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...
Main Authors: | , , , , , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
Springer Nature
2023-05-01
|
Series: | Molecular Systems Biology |
Subjects: | |
Online Access: | https://doi.org/10.15252/msb.202211148 |
_version_ | 1797279655241187328 |
---|---|
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. |
first_indexed | 2024-03-07T16:30:08Z |
format | Article |
id | doaj.art-086c71ff79a04aacae7639a3e759f974 |
institution | Directory Open Access Journal |
issn | 1744-4292 |
language | English |
last_indexed | 2024-03-07T16:30:08Z |
publishDate | 2023-05-01 |
publisher | Springer Nature |
record_format | Article |
series | Molecular Systems Biology |
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 |
work_keys_str_mv | AT lovisaorkenby stresssensitivedynamicsofmirnasandelba1indrosophilaembryogenesis AT signeskog stresssensitivedynamicsofmirnasandelba1indrosophilaembryogenesis AT helenekman stresssensitivedynamicsofmirnasandelba1indrosophilaembryogenesis AT alessandrogozzo stresssensitivedynamicsofmirnasandelba1indrosophilaembryogenesis AT unnkugelberg stresssensitivedynamicsofmirnasandelba1indrosophilaembryogenesis AT rashmiramesh stresssensitivedynamicsofmirnasandelba1indrosophilaembryogenesis AT srivathsamagadi stresssensitivedynamicsofmirnasandelba1indrosophilaembryogenesis AT gianlucazambanini stresssensitivedynamicsofmirnasandelba1indrosophilaembryogenesis AT annanordin stresssensitivedynamicsofmirnasandelba1indrosophilaembryogenesis AT claudiocantu stresssensitivedynamicsofmirnasandelba1indrosophilaembryogenesis AT danielnatt stresssensitivedynamicsofmirnasandelba1indrosophilaembryogenesis AT anitaost stresssensitivedynamicsofmirnasandelba1indrosophilaembryogenesis |