Hostname: page-component-78c5997874-t5tsf Total loading time: 0 Render date: 2024-11-04T21:17:39.611Z Has data issue: false hasContentIssue false
  • English
  • Français

Toward a unified model of vertebrate rod phototransduction

Published online by Cambridge University Press:  06 October 2005

R.D. HAMER ,
S.C. NICHOLAS ,
D. TRANCHINA ,
T.D. LAMB  and
J.L.P. JARVINEN
R.D. HAMER
Affiliation:
Smith-Kettlewell Eye Research Institute, San Francisco
S.C. NICHOLAS
Affiliation:
Smith-Kettlewell Eye Research Institute, San Francisco
D. TRANCHINA
Affiliation:
Department of Biology and Courant Institute of Mathematical Sciences, New York University, New York
T.D. LAMB
Affiliation:
JCSMR, Australian National University, Canberra, Australia Physiological Laboratory, University of Cambridge, Cambridge, UK
J.L.P. JARVINEN
Affiliation:
JCSMR, Australian National University, Canberra, Australia Physiological Laboratory, University of Cambridge, Cambridge, UK
Get access Rights & Permissions [Opens in a new window]

Abstract

Recently, we introduced a phototransduction model that was able to account for the reproducibility of vertebrate rod single-photon responses (SPRs) (Hamer et al., 2003). The model was able to reproduce SPR statistics by means of stochastic activation and inactivation of rhodopsin (R*), transducin (Gα), and phosphodiesterase (PDE). The features needed to capture the SPR statistics were (1) multiple steps of R* inactivation by means of multiple phosphorylations (followed by arrestin capping) and (2) phosphorylation dependence of the affinity between R* and the three molecules competing to bind with R* (Gα, arrestin, and rhodopsin kinase). The model was also able to account for several other rod response features in the dim-flash regime, including SPRs obtained from rods in which various elements of the cascade have been genetically disabled or disrupted. However, the model was not tested under high light-level conditions. We sought to evaluate the extent to which the multiple phosphorylation model could simultaneously account for single-photon response behavior, as well as responses to high light levels causing complete response saturation and/or significant light adaptation (LA). To date no single model, with one set of parameters, has been able to do this. Dim-flash responses and statistics were simulated using a hybrid stochastic/deterministic model and Monte-Carlo methods as in Hamer et al. (2003). A dark-adapted flash series, and stimulus paradigms from the literature eliciting various degrees of light adaptation (LA), were simulated using a full differential equation version of the model that included the addition of Ca2+-feedback onto rhodopsin kinase via recoverin. With this model, using a single set of parameters, we attempted to account for (1) SPR waveforms and statistics (as in Hamer et al., 2003); (2) a full dark-adapted flash-response series, from dim flash to saturating, bright flash levels, from a toad rod; (3) steady-state LA responses, including LA circulating current (as in Koutalos et al., 1995) and LA flash sensitivity measured in rods from four species; (4) step responses from newt rods (Forti et al., 1989) over a large dynamic range; (5) dynamic LA responses, such as the step-flash paradigm of Fain et al. (1989), and the two-flash paradigm of Murnick and Lamb (1996); and (6) the salient response features from four knockout rod preparations. The model was able to meet this stringent test, accounting for almost all the salient qualitative, and many quantitative features, of the responses across this broad array of stimulus conditions, including SPR reproducibility. The model promises to be useful in testing hypotheses regarding both normal and abnormal photoreceptor function, and is a good starting point for development of a full-range model of cone phototransduction. Informative limitations of the model are also discussed.

