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Four cases of direct ion channel gating by cyclic nucleotides

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Abstract

Four different nucleotide-gated ion channels are discussed in terms of their biophysical properties and their importance in cell physiology. Channels activated directly by cGMP are present in vertebrate and invertebrate photoreceptors. In both cases cGMP increases the fraction of time the channel remains in the open state. At least three cGMP molecules are involved in channel opening in vertebrate photoreceptors and the concentration of the cyclic nucleotide to obtain the half maximal effect is about 15 µM. The light-dependent channel of both vertebrates and invertebrates is poorly cation selective. The vertebrate channel allows divalent cations to pass through 10–15-fold more easily than monovalent ions. In agreement with their preference for divalent cations, this channel is blocked byl-cis Dialtazem, a molecule that blocks certain types of calcium channels. In olfactory neurons a channel activated by both cAMP and cGMP is found and, as in the light-dependent channel, several molecules of the nucleotide are needed to open the channel with a half maximal effect obtained in the range of 1–40 µM. The channel is poorly cationic selective. A K+ channel directly and specifically activated by cAMP is found inDrosophila larval muscle. At least three cAMP molecules are involved in the opening reaction. Half-maximal effect is obtained at about 50 µM. This channel is blocked by micromolar amount of tetraethylammonium applied internally. Interestingly, this channel has a probability of opening 10–20-fold larger in the mutantdunce, a mutant that possesses abnormally elevated intracellular cAMP level, than in the wild type.

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References

  • Anholt, R. R. H. (1987).Trends Biochem. Sci. 26, 788–795.

    Google Scholar 

  • Anholt, R. R. H., Aebi, U., and Snyder, S. H. (1986).J. Neurosci. 6, 1962–1965.

    Google Scholar 

  • Anholt, R. R. H., Mumby, S. M., Stoffers, D. A., Girard, P. R., Kuo, K. F., and Snyder, S. H. (1987).Biochemistry 26, 788–795.

    Google Scholar 

  • Bacigalupo, J. (1986). InIonic Channels in Cells and Model Systems (Latorre, R., ed.), Plenum Press, New York and London, pp. 221–233.

    Google Scholar 

  • Bacigalupo, J., Chin, K., and Lisman, J. E. (1986).J. Gen. Physiol. 87, 73–89.

    Google Scholar 

  • Bacigalupo, J., and Lisman, J. E. (1983).Nature (London)304, 268–270.

    Google Scholar 

  • Bacigalupo, J., and Lisman, J. E. (1984).Biophys. J. 45, 3–5.

    Google Scholar 

  • Bacigalupo, J., Lisman, J. E., and Johnson, E. C. (1987).Biophys. J. 51, 15a.

    Google Scholar 

  • Bacigalupo, J., Johnson, E. C., Robinson, P. R., and Lisman, J. E. (1990). InTransduction in Biological Systems. (Hidalgo, C., Bacigalupo, J., Jaimovich, E., and Vergara, J., eds.), Plenum Press, New York and London.

    Google Scholar 

  • Baylor, D. A., Lamb, T. D., and Yau, K.-W. (1979).J. Physiol. 288, 589–611.

    Google Scholar 

  • Bodola, R. D., and Detwiler, P. B. (1985).J. Physiol. 367, 183–216.

    Google Scholar 

  • Bolsover, S. R., and Brown, J. E. (1985).J. Physiol. 364, 381–393.

    Google Scholar 

  • Breer, H., Boekhoff, I., and Tareilus, E. (1990).Nature (London)345, 65–68.

    Google Scholar 

  • Brown, J. E., and Mote, M. I. (1974).J. Gen. Physiol. 63, 337–350.

    Google Scholar 

  • Brown, J. E., and Pinto, L. H. (1974).J. Physiol. 236, 575–591.

    Google Scholar 

  • Bruch, R. C., and Kalinoski, D. L. (1987).J. Biol. Chem. 262, 2401–2404.

    Google Scholar 

  • Bruch, R. C., and Teeter, J. H. (1989). InChemical Senses: Receptor Events and Transduction in Taste and Olfaction (J. G. Brand, J. H. Teeter, R. H. Cagan, and N. R. Kare, eds.), Marcel Dekker, New York.

