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Subsurface cisterns and lamellar bodies: Particular forms of the endoplasmic reticulum in the neurons

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Summary

Structures identified as subsurface cisterns (SSC's) and lamellar bodies (LB's) have been observed in the neurons, but not in the glial cells, of the rat and cat substantia nigra. The SSC's are most often opposite what appears to be glial cells, but they are also subsynaptic in position. A single, large (0.4–1.5 μ), unfenestrated, usually flattened cistern closely underlies the inner aspect of the plasma membrane of the perikaryon and proximal parts of the neuronal processes at a regular interval ranging about 100–130 Å. They are sheet-like or discoid in configuration and consists of a pentalaminar structure which usually widens at its lateral edges where its membranes are continuous with each other or with rough ER profiles. Filaments, about 70 Å thick, bridge the cleft between the SSC and the overlying plasmalemma. One or more ER cisterns devoid of ribosomes except on their outermost membrane may be stacked up parallel to an SSC and immediately subjecent to it. A dense filamentous network intervenes between the SSC and its closely applied ER cisterns. At higher magnification, it is seen to consist of a finely textured material which is apparently composed of loosely packed tiny particles. These constituent subunits in turn may represent transverse sections of very fine filaments rather than granules. A mitochondrion frequently occurs in the immediate vicinity of an SSC and may be closely applied to its deep surface. Stacks of unfenestrated, parallel, regularly spaced (about 300–400 Å) cisterns, designated lamellar bodies, appear deeper in the karyoplasm. They are most often flattened and appear as pentalaminar structures. These cisterns, as well as the dense filamentous network intervening between them, are structurally similar to those closely applied to SSC's. They are also devoid of ribosomes except on their outermost surfaces. Whorls of similar cisterns are also occasionally observed. Another particular feature of the rough ER consists of the close apposition of two cisterns without any ribosome attached to the inner membranes of the latter structure. It evokes a simplified type of LB's. It is of particular interest to point out that all these cisterns, i.e. the SSC's, their closely applied cistern(s) and those forming the LB's, are connected to the RER membranes, so that a continuous channel occurs between the nuclear membrane and the SSC which closely underlies the plasma membrane. Our observations show that the SSC's and the LB's are structurally related forms of the ER. A parallel may be drawn between the SSC and the lateral element(s) of a dyad (triad). The structural complex consisting of an SSC, the overlying plasmalemma and the cross-bridges linking them, indeed, bears some resemblance to a dyad. It is suggested that membranes which are closely applied may interact, resulting in alterations in their respective properties. These patches of the neuronal plasma membrane associated with SSC's may, therefore, have special properties because of this relationship, resulting in a non-uniform spread of an action potential on the neuronal surface. The possible significance of SSC's in relation to neuronal electrophysiology, as well as of the latter structures and LB's in relation to cell metabolism, is to be discussed.

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References

  • Adinolfi, A. M.: The fine structure of neurons and synapses in the entopeduncular nucleus of the cat. J. comp. Neurol. 135, 225–248 (1969).

    Google Scholar 

  • Anzil, A. P., Blinzinger, K., Matsushima, A.: Dark cisternal fields: Specialized formations of the endoplasmic reticulum in striatal neurons of a rat. Z. Zellforsch. 113, 553–557 (1971).

    Google Scholar 

  • Behnke, O., Kristensen, B. I., Nielsen, L. E.: Electron microscopical observations on actinoid and myosinoid filaments in blood platelets. J. Ultrastruct. Res. 37, 351–369 (1971).

    Google Scholar 

  • Bunge, R. P., Bunge, M. B., Peterson, E. R.: An electron microscope study of cultured rat spinal cord. J. Cell Biol. 24, 163–191 (1965).

    Google Scholar 

  • Ebashi, S., Endo, M.: Calcium ion and muscle contraction. Progr. Biophys. molec. Biol. 18, 123–183 (1968).

    Google Scholar 

  • Epstein, M. A.: Some unusual features of fine structure observed in HeLa cells. J. biophys. biochem. Cytol. 10, 153–162 (1961).

    Google Scholar 

  • Franzini-Armstrong, C.: Studies of the triad. I. Structure of the junction in frog twitch fibers. J. Cell Biol. 47, 488–499 (1970).

    Google Scholar 

  • Friedmann, I., Cawthorne, T., Bird, E. S.: The laminated cytoplasmic inclusions in the sensory epithelium of the human macula. Further electron microscopic observations in Menière's disease. J. Ultrastruct. Res. 12, 92–103 (1965).

    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 

  • Gray, E. G.: Axo-somatic and axo-dendritic synapses of the cerebral cortex: An electron microscope study. J. Anat. (Lond.) 93, 420–433 (1959).

    Google Scholar 

  • Gulley, R. L., Wood, R. L.: The fine structure of the neurons in the rat substantia nigra. Tissue and Cell 3, 675–690 (1971).

    Google Scholar 

  • Haguenau, F.: The ergastoplasm: Its history, ultrastructure and biochemistry. Int. Rev. Cytol. 7, 425–483 (1958).

    Google Scholar 

  • Herman, M. M., Ralston, H. J., IIIrd: Laminated cytoplasmic bodies and annulate lamellae in the cat ventrobasal and posterior thalamus. Anat. Rec. 167, 183–196 (1970).

    Google Scholar 

  • Herndon, R. M.: The fine structure of the Purkinje cell. J. Cell Biol. 18, 167–180 (1963).

    Google Scholar 

  • Herndon, R. M.: Lamellar bodies, an unusual arrangement of the granular endoplasmic reticulum. J. Cell Biol. 20, 328–342 (1964).

