Summary
The fine structure of the mesonephric kidney of the lamprey, Entosphenus japonicus Martens, has been investigated with the electron microscope and discussed from the viewpoint of comparative morphology of the mesonephros.
The structure of the capillary wall of the glomerulus essentially coincides with that of higher vertebrates, though its basement membrane is remarkably thick (300–400 mμ) because of a dense accumulation of fibrillar material between the endothelium and the basal lamina of epithelial cell. No obvious fenestration of the endothelial cell has been observed in the glomerulus or capillaries in any part of this organ.
The kidney tubule is divided into three segments: 1. neck segment composed of ciliated cells with numerous mitochondria and glycogen particles, 2. proximal tubule composed of brush bordered cells provided with extensive pinocytotic vesicles and lysosomal granules in the apical cytoplasm and with lamellar membranes in the basal, and 3. distal tubule characterized by cells which, with their abundant mitochondria and branched tubular endoplasmic reticulum (about 500 Å diameter) with a central core, closely resemble the chloride cells in the gill filament of some teleosts. The possibility that the lamellar membranes in the proximal tubule cells correspond to basal infoldings is discussed.
The extensive development of the tubular reticulum and of the mitochondria in the distal tubule cells is believed to reflect the active absorption of urine chloride in the urinary tubule of lamprey mesonephric kidney evidenced by physiologists. The proximal tubule is suggested to take a part also in the urinary transport of water and ions, as the lamellar membranes found in the cells of this portion likely correspond to the basal infoldings in more advanced forms of the kidney.
The epithelial cells of the ureteric duct are characterized by granules suggesting a mucous secretion. No fine structure implying an absorptive activity in this duct has been observed.
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References
Bargmann, W., Knoop, A., Schiebler, T. H.: Histologische, cytochemische und elektronenmikroskopische Untersuchungen am Nephron (mit Berücksichtigung der Mitochondrien). Z. Zellforsch. 42, 386–422 (1955).
Bennett, H. S., Luft, J. H.: s-Collidine as a basis for buffering fixatives. J. biophys. biochem. Cytol. 6, 113–114 (1959).
Black, V. S.: Excretion and osmoregulation. In: The physiology of fishes (M. E. Brown ed.), p. 163–205. New York: Academic Press 1957.
Bulger, R. E.: The fine structure of the aglomerular nephron of the toad fish, Opsanus tau. Amer. J. Anat. 117, 171–192 (1965).
—, Trump, B. F.: The effect of fixatives on tubular ultrastructure of aglomerular midshipman, Porichthys notatus, and the glomerular flounder, Parophrys vetulus. J. Histochem. Cytochem. 13, 719–731 (1965).
—: Renal morphology of the English sole (Parophrys vetulus). Amer. J. Anat. 123, 195–226 (1968).
Clearmont, Y., Pereira, G.: The cell web in epithelial cells of the rat kidney. Anat. Rec. 156, 215–228 (1966).
Edwards, J. G.: The epithelium of the proximal tubule in bony fish. Anat. Rec. 63, 263–279 (1935).
Ericsson, J. L. E.: Absorption and decomposition of homologous hemoglobins in renal proximal tubular cells. Acta path. microbiol. scand., Suppl. 168, 1–121 (1964).
—: Fine structure of ureteric duct epithelium in the North Atlantic hagfish (Myxine glutinosa L.). Z. Zellforsch. 83, 219–230 (1967).
—, Trump, B. F.: Electron microscopic studies of the epithelium of proximal tubule of the rat kidney. III. Microbodies, multivesicular bodies, and Golgi-apparatus. Lab. Invest. 15, 1610–1633 (1966).
Fänge, R.: Structure and function of the excretory organs of myxinoid. In: The biology of Myxine (R. Fänge and P. Brodal, ed.), p. 516–529. Oslo: Universitetforlaget 1963.
Fontaine, M.: Recherches sur le milieu interieur de la lamproie marine (Petromyzon marinus). Ses variations en fonction de celles du milieu exterieur. C. R. Acad. Sci (Paris) 191, 680–682 (1930).
Fontaine, M.: Organes excréteurs. Formes actuelles. Super-orderes des petromyzonidea et des myxinoidea. In: Traité de Zool. (P.-P. Grassé, ed.), 13, (No. 1) 97–102 (1958).
