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Ultrastructure of the labyrinth in the rat full-term placenta

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Summary

The placental labyrinth of the chorioallantoic placenta of the rat was studied with transmission and scanning electron microscopy. Full-term placentas were investigated after perfusion fixation from the maternal and fetal circulation, including thin-sectioning and freeze-fracturing.

The labyrinthal three-dimensional structure was found not to be trabecular but spongious lamellar. We propose a division of the lamellae into three groups—the first, second, and third order.

The trophoblastic layers are described in detail, showing a cellular layer I and two syncytial layers II and III. Layer I is found to be fenestrated and highly permeable. Layers II and III are connected by extended gap junction areas. It is suggested that the gap junctions function as a molecular sieve and represent the limiting barrier in diaplacental transport of the choriollantoic placenta.

Fetal capillaries are fenestrated and endothelial cells are connected by tight junctions.

The functional significance of the morphologic findings is discussed.

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References

  • Anderson, J. W.: The placental barrier of gamma-globulins in the rat. Amer. J. Anat. 104, 403–430 (1959)

    Google Scholar 

  • Barr, L., Dewey, M. M., Berger, W.: Propagation of action potentials and the structure of the nexus in cardiac muscle. J. gen. Physiol. 48, 797–824 (1965)

    Google Scholar 

  • Beck, F., Lloyd J. B., Griffiths, A.: A histochemical and biochemical study of some aspects of placental function in the rat using maternal injection of horse radish peroxidase. J. Anat. (Lond.) 101, 461–478 (1967)

    Google Scholar 

  • Björkman, N.: An atlas of placental fine structure. London: Bailliere Tindall & Casell 1970

    Google Scholar 

  • Boyd, J. D., Hamilton, W. J.: The human placenta, Cambridge: Heffer & Sons 1970

    Google Scholar 

  • Bruns, R. R., Palade, G. E.: Studies on blood capillaries. I. General organization of muscle capillaries. J. Cell Biol. 37, 244–276 (1968a)

    Google Scholar 

  • Bruns, R. R., Palade, G. E.: Studies on blood capillaries. II. Transport of ferritin molecules across the wall of muscle capillaries. J. Cell Biol. 37, 277–299 (1968b)

    Google Scholar 

  • Carpenter, S. J.: Ultrastructural observations on the maturation of the placental labyrinth of the golden hamster (days 10 to 16 of gestation). Amer. J. Anat. 143, 315–348 (1975)

    Google Scholar 

  • Davidoff, M., Schiebler, T. H.: Über den Feinbau der reifen Meerschweinchenplacenta. Z. Anat. Entwickl.-Gesch. 130, 216–233 (1970a)

    Google Scholar 

  • Davidoff, M., Schiebler, T. H.: Über den Feinbau der Meerschweinchenplacenta während der Entwicklung. Z. Anat. Entwickl.-Gesch. 130, 234–254 (1970b)

    Google Scholar 

  • Davies, J., Glaesser, S. R.: Histological and fine structural observations on the placenta of the rat. Acta anat. (Basel) 69, 542–608 (1968)

    Google Scholar 

  • Dewey, M. M., Barr, L.: A study of the structure and distribution of the nexus. J. Cell Biol. 23, 553–585 (1964)

    Google Scholar 

  • Dreifuss, J. J., Girardier, L., Forssmann, W. G.: Etude de la propagation de l'excitation dans le ventricule de rat au moyen de solutions hypertoniques. Pflügers Arch. ges. Physiol. 292, 13–33 (1966)

    Google Scholar 

  • Enders, A. C.: A comparative study of the fine structure of the trophoblast in several hemochorial placentas. Amer. J. Anat. 116, 29–68 (1965)

    Google Scholar 

  • Fels, R., Themann, H.: Die Permeabilität der Mäuseplacenta für Meerrettichperoxidase. Eine elektronenmikroskopische Untersuchung. Cytobiologie 3, 162–171 (1971)

    Google Scholar 

  • Forssmann, W. G.: La permeabilité des capillaires chez le Rat et la Souris. J. Microscopie 8, 50a (1969)

  • Forssmann, W. G.: A method for in vivo diffusion tracer studies combining perfusion fixation with intravenous tracer injection. Histochemie 20, 277–286 (1969)

    Google Scholar 

  • Forssmann, W. G.: Die Feinstruktur der Herzmuskulatur. Med. Welt 25, 21–25 (1974)

    Google Scholar 

  • Forssmann, W. G., Metz, J., Heinrich, D.: Gap junctions in the hemotrichorial placenta of the rat. J Ultrastruct. Res. (in press)

  • Franke, H.: Feinstruktur der Placenta. Elektronenoptische Untersuchungen über die reifende und reife Placenta der Ratte. Jena: VEB G. Fischer 1969

    Google Scholar 

  • Goodenough, D. A., Revel, J. P.: A fine structural analysis of intercellular junctions in the mouse liver. J. Cell Biol. 45, 272–290 (1970)

    Google Scholar 

  • Grosser, O.: Vergleichende Anatomie und Entwicklungsgeschichte der Eihäute und Placenta. Wien: Braumüller Verlag 1909

    Google Scholar 

  • Jollie, W. P.: Fine structural changes in placental labyrinth of the rat with increasing gestational age. J. Ultrastruct. Res. 10, 27–47 (1964)

    Google Scholar 

  • Jollie, W. P.: Fine structural changes in the junctional zone of the rat placenta with increasing gestational age. J. Ultrastruct. Res. 12, 420–438 (1965)

    Google Scholar 

  • Karnovsky, M.J.: The ultrastructural basis of capillary permeability studied with peroxidase as a tracer. J. Cell Biol. 27, 213–236 (1967)

    Google Scholar 

  • King, B. F.: The permeability of the guinea pig parietal yolk sac placenta to peroxidase and ferritin. Amer. J. Anat. 134, 365–376 (1972)

    Google Scholar 

  • Kirby, D. R. S., Bradbury, S.: The hemochorial mouse placenta. Anat. Rec. 152, 279–282 (1965)

    Google Scholar 

  • Loewenstein, W. R.: Permeability of membrane junctions. Ann. N.Y. Acad. Sci. 137, 441–483 (1966)

    Google Scholar 

  • Luft, J. H.: Improvements in epoxy resin embedding methods. J. biophys. biochem. Cytol. 9, 409–414 (1961)

    Google Scholar 

  • Mayersbach, von H: Zur Frage des Proteinübergangs von der Mutter zum Foeten. I. Befunde an Ratten am Ende der Schwangerschaft. Z. Zellforsch. 48, 479–504 (1958)

    Google Scholar 

  • McNutt, N. S., Weinstein, R. S.: The ultrastructure of the nexus. A correlated thin-section and freeze-cleave study. J. Cell Biol. 47, 666–688 (1970)

    Google Scholar 

  • McNutt, N. S., Weinstein, R. S.: Membrane ultrastructure at mammalian intercellular junctions. Progr. Biophys. Molec. Biol. 26, 45–101 (1973)

    Google Scholar 

  • Metz, J., Heinrich, D., Forssmann, W. G.: Gap junctions in hemodichorial and hemotrichorial placentas. Cell Tiss. Res. (in press)

  • Millonig, G.: Advantages of a phosphate buffer for OsO4 solutions in fixation. J. appl. Phys. 32, 1637–1645 (1961)

    Google Scholar 

  • Moor, H., Mühlethaler, K.: Fine structure in frozen etched yeast cells. J. Cell Biol. 17, 609–628 (1963)

    Google Scholar 

  • Mossman, H. W.: The rabbit placenta and the problem of placental transmission. Amer. J. Anat. 37, 433–457 (1926)

    Google Scholar 

  • Mossman, H. W.: Comparative morphogenesis of the fetal membranes and accessory uterine structures. Contr. Embryol. Carnegie Inst. 26, 129–141 (1937)

    Google Scholar 

  • Pfefferkorn, G., Pfautsch, M.: Preparation biologischer Objekte für die Raster-Elektronenmikroskopie. Beitr. elektronenmikroskop. Direktabb. Oberfl. 4 (1), 137–149 (1972)

    Google Scholar 

  • Revel, J. P., Karnovsky, M. J.: Hexagonal array of subunits in intercellular junctions of the mouse heart and liver. J. Cell Biol. 33, C7-C12 (1967)

    Google Scholar 

  • 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)

    Google Scholar 

  • Rhodin, J. A. G., Terzakis, J.: The ultrastructure of the human full-term placenta. J. Ultrastruct. Res. 6, 88–106 (1962)

    Google Scholar 

  • Robertson, J. D.: The occurrence of a subunit pattern in the unit membranes of club endings in Mauthner cell synapses in goldfish brains. J. Cell Biol. 19, 201–221 (1963)

    Google Scholar 

  • Robertson, T. A., Archer, J. M., Papadimitriou, J. M., Walters, M. N. J.: Transport of horseradish peroxidase in the murine placenta. J. Path. 103, 141–147 (1971)

    Google Scholar 

  • Schiebler, T. H., Kaufmann, P.: Über die Gliederung der menschlichen Placenta. Z. Zellforsch. 102, 242–265 (1969)

    Google Scholar 

  • Schiebler, T. H., Knoop, A.: Hisochemische und elektronenmikroskopische Untersuchungen an der Rattenplacenta. Z. Zellforsch. 50, 494–552 (1959)

    Google Scholar 

  • Tillack, T. W.: The transport of ferritin across the placenta of the rat. Lab. Invest. 15, 896–909 (1966)

    Google Scholar 

  • Wild, A. E.: Protein transmission across the rabbit fetal membranes. J. Embryol. exp. Morph. 24, 313–330 (1970)

    Google Scholar 

  • Wislocki, G. B., Dempsey, E. W.: Electron microscopy of the placenta of the rat. Anat. Rec. 123, 33–63 (1955)

    Google Scholar 

  • Wynn, R. M.: Morphology of the placenta. In: Assali, Biology of gestation, pp. 93–184 New York-London: Academic Press 1968

    Google Scholar 

  • Wynn, R. M., Corbett, J. R.: Ultrastructure of the canine placenta and amnion. Amer. J. Obstet. Gynec. 103, 878–887 (1969)

    Google Scholar 

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With the support of the Deutsche Forschungsgemeinschaft. Dedicated to Prof. Dr. Drs. h.c. W. Bargmann on his 70th birthday

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Metz, J., Heinrich, D. & Forssmann, W.G. Ultrastructure of the labyrinth in the rat full-term placenta. Anat. Embryol. 149, 123–148 (1976). https://doi.org/10.1007/BF00317893

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