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The Journal of Neuroscience, January 31, 2007, 27(5):1151-1160; doi:10.1523/JNEUROSCI.5010-06.2007

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Cellular/Molecular
Transducin Translocation in Rods Is Triggered by Saturation of the GTPase-Activating Complex

Ekaterina S. Lobanova,¹ Stella Finkelstein,¹ Hongman Song,² Stephen H. Tsang,³ Ching-Kang Chen,⁴ Maxim Sokolov,⁵ Nikolai P. Skiba,¹ and Vadim Y. Arshavsky¹

¹Albert Eye Research Institute, Duke University Medical Center, Durham, North Carolina 27710, ²Department of Biochemistry, West Virginia University School of Medicine, Morgantown, West Virginia 26506, ³Brown Glaucoma Laboratory, Edward Harkness Eye Institute, Columbia University, New York, New York 10032, ⁴Department of Biochemistry, Virginia Commonwealth University, Richmond, Virginia 23298, and ⁵Sensory Neuroscience Research Center and West Virginia University Eye Institute, Morgantown, West Virginia 26506

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

Light causes massive translocation of G-protein transducin from the light-sensitive outer segment compartment of the rod photoreceptor cell. Remarkably, significant translocation is observed only when the light intensity exceeds a critical threshold level. We addressed the nature of this threshold using a series of mutant mice and found that the threshold can be shifted to either a lower or higher light intensity, dependent on whether the ability of the GTPase-activating complex to inactivate GTP-bound transducin is decreased or increased. We also demonstrated that the threshold is not dependent on cellular signaling downstream from transducin. Finally, we showed that the extent of transducin subunit translocation is affected by the hydrophobicity of its acyl modification. This implies that interactions with membranes impose a limitation on transducin translocation. Our data suggest that transducin translocation is triggered when the cell exhausts its capacity to activate transducin GTPase, and a portion of transducin remains active for a sufficient time to dissociate from membranes and to escape from the outer segment. Overall, the threshold marks the switch of the rod from the highly light-sensitive mode of operation required under limited lighting conditions to the less-sensitive energy-saving mode beneficial in bright light, when vision is dominated by cones.

Key words: transducin; photoreceptor; protein translocation; GTPase; vision; retina

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Received Nov. 17, 2006; revised Dec. 22, 2006; accepted Dec. 24, 2006.

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

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