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. 1983 Apr;80(7):1892–1896. doi: 10.1073/pnas.80.7.1892

Protons block the dark current of isolated retinal rods.

P Mueller, E N Pugh Jr
PMCID: PMC393716  PMID: 6300877

Abstract

Membrane currents of isolated frog rods were recorded with the suction pipette technique and tested by perfusion techniques for their sensitivity to H+. The following facts have been established. (i) Increased [H+] suppresses the Na+ conductance of the outer segment rapidly and reversibly. (ii) H+ acts in the rod interior. (iii) The [H+] necessary to cause a 50% decrement in Na+ conductance is inversely related to the [Ca2+] over 5 orders of magnitude. (iv) The sensitivity to H+ and the sensitivity to light, as a function of [Ca2+], have the same slope. Thus, H+ act like light in effecting membrane current suppression but behave as if their effect is mediated through Ca2+. Based on these results and properties of rod disk membrane phosphodiesterase, we propose that protons produced in the light-activated hydrolysis of cGMP liberate Ca2+ from the disks by ion exchange.

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Selected References

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

  1. Baehr W., Devlin M. J., Applebury M. L. Isolation and characterization of cGMP phosphodiesterase from bovine rod outer segments. J Biol Chem. 1979 Nov 25;254(22):11669–11677. [PubMed] [Google Scholar]
  2. Bastian B. L., Fain G. L. The effects of low calcium and background light on the sensitivity of toad rods. J Physiol. 1982 Sep;330:307–329. doi: 10.1113/jphysiol.1982.sp014343. [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. Boron W. F., De Weer P. Intracellular pH transients in squid giant axons caused by CO2, NH3, and metabolic inhibitors. J Gen Physiol. 1976 Jan;67(1):91–112. doi: 10.1085/jgp.67.1.91. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Brown J. E., Coles J. A., Pinto L. H. Effects of injections of calcium and EGTA into the outer segments of retinal rods of Bufo marinus. J Physiol. 1977 Aug;269(3):707–722. doi: 10.1113/jphysiol.1977.sp011924. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cohen A. I. New evidence supporting the linkage to extracellular space of outer segment saccules of frog cones but not rods. J Cell Biol. 1968 May;37(2):424–444. doi: 10.1083/jcb.37.2.424. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Fleischman D., Denisevich M. Guanylate cyclase of isolated bovine retinal rod axonemes. Biochemistry. 1979 Nov 13;18(23):5060–5066. doi: 10.1021/bi00590a006. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. Gedney C., Ostroy S. E. Hydrogen ion effects of the vertebrate photoreceptor. The pK's of ionizable groups affecting cell permeability. Arch Biochem Biophys. 1978 May;188(1):105–113. doi: 10.1016/0003-9861(78)90362-4. [DOI] [PubMed] [Google Scholar]
  10. Gold G. H., Korenbrot J. I. Light-induced calcium release by intact retinal rods. Proc Natl Acad Sci U S A. 1980 Sep;77(9):5557–5561. doi: 10.1073/pnas.77.9.5557. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Govardovskii V. I., Berman A. L. Light-induced changes of cyclic GMP content in frog retinal rod outer segments measured with rapid freezing and microdissection. Biophys Struct Mech. 1981;7(3):125–130. doi: 10.1007/BF00539174. [DOI] [PubMed] [Google Scholar]
  12. Hagins W. A., Robinson W. E., Yoshikami S. Ionic aspects of excitation in rod outer segments. Ciba Found Symp. 1975;(31):169–189. doi: 10.1002/9780470720134.ch10. [DOI] [PubMed] [Google Scholar]
  13. Hagins W. A., Yoshikami S. Proceedings: A role for Ca2+ in excitation of retinal rods and cones. Exp Eye Res. 1974 Mar;18(3):299–305. doi: 10.1016/0014-4835(74)90157-2. [DOI] [PubMed] [Google Scholar]
