Skip to main content
PMC home page
The Journal of General Physiology logoLink to The Journal of General Physiology
. 1977 May 1;69(5):667–679. doi: 10.1085/jgp.69.5.667

Guanosine 3',5'-cyclic monophosphate and the in vitro physiology of frog photoreceptor membranes

PMCID: PMC2215081  PMID: 194013

Abstract

Frog rod outer segments freshly detached from dark-adapted retinas contain approximately 1-2 molecules of guanosine 3',5'-cyclic monophosphate (cyclic GMP) for every 100 molecules of visual pigment present. This cyclic GMP decays to 5'-GMP, and the conversion is accelerated upon illumination of the outer segments. Bleaching one rhodopsin molecule can lead to the hydrolysis of 1,000-2,000 molecules of cyclic GMP within 100-300 ms. The decline in cyclic GMP concentration becomes larger as illumination increases, and varies with the logarithm of light intensity at levels which bleach between 5 X 10(2) and 5 X 10(5) rhodopsin molecules per outer segment-second. Light suppression of plasma membrane permeability, assayed in vitro as light suppression of outer segment swelling in a modified Ringer's solution, occurs over this same range of light intensity. The correlation between cyclic GMP and permeability or swelling is maintained in the presence of two pharmacological perturbations: papaverine, a phosphodiesterase inhibitor, increases both cyclic GMP levels and the dark permeability of the plasma membrane; and beta,gamma-methylene ATP increases the effectiveness of light in suppressing both permeability and cyclic GMP levels.

Full Text

The Full Text of this article is available as a PDF (870.3 KB).

