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The Journal of Neuroscience, February 2, 2005, 25(5):1159-1168; doi:10.1523/JNEUROSCI.3953-04.2005

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Cellular/Molecular
Rapid Activity-Driven SNARE-Dependent Trafficking of Nicotinic Receptors on Somatic Spines

Zhaoping Liu, Adam W. Tearle, Qiang Nai, and Darwin K. Berg

Neurobiology Section, Division of Biological Sciences, University of California, San Diego, La Jolla, California 92093-0357

Rapid trafficking of glutamate receptors contributes importantly to synaptic plasticity, but whether similar trafficking extends to other ionotropic receptors is unknown. Nicotinic acetylcholine receptors containing 7 subunits are widely expressed in the nervous system and allow calcium influx. Because of this, 7-containing receptors regulate diverse events, depending on the signaling pathways available. We find that the receptors codistribute with target soluble N-ethylmaleimide-sensitive factor attachment protein receptors (SNAREs) postsynaptically and that nicotinic stimulation rapidly induces SNARE-dependent vesicular endocytosis accompanied by receptor internalization. At the same time, a SNARE-dependent process recruits receptors to the cell surface from internal pools. Overall, the trafficking does not markedly change the number of surface receptors or their combined whole-cell response to nicotine. SNARE-dependent trafficking is needed, however, for the receptors to remain capable of activating the transcription factor cAMP response element-binding protein and attendant gene expression when repeatedly challenged. Thus, trafficking appears to be essential for maintaining functional coupling between 7-receptor responses and downstream signaling.

Key words: nicotinic; receptor; synapse; trafficking; ciliary; postsynaptic; spine; SNARE

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Received Nov 19, 2003; revised December 6, 2004; accepted December 11, 2004.

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