Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-11-25T20:17:40.110Z Has data issue: false hasContentIssue false
  • English
  • Français

ATP-independent deactivation of squid rhodopsin

Published online by Cambridge University Press:  02 June 2009

Alon Kahana ,
Phyllis R. Robinson ,
Laura J. Lewis ,
Ete Z. Szuts  and
John E. Lisman
Alon Kahana
Affiliation:
Department of Biology, The Center for Complex Systems, Brandeis University, Waltham and Marine Biological Laboratory, Woods Hole
Phyllis R. Robinson
Affiliation:
Department of Biology, The Center for Complex Systems, Brandeis University, Waltham and Marine Biological Laboratory, Woods Hole
Laura J. Lewis
Affiliation:
Department of Biology, The Center for Complex Systems, Brandeis University, Waltham and Marine Biological Laboratory, Woods Hole
Ete Z. Szuts
Affiliation:
Department of Biology, The Center for Complex Systems, Brandeis University, Waltham and Marine Biological Laboratory, Woods Hole
John E. Lisman
Affiliation:
Department of Biology, The Center for Complex Systems, Brandeis University, Waltham and Marine Biological Laboratory, Woods Hole Reprint requests to: John E. Lisman, Department of Biology, The Center for Complex Systems, Brandeis University, Waltham, MA 02254-9110, USA.
Get access Rights & Permissions [Opens in a new window]

Abstract

Deactivation of light-activated squid rhodopsin was studied in vitro using GTPγS binding by G-protein as a direct measure of rhodopsin activity. Deactivation was inhibited by dilution of the retinal suspension or by removal of soluble components. Deactivation could be restored by addition of soluble material to washed membranes. These results indicate that the deactivation is not due entirely to a conformational transition within rhodopsin itself, but depends on the interaction with other molecules. The possibility that phosphorylation is involved in the deactivation was studied. Deactivation occurred in the presence and absence of added ATP. Deactivation also occurred in the presence of kinase inhibitors and after addition of apyrase, which reduced residual ATP levels to below 1μM. These results indicate that light-induced phosphorylation is not required for deactivation of squid rhodopsin. In this regard deactivation of squid rhodopsin is different from that of vertebrate rhodopsin, which requires phosphorylation.

Keywords

PhosphorylationInactivationArrestinG-proteinRhodopsin kinaseSwitch
Type
Research Article
Information
Visual Neuroscience , Volume 9 , Issue 6 , December 1992 , pp. 595 - 602
Copyright
Copyright © Cambridge University Press 1992

