Summary
The ultrastructure of thyroid epithelial cells in mitosis has been investigated. A spatial association is described between clusters of apical vesicles (believed to contain thyroglobulin destined for secretion into the follicular lumen) and centrioles, in late prophase and late telophase cells. Quantitative techniques demonstrate the statistical significance of this association and suggest that it is not related to proximity of the Golgi apparatus or to the location of the centriole in the cell, which changes considerably during these phases of mitosis. The physical basis for this association remains uncertain, but microtubules emanating from the pericentriolar area may be involved.
In interphase cells, centrioles are located very close to the follicular lumen, where the majority of apical vesicles are also found. The association of centrioles with clusters of apical vesicles also in mitotic cells suggests that in interphase cells the apically located centrioles may serve as a focus for apical vesicles, helping to direct these secretory vesicles toward the follicular lumen and to maintain cellular polarization. Previous studies demonstrating that centrioles can act as microtubule organizing centers in interphase cells and studies linking microtubules and secretion also tend to support this hypothesis.
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References
André, J.: Some aspects of specialization in sperm. In: General Physiology of Cell Specialization (Mazia, D. and Tyler, A., (eds.), p. 97. New York: McGraw-Hill 1963
Björkman, U., Ekholm, R., Ericson, L.E., Öfverholm, T.: Transport of thyroglobulin and peroxidase in the thyroid follicle cell. Molec. Cell. Endocrinol. 5, 3–17 (1976)
Bornens, M.: Is the centriole bound to the nuclear membrane? Nature (Lond.) 270, 80–82 (1977)
Chambant-Guerin, A., Muller, P., Rossighol, B.: Microtubules and protein secretion in rat lacrimal glands. Relationship between colchicine binding and its inhibitory effect on the intracellular transport of proteins. J. Biol. Chem. 253, 3870–3876 (1978)
Corpron, R.E.: The ultrastructure of the gastric mucosa in normal and hypophysectomized rats. Amer. J. Anat. 118, 53–90 (1966)
Cox, S., Rao, P.N., Brinkley, B.R.: Differential effects of nitrous oxide on the spindle and cytoplasmic microtubule complex. J. Cell Biol. 75, 291a (abstract) (1977)
De Brabander, M., Wanson, J.-C., Mosselmans, R., Geuens, G., Drochmans, P.: Effects of antimicrotubular compounds on monolayer cultures of adult rat hepatocytes. Biol. Cellulaire 31, 127–140 (1978)
Ebe, T., Kobayashi, S.: In: Fine Structure of Human Cells and Tissues, pp. 127, 130 and 183. New York: John Wiley and Sons, Inc. 1972
Ekholm, R., Ericson, L.E., Josefsson, J.-O., Melander, A.: In vivo action of vinblastine on thyroid ultrastructure and hormone secretion. Endocrinology 94, 641–649 (1974)
Ericson, L.E., Engström, G.: Quantitative electron microscopic studies on exocytosis and endocytosis in the thyroid follicle cell. Endocrinology 103, 883–892 (1978)
Fawcett, D.W.: The cell organelles. Centrioles. In: The Cell. An Atlas of Fine Structure, pp. 49–63. Philadelphia: W.B. Saunders Company 1966
Fuller, G.M., Brinkley, B.R.: Structure and control of assembly of cytoplasmic microtubules in normal and transformed cells. J. Supramolec. Struct. 5, 497–514 (1976)
Hoffstein, S., Goldstein, I.M., Weissman, G.: Role of microtubule assembly in lysosomal enzyme secretion from human polymorphonuclear leukocytes. A reevaluation. J. Cell Biol. 73, 242–256 (1977)
Howell, S.L., Tyhurst, M.: Role of microtubules in the intracellular transport of growth hormone. Cell Tissue Res. 190, 163–171 (1978)
Ito, S.: The pancreas. In: Histology, third edition (Greep, R.O. and Weiss L., eds.), pp. 645–660. New York: McGraw-Hill 1973
Ito, S., Winchester, R.J.: The fine structure of the gastric mucosa in the bat. J. Cell Biol. 16, 541–577 (1963)
Lacy, P.E., Malaisse, W.J.: Microtubules and beta cell secretion. Recent Prog. Horm. Res. 29, 199–221 (1973)
Malech, H.L., Root, R.K., Gallin, J.I.: Structural analysis of human neutrophil migration. Centriole, microtubule, and microfilament orientation and function during chemotaxis. J. Cell Biol. 75, 666–693 (1977)
Moe, H., Mikkelsen, H.: Light microscopical and ultrastructural observations on the effect of vinblastine on ameloblasts of rat incisors in vivo. Acta Pathol. Microbiol. Scand. Sect. A 85, 73–88 (1977)
Osborn, M., Weber, K.: Cytoplasmic microtubules in tissue culture cells appear to grow from an organizing structure toward the plasma membrane. Proc. Natl. Acad. Sci. (USA) 73, 867–871 (1976)
Paiement, J.M., Leblond, C.P.: Localization of thyroglobulin antigenicity in rat thyroid sections using antibodies labeled with peroxidase or 125I-radioiodine. J. Cell Biol. 74, 992–1015 (1977)
Reaven, E.P., Reaven, G.M.: Distribution and content of microtubules in relation to the transport of lipid. An ultrastructural quantitative study of the absorptive cell of the small intestine. J. Cell Biol. 75, 559–572 (1977)
Rhodin, J.A.G.: In: Histology. A Text and Atlas, pp. 122–123 and pp. 156–157. London: Oxford University Press 1974
Sandborn, E.B.: In: Cells and Tissues by Light and Electron Microscopy, pp. 62, 66, and 126. New York and London: Academic Press 1970
Schliwa, M., Euteneuer, U.: A microtubule-independent component may be involved in granule transport in pigment cells. Nature (Lond.) 273, 556–558 (1978)
Sherline, P., Lee, Y.-C., Jacobs, L.S.: Binding of microtubules to pituitary secretory granules and secretory granule membranes. J. Cell. Biol. 72, 380–389 (1977)
Smith, D.S.: On the significance of cross-bridges between microtubules and synaptic vesicles. Philos. Trans. R. Soc. Lond. Ser. B, Biol. Sci. 261, 395–399 (1971)
Tamarin, A., Sreebny, L.M.: The rat submaxillary salivary gland. A correlative study by light and electron microscopy. J. Morphol. 117, 295–352 (1965)
Wolff, J., Williams, J.A.: The role of microtubules and microfilaments in thyroid secretion. Recent Prog. Horm. Res. 29, 229–278 (1973)
Zeligs, J.D., Wollman, S.H.: Mitosis in thyroid epithelial cells in vivo. I. Ultrastructural changes in cytoplasmic organelles during mitotic cycle. J. Ultrastruct. Res. 66, 53–77 (1979a)
Zeligs, J.D., Wollman, S.H.: Mitosis in rat thyroid epithelial cells in vivo. II. Centrioles and pericentriolar material. J. Ultrastruct. Res. 66, 97–108 (1979b)
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The author is grateful to Drs. Jan Wolff, Lars E. Ericson, and Seymour H. Wollman for useful discussions and to Mr. Franklin E. Reed for expert technical assistance.
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Zeligs, J.D. Association of centrioles with clusters of apical vesicles in mitotic thyroid epithelial cells. Are centrioles involved in directing secretion?. Cell Tissue Res. 201, 11–21 (1979). https://doi.org/10.1007/BF00238043
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DOI: https://doi.org/10.1007/BF00238043