Brain transcriptome changes in the aging Drosophila melanogaster accompany olfactory memory performance deficits
Cognitive decline is a common occurrence of the natural aging process in animals and studying age-related changes in gene expression in the brain might shed light on disrupted molecular pathways that play a role in this decline. The fruit fly is a useful neurobiological model for studying aging due...
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| Veröffentlicht in: | PloS one 2018-12, Vol.13 (12), p.e0209405-e0209405 |
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| creator | Pacifico, Rodrigo MacMullen, Courtney M Walkinshaw, Erica Zhang, Xiaofan Davis, Ronald L |
| description | Cognitive decline is a common occurrence of the natural aging process in animals and studying age-related changes in gene expression in the brain might shed light on disrupted molecular pathways that play a role in this decline. The fruit fly is a useful neurobiological model for studying aging due to its short generational time and relatively small brain size. We investigated age-dependent changes in the Drosophila melanogaster whole-brain transcriptome by comparing 5-, 20-, 30- and 40-day-old flies of both sexes. We used RNA-Sequencing of dissected brain samples followed by differential expression, temporal clustering, co-expression network and gene ontology enrichment analyses. We found an overall decline in expression of genes from the mitochondrial oxidative phosphorylation pathway that occurred as part of aging. We also detected, in females, a pattern of continuously declining expression for many neuronal function genes, which was unexpectedly reversed later in life. This group of genes was highly enriched in memory-impairing genes previously identified through an RNAi screen. We also identified deficits in short-term olfactory memory performance in older flies of both sexes, some of which matched the timing of certain changes in the brain transcriptome. Our study provides the first transcriptome profile of aging brains from fruit flies of both sexes, and it will serve as an important resource for those who study aging and cognitive decline in this model. |
| doi_str_mv | 10.1371/journal.pone.0209405 |
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C.</contributor><creatorcontrib>Pacifico, Rodrigo ; MacMullen, Courtney M ; Walkinshaw, Erica ; Zhang, Xiaofan ; Davis, Ronald L ; Skoulakis, Efthimios M. C.</creatorcontrib><description>Cognitive decline is a common occurrence of the natural aging process in animals and studying age-related changes in gene expression in the brain might shed light on disrupted molecular pathways that play a role in this decline. The fruit fly is a useful neurobiological model for studying aging due to its short generational time and relatively small brain size. We investigated age-dependent changes in the Drosophila melanogaster whole-brain transcriptome by comparing 5-, 20-, 30- and 40-day-old flies of both sexes. We used RNA-Sequencing of dissected brain samples followed by differential expression, temporal clustering, co-expression network and gene ontology enrichment analyses. We found an overall decline in expression of genes from the mitochondrial oxidative phosphorylation pathway that occurred as part of aging. We also detected, in females, a pattern of continuously declining expression for many neuronal function genes, which was unexpectedly reversed later in life. This group of genes was highly enriched in memory-impairing genes previously identified through an RNAi screen. We also identified deficits in short-term olfactory memory performance in older flies of both sexes, some of which matched the timing of certain changes in the brain transcriptome. Our study provides the first transcriptome profile of aging brains from fruit flies of both sexes, and it will serve as an important resource for those who study aging and cognitive decline in this model.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0209405</identifier><identifier>PMID: 30576353</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Age ; Age Factors ; Aging ; Aging (natural) ; Aging - physiology ; Animal cognition ; Animals ; Biology and Life Sciences ; Brain ; Brain - metabolism ; Brain research ; Cell cycle ; Clustering ; Cognitive ability ; Cognitive Dysfunction - physiopathology ; Drosophila ; Drosophila melanogaster ; Drosophila Proteins - metabolism ; Female ; Females ; Fruit flies ; Fruits ; Gender differences ; Gene expression ; Gene Expression Profiling ; Gene Regulatory Networks - physiology ; Gene sequencing ; Genes ; Genetic aspects ; Genetic engineering ; Insects ; Male ; Males ; Medicine and Health Sciences ; Memory ; Memory - physiology ; Metabolism ; Mitochondria ; Mitochondria - metabolism ; Models, Animal ; Neurobiology ; Neurosciences ; Olfactory Perception - physiology ; Organisms ; Oxidative Phosphorylation ; Phosphorylation ; Research and Analysis Methods ; Ribonucleic acid ; RNA ; RNA polymerase ; RNA-mediated interference ; Sequence Analysis, RNA ; Sex Factors ; Sexes ; Transcriptome - physiology</subject><ispartof>PloS one, 2018-12, Vol.13 (12), p.e0209405-e0209405</ispartof><rights>COPYRIGHT 2018 Public Library of Science</rights><rights>2018 Pacifico et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 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C.