Visual Pigments of Compound Eyes — Structure, Photochemistry, and Regeneration

  • Joachim Schwemer
Conference paper

Abstract

Visual pigments comprise a family of chromoproteins which are incorporated in highly specialized membrane areas of photoreceptor cells. The function of these molecules is to absorb light quanta, which are often directed onto these membrane areas by special optical means. Absorbed light quanta cause the 11-cis chrornophore of the visual pigment to isomerize to the all-trans form, the only reaction of the visual process that requires light. This in turn leads to conformational changes of the protein. These changes initiate a complex sequence of biochemical and biophysical events that eventually lead to the excitation of the photoreceptor cell. Following transmission of these electrical signals to higher-order neurons and their processing, the information gathered through the absorption of a few light quanta may finally lead to a comprehensive behavioral response. Thus, the knowledge of how visual pigments are constructed, transformed by light, and regenerated is fundamental to the understanding of photoreceptor function. Although this brief survey will concentrate on the visual pigments of compound eyes, data from other pigment systems will be quoted for comparison whenever appropriate.

Keywords

Schiff Base Photoreceptor Cell Visual Pigment Opsin Gene Purple Membrane 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.
This is a preview of subscription content, log in to check access.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Applebury ML, Hargrave P (1986) Molecular biology of the visual pigments. Vision Res 26:1881–1895.PubMedCrossRefGoogle Scholar
  2. Autrum H (ed) (1981) Light and dark adaptation in invertebrates. In: Handbook of sensory physiology, vol VII/6C. Springer, Berlin Heidelberg New York, pp 1–91.Google Scholar
  3. Baehr W, Applebury ML (1986) Exploring visual transduction with recombinant DNA techniques. TINS 9:198–203.Google Scholar
  4. Bernard GD (1983) Bleaching of rhabdoms in eyes of intact butterflies. Science 219:69–71.PubMedCrossRefGoogle Scholar
  5. Bernard GD (1984) Dark-regeneration of butterfly rhodopsin at physiological temperatures. Invest Ophthalmol 25 (Suppl): 60.Google Scholar
  6. Bernstein PS, Law WC, Rando RR (1987) Isomerization of all-trans retinoids to 11-cis retinoids in vitro. Proc Natl Acad Sci USA 84:1849–1853.PubMedCrossRefPubMedCentralGoogle Scholar
  7. Blest AD (1980) Photoreceptor membrane turnover in arthropods: Comparative studies of breakdown processes and their implications. In: Williams TP, Baker BN (eds) The effect of constant light in visual processes. Plenum, New York, pp 217–245.CrossRefGoogle Scholar
  8. Blest AD, Stowe S, deCouet HG (1984) Turnover of photoreceptor membranes in arthropods. Sci Progr 69:83–100.PubMedGoogle Scholar
  9. Boschek CB, Hamdorf K (1976) Rhodopsin particles in the photoreceptor membrane of an insect. Z Naturforsch 39c:762.Google Scholar
  10. Bownds D (1967) Site of attachment of retinal in rhodopsin. Nature (London) 184:1178–1181.CrossRefGoogle Scholar
  11. Bridges CDB (1972) The rhodopsin-porphyropsin visual system. In: Dartnall HJA (ed) Handbook of sensory physiology, vol VII/1. Springer, Berlin Heidelberg New York, pp 417–480.Google Scholar