    Google Scholar 

  • Byers, D., Davis, R. L., and Kiger, J. A. (1981).Nature (London)289, 79–81.

    Google Scholar 

  • Cervetto, L. (1973).Science 24, 401–403.

    Google Scholar 

  • Cook, N. J., Hanke, W., and Kaupp, U. B. (1987).Proc. Natl. Acad. Sci. USA 84, 585–589.

    Google Scholar 

  • Cote, R. H., Biernbaum, M. S., Nicol, G. D., and Bownds, M. D. (1984).J. Biol. Chem. 259, 9635–9641.

    Google Scholar 

  • Dani, J. A. (1989).Curr. Opinion Cell Biol. 1, 753–764.

    Google Scholar 

  • Davis, R. L., and Kiger, J. A. (1981).J. Cell Biol. 90, 101–107.

    Google Scholar 

  • Delgado, R., Latorre, R., and Labarca, P. (1990a).Biophys. J. 57, 311a.

  • Delgado, R., Hidalgo, P., Diaz, F., Latorre, R., and Labarca, P. (1990b).Proc. Natl. Acad. Sci. USA, in press.

  • Detwiller, P. B., Conner, J. D., and Bodoia, R. D. (1982).Nature (London)300, 59–61.

    Google Scholar 

  • Dudai, Y. (1988).Annu. Rev. Neurosci. 11, 537–563.

    Google Scholar 

  • Elkins, T., Ganetzky, B., and Wu, C. F. (1986).Proc. Natl. Acad. Sci. USA 83, 8415–8419.

    Google Scholar 

  • Fain, G. L., and Lisman, J. E. (1981).Prog. Biophys. Mol. Biol. 37, 91–147.

    Google Scholar 

  • Fesenko, E. E., Kolesnikov, S. S., and Lyubarsky, A. L. (1985).Nature (London)313, 310–313.

    Google Scholar 

  • Fesenko, E. E., Kolesnikvo, S. S., and Lyubarsky, A. L. (1986).Biochim. Biophys. Acta 856, 661–671.

    Google Scholar 

  • Firestein, S., and Werblin, F. (1989).Science 244, 79–82.

    Google Scholar 

  • Frings, S., and Lindemann, B. (1988).J. Membr. Biol. 105, 233–243.

    Google Scholar 

  • Fung, B. B.-K., and Stryer, L. (1980).Proc. Natl. Acad. Sci. USA 77, 2500–2504.

    Google Scholar 

  • Getchell, T. V. (1986).Physiol. Rev. 66, 772–817.

    Google Scholar 

  • Gho, M., and Mallart, A. (1986).Pfluegers Arch. 407, 526–533.

    Google Scholar 

  • Gray, P., and Attwell, D. (1985).Proc. R. Soc. London B 223, 379–388.

    Google Scholar 

  • Hanke, W., Cook, N. J., and Kaupp, U. B. (1988).Proc. Natl. Acad. Sci. USA 85, 94–98.

    Google Scholar 

  • Hanke, W., Simmoteit, R., and Kaupp, U. B. (1990). InTransduction in Biological Systems (Hidalgo, C., Bacigalupo, J., Jaimovich, E., and Vergara, J., eds.), Plenum Press, New York and London.

    Google Scholar 

  • Haynes, L. W., and Yau, K.-W. (1990). InTransduction in Biological Systems (Hidalgo, C., Bacigalupo, J., Jaimovich, E., and Vergara, C., eds.), Plenum Press, New York and London.

    Google Scholar 

  • Haynes, L. W., Kay, A. R., and Yau, K.-W. (1986).Nature (London)321, 66–70.

    Google Scholar 

  • Hodgkin, A. L., McNaughton, P. A., and Nunn, B. J. (1985).J. Physiol. 358, 447–468.

    Google Scholar 

  • Huque, T., and Bruch, R. C. (1986).Biochem. Biophys. Res. Commun. 137, 30–33.

    Google Scholar 

  • Johnson, E. C., Robinson, P. R., and Lisman, J. E. (1986).Nature (London)324, 468–470.

