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Transcriptome profiling of aging Drosophila photoreceptors reveals gene expression trends that correlate with visual senescence

BACKGROUND: Aging is associated with functional decline of neurons and increased incidence of both neurodegenerative and ocular disease. Photoreceptor neurons in Drosophila melanogaster provide a powerful model for studying the molecular changes involved in functional senescence of neurons since dec...

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Autores principales: Hall, Hana, Medina, Patrick, Cooper, Daphne A., Escobedo, Spencer E., Rounds, Jeremiah, Brennan, Kaelan J., Vincent, Christopher, Miura, Pedro, Doerge, Rebecca, Weake, Vikki M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5698953/
https://www.ncbi.nlm.nih.gov/pubmed/29162050
http://dx.doi.org/10.1186/s12864-017-4304-3
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author Hall, Hana
Medina, Patrick
Cooper, Daphne A.
Escobedo, Spencer E.
Rounds, Jeremiah
Brennan, Kaelan J.
Vincent, Christopher
Miura, Pedro
Doerge, Rebecca
Weake, Vikki M.
author_facet Hall, Hana
Medina, Patrick
Cooper, Daphne A.
Escobedo, Spencer E.
Rounds, Jeremiah
Brennan, Kaelan J.
Vincent, Christopher
Miura, Pedro
Doerge, Rebecca
Weake, Vikki M.
author_sort Hall, Hana
collection PubMed
description BACKGROUND: Aging is associated with functional decline of neurons and increased incidence of both neurodegenerative and ocular disease. Photoreceptor neurons in Drosophila melanogaster provide a powerful model for studying the molecular changes involved in functional senescence of neurons since decreased visual behavior precedes retinal degeneration. Here, we sought to identify gene expression changes and the genomic features of differentially regulated genes in photoreceptors that contribute to visual senescence. RESULTS: To identify gene expression changes that could lead to visual senescence, we characterized the aging transcriptome of Drosophila sensory neurons highly enriched for photoreceptors. We profiled the nuclear transcriptome of genetically-labeled photoreceptors over a 40 day time course and identified increased expression of genes involved in stress and DNA damage response, and decreased expression of genes required for neuronal function. We further show that combinations of promoter motifs robustly identify age-regulated genes, suggesting that transcription factors are important in driving expression changes in aging photoreceptors. However, long, highly expressed and heavily spliced genes are also more likely to be downregulated with age, indicating that other mechanisms could contribute to expression changes at these genes. Lastly, we identify that circular RNAs (circRNAs) strongly increase during aging in photoreceptors. CONCLUSIONS: Overall, we identified changes in gene expression in aging Drosophila photoreceptors that could account for visual senescence. Further, we show that genomic features predict these age-related changes, suggesting potential mechanisms that could be targeted to slow the rate of age-associated visual decline. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-017-4304-3) contains supplementary material, which is available to authorized users.
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spelling pubmed-56989532017-12-01 Transcriptome profiling of aging Drosophila photoreceptors reveals gene expression trends that correlate with visual senescence Hall, Hana Medina, Patrick Cooper, Daphne A. Escobedo, Spencer E. Rounds, Jeremiah Brennan, Kaelan J. Vincent, Christopher Miura, Pedro Doerge, Rebecca Weake, Vikki M. BMC Genomics Research Article BACKGROUND: Aging is associated with functional decline of neurons and increased incidence of both neurodegenerative and ocular disease. Photoreceptor neurons in Drosophila melanogaster provide a powerful model for studying the molecular changes involved in functional senescence of neurons since decreased visual behavior precedes retinal degeneration. Here, we sought to identify gene expression changes and the genomic features of differentially regulated genes in photoreceptors that contribute to visual senescence. RESULTS: To identify gene expression changes that could lead to visual senescence, we characterized the aging transcriptome of Drosophila sensory neurons highly enriched for photoreceptors. We profiled the nuclear transcriptome of genetically-labeled photoreceptors over a 40 day time course and identified increased expression of genes involved in stress and DNA damage response, and decreased expression of genes required for neuronal function. We further show that combinations of promoter motifs robustly identify age-regulated genes, suggesting that transcription factors are important in driving expression changes in aging photoreceptors. However, long, highly expressed and heavily spliced genes are also more likely to be downregulated with age, indicating that other mechanisms could contribute to expression changes at these genes. Lastly, we identify that circular RNAs (circRNAs) strongly increase during aging in photoreceptors. CONCLUSIONS: Overall, we identified changes in gene expression in aging Drosophila photoreceptors that could account for visual senescence. Further, we show that genomic features predict these age-related changes, suggesting potential mechanisms that could be targeted to slow the rate of age-associated visual decline. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-017-4304-3) contains supplementary material, which is available to authorized users. BioMed Central 2017-11-21 /pmc/articles/PMC5698953/ /pubmed/29162050 http://dx.doi.org/10.1186/s12864-017-4304-3 Text en © The Author(s). 2017 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
Hall, Hana
Medina, Patrick
Cooper, Daphne A.
Escobedo, Spencer E.
Rounds, Jeremiah
Brennan, Kaelan J.
Vincent, Christopher
Miura, Pedro
Doerge, Rebecca
Weake, Vikki M.
Transcriptome profiling of aging Drosophila photoreceptors reveals gene expression trends that correlate with visual senescence
title Transcriptome profiling of aging Drosophila photoreceptors reveals gene expression trends that correlate with visual senescence
title_full Transcriptome profiling of aging Drosophila photoreceptors reveals gene expression trends that correlate with visual senescence
title_fullStr Transcriptome profiling of aging Drosophila photoreceptors reveals gene expression trends that correlate with visual senescence
title_full_unstemmed Transcriptome profiling of aging Drosophila photoreceptors reveals gene expression trends that correlate with visual senescence
title_short Transcriptome profiling of aging Drosophila photoreceptors reveals gene expression trends that correlate with visual senescence
title_sort transcriptome profiling of aging drosophila photoreceptors reveals gene expression trends that correlate with visual senescence
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5698953/
https://www.ncbi.nlm.nih.gov/pubmed/29162050
http://dx.doi.org/10.1186/s12864-017-4304-3
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