Hostname: page-component-78c5997874-s2hrs Total loading time: 0 Render date: 2024-11-04T20:27:11.439Z Has data issue: false hasContentIssue false

Sequential phosphorylation of visual arrestin in intact Limulus photoreceptors: Identification of a highly light-regulated site

Published online by Cambridge University Press:  01 September 2004

OLGA O. SINESHCHEKOVA
Affiliation:
Whitney Laboratory and Department of Neuroscience, University of Florida, St. Augustine
HELENE L.CARDASIS
Affiliation:
Whitney Laboratory and Department of Neuroscience, University of Florida, St. Augustine
EMILY G. SEVERANCE
Affiliation:
Department of Pharmacology, University of South Florida College of Medicine, Tampa
W. CLAY SMITH
Affiliation:
Department of Ophthalmology and Department of Neuroscience, University of Florida, Gainesville
BARBARA-ANNE BATTELLE
Affiliation:
Whitney Laboratory and Department of Neuroscience, University of Florida, St. Augustine

Abstract

The visual arrestins in rhabdomeral photoreceptors are multifunctional phosphoproteins. They are rapidly phosphorylated in response to light, but the functional relevance of this phosphorylation is not yet fully understood. The phosphorylation of Limulus visual arrestin is particularly complex in that it becomes phosphorylated on three sites, and one or more of these site are phosphorylated even in the dark. The purpose of this study was to examine in detail the light-stimulated phosphorylation of each of the three sites in Limulus visual arrestin in intact photoreceptors. We found that light increased the phosphorylation of all three sites (S377, S381, and S396), that S381 is a preferred phosphorylation site, and that S377 and S381 are highly phosphorylated in the dark. The major effect of light was to increase the phosphorylation of S396, the site located closest to the C-terminal and very close to the adaptin binding motif. We speculate that the phosphorylation of this site may be particularly important for regulating the light-driven endocytosis of rhabdomeral membrane.

