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Freeze-etch and histochemical evidence for cycling in crayfish photoreceptor membranes

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Summary

Freeze-etched rhabdoms and adjacent cytoplasmic organelles from crayfish compound eyes have been studied for evidence of photoreceptor membrane cycling. The protoplasmic leaflet face (PF) of split photoreceptor membrane of the microvilli is richly particulate. The particles (92±16 A in diameter in surface fractures; 70±9 A in cross fractures; density about 8000/μm2) probably indicate rhodopsin molecule localization. Closely similar particles appear in membranes of pinocytotic vesicles, multivesicular bodies (MVB) and secondary lysosomes. In contrast other retinular cell membranes like plasma membrane remote from the rhabdom are quite distinct (60±23 A particle diameter, density ca 1000/μm2). Histochemical tests for acid phosphatase demonstrate its presence in well-developed (but not early stage) MVBs, mixed lamellar vesicular bodies (LVB) and lamellar bodies. Density of PF particles decreases from 8000 in MVB to roughly 4500/μm2 in LVB indicating a degradative sequence from rhabdom to lamellar bodies. Membrane leaflet orientations show that primary endocytosis from microvilli must be followed by secondary endocytosis of fused coated vesicles to form MVB. Morphological evidence for photoreceptor membrane resynthesis has not been found yet in crayfish but some has been obtained in other crustaceans.

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References

  • Abrahams, S.J., Holtzman, E.: Secretory endocytosis in insulin stimulated rat adrenal medulla cells. J. Cell Biol. 56, 540–558 (1973)

    Google Scholar 

  • Anteunis, A.: Origin and fate of the multivesicular bodies in PHA stimulated lymphocytes. Cell Tiss. Res. 149, 497–511 (1974)

    Google Scholar 

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

    Google Scholar 

  • Bibb, C., Young, R.W.: Renewal of fatty acids in the membranes of visual cell outer segments. J. Cell Biol. 61, 327–343 (1974)

    Google Scholar 

  • Bowers, B., Olszewski, T.E.: Pinocytosis in Acanthamoeba castelanii. J. Cell Biol. 53, 681–694 (1972)

    Google Scholar 

  • Bownds, D., Brodie, A.E.: Light sensitive swelling of isolated frog rod outer segments as an in vitro assay for visual transduction and dark adaptation. J. gen. Physiol. 66, 407–425 (1975)

    Google Scholar 

  • Brandenburger, J.L., Eakin, R.M.: Pathway of incorporation of vitamin A3H2 into photoreceptors of a snail Helix aspersa. Vision Res. 10, 639–653 (1970)

    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., Staehlin, L.A., Steere, R.L., Weinstein, R.S.: Freeze-etching nomenclature. Science 190, 54–56 (1975)

    Google Scholar 

  • Branton, D., Deamer, D.W.: Membrane structure. 70 p. Berlin-Heidelberg-New York: Springer 1972

    Google Scholar 

  • Bruyn, P.P.H. de, Michelson, S., Becker, R.P.: Endocytosis, transfer tubules, and lysosomal activity in myeloid sinusoidal endothelium. J. Ultrastruct. Res. 53, 133–151 (1975)

    Google Scholar 

  • Burnel, M., Mahler, H.R., Moore, W.J.: Protein synthesis in visual cells of Limulus. J. Neurochem. 17, 1493–1499 (1970)

    Google Scholar 

  • Clark, A.W., Branton, D.: Fracture faces in frozen outer segments from the guinea pig retina. Z. Zellforsch. 91, 586–603 (1968)

    Google Scholar 

  • Cohn, Z.A.: Macrophage physiology. Fed. Proc. 34, 1725–1729 (1975)

    Google Scholar 

  • Cone, R.A.: Transductive coupling in the visual system. Structure of the retinal rod. In: Functional linkage in biomolecular systems (F.O. Schmitt, D.M. Schneider, Crothers, D.M., eds.), pp. 234–252. New York: Raven Press 1975

    Google Scholar 

  • Daemen, F.: Vertebrate rod outer segment membranes. Biochim. biophys. Acta (Amst.) 300, 255–288 (1973)

    Google Scholar 

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

    Google Scholar 

  • Eguchi, E.: Rhabdom structure and receptor potentials in single crayfish retinular cells. J. cell. comp. Physiol. 66, 411–429 (1965)

    Google Scholar 

  • Eguchi, E., Waterman, T.H.: Fine structure patterns in crustacean rhabdoms. In: The functional organization of the compound eye (C.G. Bernhard, ed.), pp. 105–124. Oxford: Pergamon Press 1966

