Hostname: page-component-848d4c4894-mwx4w Total loading time: 0 Render date: 2024-06-25T15:39:10.056Z Has data issue: false hasContentIssue false

Characterization of protein phosphatases type 1 and type 2A in Limulus nervous tissue: Their light regulation in the lateral eye and evidence of involvement in the photoresponse

Published online by Cambridge University Press:  02 June 2009

Samuel C. Edwards
Affiliation:
Departments of Biology and Pharmacology and Therapeutics and the Institute for Biomolecular Sciences, University of South Florida, Tampa
Peter M. O'Day
Affiliation:
Institute of Neuroscience and Department of Biology, University of Oregon, Eugene
Desiree C. Herrera
Affiliation:
Departments of Biology and Pharmacology and Therapeutics and the Institute for Biomolecular Sciences, University of South Florida, Tampa

Abstract

The activities of both protein phosphatases and protein kinases are responsible for the transient changes in the levels of phosphorylation and probably the functions of protein intermediates involved in the biochemical and physiological mechanisms underlying the photoresponse in photoreceptor cells from both vertebrate and invertebrate organisms. Of the known protein serine/threonine phosphatases, various forms of type I (PP 1) and type 2A (PP 2A) protein phosphatases are responsible for dephosphorylating many of the known phosphoproteins including those involved in photoreceptor cell function. In this report, we provide biochemical evidence for both PP 1– and PP 2A-like activities in the visual and nonvisual tissue of the horseshoe crab, Limulus polyphemus, that membrane and soluble forms of both enzymes are present, and that the activities of both enzymes are greater in light- than in dark-adapted lateral eyes. These activities were characterized using glycogen phosphorylase a, a substrate for both PP 1 and PP 2A, and various protein phosphatase inhibitors, including okadaic acid. We also report that okadaic acid, at concentrations required to inhibit PP 1, inhibited physiological functions of photoreceptor cells from the ventral eye, causing a delayed reduction of the resting membrane, and slowing and reducing light responses.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1996

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

REFERENCES

Bacigalupo, J. & Lisman, J.E. (1983). Single-channel currents activated by light in Limulus ventral photoreceptors. Nature 304, 268270.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, 6167.CrossRefGoogle ScholarPubMed
Bollen, M. & Stalmans, W. (1992). The structure, role and regulation of type 1 protein phosphatases. Critical Reviews in Biochemistry and Molecular Biology 27, 227281.CrossRefGoogle ScholarPubMed
Bolsover, S.R. & Brown, J.E. (1985). Calcium ion, an intracellular messenger of light adaptation, also participates in excitation in Limulus photoreceptors. Journal of Physiology 364, 381393.CrossRefGoogle ScholarPubMed
Bownds, D., Dawes, J., Miller, J. & Stahlman, M. (1972). Phosphorylation of frog photoreceptor membranes by light. Nature 237, 125127.Google ScholarPubMed
Bradford, M.M. (1976). A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein dye binding. Analytical Biochemistry 72, 248254.CrossRefGoogle Scholar
Brautigan, D.L. & Shriner, C.L. (1988). Methods to distinguish various types of protein phosphatase activity. Methods in Enzymol-ogy 159, 329347.Google ScholarPubMed
Brown, J.E. & Blinks, J.R. (1974). Changes in intracellular free Ca concentrations during illumination of invertebrate photoreceptors. Detection with aequorin. Journal of General Physiology 64, 643665.CrossRefGoogle Scholar
