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. 1995 Jun 15;485(Pt 3):699–714. doi: 10.1113/jphysiol.1995.sp020763

Spontaneous, ligand-independent activity of the cGMP-gated ion channels in cone photoreceptors of fish.

A Picones 1, J I Korenbrot 1
PMCID: PMC1158038  PMID: 7562611

Abstract

1. We studied the electrical conductance of membrane patches detached from the outer segment of single cone photoreceptors isolated from striped bass retina. 2. Only a single class of ion channels exists in the plasma membrane of the cone outer segments; they are gated by cytoplasmic cGMP and select cations over anions, but distinguish poorly among cations. In the absence of added cGMP and of divalent cations, however, membrane patches detached from the outer segments exhibit a small conductance that ideally selects cations over anions, but distinguishes poorly between Na+ and Li+. 3. The cGMP-independent conductance does not arise from the effect of residual cGMP that may remain associated with the detached membrane, because treatment of the patch with cGMP-specific phosphodiesterase does not affect this conductance. 4. The cGMP-independent conductance is pharmacologically indistinguishable from that activated by cGMP. Ca2+ and L-cis-diltiazem block both conductances at comparable concentrations and with similar quantitative characteristics. 5. We analysed the noise of Ca(2+)- or L-cis-diltiazem-dependent macroscopic currents both in the presence and in the absence of cGMP. In the presence of cGMP, the power density spectrum of the noise is well fitted by the sum of two Lorentzian components. The same function with similar corner frequencies fits the noise of the cGMP-independent currents. However, the total power in the current fluctuations is smaller in the absence of cGMP than in its presence; also, the ratio of the zero frequency asymptotes of the low over the high frequency components, S1(0)/Sh(0), is larger in the absence of cGMP than in its presence.(ABSTRACT TRUNCATED AT 250 WORDS)