  12. Brown PK, Brown PS (1958) Visual pigments of the octopus and cuttle fish. Nature (London) 182:1288–1290.CrossRefGoogle Scholar
  13. Bruno MS, Barnes SN, Goldsmith TH (1977) The visual pigment and visual cycle of the lobster, Homarus. J Comp Physiol A 120:123–142.CrossRefGoogle Scholar
  14. Chamberlain SC, Barlow RB (1984) Transient membrane shedding in Limulus photoreceptors: Control mechanisms under natural lighting. J Neurosci 4:2792–2810.PubMedGoogle Scholar
  15. Cowman AF, Zuker CS, Rubin GM (1986) An opsin gene expressed in only one photoreceptor cell type of Drosophila eye. Cell 44:705–710.PubMedCrossRefGoogle Scholar
  16. Cronin TW, Goldsmith TH (1984) Dark regeneration of rhodopsin in crayfish photoreceptors. J Gen Physiol 84:63–81.PubMedCrossRefGoogle Scholar
  17. Dixon SF, Cooper A (1987) Quantum efficiencies of the reversible photo-reaction in octopus rhodopsin. Photochem Photobiol 46:115–119.PubMedCrossRefGoogle Scholar
  18. Eguchi E, Waterman TH (1967) Changes in the retinal fine structure induced in the crab Libinia by light and dark adaptation. Z Zellforsch 79:209–229.PubMedCrossRefGoogle Scholar
  19. Findlay JBC (1986) The biosynthetic, functional and evolutionary implications of the structure of rhodopsin. In: Stieve H (ed) The molecular mechanism of photoreception. Dahlem Konf. Springer, Berlin Heidelberg New York, pp 11–30.CrossRefGoogle Scholar
  20. Fryxell KJ, Meyerowitz EM (1987) An opsin gene is expressed only in the R7 photoreceptor cell of Drosophila. EMBO J 6:443–451.PubMedPubMedCentralGoogle Scholar
  21. Goldman LJ, Barnes SN, Goldsmith TH (1975) Microspectrophotometry of rhodopsin and metarhodopsin in the moth Galleria. J Gen Physiol 66:383–404.PubMedCrossRefGoogle Scholar
  22. Goldsmith TH, Bernard GD (1985) Visual pigments of invertebrates. Photochem Photobiol 42:805–809.CrossRefGoogle Scholar
  23. Hamacher K (1981) Absorptionsspektroskopische Analyse des Astacus Rhodbpsinsystems und Nachweis einer metabolischen Regeneration des Rhodopsins nach Helladaptation. Thesis, Ber Kfa Jülich 1718,Jülich,FRG.Google Scholar
  24. Hamdorf K (1979) The physiology of invertebrate visual pigments. In: Autrum H (ed) Handbook of sensory physiology, vol VII/6A. Springer, Berlin Heidelberg New York, pp 145–224.Google Scholar
  25. Hamdorf K, Schwemer J (1975) Photoregeneration and the adaptation process in insect photoreceptors. In: Snyder AW, Menzel R (eds) Photoreceptor optics. Springer, Berlin Heidelberg New York, pp 263–289.CrossRefGoogle Scholar
  26. Hamdorf K, Schwemer J, Täuber U (1968) Der Sehfarbstoff, die Absorption der Rezeptoren und die spektrale Empfindlichkeit der Retina von Eledone moschata. Z vergl Physiol 60:375–415.CrossRefGoogle Scholar
  27. Hamdorf K, Gogala M, Schwemer J (1971) Beschleunigung der Dunkeladaptation eines UV-Rezeptors durch sichtbare Strahlung. Z Vergl Physiol 75:189–199.Google Scholar
  28. Hamdorf K, Paulsen R, Schwemer J (1973) Photoregeneration and sensitivity control of photoreceptors of invertebrates. In: Langer H (ed) Biochemistry and physiology of visual pigments. Springer, Berlin Heidelberg New York, pp 155–166.CrossRefGoogle Scholar
