Anatomy and Embryology

, Volume 160, Issue 3, pp 263–274 | Cite as

Tight junctions in the ependyma of the spinal cord of the urodele Pleurodeles waltlii

  • A. J. Zamora
  • D. Thiesson
Article

Summary

The ependymal junction pattern in the spinal cord of postmetamorphic ribbed newts has been studied, using transmission electron microscopy of ultrathin sections of normal animals and of animals perfused through the IVth ventricle with lanthanum. Contrary to what has been observed in mammalian CNS, the ependyma of the urodelan spinal cord is furnished with tight junctions that seal the luminal border of the terminal bars. These occludens junctions are made up of two to seven punctate fusions of the plasma membranes. Lanthanum tracer remains restricted inside the lumen of the central canal, being stopped at the first punctate fusion on its way through the intercellular clefts. Beyond this point, the extracellular space contains no tracer material. Besides tight junctions, intermediate, desmosomal and gap junctions are also present. Gap junctions and desmosomes are not present in CSF-contacting neurons. It is suggested that ependyma with occluding junctions (special ependyma) overlay the regions of the CNS where the ependymal cells significantly modify the composition of both intercellular and cerebrospinal fluids, through secretory, transporting and permeability control activities.

Key words

Spinal cord Ependyma Tight junctions Urodela Lanthanum 

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References

  1. Altner H (1968) Untersuchungen an Ependym und Ependymorganen im Zwischenhirn niederer Wirbeltiere (Neoceratodus, Urodelen, Anuren). Z Zellforsch 84:102–140Google Scholar
  2. Bellairs R, Breathnach AS, Gross M (1975) Freeze-fracture replication of junctional complexes in unincubated and incubated chick embryos. Cell Tissue Res 162:235–252Google Scholar
  3. Bennett MVL, Goodenough DA (1978) Gap junctions, electrotonic coupling and intercellular communication. Neurosc Res Prog Bull 16:377–486Google Scholar
  4. Bodenheimer TS, Brightman MW (1968) A blood-brain barrier to peroxidase in capillaries surrounded by perivascular spaces. Am J Anat 122:249–268Google Scholar
  5. Boulanger GA (1910) Les batraciens et principalement ceux d'Europe. Douin, ParisGoogle Scholar
  6. Bouvier D, Bouchaud C (1978) Tight junctions of the rat choroid plexus epithelium revealed by freeze-fracture. Biol Cellulaire 31:109–112Google Scholar
  7. Brightman MW (1967) The intracerebral movement of proteins injected into blood and cerebrospinal fluid of mice. Prog Brain Res 29:19–37Google Scholar
  8. Brightman MW, Palay SL (1963) The fine structure of ependyma in the brain of the rat. J Cell Biol 19:415–439Google Scholar
  9. Brightman MW, Reese TS (1969) Junctions between intimately apposed cell membranes in the vertebrate brain. J Cell Biol 40:648–677Google Scholar
  10. Brightman MW, Reese TS (1975) Membrane specializations of ependymal cells and astrocytes. In: Tower DB (ed) The Nervous System. Raven Press New York 1, pp 267–277Google Scholar
  11. Brightman MW, Prescott L, Reese TS (1975a) Intercellular junctions of special ependyma. In: Knigge KM, Scott DE, Kobayashi H, Miura-shi, Ishii S, (eds) Brain-Endocrine Interaction II. S Karger AG, Basel, pp 146–165Google Scholar
  12. Brightman MW, Shivers RR, Prescott L (1975b) Morphology of the walls around fluid compartments in nervous tissue. In: Fluid Environment of the Brain. Academic Press, New York, pp 3–29Google Scholar
  13. Butler EG, Ward MB (1967) Reconstitution of the spinal cord after ablation in adult Triturus. Dev Biol 15:464–486Google Scholar
  14. Carpenter SJ (1966) An electron microscopic study of the choroid plexuses of Necturus maculosus. J Comp Neurol 127:413–434Google Scholar
  15. Egar M, Singer M (1972) The role of ependyma in spinal cord regeneration in the urodele, Triturus. Exp Neurol 37:422–430Google Scholar
  16. Farquhar M, Palade G (1963) Junctional complexes in various epithelia. J Cell Biol 17:375–412Google Scholar
  17. Farquhar M, Palade G (1965) Cell junctions in amphibian skin. J Cell Biol 26:263–291Google Scholar
  18. Fleischhauer K (1972) Ependyma and subependymal layer. In: Bourne GH (ed) The Structure and Function of Nervous Tissue. Academic Press New York London VI, pp 1–46Google Scholar
  19. Friend DS, Gilula NB (1972) Variations in tight and gap junctions in mammalian tissues. J Cell Biol 53:758–776Google Scholar
  20. Gilula NB (1978) Structure of intercellular junctions. In: Feldman J, Gilula NB, Pitts JD (eds) Intercellular Junctions and Synapses. Chapman and Hall, London, pp 1–22Google Scholar
  21. Gilula NB, Fawcett DW, Aoki A (1976) The Sertoli cell occluding junctions and gap junctions in mature and developing mammalian testis. Dev Biol 50:142–168Google Scholar
  22. Ginzberg RD, Gilula NB (1979) Modulation of cell junctions during differentiation of the chicken otocyst sensory epithelium. Dev Biol 68:110–129Google Scholar
  23. Gulley RL, Reese TS (1976) Intercellular junctions in the reticular lamina of the organ of Corti. J Neurocytol 5:479–507Google Scholar
  24. Herrick CJ (1948) The Brain of the Tiger Salamander. The University of Chicago Press, Chicago and LondonGoogle Scholar
  25. Hull BE, Staehelin LA (1976) Functional significance of the variations in the geometrical organization of tight junction networks. J Cell Biol 68:688–704Google Scholar
  26. Inoue S, Hogg JC (1977) Freeze-etch study of the tracheal epithelium of normal guinea pigs with particular reference to intercellular junctions. J Ultrastruc Res 61:89–99Google Scholar
  27. Karnovsky MJ (1967) The ultrastructure of capillary permeability studied with peroxidase as a tracer. J Cell Biol 35:213–236Google Scholar
  28. Karnovsky MJ (1971) Use of ferrocyanide-reduced osmium tetroxide in electron microscopy. Abstracts Eleventh Annual Meeting, American Society for Cell Biology, p 146Google Scholar
  29. Kenny TP, Shivers RR (1974) The blood-brain barrier in a reptile, Anolis carolinensis. Tissue Cell 6:319–333Google Scholar
  30. Klinkerfuss GH (1964) An electron microscopic study of the ependyma and subependymal glia of the lateral ventricle of the cat. Am J Anat 115:71–100Google Scholar
  31. Knowles F (1972) Ependyma of the third ventricle in relation to pituitary function. Prog Brain Res 38:255–270Google Scholar
  32. Lane NJ, Swales LS (1979) Intercellular junctions and the development of the blood-brain barrier in Manduca sexta. Brain Res 168:227–245Google Scholar
  33. Luft JH (1961) Improvements in epoxy resin embedding methods. J Biophys Biochem Cytol 9:409–414Google Scholar
  34. Marquet E, Sobel HJ, Schwarz R, Weiss M (1972) Secretion by ependymal cells of the neurohypophysis and saccus vasculosus of Polypterus ornatipinnis (Osteichthyes). J. Morphol 137:111–130Google Scholar
  35. Montesano R, Friend DS, Perrelet A, Orci L (1975) In vivo assembly of tight junctions in fetal rat liver. J Cell Biol 67:310–319Google Scholar
  36. Montesano R, Mira-Moser F, Stefan Y, Perrelet A, Orci L (1978) Tight junctions in fetal rat liver explants grown in vitro. J Ultrastruct Res 64:182–190Google Scholar
  37. Nabeshima S, Reese TS, Landis DMD, Brightman MW (1975) Junctions in the meninges and marginal glia. J Comp Neurol 164:127–170Google Scholar