Type
Research Article
Copyright
2004 Cambridge University Press

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

Alloway, P.G. & Dolph, P.J. (1999). A role for the light-dependent phosphorylation of visual arrestin. Proceedings of the National Academy of Sciences of the U.S.A. 96, 60726077.Google Scholar
Alloway, P.G., Howard, L., & Dolph, P.J. (2000). The formation of stable rhodopsin-arrestin complexes induces apoptosis and photoreceptor cell degeneration. Neuron 28, 129138.Google Scholar
Battelle, B.-A., Andrews, A.W., Kempler, K.E., Edwards, S.C., & Smith, W.C. (2000). Visual arrestin in Limulus is phosphorylated at multiple sites in the light and in the dark. Visual Neuroscience 17, 813822.Google Scholar
Blest, A.D., Kao, L., & Powell, K. (1978). Photoreceptor membrane breakdown in the Spider Dinopis: The fate of rhabdomere products. Cell and Tissue Research 195, 425444.Google Scholar
Boyle, W.J., Van Der Geer, P., & Hunter, T. (1991). Phosphopeptide mapping and phosphoaminoacid analysis by two-dimensional separation on thin-layer cellulose plates. Methods in Enzymology 201, 110148.Google Scholar
Calman, B.G., Andrews, A.E., Rissler, H.M., Edwards, S.C., & Battelle, B.-A. (1996). Calcium/calmodulin-dependent protein kinase II and arrestin phosphorylation in Limulus eyes. Journal of Photochemistry and Photobiology B: Biology 35, 3344.Google Scholar
Castro-Obregón, S., Rao, R.V., Del Rio, G., Chen, S.E., Poksay, K.S., Rabizadeh, S., Vesce, S., Zhang, X.-K., Swanson, R.A., & Bredesen, D.E. (2004). Alternative, non-apoptotic programmed cell death mediated by arrestin 2, ERK2 and Nur77. Journal of Biological Chemistry 279, 1754317553.Google Scholar
Dolph, P.J., Ranganathan, R., Colley, N.J., Hardy, R.W., Socolich, M., & Zuker, C.S. (1993). Arrestin function in inactivation of G protein-coupled receptor rhodopsin in vivo. Science 260, 19101916.Google Scholar
Edwards, S.C. & Battelle, B.-A. (1987). Octopamine- and cAMP-stimulated phosphorylation of a protein in Limulus ventral and lateral eyes. Journal of Neuroscience 7, 28112820.Google Scholar
Edwards, S.C., Wishart, A.C., Wiebe, E.M., & Battelle, B.-A. (1989). Light-regulated proteins in Limulus ventral photoreceptor cells. Visual Neuroscience 3, 95105.Google Scholar
Eguchi, G. & Waterman, T.H. (1967). Changes in retinal fine structure induced in the crab Libinia by light and dark adaptation. Zeitschrift für Zellforschung und Mikroskopische Anatomie 79, 209229.Google Scholar
Hashimoto, Y., Perrino, B.A., & Soderling, T.R. (1990). Identification of an autoinhibitory domain in calcineurin. Journal of Biological Chemistry 265, 19241927.Google Scholar
Hendey, B., Klee, C.B., & Maxfield, F.R. (1992). Inhibition of neutrophil chemokinesis on vitronectin by inhibitors of calcineurin. Science 258, 296299.Google Scholar
Kahn, E.S. & Matsumoto, H. (1997). Calcium/calmodulin-dependent kinase II phosphorylates Drosophila visual arrestin. Journal of Neurochemistry 68, 169175.Google Scholar
Kim, Y.-M., Barak, L.S., Caron, M.G., & Benovic, J. (2002). Regulation of arrestin-3 phosphorylation by casein kinase II. Journal of Biological Chemistry 277, 1683516846.Google Scholar
Kiselev, A., Socolich, M., Vinos, J., Hardy, R.W., Zuker, C.S., & Ranganathan, R. (2000). A molecular pathway for light-dependent photoreceptor apoptosis in Drosophila. Neuron 28, 139152.Google Scholar
Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head bacteriophage T4. Nature 227, 680685.Google Scholar
Laporte, S.A., Oakley, R.H., Holt, J.A., Barak, L.S., & Caron, M.G. (2000). The interaction of β-arrestin with the AP-2 adaptor, rather than clathrin, is required for the clustering of β2-adrenergic receptor into clathrin-coated pits. Journal of Biological Chemistry 275, 2312023126.Google Scholar
Lin, F.-T., Krueger, K.M., Kendall, H.E., Daaka, Y., Fredericks, Z.L., Pitcher, J.A., & Lefkowitz, R.J. (1997). Clathrin-mediated endocytosis of the ß-adrenergic receptor is regulated by phosphorylation/dephosphorylation of the beta-arrestin 1. Journal of Biological Chemistry 272, 3105131057.Google Scholar
Lin, F.-T., Miller, W.E., Lutterll, L.M., & Lefkowitz, R.J. (1999). Feedback regulation of βarrestin1 function by extracellular signal-regulated kinases. Journal of Biological Chemistry 274, 1597115974.Google Scholar
Lin, F.-T., Chen, W., Shenoy, S., Cong, M., Exum, S.T., & Lefkowitz, R.J. (2002). Phosphorylation of βarrestin2 regulates its function in internalization of ß2-adrenergic receptors. Biochemistry 41, 1069210699.Google Scholar
Luttrell, L. & Lefkowitz, R.J. (2002). The role of βarrestins in the termination and transduction of G-protein-coupled receptor signals. Journal of Cell Science 115, 455465.Google Scholar
Matsumoto, H., Kurien, B., 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 I undergoes the earliest light-induced phosphorylation by a calcium/calmodulin-dependent protein kinase in Drosophila photoreceptors. Neuron 12, 9971010.Google Scholar
Mayeenuddin, L.H. & Mitchell, J. (2003). Squid visual arrestin: cDNA cloning and calcium-dependent phosphorylation by rhodopsin kinase (SQRK) Journal of Neurochemistry 85, 592600.Google Scholar
Perrino, B.A., Ng, L.Y., & Soderling, T.R. (1995). Calcium regulation of calcineurin phosphatase activity by its β subunit and calmodulin. Role of the autoinhibitory domain. Journal of Biological Chemistry 270, 340346.Google Scholar
Sacunas, R.B., Papuga, O.M., Malone, M.A., Pearson, A.C.Jr., Marjanovic, M., Stroope, D.G., Weiner, W.W., Chamberlain, S.C., & Battelle, B.-A. (2002). Multiple mechanisms of rhabdom shedding in the lateral eye of Limulus polyphemus. Journal of Comparative Neurology 449, 2642.Google Scholar
Smith, W.C., Greenberg, R.M., Calman, B.G., Hendrix, M.M., Hutchinson, L., Donoso, L.A., & Battelle, B.-A. (1995). Isolation and expression of an arrestin cDNA from the horseshoe crab lateral eye. Journal of Neurochemistry 64, 113.Google Scholar
Stark, W.S., Sapp, R., & Schilly, D. (1988). Rhabdomere turnover and rhodopsin cycle: maintenance of retinular cells in Drosophila melanogaster. Journal of Neurocytology 17, 499509.Google Scholar
White, R.H. (1968). The effect of light and light deprivation upon the ultrastructure of the larval mosquito eye. III. Muiltivesicular bodies and protein uptake Journal of Experimental Zoology 169, 261278.Google Scholar
Wiebe, 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.Google Scholar
Williams, D.S. (1982). Ommatidial structure in relation to turnover of photoreceptor membrane in the locust. Cell and Tissue Research 225, 595617.Google Scholar
Yamada, T., Takeuchi, Y., Komori, N., Kobayashi, H., Sakai, Y., Hotta, Y., & Matsumoto, H. (1990). A 49-kilodalton phosphoprotein is the Drosophila photoreceptor is an arrestin homolog. Science 248, 483486.Google Scholar