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The Journal of Neuroscience, July 22, 2009, 29(29):9301-9313; doi:10.1523/JNEUROSCI.1367-09.2009

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Cellular/Molecular
Retina-Specific GTPase Accelerator RGS11/Gβ5S/R9AP Is a Constitutive Heterotrimer Selectively Targeted to mGluR6 in ON-Bipolar Neurons

Yan Cao,¹ Ikuo Masuho,¹ Haruhisa Okawa,² Keqiang Xie,¹ Junko Asami,⁴ Paul J. Kammermeier,⁵ Dennis M. Maddox,⁶ Takahisa Furukawa,⁷ Takayoshi Inoue,⁴ Alapakkam P. Sampath,^2,3 and Kirill A. Martemyanov¹

¹Department of Pharmacology, University of Minnesota, Minneapolis, Minnesota 55455, ²Neuroscience Graduate Program and ³Zilkha Neurogenetic Institute and Department of Physiology and Biophysics, University of Southern California, Los Angeles, California 90089, ⁴Department of Biochemistry and Cellular Biology, National Institute of Neuroscience, National Center of Neurology and Psychiatry, Kodaira, Tokyo 187-8502, Japan, ⁵Department of Pharmacology and Physiology, University of Rochester Medical Center, Rochester, New York 14642, ⁶The Jackson Laboratory, Bar Harbor, Maine 04609, and ⁷Department of Developmental Biology, Osaka Bioscience Institute, Suita, Osaka 565-0874, Japan

Correspondence should be addressed to Dr. Kirill A. Martemyanov, Department of Pharmacology, 6-120 Jackson Hall, 321 Church Street SE, Minneapolis, MN 55455. Email: martemyanov{at}umn.edu

Members of the R7 family of the regulators of G-protein signaling (R7 RGS) proteins form multi-subunit complexes that play crucial roles in processing the light responses of retinal neurons. The disruption of these complexes has been shown to lead to the loss of temporal resolution in retinal photoreceptors and deficient synaptic transmission to downstream neurons. Despite the well established role of one member of this family, RGS9-1, in controlling vertebrate phototransduction, the roles and organizational principles of other members in the retina are poorly understood. Here we investigate the composition, localization, and function of complexes containing RGS11, the closest homolog of RGS9-1. We find that RGS11 forms a novel obligatory trimeric complex with the short splice isoform of the type 5 G-protein β subunit (Gβ5) and the RGS9 anchor protein (R9AP). The complex is expressed exclusively in the dendritic tips of ON-bipolar cells in which its localization is accomplished through a direct association with mGluR6, the glutamate receptor essential for the ON-bipolar light response. Although association with both R9AP and mGluR6 contributed to the proteolytic stabilization of the complex, postsynaptic targeting of RGS11 was not determined by its membrane anchor R9AP. Electrophysiological recordings of the light response in mouse rod ON-bipolar cells reveal that the genetic elimination of RGS11 has little effect on the deactivation of G_o in dark-adapted cells or during adaptation to background light. These results suggest that the deactivation of mGluR6 cascade during the light response may require the contribution of multiple GTPase activating proteins.

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Received March 22, 2009; revised May 27, 2009; accepted June 17, 2009.

Correspondence should be addressed to Dr. Kirill A. Martemyanov, Department of Pharmacology, 6-120 Jackson Hall, 321 Church Street SE, Minneapolis, MN 55455. Email: martemyanov{at}umn.edu

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