    Google Scholar 

  • Johnson, E. C., Bacigalupo, J., Vergara, C., and Lisman, J. E. (1991).J. Gen. Physiol., in press.

  • Jones, D. T., and Reed, R. R. (1989).Science 224, 790–795.

    Google Scholar 

  • Kaupp, U. B., Niidome, T., Tanabe, T., Tereda, S., Boenigk, W., Stuhmer, W., Cook, N. J., Kangawa, K., Matsuo, H., Hirose, T., Miyata, T., and Numa, S. (1989).Nature (London)342, 762–766.

    Google Scholar 

  • Koch, K.-W., and Kaupp, U. B. (1985).J. Biol. Chem. 260, 6788–6800.

    Google Scholar 

  • Komatzu, A., Singh, S., Rathe, M., and Wu, C.-F. (1990).Neuron. 4, 313–321.

    Google Scholar 

  • Labarca, P., and Bacigalupo, J. (1988).J. Bioenerg. Biomembr. 20, 551–568.

    Google Scholar 

  • Labarca, P., Simon, S. A., and Anholt, R. R. H. (1988).Proc. Natl. Acad. Sci. USA 85, 944–947.

    Google Scholar 

  • Lancet, D. (1986).Annu. Rev. Neurosci. 9, 329–355.

    Google Scholar 

  • Lamb, T. D., and Mathews, H. R. (1988).J. Physiol. 403, 473–494.

    Google Scholar 

  • Latorre, R., and Miller, C. (1983).J. Membr. Biol. 71, 11–30.

    Google Scholar 

  • Lee, K., and Tsien, R. W. (1983).Nature (London)302, 790–794.

    Google Scholar 

  • Levitan, I. B. (1985).J. Membr. Biol. 87, 177–190.

    Google Scholar 

  • Levy, S., and Fein, A. (1985).J. Gen. Physiol. 85, 805–841.

    Google Scholar 

  • Liebman, P. A., Parker, K., and Dratz, E. A. (1987).Annu. Rev. Physiol. 49, 765–791.

    Google Scholar 

  • Lisman, J. E., and Brown, J. E. (1972). InThe Visual System: Biophysics and Their Clinical Applications (Arden, G. B., ed.), Plenum Press, New York, pp. 23–33.

    Google Scholar 

  • Matesic, D., and Liebman, P. A. (1987).Nature (London)326, 600–603.

    Google Scholar 

  • Matthews, G., and Watanabe, S. I. (1987).Proc. Natl. Acad. Sci. USA 84, 299–302.

    Google Scholar 

  • Matthews, G. (1987).J. Physiol. 403, 389–405.

    Google Scholar 

  • Menco, B. P. M. (1980).Cell Tissue Res. 211, 5–29.

    Google Scholar 

  • Meneuse, A., Dodd, G., and Poynder, T. M. (1977).Biochem. Biophys. Res. Commun. 77, 671–677.

    Google Scholar 

  • Millecchia, R., and Mauro, A. (1969).J. Gen. Physiol. 54, 310–351.

    Google Scholar 

  • Minor, A. V., and Sakina, N. L. (1973).Neirofiziologiya 5, 415–422.

    Google Scholar 

  • Nakamura, T., and Gold, G. M. (1987).Nature (London)325, 442–444.

    Google Scholar 

  • Nakatani, K., and Yau, K.-W. (1988).J. Physiol. 395, 731–753.

    Google Scholar 

  • Nasi, E., and Gomez, M. (1990).Biophys. J. 57, 368a.

  • Nicol, G. D., Schnetkamp, P. P. M., Saimi, Y., Cragoe, E. J., Jr., and Bownds, M. D. (1987).J. Gen. Physiol. 90, 651–670.

    Google Scholar 

  • Ottoson, D. (1956).Acta Physiol. Scand. 35, 1–83.

    Google Scholar 

  • Ottoson, D. (1958).Acta Physiol. Scand. 43, 167–181.

    Google Scholar 

  • Pace, V., and Lancet, D. (1986).Proc. Natl. Acad. Sci. USA 83, 4947–4951.

    Google Scholar 

  • Pace, V., Harsk, L., Salomon, Y., and Lancet, D. (1985).Nature (London)316, 255–258.

