Does rod phototransduction involve the delayed transition of activated rhodopsin to a second, more active catalytic state?

Visual Neuroscience

Volumn 15, Issue 6, 1998, Pages 1067-1078

  Pepperberg, David R ^a  

^a UNIVERSITY OF ILLINOIS   (United States)

Author keywords

Deactivation; Photoreceptor adaptation; Phototransduction; Rhodopsin activation

Indexed keywords

RHODOPSIN;

ADAPTATION; AMPHIBIA; ANIMAL; ARTICLE; BIOLOGICAL MODEL; CATALYSIS; METABOLISM; PHOTOTRANSDUCTION; PHYSIOLOGY; RETINA ROD; TIME;

ADAPTATION, PHYSIOLOGICAL; AMPHIBIA; ANIMALS; CATALYSIS; MODELS, NEUROLOGICAL; PHOTOTRANSDUCTION; RHODOPSIN; RODS (RETINA); TIME FACTORS;

EID: 0032213182     PISSN: 09525238     EISSN: None     Source Type: Journal    
DOI: 10.1017/S0952523898156079     Document Type: Article

References (83)

1. ARNIS, S. & HOFMANN, K.P. (1993). Two different forms of metarhodopsin II: Schiff base deprotonation precedes proton uptake and signaling state. Proceedings of the National Academy of Sciences of the U.S.A. 90, 7849-7853.
2. BAYLOR, D.A. (1996). How photons start vision. Proceedings of the National Academy of Sciences of the U.S.A. 93, 560-565.
3. BAYLOR, D.A. & LAMB, T.D. (1982). Local effects of bleaching in retinal rods of the toad. Journal of Physiology 328, 49-71.
4. BAYLOR, D.A., LAMB, T.D. & YAU, K.-W. (1979a). The membrane current of single rod outer segments. Journal of Physiology 288, 589-611.
5. BAYLOR, D.A., LAMB, T.D. & YAU, K.-W. (1979b). Responses of retinal rods to single photons. Journal of Physiology 288, 613-634.
6. BAYLOR, D.A., NUNN, B.J. & SCHNAPF, J.L. (1984). The photocurrent, noise and spectral sensitivity of rods of the monkey Macaco fascicularis. Journal of Physiology 357, 575-607.
7. BENNETT, N. (1980). Optical study of the light-induced protonation changes associated with the metarhodopsin II intermediate in rod-outer-segment membranes. European Journal of Biochemistry 111, 99-103.
8. BENNETT, N. & SITARAMAYYA, A. (1988). Inactivation of photoexcited rhodopsin in retinal rods: The roles of rhodopsin kinase and 48-kDa protein. Biochemistry 27, 1710-1715.
9. BIERNBAUM. M.S. & BOWNDS, M.D. (1985). Light-induced changes in GTP and ATP in frog rod photoreceptors. Comparison with recovery of dark current and light sensitivity during dark adaptation. Journal of General Physiology 85, 107-121.
10. BOWNDS. M.D. & ARSHAVSKY, V.Y. (1995). What are the mechanisms of photoreceptor adaptation? Behavioral and Brain Sciences 18, 415-424.
11. BRUCKERT, F., VUONG, T.M. & CHABRE, M. (1988). Light and GTP dependence of transducin solubility in retinal rods. Further analysis by near infra-red light scattering. European Biophysics Journal 16, 207-218.
12. 2+-dependent interaction of recoverin with rhodopsin kinase. Journal of Biological Chemistry 270, 18060-18066.
13. CHEN, J., MARINO, C.L., PEACHEY, N.S., BAYLOR, D.A. & SIMON, M.I. (1995b). Mechanisms of rhodopsin inactivation in vivo as revealed by a COOH-terminal truncation mutant. Science 267, 374-377.
14. 296. Biochemistry 31, 12592-12601.
15. CORNWALL, M.C., FEIN, A. & wMACNICHOL, E.F., JR. (1990). Cellular mechanisms that underlie bleaching and background adaptation. Journal of General Physiology 96, 345-372.
16. CORSON, D.W., CORNWALL, M.C. & PEPPERBERG, D.R. (1994). Evidence for the prolonged photoactivated lifetime of an analogue visual pigment containing 11-cis 9-desmethylretinal. Visual Neuroscience 11, 91-98.
17. COTE, R.H., BOWNDS, M.D. & ARSHAVSKY, V.Y. (1994). cGMP binding sites on photoreceptor phosphodiesterase: Role in feedback regulation of visual transduction. Proceedings of the National Academy of Sciences of the U.S.A. 91, 4845-4849.
