Abstract
The role of calcium in the mechanism of phototransduction has yet to be defined. The observation of Yoshikami and Hagins (1971), that an application of calcium to the outside of the rod caused a reduction in the dark-current, and thus mimicked the effect of light, led to the well-known “calcium hypothesis” according to which, calcium ions, released by light from an intracellular store, were internal messengers that diffused to the plasma membrane and caused the closure of “light-sensitive” channels. This hypothesis stimulated an enormous interest in phototransduction during the subsequent decade and a half. During that time, however, several lines of evidence began to point to cyclic GMP as the internal transmitter, the recent demonstration, by Fesenko, Kolesnikov and Lyubarsky (1985, 1986), that the channels in patches of plasma membrane excised from rod outer segments (ROS) are activated by cGMP and are not blocked by calcium ions, being, perhaps, the most direct (see also Yau and Nakatani, 1985b). These channels have properties identical to those of the light-sensitive channels (Matthews, 1986).
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
Bownds, M. D. 1980, Biochemical steps in visual transduction: Roles for nucleotides and calcium ions, Photochem. Photobiol., 32:487–490.
Capovilla, M., Caretta, A., Cervetto, L. and Torre, V., 1983, Ionic movements through light-sensitive channels of toad rods, J. Physiol., 343:295–310.
Cavaggioni, A. and Sorbi, R.T., 1981, Cyclic GMP releases calcium from disk membranes of vertebrate photoreceptors, Proc. Natl. Acad. Sci. U.S.A., 78:3964–3968.
Cervetto, L., Lagnado, L. and McNaughton, P. A., 1988, Ion transport by the Na-Ca exchange in isolated rod outer segments, Proc. Natl. Acad. Sci. U.S.A., 85:4548–4552.
Cervetto, L., Lagnado, L., Perry, R. J., Robinson, D. W. and McNaughton, P. A., 1989, Extrusion of Calcium from rod outer segment is driven by both sodium and K gradient, Nature, 337:740–743.
Cervetto, L. and McNaughton, P.A., 1986, The effects of phosphodiesterase inhibitors and lanthanum ions on the light-sensitive current of toad retinal rods, J. Physiol., 370:91–100.
Connor, J.A., 1986, Digital imaging of free calcium changes and of spatial gradients in growing processes in single, mammalian central nervous system cells, Proc. Natl. Acad. Sci. U.S.A., 83:6179–6183.
Fesenko, E.E., Kolesnikov, S.S. and Lyubarsky, A.L., 1985, Induction by cyclic GMP of cationic conductance in plasma membrane of retinal rod outer segment, Nature, 313:310–313.
Fesenko, E.E., Kolesnikov, S.S. and Lyubarsky, A.L., 1986, Direct action of cGMP on the conductance of retinal rod plama membrane, Biochim. Biophys. Acta, 856:661–671.
Fleischman, D. and Denisevich, M., 1979, Guanylate cyclase of isolated bovine retinal rod axonemes, Biochem., 18:5060–5066.
Forti, S., Menini, A., Rispoli, G. and Torre, V., 1989, Kinetics of phototransduction in retinal rods of the newt triturus Cristatus, J. Physiol., 419:265–295.
George, J.S. and Hagins, W.A., 1983, Control of [Ca2+] in rod outer segment disks by light and cyclic GMP, Nature, 303:344–348.
Grynkiewicz, G.M., Poenie, M. and Tsien, R.Y., 1985, A new generation of [Ca2+] indicators with greatly improved fluorescence properties, J. Biol. Chem., 260:3440–3450.
Hodgkin, A.L., McNaughton, P.A. and Nunn, B.J., 1985, The ionic selectivity and calcium dependence of the light-sensitive pathway in toad rods, J. Physiol., 358:447–468.
Hodgkin, A.L., McNaughton, P.A. and Nunn, B.J., 1987, Measurement of sodium-calcium exchange in salamander rods, J. Physiol., 391:347–370.
Koch, K.-W. and Kaupp, U.B., 1985, cGMP directly regulates a cation conductance n membranes of bovine rods by a cooperative mechanism, J. Biol. Chem., 260:6788–6800.
Koch, K.-W. and Stryer, L., 1988, Highly cooperative feedback control of retinal rod guanylate cyclase by calcium ions, Nature, 334:64–66.