  29. Hara T, Hara R (1980) Retinochrome and rhodopsin in the extra ocular photoreceptor of the squid, Todarodes. J Gen Physiol 75:1–19.PubMedCrossRefGoogle Scholar
  30. Hara T, Hara R (1982) Cephalopod retinochrome. In: Packer L (ed) Methods in enzymology. Pt H: Visual pigments and purple membranes I, vol 81. Academic Press, New York London, pp 827–833.CrossRefGoogle Scholar
  31. Hargrave PA, McDowell JH, Curtis DR, Wang JK, Juszczak E, Fong S-L, Rao JKM Argos P (1983) The structure of bovine opsin. Biophys Struct Mech 9:235–244.PubMedCrossRefGoogle Scholar
  32. Harris AW, Ready DF, Lipson ED, Hudspeth AJ, Stark WS (1977) Vitamin A deprivation and Drosophila photopigments. Nature (London) 266:648–650.CrossRefGoogle Scholar
  33. Honig B, Dinur U, Nakanishi K, Balogh-Nair V, Gawinowicz MA, Arnaboldi M, Motto MG (1979) An external point-charge model for wavelength regulation in visual pigments. J Am Chem Soc 101:7084–7086.CrossRefGoogle Scholar
  34. Hubbard R, St. George RCC (1958) The rhodopsin system of the squid. J Gen Physiol 41:501–528.PubMedCrossRefPubMedCentralGoogle Scholar
  35. Itaya SK (1976) Rhabdom changes in the shrimp, Palaemonetes. Cell Tissue Res 166:265–273.PubMedGoogle Scholar
  36. Kirschfeld K (1986) Activation of visual pigment: Chromophore structure and function. In: Stieve H (ed) The molecular mechanism of photoreception. Dahlem Konf. Springer, Berlin Heidelberg New York, pp 31–49.CrossRefGoogle Scholar
  37. Kirschfeld K, Vogt K (1986) Does retinol serve a sensitizing function in insect photoreceptors? Vision Res 26:1771–1777.PubMedCrossRefGoogle Scholar
  38. Kropf A, Brown PK, Hubbard R (1959) Lumi-and metarhodopsin of squid and octopus. Nature (London) 183:446–448.Google Scholar
  39. Kruizinga B, Kamman RL, Stavenga DG (1983) Laser-induced visual pigment conversions in fly photoreceptors measured in vivo. Biophys Struct Mech 9:299–307.CrossRefGoogle Scholar
  40. Montell C, Jones K, Zuker CS, Rubin G (1987) A second opsin gene expressed in the ultraviolet sensitive R7 photoreceptor cell of Drosophila melanogaster. J Neurosci 7:1558–1566.PubMedGoogle Scholar
  41. Nässel DR, Waterman TH (1979) Massive diurnally modulated photoreceptor membrane turnover in crab light and dark adaptation. J Comp Physiol A 131:205–216.CrossRefGoogle Scholar
  42. Oseroff AR, Callender RH (1974) Resonance Raman spectroscopy of rhodopsin in retinal disk membranes. Biochemistry 13:4243–4248.PubMedCrossRefGoogle Scholar
  43. O’Tousa JE, Baehr W, Martin RL, Hirsh I, Pak WL, Applebury ML (1985) The Drosophila nina E gene encodes an opsin. Cell 40:839–850.PubMedCrossRefGoogle Scholar
  44. Ovchinnikov YA (1982) Rhodopsin and bacterio-rhodopsin: structure function relationships. FEBS Lett 148:179–191.PubMedCrossRefGoogle Scholar
  45. Ovchinnikov YA (1987) Structure of rhodopsin and bacteriorhodopsin. Photochem Photobiol 45:909–914.PubMedCrossRefGoogle Scholar
  46. Ozaki K, Terakita A, Hara R, Hara T (1986) Rhodopsin and retinochrome in the retina of a marine gastropod, Conomulex luhuanus. Vision Res 26:691–705.PubMedCrossRefGoogle Scholar
  47. Pande C, Pande A, Yue KT, Callender R, Ebrey TG, Tsuda M (1987a) Resonance Raman spectroscopy of octopus rhodopsin and its photoproducts. Biochemistry 26:4941–4947.PubMedCrossRefGoogle Scholar
