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The Journal of Neuroscience, August 9, 2006, 26(32):8339-8351; doi:10.1523/JNEUROSCI.0472-06.2006

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Cellular/Molecular
Activity Bidirectionally Regulates AMPA Receptor mRNA Abundance in Dendrites of Hippocampal Neurons

Sonja Y. Grooms, ^* Kyung-Min Noh, ^* Roodland Regis, ^* Gary J. Bassell, Monique K. Bryan, Reed C. Carroll,  and R. Suzanne Zukin 

Department of Neuroscience, Albert Einstein College of Medicine, Bronx, New York 10461

Correspondence should be addressed to Dr. R. Suzanne Zukin, Department of Neuroscience, Albert Einstein College of Medicine, 1300 Morris Park Avenue, Bronx, NY 10461. Email: zukin{at}aecom.yu.edu

Activity-dependent regulation of synaptic AMPA receptor (AMPAR) number is critical to NMDA receptor (NMDAR)-dependent synaptic plasticity. Using quantitative high-resolution in situ hybridization, we show that mRNAs encoding the AMPA-type glutamate receptor subunits (GluRs) 1 and 2 are localized to dendrites of hippocampal neurons and are regulated by paradigms that alter synaptic efficacy. A substantial fraction of synaptic sites contain AMPAR mRNA, consistent with strategic positioning and availability for "on-site" protein synthesis. NMDAR activation depletes dendritic levels of AMPAR mRNAs. The decrease in mRNA occurs via rise in intracellular Ca²⁺, activation of extracellular signal-regulated kinase/mitogen-activated protein kinase signaling, and transcriptional arrest at the level of the nucleus. The decrease in mRNA is accompanied by a long-lasting reduction in synaptic AMPAR number, consistent with reduced synaptic efficacy. In contrast, group I metabotropic GluR signaling promotes microtubule-based trafficking of existing AMPAR mRNAs from the soma to dendrites. Bidirectional regulation of dendritic mRNA abundance represents a potentially powerful means to effect long-lasting changes in synaptic strength.

Key words: messenger RNA; transcription; mRNA trafficking; dendrites; AMPA receptors; synaptic plasticity

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Received Feb. 1, 2006; revised June 17, 2006; accepted June 19, 2006.

Correspondence should be addressed to Dr. R. Suzanne Zukin, Department of Neuroscience, Albert Einstein College of Medicine, 1300 Morris Park Avenue, Bronx, NY 10461. Email: zukin{at}aecom.yu.edu

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