  14. Kaupp U. B., Schnetkamp P. P., Junge W. Rapid calcium release and proton uptake at the disk membrane of isolated cattle rod outer segments. 1. Stoichiometry of light-stimulated calcium release and proton uptake. Biochemistry. 1981 Sep 15;20(19):5500–5510. doi: 10.1021/bi00522a024. [DOI] [PubMed] [Google Scholar]
  15. Kilbride P., Ebrey T. G. Light-initiated changes of cyclic guanosine monophosphate levels in the frog retina measured with quick-freezing techniques. J Gen Physiol. 1979 Sep;74(3):415–426. doi: 10.1085/jgp.74.3.415. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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]
  17. 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]
  18. Liebman P. A., Pugh E. N., Jr The control of phosphodiesterase in rod disk membranes: kinetics, possible mechanisms and significance for vision. Vision Res. 1979;19(4):375–380. doi: 10.1016/0042-6989(79)90097-x. [DOI] [PubMed] [Google Scholar]
  19. Miller W. H. Physiological evidence that light-mediated decrease in cyclic GMP is an intermediary process in retinal rod transduction. J Gen Physiol. 1982 Jul;80(1):103–123. doi: 10.1085/jgp.80.1.103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Nicol G. D., Miller W. H. Cyclic GMP injected into retinal rod outer segments increases latency and amplitude of response to illumination. Proc Natl Acad Sci U S A. 1978 Oct;75(10):5217–5220. doi: 10.1073/pnas.75.10.5217. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Pannbacker R. G. Control of guanylate cyclase activity in the rod outer segment. Science. 1973 Dec 14;182(4117):1138–1140. doi: 10.1126/science.182.4117.1138. [DOI] [PubMed] [Google Scholar]
  22. Racker E., Miyamoto H., Mogerman J., Simons J., O'Neal S. Cation transport in reconstituted systems. Ann N Y Acad Sci. 1980;358:64–72. doi: 10.1111/j.1749-6632.1980.tb15386.x. [DOI] [PubMed] [Google Scholar]
  23. 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]
  24. Schnetkamp P. P. Calcium translocation and storage of isolated intact cattle rod outer segments in darkness. Biochim Biophys Acta. 1979 Jul 5;554(2):441–459. doi: 10.1016/0005-2736(79)90383-3. [DOI] [PubMed] [Google Scholar]
  25. Schnetkamp P. P. Ion selectivity of the cation transport system of isolated intact cattle rod outer segments: evidence for a direct communication between the rod plasma membrane and the rod disk membranes. Biochim Biophys Acta. 1980 May 8;598(1):66–90. doi: 10.1016/0005-2736(80)90266-7. [DOI] [PubMed] [Google Scholar]
  26. Szuts E. Z., Cone R. A. Calcium content of frog rod outer segments and discs. Biochim Biophys Acta. 1977 Jul 14;468(2):194–208. doi: 10.1016/0005-2736(77)90114-6. [DOI] [PubMed] [Google Scholar]
  27. 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]
  28. Wormington C. M., Cone R. A. Ionic blockage of the light-regulated sodium channels in isolated rod outer segments. J Gen Physiol. 1978 Jun;71(6):657–681. doi: 10.1085/jgp.71.6.657. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Yau K. W., Lamb T. D., Baylor D. A. Light-induced fluctuations in membrane current of single toad rod outer segments. Nature. 1977 Sep 1;269(5623):78–80. doi: 10.1038/269078a0. [DOI] [PubMed] [Google Scholar]
  30. Yau K. W., McNaughton P. A., Hodgkin A. L. Effect of ions on the light-sensitive current in retinal rods. Nature. 1981 Aug 6;292(5823):502–505. doi: 10.1038/292502a0. [DOI] [PubMed] [Google Scholar]
  31. Yee R., Liebman P. A. Light-activated phosphodiesterase of the rod outer segment. Kinetics and parameters of activation and deactivation. J Biol Chem. 1978 Dec 25;253(24):8902–8909. [PubMed] [Google Scholar]
  32. Yoshikami S., George J. S., Hagins W. A. Light-induced calcium fluxes from outer segment layer of vertebrate retinas. Nature. 1980 Jul 24;286(5771):395–398. doi: 10.1038/286395a0. [DOI] [PubMed] [Google Scholar]
  33. 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]

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