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Divergence of RNA localization between rat and mouse neurons reveals the potential for rapid brain evolution

BACKGROUND: Neurons display a highly polarized architecture. Their ability to modify their features under intracellular and extracellular stimuli, known as synaptic plasticity, is a key component of the neurochemical basis of learning and memory. A key feature of synaptic plasticity involves the del...

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Autores principales: Francis, Chantal, Natarajan, Shreedhar, Lee, Miler T, Khaladkar, Mugdha, Buckley, Peter T, Sul, Jai-Yoon, Eberwine, James, Kim, Junhyong
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4203888/
https://www.ncbi.nlm.nih.gov/pubmed/25301173
http://dx.doi.org/10.1186/1471-2164-15-883
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author Francis, Chantal
Natarajan, Shreedhar
Lee, Miler T
Khaladkar, Mugdha
Buckley, Peter T
Sul, Jai-Yoon
Eberwine, James
Kim, Junhyong
author_facet Francis, Chantal
Natarajan, Shreedhar
Lee, Miler T
Khaladkar, Mugdha
Buckley, Peter T
Sul, Jai-Yoon
Eberwine, James
Kim, Junhyong
author_sort Francis, Chantal
collection PubMed
description BACKGROUND: Neurons display a highly polarized architecture. Their ability to modify their features under intracellular and extracellular stimuli, known as synaptic plasticity, is a key component of the neurochemical basis of learning and memory. A key feature of synaptic plasticity involves the delivery of mRNAs to distinct sub-cellular domains where they are locally translated. Regulatory coordination of these spatio-temporal events is critical for synaptogenesis and synaptic plasticity as defects in these processes can lead to neurological diseases. In this work, using microdissected dendrites from primary cultures of hippocampal neurons of two mouse strains (C57BL/6 and Balb/c) and one rat strain (Sprague–Dawley), we investigate via microarrays, subcellular localization of mRNAs in dendrites of neurons to assay the evolutionary differences in subcellular dendritic transcripts localization. RESULTS: Our microarray analysis highlighted significantly greater evolutionary diversification of RNA localization in the dendritic transcriptomes (81% gene identity difference among the top 5% highly expressed genes) compared to the transcriptomes of 11 different central nervous system (CNS) and non-CNS tissues (average of 44% gene identity difference among the top 5% highly expressed genes). Differentially localized genes include many genes involved in CNS function. CONCLUSIONS: Species differences in sub-cellular localization may reflect non-functional neutral drift. However, the functional categories of mRNA showing differential localization suggest that at least part of the divergence may reflect activity-dependent functional differences of neurons, mediated by species-specific RNA subcellular localization mechanisms. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1471-2164-15-883) contains supplementary material, which is available to authorized users.
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spelling pubmed-42038882014-10-22 Divergence of RNA localization between rat and mouse neurons reveals the potential for rapid brain evolution Francis, Chantal Natarajan, Shreedhar Lee, Miler T Khaladkar, Mugdha Buckley, Peter T Sul, Jai-Yoon Eberwine, James Kim, Junhyong BMC Genomics Research Article BACKGROUND: Neurons display a highly polarized architecture. Their ability to modify their features under intracellular and extracellular stimuli, known as synaptic plasticity, is a key component of the neurochemical basis of learning and memory. A key feature of synaptic plasticity involves the delivery of mRNAs to distinct sub-cellular domains where they are locally translated. Regulatory coordination of these spatio-temporal events is critical for synaptogenesis and synaptic plasticity as defects in these processes can lead to neurological diseases. In this work, using microdissected dendrites from primary cultures of hippocampal neurons of two mouse strains (C57BL/6 and Balb/c) and one rat strain (Sprague–Dawley), we investigate via microarrays, subcellular localization of mRNAs in dendrites of neurons to assay the evolutionary differences in subcellular dendritic transcripts localization. RESULTS: Our microarray analysis highlighted significantly greater evolutionary diversification of RNA localization in the dendritic transcriptomes (81% gene identity difference among the top 5% highly expressed genes) compared to the transcriptomes of 11 different central nervous system (CNS) and non-CNS tissues (average of 44% gene identity difference among the top 5% highly expressed genes). Differentially localized genes include many genes involved in CNS function. CONCLUSIONS: Species differences in sub-cellular localization may reflect non-functional neutral drift. However, the functional categories of mRNA showing differential localization suggest that at least part of the divergence may reflect activity-dependent functional differences of neurons, mediated by species-specific RNA subcellular localization mechanisms. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1471-2164-15-883) contains supplementary material, which is available to authorized users. BioMed Central 2014-10-09 /pmc/articles/PMC4203888/ /pubmed/25301173 http://dx.doi.org/10.1186/1471-2164-15-883 Text en © Francis et al.; licensee BioMed Central Ltd. 2014 This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Francis, Chantal
Natarajan, Shreedhar
Lee, Miler T
Khaladkar, Mugdha
Buckley, Peter T
Sul, Jai-Yoon
Eberwine, James
Kim, Junhyong
Divergence of RNA localization between rat and mouse neurons reveals the potential for rapid brain evolution
title Divergence of RNA localization between rat and mouse neurons reveals the potential for rapid brain evolution
title_full Divergence of RNA localization between rat and mouse neurons reveals the potential for rapid brain evolution
title_fullStr Divergence of RNA localization between rat and mouse neurons reveals the potential for rapid brain evolution
title_full_unstemmed Divergence of RNA localization between rat and mouse neurons reveals the potential for rapid brain evolution
title_short Divergence of RNA localization between rat and mouse neurons reveals the potential for rapid brain evolution
title_sort divergence of rna localization between rat and mouse neurons reveals the potential for rapid brain evolution
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4203888/
https://www.ncbi.nlm.nih.gov/pubmed/25301173
http://dx.doi.org/10.1186/1471-2164-15-883
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