Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

A cGMP-gated cation channel in depolarizing photoreceptors of the lizard parietal eye

Abstract

Rods and cones of the two vertebrate lateral eyes hyperpolarize when illuminated, a response generated by a cyclic GMP cascade leading to cGMP hydrolysis and consequently the closure of cGMP-gated, non-selective cation channels that are open in darkness1–4. Lizards and other lower vertebrates also have a parietal (third) eye5, which contains ciliary photoreceptors that under dark-adapted conditions depolarize to light instead6. Depolarizing light responses are characteristic of most invertebrate rhabdomeric photoreceptors, and are thought to involve a phosphoinositide signalling pathway (see, for example, refs 7–9). Surprisingly, we have found in excised membrane patches a cGMP-gated channel that is selectively present at high density on the outer segment (the presumptive light-sensitive part) of the parietal eye photoreceptor. Like the light-activated channel of the cell, it is non-selective among cations. Inositol trisphosphate (InsP3) had no effect on the same membrane patches. These findings suggest that the photoreceptors of the parietal eye, like rods and cones, use a cGMP cascade and not an InsP3-mediated pathway for phototransduction, but in this case light increases cGMP. A unifying principle of evolutionary significance emerges: that phototransductions in various ciliary photoreceptors, whether hyperpolarizing or depolarizing, uniformly use a cGMP cascade and a cGMP-gated channel to generate the light response, although there are rich variations in the details.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Similar content being viewed by others

References

  1. Lagnado, L. & Baylor, D. A. Neuron 8, 995–1002 (1992).

    Article  CAS  Google Scholar 

  2. Pugh, E. N. Jr & Lamb, T. D. Biochim. Biophys. Acta 1141, 111–149 (1993).

    Article  CAS  Google Scholar 

  3. Yarfitz, S. & Hurley, J. B. J. Biol. Chem. 269, 14329–14332 (1994).

    CAS  PubMed  Google Scholar 

  4. Koutalos, Y. & Yau, K.-W. Trends Neursci. 19, 73–81 (1996).

    Article  CAS  Google Scholar 

  5. Eakin, R. M. The Third Eye (University of California, Berkeley, 1973).

    Google Scholar 

  6. Solessio, E. & Engbretson, G. A. Nature 364, 442–445 (1993).

    Article  ADS  CAS  Google Scholar 

  7. Hardie, R. C. & Minke, B. Cell Calcium 18, 256–274 (1995).

    Article  CAS  Google Scholar 

  8. Ranganathan, R., Malicki, D. M. & Zuker, C. S. Annu. Rev. Neurosci. 18, 283–317 (1995).

    Article  CAS  Google Scholar 

  9. Shin, J., Richard, E. A. & Lisman, J. E. Neuron 11, 845–855 (1993).

    Article  CAS  Google Scholar 

  10. Finn, J. T., Grunwald, M. E. & Yau, K.-W. Annu. Rev. Physiol. 58, 395–426 (1996).

    Article  CAS  Google Scholar 

  11. Colamartino, G., Menini, A. & Torre, V. J. Physiol. (Lond.) 440, 189–206 (1991).

    Article  CAS  Google Scholar 

  12. Picones, A. & Korenbrot, J. I. Biophys. J. 69, 120–127 (1995).

    Article  ADS  CAS  Google Scholar 

  13. Frings, S., Seifert, R., Godde, M. & Kaupp, U. B. Neuron 15, 169–179 (1995).

    Article  CAS  Google Scholar 

  14. Hille, B. Ionic Channels of Excitable Membranes, 2nd edn (Sinauer, Sunderland, MA, 1992).

    Google Scholar 

  15. Neher, E. & Sakmann, B. in Single-Channel Recording, 2nd edn (eds Sakmann, B. & Neher, E.) 637–650 (Plenum, New York, 1995).

    Google Scholar 

  16. Karpen, J. W., Loney, D. A. & Baylor, D. A. J. Physiol. (Lond.) 448, 257–274 (1992).

    Article  CAS  Google Scholar 

  17. Haynes, L. W. & Yau, K.-W. J. Physiol. (Lond.) 429, 451–481 (1990).

    Article  CAS  Google Scholar 

  18. Pu, G. A. & Dowling, J. E. J. Neurophysiol. 46, 1018–1038 (1981).

    Article  CAS  Google Scholar 

  19. Tamotsu, S. & Morita, Y. J. Comp. Phyisol. A 159, 1–5 (1986).

    Article  CAS  Google Scholar 

  20. Deguchi, T. Nature 290, 706–707 (1981).

    Article  ADS  CAS  Google Scholar 

  21. Marchiafava, P. L. & Kusmic, C. Prog. Brain Res. 95, 3–13 (1993).

    Article  CAS  Google Scholar 

  22. Dryer, S. E. & Henderson, D. Nature 353, 756–758 (1991).

    Article  ADS  CAS  Google Scholar 

  23. Autrum, H. (ed.) Handbookof Sensory Physiology Vol. VII/6A, Comparative Physiology and Evolution of Vision in Invertebrates A: Invertebrate Photoreceptors (Springer, Berlin, 1979).

  24. Gomez, M. & Nasi, E. Neuron 15, 607–618 (1995).

    Article  Google Scholar 

  25. Gotow, T., Nishi, T. & Kijima, H. Brain Res. 662, 268–272 (1994).

    Article  CAS  Google Scholar 

  26. Gomez, M. & Nasi, E. J. Physiol. (Lond.) (in the press).

  27. Robinson, R. A. & Stokes, R. H. Electrolyte Solutions 2nd edn (Butterworths, London, 1959).

    Google Scholar 

  28. Butler, J N. Biophys. J. 8, 1426–1433 (1968).

    Article  ADS  CAS  Google Scholar 

  29. Lewis, C. A. J. Physiol. (Lond.) 286, 417–445 (1979).

    Article  CAS  Google Scholar 

  30. Haynes, L. W. J. Gen. Physiol. 106, 507–523 (1995).

    Article  CAS  Google Scholar 

  31. Bönigk, W., Müller, F., Middendorff, R., Weyand, Z. & Kaupp, U. B. J. Neurosci. 16, 7458–7468 (1996).

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Finn, J., Solessio, E. & Yau, KW. A cGMP-gated cation channel in depolarizing photoreceptors of the lizard parietal eye. Nature 385, 815–819 (1997). https://doi.org/10.1038/385815a0

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/385815a0

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing