Skip to main content
SpringerLink
Log in

Turnover of Photoreceptor Membrane and Visual Pigment in Invertebrates

  • Conference paper
Book cover The Molecular Mechanism of Photoreception

Part of the book series: Dahlem Workshop Reports ((DAHLEM LIFE,volume 34))

Abstract

Numerous ultrastructural studies are dealing with the problem of membrane turnover in invertebrate photoreceptors, with special attention to changes in the structure of the rhabdom, rhabdomeres, and microvilli and to other cytological changes within the cell. Both synthesis and degradation of photoreceptor membrane involve the formation of sequences of as yet poorly defined organelles. The underlying mechanisms are not understood. Even the microvillar cytoskeleton may, amongst other functions, play an important role in both membrane assembly and degradation. The daily cycle of light and darkness sets off changes — in some species quite drastic — in the size of the rhabdom. Generally, the size of the rhabdom decreases in light and increases again in the dark, indicating an imbalance between the rates of membrane breakdown and synthesis and/or assembly. The possible mechanisms whereby membrane turnover is triggered by light or by darkness are still obscure. The diurnal effects may be modified by endogenous factors.

Relatively few studies, however, have dealt with the problem at a molecular level. Autoradiographic studies using labeled amino acids demonstrated a random distribution of the label in the rhabdomeric membrane. Although in most cases the labeled proteins were not identified, it is assumed that the bulk of proteins labeled is the visual pigment. The general observation that more label was associated with the rhabdom in the dark than in the light was taken as an indication that the breakdown of rhabdomeric proteins was more rapid in the light than in the dark. Additional information on the turnover of visual pigment has come from quantification of rhodopsin and metarhodopsin by spectrophotometry. Progress has been made by studies on blowfly photoreceptors, revealing a selective breakdown of metarhodopsin at a rate inversely proportional to the intensity of the ambient light. The other part of the visual pigment cycle, the biosynthesis of rhodopsin, has been shown to depend on the presence of the 11-cis chromophore, in other words, the all-trans isomer resulting from the degradation of metarhodopsin has first to be isomerized in order to induce the synthesis of rhodopsin. This isomerization, which occurs through a light reaction, plays a key role in the turnover of visual pigment in that it links its two aspects, the breakdown and the biosynthesis. The following is an attempt to show how ultrastructural findings can be related to the molecular events which underlie the turnover of rnabdomeric membrane and of the visual pigment.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Akino, T., and Tsuda, M. 1979. Characteristics of phospholipids in microvillar membranes of octopus photoreceptor cells. Biochim. Biophys. Acta 556: 61–71.

    Article  PubMed  CAS  Google Scholar 

  2. Anderson, E.R.; Benolken, R.M.; Kelleher, P.A.; Maude, M.B.; and Wiegand, R.D. 1978. Chemistry of photoreceptor membrane preparations from squid retinas. Biochim. Biophys. Acta 510: 316–326.

    Article  PubMed  CAS  Google Scholar 

  3. Barlow, R.B., Jr. 1983. Circadian rhythms in the Limulus visual system. J. Neurosci. 3: 856–870.

    PubMed  Google Scholar 

  4. Barlow, R.B., Jr.; Chamberlain, S.C.; and Levinson, J.Z. 1980. Limulus brain modulates the structure and function of lateral eyes. Science 210: 1037–1039.

    Article  PubMed  Google Scholar 

  5. Behrens, M.E. 1974. Photomechanical changes in the ommatidia of Limulus lateral eye during light and dark adaptation. J. Comp. Physiol. 89: 45–57.

    Article  Google Scholar 

  6. Behrens, M.E., and Krebs, W. 1976. The effect of light-dark adaptation on the ultrastructure of Limulus lateral eye retinular cells. J. Comp. Physiol. 107: 77–96.

    Article  Google Scholar 

  7. Bernard, G.D. 1983. Bleaching of rhabdoms in eyes of intact butterflies. Science 219: 69–71.

    Article  PubMed  CAS  Google Scholar 

  8. Bernard, G.D. 1983. Dark processes following photoconversion of butterfly rhodopsins. Biophys. Struct. Mech. 9: 277–286.

    Article  CAS  Google Scholar 

  9. Blest, A.D. 1980. Photoreceptor membrane turnover in arthropods: Comparative studies of breakdown processes and their implications. In The Effect of Constant Light on Visual Processes, eds. T.P. Williams and B.N. Baker, pp. 217–245. New York: Plenum Press.

    Google Scholar 

  10. Blest, A.D., and Day, W.A. 1978. The rhabdomere organization of some nocturnal pisaurid spiders in light and darkness. Phil. Trans. Roy. Soc. Lond. B 283: 1–23.

    Article  Google Scholar 

  11. Blest, A.D., and Maples, J. 1979. Exocytotic shedding and glial uptake of photoreceptor membrane by a salticid spider. Proc. Roy. Soc. Lond. B 204: 105–112.

    Article  CAS  Google Scholar 

  12. Blest, A.D.; Stowe, S.; and de Couet, H.G. 1984. Turnover of photoreceptor membranes in arthropods. Sci. Progr. 69: 83–100.

    CAS  Google Scholar 

  13. Blest, A.D.; Stowe, S.; and Eddey, W. 1982. A labile Ca2+-dependent cytoskeleton in rhabdomeral microvilli of blowflies. Cell Tiss. Res. 223: 553–573.

    Article  CAS  Google Scholar 

  14. Blest, A.D.; Stowe, S.; Eddey, W.; and Williams, D.S. 1982. The local deletion of a microvillar cytoskeleton from photoreceptors of tipulid flies during membrane turnover. Proc. Roy. Soc. Lond. 215: 469–479.

    Article  CAS  Google Scholar 

  15. Boschek, C.B., and Hamdörf, K. 1976. Rhodopsin particles in the photoreceptor membrane of an insect. Z. Naturforsch. 39c: 762.

    Google Scholar 

  16. Brandenburger, J.L. 1977. Cytochemical localization of acid phosphatases in regenerated and dark-adapted eyes of a snail, Helix aspersa. Cell Tiss. Res. 184: 301–313.

    Article  CAS  Google Scholar 

  17. Brandenburger, J.L., and Eakin, R.M. 1970. Pathway of incorporation of vitamin A 3H2 into photoreceptors of a snail, Helix aspersa. Vision Res. 10: 639–653.

    Article  PubMed  CAS  Google Scholar 

  18. Brandenburger, J.L., and Eakin, R.M. 1980. Cytochemical localization of acid phosphatase in ocelli of the seastar Patiria miniata during recycling of photoreceptor membranes. J. Exp. Zool. 214: 127–140.

    Article  CAS  Google Scholar 

  19. Brandenburger, J.L.; Reed, C.T.; and Eakin, R.M. 1975. Freezefracture studies of photoreceptors of dark and light-adapted snails. Am. Zool. 15: 782.

    Google Scholar 

  20. Bruno, M.S.; Barnes, S.N.; and Goldsmith, T.H. 1977. The visual pigment and visual cycle of the lobster, Homarus. J. Comp. Physiol. 120: 123–142.

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  22. Chamberlain, S.C., and Barlow, R.B., Jr. 1979. Light and efferent activity control rhabdom turnover in Limulus photoreceptors. Science 206: 361–363.

    Article  PubMed  CAS  Google Scholar 

  23. Chamberlain, S.C., and Barlow, R.B., Jr. 1984. Transient membrane shedding in Limulus photoreceptors: Control mechanisms under natural lighting. J. Neurosci. 4: 2792–2810.

    PubMed  CAS  Google Scholar 

  24. Cronin, T.W., and Goldsmith, T.H. 1984. Dark regeneration of rhodopsin in crayfish photoreceptors. J. Gen. Physiol. 84: 63–81.

    Article  PubMed  CAS  Google Scholar 

  25. Eakin, R.M. 1972. Structure of invertebrate photoreceptors. In Photochemistry of Vision, Handbook of Sensory Physiology, ed. H.J.A. Dartnall, vol. VII/1, pp. 625–684. Berlin, Heidelberg, New York: Springer-Verlag.

    Google Scholar 

  26. Eakin, R.M., and Brandenburger, J.L. 1975. Understanding a snailfs eye at a snail’s pace. Am. Zool. 15: 851–863.

    Google Scholar 

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

    Article  CAS  Google Scholar 

  28. Eguchi, E., and Waterman, T.H. 1976. Freeze-etch and histochemical evidence for cycling in crayfish photoreceptor membranes. Cell Tiss. Res. 169: 419–434.

    Article  CAS  Google Scholar 

  29. Goldman, L.J.: Barnes, S.N.; and Goldsmith, T.H. 1975. Microspectrophotometry of rhodopsin and metarhodopsin in the moth Galleria. J. Gen. Physiol. 66: 383–404.