Brown, J.E. & Mote, M.I. (1974). Ionic dependence of reversal voltage of the light response in Limulus ventral photoreceptors. Journal of General Physiology 63, 337350.CrossRefGoogle ScholarPubMed
Brown, J.E. & Rubin, L.J. (1984). A direct demonstration that inositol triphosphate induces an increase in intracellular calcium in Limulus photoreceptors. Biochemical and Biophysical Research Communications 125, 11371142.CrossRefGoogle Scholar
Brown, J.E., Kaupp, U.B. & Malbon, C.C. (1984 a). 3′,5′-cyclic adenosine monophosphate and adenylate cyclase in phototransduction by Limulus ventral photoreceptors. Journal of Physiology 353, 523539.CrossRefGoogle Scholar
Brown, J.E., Rubin, L.J., Ghalayini, A.J., Tarver, A.L., Irvine, R.F., Berridge, M.J. & Anderson, R.E. (1984 b). Myo-inositol polyphosphate may be a messenger for visual excitation in Limulus photoreceptors. Nature 311, 160162.CrossRefGoogle ScholarPubMed
Byk, T., Bar-Yaacov, M., Doza, Y.N., Minke, B. & Selinger, Z. (1993). Regulatory arrestin cycle secures the fidelity and maintenance of the fly photoreceptor cell. Proceedings of the National Academy of Sciences of the U.S.A. 90, 19071911.CrossRefGoogle ScholarPubMed
Calman, B.G., Andrews, A.W. & Battelle, B.-A. (1992). The 46 kD protein in Limulus photoreceptors is phosphorylated by a calcium-calmodulin dependent protein kinase. Investigative Ophthalmology and Visual Neuroscience 33, 874.Google Scholar
Calman, B.G. & Battelle, B.-A. (1994). Sequence of a CaCAM-dependent protein kinase II from Limulus eyes. Investigative Ophthalmology and Visual Neuroscience 35, 2131.Google Scholar
Chen, J., Martin, B.L. & Brautigan, D.L. (1992). Regulation of protein serine-threonine phosphatase type-2A by tyrosine phosphorylation. Science 257, 12611264.CrossRefGoogle ScholarPubMed
Chung, S., Reinhart, P.H., Martin, B.L., Brautigan, D. & Levi-tan, I.B. (1991). Protein kinase activity closely associated with a reconstituted calcium-activated potassium channel. Science 253, 560562.CrossRefGoogle ScholarPubMed
Cohen, P. (1991). Classification of protein-serine/threonine phosphatases: Identification and quantification in cell extracts. Methods in Enzymology 201, 389398.CrossRefGoogle Scholar
Cohen, P., Alemany, S., Hemmings, B.A., Resink, T.J., Stralfors, P. & Lim, Tung H.Y. (1988). Protein phosphatase-1 and protein phosphatase-2A from rabbit skeletal muscle. Methods in Enzymology 159, 391409.Google ScholarPubMed
Dobrowsky, R.T., Kamibayashi, C., Mumby, M.C. & Hannun, Y.A. (1993). Ceramide activates heterotrimeric protein phosphatase 2A. Journal of Biological Chemistry 268, 1552315530.CrossRefGoogle ScholarPubMed
Dodge, F.A., Knight, B.W. & Toyoda, J. (1968). Voltage noise in Limulus visual cells. Science 160, 8890.CrossRefGoogle ScholarPubMed
Edwards, S.C. & Battelle, B.-A. (1987). Octopamine and cyclic AMP-stimulated phosphorylation of a protein in Limulus ventral and lateral eyes. Journal of Neuroscience 7, 28112820.CrossRefGoogle ScholarPubMed
Edwards, S.C., Wishart, A.C., Wiebe, E.M. & Battelle, B.-A. (1989). Light-regulated proteins in the Limulus ventral photoreceptor. Visual Neuroscience 3, 95105.CrossRefGoogle ScholarPubMed
Ellis, D.Z. & Edwards, S.C. (1994). Characterization of a calcium/ calmodulin-dependent protein phosphatase in the Limulus nervous tissue and its light regulation in the lateral eye. Visual Neuroscience 11, 851860.CrossRefGoogle ScholarPubMed
Esguerra, M., Wang, J., Foster, C.D., Adelman, J.P., North, R.A. & Levitan, I.B. (1994). Cloned Ca2+-dependent K+ channel modulated by a functionally associated protein kinase. Nature 369, 563565.CrossRefGoogle Scholar
Fein, A., Payne, R., Corson, D.W., Berridge, M.J. & Irvine, R.F. (1984). Photoreceptor excitation and adaptation by inositol 1,4,5–triphosphate. Nature 311, 157160.CrossRefGoogle Scholar