18. DETWILER, PB. & GRAY-KELLER, M.P (1996). The mechanisms of vertebrate light adaptation: Speeded recovery versus slowed activation. Current Opinion in Neurobiology 6, 440-444.
19. ERICKSON, M.A., LAGNADO, L., ZOZULYA, S., NEUBERT, T., STRYER, L. & BAYLOR, D.A. (1996). The effect of recoverin upon the recovery of the light response occurs at high levels of calcium. Investigative Ophthalmology and Visual Science 37, S215.
20. ERICKSON, M.A., ROBINSON, P. & LISMAN. J. (1992). Deactivation of visual transduction without guanosine triphosphate hydrolysis by G protein. Science 257, 1255-1258.
21. FAHMY, K. & SAKMAR, T.P. (1993). Regulation of the rhodopsin-transducin interaction by a highly conserved carboxylic acid group. Biochemistry 32, 7229-7236.
22. 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.
23. 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.
24. 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.
25. GRAY-KELLER, M.P. & DETWILER, P.B. (1994). The calcium feedback signal in the phototransduction cascade of vertebrate rods. Neuron 13, 849-861.
26. 2+ dependence of darkand light-adapted flash responses in rod photoreceptors. Neuron 17, 323-331.
27. HAMM, H.E. & BOWNDS, M.D. (1986). Protein complement of rod outer segments of frog retina. Biochemistry 25, 4512-4523.
28. HÁROSI, F.I. (1975). Absorption spectra and linear dichroism of some amphibian photoreceptors. Journal of General Physiology 66, 357-382.
29. HELMREICH, E.J.M. & HOFMANN, K.P. (1996). Structure and function of proteins in G-protein-coupled signal transfer. Biochimica et Biophysica Acta 1286, 285-322.
30. HODGKIN, A.L., McNAUGHTON, P.A., NUNN, B.J. & YAU, K.-W. (1984). Effect of ions on retinal rods from Bufo marinus. Journal of Physiology 350, 649-680.
31. HOFMANN, K.P., PULVERMÜLLER, A., BUCZYŁKO, J., VAN HOOSER, P. & PALCZEWSKI, K. (1992). The role of arrestin and retinoids in the regeneration pathway of rhodopsin. Journal of Biological Chemistry 267, 15701-15706.
32. JOHNSON, W.C., J R., P ALCZEWSKI, K., G ORCZYCA, W.A., R IAZANCE-LAWRENCE, J.H., W ITKOWSKA, D. & POLANS, A.S. (1997). Calcium binding to recoverin: Implications for secondary structure and membrane association. Biochimica et Biophysica Acta 1342, 164-174.
33. JONES, G.J. (1995). Light adaptation and the rising phase of the flash photocurrent of salamander retinal rods. Journal of Physiology 487, 441-451.
34. JONES, G.J., C ORNWALL, M.C. & FAIN, G.L. (1996). Equivalence of background and bleaching desensitization in isolated rod photoreceptors of the larval tiger salamander. Journal of General Physiology 108, 333-340.
35. KAHLERT, M., P EPPERBERG, D.R. & HOFMANN, K.P. (1990). Effect of bleached rhodopsin on signal amplification in rod visual receptors. Nature 345, 537-539.
36. KAWAMURA, S. (1993). Rhodopsin phosphorylation as a mechanism of cyclic GMP phosphodiesterase regulation by S-modulin. Nature 362, 855-857.
37. KLENCHIN, V.A., C ALVERT, 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.
38. KOCH, K.-W. & STRYER, L. (1988). Highly cooperative feedback control of retinal rod guanylate cyclase by calcium ions. Nature 334, 64-66.
39. KOUTALOS, Y., N AKATANI. K., T AMURA, T. & YAU, K.-W. (1995a). Characterization of guanylate cyclase activity in single retinal rod outer segments. Journal of General Physiology 106, 863-890.
40. KOUTALOS, Y., N AKATANI, K. & YAU, K.-W. (1995a). The cGMP-phosphodiesterase and its contribution to sensitivity regulation in retinal rods. Journal of General Physiology 106, 891-921.
