The Lid/KDM5 histone demethylase complex activates a critical effector of the oocyte-to-zygote transition.
Following fertilization of a mature oocyte, the formation of a diploid zygote involves a series of coordinated cellular events that ends with the first embryonic mitosis. In animals, this complex developmental transition is almost entirely controlled by maternal gene products. How such a crucial tra...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
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Public Library of Science (PLoS)
2020-03-01
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| Series: | PLoS Genetics |
| Online Access: | https://doi.org/10.1371/journal.pgen.1008543 |
| _version_ | 1819141285567528960 |
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| author | Daniela Torres-Campana Shuhei Kimura Guillermo A Orsi Béatrice Horard Gérard Benoit Benjamin Loppin |
| author_facet | Daniela Torres-Campana Shuhei Kimura Guillermo A Orsi Béatrice Horard Gérard Benoit Benjamin Loppin |
| author_sort | Daniela Torres-Campana |
| collection | DOAJ |
| description | Following fertilization of a mature oocyte, the formation of a diploid zygote involves a series of coordinated cellular events that ends with the first embryonic mitosis. In animals, this complex developmental transition is almost entirely controlled by maternal gene products. How such a crucial transcriptional program is established during oogenesis remains poorly understood. Here, we have performed an shRNA-based genetic screen in Drosophila to identify genes required to form a diploid zygote. We found that the Lid/KDM5 histone demethylase and its partner, the Sin3A-HDAC1 deacetylase complex, are necessary for sperm nuclear decompaction and karyogamy. Surprisingly, transcriptomic analyses revealed that these histone modifiers are required for the massive transcriptional activation of deadhead (dhd), which encodes a maternal thioredoxin involved in sperm chromatin remodeling. Unexpectedly, while lid knock-down tends to slightly favor the accumulation of its target, H3K4me3, on the genome, this mark was lost at the dhd locus. We propose that Lid/KDM5 and Sin3A cooperate to establish a local chromatin environment facilitating the unusually high expression of dhd, a key effector of the oocyte-to-zygote transition. |
| first_indexed | 2024-12-22T11:52:01Z |
| format | Article |
| id | doaj.art-0e88534090af4489b5cf4f03152cf0a9 |
| institution | Directory Open Access Journal |
| issn | 1553-7390 1553-7404 |
| language | English |
| last_indexed | 2024-12-22T11:52:01Z |
| publishDate | 2020-03-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Genetics |
| spelling | doaj.art-0e88534090af4489b5cf4f03152cf0a92022-12-21T18:26:56ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042020-03-01163e100854310.1371/journal.pgen.1008543The Lid/KDM5 histone demethylase complex activates a critical effector of the oocyte-to-zygote transition.Daniela Torres-CampanaShuhei KimuraGuillermo A OrsiBéatrice HorardGérard BenoitBenjamin LoppinFollowing fertilization of a mature oocyte, the formation of a diploid zygote involves a series of coordinated cellular events that ends with the first embryonic mitosis. In animals, this complex developmental transition is almost entirely controlled by maternal gene products. How such a crucial transcriptional program is established during oogenesis remains poorly understood. Here, we have performed an shRNA-based genetic screen in Drosophila to identify genes required to form a diploid zygote. We found that the Lid/KDM5 histone demethylase and its partner, the Sin3A-HDAC1 deacetylase complex, are necessary for sperm nuclear decompaction and karyogamy. Surprisingly, transcriptomic analyses revealed that these histone modifiers are required for the massive transcriptional activation of deadhead (dhd), which encodes a maternal thioredoxin involved in sperm chromatin remodeling. Unexpectedly, while lid knock-down tends to slightly favor the accumulation of its target, H3K4me3, on the genome, this mark was lost at the dhd locus. We propose that Lid/KDM5 and Sin3A cooperate to establish a local chromatin environment facilitating the unusually high expression of dhd, a key effector of the oocyte-to-zygote transition.https://doi.org/10.1371/journal.pgen.1008543 |
| spellingShingle | Daniela Torres-Campana Shuhei Kimura Guillermo A Orsi Béatrice Horard Gérard Benoit Benjamin Loppin The Lid/KDM5 histone demethylase complex activates a critical effector of the oocyte-to-zygote transition. PLoS Genetics |
| title | The Lid/KDM5 histone demethylase complex activates a critical effector of the oocyte-to-zygote transition. |
| title_full | The Lid/KDM5 histone demethylase complex activates a critical effector of the oocyte-to-zygote transition. |
| title_fullStr | The Lid/KDM5 histone demethylase complex activates a critical effector of the oocyte-to-zygote transition. |
| title_full_unstemmed | The Lid/KDM5 histone demethylase complex activates a critical effector of the oocyte-to-zygote transition. |
| title_short | The Lid/KDM5 histone demethylase complex activates a critical effector of the oocyte-to-zygote transition. |
| title_sort | lid kdm5 histone demethylase complex activates a critical effector of the oocyte to zygote transition |
| url | https://doi.org/10.1371/journal.pgen.1008543 |
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