    Google Scholar 

  • Papazian, D. M., Schwarz, T. L., Tempel, L. B., Timpe, L. C., and Jan, L. Y. (1988).Annu. Rev. Physiol. 50, 379–394.

    Google Scholar 

  • Payne, R. (1990). InTransduction in Biological Systems (Hidalgo, C., Bacigalupo, J., Jaimovich, E., and Vergara, J., eds.), Plenum Press, New York.

    Google Scholar 

  • Payne, R., Corson, D. W., Fein, A., and Berridge, M. J. (1986).J. Gen. Physiol. 88, 127–142.

    Google Scholar 

  • Payne, R., Walz, B., Levy, S., and Fein, A. (1988).Philos. Trans. R. Soc. London. B 320, 359–379.

    Google Scholar 

  • Pugh, E. N., and Cobbs, W. H. (1986).Vision Res. 26, 1613–1643.

    Google Scholar 

  • Reuter, H. (1987).News Physiol. Sci. 2, 168–171.

    Google Scholar 

  • Salkoff, L. B., and Wyman, R. (1981).Nature (London)293, 228–230.

    Google Scholar 

  • Shinozawa, T., Sokabe, M., Tereda, S., Matsusaka, H., and Yoshizawa, T. (1987).J. Biochem. 102, 281–290.

    Google Scholar 

  • Singh, S., and Wu, C.-F. (1989).Neuron 2, 1325–1329.

    Google Scholar 

  • Sklar, P. B., Anholt, R. R. H., and Snyder, S. H. (1986).J. Biol. Chem. 261, 15538–15543.

    Google Scholar 

  • Solc, C. K., and Aldrich, R. W. (1988).J. Neurosci. 8, 2556–2570.

    Google Scholar 

  • Solc, C. K., Zagotta, W. N., and Aldrich, R. W. (1987).Science 236, 1094–1098.

    Google Scholar 

  • Tanaka, J. C., Furman, R. E., Cobbs, W. H., and Mueller, P. (1987).Proc. Natl. Acad. Sci. USA 84, 724–728.

    Google Scholar 

  • Tsien, R. W., Hess, P., McCleskey, E. W., and Rosenberg, R. L. (1987).Annu. Rev. Biophys. Biophys. Chem. 16, 265–290.

    Google Scholar 

  • Tully, T. (1987).Trends Neurosci. 10, 330–334.

    Google Scholar 

  • Ugarte, U., Morales, B., Delgado, R., Bacigalupo, J., and Labarca, P. (1990).Biophys. J. 57, ??.

    Google Scholar 

  • Vodyanoy, V., and Vodyanoy, I. (1987).Neurosci. Lett. 73, 235–258.

    Google Scholar 

  • Yau, K.-W., and Baylor, D. A. (1989).Annu. Rev. Neurosc. 12, 289–327.

    Google Scholar 

  • Yau, K.-W., and Nakatani, K. (1984).Nature (London)309, 352–354.

    Google Scholar 

  • Yau, K.-W., and Nakatani, K. (1985).Nature (London)317, 252–255.

    Google Scholar 

  • Yau, K.-W., McNaughton, P. A., and Hodgkin, A. L. (1981).Nature (London)292, 502–505.

    Google Scholar 

  • Yoshikami, S., and Hagins, W. A. (1973). InBiochemistry and Physiology of Visual Pigments (Langer, H., ed.), Springer, New York, pp. 245–255.

    Google Scholar 

  • Zagotta, W. N., Brainard, M. S., and Aldrich, R. W. (1988).J. Neurosci. 8, 4765–4794.

    Google Scholar 

  • Zimmermann, A., and Baylor, D. A. (1985).Biophys. J. 47, 357a.

    Google Scholar 

  • Zimmanmann, A., and Baylor, D. A. (1986).Nature (London)321, 70–72.

    Google Scholar 

  • Zimmermann, A., and Baylor, D. A. (1988).Biophys. J. 53, 472a.

    Google Scholar 

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Latorre, R., Bacigalupo, J., Delgado, R. et al. Four cases of direct ion channel gating by cyclic nucleotides. J Bioenerg Biomembr 23, 577–597 (1991). https://doi.org/10.1007/BF00785812

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