    Article  PubMed  CAS  Google Scholar 

  30. Goldsmith, T.H., and Wehner, R. 1977. Restrictions of rotational and translational diffusion of pigment in the membranes of a rhabdomeric photoreceptor. J. Gen. Physiol. 70: 453–490.

    Article  PubMed  CAS  Google Scholar 

  31. Hafner, G.S., and Bok, D. 1977. The distribution of [3H] leucine labeled protein in the retinula cells of the crayfish retina. J. Comp. Neurol. 174: 397–416.

    Article  PubMed  CAS  Google Scholar 

  32. Hamacher, K. 1981. Absorptionsspektropische Analyse des Astacus Rhodopsinsystems und Nachweis einer metabolischen Regeneration des Rhodopsins nach Helladaptation. Thesis, Berichte der Kfa Jülich Nr. 1718, Jülicn, F.R. Germany.

    Google Scholar 

  33. Hamacher, K., and Stieve, H. 1984. Spectral properties of the rhodopsin-system of the crayfish Astacus leptodactylus. Photochem. Photobiol. 39: 379–390.

    Article  CAS  Google Scholar 

  34. Hamdorf, K. 1979. The physiology of invertebrate visual pigments. In Vision in Invertebrates, Handbook of Sensory Physiology, ed. H. Autrum, vol. VII/6A, pp. 145–224. Berlin, Heidelberg, New York: Springer-Verlag.

    Chapter  Google Scholar 

  35. Hamdorf, K., and Schwemer, J. 1975. Photoregeneration and the adaptation process in insect photoreceptors. In Photoreceptor Optics, eds. A.W. Snyder and R. Menzel, pp. 263–289. Berlin, Heidelberg, New York: Springer-Verlag.

    Google Scholar 

  36. Hara, T., and Hara, R. 1982. Cephalopod retinochrome. In Methods in Enzymology. Part H: Visual Pigments and Purple Membranes I, ed. L. Packer, vol. 81, pp. 827–833. New York: Academic Press.

    Chapter  Google Scholar 

  37. Harris, A.W.; Ready, D.F.; Lipson, E.D.; Hudspeth, A.J.; and Stark, W.S. 1977. Vitamin A deprivation and Drosophila photopigments. Nature 266: 648–650.

    Article  PubMed  CAS  Google Scholar 

  38. Holtzman, E., and Mercurio, A.M. 1980. Membrane circulation in neurons and photoreceptors: some unresolved issues. Int. Rev. Cytol. 67: 1–67.

    Article  PubMed  CAS  Google Scholar 

  39. Itaya, S.K. 1976. Rhabdom changes in the shrimp, Palaemonetes. Cell Tiss. Res. 166: 265–273.

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  41. Kito, Y.; Naito, T.; and Nashima, K. 1982. Purification of squid and octopus rhodopsin. In Methods in Enzymology. Part H: Visual Pigments and Purple Membranes I, ed. L. Packer, vol. 81, pp. 167–171. New York: Academic Press.

    Chapter  Google Scholar 

  42. Kito, Y.; Seki, T.; and Hagins, F.M. 1982. Isolation and purification of squid rhabdoms. In Methods in Enzymology. Part H: Visual Pigments and Purple Membranes I, ed. L. Packer, vol. 81, pp. 43–48. New York: Academic Press.

    Chapter  Google Scholar 

  43. Krauhs, J.H.; Mahler, H.R.; Minkler, G.; and Moore, W.J. 1976. Synthesis and degradation of protein of visual receptor membranes in lateral eyes of Limulus. J. Neurochem. 26: 281–283.

    Article  PubMed  CAS  Google Scholar 

  44. Larrivee, D.C.; Conrad, S.K.; Stephenson, R.S.; and Pak, W.L. 1981. Mutation that selectively affects rhodopsin concentration in the peripheral photoreceptors of Drosophila. J. Gen. Physiol. 78: 521–545.

    Article  PubMed  CAS  Google Scholar 

  45. Laughlin, S.B.; Menzel, R.; and Snyder, A.W. 1975. Membranes, dichroism and receptor sensitivity. In Photoreceptor Optics, eds. A.W. Snyder and R. Menzel, pp. 237–259. Berlin, Heidelberg, New York: Springer-Verlag.

    Google Scholar 

  46. Nässel, D.R., and Waterman, T.H. 1979. Massive diurnally modulated photoreceptor membrane turnover in crab light-and dark adaptation. J. Comp. Physiol. 131: 205–216.

