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The routine demonstration of C cells in human and animal thyroid glands

Value of a Simple Silver Stain

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Virchows Archiv B

Summary

The silver nitrate technique developed by Grimelius was slightly modified in order to obtain a reproducible and simple method for the staining of C cells in the thyroid gland. The reliability of this method was demonstrated by comparing its results with those of immunofluorescent, cytochemical and ultrastructural studies. This staining procedure gives good and permanent results even when applied to tissues first fixed several hours after death. Its use allows the routine evaluation of the number and distribution of C cells in human and animal tissues.

Zusammenfassung

Die von Grimelius entwickelte Silberimprägnation erwies sieh in leicht abgeänderter Form als reproduzierbare und einfache Darstellungsmethode für die C-Zellen der Schilddrüse. Die Zuverlässigkeit dieser Methode wurde mittels vergleichenden immunofluorescenzoptischen, cytochemischen und elektronenmikroskopischen Untersuchungen bewiesen. Die Silberimprägnation liefert gute Resultate auch an mehrere Stunden nach dem Tode fixiertem Gewebe. Zudem sind die Präparate haltbar. Diese Silberimprägnation erlaubt damit eine Routineauswertung von Anzahl und Verteilung der C-Zellen in menschlichem und tierischem Material.

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References

  • Altmann, H.-W.: Die parafollikuläre Zelle der Schilddrüse und ihre Beziehungen zu der gelben Zelle des Darmes. Beitr. path. Anat.104, 420–454 (1940).

    Google Scholar 

  • Azzali, G.: Prime osservazionial microscopio elettronioo sulle cellule parafolliculari della tiroide. Boll. Soc. ital. Biol. sper.38, 1319–1321 (1962).

    PubMed  CAS  Google Scholar 

  • — Ultrastructure des cellules parafolliculaires de la thyroïde chez quelques mammifères. Ann. Endocr. (Paris) suppl.25, 8–13 (1964).

    Google Scholar 

  • — Ultrastructure of Parafollicular Cells. In: Calcitonin: Symposium on thyrocalcitonin and C cells, p. 152–166. Edit, by S. Taylor. London: Heinemann 1968.

    Google Scholar 

  • Baber, E. C.: Contribution to minute anatomy of thyroid gland of dog. Phil. Trans. B166, 557–568 (1876).

    Article  Google Scholar 

  • Bensley, R. R.: The thyroid gland of the opossum. Anat. Rec.8, 431–440 (1914).

    Article  Google Scholar 

  • Bussolati, G., Pearse, A. G. E.: Immunofluorescent localization of calcitonin in the “C” cells of pig and dog thyroid. J. Endocr.37, 205–209 (1967).

    PubMed  CAS  Google Scholar 

  • — Förster, G. V., Clark, M. B., Pearse, A. G. E.: Immunofluorescent localization of calcitonin in medullary (C cell) thyroid carcinoma, using antibody to the pure porcine hormone. Virchows Arch. Abt. B Zellpath.2, 234–238 (1969)a.

    CAS  Google Scholar 

  • — Rost, F. W. D., Pearse, A. G. E.: Fluorescence metachromasia in polypeptide hormoneproducing cells of the APUD series, and its significance in relation to the structure of the precursor protein. Histochem. J.1, 517–530 (1969)b.

    Article  PubMed  CAS  Google Scholar 

  • Carvalheira, A. F., Pearse, A. G. E.: Comparative cytochemistry of C cells esterases in the mammalian thyroid-parathyroid complex. Histochemie8, 175–182 (1967).

    Article  PubMed  CAS  Google Scholar 

  • Copp, D. H., Cameron, E. C., Cheney, B. A., Davidson, A. G. F., Henze, K. G.: Evidence for calcitonin — a new hormone from the parathyroid that lowers blood calcium. Endocrinology70, 638–649 (1962).

    PubMed  CAS  Google Scholar 

  • — Cockcroft, D.W., Kueh, Y.: Calcitonin from Ultimobranchial glands of Dogfish and Chickens. Science158, 924–925 (1967).