Keywords

Full-range phototransduction modelSingle-photon reproducibilityStochastic simulationLight adaptationPhototransductionRod responses
Type
Research Article
Information
Visual Neuroscience , Volume 22 , Issue 4 , July 2005 , pp. 417 - 436
Copyright
2005 Cambridge University Press

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

Ames, J.B., Porumb, T., Tanaka, T., Ikura, M., & Stryer, L. (1995). Amino-terminal myristoylation induces cooperative calcium binding to recoverin. Journal of Biological Chemistry 270, 4526–4533.Google Scholar
Ames, J.B., Ishima, R., Tanaka, T., Gordon, J.I., Stryer, L., & Ikura, M. (1997). Molecular mechanics of calcium-myristoyl switches. Nature 389, 198–202.Google Scholar
Aton, B.R., Litman, B.J., & Jackson, M.L. (1984). Isolation and identification of the phosphorylated species of rhodopsin. Biochemistry 23, 1737–1741.Google Scholar
Baylor, D.A., Hodgkin, A.L., & Lamb, T.D. (1974). The electrical response of turtle cones to flashes and steps of light. Journal of Physiology 242, 685–727.Google Scholar
Baylor, D.A., Lamb, T.D., & Yau, K.W. (1979). Responses of retinal rods to single photons. Journal of Physiology 288, 613–634.Google Scholar
Buczylko, J., Gutmann, C., & Palczewski, K. (1991). Regulation of rhodopsin kinase by autophosphorylation. Proceedings of the National Academy of Sciences of the U.S.A. 88, 2568–2572.Google Scholar
Burns, M.E., Mendez, A., Chen, J., & Baylor, D.A. (2002). Dynamics of cyclic GMP synthesis in retinal rods. Neuron 36, 81–91.Google Scholar
Chen, C.K., Burns, M.E., He, W., Wensel, T.G., Baylor, D.A., & Simon, M.I. (2000). Slowed recovery of rod photoresponse in mice lacking the GTPase accelerating protein RGS9-1. Nature 403, 557–560.Google Scholar
Chen, C.K., Burns, M.E., Spencer, M., Niemi, G.A., Chen, J., Hurley, J.B., Baylor, D.A., & Simon, M.I. (1999). Abnormal photoresponses and light-induced apoptosis in rods lacking rhodopsin kinase. Proceedings of the National Academy of Sciences of the U.S.A. 96, 3718–3722.Google Scholar
Chen, C.K., Inglese, J., Lefkowitz, R.J., & Hurley, J.B. (1995). Ca2+-dependent interaction of recoverin with rhodopsin kinase. Journal of Biological Chemistry 270, 18060–18066.Google Scholar
Cone, R.A. & Cobbs, W.H., III (1969). Rhodopsin cycle in the living eye of the rat. Nature 221, 820–822.Google Scholar
Cornwall, M.C. & Fain, G.L. (1994). Bleached pigment activates transduction in isolated rods of the salamander retina. Journal of Physiology 480 (Pt. 2), 261–279.Google Scholar
Cornwall, M.C., Jones, G.J., Kefalov, V.J., Fain, G.L., & Matthews, H.R. (2000). Electrophysiological methods for measurement of activation of phototransduction by bleached visual pigment in salamander photoreceptors. Methods in Enzymology 316, 224–252.Google Scholar
Cornwall, M.C., Matthews, H.R., Crouch, R.K., & Fain, G.L. (1995). Bleached pigment activates transduction in salamander cones. Journal of General Physiology 106, 543–557.Google Scholar
Del Castillo, J. & Katz, B. (1954). Quantal components of the end-plate potential. Journal of Physiology 124, 560–573.Google Scholar
Dodd, R.L. (1998). The role of arrestin and recoverin in signal transduction by retinal rod photoreceptors. Thesis. Stanford, CA: Stanford University.
