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Whole-transcriptome changes in gene expression accompany aging of sensory neurons in Aplysia californica

BACKGROUND: Large-scale molecular changes occur during aging and have many downstream consequences on whole-organism function, such as motor function, learning, and memory. The marine mollusk Aplysia californica can be used to study transcriptional changes that occur with age in identified neurons o...

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Autores principales: Greer, Justin B., Schmale, Michael C., Fieber, Lynne A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6042401/
https://www.ncbi.nlm.nih.gov/pubmed/29996779
http://dx.doi.org/10.1186/s12864-018-4909-1
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author Greer, Justin B.
Schmale, Michael C.
Fieber, Lynne A.
author_facet Greer, Justin B.
Schmale, Michael C.
Fieber, Lynne A.
author_sort Greer, Justin B.
collection PubMed
description BACKGROUND: Large-scale molecular changes occur during aging and have many downstream consequences on whole-organism function, such as motor function, learning, and memory. The marine mollusk Aplysia californica can be used to study transcriptional changes that occur with age in identified neurons of the brain, because its simplified nervous system allows for more direct correlations between molecular changes, physiological changes, and their phenotypic outcomes. Behavioral deficits in the tail-withdrawal reflex of aged animals have been correlated with reduced excitation in sensory neurons that control the reflex. RNASeq was used to investigate whole-transcriptome changes in tail-withdrawal sensory neurons of sexually mature and aged Aplysia to correlate transcriptional changes with reduced behavioral and physiological responses. RESULTS: Paired-end sequencing resulted in 210 million reads used for differential expression analysis. Aging significantly altered expression of 1202 transcripts in sensory neurons underlying the tail-withdrawal reflex, with an approximately equal number of these genes up- and down regulated with age. Despite overall bidirectionality of expression changes, > 80% of ion channel genes that were differentially expressed had decreased expression with age. In particular, several voltage-gated K(+) and Ca(2+) channels were down regulated. This marked decrease in ion channel expression may play an important role in previously observed declines in aged sensory neuron excitability. We also observed decreased expression of genes and pathways involved in learning and memory. Genes involved in the stress response showed increased expression in aged Aplysia neurons. CONCLUSIONS: Significantly altered expression of many genes between sexually mature and aged Aplysia suggests large molecular changes that may impact neuronal function. Decreased ion channel mRNA observed could mean fewer receptors present in aged neurons, resulting in reduced excitability of PVC sensory neurons, ultimately leading to reduced tail-withdrawal reflex observed in aged Aplysia. Significant changes in other genes and pathways, such as stress response and learning and memory, have previously been shown to occur with age in many vertebrate organisms. This suggests that some effects of aging are common across many animal phyla. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-018-4909-1) contains supplementary material, which is available to authorized users.
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spelling pubmed-60424012018-07-13 Whole-transcriptome changes in gene expression accompany aging of sensory neurons in Aplysia californica Greer, Justin B. Schmale, Michael C. Fieber, Lynne A. BMC Genomics Research Article BACKGROUND: Large-scale molecular changes occur during aging and have many downstream consequences on whole-organism function, such as motor function, learning, and memory. The marine mollusk Aplysia californica can be used to study transcriptional changes that occur with age in identified neurons of the brain, because its simplified nervous system allows for more direct correlations between molecular changes, physiological changes, and their phenotypic outcomes. Behavioral deficits in the tail-withdrawal reflex of aged animals have been correlated with reduced excitation in sensory neurons that control the reflex. RNASeq was used to investigate whole-transcriptome changes in tail-withdrawal sensory neurons of sexually mature and aged Aplysia to correlate transcriptional changes with reduced behavioral and physiological responses. RESULTS: Paired-end sequencing resulted in 210 million reads used for differential expression analysis. Aging significantly altered expression of 1202 transcripts in sensory neurons underlying the tail-withdrawal reflex, with an approximately equal number of these genes up- and down regulated with age. Despite overall bidirectionality of expression changes, > 80% of ion channel genes that were differentially expressed had decreased expression with age. In particular, several voltage-gated K(+) and Ca(2+) channels were down regulated. This marked decrease in ion channel expression may play an important role in previously observed declines in aged sensory neuron excitability. We also observed decreased expression of genes and pathways involved in learning and memory. Genes involved in the stress response showed increased expression in aged Aplysia neurons. CONCLUSIONS: Significantly altered expression of many genes between sexually mature and aged Aplysia suggests large molecular changes that may impact neuronal function. Decreased ion channel mRNA observed could mean fewer receptors present in aged neurons, resulting in reduced excitability of PVC sensory neurons, ultimately leading to reduced tail-withdrawal reflex observed in aged Aplysia. Significant changes in other genes and pathways, such as stress response and learning and memory, have previously been shown to occur with age in many vertebrate organisms. This suggests that some effects of aging are common across many animal phyla. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-018-4909-1) contains supplementary material, which is available to authorized users. BioMed Central 2018-07-11 /pmc/articles/PMC6042401/ /pubmed/29996779 http://dx.doi.org/10.1186/s12864-018-4909-1 Text en © The Author(s). 2018 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided 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 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
Greer, Justin B.
Schmale, Michael C.
Fieber, Lynne A.
Whole-transcriptome changes in gene expression accompany aging of sensory neurons in Aplysia californica
title Whole-transcriptome changes in gene expression accompany aging of sensory neurons in Aplysia californica
title_full Whole-transcriptome changes in gene expression accompany aging of sensory neurons in Aplysia californica
title_fullStr Whole-transcriptome changes in gene expression accompany aging of sensory neurons in Aplysia californica
title_full_unstemmed Whole-transcriptome changes in gene expression accompany aging of sensory neurons in Aplysia californica
title_short Whole-transcriptome changes in gene expression accompany aging of sensory neurons in Aplysia californica
title_sort whole-transcriptome changes in gene expression accompany aging of sensory neurons in aplysia californica
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6042401/
https://www.ncbi.nlm.nih.gov/pubmed/29996779
http://dx.doi.org/10.1186/s12864-018-4909-1
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