    Article  PubMed  CAS  Google Scholar 

  • Dejardin, M.: Les cholinestérases dans la glande thyroïde du cobaye. C.R. Soc. Biol. (Paris)149, 621–622 (1955).

    CAS  Google Scholar 

  • Dietrich, F. M., Rittel, W.: Antigenic site(s) of synthetic human calcitonin M. Nature (Lond.)225, 75–76 (1970).

    Article  CAS  Google Scholar 

  • Dubois, P., Dumont, L.: Aspects ultrastructuraux des cellules parafolliculaires de la thyroïde du lapin en fonction de la nature du fixateur. C.R. Soc. Biol. (Lyon)12, 2331–2334 (1966).

    Google Scholar 

  • Dumont, L.: Activité cholinestérase de cellules parafolliculaires de la thyroïde. C.R. Ass. Anat.3, 480–485 (1956).

    Google Scholar 

  • Ekholm, R., Ericson, L. E.: The ultrastructure of the Parafollicular cells of the Thyroid Gland in the Rat. J. Ultrastruct. Res.23, 378–402 (1968).

    Article  PubMed  CAS  Google Scholar 

  • Ericson, L. E.: Degranulation of the Parafollicular Cells of the Rat thyroid by Vitamin D2-induced Hypercalcemia. J. Ultrastruct. Res.24, 145–149 (1968).

    Article  PubMed  CAS  Google Scholar 

  • Falck, B., Larson, B., Mecklenburg, C. V., Rosegren, E., Svenaeus, K.: On the presence of a second specific cell system in mammalian thyroid gland. Acta physiol. scand.62, 491–492 (1964).

    PubMed  CAS  Google Scholar 

  • -Falck, B. Owman, Ch.: 5-hydroxytryptamine and related amines in endocrine cell systems. In: Advances in pharmacology, vol. 6, p. 211–231. Edit, by Garattini, S., Shore, P. A. New York 1968.

  • Forster, G. V., Baghdiantz, A., Kumar, M. A., Slack, E., Soliman, H. A., MacIntyre, I.: Thyroid origin of Calcitonin. Nature (Lond.)202, 1303–1305 (1964a).

    Article  Google Scholar 

  • — Maclntyre, I., Pearse, A. G. E.: Calcitonin production and the mitochondrion-rich cells of the dog thyroid. Nature (Lond.)203, 1029–1030 (1964)b.

    Article  Google Scholar 

  • Gabe, M.: Données histochimiques sur les cellules parafolliculaires de la glande thyroïde du chien. Acta anat. (Basel)38, 332–344 (1959).

    CAS  Google Scholar 

  • — Données histologiques sur les macrothyréocytes (cellules parafolliculaires) de quelques sauropsides et anamniotes. Acta anat. (Basel)47, 34–54 (1961).

    CAS  Google Scholar 

  • Grimelius, L.: A silver nitrate stain for alpha-2 cells in human pancreatic islets. Acta Soc. Med. Upsalien.73, 243–270 (1968)a.

    CAS  Google Scholar 

  • — The argyrophil reaction in islets cells of adult human pancreas studied with a new silver nitrate procedure. Acta Soc. Med. Upsalien.73, 271–294 (1968 b).

    CAS  Google Scholar 

  • Hamperl, H.: Über argyrophile Zellen. Virchows Arch. path. Anat.321, 482–507 (1952).

    CAS  Google Scholar 

  • Hargis, G. K., Williams, G. A., Tennenhouse, A., Arnaud, C. D.: Thyrocalcitonin: Cytological localization by immunofluorescence. Science152, 73–75 (1966).

    Article  PubMed  CAS  Google Scholar 

  • Hirsch, P. F., Gauthier, G. F., Munson, P. L.: Thyroid hypocalcemic principle and recurrent laryngeal nerve injury as factors affecting the response to parathyroidectomy in rats. Endocrinology73, 244–252 (1963).

    PubMed  CAS  Google Scholar 

  • — Voelkel, E. F., Munson, P. L.: Thyrocalcitonin: hypocalcemic hypophosphatemic principle of the thyroid gland. Science146, 412–413 (1964).