    Google Scholar 

  • Eguchi, E., Waterman, T.H.: Changes in retinal fine structure induced in the crab Libinia by light and dark adaptation. Z. Zellforsch. 79, 209–229 (1967)

    Google Scholar 

  • Eguchi, E., Waterman, T.H.: Cellular basis for polarized light perception in the spider crab, Libinia. Z. Zellforsch. 84, 87–101 (1968)

    Google Scholar 

  • Eguchi, E., Waterman, T.H., Akiyama, J.: Localization of the violet and yellow receptor cells in the crayfish retinula. J. gen. Physiol. 62, 355–374 (1973)

    Google Scholar 

  • Fahrenbach, W.H.: The visual system of the horseshoe crab Limulus polyphemus. Int. Rev. Cytol. 41, 285–349 (1975)

    Google Scholar 

  • Friend, D.S., Farquhar, M.G.: Function of coated vesicles during protein absorption in the rat vas deferens. J. Cell Biol. 35, 357–376 (1967)

    Google Scholar 

  • Hall, M.O., Bok, D.: Incorporation of [3H] vitamin A into rhodopsin in light- and dark-adapted frogs. Exp. Eye Res. 18, 105–117 (1974)

    Google Scholar 

  • Hamdorf, K., Paulsen, R., Schwemer, J.: Photoregeneration and sensitivity control of photoreceptors of invertebrates. In: Biochemistry and physiology of visual pigments (H. Langer, ed.), pp. 155–166. Berlin-Heidelberg-New York: Springer 1973

    Google Scholar 

  • Herron, W.L., Jr., Riegel, B.W.: Production rate and removal of rod outer segment material in vitamin A deficiency. Invest. Ophthal. 13, 40–53 (1974)

    Google Scholar 

  • Heuser, J.G., Reese, T.S.: Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. J. Cell Biol. 57, 315–344 (1973)

    Google Scholar 

  • Kanaseki, T., Kadota, K.: The “vesicle in a basket”. J. Cell Biol. 42, 202–220 (1969)

    Google Scholar 

  • Keirns, J.J., Miki, N., Bitensky, M.W., Keirns, M.: A link between rhodopsin and disc membrane cyclic nucleotide phosphodiesterase. Action spectrum and sensitivity to illumination. Biochem. 14, 2760–2766 (1975)

    Google Scholar 

  • Kolb, G.: Einschlüsse in Retinulazellen der Biene während der Adaptation. J. comp. Physiol. 91, 167–186 (1974)

    Google Scholar 

  • Kuwabara, T., Gorn, R.A.: Retinal damage by visible light. An electron microscopic study. Arch. Ophthal. 79, 69–78 (1968)

    Google Scholar 

  • Miller, J.A., Paulsen, R.: Phosphorylation and dephosphorylation of frog rod outer segment membranes as part of the visual process. J. biol. Chem. 250, 4427–4432 (1975)

    Google Scholar 

  • Nemanic, P.: Fine structure of the compound eye of Porcellio scaber in light and dark adaption. Tiss. Cell 7, 453–468 (1975)

    Google Scholar 

  • Nickel, E., Fernández, H.: Ultrastructural and molecular characteristics of crayfish photoreceptor membranes. (Abstr.). Exp. Brain Res. 23 Suppl., 148 (1975)

    Google Scholar 

  • Nir, I., Hall, M.O.: The ultrastructure of lipid-depleted rod photoreceptor membranes. J. Cell Biol. 63, 587–598 (1974)

    Google Scholar 

  • Noell, W.K., Albrecht, R.: Irreversible effects of visible light on the retina: role of vitamin A. Science 172, 76–80 (1971)

    Google Scholar 

  • Olive, J., Benedetti, E.L.: The structural organization of calf retinal photoreceptors derived from freeze fracture study. Mol. Biol. Reports 1, 245–249 (1974)

    Google Scholar 

  • Orci, L., Perrelet, A.: Freeze-etch histology. 168 pp. Berlin-Heidelberg-New York: Springer 1975

    Google Scholar 

  • Papermaster, D.S., Converse, C.A., Siu, J.: Membrane biosynthesis in the frog retina: opsin transport in the photoreceptor cell. Biochem. 14, 1343–1352 (1975)

    Google Scholar 

  • Pepe, I.M., Baumann, F.: Incorporation of 3H-labelled leucine into the protein fraction in the retina of the honeybee drone. J. Neurochem. 19, 507–512 (1972)

