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Synaptic-type acetylcholine receptors raise intracellular calcium levels in neurons by two mechanisms

MM Rathouz and DK Berg
Journal of Neuroscience 1 November 1994, 14 (11) 6935-6945; DOI: https://doi.org/10.1523/JNEUROSCI.14-11-06935.1994
MM Rathouz
Department of Biology, University of California, San Diego, La Jolla 92093–0357.
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DK Berg
Department of Biology, University of California, San Diego, La Jolla 92093–0357.
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Abstract

Nicotinic acetylcholine receptors (AChRs) located in the postsynaptic membrane on neurons are responsible for mediating fast, excitatory synaptic transmission. If synaptic AChRs are also highly permeable to calcium as reported recently for several kinds of neuronal AChRs, the synaptic receptors could regulate calcium-dependent events in the neurons in concert with normal transmission. Chick ciliary ganglion neurons have two classes of AChRs, one located predominantly in the synaptic membrane and responsible for synaptic signaling through the ganglion and the other located almost exclusively in nonsynaptic membrane and having no known function. The nonsynaptic receptors can readily elevate intracellular calcium concentrations. The experiments reported here indicate that synaptic-type receptors can raise intracellular calcium levels to the same extent as the nonsynaptic receptors and that they do so not only by being permeable to calcium themselves but also by activating voltage-dependent calcium channels (VDCCs). Currents of equivalent amplitude are obtained through the synaptic-type receptors when neurons are bathed in solutions containing either sodium or calcium as the sole extracellular cation. Measuring the effect of ion substitutions on the reversal potential of the receptors and applying the Goldman-Hodgkin-Katz constant field equation indicates the receptors are at least as permeable to calcium as to sodium. When neurons are loaded with the calcium-sensitive dye fluo-3 and challenged with nicotine, both the synaptic-type and nonsynaptic AChRs substantially elevate intracellular calcium levels under physiological conditions, and do so largely by activating VDCCs. Confirmation that synaptic-type AChRs can elevate intracellular calcium levels in the absence of contributions from VDCCs was obtained from voltage-clamp experiments on neurons loaded with fluo-3. The fluorescence signals indicate that the nicotine-induced calcium increases in neurons voltage clamped at rest are nearly as great as those induced in the same neurons when VDCCs are maximally activated by a voltage step. Calcium flux through AChRs may be particularly important for mediating local changes in calcium concentrations near the plasma membrane, which, in turn, could regulate specific membrane- associated calcium-dependent events.

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The Journal of Neuroscience: 14 (11)
Journal of Neuroscience
Vol. 14, Issue 11
1 Nov 1994
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Synaptic-type acetylcholine receptors raise intracellular calcium levels in neurons by two mechanisms
MM Rathouz, DK Berg
Journal of Neuroscience 1 November 1994, 14 (11) 6935-6945; DOI: 10.1523/JNEUROSCI.14-11-06935.1994

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Synaptic-type acetylcholine receptors raise intracellular calcium levels in neurons by two mechanisms
MM Rathouz, DK Berg
Journal of Neuroscience 1 November 1994, 14 (11) 6935-6945; DOI: 10.1523/JNEUROSCI.14-11-06935.1994
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