Selected References

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

  1. Bensinger R. E., Fletcher R. T., Chader G. J. Guanylate cyclase: inhibition by light in retinal photoreceptors. Science. 1974 Jan 11;183(4120):86–87. doi: 10.1126/science.183.4120.86. [DOI] [PubMed] [Google Scholar]
  2. Bownds D., Brodie A. E. Light-sensitive swelling of isolated frog rod outer segments as an in vitro assay for visual transduction and dark adaptation. J Gen Physiol. 1975 Oct;66(4):407–425. doi: 10.1085/jgp.66.4.407. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. 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]
  4. 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]
  5. Chader G., Fletcher R., Johnson M., Bensinger R. Rod outer segment phosphodiesterase: factors affecting the hydrolysis of cyclic-AMP and cyclic-GMP. Exp Eye Res. 1974 Jun;18(6):509–515. doi: 10.1016/0014-4835(74)90057-8. [DOI] [PubMed] [Google Scholar]
  6. Chader G., Johnson M., Fletcher R., Besinger R. Cyclic nucleotide phosphodiesterase of the bovine retina: activity, subcellular distribution and kinetic parameters. J Neurochem. 1974 Jan;22(1):93–99. doi: 10.1111/j.1471-4159.1974.tb12183.x. [DOI] [PubMed] [Google Scholar]
  7. Fletcher R. T., Chader G. J. Cyclic GMP: control of concentration by light in retinal photoreceptors. Biochem Biophys Res Commun. 1976 Jun 21;70(4):1297–1302. doi: 10.1016/0006-291x(76)91043-3. [DOI] [PubMed] [Google Scholar]
  8. Goldberg N. D., Haddox M. K., Nicol S. E., Glass D. B., Sanford C. H., Kuehl F. A., Jr, Estensen R. Biologic regulation through opposing influences of cyclic GMP and cyclic AMP: the Yin Yang hypothesis. Adv Cyclic Nucleotide Res. 1975;5:307–330. [PubMed] [Google Scholar]
  9. Goldberg N. D., Haddox M. K. Quantitation of cyclic GMP by enzymatic cycling. Methods Enzymol. 1974;38:73–84. doi: 10.1016/0076-6879(74)38013-5. [DOI] [PubMed] [Google Scholar]
  10. Goridis C., Virmaux N., Cailla H. L., Delaage M. A. Rapid, light-induced changes of retinal cyclic GMP levels. FEBS Lett. 1974 Dec 15;49(2):167–169. doi: 10.1016/0014-5793(74)80503-x. [DOI] [PubMed] [Google Scholar]
  11. Hagins W. A. The visual process: Excitatory mechanisms in the primary receptor cells. Annu Rev Biophys Bioeng. 1972;1:131–158. doi: 10.1146/annurev.bb.01.060172.001023. [DOI] [PubMed] [Google Scholar]
  12. Keirns J. J., Miki N., Bitensky M. W., Keirns M. A link between rhodopsin and disc membrane cyclic nucleotide phosphodiesterase. Action spectrum and sensitivity to illumination. Biochemistry. 1975 Jun 17;14(12):2760–2766. doi: 10.1021/bi00683a032. [DOI] [PubMed] [Google Scholar]
  13. Krishna G., Krishnan N., Fletcher R. T., Chader G. Effects of light on cyclic GMP metabolism in retinal photoreceptors. J Neurochem. 1976 Sep;27(3):717–722. doi: 10.1111/j.1471-4159.1976.tb10399.x. [DOI] [PubMed] [Google Scholar]
  14. Kühn H., Cook J. H., Dreyer W. J. Phosphorylation of rhodopsin in bovine photoreceptor membranes. A dark reaction after illumination. Biochemistry. 1973 Jun 19;12(13):2495–2502. doi: 10.1021/bi00737a020. [DOI] [PubMed] [Google Scholar]
  15. Liebman P. A., Entine G. Visual pigments of frog and tadpole (Rana pipiens). Vision Res. 1968 Jul;8(7):761–775. doi: 10.1016/0042-6989(68)90128-4. [DOI] [PubMed] [Google Scholar]
  16. Miki N., Baraban J. M., Keirns J. J., Boyce J. J., Bitensky M. W. Purification and properties of the light-activated cyclic nucleotide phosphodiesterase of rod outer segments. J Biol Chem. 1975 Aug 25;250(16):6320–6327. [PubMed] [Google Scholar]
  17. Miki N., Keirns J. J., Marcus F. R., Freeman J., Bitensky M. W. Regulation of cyclic nucleotide concentrations in photoreceptors: an ATP-dependent stimulation of cyclic nucleotide phosphodiesterase by light. Proc Natl Acad Sci U S A. 1973 Dec;70(12):3820–3824. doi: 10.1073/pnas.70.12.3820. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Miller J. A., Brodie A. E., Bownds M. D. Light-activated rhodopsin phosphorylation may control light sensitivity in isolated rod outer segments. FEBS Lett. 1975 Nov 1;59(1):20–23. doi: 10.1016/0014-5793(75)80331-0. [DOI] [PubMed] [Google Scholar]
  19. Rasmussen H., Jensen P., Lake W., Friedmann N., Goodman D. B. Cyclic nucleotides and cellular calcium metabolism. Adv Cyclic Nucleotide Res. 1975;5:375–394. [PubMed] [Google Scholar]
  20. Steiner A. L., Pagliara A. S., Chase L. R., Kipnis D. M. Radioimmunoassay for cyclic nucleotides. II. Adenosine 3',5'-monophosphate and guanosine 3',5'-monophosphate in mammalian tissues and body fluids. J Biol Chem. 1972 Feb 25;247(4):1114–1120. [PubMed] [Google Scholar]
  21. Virmaux N., Nullans G., Goridis C. Guanylate cyclase in vertebrate retina:evidence for specific association with rod outer segments. J Neurochem. 1976 Jan;26(1):233–235. doi: 10.1111/j.1471-4159.1976.tb04469.x. [DOI] [PubMed] [Google Scholar]
  22. Weinryb I., Michel I. M., Hess S. M. Radioimmunoassay of cyclic AMP without precipitating antibody. Anal Biochem. 1972 Feb;45(2):659–663. doi: 10.1016/0003-2697(72)90229-1. [DOI] [PubMed] [Google Scholar]
  23. 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]
  24. Zimmerman W. F., Daemen F. J., Bonting S. L. Distribution of enzyme activities in subcellular fractions of bovine retina. J Biol Chem. 1976 Aug 10;251(15):4700–4705. [PubMed] [Google Scholar]

Articles from The Journal of General Physiology are provided here courtesy of The Rockefeller University Press

RESOURCES