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Cytochemical localization of acid phosphatase in regenerated and dark-adapted eyes of a snail, Helix aspersa

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Summary

The role of the Golgi apparatus and the Golgi-endoplasmic reticulum-lysosomal complex (GERL) in the formation of lysosomes in the photosensory cells of regenerating and dark-adapted eyes of the garden snail Helix aspersa was examined with the use of acid phosphatase as a marker enzyme. In newly regenerated eyes, lead reaction deposit was restricted to the cisternae of GERL, a few small vesicles and some large secondary lysosomes. Dark-adapted sensory cells, on the other hand, were characterized by a heavy reaction product in the hypertrophied Golgi cisternae and GERL. Primary lysosomes were packaged by GERL cisternae in both the regenerating and the degenerating dark-adapted eyes. In the latter, these lysosomes may have been produced also by the Golgi apparatus. No reaction product was found in the rough endoplasmic reticulum, microvilli, or large aggregations of 800 Å photic vesicles in either kind of eye. In this study the lytic activity in differentiating sensory cells was significantly lower than that in degenerating cells suggesting that the increase in lysosomal activity in the latter was due to the absence of light. The effects of long dark-adaptation appear to be: 1. decrease in the production of photic vesicles; 2. increase in the formation of lysosomes; and 3. breakdown of photic vesicles by lysosomal activity.

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References

  • Barka, T., Anderson, P.J.: Histochemical methods for acid phosphatase using hexazonium pararosanilin as coupler. J. Histochem. Cytochem. 10, 741–753 (1962)

    Google Scholar 

  • Bentfeld, M.E., Bainton, D.F.: Cytochemical localization of lysosomal enzymes in rat megakaryocytes and platelets. J. clin. Invest. 56, 1635–1649 (1975)

    Google Scholar 

  • Boutry, J.-M., Novikoff, A.B.: Cytochemical studies on Golgi apparatus, GERL, and lysosomes in neurons of dorsal root ganglia in mice. Proc. nat. Acad. Sci. (Wash.) 72, 508–512 (1975)

    Google Scholar 

  • Brandenburger, J.L.: Two new kinds of retinal cells in the eye of a snail, Helix aspersa. J. Ultrastruct. Res. 50, 216–230 (1975)

    Google Scholar 

  • Brandenburger, J.L.: Acid phosphatase in dark-adapted eyes of a snail, Helix aspersa. J. Electron Micro. (Jap.), 26, 173 (1977)

    Google Scholar 

  • Brunk, U., Ericsson, J.L.E.: Electron microscopical studies on rat brain neurons. Localization of acid phosphatase and mode of formation of lipofuscin bodies. J. Ultrastruct. Res. 38, 1–15 (1972)

    Google Scholar 

  • Burt, R.C., Meredith, B.R., Grauer, R.C.: Histochemical study of a fluoride resistant acid phosphatase reaction in mouse duodenum. J. Histochem. Cytochem. 5, 135–139 (1957)

    Google Scholar 

  • Decker, R.S.: Lysosomal packaging in differentiating and degenerating anuran lateral motor column neurons. J. Cell Biol. 61, 599–612 (1974)

    Google Scholar 

  • Duve, C. de: Lysosome in retrospect. In: Lysosomes in biology and pathology, Vol. I, pp. 3–40 (J.T. Dingle and R.T. Dean, eds.). Amsterdam-London: North-Holland Publishing Co. 1969

    Google Scholar 

  • Eakin, R.M.: Structure of invertebrate photoreceptors. In: Photochemistry of vision, Handbook of sensory physiology, Vol. VII/1, pp. 625–684 (H.J.A. Dartnall, ed.). Berlin-Heidelberg-New York: Springer 1972

    Google Scholar 

  • Eakin, R.M., Brandenburger, J.L.: Differentiation in the eye of a pulmonate snail, Helix aspersa. J. Ultrastruct Res. 18, 391–421 (1967)

    Google Scholar 

  • Eakin, R.M., Brandenburger, J.L.: Osmic staining of amphibian and gastropod photoreceptors. J. Ultrastruct. Res. 30, 619–641 (1970)

    Google Scholar 

  • Eakin, R.M., Brandenburger, J.L.: Ultrastructural effects of dark-adaptation on eyes of a snail, Helix aspersa. J. exp. Zool. 187, 127–133 (1974)

    Google Scholar 

  • Eakin, R.M., Brandenburger, J.L.: Retinal differences between light-tolerant and light-avoiding slugs (Mollusca: Pulmonata). J. Ultrastruct. Res. 53, 382–394 (1975a)

    Google Scholar 

  • Eakin, R.M., Brandenburger, J.L.: Understanding a snail's eye at a snail's pace. Amer. Zool. 15, 851–863 (1975b)

    Google Scholar 

  • Eakin, R.M., Brandenburger, J.L.: Sensory microvilli and photic vesicles in the eye of the snail Helix aspersa. In: The structure of the eye, III, pp. 203–213 (E. Yamada and S. Mishima, eds.). Tokyo, Japan: Jap. J. Opthal. 1976

    Google Scholar 

  • Eakin, R.M., Ferlatte, M.M.: Studies on eye regeneration in a snail, Helix aspersa. J. exp. Zool. 184, 81–95 (1973)

    Google Scholar 

  • Eakin, R.M., Westfall J.A.: Dissection and oriented embedding of small specimens for ultramicrotomy. Stain Technol. 40, 13–14 (1965)

    Google Scholar 

  • Eakin, R.M., Westfall, J.A., Dennis, M.M.: Fine structure of the eye of a nudibranch mollusc, Hermissenda crassicornis. J. Cell Sci. 2, 349–358 (1967)

