Skip to main content
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1986 Feb;83(4):1150–1154. doi: 10.1073/pnas.83.4.1150

Plasma membrane calcium fluxes in intact rods are inconsistent with the "calcium hypothesis".

G H Gold
PMCID: PMC323029  PMID: 3485283

Abstract

The temporal relationship between the extracellular rod photovoltage and light-induced net Ca fluxes across the rod plasma membrane is investigated. The net Ca flux measurements are derived from extracellular Ca concentration measurements at the receptor surface of the isolated bullfrog retina. As reported previously, illumination leads to a net Ca efflux, which is followed by a net influx, during which the released Ca is taken back up. However, the net Ca flux has two characteristics that are inconsistent with the hypothesis that intracellular free Ca is the intracellular messenger for phototransduction in rods. First, during maintained photovoltage saturation, the net Ca efflux is transient, declining with a stereotypic time course that is independent of stimulus intensity and duration. Second, the significant rate of net influx during Ca uptake has no correlate in the photovoltage waveform. These observations are not consistent with the "Ca hypothesis." Rather, these data corroborate recent findings suggesting that light causes a decrease rather than an increase in intracellular free Ca concentration.

Full text

PDF
1150

Images in this article

Selected References

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

  1. Bader C. R., Macleish P. R., Schwartz E. A. A voltage-clamp study of the light response in solitary rods of the tiger salamander. J Physiol. 1979 Nov;296:1–26. doi: 10.1113/jphysiol.1979.sp012988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Baylor D. A., Lamb T. D. Local effects of bleaching in retinal rods of the toad. J Physiol. 1982 Jul;328:49–71. doi: 10.1113/jphysiol.1982.sp014252. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Blaustein M. P., Hodgkin A. L. The effect of cyanide on the efflux of calcium from squid axons. J Physiol. 1969 Feb;200(2):497–527. doi: 10.1113/jphysiol.1969.sp008704. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Blaustein M. P., Santiago E. M. Effects of internal and external cations and of ATP on sodium-calcium and calcium-calcium exchange in squid axons. Biophys J. 1977 Oct;20(1):79–111. doi: 10.1016/S0006-3495(77)85538-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bolnick D. A., Walter A. E., Sillman A. J. Barium suppresses slow PIII in perfused bullfrog retina. Vision Res. 1979;19(10):1117–1119. doi: 10.1016/0042-6989(79)90006-3. [DOI] [PubMed] [Google Scholar]
  6. DiPolo R. Characterization of the ATP-dependent calcium efflux in dialyzed squid giant axons. J Gen Physiol. 1977 Jun;69(6):795–813. doi: 10.1085/jgp.69.6.795. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. FURUKAWA T., HANAWA I. Effects of some common cations on electroretinogram of the toad. Jpn J Physiol. 1955 Dec 15;5(4):289–300. doi: 10.2170/jjphysiol.5.289. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. Gold G. H., Korenbrot J. I. Light-induced calcium release by intact retinal rods. Proc Natl Acad Sci U S A. 1980 Sep;77(9):5557–5561. doi: 10.1073/pnas.77.9.5557. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. 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]
  11. 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]
  12. Penn R. D., Hagins W. A. Kinetics of the photocurrent of retinal rods. Biophys J. 1972 Aug;12(8):1073–1094. doi: 10.1016/S0006-3495(72)86145-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Somlyo A. P., Walz B. Elemental distribution in Rana pipiens retinal rods: quantitative electron probe analysis. J Physiol. 1985 Jan;358:183–195. doi: 10.1113/jphysiol.1985.sp015547. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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]
  15. Yau K. W., Nakatani K. Cation selectivity of light-sensitive conductance in retinal rods. Nature. 1984 May 24;309(5966):352–354. doi: 10.1038/309352a0. [DOI] [PubMed] [Google Scholar]
  16. 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]
  17. 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]
  18. 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]
  19. Yoshikami S., George J. S., Hagins W. A. Light-induced calcium fluxes from outer segment layer of vertebrate retinas. Nature. 1980 Jul 24;286(5771):395–398. doi: 10.1038/286395a0. [DOI] [PubMed] [Google Scholar]
  20. Zuckerman R., Schmidt G. J., Dacko S. M. Rhodopsin-to-metarhodopsin II transition triggers amplified changes in cytosol ATP and ADP in intact retinal rod outer segments. Proc Natl Acad Sci U S A. 1982 Nov;79(21):6414–6418. doi: 10.1073/pnas.79.21.6414. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES