JUNCTIONS BETWEEN INTIMATELY APPOSED CELL MEMBRANES IN THE VERTEBRATE BRAIN (original) (raw)

Abstract

Certain junctions between ependymal cells, between astrocytes, and between some electrically coupled neurons have heretofore been regarded as tight, pentalaminar occlusions of the intercellular cleft. These junctions are now redefined in terms of their configuration after treatment of brain tissue in uranyl acetate before dehydration. Instead of a median dense lamina, they are bisected by a median gap 20–30 A wide which is continuous with the rest of the interspace. The patency of these "gap junctions" is further demonstrated by the penetration of horseradish peroxidase or lanthanum into the median gap, the latter tracer delineating there a polygonal substructure. However, either tracer can circumvent gap junctions because they are plaque-shaped rather than complete, circumferential belts. Tight junctions, which retain a pentalaminar appearance after uranyl acetate block treatment, are restricted primarily to the endothelium of parenchymal capillaries and the epithelium of the choroid plexus. They form rows of extensive, overlapping occlusions of the interspace and are neither circumvented nor penetrated by peroxidase and lanthanum. These junctions are morphologically distinguishable from the "labile" pentalaminar appositions which appear or disappear according to the preparative method and which do not interfere with the intercellular movement of tracers. Therefore, the interspaces of the brain are generally patent, allowing intercellular movement of colloidal materials. Endothelial and epithelial tight junctions occlude the interspaces between blood and parenchyma or cerebral ventricles, thereby constituting a structural basis for the blood-brain and blood-cerebrospinal fluid barriers.

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Selected References

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  1. BRIGHTMAN M. W., PALAY S. L. THE FINE STRUCTURE OF EPENDYMA IN THE BRAIN OF THE RAT. J Cell Biol. 1963 Nov;19:415–439. doi: 10.1083/jcb.19.2.415. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bairati A., Jr, Orzalesi N. The ultrastructure of the epithelium of the ciliary body. A study of the junctional complexes and of the changes associated with the production of plasmoid aqueous humour. Z Zellforsch Mikrosk Anat. 1966;69:635–658. [PubMed] [Google Scholar]
  3. Becker N. H., Novikoff A. B., Zimmerman H. M. Fine structure observations of the uptake of intravenously injected peroxidase by the rat choroid plexus. J Histochem Cytochem. 1967 Mar;15(3):160–165. doi: 10.1177/15.3.160. [DOI] [PubMed] [Google Scholar]
  4. Bennett M. V., Nakajima Y., Pappas G. D. Physiology and ultrastructure of electrotonic junctions. 3. Giant electromotor neurons of Malapterurus electricus. J Neurophysiol. 1967 Mar;30(2):209–235. doi: 10.1152/jn.1967.30.2.209. [DOI] [PubMed] [Google Scholar]
  5. Bodenheimer T. S., Brightman M. W. A blood-brain barrier to peroxidase in capillaries surrounded by perivascular spaces. Am J Anat. 1968 Mar;122(2):249–267. doi: 10.1002/aja.1001220206. [DOI] [PubMed] [Google Scholar]
  6. Brightman M. W. The distribution within the brain of ferritin injected into cerebrospinal fluid compartments. I. Ependymal distribution. J Cell Biol. 1965 Jul;26(1):99–123. doi: 10.1083/jcb.26.1.99. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Brightman M. W. The distribution within the brain of ferritin injected into cerebrospinal fluid compartments. II. Parenchymal distribution. Am J Anat. 1965 Sep;117(2):193–219. doi: 10.1002/aja.1001170204. [DOI] [PubMed] [Google Scholar]
  8. Bullivant S., Loewenstein W. R. Structure of coupled and uncoupled cell junctions. J Cell Biol. 1968 Jun;37(3):621–632. doi: 10.1083/jcb.37.3.621. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Coggeshall R. E. A fine structural analysis of the ventral nerve cord and associated sheath of Lumbricus terrestris L. J Comp Neurol. 1965 Dec;125(3):393–437. doi: 10.1002/cne.901250308. [DOI] [PubMed] [Google Scholar]
  10. Curtis A. S. Cell adhesion. Sci Prog. 1966 Spring;54(213):61–86. [PubMed] [Google Scholar]
  11. De Lorenzo A. J. Electron microscopy: tight junctions in synapses of the chick ciliary ganglion. Science. 1966 Apr 1;152(3718):76–78. doi: 10.1126/science.152.3718.76. [DOI] [PubMed] [Google Scholar]