    Article  Google Scholar 

  47. Ozaki, K.; Hara, R.; and Hara, T. 1983. Squid retinochrome. Biophys. J. 44: 127–137.

    Article  PubMed  CAS  Google Scholar 

  48. Paulsen, R., and Bentrop, J. 1984. Reversible phosphorylation of opsin induced by irradiation of blowfly retinae. J. Comp. Physiol. A 155: 39–45.

    Article  CAS  Google Scholar 

  49. Paulsen, R., and Schwemer, J. 1979. Vitamin A-deficiency reduces the concentration of visual pigment protein within blowfly photoreceptor membranes. Biochim. Biophys. Acta 557: 385–390.

    Article  PubMed  CAS  Google Scholar 

  50. Paulsen, R., and Schwemer, J. 1983. Biogenesis of blowfly photoreceptor membranes is regulated by 11-cis retinal. Eur. J. Biochem. 137: 609–614.

    Article  PubMed  CAS  Google Scholar 

  51. Paulsen, R.; Zinkler, D.; and Delmelle, M. 1983. Architecture and dynamics of microvillar photoreceptor membranes of cephalopods. Exp. Eye Res. 36: 47–56.

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  54. Robles, L.J.; Cabebe, C.S.; Aguilo, J.A.; Anyakora, P.A.; and Bok, D. 1984. Autoradiographic and biochemical analysis of photoreceptor membrane renewal in octopus retina. J. Neurocytol. 13: 145–164.

    Article  PubMed  CAS  Google Scholar 

  55. Saibil, H.R. 1982. An ordered membrane-cytoskeleton network in squid photoreceptor microvilli. J. Molec. Biol. 158: 435–456.

    Article  PubMed  CAS  Google Scholar 

  56. Schwemer, J. 1983. Pathways of visual pigment regeneration in fly photoreceptors. Biophys. Struct. Mech. 9: 287–298.

    Article  CAS  Google Scholar 

  57. Schwemer, J. 1984. Renewal of visual pigment in photoreceptors of the blowfly. J. Comp. Physiol. 154: 535–547.

    Article  CAS  Google Scholar 

  58. Schwemer, J., and Henning, U. 1984. Morphological correlates of visual pigment turnover in photoreceptors of the fly. Cell Tiss. Res. 236: 293–303.

    Article  CAS  Google Scholar 

  59. Schwemer, J.; Pepe, I.M.; Paulsen, R.; and Cugnoli, C. 1984. Light-activated trans-cis isomerization of retinal by a protein from honeybee retina. J. Comp. Physiol. 154: 549–554.

    Article  CAS  Google Scholar 

  60. Seki, T.; Hara, R.; and Hara, T. 1980. Reconstitution of squid rhodopsin in rhabdomal membranes. Photochem. Photobiol. 32: 469–479.

    Article  CAS  Google Scholar 

  61. Stavenga, D.G. 1975. Dark regeneration of invertebrate visual pigments. In Photoreceptor Optics, eds. A.W. Snyder and R. Menzel, pp. 290–295. Berlin, Heidelberg, New York: Springer-Verlag.

    Google Scholar 

  62. Stavenga, D.G., and Schwemer, J. 1984. Visual pigments of invertebrates. In Photoreception and Vision in Invertebrates, ed. M.A. Ali, pp. 11–61. New York: Plenum Press.

    Google Scholar 

  63. Stein, P.J.; Brammer, J.O.; and Ostroy, S.E. 1979. Renewal of opsin in the photoreceptor cells of the mosquito. J. Gen. Physiol. 74: 565–582.

    Article  PubMed  CAS  Google Scholar 

  64. Stowe, S. 1980. Rapid synthesis of photoreceptor membrane and assembly of new microvilli in a crab at dusk. Cell Tiss. Res. 211: 419–440.

    Article  CAS  Google Scholar 

  65. Stowe, S. 1981. Effects of illumination changes on rhabdom synthesis in a crab. J. Comp. Physiol. 142: 19–25.

    Article  Google Scholar 

  66. Stowe, S. 1982. Rhabdom synthesis in isolated eyestalks and retinae of the crab Leptograpsus variegatus. J. Comp. Physiol. 148: 313–321.

    Article  Google Scholar 

  67. Stowe, S. 1983. Light-induced and spontaneous breakdown of the rhabdoms in a crab at dawn; depolarization versus calcium levels. J. Comp. Physiol. 153: 365–375.

    Article  Google Scholar 

  68. Stowe, S. 1983. Phagocytosis of rhabdomeral membrane by crab photoreceptors (Leptograpsus variegatus). Cell Tiss. Res. 234: 463–467.

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

  70. Vogt, K. 1983. Is the fly visual pigment a rhodopsin? Z. Naturforsch. 38c: 329–333.

    CAS  Google Scholar 

  71. Vogt, K., and Kirsehfeid, K. 1984. Chemical identity of the chromophores of fly visual pigment. Naturwiss. 71: 211–212.

    Article  CAS  Google Scholar 

  72. Waddington, C.H., and Perry, M.M. 1960. The ultrastructure of the developing eye of Drosophila. Proc. Roy. Soc. Lond. B 153: 155–178.

    Article  Google Scholar 

  73. Wald. G., and Burg, S. 1957. The vitamin A of the lobster. J. Gen. Physiol. 40: 609–625.

    Article  PubMed  CAS  Google Scholar 

  74. Waterman, T.H. 1982. Fine structure and turnover of photoreceptor membranes. In Visual Cells and Evolution, ed. J.A. Westfall, pp. 23–41. New York: Raven Press.

    Google Scholar 

  75. White, R.H. 1968. The effect of light and light deprivation upon the structure of the larval mosquito eye. III. Multivesicular bodies and protein uptake. J. Exp. Zool. 169: 261–278.

    CAS  Google Scholar 

  76. White, R.H.; Brown, P.K.; Hurley, A.K.; and Bennett, R.R. 1983. Rhodopsins, retinal cell ultrastructure, and receptor potentials in the developing pupal eye of the moth Manduca sexta. J. Comp. Physiol. 150: 153–163.

    Article  Google Scholar 

  77. White, R.H.; Gifford, p.; and Michaud, N.A. 1980. Turnover of photoreceptor membrane in the larval mosquito ocellus: rhabdomeric coated vesicles and organelles of the vacuolar system. In Effects of Constant Light on Visual Processes, eds. T.P. Williams and B.N. Baker, pp. 271–296. New York: Plenum Press.

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  79. Whittle, A.C. 1976. Reticular specializations in photoreceptors: a review. Zool. Scripta 5: 191–206.

    Article  Google Scholar 

  80. Williams, D.S. 1982. Ommatidial structure in relation to turnover of photoreceptor membrane in the locust. Cell Tiss. Res. 225: 595–617.

    Article  CAS  Google Scholar 

  81. Williams, D.S. 1982. Photoreceptor membrane shedding and assembly can be initiated locally within an insect retina. Science 218: 898–900.

    Article  PubMed  CAS  Google Scholar 

  82. Williams, D.S. 1982. Rhabdom size and photoreceptor membrane turnover in a muscoid fly. Cell Tiss. Res. 226: 629–639.

    Article  CAS  Google Scholar 

  83. Williams, D.S., and Blest, A.D. 1980. Extracellular shedding of photoreceptor membrane in the open rhabdom of a tipulid fly. Cell Tiss. Res. 205: 423–438.

    Article  CAS  Google Scholar 

  84. Winterhager, E.; Dahl, G.; and Stieve, H. 1981. Ultrastructural changes of microvilli of the Astacus retina depending on the state of adaptation. Verh. Anat. Ges. 75: 959–960.

    Google Scholar 

  85. Winterhager, E., and Stieve, H. 1982. Effect of hyper-and hypoosmotic solutions on the structure of the Astacus retina. Cell Tiss. Res. 223: 267–280.

    Article  CAS  Google Scholar 

  86. Young, R.W. 1976. Visual cells and the concept of renewal. Inv. Ophthalmol. 9: 700–725.

    Google Scholar 

  87. Zinkler, D. 1974. Lipid and fatty acid composition of a rhabdomeric retina. Verh. Dtsch. Zool. Ges. 67: 28–32.

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institut für Tierphysiologie, Ruhr-Universität Bochum, 4630, Bochum 1, F.R. Germany

    J. Schwemer

Authors
  1. J. Schwemer
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

H. Stieve

Rights and permissions

Reprints and permissions

Copyright information

© 1986 Dr. S. Bernhard, Dahlem Konferenzen, Berlin

About this paper

Cite this paper

Schwemer, J. (1986). Turnover of Photoreceptor Membrane and Visual Pigment in Invertebrates. In: Stieve, H. (eds) The Molecular Mechanism of Photoreception. Dahlem Workshop Reports, vol 34. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-70444-4_18

Download citation

  • DOI: https://doi.org/10.1007/978-3-642-70444-4_18

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-642-70446-8

  • Online ISBN: 978-3-642-70444-4

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation