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. 1985 Jan 1;85(1):107–121. doi: 10.1085/jgp.85.1.107

Light-induced changes in GTP and ATP in frog rod photoreceptors. Comparison with recovery of dark current and light sensitivity during dark adaptation

PMCID: PMC2215811  PMID: 3968531

Abstract

Light decreases GTP and ATP levels in purified suspensions of physiologically active frog rod outer segments still attached to their inner segment ellipsoids (OS-IS). (a) The GTP decrease is slower in OS- IS (t1/2 = 40 s) than in isolated outer segments (t1/2 = 7 s), which suggests there is more effective buffering in OS-IS. (b) The GTP decrease becomes detectable only at intensities greater than those required to saturate the photoresponse. As the intensity of a continuous light is increased over 4 log units, GTP levels decrease linearly with log intensity by as much as 60%. GTP is reduced to steady intermediate levels during extended illumination of intermediate intensity. (c) At levels of illumination bleaching greater than 0.003% of the rhodopsin, a decrease in ATP levels becomes detectable. (d) Following a flash, GTP levels fall and then rise with a recovery time dependent on the intensity of the flash. (e) After both 0.2 and 2% flash bleaches, the recovery of GTP levels parallels the recovery of light sensitivity, which is slower than the recovery of the dark current. This raises the possibility of a link between GTP levels and light sensitivity.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bader C. R., Macleish P. R., Schwartz E. A. A voltage-clamp study of the light response in solitary rods of the tiger salamander. J Physiol. 1979 Nov;296:1–26. doi: 10.1113/jphysiol.1979.sp012988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Baylor D. A., Lamb T. D. Local effects of bleaching in retinal rods of the toad. J Physiol. 1982 Jul;328:49–71. doi: 10.1113/jphysiol.1982.sp014252. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Baylor D. A., Lamb T. D., Yau K. W. The membrane current of single rod outer segments. J Physiol. 1979 Mar;288:589–611. [PMC free article] [PubMed] [Google Scholar]
  4. Berger S. J., DeVries G. W., Carter J. G., Schulz D. W., Passonneau P. N., Lowry O. H., Ferrendelli J. A. The distribution of the components of the cyclic GMP cycle in retina. J Biol Chem. 1980 Apr 10;255(7):3128–3133. [PubMed] [Google Scholar]
  5. Biernbaum M. S., Bownds M. D. Frog rod outer segments with attached inner segment ellipsoids as an in vitro model for photoreceptors on the retina. J Gen Physiol. 1985 Jan;85(1):83–105. doi: 10.1085/jgp.85.1.83. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Biernbaum M. S., Bownds M. D. Influence of light and calcium on guanosine 5'-triphosphate in isolated frog rod outer segments. J Gen Physiol. 1979 Dec;74(6):649–669. doi: 10.1085/jgp.74.6.649. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bownds D., Dawes J., Miller J., Stahlman M. Phosphorylation of frog photoreceptor membranes induced by light. Nat New Biol. 1972 May 24;237(73):125–127. doi: 10.1038/newbio237125a0. [DOI] [PubMed] [Google Scholar]
  8. Bownds D., Gordon-Walker A., Gaide-Huguenin A. C., Robinson W. Characterization and analysis of frog photoreceptor membranes. J Gen Physiol. 1971 Sep;58(3):225–237. doi: 10.1085/jgp.58.3.225. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Bownds M. D. Biochemical steps in visual transduction: roles for nucleotides and calcium ions. Photochem Photobiol. 1980 Oct;32(4):487–490. doi: 10.1111/j.1751-1097.1980.tb03792.x. [DOI] [PubMed] [Google Scholar]
  10. Brodie A. E., Bownds D. Biochemical correlates of adaptation processes in isolated frog photoreceptor membranes. J Gen Physiol. 1976 Jul;68(1):1–11. doi: 10.1085/jgp.68.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Conner J. D. The relation between excitation and adaptation within the rod's outer segment. Neurosci Lett. 1982 Jun 30;30(3):245–250. doi: 10.1016/0304-3940(82)90407-4. [DOI] [PubMed] [Google Scholar]