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

Bacigalupo, J., Johnson, E., Robinson, P. & Lisman, J.E. (1990). Second messengers in invertebrate phototransduction. In Transduction in Biological Systems, ed. Hidalgo, C., Bacigalupo, J., Jaimovich, E. & Veoara, J., pp. 27–45. New York: Plenum Press.CrossRefGoogle Scholar
Bennett, N. & Sitaramayya, A. (1988). Inactivation of photoexcited rhodopsin in retinal rods: The roles of rhodopsin kinase and 48-kDa protein (arrestin). Biochemistry 27, 1710–1715.CrossRefGoogle ScholarPubMed
Benovic, J.L., Mayor, F. Jr, Staniszewski, C., Lefkowitz, R.J. & Caron, M.G. (1987). Purification and characterization of the β-adrenergic receptor kinase. Journal of Biological Chemistry 262, 9026–9032.CrossRefGoogle ScholarPubMed
Bentrop, J. & Paulsen, R. (1986). Light-modulated ADP-ribosylation, protein phosphorylation and protein binding in isolated fly photoreceptor membranes. European Journal of Biochemistry 161, 61–67.CrossRefGoogle ScholarPubMed
Bownds, D., Dawes, J., Miler, J. & Stahlman, M. (1972). Phosphorylation of frog photoreceptor membranes induced by light. Nature New Biology 237, 125–127.CrossRefGoogle ScholarPubMed
Buczylko, J., Gutmann, C. & Palczewski, K. (1991). Regulation of rhodopsin kinase by autophosphorylation. Proceedings of the National Academy of Sciences of the U.S.A. 88, 2568–2572.CrossRefGoogle ScholarPubMed
Chabre, M. & Deterre, P. (1989). Molecular mechanism of visual transduction. European Journal of Biochemistry 179, 255–266.CrossRefGoogle ScholarPubMed
Dixon, R.A.F., Kobilka, B.K., Strader, D.J., Benovic, J.L., Dohlman, H.B., Frielle, T., Bolanowski, M.A., Bennet, C.D., Rands, E., Diehl, R.E., Mumford, R.A., Slater, E.E., Sigal, I.S., Caron, M.G., Lefkowitz, R.J. & Stader, C.D. (1986). Cloning of the gene and cDNA for mammalian β-adrenergic receptor and homology with rhodopsin. Nature (London)321, 75–79.CrossRefGoogle ScholarPubMed
Frank, R.N., Cavanagh, H.D. & Kenyon, K.R. (1973). Light-stimulated phosphorylation of bovine visual pigments by adenosine triphosphate. Journal of Biological Chemistry 248, 596–609.CrossRefGoogle ScholarPubMed
Hall, M.D., Hoon, M.A., Ryba, J.P., Pottinger, D.D., Keen, J.N., Saibil, H.R. & Findlay, B.C. (1991). Molecular cloning and primary structure of squid (Loligo forbesi) rhodopsin, a phospholipase C-directed G-protein-linked receptor. Biochemical Journal 214, 35–40.CrossRefGoogle Scholar
Hubbard, R. & St. George, R.C.C. (1958). The rhodopsin system of the squid. Journal of General Physiology 41, 501–528.CrossRefGoogle ScholarPubMed
Hyde, D., Mecklenburg, K., Pollock, J., Vihtelic, T. & Benzer, S. (1990). Twenty Drosophila visual system cDNA clones: One is a homolog of human arrestin. Proceedings of the National Academy of Sciences of the U.S.A. 87, 1008–1012.CrossRefGoogle ScholarPubMed
Kito, Y., Seki, T. & Hagins, F.M. (1982a). Isolation and purification of squid rhabdoms. Methods in Enzymology 81, 43–46.CrossRefGoogle ScholarPubMed
Kito, Y., Naito, T. & Nashima, K. (1982). Purification of squid and octopus rhodopsin. Methods in Enzymology 81, 167–170.CrossRefGoogle ScholarPubMed
Kobilka, B.K., Dixon, R.A.F., Frielle, T., Dohlman, H.G., Bolanowski, M.A., Sigal, I.S., Yang-Feng, T.L., Francke, U., Caron, M.G. & Lefkowitz, R.J. (1987). cDNA for the human β2-adrenergic receptor: A protein with multiple membrane-spanning domains and encoded by a gene whose chromosomal location is shared with that of the receptor for platelet-derived growth factor. Proceedings of the National Academy of Sciences of the U.S.A. 84, 46–50.CrossRefGoogle Scholar
Krishnan, P.S. (1949). Studies on apyrases II. Some properties of potato apyrase. Archives of Biochemistry 20, 272–283.Google Scholar
Kubo, T., Maeda, A., Suoimoto, K., Akiba, I., Mikami, A., Takahashi, H., Haoa, T., Haoa, K., Ichiyama, A., Kangawa, K., Matsuo, H., Hirose, T. & Numa, S. (1986a). Primary structure of porcine cardiac muscarinic acetylcholine receptor deduced from the cDNA sequence. FEBS Letters 209, 367–372.CrossRefGoogle ScholarPubMed
Kubo, T., Fukuda, K., Mikami, A., Maeda, A., Takahashi, H., Mishina, M., Haga, T., Haga, K., Ichiyama, A., Kangawa, K., Kojima, M., Matsuo, H., Hirose, T. & Numa, S. (1986b). Cloning, sequencing and expression of complementary DNA encoding the muscarinic acetylcholine receptor. Nature (London) 323, 411–416.CrossRefGoogle ScholarPubMed
Kuhn, H. & Dreyer, W.J. (1972). Light dependent phosphorylation of rhodopsin by ATP. FEBS Letters 20, 1–6.CrossRefGoogle ScholarPubMed
Kuhn, H., Hall, S.W. & Wilden, U. (1984). Light-induced binding of 48-kDa protein to photoreceptor membranes is highly enhanced by phosphorylation of rhodopsin. FEBS Letters 176, 473–478.CrossRefGoogle ScholarPubMed
Liebman, P.A. & Pugh, E.N. Jr (1980). ATP mediates rapid reversal of cyclic GMP phosphodiesterase activation in visual receptor membranes. Nature (London) 287, 734–736.CrossRefGoogle ScholarPubMed
Lisman, J. (1985). The role of metarhodopsin in the generation of spontaneous quantum bumps in ultraviolet receptors of Limulus median eye. Journal of General Physiology 85, 171–187.CrossRefGoogle ScholarPubMed
