Skip to main content
SpringerLink
Log in

Freeze-fracture observations on the visceral yolk sac placenta of rats, mice and hamsters

With special reference to endodermal cell tight junctions

  • Published:
Anatomy and Embryology Aims and scope Submit manuscript

Summary

Freeze-fracture replicas of visceral yolk sac from rats, mice and hamsters in late stages of gestation were studied by electron microscopy. Special attention was directed toward determining the types of junctional specializations that exist between the columnar endoderm cells of this placental membrane. In all three species, well-developed, zonular tight (occluding) junctions were found on the contiguous lateral surfaces of the endoderm cells. The tight junctional network, located in an immediate subluminal position, was from 0.2–0.5 μm in depth and consisted at any point of 2–5, interconnecting, ∼9 ηm wide, strands (P-face) or shallow furrows (E-face). Patch-like aggregations of irregular intramembrane particles, characteristic of desmosomes (maculae adherentes), also were observed at scattered sites below the tight junctions. However, no evidence of gap (communicating) junctions was encountered. The endoderm cells of the rodent visceral yolk sac have been shown to play a central role in the selective transport of macromolecular substances from the maternal to the fetal system. Tight junctions may be vital to this endodermal cell function by preventing random paracellular fluxes of macromolecules.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • 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 horseradish peroxidase. J. Anat. 101, 461–478 (1967)

    Google Scholar 

  • Bernard, O., Ripoche, M.-A., Bennett, D.: Distribution of maternal immunoglobulins in the mouse uterus and embryo in the days after implantation. J. Exp. Med. 145, 58–75 (1977)

    Google Scholar 

  • Branton, D., Bullivant, S., Gilula, N.B., Karnovsky, M.J., Moor, H., Mühlethaler, K., Northcote, D.H., Packer, L., Satir, B., Satir, P., Speth, V., Staehelin, L.A., Steere, R.L., Weinstein, R.S.: Freeze-etching nomenclature. Science 190, 54–56 (1975)

    Google Scholar 

  • Butler, H.: The formation of the allantoic placenta in the golden hamster (Mesocricetus auratus). Z. Anat. Entwickl.-Gesch. 131, 68–85 (1970)

    Google Scholar 

  • Carpenter, S.J., Ferm, V.H.: Uptake and storage of Thorotrast by the rodent yolk sac placenta. An electron microscopic study. Am. J. Anat. 125, 429–456 (1969)

    Google Scholar 

  • Claude, P., Goodenough, D.A.: Fracture faces of zonulae occludentes from “tight” and “leaky” epithelia. J. Cell Biol. 58, 390–400 (1973)

    Google Scholar 

  • Dermietzel, R., Meller, K., Tetzlaff, W., Waelsch, M.: In vivo and in vitro formation of the junctional complex in choroid epithelium. A freeze-etching study. Cell Tissue Res. 181, 427–441 (1977)

    Google Scholar 

  • DiBona, D.R., Civan, M.M.: Pathways for movement of ions and water across toad urinary bladder. I. Anatomic site of transepithelial shunt pathways. J. Membr. Biol. 12, 101–128 (1973)

    Google Scholar 

  • Everett, J.W.: Morphological and physiological studies of the placenta in the albino rat. J. Exp. Zool. 70, 243–285 (1935)

    Google Scholar 

  • Fantel, A.G.: Fetomaternal potassium relations in the fetal rat on the twentieth day of gestation. Pediatr. Res. 9, 527–530 (1975)

    Google Scholar 

  • Farquhar, M.G., Palade, G.E.: Junctional complexes in various epithelia. J. Cell Biol. 17, 375–412 (1963)

    Google Scholar 

  • Frömter, E., Diamond, J.: Route of passive ion permeation in epithelia. Nature New Biology 235, 9–13 (1972)

    Google Scholar 

  • Goldstein, J.L., Anderson, R.G.W., Brown, M.S.: Coated pits, coated vesicles, and receptor-mediated endocytosis. Nature 279, 679–685 (1979)

    Google Scholar 

  • Hemmings, W.A.: Materno-foetal Transmission of Immunoglobulins, Cambridge Univ. Press 1976

  • Humbert, F., Pricam, C., Perrelet, A., Orci, L.: Freeze-fracture differences between plasma membranes of descending and ascending branches of the rat Henle's thin loop. Lab. Invest. 33, 407–411 (1975)

    Google Scholar 

  • Inoue, S., Hogg, J.C.: Freeze-etch study of the tracheal epithelium of normal guinea pigs with particular reference to intercellular junctions. J. Ultrastruct. Res. 61, 89–99 (1977)

    Google Scholar 

  • Inoue, S., Michel, R.P., Hogg, J.C.: Zonulae occludentes in alveolar epithelium and capillary endothelium of dog lungs studied with the freeze-fracture technique. J. Ultrastruct. Res. 56, 215–225 (1976)

    Google Scholar 

  • Jollie, W.P., Triche, T.J.: Ruthenium labeling of micropincytotic activity in the rat visceral yolk sac placenta. J. Ultrastruct. Res. 35, 541–553 (1971)

    Google Scholar 

  • Kelly, D.E., Shienvold, F.L.: The desmosome: fine structural studies with freeze-fracture replication and tannic acid staining of sectioned epidermis. Cell Tissue Res. 172, 309–323 (1976)

    Google Scholar 

  • King, B.F.: An electron microscopic study of absorption of peroxidase-conjugated immunoglobulin G by guinea pig visceral yolk sac in vitro. Am. J. Anat. 148, 447–456 (1977)

    Google Scholar 

  • King, B.F., Enders, A.C.: The fine structure of the guinea pig visceral yolk sac placenta. Am. J. Anat. 127, 397–414 (1970a)

    Google Scholar 

  • King, B.F., Enders, A.C.: Protein absorption and transport by the guinea pig visceral yolk sac placenta. Am. J. Anat. 129, 261–288 (1970b)

    Google Scholar 

  • Komatsu, M., Ishimura, K., Fujita, H.: Freeze-fracture images of the zonula occludens in the mouse oviduct epithelium. Arch. Histol. Jpn. 41, 453–458 (1978)

    Google Scholar 

  • Lambson, R.O.: An electron microscopic visualization of transport across rat visceral yolk sac. Am. J. Anat. 118, 21–52 (1966)

    Google Scholar 

  • Luciano, L., Thiele, J., Reale, E.: Development of follicles and of occluding junctions between the follicular cells of the thyroid gland. A thin section and freeze-fracture study in the fetal rat. J. Ultrastruct. Res. 66, 164–181 (1979)

    Google Scholar 

  • Machen, T.E., Erlij, D., Wooding, F.B.P.: Permeable junctional complexes. The movement of lanthanum across rabbit gallbladder and intestine. J. Cell Biol. 54, 302–312 (1972)

    Google Scholar 

  • Martínez-Palomo, A., Erlij, D.: The distribution of lanthanum in tight junctions of the kidney tubule. Pflügers Arch. 343, 267–272 (1973)

    Google Scholar 

  • Martínez-Palomo, A., Erlij, D.: Structure of tight junctions in epithelia with different permeability. Proc. Natl. Acad. Sci., U.S.A. 72, 4487–4491 (1975)

    Google Scholar 

  • Martínez-Palomo, A., Erlij, D., Bracho, H.: Localization of permeability barriers in the frog skin epithelium. J. Cell Biol. 50, 277–287 (1971)

    Google Scholar 

  • Mellor, D.J.: Potential differences between mother and foetus at different gestational ages in the rat, rabbit, and guinea-pig. J. Physiol. (Lond.) 204, 395–405 (1969)

    Google Scholar 

  • Miller, R.K., Koszalka, T.R., Brent, R.L.: The transport of molecules across placental membranes. In: The Cell Surface in Animal Embryogenesis and Development, pp. 145–223. (G. Poste and G.L. Nicolson, eds.) Amsterdam: Elsevier/North-Holland 1976

    Google Scholar 

  • Møllgård, K., Malinowska, D.H., Saunders, N.R.: Lack of correlation between tight junction morphology and permeability properties in developing choroid plexus. Nature 264, 293–294 (1976)

    Google Scholar 

  • Møllgård, K., Lauritzen, B., Saunders, N.R.: Double replica technique applied to choroid plexus from early foetal sheep: completeness and complexity of tight junctions. J. Neurocytol. 8, 139–149 (1979)

    Google Scholar 

  • Moxon, L.A., Wild, A.E.: Localization of proteins in coated micropinocytotic vesicles during transport across rabbit yolk sac endoderm. Cell Tissue Res. 171, 175–193 (1976)

    Google Scholar 

  • Padykula, H.A., Deren, J.J., Wilson, T.H.: Development of structure and function in the mammalian yolk sac. I. Developmental morphology and vitamin B12 uptake of the rat yolk sac. Dev. Biol. 13, 311–348 (1966)

    Google Scholar 

  • Pitelka, D.R., Hamamoto, S.T., Duafala, J.G., Nemamic, M.K.: Cell contacts in the mouse mammary gland. I. Normal gland in postnatal development and the secretory cycle. J. Cell Biol. 56, 797–818 (1973)