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Selected References

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  1. 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]
  2. Bodoia R. D., Detwiler P. B. Patch-clamp recordings of the light-sensitive dark noise in retinal rods from the lizard and frog. J Physiol. 1985 Oct;367:183–216. doi: 10.1113/jphysiol.1985.sp015820. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Colamartino G., Menini A., Torre V. Blockage and permeation of divalent cations through the cyclic GMP-activated channel from tiger salamander retinal rods. J Physiol. 1991;440:189–206. doi: 10.1113/jphysiol.1991.sp018703. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Ertel E. A. Excised patches of plasma membrane from vertebrate rod outer segments retain a functional phototransduction enzymatic cascade. Proc Natl Acad Sci U S A. 1990 Jun;87(11):4226–4230. doi: 10.1073/pnas.87.11.4226. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Ferrer-Montiel A. V., Montal M. S., Díaz-Muñoz M., Montal M. Agonist-independent activation of acetylcholine receptor channels by protein kinase A phosphorylation. Proc Natl Acad Sci U S A. 1991 Nov 15;88(22):10213–10217. doi: 10.1073/pnas.88.22.10213. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Fesenko E. E., Kolesnikov S. S., Lyubarsky A. L. Induction by cyclic GMP of cationic conductance in plasma membrane of retinal rod outer segment. Nature. 1985 Jan 24;313(6000):310–313. doi: 10.1038/313310a0. [DOI] [PubMed] [Google Scholar]
  7. Gordon S. E., Brautigan D. L., Zimmerman A. L. Protein phosphatases modulate the apparent agonist affinity of the light-regulated ion channel in retinal rods. Neuron. 1992 Oct;9(4):739–748. doi: 10.1016/0896-6273(92)90036-d. [DOI] [PubMed] [Google Scholar]
  8. Gray P., Attwell D. Kinetics of light-sensitive channels in vertebrate photoreceptors. Proc R Soc Lond B Biol Sci. 1985 Jan 22;223(1232):379–388. doi: 10.1098/rspb.1985.0007. [DOI] [PubMed] [Google Scholar]
  9. Haynes L. W. Block of the cyclic GMP-gated channel of vertebrate rod and cone photoreceptors by l-cis-diltiazem. J Gen Physiol. 1992 Nov;100(5):783–801. doi: 10.1085/jgp.100.5.783. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Haynes L. W., Kay A. R., Yau K. W. Single cyclic GMP-activated channel activity in excised patches of rod outer segment membrane. Nature. 1986 May 1;321(6065):66–70. doi: 10.1038/321066a0. [DOI] [PubMed] [Google Scholar]
  11. Haynes L. W., Yau K. W. Single-channel measurement from the cyclic GMP-activated conductance of catfish retinal cones. J Physiol. 1990 Oct;429:451–481. doi: 10.1113/jphysiol.1990.sp018267. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Haynes L., Yau K. W. Cyclic GMP-sensitive conductance in outer segment membrane of catfish cones. Nature. 1985 Sep 5;317(6032):61–64. doi: 10.1038/317061a0. [DOI] [PubMed] [Google Scholar]
  13. Hsu Y. T., Molday R. S. Modulation of the cGMP-gated channel of rod photoreceptor cells by calmodulin. Nature. 1993 Jan 7;361(6407):76–79. doi: 10.1038/361076a0. [DOI] [PubMed] [Google Scholar]
  14. Ildefonse M., Bennett N. Single-channel study of the cGMP-dependent conductance of retinal rods from incorporation of native vesicles into planar lipid bilayers. J Membr Biol. 1991 Aug;123(2):133–147. doi: 10.1007/BF01998084. [DOI] [PubMed] [Google Scholar]
  15. Jackson M. B. Kinetics of unliganded acetylcholine receptor channel gating. Biophys J. 1986 Mar;49(3):663–672. doi: 10.1016/S0006-3495(86)83693-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Jackson M. B. Spontaneous openings of the acetylcholine receptor channel. Proc Natl Acad Sci U S A. 1984 Jun;81(12):3901–3904. doi: 10.1073/pnas.81.12.3901. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Karpen J. W., Zimmerman A. L., Stryer L., Baylor D. A. Gating kinetics of the cyclic-GMP-activated channel of retinal rods: flash photolysis and voltage-jump studies. Proc Natl Acad Sci U S A. 1988 Feb;85(4):1287–1291. doi: 10.1073/pnas.85.4.1287. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kaupp U. B., Niidome T., Tanabe T., Terada S., Bönigk W., Stühmer W., Cook N. J., Kangawa K., Matsuo H., Hirose T. Primary structure and functional expression from complementary DNA of the rod photoreceptor cyclic GMP-gated channel. Nature. 1989 Dec 14;342(6251):762–766. doi: 10.1038/342762a0. [DOI] [PubMed] [Google Scholar]
  19. Kaupp U. B. The cyclic nucleotide-gated channels of vertebrate photoreceptors and olfactory epithelium. Trends Neurosci. 1991 Apr;14(4):150–157. doi: 10.1016/0166-2236(91)90087-b. [DOI] [PubMed] [Google Scholar]
