Origin of reproducibility in the responses of retinal rods to single photons

Biophysical Journal

Volumn 75, Issue 4, 1998, Pages 1836-1857

  Rieke, F ^a,b   Baylor, D A ^b  

^a UNIVERSITY OF WASHINGTON   (United States)

^b STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC GMP; RHODOPSIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CATALYSIS; CORRELATION FUNCTION; FEEDBACK SYSTEM; MATHEMATICAL ANALYSIS; MOLECULAR DYNAMICS; NONHUMAN; PHOSPHORYLATION; PHOTON ABSORPTIOMETRY; REPRODUCIBILITY; RETINA ROD; SIGNAL TRANSDUCTION; STOCHASTIC MODEL; TOAD;

ANIMALIA; ANURA;

EID: 0031666785     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(98)77625-8     Document Type: Article

References (51)

1. Aho, A.-C., K. Donner, C. Hydèn, L. O. Larsen, and T. Reuter. 1988. Low retinal noise in animals with low body temperature allows high visual sensitivity. Nature. 334:348-350.
2. Altenbach, C., K. Yang, D. L. Farrens, Z. T. Farahbakhsh, H. G. Khorana, and W. L. Hubbell. 1996. Structural features and light-dependent changes in the cytoplasmic interhelical E-F loop region of rhodopsin: a site-directed spin-labeling study. Biochemistry. 35:12470-12478.
3. Arshavsky, V. Yu., and M. D. Bownds. 1992. Regulation of deactivation of photoreceptor G protein by its target enzyme and cGMP. Nature. 357: 416-417.
4. Baylor, D. A., T. D. Lamb, and K.-W. Yau. 1979a. The membrane current of single rod outer segments. J. Physiol. (Lond.). 288:589-611.
5. Baylor, D. A., T. D. Lamb, and K.-W. Yau. 1979b. Responses of retinal rods to single photons. J. Physiol. (Lond.). 288:613-634.
6. Baylor, D. A., G. Matthews, and K.-W. Yau. 1980. Two components of electrical dark noise in toad retinal rod outer segments. J. Physiol. (Lond.). 309:591-621.
7. Baylor, D. A., B. J. Nunn, and J. L. Schnapf. 1984. The photocurrent, noise and spectral sensitivity of rods of the monkey Macaca fascicularis. J. Physiol. (Lond.). 357:575-607.
8. Bennett, N., and A. Sitaramayya. 1988. Inactivation of photoexcited rhodopsin in retinal rods: the roles of rhodopsin kinase and 48-kDa protein (arrestin). Biochemistry. 27:1710-1715.
9. Bialek, W., and W. G. Owen. 1990. Temporal filtering in retinal bipolar cells: elements of an optimal computation? Biophys. J. 58:1227-1233.
10. Cervetto, L., L. Lagnado, R. J. Perry, D. W. Robinson, and P. A. McNaughton. 1989. Extrusion of calcium from rod outer segments is driven by both sodium and potassium gradients. Nature. 337:740-743.
11. Chen, J., C. L. Makino, N. S. Peachey, D. A. Baylor, and M. I. Simon. 1995. Mechanisms of rhodopsin inactivation in vivo as revealed by a COOH-terminal truncation mutant. Science. 267:374-377.
12. Corson, D. W., M. C. Cornwall, and D. R. Pepperberg. 1994. Evidence for the prolonged photoactivated lifetime of an analogue visual pigment containing 11-cis-9-desmethylretinal. Vis. Neurosci. 11:91-98.
13. Erickson, M. A., L. Lagnado, S. Zozulya, T. A. Neubert, L. Stryer, and D. A. Baylor. 1998. The effect of recombinant recoverin on the photo-response of truncated rod photoreceptors. Proc. Natl. Acad. Sci. USA. 95:6474-6479.
14. Farahbakhsh, Z. T., K. D. Ridge, H. G. Khorana, and W. L. Hubbell. 1995. Mapping light-dependent structural changes in the cytoplasmic loop connecting helices C and D in rhodopsin: a site-directed spin labeling study. Biochemistry. 34:8812-8819.
15. Fung, B. K. 1983. Characterization of transducin from bovine retinal rod outer segments. I. Separation and reconstitution of the subunits. J. Biol. Chem. 258:10495-10502.
16. Gray-Keller, M. P., and P. B. Detwiler. 1994. The calcium feedback signal in the phototransduction cascade of vertebrate rods. Neuron. 13: 849-861.
17. Hecht, S., S. Shlaer, and M. Pirenne. 1942. Energy, quanta and vision. J. Gen. Physiol. 25:819-840.
18. Karpen, J. W., A. L. Zimmerman, L. Stryer, and D. A. Baylor. 1988. Gating kinetics of the cyclic-GMP-activated channel of retinal rods: flash photolysis and voltage-jump studies. Proc. Natl. Acad. Sci. USA. 85:1287-1291.
19. Kawamura, S. 1993. Rhodopsin phosphorylation as a mechanism of cyclic GMP phosphodiesterase regulation by S-modulin. Nature. 362: 855-857.
20. Koch, K. W., and L. Stryer. 1988. Highly cooperative feedback control of retinal rod guanylate cyclase by calcium ions. Nature. 334:64-66.
21. Koutalos, Y., K. Nakatani, T. Tamura, and K.-W. Yau. 1995a. Characterization of guanylate cyclase activity in single retinal rod outer segments. J. Gen. Physiol. 106:863-890.
