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Electron microscopic study on the thyroid gland of the salamander Hynobius nebulosus in the breeding season

I. Observation under normal conditions

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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.

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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).

    PubMed  Google Scholar 

  • Bargmann, W.: Die Schilddrüse. In: Handbuch der mikroskopischen Anatomie des Menschen (W. v. Möllendorff, ed.), Bd VI/2. Berlin: Springer 1939.

    Google Scholar 

  • Blähser, S., Schnorr, B.: Ultrastructur der Thyrozyten der Ratte in alimentärem Tocopherolund Ubichinonmangel und nach Substitution. Z. Zellforsch. 114, 493–514 (1971).

    PubMed  Google Scholar 

  • Boquist, L.: Intranuclear rods in pancreatic islet β-cells. J. Cell Biol. 43, 377–381 (1969).

    Article  PubMed  Google Scholar 

  • Büttner, D. W., Horstmann, E.: Stabförmige Strukturen im Interphasenkern von Epithelgeweben. Exp. Cell Res. 49, 686–687 (1968).

    PubMed  Google Scholar 

  • 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).

    PubMed  Google Scholar 

  • 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).

    PubMed  Google Scholar 

  • 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).

    PubMed  Google Scholar 

  • Donev, S., Petkov, P.: Intranuclear tubular bodies in islet cells. Arch. histol. jap. 33, 351–355 (1971).

    PubMed  Google Scholar 

  • Ekholm, R., Sjöstrand, F. S.: The ultrastructural organization of mouse thyroid gland. J. Ultrastruct. Res. 1, 178–199 (1957).

    PubMed  Google Scholar 

  • 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).

    PubMed  Google Scholar 

  • 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).

    PubMed  Google Scholar 

  • Fujita, H.: Some observations on the fine structure of thyroids of hibernating and aroused bats. Z. Zellforsch. 121, 301–318 (1971).

    Google Scholar 

  • 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).

    PubMed  Google Scholar 

  • Fujita, H., Machino, M.: Electron microscopic studies on the thyroid gland of a teleost, Seriola quinqueradiata. Anat. Rec. 152, 81–98 (1965).

    PubMed  Google Scholar 

  • 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).

    Google Scholar 

  • 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).

    PubMed  Google Scholar 

  • 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).

    PubMed  Google Scholar 

  • Herman, L.: An electron microscope study of the salamander thyroid during hormonal stimulation. J. biophys. biochem. Cytol. 7, 143–150 (1960).

    PubMed  Google Scholar 

  • Irie, M.: Electron microscopic observation on the various mammalian thyroid glands (in Japanese with English summary) Arch. histol. jap. 19, 39–74 (1960).

    Google Scholar 

  • 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).

    PubMed  Google Scholar 

  • Kitoh, J.: Electron microscopic observations on the thyroid gland of the elasmobranchs. Okajimas Folia Anat. jap. 46, 41–57 (1969).

    Google Scholar 

  • Klinck, G. H., Oertel, J. E., Winship, T.: Ultrastructure of normal human thyroid. Lab. Invest. 22, 2–22 (1970).

    PubMed  Google Scholar 

  • 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).

    PubMed  Google Scholar 

  • Magalhães, M. M.: Intranuclear bodies in cell of rabbit and rat retina. Exp. Cell. Res. 47, 628–632 (1968).

    Google Scholar 

  • Müller, O., Ratzenhofer, M.: Intranukleäre Einschlüsse in endokrinen Zellen des Kaninchenmagens. Z. Zellforsch. 117, 526–536 (1971).

    PubMed  Google Scholar 

  • Muramoto, K.: Comparative electron microscopic studies of the thyroid glands of lower vertebrates. Okajimas Folia Anat jap. 39, 321–342 (1964).

    Google Scholar 

  • Nadler, N. J., Young, B. A., Leblond, C. P., Mitmaker, B.: Elaboration of thyroglobulin in the thyroid follicle, Endocrinology, 74, 333–354 (1964).

    PubMed  Google Scholar 

  • Nakai, Y., Gorbman, A.: Cytological and functional properties of the thyroid of a chimaeroid fish, Hydrolagus colliei. Gen. comp. Endocr. 13, 285–302 (1969).

    PubMed  Google Scholar 

  • 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).

    PubMed  Google Scholar 

  • 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).

    Article  PubMed  Google Scholar 

  • Novikoff, A. B., Quintana, N., Villaverde, H., Forschirm, R.: The Golgi zone of neurons in rat spinal ganglia. J. Cell Biol. 23, 68A (1964).

    Google Scholar 

  • 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).

    PubMed  Google Scholar 

  • 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).

    PubMed  Google Scholar 

  • 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).

    Article  PubMed  Google Scholar 

  • 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).

    PubMed  Google Scholar 

  • 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).

    PubMed  Google Scholar 

  • 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).

    PubMed  Google Scholar 

  • 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).

    PubMed  Google Scholar 

  • 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).

    PubMed  Google Scholar 

  • 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).

    Article  PubMed  Google Scholar 

  • 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).

    PubMed  Google Scholar 

  • Stein, O., Gross, J.: Metabolism of I125 in the thyroid gland studied with electron microscopic autoradiography, Endocrinology, 75, 787–798 (1964).

    PubMed  Google Scholar 

  • 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).

    PubMed  Google Scholar 

  • Uhlenhuth, E.: Die Kolloidzelle und ihre Funktion in der Schilddrüse des Marmorsalamanders. Z. Zool. 125, 483–501 (1925).

    Google Scholar 

  • Uhlenhuth, E.: Die Morphologie und Physiologie der Salamander-Schilddrüse, Arch. Entwickl.-Mech. org. 109, 611–749 (1927).

    Google Scholar 

  • 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).

    PubMed  Google Scholar 

  • 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).

    PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Weindl, A., Schwink, A., Wetzstein, R.: Intranucleäre Tubuli-Bündel im Gefäßorgan der Lamina terminalis. Naturwissenschaften 54, 473 (1967).

    Google Scholar 

  • 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).

    Article  PubMed  Google Scholar 

  • 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).

    Article  PubMed  Google Scholar 

  • 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).

    Article  PubMed  Google Scholar 

  • Yoshimura, F., Irie, M.: Licht- und Elektronenmikroskopische Studie an den Kristalloiden in der Schilddrüsenzelle. Z. Zellforsch. 55, 204–219 (1961).

    PubMed  Google Scholar 

  • Youson, J., Heyningen, H. van: Dense granules (lysosomes ?) and crystals in the thyroids of senile rats. Amer. J. Anat. 122, 377–396 (1968).

    PubMed  Google Scholar 

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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

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