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J. Biol. Chem., Vol. 280, Issue 32, 29250-29255, August 12, 2005

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Recoverin Undergoes Light-dependent Intracellular Translocation in Rod Photoreceptors^*

Katherine J. Strissel, Polina V. Lishko, Lynn H. Trieu, Matthew J. Kennedy, James B. Hurley, and Vadim Y. Arshavsky¶

From the Department of Ophthalmology, Harvard Medical School and the Massachusetts Eye and Ear Infirmary, Boston, Massachusetts 02114 and the Department of Biochemistry, University of Washington, Seattle, Washington 98195

Photoreceptor cells have a remarkable capacity to adapt the sensitivity and speed of their responses to ever changing conditions of ambient illumination. Recent studies have revealed that a major contributor to this adaptation is the phenomenon of light-driven translocation of key signaling proteins into and out of the photoreceptor outer segment, the cellular compartment where phototransduction takes place. So far, only two such proteins, transducin and arrestin, have been established to be involved in this mechanism. To investigate the extent of this phenomenon we examined additional photoreceptor proteins that might undergo light-driven translocation, focusing on three Ca²⁺-binding proteins, recoverin and guanylate cyclase activating proteins 1 (GCAP1) and GCAP2. The changes in the subcellular distribution of each protein were assessed quantitatively using a recently developed technique combining serial tangential sectioning of mouse retinas with Western blot analysis of the proteins in the individual sections. Our major finding is that light causes a significant reduction of recoverin in rod outer segments, accompanied by its redistribution toward rod synaptic terminals. In both cases the majority of recoverin was found in rod inner segments, with 12% present in the outer segments in the dark and less than 2% remaining in that compartment in the light. We suggest that recoverin translocation is adaptive because it may reduce the inhibitory constraint that recoverin imposes on rhodopsin kinase, an enzyme responsible for quenching the photo-excited rhodopsin during the photoresponse. To the contrary, no translocation of rhodopsin kinase itself or either GCAP was identified.

Received for publication, February 16, 2005 , and in revised form, May 9, 2005.

^* This work was supported by National Institutes of Health Grants EY10336 (to V. Y. A.), EY06641 (to J. B. H.), and Core Grant for Vision Research EY14104 (to V. Y. A.) and a grant from the Massachusetts Lions Eye Research Fund (to V. Y. A.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

^¶ To whom correspondence should be addressed: Dept. of Ophthalmology, Duke University Medical Center, 5008 AERI, Erwin Rd., Durham, NC 27710. Tel.: 919-668-5391; Fax: 919-684-8829; E-mail: vadim.arshavsky{at}duke.edu.

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