Ebrey, T.G. (1968). The thermal decay of the intermediates of rhodopsin in situ. Vision Research 8, 965–982.Google Scholar
Fain, G.L., Lamb, T.D., Matthews, H.R., & Murphy, R.L.W. (1989). Cytoplasmic calcium as the messenger for light adaptation in salamander rods. Journal of Physiology 416, 215–243.Google Scholar
Fain, G.L. & Lisman, J.E. (1993). Photoreceptor degeneration in vitamin A deprivation and retinitis pigmentosa: The equivalent light hypothesis. Experimental Eye Research 57, 335–340.Google Scholar
Fain, G.L., Matthews, H.R., Cornwall, M.C., & Koutalos, Y. (2001). Adaptation in vertebrate photoreceptors. Physiological Review 81, 117–151.Google Scholar
Felber, S., Breuer, H.P., Petruccione, F., Honerkamp, J., & Hofmann, K.P. (1996). Stochastic simulation of the transducin GTPase cycle. Biophysical Journal 71, 3051–3063.Google Scholar
Field, G.D. & Rieke, F. (2002). Mechanisms regulating variability of the single photon responses of mammalian rod photoreceptors. Neuron 35, 733–747.Google Scholar
Findlay, J.B., Barclay, P.L., Brett, M., Davison, M., Pappin, D.J., & Thompson, P. (1984). The structure of mammalian rod opsins. Vision Research 24, 1501–1508.Google Scholar
Firsov, M.L., Kolesnikov, A.V., Golobokova, E.Y., & Govardovskii, V.I. (2005). Two realms of dark adaptation. Vision Research 45, 147–151.Google Scholar
Forti, S., Menini, A., Rispoli, G., & Torre, V. (1989). Kinetics of phototransduction in retinal rods of the newt Triturus cristatus. Journal of Physiology 419, 265–295.Google Scholar
Gibson, S.K., Parkes, J.H., & Liebman, P.A. (2000). Phosphorylation modulates the affinity of light-activated rhodopsin for G protein and arrestin. Biochemistry 39, 5738–5749.Google Scholar
Gillespie, D.T. (1976). A General method for numerically simulating the stochastic time evolution of coupled chemical reactions. Journal of Computational Physics 22, 403–434.Google Scholar
Gillespie, D.T. (1977). Exact stochastic simulation of coupled chemical reactions. Journal of Physical Chemistry 81, 2340–2361.Google Scholar
Gorczyca, W.A., Gray-Keller, M.P., Detwiler, P.B., & Palczewski, K. (1994). Purification and physiological evaluation of a guanylate cyclase activating protein from retinal rods. Proceedings of the National Academy of Sciences of the U.S.A. 91, 4014–4018.Google Scholar
Gorodovikova, E.N. & Philippov, P.P. (1993). The presence of a calcium-sensitive p26-containing complex in bovine retina rod cells. FEBS Letters 335, 277–279.Google Scholar
Granzin, J., Wilden, U., Choe, H.W., Labahn, J., Krafft, B., & Buldt, G. (1998). X-ray crystal structure of arrestin from bovine rod outer segments. Nature 391, 918–921.Google Scholar
Gray-Keller, M.P. & Detwiler, P.B. (1994). The calcium feedback signal in the phototransduction cascade of vertebrate rods. Neuron 13, 849–861.Google Scholar
Hamer, R.D. (2000a). Analysis of Ca2+-dependent gain changes in PDE activation in vertebrate rod phototransduction. Molecular Vision 6, 265–286.Google Scholar
Hamer, R.D. (2000b). Computational analysis of vertebrate phototransduction: Combined quantitative and qualitative modeling of dark- and light-adapted responses in amphibian rods. Visual Neuroscience 17, 679–699.Google Scholar
Hamer, R.D., Nicholas, S.C., Tranchina, D., Liebman, P.A., & Lamb, T.D. (2003). Multiple steps of phosphorylation of activated rhodopsin can account for the reproducibility of vertebrate rod single-photon responses. Journal of General Physiology 122, 419–444.Google Scholar
