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Dynamic regulation of gonadal transposon control across the lifespan of the naturally short-lived African turquoise killifish
Although germline cells are considered to be functionally “immortal,” both the germline and supporting somatic cells in the gonad within an organism experience aging. With increased age at parenthood, the age-related decline in reproductive success has become an important biological issue for an agi...
Autores principales: | , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Cold Spring Harbor Laboratory Press
2023
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9977155/ https://www.ncbi.nlm.nih.gov/pubmed/36577520 http://dx.doi.org/10.1101/gr.277301.122 |
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author | Teefy, Bryan B. Adler, Ari Xu, Alan Hsu, Katelyn Singh, Param Priya Benayoun, Bérénice A. |
author_facet | Teefy, Bryan B. Adler, Ari Xu, Alan Hsu, Katelyn Singh, Param Priya Benayoun, Bérénice A. |
author_sort | Teefy, Bryan B. |
collection | PubMed |
description | Although germline cells are considered to be functionally “immortal,” both the germline and supporting somatic cells in the gonad within an organism experience aging. With increased age at parenthood, the age-related decline in reproductive success has become an important biological issue for an aging population. However, molecular mechanisms underlying reproductive aging across sexes in vertebrates remain poorly understood. To decipher molecular drivers of vertebrate gonadal aging across sexes, we perform longitudinal characterization of the gonadal transcriptome throughout the lifespan in the naturally short-lived African turquoise killifish (Nothobranchius furzeri). By combining mRNA-seq and small RNA-seq from 26 individuals, we characterize the aging gonads of young-adult, middle-aged, and old female and male fish. We analyze changes in transcriptional patterns of genes, transposable elements (TEs), and piRNAs. We find that testes seem to undergo only marginal changes during aging. In contrast, in middle-aged ovaries, the time point associated with peak female fertility in this strain, PIWI pathway components are transiently down-regulated, TE transcription is elevated, and piRNA levels generally decrease, suggesting that egg quality may already be declining at middle-age. Furthermore, we show that piRNA ping-pong biogenesis declines steadily with age in ovaries, whereas it is maintained in aging testes. To our knowledge, this data set represents the most comprehensive transcriptomic data set for vertebrate gonadal aging. This resource also highlights important pathways that are regulated during reproductive aging in either ovaries or testes, which could ultimately be leveraged to help restore aspects of youthful reproductive function. |
format | Online Article Text |
id | pubmed-9977155 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | Cold Spring Harbor Laboratory Press |
record_format | MEDLINE/PubMed |
spelling | pubmed-99771552023-07-01 Dynamic regulation of gonadal transposon control across the lifespan of the naturally short-lived African turquoise killifish Teefy, Bryan B. Adler, Ari Xu, Alan Hsu, Katelyn Singh, Param Priya Benayoun, Bérénice A. Genome Res Resource Although germline cells are considered to be functionally “immortal,” both the germline and supporting somatic cells in the gonad within an organism experience aging. With increased age at parenthood, the age-related decline in reproductive success has become an important biological issue for an aging population. However, molecular mechanisms underlying reproductive aging across sexes in vertebrates remain poorly understood. To decipher molecular drivers of vertebrate gonadal aging across sexes, we perform longitudinal characterization of the gonadal transcriptome throughout the lifespan in the naturally short-lived African turquoise killifish (Nothobranchius furzeri). By combining mRNA-seq and small RNA-seq from 26 individuals, we characterize the aging gonads of young-adult, middle-aged, and old female and male fish. We analyze changes in transcriptional patterns of genes, transposable elements (TEs), and piRNAs. We find that testes seem to undergo only marginal changes during aging. In contrast, in middle-aged ovaries, the time point associated with peak female fertility in this strain, PIWI pathway components are transiently down-regulated, TE transcription is elevated, and piRNA levels generally decrease, suggesting that egg quality may already be declining at middle-age. Furthermore, we show that piRNA ping-pong biogenesis declines steadily with age in ovaries, whereas it is maintained in aging testes. To our knowledge, this data set represents the most comprehensive transcriptomic data set for vertebrate gonadal aging. This resource also highlights important pathways that are regulated during reproductive aging in either ovaries or testes, which could ultimately be leveraged to help restore aspects of youthful reproductive function. Cold Spring Harbor Laboratory Press 2023-01 /pmc/articles/PMC9977155/ /pubmed/36577520 http://dx.doi.org/10.1101/gr.277301.122 Text en © 2023 Teefy et al.; Published by Cold Spring Harbor Laboratory Press https://creativecommons.org/licenses/by-nc/4.0/This article is distributed exclusively by Cold Spring Harbor Laboratory Press for the first six months after the full-issue publication date (see https://genome.cshlp.org/site/misc/terms.xhtml). After six months, it is available under a Creative Commons License (Attribution-NonCommercial 4.0 International), as described at http://creativecommons.org/licenses/by-nc/4.0/ (https://creativecommons.org/licenses/by-nc/4.0/) . |
spellingShingle | Resource Teefy, Bryan B. Adler, Ari Xu, Alan Hsu, Katelyn Singh, Param Priya Benayoun, Bérénice A. Dynamic regulation of gonadal transposon control across the lifespan of the naturally short-lived African turquoise killifish |
title | Dynamic regulation of gonadal transposon control across the lifespan of the naturally short-lived African turquoise killifish |
title_full | Dynamic regulation of gonadal transposon control across the lifespan of the naturally short-lived African turquoise killifish |
title_fullStr | Dynamic regulation of gonadal transposon control across the lifespan of the naturally short-lived African turquoise killifish |
title_full_unstemmed | Dynamic regulation of gonadal transposon control across the lifespan of the naturally short-lived African turquoise killifish |
title_short | Dynamic regulation of gonadal transposon control across the lifespan of the naturally short-lived African turquoise killifish |
title_sort | dynamic regulation of gonadal transposon control across the lifespan of the naturally short-lived african turquoise killifish |
topic | Resource |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9977155/ https://www.ncbi.nlm.nih.gov/pubmed/36577520 http://dx.doi.org/10.1101/gr.277301.122 |
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