Hostname: page-component-cd9895bd7-7cvxr Total loading time: 0 Render date: 2024-12-25T15:58:29.445Z Has data issue: false hasContentIssue false

Light-induced GTPase activity and GTP[γS] binding in squid retinal photoreceptors

Published online by Cambridge University Press:  02 June 2009

Joel E. Brown
Affiliation:
Department of Ophthalmology and Visual Sciences, Washington University, St. Louis
Anthony Combs
Affiliation:
Department of Ophthalmology and Visual Sciences, Washington University, St. Louis
Karen Ackermann
Affiliation:
Department of Ophthalmology and Visual Sciences, Washington University, St. Louis
Craig C. Malbon
Affiliation:
Department of Pharmacology, Health Sciences Center, SUNY Stony Brook, Stony Brook

Abstract

Illumination greatly increases the GTPase activity in homogenates of squid (Loligo) whole retinas or rhabdomeric membranes. Adenylylimidodiphosphate inhibits the light-insensitive (but not the light-sensitive) GTPase activity in these homogenates. Illumination also greatly increases the binding of GTP[γS] to the rhabdomeric membranes. This binding at saturating illuminations indicates that there are approximately 10–100 times more rhodopsin molecules than G-protein molecules in squid photoreceptors. Each light-activated rhodopsin molecule activates about 10 G-protein molecules which might provide amplification for the first stage of the phototransduction cascade.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1991