  48. Pande C, Deng H, Rath P, Callender R, Schwemer J (1987b) Resonance Raman spectroscopy of an UV-sensitive insect rhodopsin. Biochemistry 26:7426–7430.PubMedCrossRefGoogle Scholar
  49. Pappin PJC, Eliopoulos E, Brett M, Findlay JBC (1984) A structural model for bovine rhodopsin. Int J Biol Macromol 6:73–76.CrossRefGoogle Scholar
  50. Paulsen R, Bentrop J (1986) Light-modulated biochemical events in fly photoreceptors. In: Lüttgau HCh (ed) Membrane control. Fortschr Zool 33:299–319.Google Scholar
  51. Paulsen R, Schwemer J (1972) Studies on the insect visual pigment sensitive to ultraviolet light: retinal as the chromophoric group. Biochim Biophys Acta 283:520–529.PubMedCrossRefGoogle Scholar
  52. Paulsen R, Schwemer J (1979) Vitamin-A deficiency reduces the concentration of visual pigment protein within blowfly photoreceptor membranes. Biochem Biophys Acta 557:385–390.PubMedCrossRefGoogle Scholar
  53. Paulsen R, Schwemer J (1983) Biogenesis of blowfly photoreceptor membranes is regulated by 11-cis retinal. Eur J Biochem 137:609–614.PubMedCrossRefGoogle Scholar
  54. Pepe IM, Schwemer J, Paulsen R (1982) Characteristics of retinal-binding protein from the honeybee retina. Vision Res 22:775–781.PubMedCrossRefGoogle Scholar
  55. Pepe IM, Cugnoli C, Peluso M, Vergani L, Boero A (1987) Structure of a protein catalyzing the formation of 11-cis retinal in the visual cycle of invertebrate eyes. Cell Biophys 10:15–22.PubMedGoogle Scholar
  56. Schwemer J (1969) Der Sehfarbstoff von Eledone moschata und seine Umsetzungen in der lebenden Netzhaut. Z Vergl Physiol 62:121–152.CrossRefGoogle Scholar
  57. Schwemer J (1979) Molekulare Grundlagen der Photorezeption bei der Schmeißfliege Calliphora erythrocephala Meig. Habil Schr, Fak Biol, Ruhr-Univ Bochum, FRG.Google Scholar
  58. Schwemer J (1983) Pathways of visual pigment regeneration in fly photoreceptors. Biophys Struct Mech 9:287–298.CrossRefGoogle Scholar
  59. Schwemer J (1984) Renewal of visual pigment in photoreceptors of the blowfly. J Comp Physiol A 154:535–547.CrossRefGoogle Scholar
  60. Schwemer J (1986) Turnover of photoreceptor membrane and visual pigment in invertebrates. In: Stieve H (ed) The molecular mechanism of photoreception. Dahlem Konf. Springer, Berlin Heidelberg New York, pp 303–326.CrossRefGoogle Scholar
  61. Schwemer J, Henning U (1984) Morphological correlates of visual pigment turnover in photoreceptors of the fly. Cell Tissue Res 236:293–303.PubMedGoogle Scholar
  62. Schwemer J, Langer H (1982) Insect visual pigments. In: Packer L (ed) Methods in enzymology. Pt H: Visual pigments and purple membranes I, vol 81. Academic Press, New York London, pp 182–190.CrossRefGoogle Scholar
  63. Schwemer J, Paulsen R (1973) Three visual pigments in Deilephila elpenor (Lepidoptera, Sphingidae). J Comp Physiol 86:215–229.CrossRefGoogle Scholar
  64. Schwemer J, Pepe IM, Paulsen R, Cugnoli C (1984) Light-activated trans-cis isomerization of retinal by a protein from honeybee retina. J Comp Physiol A 154:549–554.CrossRefGoogle Scholar
  65. Seki T, Hara R, Hara T (1980) Reconstitution of squid rhodopsin in rhabdomal membranes. Photochem Photobiol 32:469–479.CrossRefGoogle Scholar
  66. Shichida Y, Matuoka S, Yoshizawa T (1984) Formation of photorhodopsin, a precursor of bathorhodopsin, detected by picosecond laser photolysis at room temperature. Photobiochem Photobiophys 7:221–228.Google Scholar