  12. FARQUHAR M. G., PALADE G. E. Junctional complexes in various epithelia. J Cell Biol. 1963 May;17:375–412. doi: 10.1083/jcb.17.2.375. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. FURSHPAN E. J. "ELECTRICAL TRANSMISSION" AT AN EXCITATORY SYNAPSE IN A VERTEBRATE BRAIN. Science. 1964 May 15;144(3620):878–880. doi: 10.1126/science.144.3620.878. [DOI] [PubMed] [Google Scholar]
  14. Farquhar M. G., Palade G. E. Cell junctions in amphibian skin. J Cell Biol. 1965 Jul;26(1):263–291. doi: 10.1083/jcb.26.1.263. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Fenstermacher J. D., Johnson J. A. Filtration and reflection coefficients of the rabbit blood-brain barrier. Am J Physiol. 1966 Aug;211(2):341–346. doi: 10.1152/ajplegacy.1966.211.2.341. [DOI] [PubMed] [Google Scholar]
  16. Graham R. C., Jr, Karnovsky M. J. The early stages of absorption of injected horseradish peroxidase in the proximal tubules of mouse kidney: ultrastructural cytochemistry by a new technique. J Histochem Cytochem. 1966 Apr;14(4):291–302. doi: 10.1177/14.4.291. [DOI] [PubMed] [Google Scholar]
  17. Hess A. Developmental changes in the structure of the synapse on the myelinated cell bodies of the chicken ciliary ganglion. J Cell Biol. 1965 Jun;25(3 Suppl):1–19. doi: 10.1083/jcb.25.3.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hinojosa R., Robertson J. D. Ultrastructure of the spoon type synaptic endings in the nucleus vestibularis tangentialis of the chick. J Cell Biol. 1967 Aug;34(2):421–430. doi: 10.1083/jcb.34.2.421. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Johnston P. V., Roots B. I. Fixation of the central nervous system by perfusion with aldehydes and its effect on the extracellular space as seen by electron microscopy. J Cell Sci. 1967 Sep;2(3):377–386. doi: 10.1242/jcs.2.3.377. [DOI] [PubMed] [Google Scholar]
  20. KARLSSON U., SCHULTZ R. L. FIXATION OF THE CENTRAL NERVOUS SYSTEM FROM ELECTRON MICROSCOPY BY ALDEHYDE PERFUSION. I. PRESERVATION WITH ALDEHYDE PERFUSATES VERSUS DIRECT PERFUSION WITH OSMIUM TETROXIDE WITH SPECIAL REFERENCE TO MEMBRANES AND THE EXTRACELLULAR SPACE. J Ultrastruct Res. 1965 Feb;12:160–186. doi: 10.1016/s0022-5320(65)80014-4. [DOI] [PubMed] [Google Scholar]
  21. KARRER H. E. Cell interconnections in normal human cervical epithelium. J Biophys Biochem Cytol. 1960 Feb;7:181–184. doi: 10.1083/jcb.7.1.181. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. KARRER H. E. The striated musculature of blood vessels. II. Cell interconnections and cell surface. J Biophys Biochem Cytol. 1960 Sep;8:135–150. doi: 10.1083/jcb.8.1.135. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Karnovsky M. J. The ultrastructural basis of capillary permeability studied with peroxidase as a tracer. J Cell Biol. 1967 Oct;35(1):213–236. doi: 10.1083/jcb.35.1.213. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Kuffler S. W., Nicholls J. G. The physiology of neuroglial cells. Ergeb Physiol. 1966;57:1–90. [PubMed] [Google Scholar]
  25. LOCKE M. THE STRUCTURE OF SEPTATE DESMOSOMES. J Cell Biol. 1965 Apr;25:166–169. doi: 10.1083/jcb.25.1.166. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. LOEWENSTEIN W. R., KANNO Y. STUDIES ON AN EPITHELIAL (GLAND) CELL JUNCTION. I. MODIFICATIONS OF SURFACE MEMBRANE PERMEABILITY. J Cell Biol. 1964 Sep;22:565–586. doi: 10.1083/jcb.22.3.565. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Lasansky A. Cell junctions in ommatidia of Limulus. J Cell Biol. 1967 May;33(2):365–383. doi: 10.1083/jcb.33.2.365. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Lasansky A. The pathway between hyaloid blood and retinal neurons in the toad. Structural observations and permeability to tracer substances. J Cell Biol. 1967 Aug;34(2):617–626. doi: 10.1083/jcb.34.2.617. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Lenn N. J., Reese T. S. The fine structure of nerve endings in the nucleus of the trapezoid body and the ventral cochlear nucleus. Am J Anat. 1966 Mar;118(2):375–389. doi: 10.1002/aja.1001180205. [DOI] [PubMed] [Google Scholar]
  30. MARTIN A. R., PILAR G. DUAL MODE OF SYNAPTIC TRANSMISSION IN THE AVIAN CILIARY GANGLION. J Physiol. 1963 Sep;168:443–463. doi: 10.1113/jphysiol.1963.sp007202. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. MUIR A. R., PETERS A. Quintuple-layered membrane junctions at terminal bars between endothelial cells. J Cell Biol. 1962 Feb;12:443–448. doi: 10.1083/jcb.12.2.443. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Maunsbach A. B. The influence of different fixatives and fixation methods on the ultrastructure of rat kidney proximal tubule cells. I. Comparison of different perfusion fixation methods and of glutaraldehyde, formaldehyde and osmium tetroxide fixatives. J Ultrastruct Res. 1966 Jun;15(3):242–282. doi: 10.1016/s0022-5320(66)80109-0. [DOI] [PubMed] [Google Scholar]