  20. Matthews G. Comparison of the light-sensitive and cyclic GMP-sensitive conductances of the rod photoreceptor: noise characteristics. J Neurosci. 1986 Sep;6(9):2521–2526. doi: 10.1523/JNEUROSCI.06-09-02521.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Matthews G., Watanabe S. Activation of single ion channels from toad retinal rod inner segments by cyclic GMP: concentration dependence. J Physiol. 1988 Sep;403:389–405. doi: 10.1113/jphysiol.1988.sp017255. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Miller J. L., Hubbard C. M., Litman B. J., Macdonald T. L. Inhibition of transducin activation and guanosine triphosphatase activity by aluminum ion. J Biol Chem. 1989 Jan 5;264(1):243–250. [PubMed] [Google Scholar]
  23. Miller J. L., Korenbrot J. I. In retinal cones, membrane depolarization in darkness activates the cGMP-dependent conductance. A model of Ca homeostasis and the regulation of guanylate cyclase. J Gen Physiol. 1993 Jun;101(6):933–960. doi: 10.1085/jgp.101.6.933. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Miller J. L., Korenbrot J. I. Phototransduction and adaptation in rods, single cones, and twin cones of the striped bass retina: a comparative study. Vis Neurosci. 1993 Jul-Aug;10(4):653–667. doi: 10.1017/s0952523800005356. [DOI] [PubMed] [Google Scholar]
  25. Miller J. L., Picones A., Korenbrot J. I. Differences in transduction between rod and cone photoreceptors: an exploration of the role of calcium homeostasis. Curr Opin Neurobiol. 1994 Aug;4(4):488–495. doi: 10.1016/0959-4388(94)90048-5. [DOI] [PubMed] [Google Scholar]
  26. Nizzari M., Sesti F., Giraudo M. T., Virginio C., Cattaneo A., Torre V. Single-channel properties of cloned cGMP-activated channels from retinal rods. Proc Biol Sci. 1993 Oct 22;254(1339):69–74. doi: 10.1098/rspb.1993.0128. [DOI] [PubMed] [Google Scholar]
  27. Perry R. J., McNaughton P. A. Response properties of cones from the retina of the tiger salamander. J Physiol. 1991 Feb;433:561–587. doi: 10.1113/jphysiol.1991.sp018444. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Picones A., Korenbrot J. I. Analysis of fluctuations in the cGMP-dependent currents of cone photoreceptor outer segments. Biophys J. 1994 Feb;66(2 Pt 1):360–365. doi: 10.1016/s0006-3495(94)80785-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Picones A., Korenbrot J. I. Permeation and interaction of monovalent cations with the cGMP-gated channel of cone photoreceptors. J Gen Physiol. 1992 Oct;100(4):647–673. doi: 10.1085/jgp.100.4.647. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Quandt F. N., Nicol G. D., Schnetkamp P. P. Voltage-dependent gating and block of the cyclic-GMP-dependent current in bovine rod outer segments. Neuroscience. 1991;42(3):629–638. doi: 10.1016/0306-4522(91)90032-j. [DOI] [PubMed] [Google Scholar]
  31. Schnetkamp P. P., Szerencsei R. T. Silver ions induce a rapid Ca2+ release from isolated intact bovine rod outer segments by a cooperative mechanism. J Membr Biol. 1989 Apr;108(1):91–102. doi: 10.1007/BF01870428. [DOI] [PubMed] [Google Scholar]
  32. Sesti F., Straforini M., Lamb T. D., Torre V. Gating, selectivity and blockage of single channels activated by cyclic GMP in retinal rods of the tiger salamander. J Physiol. 1994 Jan 15;474(2):203–222. doi: 10.1113/jphysiol.1994.sp020014. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Stern J. H., Kaupp U. B., MacLeish P. R. Control of the light-regulated current in rod photoreceptors by cyclic GMP, calcium, and l-cis-diltiazem. Proc Natl Acad Sci U S A. 1986 Feb;83(4):1163–1167. doi: 10.1073/pnas.83.4.1163. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Stern J. H., Knutsson H., MacLeish P. R. Divalent cations directly affect the conductance of excised patches of rod photoreceptor membrane. Science. 1987 Jun 26;236(4809):1674–1678. doi: 10.1126/science.3037695. [DOI] [PubMed] [Google Scholar]
  35. Torre V., Straforini M., Sesti F., Lamb T. D. Different channel-gating properties of two classes of cyclic GMP-activated channel in vertebrate photoreceptors. Proc Biol Sci. 1992 Dec 22;250(1329):209–215. doi: 10.1098/rspb.1992.0151. [DOI] [PubMed] [Google Scholar]
  36. Watanabe S., Murakami M. Similar properties of cGMP-activated channels between cones and rods in the carp retina. Vis Neurosci. 1991 Jun;6(6):563–568. doi: 10.1017/s0952523800002546. [DOI] [PubMed] [Google Scholar]
  37. Yau K. W., Baylor D. A. Cyclic GMP-activated conductance of retinal photoreceptor cells. Annu Rev Neurosci. 1989;12:289–327. doi: 10.1146/annurev.ne.12.030189.001445. [DOI] [PubMed] [Google Scholar]
  38. Yau K. W. Cyclic nucleotide-gated channels: an expanding new family of ion channels. Proc Natl Acad Sci U S A. 1994 Apr 26;91(9):3481–3483. doi: 10.1073/pnas.91.9.3481. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Zimmerman A. L., Baylor D. A. Cation interactions within the cyclic GMP-activated channel of retinal rods from the tiger salamander. J Physiol. 1992 Apr;449:759–783. doi: 10.1113/jphysiol.1992.sp019112. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Zimmerman A. L., Baylor D. A. Cyclic GMP-sensitive conductance of retinal rods consists of aqueous pores. Nature. 1986 May 1;321(6065):70–72. doi: 10.1038/321070a0. [DOI] [PubMed] [Google Scholar]

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