Abstract
Visual phototransduction, the conversion of incoming light to an electrical signal, takes place in the outer segments of the rod and cone photoreceptor cells. Light reduces the concentration of cGMP, which, in darkness, keeps open cationic channels present in the plasma membrane of the outer segment. Ca2+plays an important role in phototransduction by modulating the cGMP-gated channels as well as cGMP synthesis and breakdown. Ca2+is involved in a negative feedback that is essential for photoreceptor adaptation to background illumination. The effects of Ca2+on the different components of rod phototransduction have been characterized and can quantitatively account for the steady state responses of the rod cell to background illumination. The propagation of the Ca2+feedback signal from the periphery toward the center of the outer segment depends on the Ca2+diffusion coefficient, which has a value of 15±1 μm2s-1. This value shows that diffusion of Ca2+in the radial direction is quite slow providing a significant barrier in the propagation of the feedback signal. Also, because the diffusion coefficient of Ca2+is much smaller than that of cGMP, the decline of Ca2+in the longitudinal direction lags behind the propagation of excitation by the decline of cGMP.
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.
Similar content being viewed by others
References
Hagins WA. The visual process: Excitatory mechanisms in the primary receptor cells. Ann Rev Biophys Bioeng 1972; 1:131–158.
Yoshikami S, Hagins WA. Control of dark current in vertebrate rods and cones. In: Langer H, ed. Biochemistry and Physiology of Visual Pigments. New York: Springer 1973:245–255.
Pugh EN Jr. The nature and identity of the internal excitational transmitter of vertebrate phototransduction. Ann Rev Physiol 1987; 49:715–741.
Hodgkin AL, McNaughton PA, Nunn BJ. The ionic selectivity and calcium dependence of the light-sensitive pathway in toad rods. J Physiol 1985; 358:447–468.
Yau K-W, Nakatani K. Electrogenic Na-Ca exchange in retinal rod outer segment. Nature 1984; 311:661–663.
Cervetto L et al. Extrusion of calcium from rod outer segments is driven by both sodium and potassium gradients. Nature 1989; 337:740–743.
Yau K-W, Nakatani K. Light-induced reduction of cytoplasmic free calcium in retinal rod outer segment. Nature 1985; 313:579–582.
McNaughton PA, Cervetto L, Nunn BJ. Measurement of the intracellular free calcium concentration in salamander rods. Nature 1986; 322:261–263.
Gray-Keller MP, Detwiler PB.The calcium feedback signal in in the phototransduction cascade of vertebrate rods. Neuron 1994; 13:849–861.
McCarthy ST, Younger JP, Owen WG. Free calcium concentrations in bullfrog rods determined in the presence of multiple forms of Fura-2. Biophys J 1994; 67:2076–2089.
Fesenko EE, Kolesnikov SS, Lyubarsky AL. Induction by cyclic GMP of cationic conductance in plasma membrane of retinal rod outer segment. Nature 1985; 313:310–313.
Nakatani K, Yau K-W. Light suppressible, cyclic-GMP-sensitive conductance in the plasma membrane of a truncated rod outer segment. Nature 1985; 317:252–255.
Pugh EN Jr, Nikonov S, Lamb TD. Molecular mechanisms of vertebrate photoreceptor light adaptation. Curr Opin Neurobiol 1999; 9:410–418.
Fain GL et al. Adaptation in vertebrate photoreceptors. Physiol Rev 2001; 81:117–151.
Ebrey TG, Koutalos Y. Vertebrate Photoreceptors. Prog Retin Eye Res 2001; 20:49–94.
Polans A, Baehr W, Palczewski K. Turned on by Ca2+! The physiology and pathology of Ca2tbinding proteins in the retina. Trends Neurosci. 1996; 19:547–554.
Dizhoor AM et al. The human photoreceptor membrane guanylyl cyclase, RetGC, is present in outer segments and is regulated by calcium and a soluble activator. Neuron 1994; 12:1345–1352.
Gorczyca WA et al. Purification and physiological evaluation of a guanylate cyclase activating protein from retinal rods. Proc Natl Acad Sci USA 1994; 91:4014–4018.
Palczewski K et al. Molecular cloning and characterization of retinal photoreceptor guanylyl cyclase-activating protein. Neuron 1994; 13:395–404.
Frins S et al. Functional characterization of a guanylyl cyclase-activating protein from vertebrate rods. Cloning, heterologous expression and localization. J Biol Chem 1996; 271:8022–8027.
Kachi S et al. Detailed localization of photoreceptor guanylate cyclase activating protein-1 and -2 in mammalian retinas using light and electron microscopy. Exp Eye Res 1999; 68:465–473.
Hsu YT, Molday RS. Modulation of the cGMP-gated channel of rod photoreceptor cells by calmodulin. Nature 1993; 361:76–79.
Dodd RL. The role of arrestin and recoverin in signal transduction by retinal rod photoreceptors [PhD Thesis]. Palo Alto: Stanford University 1998.
Erickson MA et al. The effect of recombinant recoverin on the photoresponse of truncated rod photoreceptors. Proc Natl Acad Sci USA 1998; 95:6474–6479.
Kawamura S. Rhodopsin phosphorylation as a mechanism of cyclic GMP phosphodiesterase regulation by S-modulin. Nature 1993; 362:855–857.
Gorodovikova EN et al. Recoverin mediates the calcium effect upon rhodopsin phosphorylation and cGMP hydrolysis in bovine retina rod cells. FEBS Lett. 1994; 349:187–190.
Chen CK et al. Ca2+-dependent interaction of recoverin with rhodopsin kinase. J Biol Chem 1995; 270:18060–18066.
Klenchin VA, Calvert PD, Bownds MD. Inhibition of rhodopsin kinase by recoverin. Further evidence for a negative feedback system in phototransduction. J Biol Chem 1995; 270:16147–16152.
Otto-Bruc AE et al. Phosphorylation of photolyzed rhodopsin is calcium-insensitive in retina permeabilized by alpha-toxin. Proc Natl Acad Sci USA 1998; 95:15014–15019.
Matthews HR. Static and dynamic actions of cytoplasmic Ca2+ in the adaptation of responses to saturating flashes in salamander rods. J Physiol 1996; 490:1–15.
Matthews HR. Actions of Ca2+ on an early stage in phototransduction revealed by the dynamic fall in Ca2+ concentration during the bright flash response. J Gen Physiol 1997; 109:141–146.
Lagnado L, Baylor DA. Calcium controls light-triggered formation of catalytically active rhodopsin. Nature 1994; 367:273–277.
Baylor DA, Lamb TD, Yau K-W. The membrane current of single rod outer segments. J Physiol 1979; 288:589–611.
Sampath AP et al. Bleached pigment produces a maintained decrease in outer segment Ca2+ in salamander rods. J Gen Physiol 1998; 111:53–64.
Matthews HR et al. Photoreceptor adaptation is mediated by cytoplasmic calcium concentration. Nature 1998; 334:67–69.
Nakatani K, Yau K-W. Calcium and light adaptation in retinal rods and cones. Nature 1998; 334:69–71.
Koutalos Y, Nakatani K, Yau K-W. The cGMP-phosphodiesterase and its contribution to sensitivity regulation in retinal rods. J Gen Physiol 1995; 106:891–921.
Koutalos Y, Yau K-W. Characterization of guanylyl cyclase and phosphodiesterase activities in single rod outer segments. Methods Enzymol 2000; 315:742–752.
Nakatani K, Koutalos Y, Yau K-W. Ca2+-modulation of the cGMP-gated channel of bullfrog retinal rod photoreceptors. J Physiol 1995; 484:69–76.
Gordon SE, Downing-Park J, Zimmerman AL. Modulation of the cGMP-gated ion channel in frog rods by calmodulin and an endogenous inhibitory factor. J Physiol 1995; 486:533–546.
Koutalos Y et al. Characterization of guanylate cyclase activity in single rod outer segments. J Gen Physiol 1995; 106:863–890.
Lagnado L, Cervetto L, McNaughton PA. Calcium Homeostasis in the Outer Segments of Retinal Rods from the Tiger Salamander. J Physiol 1992; 455:111–142.
Mendez A et al. Role of guanylate cyclase-activating proteins (GCAPs) in setting the flash sensitivity of rod photoreceptors. Proc Natl Acad Sci USA 2001; 98:9948–9953.
Gray-Keller MP, Detwiler PB. Ca2+ dependence of dark-and light-adapted flash responses in rod photoreceptors. Neuron 1996; 17:323–331.
Pugh EN Jr, Lamb TD. Phototransduction in vertebrate rods and cones: Molecular mechanisms of amplification, recovery and light adaptation. In: Stavenga DG, DeGrip WJ, Pugh EN Jr, eds. Handbook of Biological Physics, Volume 3. Elsevier Science B.V. 2000:183–255.
Nakatani K, Chen C, Koutalos Y. Calcium diffusion coefficient in rod photoreceptor outer segments. Biophys J 2002; 82:728–739.
Baylor DA, Nunn BJ. Electrical properties of the light-sensitive conductance of rods of the salamander Ambystoma tigrinum. J Physiol 1986; 371:115–145.
Nakatani K, Tamura T, Yau K-W. Light adaptation in retinal rods of the rabbit and two other nonprimate mammals. J Gen Physiol 1991; 97:413–435.
Koutalos Y, Nakatani K, Yau K-W. Cyclic-GMP diffusion coefficient in rod photoreceptor outer segments. Biophys J 1995; 68:373–382.
Koutalos Y et al. Diffusion coefficient of the cyclic GMP analog, 8-(fluoresceinyl) thioguanosine 3’,5’-cyclic monophosphate in the salamander rod outer segment. Biophys J 1995; 69:2163–2167.
Gray-Keller M et al. Longitudinal spread of second messenger signals in isolated rod outer segments of lizards. J Physiol 1999; 519:679–692.
Koutalos Y, Yau K-W. Regulation of sensitivity in vertebrate rod photoreceptors by calcium. Trends Neurosci. 1996; 19:73–81.
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2002 Springer Science+Business Media New York
About this chapter
Cite this chapter
Nakatani, K., Chen, C., Yau, KW., Koutalos, Y. (2002). Calcium and Phototransduction. In: Baehr, W., Palczewski, K. (eds) Photoreceptors and Calcium. Advances in Experimental Medicine and Biology, vol 514. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-0121-3_1
Download citation
DOI: https://doi.org/10.1007/978-1-4615-0121-3_1
Publisher Name: Springer, Boston, MA
Print ISBN: 978-1-4613-4933-4
Online ISBN: 978-1-4615-0121-3
eBook Packages: Springer Book Archive