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

Authors: Gou, Lan-Tao; Lim, Do-Hwan; Ma, Wubin; Aubol, Brandon E; Hao, Yajing; Wang, Xin; Zhao, Jun; Liang, Zhengyu; Shao, Changwei; Zhang, Xuan; Meng, Fan; Li, Hairi; Zhang, Xiaorong; Xu, Ruiming; Li, Dangsheng; Rosenfeld, Michael G; Mellon, Pamela L; Adams, Joseph A; Liu, Mo-Fang; Fu, Xiang-Dong

Published In Cell, (2020 03 19)

Abstract: The paternal genome undergoes a massive exchange of histone with protamine for compaction into sperm during spermiogenesis. Upon fertilization, this process is potently reversed, which is essential for parental genome reprogramming and subsequent activation; however, it remains poorly understood how this fundamental process is initiated and regulated. Here, we report that the previously characterized splicing kinase SRPK1 initiates this life-beginning event by catalyzing site-specific phosphorylation of protamine, thereby triggering protamine-to-histone exchange in the fertilized oocyte. Interestingly, protamine undergoes a DNA-dependent phase transition to gel-like condensates and SRPK1-mediated phosphorylation likely helps open up such structures to enhance protamine dismissal by nucleoplasmin (NPM2) and enable the recruitment of HIRA for H3.3 deposition. Remarkably, genome-wide assay for transposase-accessible chromatin sequencing (ATAC-seq) analysis reveals that selective chromatin accessibility in both sperm and MII oocytes is largely erased in early pronuclei in a protamine phosphorylation-dependent manner, suggesting that SRPK1-catalyzed phosphorylation initiates a highly synchronized reorganization program in both parental genomes.

PubMed ID: 32169215 Exiting the NIEHS site

MeSH Terms: Animals; Cell Cycle Proteins/metabolism; Cell Nucleus/metabolism; Chromatin Assembly and Disassembly/genetics; Chromatin Assembly and Disassembly/physiology; Chromatin/metabolism*; Chromatin/physiology; Fertilization/genetics; Histones/metabolism; Male; Mice; Mice, Inbred BALB C; Mice, Inbred C57BL; Mice, Knockout; Oocytes/metabolism; Oocytes/physiology; Phosphorylation; Protamine Kinase/genetics; Protamine Kinase/metabolism; Protamines/genetics; Protamines/metabolism*; Protein-Serine-Threonine Kinases/metabolism*; Protein-Serine-Threonine Kinases/physiology; RNA Splicing/genetics; RNA Splicing/physiology; Spermatozoa/metabolism; Transcription Factors/metabolism; Zygote/metabolism

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