41. KOUTALOS, Y. & YAU, K.-W. (1996). Regulation of sensitivity in vertebrate rod photoreceptors by calcium. Trends in Neuroscience 19, 73-81.
42. LAGNADO, L. & BAYLOR, D.A. (1994). Calcium controls light-triggered formation of catalytically active rhodopsin. Nature 367, 273-277.
43. LAGNADO, L., C ERVETTO, L. & MCNAUGHTON, P.A. (1992). Calcium homeostasis in the outer segments of retinal rods from the tiger salamander. Journal of Physiology 455, 111-142.
44. LAITKO, U. & HOFMANN. K.P. (1998). A model for the recovery kinetics of rod phototransduction, based on the enzymatic deactivation of rhodopsin. Biophysical Journal 74, 803-815.
45. LAMB, T.D. (1996). Gain and kinetics of activation in the G-protein cascade of phototransduction. Proceedings of the National Academy of Sciences of the U.S.A. 93, 566-570.
46. LEE, R.H., T ING, T.D., L IEBERMAN. B.S., T OBIAS, D.E., L OLLEY, R.N. & Ho, Y.-K. (1992). Regulation of retinal cGMP cascade by phosducin in bovine rod photoreceptor cells. Interaction of phosducin and transducin. Journal of Biological Chemistry 267, 25104-25112.
47. LEIBROCK, C.S. & LAMB, T.D. (1997). Effect of hydroxylamine on photonlike events during dark adaptation in toad rod photoreceptors. Journal of Physiology 501, 97-109.
48. LEWIS, J.W. & KLIGER, D.S. (1992), Photointermediates of visual pigments. Journal of Bioenergetics and Biomembranes 24, 201-210.
49. LIEBMAN, P.A., M UELLER, P. & PUGH, E.N., J R. (1984). Protons suppress the dark current of frog retinal rods. Journal of Physiology 347, 85-110.
50. 2+. Journal of General Physiology 107, 19-34.
51. 2+ in the adaptation of responses to saturating flashes in salamander rods. Journal of Physiology 490, 1-15.
52. 2+ concentration during the bright flash response. Journal of General Physiology 109, 141-146.
53. MATTHEWS, H.R., M URPHY, R.L.W., F AIN, G.L. & LAMB, T.D. (1988). Photoreceptor light adaptation is mediated by cytoplasmic calcium concentration. Nature 334, 67-69.
54. MCCARTHY, S.T., Y OUNGER, J.P. & OWEN, W.G. (1996). Dynamic, spatially nonuniform calcium regulation in frog rods exposed to light. Journal of Neurophysiology 76, 1991-2004.
55. MELIA, T.J., C OWAN, C.W., A NGLESON, 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.
56. MILLER, D.L. & KORENBROT, J.I. (1987). Kinetics of light-dependent Ca fluxes across the plasma membrane of rod outer segments. A dynamic model of the regulation of the cytoplasmic Ca concentration. Journal of General Physiology 90, 397-425.
57. MILLER, J.L., F ox, D.A. & LITMAN, B.J. (1986). Amplification of phosphodiesterase activation is greatly reduced by rhodopsin phosphorylation. Biochemistry 25, 4983-4988.
58. MORRISON, D.F., T ING, T.D., V ALLURY, V., H o, Y.-K., C ROUCH, R.K., C ORSON, D.W., M ANGINI, N.J. & PEPPERBERG, D.R. (1995). Reduced light-dependent phosphorylation of an analog visual pigment containing 9-demethylretinal as its chromophore. Journal of Biological Chemistry 270, 6718-6721.
59. 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.
60. NAKATANI, K. & YAU, K.-W. (1988). Calcium and light adaptation in retinal rods and cones. Nature 334, 69-71.
61. NIKONOV, S., E NGHETA, N. & PUGH, E.N., J R. (1998). Kinetics of recovery of the dark-adapted salamander rod photoresponse. Journal of General Physiology 111, 7-37.
62. OHGURO, H., V AN HOOSER, J.P., M ILAM, A.H. & PALCZEWSKI, K. (1996). Rhodopsin phosphorylation and dephosphorylation in vivo. Journal of Biological Chemistry 270, 14259-14262.