Hamm, H.E. & Bownds, M.D. (1986). Protein complement of rod outer segments of frog retina. Biochemistry 25, 4512–4523.Google Scholar
He, W. & Wensel, T.G. (2002). RGS function in visual signal transduction. Methods in Enzymology 344, 724–740.Google Scholar
Hirsch, J.A., Schubert, C., Gurevich, V.V., & Sigler, P.B. (1999). The 2.8 A crystal structure of visual arrestin: A model for arrestin's regulation. Cell 97, 257–269.Google Scholar
Hsu, Y.T. & Molday, R.S. (1993). Modulation of the cGMP-gated channel of rod photoreceptor cells by calmodulin. Nature 361, 76–79.Google Scholar
Kawamura, S. (1993). Rhodopsin phosphorylation as a mechanism of cyclic GMP phosphodiesterase regulation by S-modulin. Nature 362, 855–857.Google Scholar
Kawamura, S., Hisatomi, O., Kayada, S., Tokunaga, F., & Kuo, C.H. (1993). Recoverin has S-modulin activity in frog rods. Journal of Biological Chemistry 268, 14579–14582.Google Scholar
Kawamura, S. & Murakami, M. (1991). Calcium-dependent regulation of cyclic GMP phosphodiesterase by a protein from frog retinal rods. Nature 349, 420–423.Google Scholar
Kennedy, M.J., Lee, K.A., Niemi, G.A., Craven, K.B., Garwin, G.G., Saari, J.C., & Hurley, J.B. (2001). Multiple phosphorylation of rhodopsin and the in vivo chemistry underlying rod photoreceptor dark adaptation. Neuron 31, 87–101.Google Scholar
Keresztes, G., Martemyanov, K.A., Krispel, C.M., Mutai, H., Yoo, P.J., Maison, S.F., Burns, M.E., Arshavsky, V.Y., & Heller, S. (2004). Absence of the RGS9.Gbeta5 GTPase-activating complex in photoreceptors of the R9AP knockout mouse. Journal of Biological Chemistry 279, 1581–1584.Google Scholar
Klenchin, V.A., Calvert, P.D., & Bownds, M.D. (1995). Inhibition of rhodopsin kinase by recoverin. Further evidence for a negative feedback system in phototransduction. Journal of Biological Chemistry 270, 16147–16152.Google Scholar
Koch, K.W. & Stryer, L. (1988). Highly cooperative feedback control of retinal rod guanylate cyclase by calcium ions. Nature 334, 64–66.Google Scholar
Korenbrot, J.I. & Miller, D.L. (1989). Cytoplasmic free calcium in dark-adapted retinal rod outer segments. Vision Research 29, 939–948.Google Scholar
Koutalos, Y., Nakatani, K., & Yau, K.W. (1995). The cGMP-phosphodiesterase and its contribution to sensitivity regulation in retinal rods. Journal of General Physiology 106, 891–921.Google Scholar
Krispel, C.M., Chen, C.K., Simon, M.I., & Burns, M.E. (2003). Prolonged photoresponses and defective adaptation in rods of Gbeta5−/− mice. Journal of Neuroscience 23, 6965–6971.Google Scholar
Krupnick, J.G., Gurevich, V.V., & Benovic, J.L. (1997). Mechanism of quenching of phototransduction. Binding competition between arrestin and transducin for phosphorhodopsin. Journal of Biological Chemistry 272, 18125–18131.Google Scholar
Kühn, H. & Wilden, U. (1982). Assay of phosphorylation of rhodopsin in vitro and in vivo. Methods in Enzymology 81, 489–496.Google Scholar
Lagnado, L., Cervetto, L., & McNaughton, P.A. (1992). Calcium homeostasis in the outer segments of retinal rods from the tiger salamander. Journal of Physiology 455, 111–142.Google Scholar
Lamb, T.D. (1981). The involvement of rod photoreceptors in dark adaptation. Vision Research 21, 1771–1782.Google Scholar
Lamb, T.D., Matthews, H.R., & Torre, V. (1986). Incorporation of calcium buffers into salamander retinal rods: A rejection of the calcium hypothesis of phototransduction. Journal of Physiology 372, 315–349.Google Scholar
