Summary
The marginal band of nucleated erythrocytes in the toadfish is found, in electron micrographs, to be composed of about twenty-five microtubules approximately 200 Å in diameter. These form a bundle that encircles the erythrocyte just beneath the plasma membrane. These observations support the interpretation of Meves 1904, that this relatively stiff equatorial band may contribute to the maintenance of the discoid shape of nucleated erythrocytes in fish, amphibians, reptiles and birds.
Similar microtubules form an annular bundle encircling the nucleus in fish thrombocytes. The number of tubular elements involved here is in excess of one hundred and they are located deep to the ectoplasmic layer instead of immediately beneath the plasmalemma. The term endoplasmic ring is therefore proposed for this structure.
Comparative observations on nucleated erythrocytes of various species are presented showing that the density and fine structure of the material occupying the interchromosomal areas of the nucleus, always matches the cytoplasm and is related to the hemoglobin concentration of the species. These ultrastructural observations are consistent with the optical absorption and biochemical findings of other investigators indicating the presence of intranuclear hemoglobin in nucleated erythrocytes. Crystalline order is occasionally found in electron micrographs of the hemoglobin rich areas of the nucleus in toadfish erythrocytes but is not found in the cytoplasm.
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References
Allfrey, V., and A. E. Mirsky: The incorporation of N15 glycine by avian erythrocytes and reticulocytes in vitro. J. gen. Physiol. 35, 841–846 (1952).
Barcroft, J.: The respiratory function of blood. II. Haemoglobin. Cambridge: Cambridge Univ. Press 1938.
Barer, R.: In: Cytology and cell physiology (Bourne, G. H., ed.). Oxford: Oxford Univ. Press 1951.
Bennett, H. S., and J. H. Luft: S-collidine as a basis for buffering fixatives. J. biophys. biochem. Cytol. 6, 113–114 (1959).
Burgos, M. H., and D. W. Fawcett: Studies on the fine structure of the mammalian testis. I. Differentiation of the spermatids in the cat (Felis domestica). J. biophys. biochem. Cytol. 1, 287–300 (1955).
Christensen, A. K.: Fine structure of an unusual spermatozoan in the flatworm Plagiostomum. Biol. Bull. 121, 416 (1960).
Davies, H. G.: Structure in nucleated erythrocytes. J. biophys. biochem. Cytol. 9, 671–987 (1961).
, M. Spencer: The variation in the structure of the erythrooyte nuclei with fixation. J. Cell Biol. 14, 445–458 (1962).
Davison, J.: Studies on the form of the amphibian red cell. Anat. Rec. 132, 426 (1958).
Dawson, A. B.: Changes in erythrocytes of Necturus associated with the intracellular crystallization of hemoglobin. Anat. Rec. 46, 161–170 (1930).
: Intracellular crystallization of hemoglobin in the erythrocytes of the norther pipefish, Syngnathus fuscus. Biol. Bull. 63, 492–495 (1932).
Dehler, A.: Beiträge zur Kenntnis des feineren Baues der roten Blutkörperchen beim Hühnerembryo. Arch. mikr. Anat. 46, 414–430 (1895).
Downey, H. (editor): Handbook of Haematology. New York: P. B. Hoeber, Inc. 1938.
Fawcett, D. W.: Electron microscopic observations on the marginal band of nucleated erythrocytes. Anat. Rec. 133, 379 (1959).
: Physiologically significant specializations of the cell surface. Circulation 26, 1105–1125 (1962).
Guerber, A.: Endocytäre Hämoglobinkristalle. Sitzungsber. Ges. Beförder. ges. Naturwiss. Marburg 62, 294–299 (1927). Cited. by Dawson 1930.
Hall, F. G., and I. E. Gray: The hemoglobin concentration of the blood of marine fishes. J. biol. Chem. 81, 589–594 (1929).
Hay, E. D.: The fine structure of an unusual supporting network in the Leydig cells of Amblystoma epidermis. J. biophys. biochem. Cytol. 10, 457–463 (1961).
Jordan, H. E. and C. C. Speidel: The hemocytopoetic effect of splenectomy in the salamander, Triturus viridescens. Amer. J. Anat. 46, 55–90 (1930).
