The Amplifying Transduction Cascade Triggered by Rhodopsin in Visual Receptor Cells Biochemical and Biophysical Approaches

  • Marc Charbre
  • T. Minh Vuong
Part of the NATO ASI Series book series (NSSA, volume 133)


After a long rivalry with Hagins’ “calcium hypothesis” cyclic GMP is now solidly established as the cytoplasmic transmitter of the visual excitation process in the vertebrate photoreceptor1,2: in these cells cGMP directly controls the conductance of the Na+ channels in the plasma membrane; in this respect, the visual transduction process differs from the usual pathway of cyclic nucleoside dependent kinase activation, found in the transduction process of many hormonal or neuronal signals. In many other respects the light sensitive and the hormone sensitive systems present striking similarities. The Rhodopsin-Transducin-cGMP phosphodiesterase cascade parallels exactly that of hormone receptor-G protein-AMPcyclase. It became clear a few years ago that transducin, the GTP binding protein of the visual system, is a member of the growing family of G proteins responsible for the coupling of hormonal or neuronal membrane receptors to their various intracellular effectors: AMP cyclase, phosphodiesterase or phospholipase specific for phosphatidylinositol hydrolysis. This analogy between the transducin cascade and the other G protein mediated processes had led a few years ago to the suggestion that rhodopsin might be considered as a special type of hormone receptor3.


