Summary
The thyroid gland of adult salamanders, Hynobius nebulosus, in the breeding season was studied by electron microscopy. The follicular cells are different in cell height and fine structures; the taller cells with many cell organelles and granules and the lower cells with a few cell organelles and granules are both present in the same follicle. In the cytoplasm, three types of membrane-bounded granules, namely, cytosomes, colloid droplets, and vacuolar bodies and circular membrane complexes occur. The vacuolar bodies are subdivided into two types; the ordinary type having loosely distributed particles and the specific type containing tubules and/or closely packed filaments, crystalloid structures, except for the particles. The chromophobe colloids within the Bensley-cells correspond to extremely large, ordinary type vacuolar bodies, while the Langendorff-colloid cells possess increased numbers of granular cisternae of endoplasmic reticulum and a ribosome-rich, dense cytoplasmic matrix but not extremely large colloid. The intracytoplasmic circular membrane complexes appear in the Golgi area of cytosome-rich cells. It is suggested that they originate from the Golgi apparatus which was activated to produce many cytosomes. Intranuclear inclusions consisting of microtubules and filaments and tight junctions between two adjacent lateral plasma membranes are occasionally encountered.
Similar content being viewed by others
References
Arstila, A. U., Hopsu-Havu, V. K.: Nuclear and cytoplasmic microfilaments in the pineal chief cells of the rat. Z. Zellforsch. 80, 22–28 (1967).
Bargmann, W.: Die Schilddrüse. In: Handbuch der mikroskopischen Anatomie des Menschen (W. v. Möllendorff, ed.), Bd VI/2. Berlin: Springer 1939.
Blähser, S., Schnorr, B.: Ultrastructur der Thyrozyten der Ratte in alimentärem Tocopherolund Ubichinonmangel und nach Substitution. Z. Zellforsch. 114, 493–514 (1971).
Boquist, L.: Intranuclear rods in pancreatic islet β-cells. J. Cell Biol. 43, 377–381 (1969).
Büttner, D. W., Horstmann, E.: Stabförmige Strukturen im Interphasenkern von Epithelgeweben. Exp. Cell Res. 49, 686–687 (1968).
Coleman, R., Evennett, P. J., Dodd, J. M.: Ultrastructural observations on the thyroid gland of Xenopus laevis Daudin throughout metamorphosis. Gen. comp. Endocr. 10, 34–46 (1968a).
Coleman, R., Evennett, P. J., Dodd, J. M.: Ultrastructural observations on the droplets of experimentally-induced goitres in Xenopus laevis with special reference to the development of Uhlenhuth colloid cells. Z. Zellforsch. 84, 490–496 (1968 b).
Coleman, R., Evennett, P. J., Dodd, J. M.: Ultrastructural observations on some membranous cytoplasmic inclusion bodies in follicular cells of experimentally-induced goitres in tadopoles and toads of Xenopus laevis Daudin. Z. Zellforsch. 84, 497–505 (1968 c).
Donev, S., Petkov, P.: Intranuclear tubular bodies in islet cells. Arch. histol. jap. 33, 351–355 (1971).
Ekholm, R., Sjöstrand, F. S.: The ultrastructural organization of mouse thyroid gland. J. Ultrastruct. Res. 1, 178–199 (1957).
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).
Fujita, H.: Electron microscopic studies on the thyroid gland of domestic fowl, with special reference to the mode of secretion and the occurrence of a central flagellum in the follicular cell. Z. Zellforsch. 60, 615–632 (1963).
Fujita, H.: Some observations on the fine structure of thyroids of hibernating and aroused bats. Z. Zellforsch. 121, 301–318 (1971).
Fujita, H., Homma, Y.: Electron microscopical studies on the thyroid of a cyclostoma, Lampetra japonica, during its upstream migration, Z. Zellforsch. 73, 559–575 (1966).
Fujita, H., Machino, M.: Electron microscopic studies on the thyroid gland of a teleost, Seriola quinqueradiata. Anat. Rec. 152, 81–98 (1965).
