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. 1986 Sep;83(18):7109–7113. doi: 10.1073/pnas.83.18.7109

Role of calcium in regulating the cyclic GMP cascade of phototransduction in retinal rods.

V Torre, H R Matthews, T D Lamb
PMCID: PMC386662  PMID: 3018756

Abstract

Both cGMP and Ca2+ appear to be involved in the process of phototransduction in vertebrate rods, but their precise roles have been the subject of debate. To investigate the role of Ca2+ we have artificially increased the calcium buffering capacity of the rod by using a patch pipet to incorporate the calcium buffer 1,2-bis(o-aminophenoxy)ethane-N,N,N',N'-tetraacetic acid (BAPTA) into the rod cytoplasm. In the presence of buffer the Na+-Ca2+ exchange current became greatly slowed, suggesting that the cytoplasmic calcium concentration (Cai) had indeed been buffered substantially. Although the presence of buffer had negligible effect on the rising phase of the light response, it profoundly altered the later behavior. Responses to brief flashes became prolonged and exhibited an overshoot, apparently because the shut-off process was modified. The normal acceleration of time-to-peak with brighter flashes (an early sign of light adaptation) disappeared. Responses to steady adapting illumination took much longer than normal to settle to a steady level, although the final level represented a similar fractional suppression of current. With superimposed test flashes the presence of such adapting illumination caused a more rapid recovery, whereas the presence of calcium buffer slowed the recovery. The results are consistent with the idea that the rapid drop in Cai, which has recently been shown to accompany the light response, is involved in terminating the light response, and that Cai is thereby involved in setting the operating point and sensitivity of phototransduction. From comparison with other work we infer that Cai appears to act, at least in part, by means of control of cGMP phosphodiesterase activity.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bastian B. L., Fain G. L. Light adaptation in toad rods: requirement for an internal messenger which is not calcium. J Physiol. 1979 Dec;297(0):493–520. doi: 10.1113/jphysiol.1979.sp013053. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Baylor D. A., Fuortes M. G. Electrical responses of single cones in the retina of the turtle. J Physiol. 1970 Mar;207(1):77–92. doi: 10.1113/jphysiol.1970.sp009049. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Baylor D. A., Hodgkin A. L. Changes in time scale and sensitivity in turtle photoreceptors. J Physiol. 1974 Nov;242(3):729–758. doi: 10.1113/jphysiol.1974.sp010732. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Baylor D. A., Lamb T. D., Yau K. W. Responses of retinal rods to single photons. J Physiol. 1979 Mar;288:613–634. [PMC free article] [PubMed] [Google Scholar]
  5. Baylor D. A., Lamb T. D., Yau K. W. The membrane current of single rod outer segments. J Physiol. 1979 Mar;288:589–611. [PMC free article] [PubMed] [Google Scholar]
  6. Baylor D. A., Nunn B. J. Electrical properties of the light-sensitive conductance of rods of the salamander Ambystoma tigrinum. J Physiol. 1986 Feb;371:115–145. doi: 10.1113/jphysiol.1986.sp015964. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bodoia R. D., Detwiler P. B. Patch-clamp recordings of the light-sensitive dark noise in retinal rods from the lizard and frog. J Physiol. 1985 Oct;367:183–216. doi: 10.1113/jphysiol.1985.sp015820. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bownds M. D. Biochemical steps in visual transduction: roles for nucleotides and calcium ions. Photochem Photobiol. 1980 Oct;32(4):487–490. doi: 10.1111/j.1751-1097.1980.tb03792.x. [DOI] [PubMed] [Google Scholar]
  9. Cervetto L., Torre V., Rispoli G., Marroni P. Mechanisms of light adaptation in toad rods. Exp Biol. 1985;44(3):147–157. [PubMed] [Google Scholar]
  10. Cobbs W. H., Barkdoll A. E., 3rd, Pugh E. N., Jr Cyclic GMP increases photocurrent and light sensitivity of retinal cones. Nature. 1985 Sep 5;317(6032):64–66. doi: 10.1038/317064a0. [DOI] [PubMed] [Google Scholar]
  11. Cobbs W. H., Pugh E. N., Jr Cyclic GMP can increase rod outer-segment light-sensitive current 10-fold without delay of excitation. Nature. 1985 Feb 14;313(6003):585–587. doi: 10.1038/313585a0. [DOI] [PubMed] [Google Scholar]
  12. Cohen A. I., Hall I. A., Ferrendelli J. A. Calcium and cyclic nucleotide regulation in incubated mouse retinas. J Gen Physiol. 1978 May;71(5):595–612. doi: 10.1085/jgp.71.5.595. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. FUORTES M. G., HODGKIN A. L. CHANGES IN TIME SCALE AND SENSITIVITY IN THE OMMATIDIA OF LIMULUS. J Physiol. 1964 Aug;172:239–263. doi: 10.1113/jphysiol.1964.sp007415. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Fain G. L. Sensitivity of toad rods: Dependence on wave-length and background illumination. J Physiol. 1976 Sep;261(1):71–101. doi: 10.1113/jphysiol.1976.sp011549. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Fesenko E. E., Kolesnikov S. S., Lyubarsky A. L. Induction by cyclic GMP of cationic conductance in plasma membrane of retinal rod outer segment. Nature. 1985 Jan 24;313(6000):310–313. doi: 10.1038/313310a0. [DOI] [PubMed] [Google Scholar]
