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Two opposite effects of ATP on the apparent sensitivity of the cGMP-gated channel of the carp retinal cone

Published online by Cambridge University Press:  02 June 2009

Shu-Ichi Watanabe  and
Jing Shen
Shu-Ichi Watanabe
Affiliation:
Department of Physiology, Keio University School of Medicine, Shinjuku-ku, Tokyo, Japan
Jing Shen
Affiliation:
Department of Physiology, Keio University School of Medicine, Shinjuku-ku, Tokyo, Japan
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Abstract

Effects of ATP on the activity of cGMP-gated channels from carp cone photoreceptors were studied. In 29% of the patches examined (N = 45), ATP (1 mM) enhanced a current evoked by cGMP (20 μM, up to about 100%), in 33%, ATP suppressed it by up to about 90%, and in the remaining 38%, ATP had no effect. ATP showed similar effects on a current evoked by 8-bromoguanosine 3′,5′-cyclic monophosphate (2 μM, enhancing in 42% of the patches, suppressing in 25%, no effect in 33%, N = 12), suggesting that the effects were not through modulation of the phosphodiesterase. Both of the effects, enhancement and suppression, were produced by a change in apparent affinity for cGMP, since (1) the maximum current evoked by cGMP of the saturating concentration (≥1 mM) was not affected, and (2) the A1/2 value decreased by approximately 45% (N = 2) or increased by approximately 25% (N = 2). A lower pH (approximately 6) facilitated the enhancing effect. ATP-γ-S (1 mM) showed a suppressing effect in 80% of the patches and no effect in 20% of the patches (N = 10). However, ATP-γ-S did not show an enhancing effect. Thus, ATP had two opposite effects through different mechanisms on the apparent sensitivity of the channel to cGMP; increasing and decreasing.

Keywords

Cone photoreceptorcGMP-gated channelATPATP-γ-SRetina
Type
Research Articles
Information
Visual Neuroscience , Volume 14 , Issue 4 , July 1997 , pp. 609 - 615
Copyright
Copyright © Cambridge University Press 1997