Lamb, T.D., McNaughton, P.A., & Yau, K.W. (1981). Spatial spread of activation and background desensitization in toad rod outer segments. Journal of Physiology 319, 463–496.Google Scholar
Lamb, T.D. & Pugh, E.N., Jr. (1992). G-protein cascades: Gain and kinetics. Trends in Neuroscience 15, 291–298.Google Scholar
Leibrock, C.S., Reuter, T., & Lamb, T.D. (1994). Dark adaptation of toad rod photoreceptors. Vision Research 34, 2787–2800.Google Scholar
Leibrock, C.S., Reuter, T., & Lamb, T.D. (1998). Molecular basis of dark adaptation in rod photoreceptors. Eye 12, 511–520.Google Scholar
Leskov, I.B., Klenchin, V.A., Handy, J.W., Whitlock, G.G., Govardovskii, V.I., Bownds, M.D., Lamb, T.D., Pugh, E.N., Jr., & Arshavsky, V.Y. (2000). The gain of rod phototransduction: Reconciliation of biochemical and electrophysiological measurements. Neuron 27, 525–537.Google Scholar
Lishko, P.V., Martemyanov, K.A., Hopp, J.A., & Arshavsky, V.Y. (2002). Specific binding of RGS9-Gbeta 5L to protein anchor in photoreceptor membranes greatly enhances its catalytic activity. Journal of Biological Chemistry 277, 24376–24381.Google Scholar
Makino, C.L., Dodd, R.L., Chen, J., Burns, M.E., Roca, A., Simon, M.I., & Baylor, D.A. (2004). Recoverin regulates light-dependent phosphodiesterase activity in retinal rods. Journal of General Physiology 123, 729–741.Google Scholar
Martemyanov, K.A. & Arshavsky, V.Y. (2002). Noncatalytic domains of RGS9-1.Gbeta 5L play a decisive role in establishing its substrate specificity. Journal of Biological Chemistry 277, 32843–32848.Google Scholar
Martemyanov, K.A., Lishko, P.V., Calero, N., Keresztes, G., Sokolov, M., Strissel, K.J., Leskov, I.B., Hopp, J.A., Kolesnikov, A.V., Chen, C.K., Lem, J., Heller, S., Burns, M.E., & Arshavsky, V.Y. (2003). The DEP domain determines subcellular targeting of the GTPase activating protein RGS9 in vivo. Journal of Neuroscience 23, 10175–10181.Google Scholar
Matthews, H.R. (1991). Incorporation of chelator into guinea-pig rods shows that calcium mediates mammalian photoreceptor light adaptation. Journal of Physiology 436, 93–105.Google Scholar
Matthews, H.R. (1995). Effects of lowered cytoplasmic calcium concentration and light on the responses of salamander rod photoreceptors. Journal of Physiology 484 (Pt. 2), 267–286.Google Scholar
Matthews, H.R. (1996). Static and dynamic actions of cytoplasmic Ca2+ in the adaptation of responses to saturating flashes in salamander rods. Journal of Physiology 490, 1–5.Google Scholar
Matthews, H.R., Murphy, R.L., Fain, G.L., & Lamb, T.D. (1988). Photoreceptor light adaptation is mediated by cytoplasmic calcium concentration. Nature 334, 67–69.Google Scholar
McCarthy, S.T., Younger, R.L., & Owen, W.G. (1994). Free calcium concentrations in bullfrog rods determined in the presence of multiple forms of Fura-2. Biophysical Journal 67, 2076–2089.Google Scholar
Melia, T.J., Jr., Cowan, C.W., Angleson, J.K., & Wensel, T.G.. (1997). A comparison of the efficiency of G protein activation by ligand-free and light-activated forms of rhodopsin. Biophysical Journal 73, 3182–3191.Google Scholar
Mendez, A., Burns, M.E., Roca, A., Lem, J., Wu, L.W., Simon, M.I., Baylor, D.A., & Chen, J. (2000). Rapid and reproducible deactivation of rhodopsin requires multiple phosphorylation sites. Neuron 28, 153–164.Google Scholar
Miller, J.L. & Dratz, E.A. (1984). Phosphorylation at sites near rhodopsin's carboxyl-terminus regulates light initiated cGMP hydrolysis. Vision Research 24, 1509–1521.Google Scholar