  12. Cote R. H., Biernbaum M. S., Nicol G. D., Bownds M. D. Light-induced decreases in cGMP concentration precede changes in membrane permeability in frog rod photoreceptors. J Biol Chem. 1984 Aug 10;259(15):9635–9641. [PubMed] [Google Scholar]
  13. Dontsov A. E., Zak P. P., Ostrovskii M. A. Regeneratsiia ATP v naruzhnykh segmentakh fotoretseptorov liagushki. Biokhimiia. 1978;43(4):592–596. [PubMed] [Google Scholar]
  14. Fain G. L. Sensitivity of toad rods: Dependence on wave-length and background illumination. J Physiol. 1976 Sep;261(1):71–101. doi: 10.1113/jphysiol.1976.sp011549. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Fleischman D., Denisevich M., Raveed D., Pannbacker R. G. Association of guanylate cyclase with the axoneme of retinal rods. Biochim Biophys Acta. 1980 Jun 19;630(2):176–186. doi: 10.1016/0304-4165(80)90419-5. [DOI] [PubMed] [Google Scholar]
  16. Fung B. K. Characterization of transducin from bovine retinal rod outer segments. I. Separation and reconstitution of the subunits. J Biol Chem. 1983 Sep 10;258(17):10495–10502. [PubMed] [Google Scholar]
  17. Fung B. K., Hurley J. B., Stryer L. Flow of information in the light-triggered cyclic nucleotide cascade of vision. Proc Natl Acad Sci U S A. 1981 Jan;78(1):152–156. doi: 10.1073/pnas.78.1.152. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Goldberg N. D., Ames A. A., 3rd, Gander J. E., Walseth T. F. Magnitude of increase in retinal cGMP metabolic flux determined by 18O incorporation into nucleotide alpha-phosphoryls corresponds with intensity of photic stimulation. J Biol Chem. 1983 Aug 10;258(15):9213–9219. [PubMed] [Google Scholar]
  19. Hermolin J., Karell M. A., Hamm H. E., Bownds M. D. Calcium and cyclic GMP regulation of light-sensitive protein phosphorylation in frog photoreceptor membranes. J Gen Physiol. 1982 Apr;79(4):633–655. doi: 10.1085/jgp.79.4.633. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Hurley J. B., Stryer L. Purification and characterization of the gamma regulatory subunit of the cyclic GMP phosphodiesterase from retinal rod outer segments. J Biol Chem. 1982 Sep 25;257(18):11094–11099. [PubMed] [Google Scholar]
  21. Kawamura S., Bownds M. D. Light adaption of the cyclic GMP phosphodiesterase of frog photoreceptor membranes mediated by ATP and calcium ions. J Gen Physiol. 1981 May;77(5):571–591. doi: 10.1085/jgp.77.5.571. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Kimble E. A., Svoboda R. A., Ostroy S. E. Oxygen consumption and ATP changes of the vertebrate photoreceptor. Exp Eye Res. 1980 Sep;31(3):271–288. doi: 10.1016/s0014-4835(80)80037-6. [DOI] [PubMed] [Google Scholar]
  23. Kleinschmidt J., Dowling J. E. Intracellular recordings from gecko photoreceptors during light and dark adaptation. J Gen Physiol. 1975 Nov;66(5):617–648. doi: 10.1085/jgp.66.5.617. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Kwok-Keung Fung B., Stryer L. Photolyzed rhodopsin catalyzes the exchange of GTP for bound GDP in retinal rod outer segments. Proc Natl Acad Sci U S A. 1980 May;77(5):2500–2504. doi: 10.1073/pnas.77.5.2500. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Kühn H., Bennett N., Michel-Villaz M., Chabre M. Interactions between photoexcited rhodopsin and GTP-binding protein: kinetic and stoichiometric analyses from light-scattering changes. Proc Natl Acad Sci U S A. 1981 Nov;78(11):6873–6877. doi: 10.1073/pnas.78.11.6873. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Kühn H., Dreyer W. J. Light dependent phosphorylation of rhodopsin by ATP. FEBS Lett. 1972 Jan 15;20(1):1–6. doi: 10.1016/0014-5793(72)80002-4. [DOI] [PubMed] [Google Scholar]
  27. Kühn H. Light- and GTP-regulated interaction of GTPase and other proteins with bovine photoreceptor membranes. Nature. 1980 Feb 7;283(5747):587–589. doi: 10.1038/283587a0. [DOI] [PubMed] [Google Scholar]
  28. Lamb T. D., McNaughton P. A., Yau K. W. Spatial spread of activation and background desensitization in toad rod outer segments. J Physiol. 1981;319:463–496. doi: 10.1113/jphysiol.1981.sp013921. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Liebman P. A., Mueller P., Pugh E. N., Jr Protons suppress the dark current of frog retinal rods. J Physiol. 1984 Feb;347:85–110. doi: 10.1113/jphysiol.1984.sp015055. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Liebman P. A., Pugh E. N., Jr ATP mediates rapid reversal of cyclic GMP phosphodiesterase activation in visual receptor membranes. Nature. 1980 Oct 23;287(5784):734–736. doi: 10.1038/287734a0. [DOI] [PubMed] [Google Scholar]
  31. Pober J. S., Bitensky M. W. Light-regulated enzymes of vertebrate retinal rods. Adv Cyclic Nucleotide Res. 1979;11:265–301. [PubMed] [Google Scholar]
  32. Polans A. S., Hermolin J., Bownds M. D. Light-induced dephosphorylation of two proteins in frog rod outer segments: influence of cyclic nucleotides and calcium. J Gen Physiol. 1979 Nov;74(5):595–613. doi: 10.1085/jgp.74.5.595. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Polans A. S., Kawamura S., Bownds M. D. Influence of calcium on guanosine 3',5'-cyclic monophosphate levels in frog rod outer segments. J Gen Physiol. 1981 Jan;77(1):41–48. doi: 10.1085/jgp.77.1.41. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Robinson P. R., Kawamura S., Abramson B., Bownds M. D. Control of the cyclic GMP phosphodiesterase of frog photoreceptor membranes. J Gen Physiol. 1980 Nov;76(5):631–645. doi: 10.1085/jgp.76.5.631. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Robinson W. E., Hagins W. A. GTP hydrolysis in intact rod outer segments and the transmitter cycle in visual excitation. Nature. 1979 Aug 2;280(5721):398–400. doi: 10.1038/280398a0. [DOI] [PubMed] [Google Scholar]
  36. Schnetkamp P. P., Daemen F. J. Transfer of high-energy phosphate in bovine rod outer segments. A nucleotide buffer system. Biochim Biophys Acta. 1981 Feb 5;672(3):307–312. doi: 10.1016/0304-4165(81)90298-1. [DOI] [PubMed] [Google Scholar]
  37. Sitaramayya A., Liebman P. A. Phosphorylation of rhodopsin and quenching of cyclic GMP phosphodiesterase activation by ATP at weak bleaches. J Biol Chem. 1983 Oct 25;258(20):12106–12109. [PubMed] [Google Scholar]
  38. Toyoda J., Hashimoto H., Anno H., Tomita T. The rod response in the frog and studies by intracellular recording. Vision Res. 1970 Nov;10(11):1093–1100. doi: 10.1016/0042-6989(70)90026-x. [DOI] [PubMed] [Google Scholar]
  39. Woodruff M. L., Bownds D., Green S. H., Morrisey J. L., Shedlovsky A. Guanosine 3',5'-cyclic monophosphate and the in vitro physiology of frog photoreceptor membranes. J Gen Physiol. 1977 May;69(5):667–679. doi: 10.1085/jgp.69.5.667. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Woodruff M. L., Bownds M. D. Amplitude, kinetics, and reversibility of a light-induced decrease in guanosine 3',5'-cyclic monophosphate in frog photoreceptor membranes. J Gen Physiol. 1979 May;73(5):629–653. doi: 10.1085/jgp.73.5.629. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Yamazaki A., Stein P. J., Chernoff N., Bitensky M. W. Activation mechanism of rod outer segment cyclic GMP phosphodiesterase. Release of inhibitor by the GTP/GTP-binding protein. J Biol Chem. 1983 Jul 10;258(13):8188–8194. [PubMed] [Google Scholar]
  42. Yoshikami S., Robinson W. E., Hagins W. A. Topology of the outer segment membranes of retinal rods and cones revealed by a fluorescent probe. Science. 1974 Sep 27;185(4157):1176–1179. doi: 10.1126/science.185.4157.1176. [DOI] [PubMed] [Google Scholar]
  43. Zuckerman R., Schmidt G. J., Dacko S. M. Rhodopsin-to-metarhodopsin II transition triggers amplified changes in cytosol ATP and ADP in intact retinal rod outer segments. Proc Natl Acad Sci U S A. 1982 Nov;79(21):6414–6418. doi: 10.1073/pnas.79.21.6414. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. de Azeredo F. A., Lust W. D., Passonneau J. V. Light-induced changes in energy metabolites, guanine nucleotides, and guanylate cyclase within frog retinal layers. J Biol Chem. 1981 Mar 25;256(6):2731–2735. [PubMed] [Google Scholar]

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