22. Koutalos, Y., K. Nakatani, and K.-W. Yau. 1995b. The cGMP-phosphodiesterase and its contribution to sensitivity regulation in retinal rods. J. Gen. Physiol. 106:891-921.
23. Koutalos, Y., and K.-W. Yau. 1996. Regulation of sensitivity in vertebrate rod photoreceptors by calcium. Trends Neurosci. 19:73-81.
24. Krupnick, J. G., V. V. Gurevich, and J. L. Benovic. 1997. Mechanism of quenching of phototransduction. Binding competition between arrestin and transducin for phosphorhodopsin. J. Biol. Chem. 272:18125-18131.
25. Lagnado, L., and D. A. Baylor. 1992. Signal flow in visual transduction. Neuron. 8:995-1002.
26. Lagnado, L., and D. A. Baylor. 1994. Calcium controls light-triggered formation of catalytically active rhodopsin. Nature. 367:273-277.
27. Langlois, G., C. K. Chen, K. Palczewski, J. B. Hurley, and T. M. Vuong. 1996. Responses of the phototransduction cascade to dim light. Proc. Natl. Acad. Sci. USA. 93:4677-4682.
28. i. J. Gen. Physiol. 107:19-34.
29. Matthews, H. R., R. L. W. Murphy, G. L. Fain, and T. D. Lamb. 1988. Photoreceptor light adaptation is mediated by cytoplasmic calcium concentration. Nature. 334:67-69.
30. McCarthy, S. T., J. P. Younger, and W. G. Owen. 1996. Dynamic spatially non-uniform calcium regulation in frog rods exposed to light. J. Neurophysiol. 76:1991-2004.
31. Miller, J. L., and E. A. Dratz. 1984. Phosphorylation at sites near rhodopsin's carboxyl-terminus regulates light initiated cGMP hydrolysis. Vision Res. 24:1509-1521.
32. Murnick, J. G., and T. D. Lamb. 1996. Kinetics of desensitization induced by saturating flashes in toad and salamander rods. J. Physiol. (Lond.). 495:1-13.
33. Nakatani, K., and K.-W. Yau. 1988a. Calcium and light adaptation in retinal rods and cones. Nature. 334:69-71.
34. Nakatani, K., and K.-W. Yau. 1988b. Calcium and magnesium fluxes across the plasma membrane of the toad rod outer segment. J. Physiol. (Lond.). 395:695-729.
35. Nakatani, K., and K.-W. Yau. 1988c. Guanosine 3′,5′-cyclic monophosphate-activated conductance studied in a truncated rod outer segment of the toad. J. Physiol. (Lond.). 395:731-753.
36. Nikonov, S., N. Enghet, and E. N. Pugh. 1998. Kinetics of recovery of the dark-adapted salamander rod photoresponse. J. Gen. Physiol. 111:7-37.
37. Ohguro, H., J. P. Van-Hooser, A. H. Milam, and K. Palczewski. 1995. Rhodopsin phosphorylation and dephosphorylation in vivo. J. Biol. Chem. 270:14259-14262.
38. Palczewski, K., G. Rispoli, and P. B. Detwiler. 1992. The influence of arrestin (48K protein) and rhodopsin kinase on visual transduction. Neuron. 8:117-126.
39. Pepperberg, D. R., J. Jin, and G. J. Jones. 1994. Modulation of transduction gain in light adaptation of retinal rods. Vis. Neurosci. 11:53-62.
40. Pugh, E. N., Jr., and T. D. Lamb. 1993. Amplification and kinetics of the activation steps in phototransduction. Biochim. Biophys. Acta. 1141: 111-149.
41. Rieke, F., and D. A. Baylor. 1996. Molecular origin of continuous dark noise in rod photoreceptors. Biophys. J. 71:2553-2572.
42. Rispoli, G., W. A. Sather, and P. B. Detwiler. 1993. Visual transduction in dialysed detached rod outer segments from lizard retina. J. Physiol. (Lond.). 465:513-537.
43. Sagoo, M. S., and L. Lagnado. 1997. G-protein deactivation is rate-limiting for shut-off of the phototransduction cascade. Nature. 389:392-395.
44. Sakitt, B. 1972. Counting every quantum. J. Physiol (Lond.). 223:131-150.
45. Schnapf, J. L. 1983. Dependence of the single photon response on longitudinal position of absorption in toad rod outer segments. J. Physiol (Lond.). 343:147-159.
46. Torre, V., H. R. Matthews, and T. D. Lamb. 1986. Role of calcium in regulating the cyclic GMP cascade of phototransduction in retinal rods. Proc. Natl. Acad. Sci. USA. 83:7109-7113.
47. van der Velden, H. A. 1946. The number of quanta necessary for the perception of light in the human eye. Opthalmologica. 111:321-331.
48. Xu, J., R. L. Dodd, C. L. Makino, M. I. Simon, D. A. Baylor, and J. Chen. 1997. Prolonged photoresponses in transgenic mouse rods lacking arrestin. Nature. 389:505-509.
49. Yau, K.-W., and K. Nakatani. 1985. Light-suppressible, cyclic GMP-sensitive conductance in the plasma membrane of a truncated rod outer segment. Nature. 317:252-255.
50. Zagotta, W. N., T. Hoshi, and R. W. Aldrich. 1994. Shaker potassium channel gating. III. Evaluation of kinetic models for activation. J. Gen. Physiol. 103:321-362.
51. Zimmerman, A. L., and D. A. Baylor. 1986. Cyclic GMP-sensitive conductance of retinal rods consists of aqueous pores. Nature. 321:70-72.