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The Journal of Neuroscience, December 1, 2004, 24(48):10980-10992; doi:10.1523/JNEUROSCI.3869-04.2004
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Cellular/Molecular
Phosphotidylinositol 4,5-Bisphosphate Signals Underlie Receptor-Specific Gq/11-Mediated Modulation of N-Type Ca2+ Channels
Nikita Gamper,1 Vitaliy Reznikov,1 Yoichi Yamada,2 Jian Yang,2 andMark S. Shapiro1 1Department of Physiology, University of Texas Health Science Center at San Antonio, San Antonio, Texas 78229, and 2Department of Biological Sciences, Columbia University, New York, New York 10027
Modulation of voltage-gated Ca2+ channels via G-protein-coupled receptors is a prime mechanism regulating neurotransmitter release and synaptic plasticity. Despite extensive studies, the molecular mechanism underlying Gq/11-mediated modulation remains unclear. We found cloned and native N-type Ca2+ channels to be regulated by phosphotidylinositol 4,5-bisphosphate (PIP2). In inside-out oocyte patches, PIP2 greatly attenuated or reversed the observed rundown of expressed channels. In sympathetic neurons, muscarinic M1 ACh receptor suppression of the Ca2+ current (ICa) was temporally correlated with PIP2 hydrolysis, blunted by PIP2 in whole-cell pipettes, attenuated by expression of PIP2-sequestering proteins, and became irreversible when PIP2 synthesis was blocked. We also probed mechanisms of receptor specificity. Although bradykinin also induced PIP2 hydrolysis, it did not inhibit ICa. However, bradykinin receptors became nearly as effective as M1 receptors when PIP2 synthesis, IP3 receptors, or the activity of neuronal Ca2+ sensor-1 were blocked, suggesting that bradykinin receptor-induced intracellular Ca2+ increases stimulate PIP2 synthesis, compensating for PIP2 hydrolysis. We suggest that differential use of PIP2 signals underlies specificity of Gq/11-coupled receptor actions on the channels.
Key words: calcium channel; muscarinic receptor; lipid signaling; bradykinin, G-protein; patch clamp
Received Sep 17, 2004; revised October 20, 2004; accepted October 22, 2004.
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