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The Journal of Neuroscience, May 16, 2007, 27(20):5484-5494; doi:10.1523/JNEUROSCI.1421-07.2007

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Cellular/Molecular
Subunit Dissociation and Diffusion Determine the Subcellular Localization of Rod and Cone Transducins

Derek H. Rosenzweig,^1 * K. Saidas Nair,^1 * Junhua Wei,² Qiang Wang,¹ Greg Garwin,³ John C. Saari,³ Ching-Kang Chen,⁴ Alan V. Smrcka,⁵ Anand Swaroop,⁶ Janis Lem,⁷ James B. Hurley,² and Vladlen Z. Slepak¹

¹Department of Molecular and Cellular Pharmacology and Neuroscience Program, University of Miami Miller School of Medicine, Miami, Florida 33136, Departments of ²Biochemistry and ³Ophthalmology, University of Washington, Seattle, Washington 98195, ⁴Department of Biochemistry, Virginia Commonwealth University, Richmond, Virginia 23284, ⁵Department of Pharmacology and Physiology, University of Rochester School of Medicine and Dentistry, Rochester, New York 14603, ⁶Departments of Ophthalmology and Visual Sciences, and Human Genetics, University of Michigan, Ann Arbor, Michigan 48109, and ⁷Molecular Cardiology Research Institute, Tufts–New England Medical Center, Boston, Massachusetts 02111

Correspondence should be addressed to either of the following: Vladlen Z. Slepak, Department of Molecular and Cellular Pharmacology and Neuroscience Program, University of Miami Miller School of Medicine, Miami, FL 33136, Email: v.slepak{at}miami.edu; or James B. Hurley, Department of Biochemistry, University of Washington, Seattle, WA 98195, Email: jbhhh{at}u.washington.edu

Activation of rod photoreceptors by light induces a massive redistribution of the heterotrimeric G-protein transducin. In darkness, transducin is sequestered within the membrane-enriched outer segments of the rod cell. In light, it disperses throughout the entire neuron. We show here that redistribution of rod transducin by light requires activation, but it does not require ATP. This observation rules out participation of molecular motors in the redistribution process. In contrast to the light-stimulated redistribution of rod transducin in rods, cone transducin in cones does not redistribute during activation. Remarkably, when cone transducin is expressed in rods, it does undergo light-stimulated redistribution. We show here that the difference in subcellular localization of activated rod and cone G-proteins correlates with their affinity for membranes. Activated rod transducin releases from membranes, whereas activated cone transducin remains bound to membranes. A synthetic peptide that dissociates G-protein complexes independently of activation facilitates dispersion of both rod and cone transducins within the cells. This peptide also facilitates detachment of both G-proteins from the membranes. Together, these results show that it is the dissociation state of transducin that determines its localization in photoreceptors. When rod transducin is stimulated, its subunits dissociate, leave outer segment membranes, and equilibrate throughout the cell. Cone transducin subunits do not dissociate during activation and remain sequestered within the outer segment. These findings indicate that the subunits of some heterotrimeric G-proteins remain associated during activation in their native environments.

Key words: retina; rod; cone; transducin; signal transduction; diffusion

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Received Feb. 7, 2007; accepted April 16, 2007.

Correspondence should be addressed to either of the following: Vladlen Z. Slepak, Department of Molecular and Cellular Pharmacology and Neuroscience Program, University of Miami Miller School of Medicine, Miami, FL 33136, Email: v.slepak{at}miami.edu; or James B. Hurley, Department of Biochemistry, University of Washington, Seattle, WA 98195, Email: jbhhh{at}u.washington.edu

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