LSM1-mediated Major Satellite RNA decay is required for nonequilibrium histone H3.3 incorporation into parental pronuclei

Jiang Zhu, Kang Chen, Yu H. Sun, Wen Ye, Juntao Liu, Dandan Zhang, Nan Su, Li Wu, Xiaochen Kou, Yanhong Zhao, Hong Wang, Shaorong Gao () and Lan Kang ()
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Jiang Zhu: Tongji University
Kang Chen: Tongji University
Yu H. Sun: University of Rochester
Wen Ye: Tongji University
Juntao Liu: Tongji University
Dandan Zhang: Tongji University
Nan Su: Tongji University
Li Wu: Tongji University
Xiaochen Kou: Tongji University
Yanhong Zhao: Tongji University
Hong Wang: Tongji University
Shaorong Gao: Tongji University
Lan Kang: Tongji University

Nature Communications, 2023, vol. 14, issue 1, 1-16

Abstract: Abstract Epigenetic reprogramming of the parental genome is essential for zygotic genome activation and subsequent embryo development in mammals. Asymmetric incorporation of histone H3 variants into the parental genome has been observed previously, but the underlying mechanism remains elusive. In this study, we discover that RNA-binding protein LSM1-mediated major satellite RNA decay plays a central role in the preferential incorporation of histone variant H3.3 into the male pronucleus. Knockdown of Lsm1 disrupts nonequilibrium pronucleus histone incorporation and asymmetric H3K9me3 modification. Subsequently, we find that LSM1 mainly targets major satellite repeat RNA (MajSat RNA) for decay and that accumulated MajSat RNA in Lsm1-depleted oocytes leads to abnormal incorporation of H3.1 into the male pronucleus. Knockdown of MajSat RNA reverses the anomalous histone incorporation and modifications in Lsm1-knockdown zygotes. Our study therefore reveals that accurate histone variant incorporation and incidental modifications in parental pronuclei are specified by LSM1-dependent pericentromeric RNA decay.

Date: 2023
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DOI: 10.1038/s41467-023-36584-z

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