  38. Nadol JB Jr, Mulroy MJ, Goodenough DA, Weiss TF (1976) Tight and gap junctions in a vertebrate inner ear. Am J Anat 147:281–302Google Scholar
  39. Nakai Y (1971) Fine structure and its functional properties of the ependymal cell in the frog median eminence. Z Zellforsch 122:15–25Google Scholar
  40. Nakai Y, Ochiai H, Uchida M (1977) Fine structure of ependymal cells in the median eminence of the frog and mouse revealed by freeze-etching. Cell Tissue Res 181:311–318Google Scholar
  41. Noble GK (1931) Biology of Amphibia. Dover Publisher Inc, New YorkGoogle Scholar
  42. Nordlander RH, Singer M (1978) The role of ependyma in regeneration of the spinal cord in the urodele amphibian tail. J Comp Neurol 180:349–374Google Scholar
  43. Pesetsky I (1969) Carbonic anhydrase activity in ependymoglial cells of lower vertebrates. Histochimie 19:281–287Google Scholar
  44. Peters A, Palay SL, Webster H de F (1976) The fine structure of the Nervous System: The Neurons and Supporting Cells. WB Saunders Company, Philadephia London Toronto, pp 264–279Google Scholar
  45. Reale E, Luciano L, Franke K, Pannese E, Wermbter G, Iurato S (1975) Intercellular junctions in the vascular stria and spiral ligament. J Ultrastruct Res 53:284–297Google Scholar
  46. Revel JP, Brown SS (1976) Cell junctions in development, with particular reference to the neural tube. Cold Spring Harbor Symp Quantitative Biol 40:443–455Google Scholar
  47. Revel JP, Karnovsky MJ (1967) Hexagonal arrays of subunits in intercellular junctions of the mouse heart and liver. J Cell Biol 33:C7-C12Google Scholar
  48. Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208–212Google Scholar
  49. Richards JG (1978) Permeability of intercellular junctions in brain epithelia and endothelia to exogenous amine: cytochemical localization of extracellular 5-hydroxydopamine. J Neurocytol 7:61–70Google Scholar
  50. Riddle CV, Ernst SA (1979) Structural simplicity of the zonula occludens in the electrolite secreting epithelium of the avian salt gland. J Membrane Biol 45:21–35Google Scholar
  51. Saland LC, Evan AP, Demski LS (1974) Ultrastructure of ependymal cells of the shark median eminence. Anat Rec 178:657–666Google Scholar
  52. Sandri C, Akert K, Bennett MVL (1978) Junctional complexes and variations in gap junctions between spinal cord ependymal cells of a Teleost, Sternachus albifrons (Gymnotoidei). Brain Res 143:27–41Google Scholar
  53. Sarnat HB, Campa JF, Lloyd JM (1975) Inverse prominence of ependyma and capillaries in the spinal cord of vertebrates: a comparative histochemical study. Am J Anat 143:439–450Google Scholar
  54. Staehelin LA (1974) Structure and function of intercellular junctions. Int Rev Cytol 39:191–283Google Scholar
  55. Thorn R (1968) Les salamandres d'Europe, d'Asie et d'Afrique du Nord. Paul Lechevalier Editions, ParisGoogle Scholar
  56. Tice LW, Wollman SH, Carter RC (1975) Changes in tight junctions of thyroid epithelium with changes in thyroid activity. J Cell Biol 66:657–663Google Scholar
  57. van Deurs B, Koehler JK (1979) Tight junctions in the choroid plexus epithelium. A freeze-fracture study including complementary replicas. J Cell Biol 80:662–673Google Scholar
  58. Zamora AJ (1978) The ependymal and glial configuration in the spinal cord of Urodeles. Anat Embryol 154:67–82Google Scholar

Copyright information

© Springer-Verlag 1980

Authors and Affiliations

  • A. J. Zamora
    • 1
    • 2
  • D. Thiesson
    • 1
    • 2
  1. 1.Unité de Recherches NeurobiologiquesINSERM-U 6MarseilleFrance
  2. 2.CNRS-GR. 45MarseilleFrance

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