  33. Muir A. R. The effects of divalent cations on the ultrastructure of the perfused rat heart. J Anat. 1967 Apr;101(Pt 2):239–261. [PMC free article] [PubMed] [Google Scholar]
  34. PARSONS D. F. A simple method for obtaining increased contrast in araldite sections by using postfixation staining of tissues with potassium permanganate. J Biophys Biochem Cytol. 1961 Nov;11:492–497. doi: 10.1083/jcb.11.2.492. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. PETERS A. Plasma membrane contacts in the central nervous system. J Anat. 1962 Apr;96:237–248. [PMC free article] [PubMed] [Google Scholar]
  36. Peachey L. D. The sarcoplasmic reticulum and transverse tubules of the frog's sartorius. J Cell Biol. 1965 Jun;25(3 Suppl):209–231. doi: 10.1083/jcb.25.3.209. [DOI] [PubMed] [Google Scholar]
  37. ROBERTSON J. D., BODENHEIMER T. S., STAGE D. E. THE ULTRASTRUCTURE OF MAUTHNER CELL SYNAPSES AND NODES IN GOLDFISH BRAINS. J Cell Biol. 1963 Oct;19:159–199. doi: 10.1083/jcb.19.1.159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. ROBERTSON J. D. New observations on the ultrastructure of the membranes of frog peripheral nerve fibers. J Biophys Biochem Cytol. 1957 Nov 25;3(6):1043–1048. doi: 10.1083/jcb.3.6.1043. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. 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. 1963 Oct;19:201–221. doi: 10.1083/jcb.19.1.201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Raviola G., Raviola E. Light and electron microscopic observations on the inner plexiform layer of the rabbit retina. Am J Anat. 1967 May;120(3):403–425. doi: 10.1002/aja.1001200303. [DOI] [PubMed] [Google Scholar]
  41. Reese T. S., Karnovsky M. J. Fine structural localization of a blood-brain barrier to exogenous peroxidase. J Cell Biol. 1967 Jul;34(1):207–217. doi: 10.1083/jcb.34.1.207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Reger J. F. The fine structure of neuromuscular junctions and contact zones between body wall muscle cells of Ascaris lumbricoides (var. suum). Z Zellforsch Mikrosk Anat. 1965 Jul 15;67(2):196–210. doi: 10.1007/BF00344469. [DOI] [PubMed] [Google Scholar]
  43. Revel J. P., Karnovsky M. J. Hexagonal array of subunits in intercellular junctions of the mouse heart and liver. J Cell Biol. 1967 Jun;33(3):C7–C12. doi: 10.1083/jcb.33.3.c7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Rosenbluth J. Ultrastructure of somatic muscle cells in Ascaris lumbricoides. II. Intermuscular junctions, neuromuscular junctions, and glycogen stores. J Cell Biol. 1965 Aug;26(2):579–591. doi: 10.1083/jcb.26.2.579. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. SEDAR A. W., FORTE J. G. EFFECTS OF CALCIUM DEPLETION ON THE JUNCTIONAL COMPLEX BETWEEN OXYNTIC CELLS OF GASTRIC GLANDS. J Cell Biol. 1964 Jul;22:173–188. doi: 10.1083/jcb.22.1.173. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. SMITH R. E., FARQUHAR M. G. PREPARATION OF THICK SECTIONS FOR CYTOCHEMISTRY AND ELECTRON MICROSCOPY BY A NON-FREEZING TECHNIQUE. Nature. 1963 Nov 16;200:691–691. doi: 10.1038/200691a0. [DOI] [PubMed] [Google Scholar]
  47. SMITH T. G., BAUMANN F., FUORTES M. G. ELECTRICAL CONNECTIONS BETWEEN VISUAL CELLS IN THE OMMATIDIUM OF LIMULUS. Science. 1965 Mar 19;147(3664):1446–1448. doi: 10.1126/science.147.3664.1446. [DOI] [PubMed] [Google Scholar]
  48. Shakib M., Cunha-Vaz J. G. Studies on the permeability of the blood-retinal barrier. IV. Junctional complexes of the retinal vessels and their role in the permeability of the blood-retinal barrier. Exp Eye Res. 1966 Jul;5(3):229–234. doi: 10.1016/s0014-4835(66)80011-8. [DOI] [PubMed] [Google Scholar]
  49. Takahashi K., Hama K. Some observations on the fine structure of the synaptic area in the ciliary ganglion of the chick. Z Zellforsch Mikrosk Anat. 1965 Jul 15;67(2):174–184. doi: 10.1007/BF00344467. [DOI] [PubMed] [Google Scholar]
  50. VANHARREVELD A., CROWELL J., MALHOTRA S. K. A STUDY OF EXTRACELLULAR SPACE IN CENTRAL NERVOUS TISSUE BY FREEZE-SUBSTITUTION. J Cell Biol. 1965 Apr;25:117–137. doi: 10.1083/jcb.25.1.117. [DOI] [PMC free article] [PubMed] [Google Scholar]