    Google Scholar 

  • Ishikawa, H., Bischoff, R., Holtzer, H.: Formation of arrowhead complexes with heavy meromyosin in a variety of cell types. J. Cell Biol. 43, 312–328 (1969).

    Google Scholar 

  • Kelly, D. E.: The fine structure of skeletal muscle triad junctions. J. Ultrastruct. Res. 29, 37–49 (1969).

    Google Scholar 

  • Kessel, R. G.: Electron microscopic studies on the origin of annulate lamellae in oocytes of Necturus. J. Cell Biol. 19, 391–414 (1963).

    Google Scholar 

  • Kessel, R. G.: Annulate Lamellae. J. Ultrastruct. Res., Suppl. 10, 1–82 (1968).

  • Kruger, L., Maxwell, D. S.: Cytoplasmic laminar bodies in the striate cortex. J. Ultrastruct. Res. 26, 387–390 (1969).

    Google Scholar 

  • Le Beux, Y. J.: An ultrastructural study of the neurosecretory cells of the medial vascular prechiasmatic gland, the preoptic recess and the anterior part of the suprachiasmatic area. I. Cytoplasmic inclusions resembling nucleoli. Z. Zellforsch. 114, 404–440 (1971).

    Google Scholar 

  • Le Beux, Y. J.: An ultrastructural study of a cytoplasmic filamentous body, termed nematosome, in the neurons of the rat and cat substantia nigra. The association of nematosomes with the other cytoplasmic organelles in the neurons. Z. Zellforsch. 133, 289–325 (1972).

    Google Scholar 

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

    Google Scholar 

  • Morales, R., Duncan, D.: Multilaminated bodies and other unusual configurations of endoplasmic reticulum in the cerebellum of the cat. An electron microscope study. J. Ultrastruct. Res. 15, 480–489 (1966).

    Google Scholar 

  • Morales, R., Duncan, D., Rehmet, R.: A distinctive laminated cytoplasmic body in the lateral geniculate body neurons of the cat. J. Ultrastruct. Res. 10, 116–123 (1964).

    Google Scholar 

  • Pannese, E.: Developmental changes of the endoplasmic reticulum and ribosomes in nerve cells of the spinal ganglia of the domestic fowl. J. comp. Neurol. 132, 331–364 (1968).

    Google Scholar 

  • Pappas, G. D., Purpura, D. P.: Fine structure of dendrites in the superficial neocortical neuropil. Exp. Neurol. 4, 507–530 (1961).

    Google Scholar 

  • Peters, A., Palay, S. L.: The morphology of laminae A and A1 of the dorsal nucleus of the lateral geniculate body of the cat. J. Anat. (Lond.) 100, 451–486 (1966).

    Google Scholar 

  • Peters, A., Proskauer, C. C., Kaiserman-Abramof, I. F.: The small pyramidal neuron of the rat cerebral cortex. The axon hillock and initial segment. J. Cell Biol. 39, 604–619 (1968).

    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 

  • Revel, J. P., Olson, W., Karnovsky, M. J.: A twenty-angström gap junction with a hexagonal array of subunits in smooth muscle. J. Cell Biol. 35, 112A (1967).

    Google Scholar 

  • Rosenbluth, J.: The fine structure of acoustic ganglia in the rat. J. Cell Biol. 12, 329–359 (1962a).

    Google Scholar 

  • Rosenbluth, J.: Subsurface cisterns and their relationship to the neuronal plasma membrane. J. Cell Biol. 13, 405–421 (1962b).

    Google Scholar 

  • Rosenbluth, J.: Redundant myelin sheaths and other ultrastructural features of the toad cerebellum. J. Cell Biol. 28, 73–93 (1966).

    Google Scholar 

  • Rosenbluth, J., Palay, S. L.: The fine structure of nerve cell bodies and their myelin sheaths in the eighth nerve ganglion of the goldfish. J. biophys. biochem. Cytol. 9, 853–877 (1961).

    Google Scholar 

  • Rostgaard, J., Kristensen, B. I., Nielsen, L. E.: Characterization of 60 Å filaments in endothelial, epithelial, and smooth muscle cells of rat by reaction with heavy meromyosin. J. Ultrastruct. Res. 38, 207 (1972).

    Google Scholar 

  • Siegesmund, K. A.: The fine structure of subsurface cisterns. Anat. Rec. 162, 187–196 (1968).

    Google Scholar 

  • Smith, J. M., O'Leary, J. L., Harris, A. B., Gay, A. J.: Ultrastructural features of the lateral geniculate nucleus of the cat. J. comp. Neurol. 123, 357–377 (1964).

    Google Scholar 

  • Somlyo, A. V., Somlyo, A. P.: Strontium accumulation by sarcoplasmic reticulum and mitochondria in vascular smooth muscle. Science (Wash.) 174, 955–958 (1971).

    Google Scholar 

  • Takahashi, K., Wood, R. L.: Subsurface cisterns in the Purkinje cells of cerebellum of syrian hamster. Z. Zellforsch. 110, 311–320 (1970).

    Google Scholar 

  • Venable, J. H., Coggeshall, R.: A simplified lead citrate stain for use in electron microscopy. J. Cell Biol. 25, 407 (1965).

    Google Scholar 

  • Weis, P.: Confronting subsurface cisternae in chick embryo spinal ganglia. J. Cell Biol. 39, 485–488 (1968).

    Google Scholar 

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This work was supported by grant MA-3448 from the Medical Research Council of Canada. The skilful technical assistance of Mrs. Marjolaine Turcotte is gratefully acknowledged.

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Le Beux, Y.J. Subsurface cisterns and lamellar bodies: Particular forms of the endoplasmic reticulum in the neurons. Z.Zellforsch 133, 327–352 (1972). https://doi.org/10.1007/BF00307242

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