Light Flash Release Signal Inhibitory Subunit Forward Detector cGMP Phosphodiesterase 
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  1. 1.
    M. Chabre. Trigger and amplification mechanisms in visual phototransduction, Ann. Rev. Biophys. Biophys.Chem. 14, 331–360 (1985).CrossRefGoogle Scholar
  2. 2.
    L. Stryer. Cyclic GMP cascade of vision, Ann. Rev. Neurosci. 9, 87–119 (1986).PubMedCrossRefGoogle Scholar
  3. 3.
    M. Chabre, C. Pfister, P. Deterre and H. Kühn. The mechanism of control of cGMP phosphodiesterase by photoexcited rhodopsin. Analogies with hormone controlled systems. In “Hormone and Cell regulation”. Vol. 8, p. 87–98. J. Dumont and J. Nunez ed. Elsevier (1984).Google Scholar
  4. 4.
    R.A. Dixon et al. Cloning of the gene and cDNA for mammalian β adrenergic receptor and homology with rhodopsin. Nature 321, 75–79 (1986).PubMedCrossRefGoogle Scholar
  5. 5.
    Tikubo et al. Cloning, sequencing and expression of complementary DNA encoding the muscarinic acetylcholine receptor. Nature 323, 411–416 (1986).CrossRefGoogle Scholar
  6. 6.
    J.L. Benovic, R.A. Strasser, M.G. Caron and R. Lefkowitz. 0 adrenergic receptor kinase: identification of a novel protein kinase that phosphorylates the agonist occupied form of the receptor. Proc. Natl. Acad. Sc. US 83, 2797–2801 (1986).CrossRefGoogle Scholar
  7. 7.
    E.A. Dratz and P.A. Hargrave. The structure of rhodopsin and the rod outer segment disk membrane. TIBS 8, 128–131 (1983).Google Scholar
  8. 8.
    H. Kühn. Interactions between photoexcited rhodopsin and light-activated enzymes in rods. In “Progress in Retinal Research”, eds. N. Osborne and J. Chader, vol. 3, pp. 123–156. Oxford: Pergamon Press (1984).Google Scholar
  9. 9.
    C. Pfister, M. Chabre, J. Plouet, V.V. Tuyen, Y. De Kozak, J.P. Faure and H. Kühn. Retinal S antigen identified as the 48K protein regulating light dependent phosphodiesterase in rods. Science, 228, 891–893 (1985).PubMedCrossRefGoogle Scholar
  10. 10.
    B. Honig, T. Ebrey, R.H. Callender, U. Dinur and M. Ottolenghi. Photoisomerisation, energy storage, and charge separation. A model for light energy transduction in visual pigment and bacteriorhodopsin. Proc. Natl. Acad. Sci., USA, 76, 2503–7 (1979).PubMedCrossRefGoogle Scholar
  11. 11.
    A. Cooper. “Energy uptake in the first step of visual excitation”. Nature, London, 282, 531–3 (1979).CrossRefGoogle Scholar
  12. 12.
    M. Chabre. Conformational and functional change induced in vertebrate rhodopsin by photon capture. In “The Biology of photoreception” eds D.J. Cosens and D. Vince Prue. S.E.B. Symposia XXXVI. Cambridge University Press (1983).Google Scholar
  13. 13.
    N. Bennett, M. Miche1-Villaz, H. Kühn. Light-induced interaction between rhodopsin and the GTP-binding protein. Metarhodopsin II is the major photoproduct involved. Eur. J. Biochem. 127, 97–103 (1982).PubMedCrossRefGoogle Scholar
  14. 14.
    D. Emeis, H. Kühn, J. Reichert and K.P. Hofmann. Complex formation between metarhodopsin II and GTP-binding protein in bovine photoreceptor membranes leads to a shift of the photoproduct equilibrium. FEBS Lett. 143, 29–34 (1982).PubMedCrossRefGoogle Scholar
  15. 15.
    H. Kühn. Light- and GTP-regulated interaction of GTPase and other proteins with bovine photoreceptor membranes. Nature 283, 587–589 (1981).CrossRefGoogle Scholar
  16. 16.
    U.A. Wilden and H. Kühn. Light-dependent phosphorylation of rhodopsin: number of phosphorylation sites. Biochemistry 21, 3014–3022 (1982).PubMedCrossRefGoogle Scholar
  17. 17.
    N. Bennett and Y. Dupont. The G protein of retinal rod outer segments (Transducin): Mechanism of interaction with rhodopsin and nucleotides. J. Biol. Chem. 260, 4156–4168 (1985).PubMedGoogle Scholar
  18. 18.
    B.K.K. Fung and L. Stryer. Photolyzed rhodopsin catalyses the exchange of GTP for bound GDP in retinal rod outer segments. Proc. Natl. Acad. Sci. USA 77, 2500–2504 (1980).CrossRefGoogle Scholar
  19. 19.
    P.A. Liebman and E.N. Pugh. ATP mediates rapid reversal of cyclic GMP phosphodiesterase activation in visual receptor membranes. Nature 287, 734–736 (1980).PubMedCrossRefGoogle Scholar
  20. 20.
    U. Wilden, S.W. Hall, H. Kühn. Phosphodiesterase activation by photoexcited rhodopsin is quenched when rhodopsin is phosphorylated and binds the 48KD protein of rod outer segments. Proc. Acad. Sc. USA, 83, 1174–1178 (1986).CrossRefGoogle Scholar
  21. 21.
    C. Pfister, M. Chabre, J. Plouet, V. Tuyen, Y. De Kozak, J.P. Faure and H. Kühn. Retinal S antigen identified as the 48K protein regulating light dependent phosphodiesterase in rods. Science 228, 891–893 (1985).PubMedCrossRefGoogle Scholar
  22. 22.
    P. Deterre, J. Bigay, M. Robert, C. Pfister, H. Kühn and M. Chabre. Activation of retinal rod cyclic GMP phosphodiesterase by Transducin. Characterization of the complex formed by phosphodiesterase inhibitor and transducin. Proteins Struct. Funct. Gen. 1, n° 2 (1986).Google Scholar
  23. 23.
    A.G. Gilman. “G proteins and dual control of adenylate cyclase”. Cell 36, 577–579 (1984).PubMedCrossRefGoogle Scholar
  24. 24.
    H. Kühn, N. Bennett, M. Michel-Villaz and M. Chabre. Interactions between photoexcited rhodopsin and GTP-binding protein: kinetic and stoichiometric analysis from light-scattering changes. Proc. Natl. Acad. Sci. USA 18, 6873–6877 (1981).CrossRefGoogle Scholar
  25. 25.
    T.M. Vuong, M. Chabre and L. Stryer. Millisecond activation of transducin in the cyclic nucleotide cascade of vision. Nature 311, 659–661 (1984).PubMedCrossRefGoogle Scholar
  26. 26.
    H. Saibil, M. Chabre and D.L. Worcester. Neutron diffraction studies of retinal rod outer segments membranes. Nature 262, 266–270 (1976).PubMedCrossRefGoogle Scholar

Copyright information

© Plenum Press, New York 1987

Authors and Affiliations

  • Marc Charbre
    • 1
  • T. Minh Vuong
    • 1
  1. 1.Laboratoire de Biophysique Moléculaire and Cellulaire, (UA CNRS 520)DRF-CENGGrenobleFrance

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