    Google Scholar 

  • Essner, E.: Phosphatases. In: Electron microscopy of enzymes. Principles and methods, Vol. 1, pp. 44–76 (M.A. Hayat, ed.). New York: Van Nostrand Reinhold Co. 1973

    Google Scholar 

  • Holtzman, E., Novikoff, A.B.: Lysosomes in the rat sciatic nerve following crush. J. Cell Biol. 27, 651–669 (1965)

    Google Scholar 

  • Holtzman, E., Novikoff, A.B., Villaverde, H.: Lysosomes and GERL in normal and chromatolytic neurons of the rat ganglion nodosum. J. Cell Biol. 33, 419–435 (1967)

    Google Scholar 

  • Hughes, H.P.I.: Structure and regeneration of the eyes of strombid gastropods. Cell Tiss. Res. 171, 259–271 (1976)

    Google Scholar 

  • Hugon, J., Borgers, M.: Fine structural localization of acid and alkaline phosphatase activities in the absorbing cells of the duodenum of rodents. Histochemie 12, 42–66 (1968)

    Google Scholar 

  • Jacklet, J.W., Alvarez, R., Bernstein, B.: Ultrastructure of the eye of Aplysia. J. Ultrastruct. Res. 38, 246–261 (1972)

    Google Scholar 

  • Kataoka, S.: Fine structure of the retina of a slug, Limax flavus L. Vision Res. 15, 681–686 (1975)

    Google Scholar 

  • McClurkin, I.T.: A method for the cytochemical demonstration of sodium-activated adenosine triphosphatase. J. Histochem. Cytochem. 12, 654–658 (1964)

    Google Scholar 

  • Newell, P.F., Newell, G.E.: The eye of the slug, Agriolimax reticulatus (Müll.). In: Invertebrate receptors. Symposia of the Zoological Society of London, No. 23, pp. 97–111 (J.D. Carthy and G.E. Newell, eds.). London: Academic Press 1968

    Google Scholar 

  • Nichols, B.A.: Normal rabbit alveolar macrophages. II. Their primary and secondary lysosomes as revealed by electron microscopy and cytochemistry. J. exp. Med. 144, 920–932 (1976)

    Google Scholar 

  • Nichols, B.A., Bainton, D.F., Farquhar, M.G.: Differentiation of monocytes. Origin, nature and fate of their azurophil granules. J. Cell Biol. 50, 498–515 (1971)

    Google Scholar 

  • Novikoff, A.B.: Lysosomes in the physiology and pathology of cells: Contributions of staining methods. In: Lysosomes, pp. 36–77 (A.V.S. de Reuck and M.P. Cameron, eds.). Boston, Mass.: Little, Brown and Co. 1963

    Google Scholar 

  • Novikoff, A.B.: GERL, its form and function in neurons of rat spinal ganglia. Biol. Bull. 127, 358 (1964)

    Google Scholar 

  • Novikoff, A.B.: Enzyme localization and ultrastructure of neurons. In: The neuron, pp. 255–318 (H. Hydén, ed.). Amsterdam: Eisevier Publishing Co. 1967

    Google Scholar 

  • Novikoff, A.B.: The endoplasmic reticulum: A cytochemist's view. (A review) Proc. nat. Acad. Sci. (Wash.) 73, 2781–2787 (1976)

    Google Scholar 

  • Novikoff, A.B., Drucker, J., Shin, W.-Y., Goldfischer, S.: Further studies of the apparent adenosinetriphosphatase activity of cell membranes in formol-calcium-fixed tissues. J. Histochem. Cytochem. 9, 434–451 (1961)

    Google Scholar 

  • Novikoff, P.M., Novikoff, A.B., Quintana, N., Hauw, J.-J.: Golgi apparatus, GERL, and lysosomes of neurons in rat dorsal root ganglia studied by thick section and thin section cytochemistry. J. Cell Biol. 50, 859–886 (1971)

    Google Scholar 

  • Röhlich, P., Török, L.J.: Die Feinstruktur des Auges der Weinbergschnecke (Helix pomatia L.). Z. Zellforsch. 60, 348–368 (1963)

    Google Scholar 

  • Schwalbach, G., Lickfeld, K.G., Hahn, M.: Der mikromorphogische Aufbau des Linsenauges der Weinbergschnecke (Helix pomatia L.). Protoplasma (Wien) 56, 242–273 (1963)

    Google Scholar 

  • Skou, J.C.: Enzymatic basis for active transport of Na+ and K+ across cell membrane. Physiol. Rev. 45, 596–617 (1965)

    Google Scholar 

  • Stoll, C.J.: Observations on the ultrastructure of the eye of the basommatophoran snail Lymnaea stagnalis (L.). Proc. kon. ned. Akad. Wet. Ser. C 76, 414–424 (1973)

    Google Scholar 

  • Tonosaki, A.: Fine structure of the retina in Haliotis discus. Z. Zellforsch. 79, 469–480 (1967)

    Google Scholar 

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Supported by a grant-in-aid to Richard M. Eakin from the U.S. Public Health Service (GM10292)

The author is grateful to Drs. Richard M. Eakin, Mary E. Bentfeld, and Barbara A. Nichols for their advice and critical reading of the manuscript, to Lionel Thomas for technical assistance and to Dr. Dorothy R. Pitelka for the use of the Siemens Elmiskop 102

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Brandenburger, J.L. Cytochemical localization of acid phosphatase in regenerated and dark-adapted eyes of a snail, Helix aspersa . Cell Tissue Res. 184, 301–313 (1977). https://doi.org/10.1007/BF00219892

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