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Engram-specific transcriptome profiling of contextual memory consolidation

Sparse populations of neurons in the dentate gyrus (DG) of the hippocampus are causally implicated in the encoding of contextual fear memories. However, engram-specific molecular mechanisms underlying memory consolidation remain largely unknown. Here we perform unbiased RNA sequencing of DG engram n...

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Autores principales: Rao-Ruiz, Priyanka, Couey, Jonathan J., Marcelo, Ivo M., Bouwkamp, Christian G., Slump, Denise E., Matos, Mariana R., van der Loo, Rolinka J., Martins, Gabriela J., van den Hout, Mirjam, van IJcken, Wilfred F., Costa, Rui M., van den Oever, Michel C., Kushner, Steven A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6527697/
https://www.ncbi.nlm.nih.gov/pubmed/31110186
http://dx.doi.org/10.1038/s41467-019-09960-x
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author Rao-Ruiz, Priyanka
Couey, Jonathan J.
Marcelo, Ivo M.
Bouwkamp, Christian G.
Slump, Denise E.
Matos, Mariana R.
van der Loo, Rolinka J.
Martins, Gabriela J.
van den Hout, Mirjam
van IJcken, Wilfred F.
Costa, Rui M.
van den Oever, Michel C.
Kushner, Steven A.
author_facet Rao-Ruiz, Priyanka
Couey, Jonathan J.
Marcelo, Ivo M.
Bouwkamp, Christian G.
Slump, Denise E.
Matos, Mariana R.
van der Loo, Rolinka J.
Martins, Gabriela J.
van den Hout, Mirjam
van IJcken, Wilfred F.
Costa, Rui M.
van den Oever, Michel C.
Kushner, Steven A.
author_sort Rao-Ruiz, Priyanka
collection PubMed
description Sparse populations of neurons in the dentate gyrus (DG) of the hippocampus are causally implicated in the encoding of contextual fear memories. However, engram-specific molecular mechanisms underlying memory consolidation remain largely unknown. Here we perform unbiased RNA sequencing of DG engram neurons 24 h after contextual fear conditioning to identify transcriptome changes specific to memory consolidation. DG engram neurons exhibit a highly distinct pattern of gene expression, in which CREB-dependent transcription features prominently (P = 6.2 × 10(−13)), including Atf3 (P = 2.4 × 10(−41)), Penk (P = 1.3 × 10(−15)), and Kcnq3 (P = 3.1 × 10(−12)). Moreover, we validate the functional relevance of the RNAseq findings by establishing the causal requirement of intact CREB function specifically within the DG engram during memory consolidation, and identify a novel group of CREB target genes involved in the encoding of long-term memory.
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spelling pubmed-65276972019-05-22 Engram-specific transcriptome profiling of contextual memory consolidation Rao-Ruiz, Priyanka Couey, Jonathan J. Marcelo, Ivo M. Bouwkamp, Christian G. Slump, Denise E. Matos, Mariana R. van der Loo, Rolinka J. Martins, Gabriela J. van den Hout, Mirjam van IJcken, Wilfred F. Costa, Rui M. van den Oever, Michel C. Kushner, Steven A. Nat Commun Article Sparse populations of neurons in the dentate gyrus (DG) of the hippocampus are causally implicated in the encoding of contextual fear memories. However, engram-specific molecular mechanisms underlying memory consolidation remain largely unknown. Here we perform unbiased RNA sequencing of DG engram neurons 24 h after contextual fear conditioning to identify transcriptome changes specific to memory consolidation. DG engram neurons exhibit a highly distinct pattern of gene expression, in which CREB-dependent transcription features prominently (P = 6.2 × 10(−13)), including Atf3 (P = 2.4 × 10(−41)), Penk (P = 1.3 × 10(−15)), and Kcnq3 (P = 3.1 × 10(−12)). Moreover, we validate the functional relevance of the RNAseq findings by establishing the causal requirement of intact CREB function specifically within the DG engram during memory consolidation, and identify a novel group of CREB target genes involved in the encoding of long-term memory. Nature Publishing Group UK 2019-05-20 /pmc/articles/PMC6527697/ /pubmed/31110186 http://dx.doi.org/10.1038/s41467-019-09960-x Text en © The Author(s) 2019 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Rao-Ruiz, Priyanka
Couey, Jonathan J.
Marcelo, Ivo M.
Bouwkamp, Christian G.
Slump, Denise E.
Matos, Mariana R.
van der Loo, Rolinka J.
Martins, Gabriela J.
van den Hout, Mirjam
van IJcken, Wilfred F.
Costa, Rui M.
van den Oever, Michel C.
Kushner, Steven A.
Engram-specific transcriptome profiling of contextual memory consolidation
title Engram-specific transcriptome profiling of contextual memory consolidation
title_full Engram-specific transcriptome profiling of contextual memory consolidation
title_fullStr Engram-specific transcriptome profiling of contextual memory consolidation
title_full_unstemmed Engram-specific transcriptome profiling of contextual memory consolidation
title_short Engram-specific transcriptome profiling of contextual memory consolidation
title_sort engram-specific transcriptome profiling of contextual memory consolidation
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6527697/
https://www.ncbi.nlm.nih.gov/pubmed/31110186
http://dx.doi.org/10.1038/s41467-019-09960-x
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