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The Journal of Neuroscience, January 15, 2003, 23(2):403-415

Modulation of Type 1 Inositol (1,4,5)-Trisphosphate Receptor Function by Protein Kinase A and Protein Phosphatase 1

Tie-Shan Tang^*, Huiping Tu^*, Zhengnan Wang, and Ilya Bezprozvanny

Department of Physiology, University of Texas Southwestern Medical Center, Dallas, Texas 75390

Type 1 inositol (1,4,5)-trisphosphate receptors (InsP₃R1s) play a major role in neuronal calcium (Ca²⁺) signaling. The InsP₃R1s are phosphorylated by protein kinase A (PKA), but the functional consequences of InsP₃R1 phosphorylation and the mechanisms that control the phosphorylated state of neuronal InsP₃R1s are poorly understood. In a yeast two-hybrid screen of rat brain cDNA library with the InsP₃R1-specific bait, we isolated the protein phosphatase 1 (PP1). In biochemical experiments, we confirmed the specificity of the InsP₃R1-PP1 association and immunoprecipitated the InsP₃R1-PP1 complex from rat brain synaptosomes and from the neostriatal lysate. We also established that the association with PP1 facilitates dephosphorylation of PKA-phosphorylated InsP₃R1 by the endogenous neostriatal PP1 and by the recombinant PP1. We demonstrated that exposure of neostriatal slices to 8-bromo-cAMP, dopamine, calyculin A, or cyclosporine A, but not to 10 nM okadaic acid, promotes the phosphorylation of neostriatal InsP₃R1 by PKA in vivo. We discovered that PKA activates and PP1 inhibits the activity of recombinant InsP₃R1 reconstituted into planar lipid bilayers. We found that phosphorylation of InsP₃R1 by PKA induces at least a fourfold increase in the sensitivity of InsP₃R1 to activation by InsP₃ without shifting the peak of InsP₃R1 bell-shaped Ca²⁺ dependence. Based on these data, we suggest that InsP₃R1 may participate in cross talk between cAMP and Ca²⁺ signaling in the neostriatum and possibly in other regions of the brain.

Key words: inositol trisphosphate receptor; calcium signaling; dopamine; protein phosphorylation; yeast two-hybrid; planar lipid bilayers

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^* T.-S.T. and H.T. contributed equally to this work

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Copyright © 2003 Society for Neuroscience  0270-6474/03/232403-13$05.00/0

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