Light-dependent control of calcium in intact rods of the bullfrog Rana catesbeiana

Journal of Neurophysiology

Volumn 75, Issue 1, 1996, Pages 354-366

  Younger, James P ^a   McCarthy, Sean T ^a   Owen, W Geoffrey ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; CYCLIC GMP; FURA 2; GUANIDINE; GUANYLATE CYCLASE; POTASSIUM ION; SODIUM ION;

ANIMAL CELL; ARTICLE; CALCIUM TRANSPORT; CONTROLLED STUDY; CYTOSOL; DARK ADAPTATION; ENZYME ACTIVITY; FROG; ION EXCHANGE; LIGHT ADAPTATION; LIGHT DARK CYCLE; NONHUMAN; PHOTORECEPTOR; PRIORITY JOURNAL; RETINA ROD OUTER SEGMENT; SECOND MESSENGER; STEADY STATE;

EID: 0030048778     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.1996.75.1.354     Document Type: Article

References (80)

1. BARKDOLL, A. E., PUGH, E. N., JR., AND SITARAMAYYA, A. Calcium dependence of the activation and inactivation kinetics of the light-activated phosphodiesterase of retinal rods. J. Gen. Physiol. 93: 1091-1108, 1989.
2. BAYLOR, D. A., LAMB, T. D., AND YAU, K.-W. The membrane current of single rod outer segments. J. Physiol. Lond. 288: 589-611, 1979
3. CAPOVILLA, M., CERVETTO, L., AND TORRE, V. The effect of phosphodiesterase inhibitors on the electrical activity of toad rods. J. Physiol. Lond. 343: 277-294, 1983.
4. CAPOVILLA, M., HARE, W. A., AND OWEN, W. G. Voltage gain of signal transfer from retinal rods to bipolar cells in tiger salamander retina. J. Physiol. Lond. 391: 125-140, 1987.
5. 2+. J. Physiol. Lond. 382: 135P, 1987.
6. COCCIA, V. J. AND COTE, R. H. Regulation of intracellular cyclic GMP concentration by light and calcium in electropermeabilized rod photoreceptors. J. Gen. Physiol. 103: 67-86, 1994.
7. COPENHAGEN, D. R. AND OWEN, W. G. Functional characteristics of lateral interactions between rods in the retina of the snapping turtle J. Physiol. Lond. 259: 251-282, 1976.
8. DIZHOOR, A. M., LOWE, D. G., OLSHEVSKAYA, E. V., LAURA, R. P., AND HURLEY, J. B. The human photoreceptor membrane guanylate cyclase, RetGC, is present in outer segments and is regulated by calcium and a soluble activator. Neuron 12: 1345-1352, 1994.
9. DIZHOOR, A. M., RAY, S., KUMAR, S., NIEMI, G., SPENCER, M., BROLLEY, D., WALSH, K. A., PHILLIPOV, P. P., HURLEY, J. B., AND STRYER, L. Recoverin: A calcium sensitive activator of retinal rod guanylate cyclase. Science Wash. DC 251: 915-918, 1991.
10. FAIN, G. L. Sensitivity of toad rods: dependence on wavelength and background illumination. J. Physiol. Lond. 261: 71-101, 1976.
11. FAIN, G. L., QUANDT, F. N., AND BASTIAN, B. L. Contribution of a caesium-sensitive conductance increase to the photoresponse. Nature Lond. 272: 467-469, 1978.
12. FAIN, G. L. AND SCHRODER, W. H. Calcium in dark-adapted toad rods: evidence for pooling and cyclic-guanosine-3′-5′-monophosphate-dependent release. J. Physiol. Lond. 389: 361-384, 1987.
13. FAIN, G. L. AND SCHRODER, W. H. Light induced calcium release and reuptake in toad rods. J. Neurosci. 10: 2238-2249, 1990.
14. FESENKO, E. E., KOLESHNIKOV, S. S., AND LUBYARSKI, A. L. Induction by cyclic GMP of cation conductance in plasma membrane of retinal rod outer segment. Nature Lond. 313: 310-313, 1985.
15. FLEISCHMAN, D. AND DENISEVICH, M. Guanylate cyclase of isolated bovine retinal rod axonemes. Biochemistry 18: 5060-5066, 1979.
16. FURAKAWA, T. AND HANAWA, I. Effects of some common cations on electroretinogram of the toad. Jpn. J. Physiol. 5: 289-300, 1955.