Foulkes, J.G. & Cohen, P. (1980). The regulation of glycogen metabolism. Purification and properties of protein phosphatase inhibitor-2 from rabbit skeletal muscle. European Journal of Biochemistry 105, 195203.CrossRefGoogle ScholarPubMed
Fowles, C., Akhtar, M. & Cohen, P. (1989). Interplay of phosphorylation and dephosphorylation in vision: Protein phosphatases of bovine rod outer segments. Biochemistry 28, 93859391.CrossRefGoogle ScholarPubMed
Frace, A.M. & Hartzell, H.C. (1993). Opposite effects of phosphatase inhibitors on L-type calcium and delayed rectifier currents in frog cardiac myocytes. Journal of Physiology 472, 305326.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, 596609.CrossRefGoogle ScholarPubMed
Gergely, P., Erdödi, F. & Bot, G. (1984). Heparin inhibits the activity of protein phosphatase-1. FEBS Letters 169, 4548.CrossRefGoogle ScholarPubMed
Gordon, S.E., Brautigan, D.L. & Zimmerman, A.L. (1992). Protein phosphatases modulate the apparent affinity of the light-regulated ion channel in retinal rods. Neuron 9, 739748.CrossRefGoogle ScholarPubMed
Gray-Keller, M.P. & Detwiler, P.B. (1994). The calcium feedback signal in the phototransduction cascade of vertebrate rods. Nature 13, 849861.Google ScholarPubMed
Guo, H. & Damuni, Z. (1992). Autophosphorylation-activated protein kinase phosphorylates and inactivates protein phosphatase 2A. Proceedings of the National Academy of Sciences of the U.S.A. 88, 43334337.Google Scholar
Hardie, D.G., Haystead, T.A.J. & Sim, A.T.R. (1991). Use of oka-daic acid to inhibit protein phosphatases in intact cells. Methods in Enzymology 201, 469476.CrossRefGoogle ScholarPubMed
Hayashi, F., Lin, G.Y., Matsumoto, H. & Yamazaki, A. (1991). Phosphatidylinositol-stimulated phosphorylation of cGMP phosphodiesterase in vertebrate photoreceptors. Proceedings of the National Academy of Sciences of the U.S.A. 88, 43334337.CrossRefGoogle Scholar
Hemmings, H.C. Jr., Greengard, P., Tung, H.Y.L. & Cohen, P. (1984). DARPP-32, a dopamine-regulated neuronal phosphoprotein, is a potent inhibitor of protein phosphatase-1. Nature 310, 503505.CrossRefGoogle ScholarPubMed
Huang, F.L. & Glinsmann, W.H. (1976). Separation and characterization of two phosphorylase phosphatase inhibitors from rabbit skeletal muscle. Journal of Biochemistry 70, 419426.Google ScholarPubMed
Kamibayashi, C., Estes, R., Slaughter, C. & Mumby, M.C. (1991). Subunit interactions control protein phosphatase 2A. Effects of limited proteolysis, N-ethylmaleimide, and heparin on the interaction of the B subunit. Journal of Biological Chemistry 266, 1325113260.CrossRefGoogle ScholarPubMed
Kass, L. & Renninger, G.H. (1988). Circadian change in function of Limulus ventral photoreceptors. Visual Neuroscience 1, 311.CrossRefGoogle ScholarPubMed
Khatra, B.S., Printz, R., Cobb, C.E. & Corbin, J.D. (1985). Regulatory subunit of cAMP-dependent protein kinase inhibits phos-phoprotein phosphatase. Biochemical and Biophysical Research Communications 130, 567573.CrossRefGoogle ScholarPubMed
Kincaid, R.L. & Vaughan, M. (1988). Purification and properties of calmodulin-activated cyclic nucleotide phosphodiesterase from mammalian brain. Methods in Enzymology 159, 557573.CrossRefGoogle ScholarPubMed
King, A.J., Andjelkovic, N., Hemmings, B.A. & Akhtar, M. (1994). The phosph-opsin phosphatase from bovine rod outer segments. An insight into the mechanism of stimulation of type-2A protein phosphatase activity. European Journal of Biochemistry 225, 383394.CrossRefGoogle ScholarPubMed
