Hostname: page-component-cd9895bd7-p9bg8 Total loading time: 0 Render date: 2024-12-23T00:30:11.041Z Has data issue: false hasContentIssue false
  • English
  • Français

Modulation of rod, but not cone, cGMP-gated photoreceptor channels by calcium-calmodulin

Published online by Cambridge University Press:  02 June 2009

Lawrence W. Haynes  and
Stephanie C. Stotz
Lawrence W. Haynes
Affiliation:
Department of Physiology and Biophysics and Neuroscience Research Group, Faculty of Medicine, University of Calgary, Calgary, Alberta, Canada
Stephanie C. Stotz
Affiliation:
Department of Physiology and Biophysics and Neuroscience Research Group, Faculty of Medicine, University of Calgary, Calgary, Alberta, Canada
Get access Rights & Permissions [Opens in a new window]

Abstract

Inside-out patches containing cGMP-gated channels were excised from catfish rod or cone outer segments and held under voltage clamp. The net cGMP-dependent currents elicited by saturating and subsaturating concentrations of cGMP at ±30 mV were measured and the dependence of current upon cGMP concentration was determined. The apparent affinity of the channel for its ligand was estimated by fitting these data with the Hill equation. The concentration of cGMP required to give half the maximum current (K1/2) in rod and cone channels at +30 mV was ~28 μM and ~37 μM, respectively, and was weakly voltage dependent. Thus, cone channels have an intrinsically higher K1/2 than rod channels. For both types of channel, the Hill coefficient was ~2.3. In the presence of calcium-calmodulin, the apparent affinity of the rod channel for cGMP decreased by about twofold, but the apparent affinity of the cone channels was unaffected. These results indicate that the open probability of the cone channel for its ligand cannot be modulated by calmodulin. This represents the first significant departure between rod and cone photoreceptors in mechanisms used by phototransduction and suggests that the β subunit of the cone channel must be different from that of the rod channel.

Keywords

PhototransductionRetinal rodRetinal coneIon channel
Type
Research Articles
Information
Visual Neuroscience , Volume 14 , Issue 2 , March 1997 , pp. 233 - 239
Copyright
Copyright © Cambridge University Press 1997

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Bauer, P.J. (1996). Ca-Calmodulin binding to cGMP-gated channels: Affinity stoichiometry and binding site density. Biophysical Journal 70, A137.Google Scholar
Bönigk, W., Altenhofen, W., Müller, R, Dose, A., Illing, M., Molday, R.S. & Kaupp, U.B. (1993). Rod and cone photoreceptor cells express distinct genes for cGMP-gated channels. Neuron 10, 865–877.CrossRefGoogle ScholarPubMed
Borisy, F.F., Ronnett, G.V., Cunningham, A.M., JUILFS, D., Beavo, J. & Snyder, S.H. (1992). Calcium/calmodulin-activaled phosphodiesterase expressed in olfactory receptor neurons. Journal of Neuroscience 12, 915–923.CrossRefGoogle ScholarPubMed
Chen, T.-Y, Peng, Y.-W., Dhallan, R.S., Ahamed, B., Reed, R.R. & Yau, K-.W. (1993). A new subunit of the cyclic nucleotide-gated cation channel in retinal rods. Nature 362, 764–767.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
Colamartino, G., Menini, A. & Torre, V. (1991). Blockage and permeation of divalent cations through the cyclic GMP-activated channel from tiger salamander retinal rods. Journal of Physiology 440, 189–206.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
Fesenko, E.E., Kolesnikov, S.S. & Lyubarsky, A.L. (1985). Induction by cyclic GMP of cationic conductance in plasma membrane of retinal rod outer segment. Nature 313, 310–313.CrossRefGoogle ScholarPubMed
Furman, R.E. & Tanaka, J.C. (1990). Monovalent selectivity of the cyclic guanosine monophosphate-activated ion channel. Journal of General Physiology 96, 57–82.CrossRefGoogle ScholarPubMed
Gordon, S.E., Brautigan, D.L. & Zimmerman, A.L. (1992). Protein phosphatases modulate the apparent agonist affinity of the light-regulated ion channel in retinal rods. Neuron 9, 739–748.CrossRefGoogle ScholarPubMed
Gordon, S.E., Downing-Park, J. & Zimmerman, A.L. (1995). Modulation of cGMP-gated ion channel in frog rods by calmodulin and an endogenous inhibitory factor. Journal of Physiology 486, 533–546.CrossRefGoogle Scholar
Haynes, L.W. (1992). Block of the cyclic GMP-gated channel of vertebrate rod and cone photoreceptors by L-cis-diltiazem. Journal of General Physiology 100, 783–801.CrossRefGoogle ScholarPubMed
Haynes, L.W. (1995 a). Permeation and block by internal and external divalent cations of the catfish cone photoreceptor cGMP-gated channel. Journal of General Physiology 106, 485–505.CrossRefGoogle ScholarPubMed
Haynes, L.W. (1995 b). Permeation of internal and external monovalent cations through the catfish cone photoreceptor cGMP-gated channel. Journal of General Physiology 106, 507–523.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.W. & Stotz, S.C. (1996). Modulation of cone photoreceptor cGMP-gated channels. Biophysical Journal 70, A138.Google Scholar
Haynes, L.W. & 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 measurements 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
Kaupp, U.B. & Koch, K.-W. (1992). Role of cGMPand Ca2+ in vertebrate photoreceptor excitation and adaptation. Annual Review of Physiology 54, 153–175.CrossRefGoogle Scholar
Kurahashi, T. (1989). Activation by odorants of cation-selective conductance in the olfactory receptor cell isolated from the newt. Journal of Physiology 419, 77–192.CrossRefGoogle ScholarPubMed
Kurahashi, T., Kaneko, A. & Shibuya, T. (1990). Ionic mechanisms of the olfactory transduction studied on isolated receptor cells of the newt. Neuroscience Research (Suppl.) 12, S85–S96.Google ScholarPubMed
Matthews, G. & Watanabe, S.-I. (1988). Activation of single ion channels from toad retinal rod inner segments by cyclic GMP: Concentration dependence. Journal of Physiology 403, 389–405.CrossRefGoogle ScholarPubMed
Matthews, H.R., Murphy, R.L.W., Fain, G.L. & Lamb, T.D. (1988). Photoreceptor light adaptation is mediated by cytoplasmic calcium concentration. Nature 334, 67–69.CrossRefGoogle ScholarPubMed
Menini, A. (1990). Currents carried by monovalent cations through cyclic GMP-activated channels in excised patches from salamander rods. Journal of Physiology 424, 167–185.CrossRefGoogle ScholarPubMed
Nakamura, T. & Gold, G.H. (1987). A cyclic nucleotide-gated conductance in olfactory receptor cilia. Nature 325, 442–444.CrossRefGoogle ScholarPubMed
Nakatani, K., Koutalos, Y. & Yau, K.-W. (1995). Ca2+ modulation of the cGMP-gated channel of bullfrog retinal rod photoreceptors. Journal of Physiology 484, 69–76.CrossRefGoogle ScholarPubMed
Nakatani, K. & Yau, K.-W. (1988). Calcium and light adaptation in retinal rods and cones. Nature 334, 69–71.CrossRefGoogle ScholarPubMed
Picones, A. & Korenbrot, J.L. (1992). Permeation and interaction of monovalent cations with the cGMP-gated channel of cone photoreceptors. Journal of General Physiology 100, 647–673.CrossRefGoogle ScholarPubMed
Picones, A. & Korenbrot, J.L. (1995 a). Permeability and interaction of Ca2+ with cGMP-gated ion channels differ in retinal rod and cone photoreceptors. Biophysical Journal 69, 120–127.CrossRefGoogle ScholarPubMed
Picones, A. & Korenbrot, J.L. (1995 b). Spontaneous, ligand-independent activity of the cGMP-gated ion channels in cone photoreceptors of fish. Journal of Physiology 485, 699–714.CrossRefGoogle ScholarPubMed
Pugh, E.N. Jr & Lamb, T.D. (1993). Amplification and kinetics of the activation steps in phototransduction. Biochimica et Biophysica Acta 1141, 111–149.CrossRefGoogle ScholarPubMed
Schnetkamp, P.P.M., Li, X.-B., Basu, D.K. & Szerencsei, R.T. (1991). Regúlation of free cytosolic Ca2+ concentration in the outer segments of bovine retinal rods by Na-Ca-K exchange measured with Fluo-3. Journal of Biological Chemistry 266, 22975–22982.CrossRefGoogle ScholarPubMed
Taylor, W.R. & Baylor, D.A. (1995). Conductance and kinetics of single cGMP-activated channels in salamander rod outer segments. Journal of Physiology 483, 567–582.CrossRefGoogle 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
Yau, K.-W. & Haynes, L.W. (1986). Effect of divalent cations on the macroscopic cGMP-activated current in excised rod membrane patches. Biophysical Journal 49, 33a.Google Scholar
Young, R.W. (1976). Visual cells and the concept of renewal. Investigative Ophthalmology 15, 700–725.Google 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. & Baylor, D.A. (1992). Cation interactions within the cyclic GMP-activated channel of retinal rods from the tiger salamander. Journal of Physiology 449, 759–783.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