Korenbrot, J. I. and Miller, D.L., 1989, Cytoplasmic free calcium concentration in dark-adapted retinal rod outer segments, Vision Res., In press.
Lagnado, L., Cervetto, L. and McNaughton, P.A., 1988, Ion transport by the Na-Ca exchange in isolated rod outer segments, Proc. Natl. Acad. Sci. U.S.A., 85:4548–4552.
Lamb, T. D. 1986, Transduction in vertebrate photoreceptors: The roles of cyclic GMP and calcium, Trends Neurosci., 9:224–228.
Lolley, R. N. and Racz, E., 1982, Calcium modulation of cyclic GMP synthesis in rat visual cells, Vision Res., 22:1481–1486.
Matthews, G. 1986, Comparison of the light-sensitive and cyclic GM P-sensitive conductances in the rod photoreceptor: Noise characteristics, J. Neurosci., 6:2521–2526.
Matthews, H.R., Murphy, R.L.W., Fain, G. and Lamb, T.D., 1988, Photoreceptor light adaptation is mediated by cytoplasmic calcium concentration, Nature, 334:67–69.
McNaughton, P.A., Cervetto, L. and Nunn, B.J., 1986, Measurement of intracellular free calcium concentration in salamander rods, Nature, 322:261–263.
Miller, D.L. and Korenbrot, J.I., 1986, Effects of the intracellular calcium buffer Quin-2 on the photocurrent responses of toad rods, Biophys. J., 49:281a.
Miller, D.L. and Korenbrot, J.I., 1987, Kinetics of light-dependent Ca fluxes across the plasma membrane if rod outer segments, J. Gen. Physiol., 90:397–425.
Nakatani, K. and Yau, K. -W., 1988, Calcium and light adaptation in retinal rods and cones, Nature, 334:69–71.
Pepe, I.M., Panfoli, I. and Cugnoli, C., 1986, Guanylate cyclase in rod outer segments of the toad retina, FEBS Lett., 203:73.
Ratto, G.M., Payne, R., Owen, W.G. and Tsien, R.Y., 1988, The concentration f cytosolic free calcium in vertebrate rod outer segments measured with Fura-2, J. Neu rosci., 8(9):3240–3246.
Robinson, P. R., Kawamura, S., Abramson, B. and Bownds, D., 1980, Control of the cyclic GMP phosphodiesterase of frog photoreceptor membranes, J. Gen. Physiol., 76:631–645.
Sickel, W., 1965, Respiratory and electrical responses to light stimulation in the retina of the frog, Science, 148:648–651.
Steinemann, A. and Stryer, L., 1973, Biochemistry, 12:1499–1502.
Torre, V., Matthews, H.R. and Lamb, T.D., 1986, The role of calcium in regulating the cyclic GMP cascade of phototransduction, Proc. Natl. Acad. Sci. U.S.A., 83:7109–7113.
Yau, K.-W. and K. Nakatani, 1984, Electrogenic Na-Ca exchange in retinal rod outer segment, Nature, 311, 661:663.
Yau, K.-W. and Nakatani, K., 1985a, Light-induced reduction of cytoplasmic free calcium in retinal rod outer segment, Nature, 313:579–582.
Yau, K.-W. and Nakatani, K., 1985b, Light-suppressible, cGM P-sensitive conductance in the plasma membrane of a truncated rod outer segment, Nature, 317:252–255.
Yoshikami, S. and Hagins, W.A., 1971, Light, calcium, and the photocurrent of rods and cones, Biophys. J., 11:47a.
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 1990 Plenum Press, New York
About this chapter
Cite this chapter
Owen, W.G., Ratto, G.M. (1990). The Cytosolic Concentration of Free Ca2+ in Vertebrate Rod Outer Segments. In: Borsellino, A., Cervetto, L., Torre, V. (eds) Sensory Transduction. NATO ASI Series, vol 194. Springer, Boston, MA. https://doi.org/10.1007/978-1-4684-5841-1_15
Download citation
DOI: https://doi.org/10.1007/978-1-4684-5841-1_15
Publisher Name: Springer, Boston, MA
Print ISBN: 978-1-4684-5843-5
Online ISBN: 978-1-4684-5841-1
eBook Packages: Springer Book Archive