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Originally published In Press as doi:10.1074/jbc.M101482200 on April 30, 2001

J. Biol. Chem., Vol. 276, Issue 26, 23805-23815, June 29, 2001
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Modulation of the G Protein Regulator Phosducin by Ca2+/Calmodulin-dependent Protein Kinase II Phosphorylation and 14-3-3 Protein Binding*

Craig D. ThulinDagger §, Justin R. SavageDagger §, Joseph N. McLaughlinDagger , Steven M. TruscottDagger , William M. Old, Natalie G. Ahn||, Katheryn A. Resing, Heidi E. Hamm**, Mark W. BitenskyDagger Dagger , and Barry M. WillardsonDagger §§

From the Dagger  Department of Chemistry and Biochemistry, Brigham Young University, Provo, Utah 84602, the  Department of Chemistry and Biochemistry and the || Howard Hughes Medical Institute, University of Colorado, Boulder, Colorado 80309, the ** Department of Molecular Pharmacology and Biological Chemistry, Northwestern University Medical School, Chicago, Illinois 60611, and the Dagger Dagger  Department of Biomedical Engineering, Boston University, Boston, Massachusetts 02215

Phototransduction is a canonical G protein-mediated cascade of retinal photoreceptor cells that transforms photons into neural responses. Phosducin (Pd) is a Gbeta gamma -binding protein that is highly expressed in photoreceptors. Pd is phosphorylated in dark-adapted retina and is dephosphorylated in response to light. Dephosphorylated Pd binds Gbeta gamma with high affinity and inhibits the interaction of Gbeta gamma with Galpha or other effectors, whereas phosphorylated Pd does not. These results have led to the hypothesis that Pd down-regulates the light response. Consequently, it is important to understand the mechanisms of regulation of Pd phosphorylation. We have previously shown that phosphorylation of Pd by cAMP-dependent protein kinase moderately inhibits its association with Gbeta gamma . In this study, we report that Pd was rapidly phosphorylated by Ca2+/calmodulin-dependent kinase II, resulting in 100-fold greater inhibition of Gbeta gamma binding than cAMP-dependent protein kinase phosphorylation. Furthermore, Pd phosphorylation by Ca2+/calmodulin-dependent kinase II at Ser-54 and Ser-73 led to binding of the phosphoserine-binding protein 14-3-3. Importantly, in vivo decreases in Ca2+ concentration blocked the interaction of Pd with 14-3-3, indicating that Ca2+ controls the phosphorylation state of Ser-54 and Ser-73 in vivo. These results are consistent with a role for Pd in Ca2+-dependent light adaptation processes in photoreceptor cells and also suggest other possible physiological functions.

* The work was supported by National Institutes of Health Grants EY12287 (to B. M. W.), AR43768 (to K. A. R.), and EY06062 (to H. E. H.) and by the Howard Hughes Medical Institute (to N. G. A.).The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

§ These two authors contributed equally to this work.

§§ To whom correspondence should be addressed. Tel.: 801-378-2785; Fax: 801-378-5474; E-mail: bmwillardson@chemdept.byu. edu.

Copyright © 2001 by The American Society for Biochemistry and Molecular Biology, Inc.
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