Komalavilas, P. & Lincoln, T.M. (1994). Phosphorylation of the inositol 1,4,5–triphosphate receptor by cyclic GMP-dependent protein kinase. Journal of Biological Chemistry 269, 87018707.CrossRefGoogle ScholarPubMed
Kühn, H. (1974). Light-dependent phosphorylation of rhodopsin in living frogs. Nature 250, 588590.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, 473478.CrossRefGoogle ScholarPubMed
Laemmli, U.K. (1970). Cleavage of structural proteins during assembly of the head of phage T4. Nature 277, 680685.CrossRefGoogle Scholar
Lambrecht, H.-G. & Koch, K.-W. (1991). Phosphorylation of recoverin, the calcium-sensitive activator of photoreceptor guanylyl cyclase. FEBS Letters 294, 207209.CrossRefGoogle ScholarPubMed
Lee, R.H., Brown, B.M. & Lolley, R.N. (1984). Light-induced dephosphorylation of a 33 K protein in rod outer segments of rat retina. Biochemistry 23, 19721977.CrossRefGoogle Scholar
Lee, R.H. & Brown, B.M. (1991). Phosphoprotein phosphatases of bovine retinas: Purification and characterization. Investigative Ophthalmology and Visual Neuroscience 32, 1054.Google Scholar
Lee, R.H., Brown, B.M. & Lolley, R.N. (1990). Protein kinase A phosphorylates retinal phosducin on serine 73 in situ. Journal of Biological Chemistry 265, 1586015866.CrossRefGoogle ScholarPubMed
LeVine, H. III., Smith, D.P., Whitney, M., Malicki, D.M., Dolph, P.J., Smith, G.F.H., Burkhart, W. & Zucker, C.S. (1991). Isolation of a novel visual-system-specific arrestin: An in vivo substrate for light-dependent phosphorylation. Mechanisms of Development 33, 1926.CrossRefGoogle Scholar
Levy, S. & Fein, A. (1985). Relationship between light sensitivity and intracellular free Ca concentration in Limulus ventral photoreceptors. A quantitative study using Ca-selective microelectrodes. Journal of General Physiology 85, 805841.CrossRefGoogle Scholar
Lisman, J. & Brown, J.E. (1972). Effects of intracellular ionophoretic injection of calcium and sodium ions on the light response of Limulus ventral photoreceptors. Journal of General Physiology 59, 701719.CrossRefGoogle Scholar
Lisman, J. & Brown., J.E. (1975). Effects of intracellular ionophoretic injection of calcium buffers on light adaptation in Limulus ventral photoreceptors. Journal of General Physiology 66, 489506.CrossRefGoogle Scholar
Lisman, J.E., Faine, G.L. & O'Day, P.M. (1982). Voltage-dependent conductances in Limulus ventral photoreceptors. Journal of General Physiology 79, 187209.CrossRefGoogle ScholarPubMed
Matsumoto, H., Kurien, B.T., Takagi, Y., Kahn, E.S., Kinumi, T., Komori, N., Yamada, T., Hayashi, F., Isono, K., Pak, W.L., Jackson, K.W. & Tobin, S.L. (1994). Phosrestin 1 undergoes the earliest light-induced phosphorylation by a calcium/calmodulin-dependent protein kinase in Drosophila photoreceptors. Neuron 12, 9971010.CrossRefGoogle Scholar
Matsumoto, H. & Pak, W.L. (1984). Light-induced phosphorylation of retina-specific polypeptides of Drosophila in vivo. Science 217, 184186.CrossRefGoogle Scholar
Mayer-Jaekel, R. & Hemmings, B. (1994). Protein phosphatase 2A-a ‘ménage á trois.Trends in Cell Biology 4, 287291.CrossRefGoogle ScholarPubMed
Mulkey, R.M., Endo, S., Shenolikar, S. & Malenka, R.C. (1994). Involvement of a calcineurin/ inhibitor-1 phosphatase cascade in hippocampal long-term depression. Nature 369, 486488.CrossRefGoogle ScholarPubMed
Newton, A.C. & Williams, D.S. (1991). Involvement of protein kinase C in the phosphorylation of rhodopsin. Journal of Biological Chemistry 266, 1772517728.CrossRefGoogle ScholarPubMed
Nimmo, G.A. & Cohen, P. (1978). The regulation of glycogen metabolism. Purification and characterization of protein phosphatase inhibitor-1 from rabbit skeletal muscle. European Journal of Biochemistry 87, 341351.CrossRefGoogle ScholarPubMed