Fujita, H., Machino, M., Nakagami, K.: Electron microscopic studies on the rat thyroid gland following administration of propylthiouracil and thyradin, with special reference to the inclusion body to the follicular cell. Okajimas Fol. anat. jap. 39, 157–177 (1963).
Fujita, H., Suemasa, H., Homma, Y.: An electron microscopic study of the thyroid gland of the silver eel, Anguilla japonica. Arch. histol. jap. 27, 153–163 (1966).
Hearing, V. J., Eppig, J. T., Jr: Electron microscopy of the normal and I131 treated thyroid gland of the newt, Notophthalmus viridescens. J. Morph. 128, 369–386 (1969).
Herman, L.: An electron microscope study of the salamander thyroid during hormonal stimulation. J. biophys. biochem. Cytol. 7, 143–150 (1960).
Irie, M.: Electron microscopic observation on the various mammalian thyroid glands (in Japanese with English summary) Arch. histol. jap. 19, 39–74 (1960).
Karlsson, U.: Three-dimensional studies of neurons in the lateral geniculate nucleus of the rat. I. Organelle organization in the perikaryon and its proximal branches. J. Ultrastruct. Res. 16, 429–481 (1966).
Kitoh, J.: Electron microscopic observations on the thyroid gland of the elasmobranchs. Okajimas Folia Anat. jap. 46, 41–57 (1969).
Klinck, G. H., Oertel, J. E., Winship, T.: Ultrastructure of normal human thyroid. Lab. Invest. 22, 2–22 (1970).
Langendorff, O.: Beiträge zur Kenntnis der Schilddrüse. Arch. Anat. Physiol., Physiol. Abth. Suppl., 219–242 (1889).
Larsen, J. H., Jr: Ultrastructure of thyroid follicle cells of three salamanders (Ambystoma, Amphiuma and Necturus) exhibiting varying degrees of neoteny. J. Ultrastruct. Res. 24, 190–209 (1968).
Magalhães, M. M.: Intranuclear bodies in cell of rabbit and rat retina. Exp. Cell. Res. 47, 628–632 (1968).
Müller, O., Ratzenhofer, M.: Intranukleäre Einschlüsse in endokrinen Zellen des Kaninchenmagens. Z. Zellforsch. 117, 526–536 (1971).
Muramoto, K.: Comparative electron microscopic studies of the thyroid glands of lower vertebrates. Okajimas Folia Anat jap. 39, 321–342 (1964).
Nadler, N. J., Young, B. A., Leblond, C. P., Mitmaker, B.: Elaboration of thyroglobulin in the thyroid follicle, Endocrinology, 74, 333–354 (1964).
Nakai, Y., Gorbman, A.: Cytological and functional properties of the thyroid of a chimaeroid fish, Hydrolagus colliei. Gen. comp. Endocr. 13, 285–302 (1969).
Nakai, Y., Nanba, H., Fujita, H.: Fine structure and functional properties of the thyroid of the anura, Rana nigromaculata nigromaculata, Arch. histol. jap. 31, 421–432 (1970).
Novikoff, P. M., Novikoff, A. B., Quintana, N., Hauw, J.-J.: Golgi apparatus, GERL, and lysosomes of neurons in rat dorsal root ganglia, studied by thick section and thin section cytochemistry. J. Cell. Biol. 50, 859–886 (1971).
Novikoff, A. B., Quintana, N., Villaverde, H., Forschirm, R.: The Golgi zone of neurons in rat spinal ganglia. J. Cell Biol. 23, 68A (1964).
Nunez, E. A., Becker, D. V.: Secretory processes in follicular cells of the bat thyroid. I. Ultrastructural changes during the pre-, early and mid-hibernation periods with some comments on the origin of autophagic vacuoles. Amer. J. Anat. 129, 369–398 (1970).
Regard, E., Mauchamp, J.: Ultrastructure de la glande thyroïde du Xénope larvaire normal et hypophysectomisé: corrélations avec la biosynthèse de la thyroglobuline. J. Ultrastruct. Res. 37, 664–678 (1971).
Reynolds, F. S.: The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol. 17, 208–212 (1963).
Seljelid, R.: Electron microscopic localization of acid phosphatase in rat thyroid follicle cells after stimulation with thyrotropic hormone. J. Histochem. Cytochem. 13, 687–690 (1965).
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, 195–219 (1967 a).
Seljelid, R.: Endocytosis in thyroid follicle cells. II. A microinjection study of the origin of colloid droplets. J. Ultrastruct. Res. 17, 401–420 (1967 b).
Seljelid, R.: Endocytosis in thyroid follicle cells. III. An electron microscopic study of the cell surface and related structures. J. Ultrastruct. Res. 18, 1–24 (1967 c).
Seljelid, R.: Endocytosis in thyroid follicle cells. IV. On the acid phosphatase activity in thyroid follicle cells, with special reference to the quantitative aspects. J. Ultrastruct. Res. 18, 237–256 (1967 d).
Sheldon, M., McKenzie, J. M., Van Nimwegan, D.: Electron microscopic autoradiography. The localization of I125 in suppressed and thyrotropin-stimulated mouse thyroid gland. J. Cell Biol. 23, 200–205 (1964).
Siegesmund, K. A., Dutta, C. R., Fox, C. A.: The ultrastructure of the intranuclear rodlet in certain nerve cells. J. Anat. (Lond.) 98, 93–97 (1964).
Stein, O., Gross, J.: Metabolism of I125 in the thyroid gland studied with electron microscopic autoradiography, Endocrinology, 75, 787–798 (1964).
Suemasa, W., Homma, Y., Fujita, H.: Electron microscopic observations on the thyroid gland of two species of teleost, Semicossyphus reticulatus and Sebastiscus marmoratus. Arch. histol. jap. 29, 363–375 (1968).
Uhlenhuth, E.: Die Kolloidzelle und ihre Funktion in der Schilddrüse des Marmorsalamanders. Z. Zool. 125, 483–501 (1925).
Uhlenhuth, E.: Die Morphologie und Physiologie der Salamander-Schilddrüse, Arch. Entwickl.-Mech. org. 109, 611–749 (1927).
Van Heyningen, H. E.: Correlated light and electron microscope observations on glycoprotein-containing globules in the follicular cells of the thyroid gland of the rat. J. Histochem. Cytochem. 13, 286–295 (1965).
Watari, N.: Elektronenmikroskopische Untersuchungen über die Schilddrüse bei der Schlange (Natrix tigrina tigtina) (in Japanese with German summary). Arch. histol. jap. 23, 21–51 (1962).
Watson, M. L.: Staining of tissue section for electron microscopy with heavy metals. J. biophys. biochem. Cytol. 4, 475–478 (1958).
Weindl, A., Schwink, A., Wetzstein, R.: Intranucleäre Tubuli-Bündel im Gefäßorgan der Lamina terminalis. Naturwissenschaften 54, 473 (1967).
Wetzel, B. K., Spicer, S. S., Wollmann, S. H.: Changes in fine structure and acid phosphatase localization in rat thyroid cells following thyrotropin administration. J. Cell Biol. 25, 593–618 (1965).
Whur, P., Herscovics, A., Leblond, C. P.: Radioautographic visualization of the incorporation of galactose-3H and mannose-3H by rat thyroids in vitro in relation to the stages of thyroglobulin synthesis. J. Cell Biol. 43. 289–311 (1969).
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).
Yoshimura, F., Irie, M.: Licht- und Elektronenmikroskopische Studie an den Kristalloiden in der Schilddrüsenzelle. Z. Zellforsch. 55, 204–219 (1961).
Youson, J., Heyningen, H. van: Dense granules (lysosomes ?) and crystals in the thyroids of senile rats. Amer. J. Anat. 122, 377–396 (1968).
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Setoguti, T. Electron microscopic study on the thyroid gland of the salamander Hynobius nebulosus in the breeding season. Z. Zellforsch 137, 177–194 (1973). https://doi.org/10.1007/BF00307429
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00307429