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Initiation of Parental Genome Reprogramming in Fertilized Oocyte by Splicing Kinase SRPK1-Catalyzed Protamine Phosphorylation

ABSTRACT: We performed ATAC-seq in mouse sperms and fertilized eggs with wild-type or P1 mutation (phosphorylation sites by SRPK1) to capture early genome reprogramming events ~5 hours post insemination. Surprisingly, we detected broadly distributed ATAC-seq reads across the mouse genome to paternal and maternal gametes formed with wild-type and single mutant sperm, and in contrast, we saw individual peaks with zygotes formed with the double mutant sperm. After assigning to paternal and maternal genomes, we found that the reads assignable to paternal genome was decreased with single and double mutants, compare with wild-type. Furthermore, we found the paternal genome in eggs fertilized with the double mutant sperm essentially retained all sperm-specific ATAC-seq peaks, which were also overlapped with the published H3.3 ChIP-seq signals on wild-type sperm, mostly corresponding to TSSs. Strikingly, the ATAC-seq signals on the maternal genome from eggs fertilized with the double mutant P1 sperm were literally identical to those in MII oocyte. Based on these data, we draw two important conclusions: (i) dramatic chromatin remodeling takes place in a highly coordinated fashion in both paternal and maternal pronuclei before they merge, and (ii) SRPK1-catalyzed protamine phosphorylation initiates such synchronized genome reprogramming in both gametes.

ORGANISM(S): Mus musculus

PROVIDER: GSE136403 | GEO | 2020/03/16

REPOSITORIES: GEO

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Project description:Zygotic repair of paternal genome is a key event after fertilization. Spermatozoa accumulate DNA single and double strand breaks during spermatogenesis and can suffer additional damage before fertilization by different factors, including cryopreservation. Fertilization with DNA damaged spermatozoa (DDS) is considered to promote implantation failures and abortions, but also long term effects in the progeny that could be related to a defective repair. Base excision repair (BER) pathway is considered the most active in zygotic DNA repair, but healthy oocytes contain enzymes for all repairing pathways. In this study the effects of the inhibition of the BER pathway in the zygote, were analyzed on the progeny obtained after fertilization with differentially DDS. Massive gene expression (37.394 transcripts) was analyzed after hatching using microarrays. Trout oocytes are easily fertilized with DDS and the high prolificacy allows obtaining live progeny even with a high rate of abortions. Results showed that DDS, even if increased the number of abortions, provided normal progeny. Nevertheless, the zygotic inhibition of PARP, upstream the BER pathway, result 810 differentially expressed genes (DEGs) after hatching. DEGs are related to DNA repair, apoptosis, telomere maintenance or growth and development, revealing a scenario of impaired DNA damage signalization and repair. Down-regulation of the apoptotic cascade was noticed, suggesting a selection of embryos tolerant to residual DNA damage during embryo development. Our results suggest a high zygotic capacity to repair paternal DNA damage and reveals changes in the progeny from defective repairing zygotes whose long term consequences should be deeply analyzed Gene expression was analyzed in trout larvae one day after hatching obtained from differentially DNA damaged sperm with or without zygotic inhibition of the BER pathway of DNA repair. Eggs from two females were pooled and fertilized with sperm fresh (F samples) or cryopreserved using different procedures (LDL and EY samples). Ten min later two batches from each sperm kind were treated with 3-aminobenzamide (3AB) to inhibit the PARP activity. Ten larvae per each one of the 6 treatments (3sperm kind x 2 zygotic treatments) were analyzed after pooling RNA. Four replicates per treatment were done fertilizing eggs from the same females with sperm from 4 different males.

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Initiation of Parental Genome Reprogramming in Fertilized Oocyte by Splicing Kinase SRPK1-Catalyzed Protamine Phosphorylation

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