</contributor><creatorcontrib>Pacifico, Rodrigo</creatorcontrib><creatorcontrib>MacMullen, Courtney M</creatorcontrib><creatorcontrib>Walkinshaw, Erica</creatorcontrib><creatorcontrib>Zhang, Xiaofan</creatorcontrib><creatorcontrib>Davis, Ronald L</creatorcontrib><title>Brain transcriptome changes in the aging Drosophila melanogaster accompany olfactory memory performance deficits</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Cognitive decline is a common occurrence of the natural aging process in animals and studying age-related changes in gene expression in the brain might shed light on disrupted molecular pathways that play a role in this decline. The fruit fly is a useful neurobiological model for studying aging due to its short generational time and relatively small brain size. We investigated age-dependent changes in the Drosophila melanogaster whole-brain transcriptome by comparing 5-, 20-, 30- and 40-day-old flies of both sexes. 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Our study provides the first transcriptome profile of aging brains from fruit flies of both sexes, and it will serve as an important resource for those who study aging and cognitive decline in this model.</description><subject>Age</subject><subject>Age Factors</subject><subject>Aging</subject><subject>Aging (natural)</subject><subject>Aging - physiology</subject><subject>Animal cognition</subject><subject>Animals</subject><subject>Biology and Life Sciences</subject><subject>Brain</subject><subject>Brain - metabolism</subject><subject>Brain research</subject><subject>Cell cycle</subject><subject>Clustering</subject><subject>Cognitive ability</subject><subject>Cognitive Dysfunction - physiopathology</subject><subject>Drosophila</subject><subject>Drosophila melanogaster</subject><subject>Drosophila Proteins - metabolism</subject><subject>Female</subject><subject>Females</subject><subject>Fruit flies</subject><subject>Fruits</subject><subject>Gender differences</subject><subject>Gene expression</subject><subject>Gene Expression Profiling</subject><subject>Gene Regulatory Networks - 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C.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Brain transcriptome changes in the aging Drosophila melanogaster accompany olfactory memory performance deficits</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2018-12-21</date><risdate>2018</risdate><volume>13</volume><issue>12</issue><spage>e0209405</spage><epage>e0209405</epage><pages>e0209405-e0209405</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Cognitive decline is a common occurrence of the natural aging process in animals and studying age-related changes in gene expression in the brain might shed light on disrupted molecular pathways that play a role in this decline. The fruit fly is a useful neurobiological model for studying aging due to its short generational time and relatively small brain size. We investigated age-dependent changes in the Drosophila melanogaster whole-brain transcriptome by comparing 5-, 20-, 30- and 40-day-old flies of both sexes. We used RNA-Sequencing of dissected brain samples followed by differential expression, temporal clustering, co-expression network and gene ontology enrichment analyses. We found an overall decline in expression of genes from the mitochondrial oxidative phosphorylation pathway that occurred as part of aging. We also detected, in females, a pattern of continuously declining expression for many neuronal function genes, which was unexpectedly reversed later in life. This group of genes was highly enriched in memory-impairing genes previously identified through an RNAi screen. We also identified deficits in short-term olfactory memory performance in older flies of both sexes, some of which matched the timing of certain changes in the brain transcriptome. Our study provides the first transcriptome profile of aging brains from fruit flies of both sexes, and it will serve as an important resource for those who study aging and cognitive decline in this model.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>30576353</pmid><doi>10.1371/journal.pone.0209405</doi><tpages>e0209405</tpages><orcidid>https://orcid.org/0000-0003-2581-6818</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Age Age Factors Aging Aging (natural) Aging - physiology Animal cognition Animals Biology and Life Sciences Brain Brain - metabolism Brain research Cell cycle Clustering Cognitive ability Cognitive Dysfunction - physiopathology Drosophila Drosophila melanogaster Drosophila Proteins - metabolism Female Females Fruit flies Fruits Gender differences Gene expression Gene Expression Profiling Gene Regulatory Networks - physiology Gene sequencing Genes Genetic aspects Genetic engineering Insects Male Males Medicine and Health Sciences Memory Memory - physiology Metabolism Mitochondria Mitochondria - metabolism Models, Animal Neurobiology Neurosciences Olfactory Perception - physiology Organisms Oxidative Phosphorylation Phosphorylation Research and Analysis Methods Ribonucleic acid RNA RNA polymerase RNA-mediated interference Sequence Analysis, RNA Sex Factors Sexes Transcriptome - physiology |
| title | Brain transcriptome changes in the aging Drosophila melanogaster accompany olfactory memory performance deficits |
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