Novak-Hofer, I., Lemos, J.R., Villermain, M. & Levitan, I.B. (1985). Valcium- and cyclic nucleotide-dependent protein kinases and their substrates in Aplysia nervous system. Journal of Biological Chemistry 269, 1028310287.Google Scholar
O'Day, P.M., Gray-Keller, M.P. & Lonergan, M. (1991). Physiological roles of Na+/Ca2+ exchange in Limulus ventral photoreceptors. Journal of General Physiology 97, 369391.CrossRefGoogle ScholarPubMed
O'Day, P.M., Lisman, J.E. & Goldring, M. (1982). Functional significance of voltage-dependent conductances in Limulus ventral photoreceptors. Journal of General Physiology 79, 211232.CrossRefGoogle ScholarPubMed
Orgad, S., Dudai, Y. & Cohen, P. (1987). The protein phosphatases of Drosophila melanogaster and their inhibitors. European Journal of Biochemistry 164, 3138.CrossRefGoogle ScholarPubMed
Palczewski, K., Farber, D.B. & Hargrave, P.A. (1991). Elevated level of protein phosphatase 2A in retinas of rd mice. Experimental Eye Research 53, 101105.CrossRefGoogle ScholarPubMed
Palczewski, K., Hargrave, P.A., McDowell, J.H. & Ingebritsen, T.S. (1989 a). The catalytic subunit of phosphatase 2A dephosphor-ylates phosphoopsin. Biochemistry 28, 415419.CrossRefGoogle ScholarPubMed
Palczewski, K., McDowell, J.H., Ingebritsen, T.S. & Hargrave, P.A. (1989 b). Regulation of rhodopsin dephosphorylation by arrestin. Journal of Biological Chemistry 264, 1577015773.CrossRefGoogle ScholarPubMed
Paulsen, R. & Bentrop, J. (1984). Reversible phosphorylation of opsin induced by irradiation of blowfly retinae. Journal of Comparative Physiology A 155, 3945.CrossRefGoogle Scholar
Payne, R., Corson, D.W., Fein, A. & Berridge, M.J. (1986). Excitation and adaptation of Limulus ventral photoreceptors by inositol 1,4,5 trisphosphate result from a rise in intracellular calcium. Journal of General Physiology 88, 127142.CrossRefGoogle ScholarPubMed
Payne, R. & Fein, A. (1987). Inositol 1,4,5 trisphosphate release cal-cium from specialized sites within Limulus photoreceptors. Journal of Cell Biology 104, 933937.CrossRefGoogle Scholar
Pelech, S. & Cohen, P. (1985). The protein phosphatases involved in cellular regulation. 1. Modulation of protein phosphatases-1 and 2A by histone HI, protamine, polylysine, and heparin. European Journal of Biochemistry 148, 245251.CrossRefGoogle Scholar
Pepose, J.S. & Lisman, J.E. (1978). Voltage-sensitive potassium channels in Limulus photoreceptors. Journal of General Physiology 71, 101120.CrossRefGoogle Scholar
Peterson, G.L. (1977). A simplification of the protein assay method of Lowry et al. which is more applicable. Analytical Biochemistry 83, 346356.CrossRefGoogle Scholar
Reinhardt, P.H., Chung, S., Martin, B.L., Brautigan, D.L. & Levi-tan, I.B. (1991). Modulation of calcium-activated potassium channels from rat brain by protein kinase A and phosphatase 2A. Journal of Neuroscience 11, 16271635.CrossRefGoogle Scholar
Richard, E.A. & Lisman, J.E. (1992). Rhodopsin inactivation is a modulated process in Limulus photoreceptors. Nature 356, 336338.CrossRefGoogle ScholarPubMed
Schmidt, J.A. & Farber, D.B. (1980). Light-induced changes in cAMP levels in Limulus photoreceptors. Biochemical and Biophysical Research Communications 94, 438442.CrossRefGoogle ScholarPubMed
Shin, J., Richard, E. & Lisman, J. (1993). Ca2+ is an obligatory intermediate in the excitation cascade of Limulus photoreceptors. Neuron 11, 845855.CrossRefGoogle ScholarPubMed
Sim, A.T., Ratcliff, E., Mumby, M.C., Villa-Moruzzi, E. & Rostas, J.A.P. (1994). Differential activities of protein phosphatase types 1 and 2A in cytosolic and particulate fractions from rat forebrain. Journal of Neurochemistry 62, 15521559.CrossRefGoogle ScholarPubMed