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References

Biernbaum, M.S. & Bownds, M.D. (1985). Light-induced changes in GTP and ATP in frog rod photoreceptors. Comparison with recovery of dark current and light sensitivity during dark adaptation. Journal of General Physiology 85, 107–121.CrossRefGoogle ScholarPubMed
Chen, T.-Y., Illing, M., Molday, L.L., Hsu, Y.-T., Yau, K.-W. & Molday, R.S. (1994). Subunit 2 (or β) of retinal rod cGMP-gated cation channel is a component of the 240-kDa channel-associated protein and mediates Ca2+-calmodulin modulation. Proceedings of the National Academy of Sciences of the U.S.A. 91, 11757–11761.CrossRefGoogle Scholar
Chen, T.-Y. & Yau, K.-W. (1994). Direct modulation by Ca2+-calmodulin of cyclic nucleotide-activated channel of rat olfactory receptor neurons. Nature 368, 545–548.CrossRefGoogle Scholar
Eckstein, F. (1985). Nucleoside phosphorothioates. Annual Review of Biochemistry 54, 367–402.CrossRefGoogle ScholarPubMed
Ertel, E.A. (1990). Excised patches of plasma membrane from vertebrate rod outer segments retain a functional phototransduction enzymatic cascade. Proceedings of the National Academy of Sciences of the U.S.A. 87, 4226–4230.CrossRefGoogle ScholarPubMed
Ertel, E.A. (1994). Modulation of guanylate cyclase and phosphodiesterase by monovalent cations and nucleotide triphosphates in lightsensitive excised patches of rod outer segment. Pflügers Archiv 428, 372–381.CrossRefGoogle Scholar
Ertel, E.A., Sather, W.A. & Detwiler, P.D. (1989). Light and nucleoside triphosphates influence cGMP-induced currents in excised patches from rod photorcceptors. Biophysical Journal 55, 458a.Google Scholar
Fesenko, E.E., Kolesnikov, S.S. & Lyubarsky, A. (1985). Induction by cyclic GMP of cationic conductance in plasma membrane of retinal rod outer segment. Nature 313, 310–313.CrossRefGoogle ScholarPubMed
Filatov, G.N., Jainazarov, A.B., Kolesnikov, S.S., Lyubarsky, A.L. & Fesenko, E.G. (1989). The effect of ATP, GTP and cAMP on the cGMP-dependent conductance of the fragments from frog rod plasma membrane. FEBS Letters 245, 185–188.CrossRefGoogle ScholarPubMed
Fukada, Y., Kokame, K., Okano, T., Shichida, Y. & Yoshizawa, T. (1990). Phosphorylation of iodopsin, chicken red-sensitive cone visual pigment. Biochemistry 29, 10102–10106.CrossRefGoogle ScholarPubMed
Gordon, S.E., Brautigan, D.L. & Zimmerman, A.L. (1992). Protein phosphatases modulate the apparent agonist affinity of the lightregulated ion channel in retinal rod. Neuron 9, 739–748.CrossRefGoogle Scholar
Gordon, S.E., Downing-Park, J. & Zimmerman, A.L. (1995 a). Modulation of the cGMP-gated ion channel in frog rods by calmodulin and an endogenous inhibitory factor. Journal of Physiology 486.3, 533–546.CrossRefGoogle Scholar
Gordon, S.E., Downing-Park, J., Tam, B. & Zimmerman, A.L. (1995 b). Diacylglycerol analogs inhibit the rod cGMP-gated channel by a phosphorylation-independent mechanism. Biophysical Journal 69, 409–417.CrossRefGoogle ScholarPubMed
Gray-Keller, M.P. & Detwiler, P.B. (1994). The calcium feedback signal in the phototransduction cascade of vertebrate rods. Neuron 13, 849–861.CrossRefGoogle ScholarPubMed
Hamill, O.P., Marty, A., Neuer, E., Sakmann, B. & Sigworth, F.J. (1981). Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers Archiv 391, 85–100.CrossRefGoogle ScholarPubMed
Haynes, L.W., Kay, A.R. & Yau, K.-W. (1986). Single cyclic GMP-activated channel activity in excised patches of rod outer segment membrane. Nature 321, 66–70.CrossRefGoogle ScholarPubMed
Haynes, L. & Yau, K.-W. (1985). Cyclic GMP-sensitive conductance in outer segment membrane of catfish cones. Nature 317, 61–64.CrossRefGoogle ScholarPubMed
Haynes, L.W. & Yau, K.-W. (1990). Single-channel measurement from the cyclic GMP-activated conductance of catfish retinal cones. Journal of Physiology 429, 451–481.CrossRefGoogle ScholarPubMed
Hsu, Y.-T. & Molday, R.S. (1993). Modulation of the cGMP-gated channel of rod photoreceptor cells by calmodulin. Nature 361, 76–79.CrossRefGoogle ScholarPubMed
Kawamura, S. & Murakami, M. (1991). Calcium-dependent regulation of cyclic GMP phosphodiesterase by a protein from frog retinal rods. Nature 349, 420–423.CrossRefGoogle ScholarPubMed
Koch, K.-W. (1992). Biochemical mechanism of light adaptation in vertebrate photoreceptors. Trends in Biochemical Sciences 17, 307–311.CrossRefGoogle ScholarPubMed
Koutalos, Y. & Yau, K.-W. (1996). Regulation of sensitivity in vertebrate rod photoreceptors by calcium. Trends in Neurosciences 19, 73–81.CrossRefGoogle ScholarPubMed
Kramer, R.H. & Siegelbaum, S.A. (1992). Intracellular Ca2+ regulates the sensitivity of cyclic nucleotide-gated channels in olfactory receptor neurons. Neuron 9, 897–906.CrossRefGoogle ScholarPubMed
Liebman, P.A. & Pugh, E.N. Jr. (1980). ATP mediates rapid reversal of cyclic GMP phosphodiesterase activation in visual receptor membranes. Nature 287, 734–736.CrossRefGoogle ScholarPubMed
Marc, R.E. & Sperling, H.G. (1976). Color receptor identities of goldfish cones. Science 191, 487–489.CrossRefGoogle ScholarPubMed
Matthews, G. & Watanabe, S.-I. (1987). Properties of ion channels closed by light and opened by guanosine 3′,5′-cyclic monophosphate in toad retinal rods. Journal of Physiology 389, 691–715.CrossRefGoogle Scholar
Matthews, G. & Watanabe, S.-I. (1988). Activation of single ion channel from toad retinal rod inner segments by cyclic GMP: Concentration dependence. Journal of Physiology 403, 389–405.CrossRefGoogle ScholarPubMed
Menini, A. & Nunn, B.J. (1990). The effect of pH on the cyclic GMP-gated conductance in retinal rods. In Sensory Transduction, ed. Borsellino, A., Cervetto, L. & Torre, V., pp. 175–181. New York: Plenum Press.CrossRefGoogle Scholar
Nakatani, K., Koutalos, Y. & Yau, K.-W. (1994). Ca2+ modulation of the cGMP-gated channel of bullfrog retinal rod photoreceptors. Journal of Physiology 484, 69–76.CrossRefGoogle Scholar
Picones, A. & Korenbrot, J.I. (1992). Permeation and interaction of monovalent cations with cGMP-gated channel of cone photoreceptor. Journal of General Physiology 100, 647–673.CrossRefGoogle Scholar
Shen, J., Watanabe, S.-I. & Kaneko, A. (1995). Cell dissociation with papain reduces the density of cGMP-activated channels of the retinal rod. Japanese Journal of Physiology 45, 151–164.Google ScholarPubMed
Stell, W.K. & Harosi, F.I. (1976). Cone structure and visual pigment content in the retina of goldfish. Vision Research 16, 647–657.CrossRefGoogle ScholarPubMed
Tanaka, J.C. (1993). The effects of protons on 3′,5′-cGMP-activated currents in photoreceptor patches. Biophysical Journal 65, 2517–2523.CrossRefGoogle ScholarPubMed
Watanabe, S.-I. & Matthews, G. (1990). Cyclic GMP-activated channels of rod photoreceptors show neither fast nor slow desensitization. Visual Neuroscience 4, 481–487.CrossRefGoogle ScholarPubMed
Watanabe, S.-I. & Murakami, M. (1991). Similar properties of cGMP-activated channels between cones and rods in the carp retina. Visual Neuroscience 6, 563–568.CrossRefGoogle ScholarPubMed
Watanabe, S.-I. & Murakami, M. (1992). Phototransduction in cones as examined in excised membrane patch. Japanese Journal of Physiology 42, 309–320.Google ScholarPubMed
Yau, K.-W. & Baylor, D.A. (1989). Cyclic GMP-activated conductance of retinal photoreceptor cells. Annual Review of Neuroscience 12, 289–327.CrossRefGoogle ScholarPubMed
Zimmerman, A.L. & Baylor, D.A. (1986). Cyclic GMP-sensitive conductance of retinal rods consists of aqueous pores. Nature 321, 70–72.CrossRefGoogle ScholarPubMed
Zimmerman, A.L., Yamanaka, G., Eckstein, F., Baylor, D.A. & Stryer, L. (1985). Interaction of hydrolysis-resistant analogs of cyclic GMP with the phosphodiesterase and light-sensitive channel of retinal rod outer segments. Proceedings of the National Academy of Sciences of the U.S.A. 82, 8813–8817.CrossRefGoogle ScholarPubMed