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Birnbaumer, L., Abramowitz, J. & Brown, A.M. (1990). Receptor-effector coupling by G-proteins. Biochimica et Biophysica Acta 1031, 163224.Google Scholar
Blumenfeld, A., Erusalimsky, J., Heichal, O., Selinger, Z. & Minke, B. (1985). Light-activated guanosinetriphosphatase in Musca eye membranes resembles the prolonged depolarizing afterpotential in photoreceptor cells. Proceedings of the National Academy of Sciences of the U.S.A. 82, 71167120.Google Scholar
Bolsover, S.R. & Brown, J.E. (1982). Injection of guanosine and adenosine nucleotides into Limulus ventral photoreceptor cells. Journal of Physiology 332, 325342.Google Scholar
Calhoon, R., Tsuda, M. & Ebrey, T.G. (1980). A light-activated GTPase from octopus photoreceptors. Biochemical and Biophysical Research Communications 94, 14521457.CrossRefGoogle ScholarPubMed
Chabre, M. & Deterre, P. (1989). Molecular mechanism of visual transduction. European Journal of Biochemistry 179, 255266.CrossRefGoogle ScholarPubMed
Dartnall, H.J.A. (1962). The properties of visual pigments in photoreceptors. In The Eye, Vol. 2, ed. Davson, H., pp. 473533. New York: Academic Press.Google Scholar
Devary, O., Heichal, O., Blumenfeld, A., Cassel, D., Suss, E., Barash, S., Rubinstein, C.T., Minke, B. & Selinger, Z. (1987). Coupling of photoexcited rhodopsin to inositol phospholipid hydrolysis in fly photoreceptors. Proceedings of the National Academy of Sciences of the U.S.A. 84, 69396943.CrossRefGoogle ScholarPubMed
Fung, B.K.-K. & Stryer, L. (1980). Photolyzed rhodopsin catalyzes the exchange of GTP for bound GDP in retinal rod outer segments. Proceedings of the National Academy of Sciences of the U.S.A. 77, 25002504.CrossRefGoogle Scholar
Goldsmith, T.H. & Wehner, R. (1977). Restrictions on rotational and translational diffusion of pigment in the membranes of a rhabdomeric photoreceptor. Journal of General Physiology 70, 453490.CrossRefGoogle ScholarPubMed
Hara, T. & Hara, R. (1967). Rhodopsin and retinochrome in the squid retina. Nature 214, 572575.Google Scholar
Higashijima, T., Uzu, S., Nakajima, T. & Ross, E.M. (1988). Mastoparan, A Peptide Toxin From Wasp Venom, Mimics Receptors By Activating Gtp-Binding Regulatory Proteins (G Proteins). Journal of Biological Chemistry 263, 64916494.CrossRefGoogle ScholarPubMed
Hubbard, R. & St., George R.C.C. (1958). The rhodopsin system of the squid. Journal of General Physiology 41, 501528.CrossRefGoogle ScholarPubMed
Inoue, M., Ackermann, K. & Brown, J.E. (1992). cGMP phosphodiesterase in photoreceptor cells in Limulus ventral eye. In Signal Transduction in Photoreceptor Cells, ed. Hargrave, P., Hofmann, K.P. & Kaupp, U.B. (in press).Google Scholar
Inoue, M. & Brown, J.E. (1988). Cyclic GMP phosphodiesterase in Limulus ventral eye. Investigative Ophthalmology and Visual Science 29, 218.Google Scholar
Kirkwood, A., Weiner, D. & Lisman, J.E. (1989). An estimate of the number of G regulatory proteins activated per excited rhodopsin in living Limulus ventral photoreceptors. Proceedings of the National Academy of Science of the U.S.A. 86, 38723876.CrossRefGoogle ScholarPubMed
Kito, Y., Seki, T. & Hagins, F.M. (1982). Isolation and purification of squid rhabdoms. Methods in Enzymology 84, 4348.CrossRefGoogle Scholar
Paulsen, R. & Bentrop, J. (1986). Light-modulated biochemical events in fly photoreceptors. Fortschritte der Zoologie 33, 299319.Google Scholar
Robinson, P.R. & Cote, R.H. (1989). Characterization of guanylate cyclase in squid photoreceptors. Visual Neuroscience 3, 17.CrossRefGoogle ScholarPubMed
Robinson, P.R., Wood, S.F., Szuts, E.Z., Fein, A. & Hamm, H.E. (1990). Light-dependent GTP-binding proteins in squid photoreceptors. Biochemical Journal 272, 7985.CrossRefGoogle ScholarPubMed
Saibil, H.R. (1990). Structure and function of the squid eye. In Squid as Experimental Animals, ed. Gilbert, D.L., Adelman, W.J. & Arnold, J.M., pp. 371397. New York: Plenum.CrossRefGoogle Scholar
Saibil, H.R. & Michel-Villaz, M. (1984). Squid rhodopsin and GTP-binding protein crossreact with vertebrate photoreceptor enzymes. Proceedings of the National Academy of Sciences of the U.S.A. 81, 51115115.Google Scholar
Smith, P.K., Krohn, R.I., Hermanson, G.T., Mallia, A.K., Gartner, F.H., Provenzano, M.D., Fujimoto, E.K., Goeke, N.M., Olson, B.J. & Klenk, D.C. (1985). Measurement of protein using bicinchoninic acid. Analytical Biochemistry 150, 7685.CrossRefGoogle ScholarPubMed
Stocchi, V., Cucchiarini, L., Canestrari, F., Piacentini, M.P. & Fornaini, G. (1987). A very fast ion-pair reversed-phased HPLC method for the separation of the most significant nucleotides and their degradation products in human red blood cells. Analytical Biochemistry 167, 181190.CrossRefGoogle Scholar
Stryer, L. (1986). Cyclic GMP cascade of vision. Annual Review of Neuroscience 9, 87119.Google Scholar
Tsuda, M. (1987). Photoreception and phototransduction in invertebrate photoreceptors. Photochemistry and Photobiology 45, 915931.CrossRefGoogle Scholar
Vandenberg, C.A. & Montal, M. (1984). Light-regulated biochemical events in invertebrate photoreceptors. I. Light-activated guanosinetriphosphatase, guanine nucleotide binding, and cholera toxin catalyzed labeling of squid photoreceptor membranes. Biochemistry 23, 23392347.Google Scholar