  16. Fleischman D., Denisevich M. Guanylate cyclase of isolated bovine retinal rod axonemes. Biochemistry. 1979 Nov 13;18(23):5060–5066. doi: 10.1021/bi00590a006. [DOI] [PubMed] [Google Scholar]
  17. Gold G. H. Plasma membrane calcium fluxes in intact rods are inconsistent with the "calcium hypothesis". Proc Natl Acad Sci U S A. 1986 Feb;83(4):1150–1154. doi: 10.1073/pnas.83.4.1150. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hagins W. A., Penn R. D., Yoshikami S. Dark current and photocurrent in retinal rods. Biophys J. 1970 May;10(5):380–412. doi: 10.1016/S0006-3495(70)86308-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Haynes L., Yau K. W. Cyclic GMP-sensitive conductance in outer segment membrane of catfish cones. Nature. 1985 Sep 5;317(6032):61–64. doi: 10.1038/317061a0. [DOI] [PubMed] [Google Scholar]
  20. Hodgkin A. L., McNaughton P. A., Nunn B. J. The ionic selectivity and calcium dependence of the light-sensitive pathway in toad rods. J Physiol. 1985 Jan;358:447–468. doi: 10.1113/jphysiol.1985.sp015561. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Hodgkin A. L., McNaughton P. A., Nunn B. J., Yau K. W. Effect of ions on retinal rods from Bufo marinus. J Physiol. 1984 May;350:649–680. doi: 10.1113/jphysiol.1984.sp015223. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Lamb T. D. Effects of temperature changes on toad rod photocurrents. J Physiol. 1984 Jan;346:557–578. doi: 10.1113/jphysiol.1984.sp015041. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Lamb T. D., Matthews H. R., Torre V. Incorporation of calcium buffers into salamander retinal rods: a rejection of the calcium hypothesis of phototransduction. J Physiol. 1986 Mar;372:315–349. doi: 10.1113/jphysiol.1986.sp016011. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Lolley R. N., Racz E. Calcium modulation of cyclic GMP synthesis in rat visual cells. Vision Res. 1982;22(12):1481–1486. doi: 10.1016/0042-6989(82)90213-9. [DOI] [PubMed] [Google Scholar]
  25. Matthews H. R., Torre V., Lamb T. D. Effects on the photoresponse of calcium buffers and cyclic GMP incorporated into the cytoplasm of retinal rods. Nature. 1985 Feb 14;313(6003):582–585. doi: 10.1038/313582a0. [DOI] [PubMed] [Google Scholar]
  26. Robinson P. R., Kawamura S., Abramson B., Bownds M. D. Control of the cyclic GMP phosphodiesterase of frog photoreceptor membranes. J Gen Physiol. 1980 Nov;76(5):631–645. doi: 10.1085/jgp.76.5.631. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Stryer L. Cyclic GMP cascade of vision. Annu Rev Neurosci. 1986;9:87–119. doi: 10.1146/annurev.ne.09.030186.000511. [DOI] [PubMed] [Google Scholar]
  28. Tomita T. Electrical activity of vertebrate photoreceptors. Q Rev Biophys. 1970 May;3(2):179–222. doi: 10.1017/s0033583500004571. [DOI] [PubMed] [Google Scholar]
  29. Tsien R. Y. New calcium indicators and buffers with high selectivity against magnesium and protons: design, synthesis, and properties of prototype structures. Biochemistry. 1980 May 27;19(11):2396–2404. doi: 10.1021/bi00552a018. [DOI] [PubMed] [Google Scholar]
  30. Woodruff M. L., Fain G. L. Ca2+-dependent changes in cyclic GMP levels are not correlated with opening and closing of the light-dependent permeability of toad photoreceptors. J Gen Physiol. 1982 Oct;80(4):537–555. doi: 10.1085/jgp.80.4.537. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Yau K. W., McNaughton P. A., Hodgkin A. L. Effect of ions on the light-sensitive current in retinal rods. Nature. 1981 Aug 6;292(5823):502–505. doi: 10.1038/292502a0. [DOI] [PubMed] [Google Scholar]
  32. Yau K. W., Nakatani K. Electrogenic Na-Ca exchange in retinal rod outer segment. Nature. 1984 Oct 18;311(5987):661–663. doi: 10.1038/311661a0. [DOI] [PubMed] [Google Scholar]
  33. Yau K. W., Nakatani K. Light-induced reduction of cytoplasmic free calcium in retinal rod outer segment. Nature. 1985 Feb 14;313(6003):579–582. doi: 10.1038/313579a0. [DOI] [PubMed] [Google Scholar]
  34. Yau K. W., Nakatani K. Light-suppressible, cyclic GMP-sensitive conductance in the plasma membrane of a truncated rod outer segment. Nature. 1985 Sep 19;317(6034):252–255. doi: 10.1038/317252a0. [DOI] [PubMed] [Google Scholar]
  35. Zimmerman A. L., Yamanaka G., Eckstein F., Baylor D. A., Stryer L. Interaction of hydrolysis-resistant analogs of cyclic GMP with the phosphodiesterase and light-sensitive channel of retinal rod outer segments. Proc Natl Acad Sci U S A. 1985 Dec;82(24):8813–8817. doi: 10.1073/pnas.82.24.8813. [DOI] [PMC free article] [PubMed] [Google Scholar]

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