63. PALCZEWSKI, K., J ÄGER, S., B UCZYŁKO. J., C ROUCH, R.K., B REDBERG, D.L., H OFMANN, K.P., A SSON-BATRES, M.A. & SAARI, J.C. (1994). Rod outer segment retinol dehydrogenase: Substrate specificity and role in phototransduction. Biochemistry 33, 33741-13750.
64. PEPPERBERG, D.R., B ROWN, P.K., L URIE, M. & DOWLING, J.E. (1978). Visual pigment and photoreceptor sensitivity in the isolated skate retina. Journal of General Physiology 71, 369-396.
65. PEPPERBERG, D.R., C ORNWALL, M.C., K AHLERT, M., H OFMANN, K.P., J IN, J., J ONES, G.J. & RIPPS, H. (1992). Light-dependent delay in the falling phase of the retinal rod photoresponse. Visual Neuroscience 8, 9-18.
66. PEPPERBERG, D.R., J IN. J. & JONES, G.J. (1994). Modulation of transduction gain in light adaptation of retinal rods. Visual Neuroscience 11, 53-62.
67. PEPPERBERG, D.R., K AHLERT, M., K RAUSE, A. & HOFMANN, K.P. (1988). Photic modulation of a highly sensitive, near-infrared light-scattering signal recorded from intact retinal photoreceptors. Proceedings of the National Academy of Sciences of the U.S.A. 85, 5531-5535.
68. PUGH, E.N., J R., & LAMB, T.D. (1993). Amplification and kinetics of the activation steps in phototransduction. Biochimica et Biophysica Acta 1141, 111-149.
69. PULVERMÜLLER, A., P ALCZEWSKI, K. & HOFMANN, K.P. (1993). Interaction between photoactivated rhodopsin and its kinase: Stability and kinetics of complex formation. Biochemistry 32, 14082-14088.
70. 44, with rhodopsin. Biochemistry 36, 9253-9260.
71. ROBINSON, W.E. & HAGINS, W.A. (1979). GTP hydrolysis in intact rod outer segments and the transmitter cycle in visual excitation. Nature 280, 398-400.
72. ROOF, D.J., K ORENBROT, J.I. & HEUSER. J.E. (1982). Surfaces of rod photoreceptor disk membranes: Light-activated enzymes. Journal of Cell Biology 95, 501-509.
73. SAGOO, M.S. & LAGNADO, L. (1997a). G-protein deactivation is ratelimiting for shut-off of the phototransduction cascade. Nature 389, 392-395.
74. 2+ increases the apparent affinity of transducin for GTP. Investigative Ophthalmology and Visual Science 38, S614.
75. 2+ in salamander rods. Journal of General Physiology 111, 53-64.
76. SCHNEEWEIS, D.M. & SCHNAPF, J.L. (1995). Photovoltage of rods and cones in the macaque retina. Science 268, 1053-1056.
77. STRAUME, M., M ITCHELL, D.C., M ILLER, J.L. & LITMAN, B.J. (1990). Interconversion of metarhodopsins I and II: A branched photointermediate decay model. Biochemistry 29, 9135-9142.
78. TORRE, V., M ATTHEWS, 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.
79. TRANCHTNA, D. (1998). The calculus of rod phototransduction. Journal of General Physiology 111, 3-6.
80. TSUBOK S., M ATSUMOTO, H. & YAMAZAKI. A. (1994). Phosphorylation of an inhibitory subunit of cGMP phosphodiesterase in Rana catesbiana rod photoreceptors. II. A possible mechanism for the turnoff of cGMP phosphodiesterase without GTP hydrolysis. Journal of Biological Chemistry 269, 15024-15029.
81. WILDEN, U., H ALL, S.W. & KUHN, H. (1986). Phosphodiesterase activation by photoexcited rhodopsin is quenched when rhodopsin is phosphorylated and binds the intrinsic 48-kDa protein of rod outer segments. Proceedings of the National Academy of Sciences of the U.S.A. 83, 1174-1178.
82. Xu, J., D ODD, R.L., M AKING. C.L., S IMON, M.I., B AYLOR, D.A. & CHEN, J. (1997). Prolonged photoresponses in transgenic mouse rods lacking arrestin. Nature 389, 505-509.
83. YOUNGER, J.P., M CCARTHY, S.T. & OWEN, W.G. (1996). Light-dependent control of calcium in intact rods of the bullfrog Rana catesbeiana. Journal of Neurophysiology 75, 354-366.