Abstract
ABSTRACTDuring the maternal-to-zygotic transition (MZT), mRNAs and proteins stored in oocytes are degraded and zygotic genes are activated. We have previously shown that the ubiquitin-proteasome system (UPS)-mediated degradation of maternal proteins plays a role in the onset of zygotic transcription. However, it is still unclear which maternal proteins should be degraded for zygotic genome activation and ensuring subsequent embryonic development. In this study, we screen for these maternal factors that are degraded via the UPS. We thus identified a maternal protein PIASy (protein inhibitor of activated STATy), which is an E3 SUMO ligase. The overexpression of PIASy in fertilized embryos causes developmental arrest at the two-cell stage due to severe abnormal chromosome segregation and impaired zygotic transcription. We find that this developmental role of PIASy is related to its SUMOylation activity. Moreover, PIASy overexpression leads to increased trimethylation of histone H3 lysine 9 (H3K9me3) in two-cell nuclei and enhanced translocation of H3K9me3 methyltransferase to the pronucleus. Hence, PIASy is a maternal factor that is degraded after fertilization and may be important for the proper induction of zygotic genome activation and embryonic development.
Highlights
Oocytes can acquire totipotency through fertilization by sperm
PIASy overexpression in mouse fertilized oocytes causes early developmental arrest Maternal proteins, which are degraded by the ubiquitin-proteasome system (UPS) during maternal-to-zygotic transition (MZT) and can contribute to zygotic transcription and normal development, have not been identified in mice
Proteins for this study were selected based on the following criteria: they were possibly degraded by the UPS after fertilization and were related to transcriptional repression based on the hypothesis in this study: that zygotic genome activation (ZGA) occurs by the degradation of the transcriptional repressor (Fig. 1A, see Materials and Methods for details)
Summary
During the maternal-to-zygotic transition (MZT), maternally inherited RNAs/proteins stored in oocytes are gradually replaced with zygotic transcripts and proteins produced from the genome of the fertilized oocytes, referred to as zygotic genome activation (ZGA). In order to understand the process of acquiring totipotency, factors that contribute to ZGA have been investigated. Dynamic chromatin remodeling plays a role in ZGA Transcriptional activation of the zygotic genome seems regulated by multiple factors, but the mechanisms underlying ZGA have not been fully elucidated
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