    Google Scholar 

  • Pricam, C., Humbert, F., Perrelet, A., Orci, L.: A freeze-etch study of the tight junctions of the rat kidney tubules. Lab. Invest 30, 286–291 (1974)

    Google Scholar 

  • Rugh, Roberts: The Mouse. Its Reproduction and Development. Minneapolis: Burgess Publishing Co. 1968

    Google Scholar 

  • Schneeberger, E.E., Walters, D.V., Olver, R.E.: Development of intercellular junctions in the pulmonary epithelium of the foetal lamb. J. Cell Sci. 32, 307–324 (1978)

    Google Scholar 

  • Schultz, P.W., Reger, J.F., Schultz, R.L.: Effects of Triton WR-1339 on the rat yolk sac placenta. Am. J. Anat. 119, 199–234 (1966)

    Google Scholar 

  • Seibel, W.: An ultrastructural comparison of the uptake and transport of horseradish peroxidase by the rat visceral yolk-sac placenta during mid- and late gestation. Am. J. Anat. 140, 213–236 (1974)

    Google Scholar 

  • Staehelin, L.A.: Structure and function of intercellular junctions. Int. Rev. Cytol. 39, 191–283 (1974)

    Google Scholar 

  • Staehelin, L.A., Hull, B.E.: Junctions between living cells. Sci. Am. 238, 140–152 (1978)

    Google Scholar 

  • Staehelin, L.A., Mukherjee, T.M., Williams, A.W.: Freeze-etch appearance of the tight junctions in the epithelium of small and large intestine of mice. Protoplasma 67, 165–184 (1969)

    Google Scholar 

  • Suzuki, F., Nagano, T.: Development of tight junctions in the caput epididymal epithelium of the mouse. Dev. Biol. 63, 321–334 (1978)

    Google Scholar 

  • Tice, L.W., Wollman, S.H., Carter, R.C.: Changes in tight junctions of thyroid epithelium with changes in thyroid activity. J. Cell Biol. 66, 657–663 (1975)

    Google Scholar 

  • Tice, L.W., Carter, R.L., Cahill, M.C.: Tracer and freeze fracture observations on developing tight junctions in fetal rat thyroid. Tissue Cell 9, 395–417 (1977)

    Google Scholar 

  • Tisher, C.C., Yarger, W.E.: Lanthanum permeability of the tight junction (zonula occludens) in the renal tubule of the rat. Kidney Int. 3, 238–250 (1973)

    Google Scholar 

  • Van Deurs, B., Koehler, J.K.: Tight junctions in the choroid plexus epithelium. A freeze-fracture study including complementary replicas. J. Cell Biol. 80, 662–673 (1979)

    Google Scholar 

  • Wade, J.B., Karnovsky, M.J.: Fracture faces of osmotically disrupted zonulae occludentes. J. Cell Biol. 62, 344–350 (1974)

    Google Scholar 

  • Whittembury, G., Rawlins, F.A.: Evidence of a paracellular pathway for ion flow in the kidney proximal tubule: electromicroscopic demonstration of lanthanum precipitate in the tight junction. Pflügers Arch. 330, 302–309 (1971)

    Google Scholar 

  • Wild, A.E.: Transport of immunoglobulins and other proteins from mother to young. In: Lysosomes in Biology and Pathology, Vol. 3, pp. 169–215. (J.T. Dingle, ed.) Amsterdam: North-Holland 1973

    Google Scholar 

  • Wild, A.E.: Protein transport across the placenta. In: Symp. Soc. Exp. Biol. Vol. 28, Transport at the Cellular Level, pp. 521–546 (M.A. Sleigh and D.H. Jennings, eds.). Cambridge Univ. Press 1974

  • Wild, A.E.: Mechanism of protein transport across the rabbit yolk sac endodrm. In: Materno-Foetal Transmission of Immunoglobulins, pp. 155–165. (W.A. Hemmings, ed.). Cambridge Univ. Press 1976

Download references

Author information

Authors and Affiliations

  1. Department of Anatomy, Dartmouth Medical School, 03755, Hanover, New Hampshire, USA

    Stanley J. Carpenter & Mark T. Dishaw

Authors
  1. Stanley J. Carpenter
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mark T. Dishaw
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

This investigation was supported by U.S. National Institutes of Health Grant HD-09585

Rights and permissions

Reprints and permissions

About this article

Cite this article

Carpenter, S.J., Dishaw, M.T. Freeze-fracture observations on the visceral yolk sac placenta of rats, mice and hamsters. Anat Embryol 157, 255–268 (1979). https://doi.org/10.1007/BF00304993

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00304993

Key words

Search

Navigation