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The Journal of Neuroscience, February 15, 2002, 22(4):1280-1289

Tamalin, a PDZ Domain-Containing Protein, Links a Protein Complex Formation of Group 1 Metabotropic Glutamate Receptors and the Guanine Nucleotide Exchange Factor Cytohesins

Jun Kitano¹, Kouji Kimura¹, Yoshimitsu Yamazaki¹, Takeshi Soda¹, Ryuichi Shigemoto², Yoshiaki Nakajima¹, and Shigetada Nakanishi¹

¹ Department of Biological Sciences, Faculty of Medicine, and Department of Molecular and System Biology, Graduate School of Biostudies, Kyoto University, Kyoto, 606-8501, Japan, and ² Division of Cerebral Structure, National Institute for Physiological Sciences, Okazaki, 444-8585, Japan

In this investigation, we report identification and characterization of a 95 kDa postsynaptic density protein (PSD-95)/discs-large/ZO-1 (PDZ) domain-containing protein termed tamalin, also recently named GRP1-associated scaffold protein (GRASP), that interacts with group 1 metabotropic glutamate receptors (mGluRs). The yeast two-hybrid system and in vitro pull-down assays indicated that the PDZ domain-containing, amino-terminal half of tamalin directly binds to the class I PDZ-binding motif of group 1 mGluRs. The C-terminal half of tamalin also bound to cytohesins, the members of guanine nucleotide exchange factors (GEFs) specific for the ADP-ribosylation factor (ARF) family of small GTP-binding proteins. Tamalin mRNA is expressed predominantly in the telencephalic region and highly overlaps with the expression of group 1 mGluR mRNAs. Both tamalin and cytohesin-2 were enriched and codistributed with mGluR1a in postsynaptic membrane fractions. Importantly, recombinant and native mGluR1a/tamalin/cytohesin-2 complexes were coimmunoprecipitated from transfected COS-7 cells and rat brain tissue, respectively. Transfection of tamalin and mutant tamalin lacking a cytohesin-binding domain caused an increase and decrease in cell-surface expression of mGluR1a in COS-7 cells, respectively. Furthermore, adenovirus-mediated expression of tamalin and dominant-negative tamalin facilitated and reduced the neuritic distribution of endogenous mGluR5 in cultured hippocampal neurons, respectively. The results indicate that tamalin plays a key role in the association of group 1 mGluRs with the ARF-specific GEF proteins and contributes to intracellular trafficking and the macromolecular organization of group 1 mGluRs at synapses.

Key words: yeast two-hybrid system; protein interaction; PDZ domain; metabotropic glutamate receptor; tamalin; cytohesin; guanine nucleotide exchange factor (GEF); ADP-ribosylation factor (ARF); cell-surface expression; receptor trafficking

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Copyright © 2002 Society for Neuroscience  0270-6474/02/2241280-10$05.00/0

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