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Dynamic expression of long noncoding RNAs and repeat elements in synaptic plasticity

Long-term potentiation (LTP) of synaptic transmission is recognized as a cellular mechanism for learning and memory storage. Although de novo gene transcription is known to be required in the formation of stable LTP, the molecular mechanisms underlying synaptic plasticity remain elusive. Noncoding R...

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Autores principales: Maag, Jesper L. V., Panja, Debabrata, Sporild, Ida, Patil, Sudarshan, Kaczorowski, Dominik C., Bramham, Clive R., Dinger, Marcel E., Wibrand, Karin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4589673/
https://www.ncbi.nlm.nih.gov/pubmed/26483626
http://dx.doi.org/10.3389/fnins.2015.00351
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author Maag, Jesper L. V.
Panja, Debabrata
Sporild, Ida
Patil, Sudarshan
Kaczorowski, Dominik C.
Bramham, Clive R.
Dinger, Marcel E.
Wibrand, Karin
author_facet Maag, Jesper L. V.
Panja, Debabrata
Sporild, Ida
Patil, Sudarshan
Kaczorowski, Dominik C.
Bramham, Clive R.
Dinger, Marcel E.
Wibrand, Karin
author_sort Maag, Jesper L. V.
collection PubMed
description Long-term potentiation (LTP) of synaptic transmission is recognized as a cellular mechanism for learning and memory storage. Although de novo gene transcription is known to be required in the formation of stable LTP, the molecular mechanisms underlying synaptic plasticity remain elusive. Noncoding RNAs have emerged as major regulatory molecules that are abundantly and specifically expressed in the mammalian brain. By combining RNA-seq analysis with LTP induction in the dentate gyrus of live rats, we provide the first global transcriptomic analysis of synaptic plasticity in the adult brain. Expression profiles of mRNAs and long noncoding RNAs (lncRNAs) were obtained at 30 min, 2 and 5 h after high-frequency stimulation of the perforant pathway. The temporal analysis revealed dynamic expression profiles of lncRNAs with many positively, and highly, correlated to protein-coding genes with known roles in synaptic plasticity, suggesting their possible involvement in LTP. In light of observations suggesting a role for retrotransposons in brain function, we examined the expression of various classes of repeat elements. Our analysis identifies dynamic regulation of LINE1 and SINE retrotransposons, and extensive regulation of tRNA. These experiments reveal a hitherto unknown complexity of gene expression in long-term synaptic plasticity involving the dynamic regulation of lncRNAs and repeat elements. These findings provide a broader foundation for elucidating the transcriptional and epigenetic regulation of synaptic plasticity in both the healthy brain and in neurodegenerative and neuropsychiatric disorders.
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spelling pubmed-45896732015-10-19 Dynamic expression of long noncoding RNAs and repeat elements in synaptic plasticity Maag, Jesper L. V. Panja, Debabrata Sporild, Ida Patil, Sudarshan Kaczorowski, Dominik C. Bramham, Clive R. Dinger, Marcel E. Wibrand, Karin Front Neurosci Genetics Long-term potentiation (LTP) of synaptic transmission is recognized as a cellular mechanism for learning and memory storage. Although de novo gene transcription is known to be required in the formation of stable LTP, the molecular mechanisms underlying synaptic plasticity remain elusive. Noncoding RNAs have emerged as major regulatory molecules that are abundantly and specifically expressed in the mammalian brain. By combining RNA-seq analysis with LTP induction in the dentate gyrus of live rats, we provide the first global transcriptomic analysis of synaptic plasticity in the adult brain. Expression profiles of mRNAs and long noncoding RNAs (lncRNAs) were obtained at 30 min, 2 and 5 h after high-frequency stimulation of the perforant pathway. The temporal analysis revealed dynamic expression profiles of lncRNAs with many positively, and highly, correlated to protein-coding genes with known roles in synaptic plasticity, suggesting their possible involvement in LTP. In light of observations suggesting a role for retrotransposons in brain function, we examined the expression of various classes of repeat elements. Our analysis identifies dynamic regulation of LINE1 and SINE retrotransposons, and extensive regulation of tRNA. These experiments reveal a hitherto unknown complexity of gene expression in long-term synaptic plasticity involving the dynamic regulation of lncRNAs and repeat elements. These findings provide a broader foundation for elucidating the transcriptional and epigenetic regulation of synaptic plasticity in both the healthy brain and in neurodegenerative and neuropsychiatric disorders. Frontiers Media S.A. 2015-10-01 /pmc/articles/PMC4589673/ /pubmed/26483626 http://dx.doi.org/10.3389/fnins.2015.00351 Text en Copyright © 2015 Maag, Panja, Sporild, Patil, Kaczorowski, Bramham, Dinger and Wibrand. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Genetics
Maag, Jesper L. V.
Panja, Debabrata
Sporild, Ida
Patil, Sudarshan
Kaczorowski, Dominik C.
Bramham, Clive R.
Dinger, Marcel E.
Wibrand, Karin
Dynamic expression of long noncoding RNAs and repeat elements in synaptic plasticity
title Dynamic expression of long noncoding RNAs and repeat elements in synaptic plasticity
title_full Dynamic expression of long noncoding RNAs and repeat elements in synaptic plasticity
title_fullStr Dynamic expression of long noncoding RNAs and repeat elements in synaptic plasticity
title_full_unstemmed Dynamic expression of long noncoding RNAs and repeat elements in synaptic plasticity
title_short Dynamic expression of long noncoding RNAs and repeat elements in synaptic plasticity
title_sort dynamic expression of long noncoding rnas and repeat elements in synaptic plasticity
topic Genetics
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4589673/
https://www.ncbi.nlm.nih.gov/pubmed/26483626
http://dx.doi.org/10.3389/fnins.2015.00351
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