorption measurements. Biochim. biophys. Acta (Amst.) 108, 333–339 (1965).
Freinkel, N.: The intermediary metabolism of thyroid tissue in the thyroid gland. Ed. by Pitt-Rivers, R., and Trotter, W. R., p. 131–162. London: Butterworths 1964.
Fujita, H., Honma, Y.: Electron microscopical studies on the thyroid of a cyclostome, Lampetra japonica, during its upstream migration. Z. Zellforsch. 73, 559–575 (1966).
Gedda, O.: On the effect of thyrotropic hormone on thyroid in the guinea pig. Acta endocr. (Kbh.), Suppl. 56, 1–93 (1960).
Heiman, P.: Ultrastructure of human thyroid. Acta endocr. (Kbh.), Suppl. 110, 1–102 (1966).
Heyningen, H. E. van: Correlated light and electron microscopic observations on glycoprotein containing globules in the follicular cells of the thyroid gland of the rat. J. Histochem. Cytochem. 13, 286–295 (1965).
Karnovsky, M. J.: Simple method for “staining with lead” at high pH in electron microscopy. J. Cell Biol. 11, 729–731 (1961).
Kerkof, P. R., Tata, J. R.: Simultaneous acceleration in vivo of the formation of thyroid ribonucleic acid, phospholipid and iodoprotein by thyroid stimulating hormone. Biochem. biophys. Res. Commun. 28, 111–116 (1967).
Kosanovic, M., Ekholm, R., Stranberg, U., Smeds, S.: The effect of the TSH on the acid phosphatase and thyroglobulin hydrolyzing activities in the guinea pig thyroid. Exp. Cell Res. 52, 147–160 (1968).
Luft, J.: Improvements in epoxy embedding methods. J. Cell Biol. 9, 409–414 (1961).
Lupulescu, A., Petrovici, A.: Ultrastructure of the thyroid gland. London: W. Heinemann Medical Books. 1968.
Matovinovic, J., Vickery, P.: Relation of nucleic acids to the structure and function of the guinea pig thyroid gland. Endocrinology 64, 149–159 (1959).
McKenzie, J. M.: The long-acting thyroid stimulator: its role in Grave disease. Recent Progr. Hormone Res. 23, 1646 (1967).
Millonig, G.: Further observations on a phosphate buffer for osmium solutions. Vth Intern. Congr. Electron Microscopy, p. 8. Philadelphia: Academic Press 1962.
Nadler, N. J., Sarkar, S. K., Leblond, C. P.: Origin of intracellular colloid droplets in the rat thyroid. Endocrinology 71, 120–129 (1962).
Nakken, K. F.: Endocytosis of thyroglobulin and the release of thyroid hormone. Scand. J. clin. Lab. Invest., Suppl. 106, 125–143 (1969).
Nève, P.: Ultrastructure des cellules folliculaires d'une thyroide humaine normale. J. Microscopie 4, 811–814 (1965).
—: The ultrastructure of thyroid in chronic autoimmune thyroiditis. Virchows Arch. path. anat. Abt. A Path. Anat. 346, 302–317 (1969).
Pantic, V.: Ultrastructure of deer and Roe-Buck thyroid. Z. Zellforsch. 81, 487–500 (1967).
Reynolds, E. S.: The use of lead citrate at high pH as electron opaque stain in electron microscopy. J. Cell Biol. 17, 208–213 (1963).
Seljelid, R.: Endocytosis in thyroid follicle cells. I. Structure and significance of different types of single membrane-limited vacuoles and bodies. J. Ultrastruct. Res. 17, 195–220 (1967a).
—: Endocytosis in thyroid follicle cells. II. A microinjection study of the origin of colloid droplets. J. Ultrastruct.Res. 17, 401–420 (1967b).
—: Endocytosis in thyroid follicle cells. III. An electron microscopy study of the cell surface and related structures. J. Ultrastruct. Res. 18, 1–24 (1967c).
—: Endocytosis in thyroid follicle cells. IV. On the acid phosphatase activity in thyroid follicle cells, with special reference to the quantitative aspect. J. Ultrastruct. Res. 18, 237–256 (1967d).
—: Endocytosis in thyroid follicle cells. V. On the redistribution of cytosomes following stimulation with thyrotropic hormone. J. Ultrastruct. Res. 18, 479–488 (1967e).
Sheldon, H., McKenzie, J. M., Nimwegan, D. van: Electron microscopic autoradiography. The localization of 125I in suppressed and thyrotropin stimulated mouse thyroid gland. J. Cell Biol. 23, 200–205 (1964).
Sobel, H. J., Geller, J.: Experimental thyroiditis in the guinea pig. II. Electron microscopy. Amer. J. clin. Path. 46, 149–163 (1965).
Solomon, D. H.: Effects of thyrotropin on thyroidal water and electrolytes in the chick. Endocrinology 69, 939–957 (1961).
Sonenberg, M.: Chemistry and physiology of the thyroid stimulating hormone. Vitam. and Horm. 16, 205–261 (1968).
Stein, O., Gross, J.: Metabolism of 125I in the thyroid gland studied with electron microscopic autoradiography. Endocrinology 75, 787–798 (1964).
Tashiro, M., Sugiyama, S.: Electron microscopic studies of the follicle cells in the thyroid gland of the dog. Okajimas Folia anat. jap. 40, 131–159 (1964).
Tata, J.: The formation and distribution of ribosomes during hormone induced growth and development. Biochem. J. 104, 1–26 (1967).
Uotila, V. V., Kannas, O.: Quantitative histological method of determining the proportions of the principal components of thyroid tissue. Acta endocr. (Kbh.) 11, 49–60 (1952).
Wetzel, B. K., Spicer, S. S., Wollman, S. H.: Change in fine structure and rat acid phosphatase localization in rat thyroid cells following thyrotropin administration. J. Cell Biol. 25, 593–618 (1965).
Wissig, S. L.: The anatomy of secretion in the follicular cells of the thyroid gland. I. The fine structure of the gland in the normal rat. J. biophys. biochem. Cytol. 7, 419–432 (1960).
—: The anatomy of secretion in the follicular cells of the thyroid gland. II. The effect of acute thyrotropic hormone stimulation on the secretory apparatus. J. Cell Biol. 16, 93–117 (1963).
Wollman, S. H., Spicer, S. S., Burstone, M. S.: Localization of esterase and acid phosphatase in granules and colloid droplets in rat thyroid epithelium. J. Cell Biol. 21, 191–201 (1964).
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Work carried out in part under contract Euratom — University of Brussels — University of Pisa n∘ 026-63-4 BIAC, and supported by grant 1011 of the Fonds de la Recherche Scientifique Médicale and a grant of the Fonds National de la Recherche Scientifique (Crédit aux Chercheurs: P. Nève).
Our thanks are due to Professor P. Dustin for his help, to Doctor P. Rocmans for his surgical assistance, to Miss E. Bricourt and Mr. G. Vienne for their technical assistance, and to Miss Ch. Borrey for the typing of the manuscript.
Contribution n∘ 496 of the Biology Department, Euratom.
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Néve, P., Dumont, J.E. Time sequence of ultrastructural changes in the stimulated dog thyroid. Z. Zellforsch. 103, 61–74 (1970). https://doi.org/10.1007/BF00335401
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DOI: https://doi.org/10.1007/BF00335401