  67. Stavenga DG, Schwemer J (1984) Visual pigments of invertebrates. In: Ali MA (ed) Photoreception and vision in invertebrates. Plenum, Oxford New York, pp 11–61.CrossRefGoogle Scholar
  68. Stavenga DG, Zantema A, Kuiper JW (1973) Rhodopsin processes and the function of the pupil mechanism in flies. In: Langer H (ed) Biochemistry and physiology of visual pigments. Springer, Berlin Heidelberg New York, pp 175–180.CrossRefGoogle Scholar
  69. Stein PJ, Brammer JO, Ostroy SE (1978) Renewal of opsin in the photoreceptor cells of the mosquito. J Gen Physiol 74:565–582.CrossRefGoogle Scholar
  70. Stowe S (1983) Light-induced and spontaneous breakdown of the rhabdoms in a crab at dawn; depolarization versus calcium levels. J Comp Physiol A 153:365–375.CrossRefGoogle Scholar
  71. Suzuki T, Makino-Tasaka M, Eguchi E (1984) 3-dehydroretinal (vitamin A2 aldehyde) in crayfish eye. Vision Res. 24:783–789.PubMedCrossRefGoogle Scholar
  72. Tsuda M (1987) Photoreception and phototransduction in invertebrate photoreceptors. Photochem Photobiol 45:915–931.CrossRefGoogle Scholar
  73. Uematsu J, Hara R, Nishimura I, Wada K, Matsubara H, Hara T (1986) Amino-terminal sequence of squid retinochrome. Photobiochem Photobiophys 13:197–201.Google Scholar
  74. Vogt K (1983) Is the fly visual pigment a rhodopsin? Z Naturforsch 38c:329–333.Google Scholar
  75. Vogt K, Kirschfeld K (1983) C 40-Carotinoide in Fliegenaugen. Verh Dtsch Zool Ges 76:330.Google Scholar
  76. Vogt K, Kirschfeld K (1984) Chemical identity of the chromophores of fly visual pigment. Naturwissenschaften 71:211–213.CrossRefGoogle Scholar
  77. Waterman TH (1982) Fine structure and turnover of photoreceptor membranes. In: Westfall JA (ed) Visual cells and evolution. Raven, New York, pp 23–41.Google Scholar
  78. White RH (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.PubMedCrossRefGoogle Scholar
  79. White RH (1985) Insect visual pigments and color vision. In: Kerkut GA, Gilbert Ll (eds) Comprehensive insect physiology, biochemistry and pharmacology, vol 6. Pergamon, New York, pp 431–493.Google Scholar
  80. Williams DS (1982) Rhabdom size and photoreceptor membrane turnover in a muscoid fly. Cell Tissue Res 226:629–639.PubMedGoogle Scholar
  81. Williams DS, Blest AD (1980) Extracellular shedding of photoreceptor membrane in the open rhabdom of a tipulid fly. Cell Tissue Res 205:423–438.PubMedGoogle Scholar
  82. Yoshizawa T, Shichida Y (1982) Low-temperature spectrophotometry of intermediates of rhodopsin. In: Packer L (ed) Methods in enzymology. Pt H: Visual pigments and purple membranes I, vol 81. Academic Press, New York London, pp 333–353.CrossRefGoogle Scholar
  83. Zuker CS, Cowman AF, Rubin GM (1985) Isolation and structure of a rhodopsin gene from D. melanogaster. Cell 40:851–858.PubMedCrossRefGoogle Scholar
  84. Zuker CS, Montell C, Jones K, Raverty T, Rubin GM (1987) A rhodopsin gene is expressed in photoreceptor cell R7 of the Drosophila eye: homology with other signal transducing molecules. J Neurosci 7:1550–1557.PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1989

Authors and Affiliations

  • Joachim Schwemer
    • 1
  1. 1.BochumGermany

Personalised recommendations