Summary
Cytoplasmic annulate lamellae were found in the islet organ of a cyclostome, the hagfish (Myxine glutinosa), predominantly in cells interpreted as young proliferating β-cells, and also in endocrine cells and enterocytes of the bile duct and gut and in the endothelial cells of small blood vessels. A close association was observed between annulate lamellae and granular endoplasmic reticulum. Both in cells with and in those without annulate lamellae, crystalline inclusions probably of proteinaceous nature were seen in granular endoplasmic reticulum. These inclusions were occasionally closely associated to annulate lamellae, and a direct continuity could be seen between granular endoplasmic reticulum and the outer nuclear membrane surrounding an inclusion partially situated in the perinuclear cisterna. Rod-shaped structures and rounded electron dense bodies were seen in the nuclei of some islet parenchymal cells.
The presence of annulate lamellae in the islet organ and associated tissues of Myxine glutinosa is believed to be related to the very high phylogenetic age of this species. The close association observed between annulate lamellae, granular endoplasmic reticulum, crystalline inclusions, and sometimes also nuclear membranes, may be of functional significance.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Altenähr, E., Scifert, G.: Ultrastruktureller Vergleich menschlicher Epithelkörperchen bei sekundärem Hyperparathyroidismus und primärem Adenom. Virchows Arch. Abt. A 353, 60–85 (1971)
Benzo, C. A.: The annulate lamellae of chick embryo liver cells in organ culture. Anat. Res. 174, 399–405 (1972)
Boquist, L.: Intranuclear rods in pancreatic islet β-cells. J. Cell Biol. 43, 377–381 (1969)
Boquist, L.: Annulate lamellae in human parathyroid adenoma. Virchows Arch. Abt. B 6, 234–246 (1970a)
Boquist, L.: Tubular cytoplasmic bodies in pancreatic islet B-cells of mice. Z. Zellforsch. 106, 69–78 (1970b)
Boquist, L., Bergdahl, L.: Parathyroid morphology in normal dogs. Path. Europ. 8, 95–103 (1973)
Clark, N. B.: Calcium regulation in reptiles. Gen. comp. Endocr., Suppl. 3, 430–440 (1972)
Cresti, M., Pacini, E., Simoncioli, C.: Uncommon paracrystalline structures found in the endoplasmic reticulum of the integumentary cells of Diplotaxis erucoides ovules. J. Ultrastruct. Res. 49, 218–223 (1974)
Elliott, R. L., Arhelger, R. B.: Fine structure of parathyroid adenomas. Arch. Path. 81, 200–212 (1966)
Falkmer, S., Patent, G. J.: Comparative and embryological aspects of the pancreatic islets. In: Handbook of physiology, vol. I. The endocrine pancreas (D. F. Steiner, N. Freinkel, eds.), p. 1–23. Baltimore: Williams and Wilkins Co. 1972
Falkmer, S., Thomas, N.W., Boquist, L.: Endocrinology of the cyclostomata. In: Chemical zoology, vol. VIII. Deuterostomians, cyclostomes and fishes (M. Florkin, B. T. Scheer, eds.), p. 195–257. New York and London: Academic Press 1974
Falkmer, S., Winbladh, L.: An investigation of the pancreatic islet tissue of the hagfish (Myxine glutinosa) by light and electron microscopy. In: The structure and metabolism of the pancreatic islets (S. E. Brolin, B. Hellman, H. Knutson, eds.), p. 17–32. Oxford: Pergamon Press 1964
Fernholm, B.: The ultrastructure of the adenohypophysis of Myxine glutinosa. Z. Zellforsch. 132, 451–472 (1972)
Hach, P., Uerlings, I.: Zur Struktur und Genese von Kristalloiden im granulären endoplasmatischen Retikulum embryonaler Pankreaszellen. Exp. Path. 3, 132–137 (1969)
Harrison, G. A.: Some observation on the presence of annulate lamellae in alligator and sea gull adrenal cortical cells. J. Ultrastruct. Res. 14, 158–166 (1966)
Jarvik, E.: Aspects of vertebrate phylogeny. In: Proc. of the Fourth Nobel Symposium. Current problems of lower vertebrate phylogeny (T. Orvig, ed.), p. 497–527. New York 1968
Kessel, R. G.: Annulate lamellae. J. Ultrastruct. Res., Suppl. 10 (1968)
Kim, K. S. W., Boatman, E. S.: Electron microscopy of monkey kidney cell cultures infected with rubella virus. J. Virol. 1, 205–214 (1967)
Krishan, A., Hsu, D., Hutchins, P.: Hypertrophy of granular endoplasmic reticulum and annulate lamellae in Earle's C cells exposed to vinblastine sulphate. J. Cell Biol. 39, 211–216 (1968)
Leak, L. V.: Electron microscopy of cardiac tissue in a primitive vertebrate Myxine glutinosa. J. Morph. 128, 131–158 (1969)
Nybelin, O.: Phylogeny of the hagfish and the lampreys. Acta Reg. Soc. Sci. Litt. Gothoburg., Zool. 8, 8–13 (1973)
Östberg, Y., Boquist, L., Noorden, S. van: Cytochemical, fluorescence-microscopical and ultrastructural characterization of endocrine islet cells in the bile duct mucosa of a cyclostome, Myxine glutinosa. In manuscript (1975b)
Östberg, Y., Noorden, S. van, Pearse, A. G. E.: Cytochemical, immunofluorescence, and ultrastructural investigations on polypeptide hormone localization in the islet parenchyma and bile duct mucosa of a cyclostome, Myxine glutinosa. Gen. comp. Endocr., in press (1975a)
Patrizi, G., Middelkamp, J. N.: Development and changes of annulate lamellae complexes in rubella virus-infected RK-13 cells. J. Ultrastruct. Res. 31, 407–423 (1970)
Pictet, R., Rutter, W. J.: Development of the embryonic endocrine pancreas. In: Handbook of physiology. The endocrine pancreas (D. F. Steiner, N. Freinkel, eds.), vol. I, p. 25–66. Baltimore: Williams & Wilkins Co. 1972
Porter, K. R.: The ground substance; observations from electron microscopy. In: The cell (J. Brachet, A. E. Mirsky, eds.), vol. II, p. 621. New York: Academic Press 1961
Ross, M. H.: Annulate lamellae in the adrenal cortex of the foetal rat. J. Ultrastruct. Res. 7, 373–382 (1962)
Stensiö, E.: The cyclostome with special reference to the diphyletic origin of the Petromyzontida and Myxinoidea. In: Proc. of the Fourth Nobel Symposium. Current problems of lower vertebrate phylogeny (T. Ørvig, ed.), p. 13–71. New York: Interscience 1968
Swift, H.: The fine structure of annulate lamellae. J. biophys. biochem. Cytol. 2, 415–418 (1956)
Thomas, N. W., Östberg, Y., Falkmer, S.: A second granular cell in the endocrine pancreas of the hagfish Myxine glutinosa? Acta Zool. 54, 201–207 (1973)
Waugh, R. A., Sommer, J. R.: Lamellar junctional sarcoplasmic reticulum. A specialization of cardiac sarcoplasmic reticulum. J. Cell Biol. 63, 337–343 (1974)
Wischnitzer, S.: The annulate lamellae. Int. Rev. Cytol. 27, 65–100 (1970)
Author information
Authors and Affiliations
Additional information
Supported by grants from the Nordic Insulin Fund, the Swedish Medical Research Council (Project No. 12X-718), and the Board for Medical Research of Swedish Life Insurance Companies.
Rights and permissions
About this article
Cite this article
Boquist, L., Östberg, Y. Annulate lamellae and crystalline inclusions in granular endoplasmic reticulum of the islet organ and associated tissues of a cyclostome, Myxine glutinosa . Cell Tissue Res. 158, 75–87 (1975). https://doi.org/10.1007/BF00219952
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00219952