    Article  PubMed  CAS  Google Scholar 

  • Kracht, J., Hachmeister, U., Breustedt, H.-J., Lenke, M.: Immunohistological studies on thyrocalcitonin in C-cells. Endokrinologie52, 395–401 (1968)a.

    PubMed  Google Scholar 

  • — Hachmeister, U., Kruse, H.: Thyrocaleitonin und die C-Zellen der Schilddrüse. Manch, med. Wschr.110, 203–208 (1968)b.

    CAS  Google Scholar 

  • Larson, B., Owman, Ch., Sundler, F.: Monoaminergic mechanisms in parafollicular cells of the mouse thyroid gland. Endocrinology78, 1109–1114 (1966).

    PubMed  CAS  Google Scholar 

  • Lietz, H., Schmähling, H.U., Zippel, H.: Veränderung an den C-Zellen der Rattenschilddrüse bei Hyper- und Hypocalcämie. Virchows Arch. Abt. A Path. Anat.348, 290–305 (1969).

    Article  CAS  Google Scholar 

  • Luciano, L., Reale, E.: Elektronenmikroskopische Beobachtungen an parafollikulären Zellen der Ratten-Schilddrüse. Z. Zellforsch.64, 751–766 (1964).

    Article  PubMed  CAS  Google Scholar 

  • Ludwig, K. G.: Beiträge zur Schilddrüsenstruktur: II. Gibt es „interoder parafollikuläres Epithel in der Schilddrüse“? Acta anat.19, 28–50 (1953).

    PubMed  CAS  Google Scholar 

  • Matsuzawa, T., Kurosumi, K.: Morphological changes in parafollicular cells of rat thyroid gland after administration of calcium shown by electron microscopy. Nature (Lond.)213, 927–928 (1967).

    Article  CAS  Google Scholar 

  • Meyer, J. S., Abdel-Bari, W.: Granules and thyrocalcitonin-like activity in medullary carcinoma of the thyroid gland. New Engl. J. Med.278, 523–529 (1968)

    PubMed  CAS  Google Scholar 

  • Moseley, J. M., Matthews, E. W., Breed, R. H., Galante, L., Tse, A., Maclntyre, I.: The ultimobranchial origin of calcitonin. Lancet1968 I, 108–110.

  • Nairn, R. C.: Fluorescent protein tracing, 1st ed. p. 122–126, Livingstone, Edinburgh & London 1962.

    Google Scholar 

  • Nonidez, J. F.: The origin of the “parafollicular” cells, a second epithelial component of the thyroid of the dog. Amer. J. Anat.49, 479–505 (1932)a.

    Article  Google Scholar 

  • — Further observations on the parafollicular cells of the mammalian thyroid. Anat. Rec.53, 339–347 (1932)b.

    Article  Google Scholar 

  • Nunez, E. A., Gould R. P., Hamilton, D. W., Hayward, J. S., Holt, S. J.: Seasonal changes in the fine structure of the basal granular cells of the bat thyroid. J. Cell Sci.2, 401–410 (1967).

    PubMed  CAS  Google Scholar 

  • — Gould, R. P., Holt, S. J.: A study of granule formation in the bat parafollicular cell. J. Cell Sci.5, 531–559 (1969).

    PubMed  CAS  Google Scholar 

  • Owman, Ch., Sundler, F.: Indole metabolism in thyroid C cells of the mouse: Effects of thyrocaleitonin and thiouracyl. In: Calcitonin: Symposium on thyrocalcitonin and C cells, p. 110–121. Edited by S. Taylor, London: Heinemann (1968).

    Google Scholar 

  • Pearse, A. G. E.: The cytochemistry of the thyroid C cells and their relationship to calcitonin. Proc. roy. Soc. B164, 478–487 (1966)a.

    CAS  Google Scholar 

  • — 5-hydroxytryptophan uptake by dog thyroid C cells and its possible significance in polypeptide hormone production. Nature (Lond.)211, 598–600 (1966)b.

    Article  CAS  Google Scholar 

  • — Common cytochemical and ultrastructural characteristics of cells producing polypetide hormones (the APUD series) and their relevance to thyroid and ultimobranchial C cells and calcitonin. Proc. roy. Soc. B170, 71–80 (1968).