17. GORCZYCA, W. A., GRAY-KELLER, M. P., DETWILER, P. B., AND PALCZEWSKI, K. Purification and physiological evaluation of a guanylate cyclase activating protein from retinal rods. Proc. Natl. Acad. Sci. USA 91: 4014-4018, 1994.
18. GORDON, S. E., BRAUTIGAN, D. L., AND ZIMMERMAN, A. L. Protein phosphotases modulate the apparent agonist affinity of the light-regulated ion channel in retinal rods. Neuron 9: 739-748, 1992.
19. GRAY-KELLER, M. P. AND DETWILER, P. B. The calcium feedback signal in the phototransduction cascade of vertebrate rods. Neuron 13: 849-861, 1994
20. GRODEN, D. L., GUAN, Z., AND STOKES, B. T. Determination of fura-2 dissociation constants following adjustment of the apparent Ca-EGTA association constant for temperature and ionic strength. Cell Calcium 12: 279-287, 1991.
21. 2- indicators with greatly improved fluorescent properties. J. Biol. Chem. 260: 3440-3450, 1985.
22. HAGINS, W. A., PENN, R. D., AND YOSHIKAMI, S. Dark current and photocurrent in retinal rods. Biophys. J. 10: 380-412, 1970.
23. HAROSI, F. I. Absorption spectra and linear dichroism of some amphibian photoreceptors. J. Gen. Physiol. 66: 357-382, 1975.
24. HESTRIN, S. AND KORENBROT, J. I. Effects of cGMP on the kinetics of the photocurrent in rods and in detached rod outer segments. J. Gen. Physiol. 90: 527-551, 1987.
25. HODGKIN, A. L., MCNAUGHTON, P. A., AND NUNN, B. J. The ionic selectivity and calcium dependence of the light-sensitive pathway in toad rods. J Physiol. Lond. 358: 447-468, 1985.
26. HODGKIN, A L., MCNAUGHTON, P. A., AND NUNN, B. J. Measurement of the sodium-calcium exchange in salamander rods. J. Physiol. Lond. 391: 347-370, 1987.
27. HODGKIN, A. L., MCNAUGHTON, P. A., NUNN, B. J., AND YAU, K.-W. Effect of ions on retinal rods from Bufo marinus J. Physiol. Lond. 350: 649-680, 1984.
28. HSU, Y. T. AND MOLDAY, R. S. Modulation of the cGMP-gated channel of rod photoreceptor cells by calmodulin. Nature Lond. 361: 76-79, 1993.
29. ICHIKAWA, K. Critical processes which characterize the photocurrent of retinal rod outer segments to flash stimuli. Neurosci. Res. 19: 201-212, 1994.
30. KAWAMURA, S. AND MURAKAMI, M. Regulation of cGMP levels by guanylate cyclase in truncated frog rod outer segments. J. Gen. Physiol. 94: 649-668, 1989.
31. KOCH, K.-W. AND STRYER, L. Highly cooperative feedback control of retinal guanylate cyclase by calcium ions. Nature Lond. 334: 64-66, 1988.
32. KORENBROT, J. I. AND MILLER, D. L. Calcium ions act as modulators of intracellular information flow in retinal rod phototransduction. Neurosci. Res. Suppl. 4: S11-S34, 1986.
33. KORENBROT, J. I. AND MILLER, D. L. Cytoplasmic free calcium concentration in dark-adapted retinal rod outer segments. Vision Res. 29: 939-948, 1989
34. LAGNADO, L. AND BAYLOR D. A. Calcium controls light-triggered formation of catalytically active rhodopsin. Nature Lond. 367: 273-277, 1994.
35. LAGNADO, L., CERVETTO, L., AND MCNAUGHTON, P. A. Ion transport by the Na-Ca exchange in isolated rod outer segments. Proc. Natl. Acad. Sci. USA 85: 4548-4552, 1988.
36. LAGNADO, L., CERVETTO, L , AND MCNAUGHTON, P. A. Calcium homeostasis in the outer segments of retinal rods from the tiger salamander. J. Physiol. Lond. 455: 111-142, 1992.
37. LAMB, T. D. AND PUGH, E. N., JR. A quantitative account of the activation steps involved in phototransduction in amphibian photoreceptors. J. Physiol. Lond. 449: 719-758, 1992.
