Stress‐sensitive dynamics of miRNAs and Elba1 in Drosophila embryogenesis

Abstract 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 t...

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Main Authors: Lovisa Örkenby, Signe Skog, Helen Ekman, Alessandro Gozzo, Unn Kugelberg, Rashmi Ramesh, Srivathsa Magadi, Gianluca Zambanini, Anna Nordin, Claudio Cantú, Daniel Nätt, Anita Öst
Format: Article
Language:English
Published: Springer Nature 2023-05-01
Series:Molecular Systems Biology
Subjects:
Online Access:https://doi.org/10.15252/msb.202211148
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author Lovisa Örkenby
Signe Skog
Helen Ekman
Alessandro Gozzo
Unn Kugelberg
Rashmi Ramesh
Srivathsa Magadi
Gianluca Zambanini
Anna Nordin
Claudio Cantú
Daniel Nätt
Anita Öst
author_facet Lovisa Örkenby
Signe Skog
Helen Ekman
Alessandro Gozzo
Unn Kugelberg
Rashmi Ramesh
Srivathsa Magadi
Gianluca Zambanini
Anna Nordin
Claudio Cantú
Daniel Nätt
Anita Öst
author_sort Lovisa Örkenby
collection DOAJ
description Abstract 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 wm4h 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 doaj.art-086c71ff79a04aacae7639a3e759f9742024-03-03T11:18:18ZengSpringer NatureMolecular Systems Biology1744-42922023-05-01195n/an/a10.15252/msb.202211148Stress‐sensitive dynamics of miRNAs and Elba1 in Drosophila embryogenesisLovisa Örkenby0Signe Skog1Helen Ekman2Alessandro Gozzo3Unn Kugelberg4Rashmi Ramesh5Srivathsa Magadi6Gianluca Zambanini7Anna Nordin8Claudio Cantú9Daniel Nätt10Anita Öst11Department of Biomedical and Clinical Sciences Linköping University Linköping SwedenDepartment of Biomedical and Clinical Sciences Linköping University Linköping SwedenDepartment of Biomedical and Clinical Sciences Linköping University Linköping SwedenDepartment of Biomedical and Clinical Sciences Linköping University Linköping SwedenDepartment of Biomedical and Clinical Sciences Linköping University Linköping SwedenDepartment of Biomedical and Clinical Sciences Linköping University Linköping SwedenDivision of Neurobiology (NEURO) Linköping University Linköping SwedenDivision of Molecular Medicine and Virology (MMV) Linköping University Linköping SwedenDivision of Molecular Medicine and Virology (MMV) Linköping University Linköping SwedenDivision of Molecular Medicine and Virology (MMV) Linköping University Linköping SwedenDepartment of Biomedical and Clinical Sciences Linköping University Linköping SwedenDepartment of Biomedical and Clinical Sciences Linköping University Linköping SwedenAbstract 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 wm4h 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.https://doi.org/10.15252/msb.202211148DrosophilaElba1EmbryogenesismiRNA/MZT
spellingShingle Lovisa Örkenby
Signe Skog
Helen Ekman
Alessandro Gozzo
Unn Kugelberg
Rashmi Ramesh
Srivathsa Magadi
Gianluca Zambanini
Anna Nordin
Claudio Cantú
Daniel Nätt
Anita Öst
Stress‐sensitive dynamics of miRNAs and Elba1 in Drosophila embryogenesis
Molecular Systems Biology
Drosophila
Elba1
Embryogenesis
miRNA/MZT
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 Drosophila
Elba1
Embryogenesis
miRNA/MZT
url https://doi.org/10.15252/msb.202211148
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