Smith, W.C., Greenberg, R.M., Hendrix, M.M. & Battelle, B.-A. (1995). Cloning of arrestin from the horsehoe crab lateral eye: Limulus arrestin is a phosphoprotein. Journal of Neurochemistry 64, 113.CrossRefGoogle Scholar
Smith, W.C., Eschweiler, B., Andrews, A.W., Greenberg, R.M. & Battelle, B.-A. (1993). Orcadian efferent input to Limulus retina stimulates the phosphorylation of a protein similar to ninaC gene products of Drosophila. Society for Neuroscience Abstracts 19, 1199.Google Scholar
StrÅlfors, P., Hemmings, H.C. & Greengard, P. (1989). Inhibitors of protein phosphatase-1. Inhibitor-1 of bovine adipose tissue and a dopamine- and cAMP-regulated phosphoprotein of bovine brain are identical. European Journal of Biochemistry 180, 143148.CrossRefGoogle Scholar
Towbin, H., Staehelin, T. & Gorden, J. (1979). Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets. Procedure and some applications. Proceedings of the National Academy of Sciences of the U.S.A. 74, 43504354.CrossRefGoogle Scholar
Tsibris, A.M.N., VanDyke, T.H. & Edwards, S.C. (1994). Protein phosphatase type 2A removes arrestin from the membrane of Limulus photoreceptors and is inhibited by PKA phosphorylation. Society for Neuroscience Abstracts 20, 131.Google Scholar
Tsuda, M., Tsuda, T. & Hirata, H. (1989). Cyclic nucleotides and GTP analogues stimulate light-induced phosphorylation of octopus rhodopsin. FEBS Letters 257, 3840.CrossRefGoogle ScholarPubMed
Tung, H.Y., Alemany, S. & Cohen, P. (1985). The protein phosphatases involved in cellular regulation. 2. Purification, subunit structure and properties of protein phosphatase-2A0, 2A1, and 2A2, from rabbit skeletal muscle. European Journal of Biochemistry 148, 253263.CrossRefGoogle ScholarPubMed
Vandenberg, C.A. & Montal, M. (1984). Light-regulated biochemical events in invertebrate photoreceptors. 2. Light-regulated phosphorylation of rhodopsin and phosphoinisitides in squid photoreceptor membranes. Biochemistry 23, 23472352.CrossRefGoogle ScholarPubMed
Van Dyke, T.H., Windelspeckt, M., Shah, M., Edwards, S.C. & Smith, W.C. (1994). Protein phosphatase 2A-characterization and evidence for Limulus and Drosophila arrestin dephosphorylation. Investigative Ophthalmology and Visual Neuroscience 35, 2129.Google Scholar
Vereb, G., Erdödi, F., Tóth, B. & Bot, G. (1986). Regulatory sub-unit of type II cAMP-dependent protein kinase as substrate and inhibitor of protein phosphatase-1 and -2A. FEBS Letters 197, 139142.CrossRefGoogle Scholar
Wang, L.Y., Orser, B.A., Brautigan, D.L. & MacDonald, J.F. (1994). Regulation of NMDA receptors in cultured hippocampal neurons by protein phosphatases 1 and 2A. Neuron 369, 230232.Google ScholarPubMed
Warren, M.K. & Pierce, S.K. (1982). Two cell volume regulatory systems in the Limulus myocardium: An interaction of ions and quaternary ammonium compounds. Biological Bulletin 163, 504516.CrossRefGoogle Scholar
Weibe, E.M., Wishart, A.C., Edwards, S.C. & Battelle, B.-A. (1989). Calcium/calmodulin-stimulated phosphorylation of photoreceptor proteins in Limulus. Visual Neuroscience 3, 107118.CrossRefGoogle Scholar
White, R.E., Lee, A.B., Shcherbatko, A.D., Lincoln, T.M., Schon-brunn, A. & Armstrong, D.L. (1993). Potassium channel stimulation by natriuretic peptides through cGMP-dependent dephosphorylation. Nature 361, 263266.CrossRefGoogle ScholarPubMed
Wilden, U., Hall, S.W. & Kühn, 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, 11741178.CrossRefGoogle ScholarPubMed
Yamada, T., Takeuchi, Y., Komori, N., Kobashi, H., Sakai, Y., Hotta, Y. & Matsumoto, H. (1990). A 49–kilodalton phosphoprotein in the Drosophila photoreceptor is an arrestin-homolog. Science 248, 483486.CrossRefGoogle ScholarPubMed