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3 March 2022 KDM5-mediated redistribution of H3K4me3 is required for oocyte-to-embryonic transition in cattle
Yanna Dang, Lei Luo, Yan Shi, Shuang Li, Shaohua Wang, Kun Zhang
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Abstract

Reprogramming of histone modifications is critical to safeguard correct gene expression profile during preimplantation development. Of interest, trimethylation of lysine 4 on histone 3 (H3K4me3) exhibits a unique and dynamic landscape with a potential species-specific feature. Here, we address how it is reprogrammed and its functional significance during oocyte maturation and early embryonic development in cows. Notably, the overall signal of H3K4me3 decreased sharply during embryonic genome activation (EGA). By using low input ChIP-seq, we find widespread broad H3K4me3 domains in oocytes and early cleaved embryos. The broad domains are gradually removed after fertilization, which is obviously seen during EGA. Meanwhile, H3K4me3 becomes enriched at promoter regions after the removal of broad H3K4me3. Interestingly, the gene expression level displays a positive correlation with the relative H3K4me3 signal of their promoters when embryos reach 16-cell stage. Importantly, disruption of KDM5 (H3K4me3 demethylases) increases H3K4me3 level, decreases the embryonic developmental rate, and results in dysregulation of over a thousand genes. Meanwhile, KDM5 deficiency causes a redistribution of H3K4me3 across genome. In particular, H3K4me3 in gene body or intergenic regions cannot be removed, and H3K4me3 in promoter regions is aberrantly reduced. Besides, the positive correlation between promoter H3K4me3 enrichment and gene expression level disappears. Overall, we describe the genomic reprogramming of H3K4me3 with a greater resolution during bovine preimplantation development and propose that KDM5-mediated redistribution of H3K4me3 plays an important role in modulating oocyte-to-embryonic transition.

Summary Sentence

KDM5-mediated redistribution of H3K4me3 plays an important role in modulating oocyte-to-embryonic transition.

© The Author(s) 2022. Published by Oxford University Press on behalf of Society for the Study of Reproduction. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com
Yanna Dang, Lei Luo, Yan Shi, Shuang Li, Shaohua Wang, and Kun Zhang "KDM5-mediated redistribution of H3K4me3 is required for oocyte-to-embryonic transition in cattle," Biology of Reproduction 106(6), 1059-1071, (3 March 2022). https://doi.org/10.1093/biolre/ioac047
Received: 26 November 2021; Accepted: 18 February 2022; Published: 3 March 2022
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KEYWORDS
chromatin
Cow
EGA
embryo
H3K4me3
preimplantation
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