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The Journal of Neuroscience, May 10, 2006, 26(19):5204-5214; doi:10.1523/JNEUROSCI.4917-05.2006

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Cellular/Molecular
Two mRNA-Binding Proteins Regulate the Distribution of Syntaxin mRNA in Aplysia Sensory Neurons

Jinming Liu, Jiang-Yuan Hu, Fang Wu, James H. Schwartz, and Samuel Schacher

Center for Neurobiology and Behavior, College of Physicians and Surgeons, Columbia University, New York State Psychiatric Institute, New York, New York 10032

Correspondence should be addressed to Dr. Schacher at the above address. Email: sms2{at}columbia.edu

Targeting mRNAs to different functional domains within neurons is crucial to memory storage. In Aplysia sensory neurons, syntaxin mRNA accumulates at the axon hillock during long-term facilitation of sensory-motor neuron synapses produced by serotonin (5-HT). We find that the 3' untranslated region of Aplysia syntaxin mRNA has two targeting elements, the cytosolic polyadenylation element (CPE) and stem-loop double-stranded structures that appear to interact with mRNA-binding proteins CPEB and Staufen. Blocking the interaction between these targeting elements and their RNA-binding proteins abolished both accumulation at the axon hillock and long-term facilitation. CPEB, which we previously have shown to be upregulated after stimulation with 5-HT, is required for the relocalization of syntaxin mRNA to the axon hillock from the opposite pole in the cell body of the sensory neuron during long-term facilitation, whereas Staufen is required for maintaining the accumulation of the mRNA both at the axon hillock after the treatment with 5-HT and at the opposite pole in stable, unstimulated sensory neurons. Thus, the cooperative actions of the two mRNA-binding proteins serve to direct the distribution of an mRNA encoding a key synaptic protein.

Key words: long-term synaptic plasticity; mRNA-binding proteins; RNA trafficking; double-stranded stem loop structures; long-term memory; cell culture

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Received Nov. 17, 2005; revised April 10, 2006; accepted April 10, 2006.

Correspondence should be addressed to Dr. Schacher at the above address. Email: sms2{at}columbia.edu

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