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The Journal of Neuroscience, January 25, 2006, 26(4):1146-1153; doi:10.1523/JNEUROSCI.4289-05.2006

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Cellular/Molecular
Arrestin Translocation Is Induced at a Critical Threshold of Visual Signaling and Is Superstoichiometric to Bleached Rhodopsin

Katherine J. Strissel,¹ Maxim Sokolov,^1,2 Lynn H. Trieu,¹ and Vadim Y. Arshavsky^1,3

¹Department of Ophthalmology, Harvard Medical School and the Massachusetts Eye and Ear Infirmary, Boston, Massachusetts 02114, ²Department of Ophthalmology, West Virginia University and the West Virginia University Eye Institute, Morgantown, West Virginia 26506, and ³Departments of Ophthalmology and Neurobiology, Duke University, Durham, North Carolina 27710

Correspondence should be addressed to Vadim Arshavsky, Department of Ophthalmology, Duke University Medical Center, 5008 Albert Eye Research Institute, 2351 Erwin Road, Durham, NC 27710. Email: vadim.arshavsky{at}duke.edu

Light induces massive translocation of major signaling proteins between the subcellular compartments of photoreceptors. Among them is visual arrestin responsible for quenching photoactivated rhodopsin, which moves into photoreceptor outer segments during illumination. Here, for the first time, we determined the light dependency of arrestin translocation, which revealed two key features of this phenomenon. First, arrestin translocation is triggered when the light intensity approaches a critical threshold corresponding to the upper limits of the normal range of rod responsiveness. Second, the amount of arrestin entering rod outer segments under these conditions is superstoichiometric to the amount of photoactivated rhodopsin, exceeding it by at least 30-fold. We further showed that it is not the absolute amount of excited rhodopsin but rather the extent of downstream cascade activity that triggers translocation. Finally, we demonstrated that the total amount of arrestin in the rod cell is nearly 10-fold higher than previously thought and therefore sufficient to inactivate the entire pool of rhodopsin at any level of illumination. Thus, arrestin movement to the outer segment leads to an increase in the free arrestin concentration and thereby may serve as a powerful mechanism of light adaptation.

Key words: arrestin; photoreceptor; protein translocation; rhodopsin; vision; retina

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Received Oct. 7, 2005; revised Dec. 1, 2005; accepted Dec. 12, 2005.

Correspondence should be addressed to Vadim Arshavsky, Department of Ophthalmology, Duke University Medical Center, 5008 Albert Eye Research Institute, 2351 Erwin Road, Durham, NC 27710. Email: vadim.arshavsky{at}duke.edu

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