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
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Lagnado, L. & Baylor, D. A. Neuron 8, 995–1002 (1992).
Pugh, E. N. Jr & Lamb, T. D. Biochim. Biophys. Acta 1141, 111–149 (1993).
Yarfitz, S. & Hurley, J. B. J. Biol. Chem. 269, 14329–14332 (1994).
Koutalos, Y. & Yau, K.-W. Trends Neursci. 19, 73–81 (1996).
Eakin, R. M. The Third Eye (University of California, Berkeley, 1973).
Solessio, E. & Engbretson, G. A. Nature 364, 442–445 (1993).
Hardie, R. C. & Minke, B. Cell Calcium 18, 256–274 (1995).
Ranganathan, R., Malicki, D. M. & Zuker, C. S. Annu. Rev. Neurosci. 18, 283–317 (1995).
Shin, J., Richard, E. A. & Lisman, J. E. Neuron 11, 845–855 (1993).
Finn, J. T., Grunwald, M. E. & Yau, K.-W. Annu. Rev. Physiol. 58, 395–426 (1996).
Colamartino, G., Menini, A. & Torre, V. J. Physiol. (Lond.) 440, 189–206 (1991).
Picones, A. & Korenbrot, J. I. Biophys. J. 69, 120–127 (1995).
Frings, S., Seifert, R., Godde, M. & Kaupp, U. B. Neuron 15, 169–179 (1995).
Hille, B. Ionic Channels of Excitable Membranes, 2nd edn (Sinauer, Sunderland, MA, 1992).
Neher, E. & Sakmann, B. in Single-Channel Recording, 2nd edn (eds Sakmann, B. & Neher, E.) 637–650 (Plenum, New York, 1995).
Karpen, J. W., Loney, D. A. & Baylor, D. A. J. Physiol. (Lond.) 448, 257–274 (1992).
Haynes, L. W. & Yau, K.-W. J. Physiol. (Lond.) 429, 451–481 (1990).
Pu, G. A. & Dowling, J. E. J. Neurophysiol. 46, 1018–1038 (1981).
Tamotsu, S. & Morita, Y. J. Comp. Phyisol. A 159, 1–5 (1986).
Deguchi, T. Nature 290, 706–707 (1981).
Marchiafava, P. L. & Kusmic, C. Prog. Brain Res. 95, 3–13 (1993).
Dryer, S. E. & Henderson, D. Nature 353, 756–758 (1991).
Autrum, H. (ed.) Handbookof Sensory Physiology Vol. VII/6A, Comparative Physiology and Evolution of Vision in Invertebrates A: Invertebrate Photoreceptors (Springer, Berlin, 1979).
Gomez, M. & Nasi, E. Neuron 15, 607–618 (1995).
Gotow, T., Nishi, T. & Kijima, H. Brain Res. 662, 268–272 (1994).
Gomez, M. & Nasi, E. J. Physiol. (Lond.) (in the press).
Robinson, R. A. & Stokes, R. H. Electrolyte Solutions 2nd edn (Butterworths, London, 1959).
Butler, J N. Biophys. J. 8, 1426–1433 (1968).
Lewis, C. A. J. Physiol. (Lond.) 286, 417–445 (1979).
Haynes, L. W. J. Gen. Physiol. 106, 507–523 (1995).
Bönigk, W., Müller, F., Middendorff, R., Weyand, Z. & Kaupp, U. B. J. Neurosci. 16, 7458–7468 (1996).
Author information
Authors and Affiliations
Rights 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
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1038/385815a0
This article is cited by
-
Light-sensitive neurons and channels mediate phototaxis in C. elegans
Nature Neuroscience (2008)
-
Cyclic GMP-dependent feedback inhibition of AMPA receptors is independent of PKG
Nature Neuroscience (2000)
-
The ordered visual transduction complex of the squid photoreceptor membrane
Molecular Neurobiology (1999)
-
Opening the third eye
Nature Neuroscience (1998)
-
An unusual cGMP pathway underlying depolarizing light response of the vertebrate parietal-eye photoreceptor
Nature Neuroscience (1998)
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.