Murnick, J.G. & Lamb, T.D. (1996). Kinetics of desensitization induced by saturating flashes in toad and salamander rods. Journal of Physiology 495, 1–13.Google Scholar
Nakatani, K. & Yau, K.W. (1988). Calcium and magnesium fluxes across the plasma membrane of the toad rod outer segment. Journal of Physiology 395, 695–729.Google Scholar
Nikonov, S., Engheta, N., & Pugh, E.N., Jr. (1998). Kinetics of recovery of the dark-adapted salamander rod photoresponse. Journal of General Physiology 111, 7–37.Google Scholar
Nikonov, S., Lamb, T.D., & Pugh, E.N., Jr. (2000). The role of steady phosphodiesterase activity in the kinetics and sensitivity of the light-adapted salamander rod photoresponse. Journal of General Physiology 116, 795–824.Google Scholar
Ohguro, H., Palczewski, K., Ericsson, L.H., Walsh, K.A., & Johnson, R.S. (1993). Sequential phosphorylation of rhodopsin at multiple sites. Biochemistry 32, 5718–5724.Google Scholar
Ohguro, H., Johnson, R.S., Ericsson, L.H., Walsh, K.A., & Palczewski, K. (1994). Control of rhodopsin multiple phosphorylation. Biochemistry 33, 1023–1028.Google Scholar
Ohguro, H., Van Hooser, J.P., Milam, A.H., & Palczewski, K. (1995). Rhodopsin phosphorylation and dephosphorylation in vivo. Journal of Biological Chemistry 270, 14259–14262.Google Scholar
Ohguro, H., Rudnicka-Nawrot, M., Buczylko, J., Zhao, X., Taylor, J.A., Walsh, K.A., & Palczewski, K. (1996). Structural and enzymatic aspects of rhodopsin phosphorylation. Journal of Biological Chemistry 271, 5215–5224.Google Scholar
Ohyama, T., Hackos, D.H., Frings, S., Hagen, V., Kaupp, U.B., & Korenbrot, J.I. (2000). Fraction of the dark current carried by Ca2+ through cGMP-gated ion channels of intact rod and cone photoreceptors. Journal of General Physiology 116, 735–754.Google Scholar
Palczewski, K., Buczylko, J., Kaplan, M.W., Polans, A.S., & Crabb, J.W. (1991). Mechanism of rhodopsin kinase activation. Journal of Biological Chemistry 266, 12949–12955.Google Scholar
Pepperberg, D.R., Cornwall, M.C., Kahlert, M., Hofmann, K.P., Jin, J., Jones, G.J., & Ripps, H. (1992). Light-dependent delay in the falling phase of the retinal rod photoresponse. Visual Neuroscience 8, 9–18.Google Scholar
Pepperberg, D.R., Jin, J., & Jones, G.J. (1994). Modulation of transduction gain in light adaptation of retinal rods. Visual Neuroscience 11, 53–62.Google Scholar
Pfister, C., Kühn, H., & Chabre, M. (1983). Interaction between photoexcited rhodopsin and peripheral enzymes in frog retinal rods. Influence on the postmetarhodopsin II decay and phosphorylation rate of rhodopsin. European Journal of Biochemistry 136, 489–499.Google Scholar
Pugh, E.N., Jr. (1999). Variability in single photon responses: A cut in the Gordian knot of rod phototransduction? Neuron 23, 205–208.Google Scholar
Pugh, E.N., Jr. & Lamb, T.D. (1990). Cyclic GMP and calcium: The internal messengers of excitation and adaptation in vertebrate photoreceptors. Vision Research 30, 1923–1948.Google Scholar
Pugh, E.N., Jr. & Lamb, T.D. (1993). Amplification and kinetics of the activation steps in phototransduction. Biochimica et Biophysica Acta 1141, 111–149.Google Scholar
Pugh, E.N., Jr. & Lamb, T.D. (2000). Phototransduction in vertebrate rods and cones: molecular mechanisms of amplification, recovery and light-adaptation. In Handbook of Biological Physics, Volume 3, Molecular Mechanisms of Visual Transduction, ed. Stavenga, D.G., de Grip, W.J., Pugh & E.N., Jr., pp. 183–255. Amsterdam, Netherlands: Elsevier Science B.V.