38. LAMBRECHT, H. G. AND KOCH, K.-W. A 26 kD calcium binding protein from bovine rod outer segments as modulator of photoreceptor guanylate cyclase. EMBO J. 10: 793-798, 1991.
39. LOLLEY, R. AND RACZ, E. Calcium modulation of cyclic GMP synthesis in rat visual cells. Vision Res. 22: 1481-1486, 1982.
40. MARGULIS, A., GORACZNIAK, R. M., DUDA, T., SHARMA, R. K., AND SITARAMAYA, A. Structural and biochemical identity of retinal rod outer segment membrane guanylate cyclase. Biochem. Biophys. Res. Commun. 194: 855-861, 1993.
41. MARTELL, A. E. AND SMITH, R. M Critical Stability Constants. New York: Plenum, 1974, vol. 1, p. 269-272.
42. MATTHEWS, G. Single-channel recordings demonstrate that cGMP opens the light-sensitive channel of rod photoreceptor. Proc. Natl. Acad. Sci. USA 84: 299-302, 1987.
43. MATTHEWS, H. R., MURPHY, R. L. W., FAIN, G. L., AND LAMB, T. D. Photoreceptor light adaptation is mediated by cytoplasmic calcium concentration. Nature Lond. 334: 67-69, 1988.
44. MCCARTHY, S. T. Calcium, cGMP Hydrolysis and Light Adaptation in Rods of the Bullfrog (PhD thesis). Berkeley, CA: Univ. of California, 1993.
45. MCCARTHY, S. T., YOUNGER, J. P., AND OWEN, W. G. Disk structure, buffering and kinetics of cytosolic free calcium concentrations in bullfrog rod outer segments (Abstract). Invest. Ophthalmol. Visual Sci. 34: 1327a, 1993.
46. MCCARTHY, S. T., YOUNGER, J. P., AND OWEN, W. G. Free calcium concentrations in bullfrog rods determined in the presence of multiple forms of fura-2. Biophys. J. 67: 2076-2089, 1994.
47. MCNAUGHTON, P. A., CERVETTO, L., AND NUNN, B. J. Measurement of intracellular free calcium concentration in salamander rods. Nature Lond. 322: 261-263, 1986.
48. MENINI, A. Currents earned by monovalent cations through cyclic GMP activated channels in excised patches from salamander rods. J. Physiol. Lond. 424: 167-185, 1990.
49. MENINI, A., RISPOLI, G., AND TORRE, V. Ionic selectivity of the light-sensitive current in isolated rods of the tiger salamander. J. Physiol. Lond. 402: 279-300, 1988.
50. MILLER, D. L. AND KORENBROT, J. I. Kinetics of light-dependent Ca fluxes across the plasma membrane of rod outer segments. J. Gen. Physiol. 90: 397-425, 1987.
51. NAKATANI, K. AND YAU, K.-W. Calcium and light adaptation in retinal rods and cones. Nature Lond. 334. 69-71, 1988.
52. NEGULESCU, P. A. AND MACHEN, T. E. Intracellular ion activities and membrane transport in parietal cells measured with fluorescent dyes. Methods Enzymol. 192: 38-81, 1990.
53. OAKLEY, B., II, AND WEN, R. Extracellular pH in the isolated retina of the load in darkness and during illumination. J. Physiol. Lond. 419: 353-378, 1989.
54. OWEN, W. G. AND TORRE, V. High-pass filtering of small signals by retinal rods: ionic studies. Biophys. J. 41: 325-339, 1983.
55. PANFOLI, I. AND MORELLI, A. Calcium adenosinetriphosphotase of bovine retinal rod outer segment disk. Boll. Soc. Ital. Biol. Sper. 68: 593-595, 1992.
56. PANNBACKER, R. G. Control of guanylate cyclase activity in rod outer segment. Science Wash. DC 182: 1138-1140, 1973.
57. PEPE, I. M., BOERO, A., VERGANI, L., PANFOLI, I., AND CUGNOLI, C. Effect of light and calcium on cyclic GMP synthesis in rod outer segments of toad retina. Biochem. Biophys. Acta 889: 271-276, 1986.
58. o binding sites of the Na-Ca,K exchange in isolated salamander rod outer segments (Abstract). J. Physiol. Lond. 434: 70P, 1991.