Lehmann, H., and R. G. Huntsman: Why are red cells the shape they are? The evolution of the human red cell, chap. 2, in: Functions of the blood (R. G. Macfarlane, and A. H. T. Robb-Smith, eds.) New York: Academic Press 1961.
Luft, J. H.: Improvements in epoxy resin embedding methods. J. biophys. biochem. Cytol. 9, 409–414 (1961).
Meves, Fr.: Die Hünefeld-Hensenchen Bilder der roten Blutkörperchen der Amphibien. Anat. Anz. 24, 465–476 (1904).
Meves, Fr.: Gesammelte Studien an den roten Blutkörperchen der Amphibien. Arch. mikr. Anat. 77, 465–540 (1911).
Mirsky, A. E., and A. Osawa: The interphase nucleus, chapt. 10, in: The Cell, vol. 2, pp. 677 to 770. New York: Academic Press 1961.
Nicholas, A.: Sur quelques particularités de structure des erythrocytes nuclées après coloration par d'hematoxyline ferrique. Bibl. anat. (Basel) 4, 16–20 (1896).
Palade, G. E.: A study of fixation for electron microscopy. J. exp. Med. 95, 285–298 (1952).
Philpott, C. W., and M. D. Maser: Marginal bands of nucleated erythrocytes. Proc. Electron Microscope Soc. of America. Abstract B-30, p. 16 (1963).
Randall, J. T.: The fine structure of the protozoan Spirostomum ambiguum. S.E.B. Symp. X. Mitochondria and other Cytoplasmic Inclusions, pp. 185–198 (1957).
Ranvier, L.: Recherches sur les élements du sang. Arch. de Phys., D.S. 2, 1–15 (1875).
Rebhun, L. I.: Nuclear changes during spermatogenesis in a pulmonate snail. J. biophys. biochem. Cytol. 3, 509–524 (1957).
Reynolds, E. S.: The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol. 17, 208–212 (1963).
Roth, L. E.: An E-M study of the cytology of the protozoan Euplotes patella. J. biophys. biochem. Cytol. 3, 985–1000 (1957).
: A filamentous componen of protozoan fibrillar systems. J. Ultrastruct. Res. 1, 223–235 (1958).
Sabatini, D. D., K. G. Bensch, and R. J. Barrnett: New means of fixation for electron microscopy and histochemistry. Amat. Rec. 142, 274 (1962).
Slautterback, D. B.: Cytoplasmic microtubules. I. Hydra. J. Cell Biol. 18, 367 (1963).
Steinert, M., and A. B. Novikoff: The existence of a cytostome and the occurrence of pinocytosis in the trypanosome, Trypanosoma mega. J. biophys. biochem. Cytol. 8, 563–569 (1960).
Stern, H., V. Allfrey, A. E. Mirsky, and H. Saetren: Some enzymes of isolated nuclei. J. gen. Physiol. 35, 559–578 (1951).
Tooze, J., and H. G. Davies: The occurrence and possible significance of hemoglobin in the chromosomal regions of nature. Erythrocyte nuclei of the newt, Triturus cristatus cristatus. J. Cell Biol. 16, 501–511 (1963).
Trotter, W. D.: Banding in salamander erythrocytes. Exp. Cell Res. 11, 587–603 (1956).
Watson, M. L.: Staining of tissues for electron microscopy with heavy metals. II. Applacation of solutions containing lead; and barium. J. biophys. biochem. Cytol. 4, 727–730 (1958).
Weidenreich, Er.: Studien über das Blut und die blutbildenden und -zerstörenden Organe. III. Über den Bau der Amphibienerythrocyten. Arch. mikr. Anat. 66, 270–298 (1905).
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This research was supported by grant G-12916 of the National Science Foundation.
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Fawcett, D.W., Witebsky, F. Observations on the ultrastructure of nucleated erythrocytes and thrombocytes, with particular reference to the structural basis of their discoidal shape. Zeitschrift für Zellforschung 62, 785–806 (1964). https://doi.org/10.1007/BF00342184
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DOI: https://doi.org/10.1007/BF00342184