    Article  CAS  Google Scholar 

  • — Cytochemical evidence for random coil conformation of polypeptide hormone precursor protein in endocrine cells. Nature (Lond.)221, 1210–1211 (1969).

    Article  CAS  Google Scholar 

  • — Carvalheira, A. F.: Cytochemical evidence for an ultimobranchial origin of rodent thyroid C cells. Nature (Lond.)214, 929–930 (1967).

    Article  CAS  Google Scholar 

  • Pepler, W. J., Pearse, A. G. E.: A histological study of the esterases of rat thyroid and their behaviour under experimental conditions. Brit. J. exp. Path.38, 221–226 (1967).

    Google Scholar 

  • Ritzen, M., Hammarström, L., Ullberg, S.: Autoradiographic distribution of 5-hydroxytryptamine and 5-hydroxytryptophan in the mouse. Biochem. Pharmacol.14, 313–321 (1965).

    Article  PubMed  CAS  Google Scholar 

  • Rohr, H. P., Hasler, K.: The parafollicular cells of the thyroid gland as a possible site of production of thyrocalcitonin. An electron-microscopic examination of the thyroid gland of the rat after stimulation by calcium acetate and vitamin D3. Experimentia (Basel)24, 152–153 (1968).

    CAS  Google Scholar 

  • Saito, K., Shibata, K.: Parafollicular cell in the rat thyroid. Endocr. jap.4, 253–261 (1957).

    PubMed  CAS  Google Scholar 

  • Sandritter, W., Klein, K. H.: Über argyrophile Zellen in der Schilddrüse. Frankfurt. Z. Path.65, 204–218 (1954).

    PubMed  CAS  Google Scholar 

  • Seecof, D. P.: Studies on mitochondria. II. The occurrence of mitochondria-rich and mitochondria-poor cells in the thyroid gland of man and animals. Amer. J. Path.3, 365–383 (1927).

    Google Scholar 

  • Solcia, E., Vassallo, G., Capeila, C.: Selective staining of endocrine cells by basic dyes after acid hydrolysis. Stain Technol.43, 257–263 (1968).

    PubMed  CAS  Google Scholar 

  • Steiner, H.: Endokrin-aktive Tumoren mit Amyloidstroma. Eine morphologische Untersuchung von Insulinomen und einen Calcitonin produzierenden Tumor. Virchows Arch. Abt. A Path. Anat.348, 257–263 (1969).

    Article  Google Scholar 

  • Stoeckel, M. E., Porte, A., Ganguilhem, B.: Sur l’infrastructure des cellules parafolliculaires de la thyroïde du Hamster sauvage (Cricetus cricetus). C. R. Acad. Sci. (Paris)264, 2490–2492 (1967).

    CAS  Google Scholar 

  • — Localisation ultimobranchiale et thyroïdienne des cellules C (cellules à calcitonine) chez deux Columbidae: le pigeon et le tourtereau. Etude au microscope électronique. Z. Zeilforsch.102, 376–386 (1969).

    Article  CAS  Google Scholar 

  • Takagi, K.: A cytological study on the dog’s thyroid gland. Folia anat. jap.1, 69–100 (1922).

    Google Scholar 

  • Tashiro, M.: Electron microscopic studies of the parafollicular cells in the thyroid gland of the dog. Okajimas Folia anat. jap.39, 191–211 (1964).

    CAS  Google Scholar 

  • Tauber, S.D.: Ultimobranchial origin of thyrocalcitonin. Proc. nat. Acad. Sci. (Wash.)58, 1684–1687 (1967).

    Article  CAS  Google Scholar 

  • Wissig, S. L.: The fine structure of parafollicular (light) cells of the rat thyroid gland. Proc. 5th Intern. Congr. Electron. Micr. 2, WW-1. (1962).

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De Grandi, P. The routine demonstration of C cells in human and animal thyroid glands. Virchows Arch. Abt. B Zellpath. 6, 137–150 (1970). https://doi.org/10.1007/BF02899119

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