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Stress‐sensitive dynamics of miRNAs and Elba1 in Drosophila embryogenesis

Early‐life stress can result in life‐long effects that impact adult health and disease risk, but little is known about how such programming is established and maintained. Here, we show that such epigenetic memories can be initiated in the Drosophila embryo before the major wave of zygotic transcript...

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Autores principales: Örkenby, Lovisa, Skog, Signe, Ekman, Helen, Gozzo, Alessandro, Kugelberg, Unn, Ramesh, Rashmi, Magadi, Srivathsa, Zambanini, Gianluca, Nordin, Anna, Cantú, Claudio, Nätt, Daniel, Öst, Anita
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10167479/
https://www.ncbi.nlm.nih.gov/pubmed/36938679
http://dx.doi.org/10.15252/msb.202211148
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author Örkenby, Lovisa
Skog, Signe
Ekman, Helen
Gozzo, Alessandro
Kugelberg, Unn
Ramesh, Rashmi
Magadi, Srivathsa
Zambanini, Gianluca
Nordin, Anna
Cantú, Claudio
Nätt, Daniel
Öst, Anita
author_facet Örkenby, Lovisa
Skog, Signe
Ekman, Helen
Gozzo, Alessandro
Kugelberg, Unn
Ramesh, Rashmi
Magadi, Srivathsa
Zambanini, Gianluca
Nordin, Anna
Cantú, Claudio
Nätt, Daniel
Öst, Anita
author_sort Örkenby, Lovisa
collection PubMed
description Early‐life stress can result in life‐long effects that impact adult health and disease risk, but little is known about how such programming is established and maintained. Here, we show that such epigenetic memories can be initiated in the Drosophila embryo before the major wave of zygotic transcription, and higher‐order chromatin structures are established. An early short heat shock results in elevated levels of maternal miRNA and reduced levels of a subgroup of zygotic genes in stage 5 embryos. Using a Dicer‐1 mutant, we show that the stress‐induced decrease in one of these genes, the insulator‐binding factor Elba1, is dependent on functional miRNA biogenesis. Reduction in Elba1 correlates with the upregulation of early developmental genes and promotes a sustained weakening of heterochromatin in the adult fly as indicated by an increased expression of the PEV w ( m4h ) reporter. We propose that maternal miRNAs, retained in response to an early embryonic heat shock, shape the subsequent de novo heterochromatin establishment that occurs during early development via direct or indirect regulation of some of the earliest expressed genes, including Elba1.
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spelling pubmed-101674792023-05-10 Stress‐sensitive dynamics of miRNAs and Elba1 in Drosophila embryogenesis Örkenby, Lovisa Skog, Signe Ekman, Helen Gozzo, Alessandro Kugelberg, Unn Ramesh, Rashmi Magadi, Srivathsa Zambanini, Gianluca Nordin, Anna Cantú, Claudio Nätt, Daniel Öst, Anita Mol Syst Biol Articles Early‐life stress can result in life‐long effects that impact adult health and disease risk, but little is known about how such programming is established and maintained. Here, we show that such epigenetic memories can be initiated in the Drosophila embryo before the major wave of zygotic transcription, and higher‐order chromatin structures are established. An early short heat shock results in elevated levels of maternal miRNA and reduced levels of a subgroup of zygotic genes in stage 5 embryos. Using a Dicer‐1 mutant, we show that the stress‐induced decrease in one of these genes, the insulator‐binding factor Elba1, is dependent on functional miRNA biogenesis. Reduction in Elba1 correlates with the upregulation of early developmental genes and promotes a sustained weakening of heterochromatin in the adult fly as indicated by an increased expression of the PEV w ( m4h ) reporter. We propose that maternal miRNAs, retained in response to an early embryonic heat shock, shape the subsequent de novo heterochromatin establishment that occurs during early development via direct or indirect regulation of some of the earliest expressed genes, including Elba1. John Wiley and Sons Inc. 2023-03-20 /pmc/articles/PMC10167479/ /pubmed/36938679 http://dx.doi.org/10.15252/msb.202211148 Text en © 2023 The Authors. Published under the terms of the CC BY 4.0 license. https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Articles
Örkenby, Lovisa
Skog, Signe
Ekman, Helen
Gozzo, Alessandro
Kugelberg, Unn
Ramesh, Rashmi
Magadi, Srivathsa
Zambanini, Gianluca
Nordin, Anna
Cantú, Claudio
Nätt, Daniel
Öst, Anita
Stress‐sensitive dynamics of miRNAs and Elba1 in Drosophila embryogenesis
title Stress‐sensitive dynamics of miRNAs and Elba1 in Drosophila embryogenesis
title_full Stress‐sensitive dynamics of miRNAs and Elba1 in Drosophila embryogenesis
title_fullStr Stress‐sensitive dynamics of miRNAs and Elba1 in Drosophila embryogenesis
title_full_unstemmed Stress‐sensitive dynamics of miRNAs and Elba1 in Drosophila embryogenesis
title_short Stress‐sensitive dynamics of miRNAs and Elba1 in Drosophila embryogenesis
title_sort stress‐sensitive dynamics of mirnas and elba1 in drosophila embryogenesis
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10167479/
https://www.ncbi.nlm.nih.gov/pubmed/36938679
http://dx.doi.org/10.15252/msb.202211148
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