—, Koch, H. J.: Les variations d'euryhalinité et d'osmoregulation chez les poissons. J. Physiol. (Paris) 42, 287–318 (1950).
Forster, R. P.: Kidney cells. In: The cell (J. Brachet and A. E. Mirsky, ed.), vol. 5, chapt. 2, p. 89–161. New York and London: Academic Press 1961.
Gérard, P.: Organes urogénitaux. I. Excréteurs. In: Traité de Zool. (P.-P. Grassé, ed.), 12, 974–1043 (1954).
- Apparail excréteur. Super-classe des Poissons. In: Traité de Zool. (P.-P. Grassé ed.), 13, (No. 2) 1545–1558 (1958).
—: The organization of cilia and flagella. In: Molecular organization and biological function (J. M. Allen ed.), p. 211–237. New York, Evanston and London: Haper & Row, Publisher 1966.
Gritzka, T. L.: The ultrastructure of the proximal convoluted tubule of a euryhaline teleost, Fundulus heteroclitus. Anat. Rec. 145, 235–236 (1963).
Ito, S., Winchester, R. J.: The fine structure of the gastric mucosa in the bat. J. Cell Biol. 16, 541–577 (1963).
Kessel, R. G., Beams, H. W.: Electron microscopic studies on the gill filaments of Fundulus heteroclitus from sea water and fresh water with special reference to the ultrastructural organization of the chloride cell. J. Ultrastruct. Res. 6, 77–87 (1962).
Krogh, A.: Osmotic regulation in aquatic animals. Cambridge: Univ. Press 1939.
Kurosumi, K.: Electron microscopic analysis of the secretion mechanism. In: Int. Rev. Cytol. (G. H. Bourne and J. F. Danielli, ed.), vol. 12, p. 1–124. New York and London: Academic Press 1961.
Latta, H., Maunsbach, A. B., Osvaldo, L.: The fine structure of renal tubules in cortex and medulla. In: Ultrastructure of the kidney (A. J. Dalton and F. Haguenau, ed.), p. 2–56. New York and London: Academic Press 1967.
Linss, W.: Licht- und elektronenmikroskopische Befunde an den Tubuli der Niere des Hechtes. Anat. Anz. 124, 85–104 (1969).
Luft, J. H.: Improvements in epoxy resin embedding methods. J. biophys. biochem. Cytol. 9, 409–414 (1961).
Marshall, E. K.: The comparative physiology of the kidney in relation to theories of renal secretion. Physiol. Rev. 14, 133–159 (1934).
Menefee, M. G., Mueller, C. B.: Some morphological considerations of transport in the glomerulus. In: Ultrastructure of the kidney (H. G. Dalton and F. Haguenau, ed.), p. 73–100. New York and London: Academic Press 1967.
Miller, F.: Hemoglobin absorption by the cells of the proximal convoluted tubule in mouse kidney. J. biophys. biochem. Cytol. 8, 689–718 (1960).
Millonig, G.: A modified procedure for lead staining of thin sections. J. biophys. biochem. Cytol. 11, 736–739 (1961).
—: Further observation on a phosphate buffer for osmium solution in fixation. In: Electron microscopy. Fifth Int. Congr. Electron Microscopy in Philadelphia (S. S. Breese Jr., ed.), vol. 2, P-8. New York: Academic Press 1962.
Möllendorff, W. von: Der Exkretionsapparat. In: Handbuch der mikroskopischen Anatomie des Menschen (W. von Möllendorff, ed.), S. 1–328 Berlin: Springer 1930.
Morris, R.: General problems of osmoregulation with special reference to cyclostomes. Symp. Zool. Soc. London 1, 1–16 (1960).
Neustein, H. B., Maunsbach, A. M.: Hemoglobin absorption by proximal tubule cells of the rabbit kidney. A study by electron microscopic autoradiography. J. Ultrastruct. Res. 16, 141–157 (1966).
Pak Poy, R. K. E.: Electron microscopy of amphibian renal glomerulus. Aust. J. exp. Biol. med. Sci. 35, 583–593 (1957).
Pak Poy, R. K. E.: Electron microscopy of the piscine (Carassius auratus) renal glomerulus. Aust. J. exp. Biol. med. Sci. 36, 191–209 (1958).
Palay, S. L., Karline, J. L.: An electron microscopic study of the intestinal villus. II. The pathway of fat absorption. J. biophys. biochem. Cytol. 5, 363–384 (1959).
Petrik, P.: The demonstration of chloride ions in the “chloride cells” of the gills of eels (Anguilla anguilla L.) adapted to sea water. Z. Zellforsch. 92, 422–427 (1968).
Philpott, C. W.: The use of horseradish peroxidase to demonstrate functional continuity between the plasmalemma and the unique tubular system of chloride cell. J. Cell Biol. 31, 68-A (1966).
—, Copeland, D. E.: Fine structure of chloride cells from species of Fundulus. J. Cell Biol. 18, 389–404 (1963).
Potts, W. T. W., Parry, G.: Osmotic and ion regulation in animals. Oxford: Pergamon Press 1964.
Prosser, C. L.: Water: Osmotic balance. In: Comparative animal physiology (C. L. Prosser and F. A. Brown, ed.), chapt. 2, p. 6–56. Philadelphia: W. B. Saunder Company 1962.
Regaud, C., Policard, A.: Note histologiques sur la sécrétion rénale de la Lamproie. I. Notes histologiques sur la sécrétion rénale. C. R. Soc. Biol. (Paris) 53, 1186–1188 (1902); - II. Le segment cilié du tube urinifère de la lamproie. C. R. Soc. Biol. Paris 54, 91–93 (1902); - III. Le segment a bordure en brosse du tube urinifère de la lamproie. C. R. Soc. Biol. (Paris) 54, 129–131 (1902); - IV. Les diverticules glandulaires du tube contourné de la lamproie. C. R. Soc. Biol. (Paris) 54, 554–555 (1902).
Rhodin, J.: Anatomy of kidney tubules. In: Int. Rev. Cytol. (G. H. Bourne and J. F. Danielli, ed.), vol 7, p. 485–534, New York and London: Academic Press 1958.
—: Studies on the nephron ultrastructure in mouse, goosefish and dogfish. Cit. from R. E. Bulger's (1965) paper, The fine structure of the aglomerular nephron of the toad fish, Opsanus tau. Amer. J. Anat. 117, 171–192 (1965).
Robertson, J. D.: The chemical composition of the blood of some aquatic chordates, including members of the Tunicata, Cyclostomata and Osteichthys. J. exp. Biol. 31, 424–442 (1954).
Sawyer, M.: Cit. from V. S. Black's review: Excretion and osmoregulation. In: The physiology of fishes (M. E. Brown, ed.), p. 163–205. New York: Academic Press 1957.
Schneider, S.: Ein Beitrag zur Kenntnis der Physiologie der Niere niederer Wirbeltiere. Skand. Arch. Physiol. (Berl. u. Lpz.) 14, 383–389 (1903).
Suzuki, Y.: On the fine structure of the renal glomerulus in Xenopus laevis. In: Electron microscopy. Sixth. Int. Congr. Electron Microscopy in Kyoto, Japan (R. Uyeda, ed.), vol. II, p. 667–668. Tokyo: Maruzen Co., LTD 1966.
Wickgren, B.: Osmotic regulation in some aquatic animals with special reference to the influence of temperature. Acta zool. fenn. 71, 1–102 (1953).
Yamada, E.: Collagen fibrils within the renal glomerulus. J. biophys. biochem. Cytol. 7, 407–408 (1960).
Yamamoto, T.: Observation on the special cell (type of chloride cell in gill filament) of the kidney tubules in fresh water cat fish (Parasilurus asotus). In: Electron microscopy. Sixth Int. Congr. Electron Microscopy in Kyoto (R. Uyeda, ed.), vol. II, p. 675–676. Tokyo: Maruzen Co., LTD 1966.
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Miyoshi, M. The fine structure of the mesonephros of the lamprey, Entosphenus japonicus Martens. Z. Zellforsch. 104, 213–230 (1970). https://doi.org/10.1007/BF00309732
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DOI: https://doi.org/10.1007/BF00309732