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Transcription of new RNA is crucial for maintaining synaptic plasticity, learning and memory. Although the importance of synaptic plasticity-related messenger RNAs (mRNAs) is well established, the role of a large group of long non-coding RNAs (lncRNAs) in long-term potentiation (LTP) is not known. In this study, we demonstrated the expression of a lncRNA cluster, namely maternally expressed gene 3 ( Meg3 ), retrotransposon-like gene 1-anti-sense ( Rtl1-AS ),  Meg8  and  Meg9 , which is located in the maternally imprinted  Dlk1-Dio3  region on mouse chromosome 12qF1, in primary cortical neurons following glycine stimulation in an N-Methyl-D-aspartate receptor (NMDAR)-dependent manner. Importantly, we also validated the expression of  Meg3 ,  Meg8  and  Meg9  in the hippocampus of mice following cued fear conditioning  in vivo . Interestingly,  Meg3  is the only lncRNA that is expressed in the nucleus and cytoplasm. Further analysis revealed that  Meg3  loss of function blocked the glycine-induced increase of the GluA1 subunit of AMPA receptors on the plasma membrane, a major hallmark of LTP. This aberrant trafficking of AMPA receptors correlated with the dysregulation of the phosphatidylinoside-3-kinase (PI3K)/AKT signaling pathway and the downregulation of the lipid phosphatase and tensin homolog (PTEN). These findings provide the first evidence for a functional role of the lncRNA  Meg3  in the intricate regulation of the PTEN/PI3K/AKT signaling cascade during synaptic plasticity in neurons.

The Activity-Induced Long Non-Coding RNA Meg3 Modulates AMPA Receptor Surface Expression in Primary Cortical Neurons