Lisman, J. & Goldring, M. (1985). Early events in visual transduction in Limulus photoreceptors. Neuroscience Research (Suppl.) 2, S101–S117.Google ScholarPubMed
Lohse, M.J., Benovic, J.L., Codina, J., Caron, M.G. & Lefkowitz, R.J. (1990). β-arrestin: A protein that regulates β-adrenergic receptor function. Science 248, 1547–1550.CrossRefGoogle ScholarPubMed
O'tousa, J.E., Baehr, W., Martin, R.L., Hirsch, J., Pak, W.L. & Applebury, M.L. (1985). The Drosophila ninaE gene encodes an opsin. Cell 40, 839–850.CrossRefGoogle ScholarPubMed
Ovchinnikov, Y.A., Abdulaev, N.G., Zolotarev, A.S., Artamonov, I.D., Bespalov, I.A., Dergachev, A.E. & Tsuda, M. (1988). Octopus rhodopsin: Amino acid sequence deduced from cDNA. FEBS Letters 232, 69–72.CrossRefGoogle Scholar
Palczewski, K. & Benovic, J.L. (1991). G-protein-coupled receptor kinases. Trends in Biochemical Sciences 16, 387–391.CrossRefGoogle ScholarPubMed
Palczewski, K., Kahn, N. & Hargrave, P.A. (1990). Nucleoside inhibitors of rhodopsin kinase. Biochemistry 29, 6276–6282.CrossRefGoogle ScholarPubMed
Palczewski, K., McDowell, J.H. & Hargrave, P.A. (1988). Purification and characterization of rhodopsin kinase. Journal of Biological Chemistry 263, 14067–14073.CrossRefGoogle ScholarPubMed
Paulsen, R. & Hoppe, I. (1978). Light-activated phosphorylation of cephalopod rhodopsin. FEBS Letters 96, 55–58.CrossRefGoogle ScholarPubMed
Paulsen, R., Bentrop, J., Hinsch, K.D. & Schultz, G. (1988). Invertebrate phototransduction: G-proteins and the function of 49 kDa protein. Proceedings of the Yamada Conference XXI, 227–232.Google Scholar
Pepperberg, D.R., Cornwall, M.C., Kahlert, M., Hofmann, K.P., Jin, J., Jones, G.R. & Ripps, H. (1992). Light-dependent delay in the falling phase of the retinal rod photoresponse. Visual Neuroscience 8, 9–18.CrossRefGoogle ScholarPubMed
Richard, E.A. & Lisman, J.E. (1992). Rhodopsin inactivation is a modulated process in Limulus photoreceptors. Nature 356, 336–338.CrossRefGoogle ScholarPubMed
Robinson, P.R., Radeke, M.J., Cote, R.H. & Bownds, M.D. (1986). cGMP influences guanine nucleotide binding to frog photoreceptor G-protein. Journal of Biological Chemistry 261, 313–318.CrossRefGoogle ScholarPubMed
Robinson, P.R., Wood, S.F., Szuts, E.Z., Fein, A., Hamm, H.E. & Lisman, J.E. (1990). Light-dependent GTP-binding proteins in squid photoreceptors. Biochemical Journal 272, 79–85.CrossRefGoogle ScholarPubMed
Sibley, R.H., Strasser, R.H., Caron, M.G. & Lefkowitz, R.J. (1985). Homologous desensitization of adenylate cyclase is associated with phosphorylation of the β-adrenergic receptor. Journal of Biological Chemistry 260, 3883–3886.CrossRefGoogle ScholarPubMed
Smith, D.P., Shieh, B.H. & Zuker, C.S. (1990). Isolation and structure of an arrestin gene from Drosophila. Proceedings of the National Academy of Sciences of the U.S.A. 87, 1003–1007.CrossRefGoogle ScholarPubMed
Strasser, R.H., Sibley, D.R. & Lefkowitz, R.J. (1986). A novel catecholamine-activated adenosine cyclic 3′, 5′-phosphate independent pathway for β-adrenergic receptor phosphorylation in wild-type and mutant S49 lymphoma cells: mechanism of homologous desensitization of adenylate cyclase. Biochemistry 25, 1371–1377.CrossRefGoogle ScholarPubMed
Stryer, L. (1986). Cyclic GMP cascade of vision. Annual Review of Neuroscience 9, 87.CrossRefGoogle ScholarPubMed
Thompson, P. & Findlay, J.B.C. (1984). Phosphorylation of ovine rhodopsin. Biochemical Journal 220, 773–780.CrossRefGoogle ScholarPubMed
Uhl, R., Wagment, R. & Ryba, N. (1990). Watching G proteins at work. Trends in Neuroscience 13, 64–70.CrossRefGoogle ScholarPubMed
Vandenberg, C.A. & Montal, M. (1984). Light-regulated biochemical events in invertebrate photoreceptors. 2. Light-regulated phosphorylation of rhodopsin and phosphoinositides in squid photoreceptor membranes. Biochemistry 23, 2347–2352.CrossRefGoogle ScholarPubMed
Wilden, U., Hall, S.W. & Kuhn, H. (1986). Phosphodiesterase activation by photoexcited rhodopsin is quenched when rhodopsin is phosphorylated and binds the intrinsic 48 kDa protein of rod outer segments. Proceedings of the National Academy of Sciences of the U.S.A. 83, 1174–1178.CrossRefGoogle ScholarPubMed
Wood, S.F., Szuts, E.Z. & Fein, A. (1989). Inositol trisphosphate production in squid photoreceptors. Journal of Biological Chemistry 264, 12970–12976.CrossRefGoogle ScholarPubMed
Yamada, T., Takeuchi, Y., Komori, N., Kobayashi, H., Sakai, Y., Hotta, Y. & Matsumoto, H. (1990). A 49-kilodalton phosphoprotein in the Drosophila photoreceptor is an arrestin homolog. Science 248, 483–486.CrossRefGoogle ScholarPubMed
Yount, R.G., Babcock, D., Ballantyne, W. & Ojala, D. (1971). Adenylyl imidodiphosphate, an adenosine triphosphate analog containing a P-N-P linkage. Biochemistry 10(13), 2484–2489.CrossRefGoogle ScholarPubMed
Zuker, C.S., Cowman, A.F. & Rubin, G.M. (1985). Isolation and structure of a rhodopsin gene from D. melanogaster. Cell 40, 851–858.CrossRefGoogle ScholarPubMed