    Google Scholar 

  • Perrelet, A.: Protein synthesis in the visual cells of the honeybee drone as studied with electron microscope radioautography. J. Cell Biol. 55, 595–605 (1972)

    Google Scholar 

  • Perrelet, A., Bauer, H., Fryder, V.: Fracture faces of an insect rhabdome. J. Microscopie 13, 97–106 (1972)

    Google Scholar 

  • Raubach, R.A., Nemes, P.P., Dratz, E.A.: Chemical labelling and freeze-fracture studies on the localization of rhodopsin in the rod outer segment disk membrane. Exp. Eye Res. 18, 1–12 (1974)

    Google Scholar 

  • Roach, J.L.M., Wiersma, C.A.G.: Differentiation and degeneration of crayfish photoreceptors in darkness. Cell Tiss. Res. 153, 137–144 (1974)

    Google Scholar 

  • Seitz, G.: Nachweis einer Pupillenreaktion im Auge der Schmeißfliege. Z. vergl. Physiol. 69, 169–185 (1970)

    Google Scholar 

  • Sickel, W.: Thermal and photic regeneration of rhodopsin in perfused frog retina. In: Biochemistry of sensory function (L. Jaenicke, ed.), pp. 33–35. Berlin-Heidelberg-New York: Springer 1974

    Google Scholar 

  • Smith, R.E., Farquhar, M.G.: Lysosome function in the regulation of the secretory process in cells of the anterior pituitary gland. J. Cell Biol. 31, 319–347 (1966)

    Google Scholar 

  • Stieve, H.: Zur Biophysik des Sehvorgangs. Naturwissenschaften 62, 425–433 (1975)

    Google Scholar 

  • Teichberg, S., Holtzman, E., Crain, S.M., Peterson, E.R.: Circulation and turnover of synaptic vesicle membrane in cultured fetal mammalian spinal cord neurons. J. Cell Biol. 67, 215–230 (1975)

    Google Scholar 

  • Tuurala, O., Lehtinen, A.: Inkorporierung des tritiummarkierten Leucins in den Sehzellen von Oniscus asellus L. (Isopoda, Oniscoidea). Ann. Zool. Fenn. 11, 135–140 (1974)

    Google Scholar 

  • Waterman, T.H.: Expectation and achievement in comparative physiology. J. exp. Zool. 194, 309–343 (1975)

    Google Scholar 

  • Waterman, T.H., Fernández, H.R.: E-vector and wavelength discrimination by retinular cells of the crayfish Procambarus. Z. vergl. Physiol. 68, 154–174 (1970)

    Google Scholar 

  • Waterman, T.H., Horch, K.W.: Mechanism of polarized light perception. Science 154, 467–475 (1966)

    Google Scholar 

  • White, R.H.: The effect of light and light deprivation upon the ultrastructure of the larval mosquito eye. III. Multivesicular bodies and protein uptake. J. exp. Zool. 169, 261–278 (1968)

    Google Scholar 

  • White, R.H., Lord, E.: Diminution and enlargement of the mosquito rhabdom in light and darkness. J. gen. Physiol. 65, 583–598 (1975)

    Google Scholar 

  • Williams, T.P., Baker, B.N., Eder, D.J.: Interconversion of metarhodopsins. In: Biochemistry and physiology of visual pigments (H. Langer, ed.), pp. 83–88. Berlin-Heidelberg-New York: Springer 1973

    Google Scholar 

  • Young, R.W.: The renewal of photoreceptor cell outer segments. J. Cell Biol. 33, 61–72 (1967)

    Google Scholar 

  • Young, R.W.: The renewal of rod and cone outer segments in the rhesus monkey. J. Cell Biol. 49, 303–318 (1971)

    Google Scholar 

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This research was supported by grants from the U.S. National Institutes of Health (EY 00405), the National Geographic Society and the Japan Society for the Promotion of Science

The authors are grateful to Mr. Washioka of the JEOL Co. Research Laboratory for his essential help in effecting the freeze-etch preparations. They also thank Professor Ryoji Kikuchi of Tokyo Women's Medical College for welcome cooperation and hospitality as well as Dr. Karl Pfenninger of Yale University for his generous assistance in interpreting the freeze-etch data. Technical advice and help were also kindly provided on the acid phosphatase histochemistry by Professor Marilyn Farquhar and others in the Yale Cell Biology Section

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Eguchi, E., Waterman, T.H. Freeze-etch and histochemical evidence for cycling in crayfish photoreceptor membranes. Cell Tissue Res. 169, 419–434 (1976). https://doi.org/10.1007/BF00218144

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