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Biophysics of structure and mechanism

, Volume 9, Issue 4, pp 269–276 | Cite as

Light-mediated cyclic GMP hydrolysis controls important aspects of kinetics of retinal rod voltage response

  • W. H. Miller
  • S. B. Laughlin
Article

Abstract

Pulsatile injections of cyclic GMP into rod outer segments of the isolated toad retina cause transient depolarizations that are reduced in amplitude in proportion with the receptor potential by low Na+ Ringer's. This reduction in the amplitude of the cyclic GMP depolarization may be due to the direct effect of external Na+ concentration on dark current and an indirect effect resulting from the inactivation of a sodium-calcium exchange mechanism raising the intracellular Ca2+ concentration. By comparison the reduction in cyclic GMP response amplitude effected by illumination is accompanied by faster kinetics. This difference suggests that the reduced amplitude and speedier response reflect a light induced increase in phosphodiesterase (PDE) activity rather than the effects of Ca2+. Large doses of cyclic GMP can distort the kinetics of both the light response and the recovery from a depolarization caused by a pulse of cyclic GMP by similarly slowing both types of responses. This similarity in the kinetics of the cyclic GMP response and the initial hyperpolarizing phase of the receptor potential suggests that the kinetics of the initial phase of the receptor potential are controlled by light-mediated cyclic GMP hydrolysis.

Key words

Phototransduction Cyclic GMP Rods Response kinetics 

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References

  1. Bennett N (1982) Light-induced interactions between rhodopsin and the GTP-binding protein, relation with phosphodiesterase action. Eur J Biochem 123: 133–139Google Scholar
  2. Brown JE, Waloga G (1981) Effects of cyclic nucleotides and calcium ions on Bufo rods. Curr Top Membr Transp 15: 369–380Google Scholar
  3. Cavaggioni A, Sorbi RT (1981) Cyclic GMP releases calcium from disc membranes of vertebrate photoreceptors. Proc Natl Acad Sci USA 78: 3964–3968Google Scholar
  4. Fain GL, Lisman JE (1981) Membrane conductances of photoreceptors. Prog Biophys Mol Biol 37: 91–147Google Scholar
  5. Fung BK-K, Stryer L (1980) Photolyzed rhodopsin catalyzes the exchange of GTP for bound GDP in retinal rod outer segments. Proc Natl Acad Sci USA 77: 2500–2504Google Scholar
  6. Gold GH, Korenbrot JI (1981) The regulation of calcium in the intact rod: a study of light-induced calcium release by the outer segment. Curr Top Membr Transp 15: 307–330Google Scholar
  7. Kuhn H, Bennett N, Michel-Villaz M, Chabre M (1981) Interactions between photoexcited rhodopsin and GTP-binding protein: kinetic and stoichiometric analysis from light-scattering changes. Proc Natl Acad Sci USA 78: 6873–6877Google Scholar
  8. Miller WH (1982) Physiological evidence that light mediated decrease in cyclic GMP is an intermediary process in retinal rod transduction. J Gen Physiol 80: 103–123Google Scholar
  9. Miller WH (1983) Physiological effects of cyclic GMP in the vertebrate retinal rod outer segment. In: Greengard P, Robison A (eds) Advances in Cyclic nucleotide research, vol 15, Chap 10 (in press)Google Scholar
  10. Miller WH, Nicol GD (1979) Evidence that cyclic GMP regulates membrane potential in rod photoreceptors. Nature 280: 64–66Google Scholar
  11. Miller WH, Nicol GD (1981) Cyclic GMP induced depolarization and increased response latency of rods: antagonism by light. Curr Top Membr Transp 15: 417–437Google Scholar
  12. Nicol GD, Miller WH (1978) Cyclic GMP injected into retinal rod outer segments increases latency and amplitude of response to illumination. Proc Natl Acad Sci USA 75: 5217–5220Google Scholar
  13. Owen WG, Torre V (1981) Ionic studies of vertebrate rods. Curr Top Membr Transp 15: 33–54Google Scholar
  14. Polans AS, Hermolin J, Bownds MD (1979) Light-induced dephosphorylation of two proteins in frog rod outer segments. J Gen Physiol 74: 595–613Google Scholar
  15. Pugh EN Jr, Mueller P, Liebman PA (1982) Protons: a possible link in visual transduction. Invest Ophthalmol Visual Sci (Suppl) 22: 80Google Scholar
  16. Schnetkamp PPM (1980) Ion selectivity of the cation transport system of isolated intact cattle rod outer segments: evidence for a direct communication between the rod plasma and the rod disk membranes. Biochim Biophys Acta 598: 66–90Google Scholar
  17. Stryer L, Hurley JB, Fung BK-K (1981) First stage of amplification in the cyclic nucleotide cascade of vision. Curr Top Membr Transp 15: 93–107Google Scholar
  18. Woodruff ML, Bownds MD (1979) Amplitude, kinetics and reversibility of a light-induced decrease in 3′,5′-cyclic monophosphate in frog photoreceptor membranes. J Gen Physiol 73: 629–653Google Scholar
  19. Yee R, Liebman PA (1978) Light-activated phosphodiesterase of the rod outer segment: kinetics and parameters of activation and deactivation. J Biol Chem 253: 1802–1809Google Scholar

Copyright information

© Springer-Verlag 1983

Authors and Affiliations

  • W. H. Miller
    • 1
  • S. B. Laughlin
    • 1
  1. 1.Department of Ophthalmology and Visual ScienceYale Medical SchoolNew HavenUSA

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