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The Journal of Neuroscience, February 2, 2005, 25(5):1037-1049; doi:10.1523/JNEUROSCI.4554-04.2005
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Cellular/Molecular
Association of CaV1.3 L-Type Calcium Channels with Shank
Hua Zhang,1 Anton Maximov,1 Yu Fu,1 Fang Xu,1 Tie-Shan Tang,1 Tatiana Tkatch,2 D. James Surmeier,2 andIlya Bezprozvanny1 1Department of Physiology, University of Texas Southwestern Medical Center at Dallas, Dallas, Texas 75390, and 2Department of Physiology, Feinberg School of Medicine, Northwestern University, Chicago, Illinois 60611
Neurons express multiple types of voltage-gated calcium (Ca2+) channels. Two subtypes of neuronal L-type Ca2+ channels are encoded by CaV1.2 and CaV1.3 pore-forming subunits. Both CaV1.2 and CaV1.3 subunits contain class I PDZ (postsynaptic density-95/Discs large/zona occludens-1) domain-binding consensus at their C termini. In yeast two-hybrid screen of rat brain cDNA library with the C-terminal bait of CaV1.3a (long C-terminal splice variant) L-type Ca2+ channel subunit, we isolated multiple clones of postsynaptic adaptor protein Shank. We demonstrated a specific association of CaV1.3a C termini, but not of CaV1.2 C termini, with Shank PDZ domain in vitro. We further demonstrated that the proline-rich region present in C termini of CaV1.3a subunit binds to Shank Src homology 3 domain. We established that CaV1.3a and Shank localized to postsynaptic locations in cultured rat hippocampal neurons. By expressing epitope-tagged recombinant CaV1.3 subunits in rat hippocampal neuronal cultures, we demonstrated that the presence of Shank-binding motifs in CaV1.3a sequence is both necessary and sufficient for synaptic clustering of CaV1.3 L-type Ca2+ channels. In experiments with dominant-negative peptides and dihydropyridine-resistant CaV1.3a mutants, we demonstrated an importance of Shank-binding motif in CaV1.3a sequence for phosphorylated cAMP response element-binding protein (pCREB) signaling in cultured hippocampal neurons. Our results directly link CaV1.3 neuronal L-type Ca2+ channels to macromolecular signaling complex formed by Shank and other modular adaptor proteins at postsynaptic density and provide novel information about the role played by CaV1.3 L-type Ca2+ channels in pCREB signaling.
Key words: calcium channels; PDZ domains; protein targeting; postsynaptic density; CREB; synapse; synaptic plasticity
Received Aug 9, 2004; revised December 10, 2004; accepted December 14, 2004.
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