Pulvermuller, A., Palczewski, K., & Hofmann, K.P. (1993). Interaction between photoactivated rhodopsin and its kinase: Stability and kinetics of complex formation. Biochemistry 32, 14082–14088.Google Scholar
Rieke, F. & Baylor, D.A. (1996). Molecular origin of continuous dark noise in rod photoreceptors. Biophysical Journal 71, 2553–2572.Google Scholar
Rieke, F. & Baylor, D.A. (1998a). Origin of reproducibility in the responses of retinal rods to single photons. Biophysical Journal 75, 1836–1857.Google Scholar
Rieke, F.B. & Baylor, D.A. (1998b). Single-photon detection by rod cells of the retina. Reviews of Modern Physics 70, 1027–1036.Google Scholar
Rodieck, R.W. (1998). The First Steps in Seeing. Sunderland, Massachusetts: Sinauer Associates, Inc.
Sampath, A.P., Matthews, H.R., Cornwall, M.C., & Fain, G.L. (1998). Bleached pigment produces a maintained decrease in outer segment Ca2+ in salamander rods. Journal of General Physiology 111, 53–64.Google Scholar
Schnapf, J.L. (1983). Dependence of the single photon response on longitudinal position of absorption in toad rod outer segments. Journal of Physiology 343, 147–159.Google Scholar
Schneeweis, D.W. & Schnapf, J.L. (1995). Photovoltage of rods and cones in the macaque retina. Science 268, 1053–1056.Google Scholar
Schroder, K., Pulvermuller, A., & Hofmann, K.P. (2002). Arrestin and its splice variant Arr1-370A (p44). Mechanism and biological role of their interaction with rhodopsin. Journal of Biological Chemistry 277, 43987–43996.Google Scholar
Skiba, N.P., Martemyanov, K.A., Elfenbein, A., Hopp, J.A., Bohm, A., Simonds, W.F., & Arshavsky, V.Y. (2001). RGS9-G beta 5 substrate selectivity in photoreceptors. Opposing effects of constituent domains yield high affinity of RGS interaction with the G protein-effector complex. Journal of Biological Chemistry 276, 37365–37372.Google Scholar
Tamura, T., Nakatani, K., & Yau, K.W. (1991). Calcium feedback and sensitivity regulation in primate rods. Journal of General Physiology 98, 95–130.Google Scholar
Thompson, P. & Findlay, J.B. (1984). Phosphorylation of ovine rhodopsin. Identification of the phosphorylated sites. Biochemical Journal 220, 773–780.Google Scholar
Torre, V., Matthews, H.R., & Lamb, T.D. (1986). Role of calcium in regulating the cyclic GMP cascade of phototransduction in retinal rods. Proceedings of the National Academy of Sciences of the U.S.A. 83, 7109–7113.Google Scholar
Whitlock, G.G. & Lamb, T.D. (1999). Variability in the time course of single photon responses from toad rods: Termination of rhodopsin's activity. Neuron 23, 337–351.Google Scholar
Wilden, U. (1995). Duration and amplitude of the light-induced cGMP hydrolysis in vertebrate photoreceptors are regulated by multiple phosphorylation of rhodopsin and by arrestin binding. Biochemistry 34, 1446–1454.Google Scholar
Wilden, U. & Kühn, H. (1982). Light-dependent phosphorylation of rhodopsin: Number of phosphorylation sites. Biochemistry 21, 3014–3022.Google Scholar
Xu, J., Dodd, R.L., Makino, C.L., Simon, M.I., Baylor, D.A., & Chen, J. (1997). Prolonged photoresponses in transgenic mouse rods lacking arrestin. Nature 389, 505–509.Google Scholar
Yau, K.W. (1994). Phototransduction mechanism in retinal rods and cones. The Friedenwald Lecture. Investigative Ophthalmology and Visual Science 35, 9–32.Google Scholar