59. RATTO, G. M., PAYNE, R , OWEN, W. G., AND TSIEN, R. Y. The concentration of cytosolic free calcium in vertebrate rod outer segments measured with fura-2. J. Neurosci. 8: 3240-3246, 1988.
60. ROSENKRANZ, J. New aspects of the ultrastructure of frog rod outer segments. Int. Rev. Cytol. 50: 24-158, 1977.
61. 2+ release from bovine rod outer segment disks. Biochemistry 26: 3249-3253, 1987.
62. +. Am. J. Physiol. 257 (Cell Physiol. 26): C153-C157, 1989.
63. SCHNETKAMP, P. P. M., LI, X -B., BASU, D. K , AND SZERENCSEI, R. T. Regulation of free cytosolic Ca concentration in the outer segments of bovine retinal rods by Na-Ca-K exchange measured with fluo-3. J. Biol. Chem. 266: 22983-22990, 1991a.
64. SCHNETKAMP, P. P. M., SZERENCSEI, R. T., AND BASU, D. K. Unidirectional Na, Ca, and K fluxes through the bovine rod outer segment Na-Ca-K exchanger. J. Biol. Chem. 266: 198-206, 1991b.
65. SCHRÖDER, W. H. AND FAIN, G. L. Light-dependent calcium release from photoreceptors measured by laser micro mass analysis. Nature Lond. 309: 268-270, 1984.
66. TANAKA, J. C. AND FURMAN, R. E. Divalent effects on cGMP-activated currents in excised patches from amphibian photoreceptors. J. Membr. Biol. 131: 245-256, 1993.
67. TOMITA, T. Electrophysiological study of the mechanisms subserving color coding in the fish. Cold Spring Harbor Symp. Quant. Biol. 30: 559-566, 1965.
68. TORRE, V., MATTHEWS, H. R., AND LAMB, T. D. Role of calcium in regulating the cyclic GMP cascade in retinal rods. Proc. Natl. Acad. Sci. USA 83: 7109-7113, 1986.
69. TOYODA, J., NOSAKI, H., AND TOMITA, T. Light-induced resistance changes in single photoreceptors of Necturus and Gekko. Vision Res. 9: 453-463, 1969.
70. TRANCHINA, D., SNEYD, J., AND CADENAS, I. D. Light adaptation in turtle cones: testing and analysis of a model for phototransduction. Biophys. J. 60: 217-237, 1991.
71. 2+ concentrations. Cell Calcium 12: 29-37, 1991.
72. WATANABE, S.-I. AND MATTHEWS, G. Dose-response relation of cyclic GMP-activated channels in retinal rod photoreceptors. Neurosci. Res. Suppl. 10: S1-S8, 1989.
73. WERBLIN, F. S. AND DOWLING, J. E. Organization of the retina of the mudpuppy, Necturus maculosus. II. Intracellular recording. J. Neurophysiol. 32: 339-355, 1969.
74. YAU, K.-W. Phototransduction mechanism in retinal rods and cones. Invest. Ophthalmol. Visual Sci. 35: 9-32, 1994.
75. YAU, K.-W. AND NAKATANI, K. Electrogenic Na-Ca exchange in retinal rod outer segments. Nature Lond. 311: 661-663, 1984.
76. YAU, K.-W. AND NAKATANI, K. Light-induced reduction of cytoplasmic free calcium in retinal rod outer segment. Nature Lond. 313: 579-582, 1985.
77. YOUNGER, J. P. Calcium Regulation of the Light Response of Vertebrate Photoreceptors (PhD thesis). Berkeley, CA: Univ. of California, 1991.
78. YOUNGER, J. P., MCCARTHY, S. T., AND OWEN, W. G. Weakly adapting backgrounds reduce the resting level of cytosolic free calcium in rod photoreceptors (Abstract). Invest. Ophthalmol. Visual Sci. 32: 907a, 1991.
79. YOUNGER, J. P., MCCARTHY, S. T., AND OWEN, W. G. Modulation of cytosolic free calcium and changes in sensitivity and circulating current occur over the same range of steady-state adapting lights in rod photoreceptors (Abstract). Invest. Ophthalmol. Visual Sci. 33: 1140a, 1992.
80. ZIMMERMAN, A. L., YAMANAKA, G., ECKSTEIN, F., AND BAYLOR, D. A. Interaction of hydrolysis-resistant analogs of cyclic GMP with the phosphodiesterase and light-sensitive channel of retinal rod outer segments. Proc. Natl. Acad. Sci. USA 82: 8813-8817, 1985.