IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-36584-z.html
   My bibliography  Save this article

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

Author

Listed:
  • Jiang Zhu

    (Tongji University
    Tongji University)

  • Kang Chen

    (Tongji University
    Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • 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
    Tongji University
    Tongji University)

  • Lan Kang

    (Tongji University
    Tongji University)

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.

Suggested Citation

  • 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 & Lan Kang, 2023. "LSM1-mediated Major Satellite RNA decay is required for nonequilibrium histone H3.3 incorporation into parental pronuclei," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-36584-z
    DOI: 10.1038/s41467-023-36584-z
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-36584-z
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-36584-z?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Xiongjun Wang & Ruilong Liu & Wencheng Zhu & Huiying Chu & Hua Yu & Ping Wei & Xueyuan Wu & Hongwen Zhu & Hong Gao & Ji Liang & Guohui Li & Weiwei Yang, 2019. "UDP-glucose accelerates SNAI1 mRNA decay and impairs lung cancer metastasis," Nature, Nature, vol. 571(7763), pages 127-131, July.
    2. Tie-Gang Meng & Qian Zhou & Xue-Shan Ma & Xiao-Yu Liu & Qing-Ren Meng & Xian-Ju Huang & Hong-Lin Liu & Wen-Long Lei & Zheng-Hui Zhao & Ying-Chun Ouyang & Yi Hou & Heide Schatten & Xiang-Hong Ou & Zhen, 2020. "PRC2 and EHMT1 regulate H3K27me2 and H3K27me3 establishment across the zygote genome," Nature Communications, Nature, vol. 11(1), pages 1-12, December.
    3. S. Sanulli & M. J. Trnka & V. Dharmarajan & R. W. Tibble & B. D. Pascal & A. L. Burlingame & P. R. Griffin & J. D. Gross & G. J. Narlikar, 2019. "HP1 reshapes nucleosome core to promote phase separation of heterochromatin," Nature, Nature, vol. 575(7782), pages 390-394, November.
    4. Azusa Inoue & Lan Jiang & Falong Lu & Tsukasa Suzuki & Yi Zhang, 2017. "Maternal H3K27me3 controls DNA methylation-independent imprinting," Nature, Nature, vol. 547(7664), pages 419-424, July.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Ting Peng & Yingping Hou & Haowei Meng & Yong Cao & Xiaotian Wang & Lumeng Jia & Qing Chen & Yang Zheng & Yujie Sun & Hebing Chen & Tingting Li & Cheng Li, 2023. "Mapping nucleolus-associated chromatin interactions using nucleolus Hi-C reveals pattern of heterochromatin interactions," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    2. Mathew Pette & Andrew Dimond & António M. Galvão & Steven J. Millership & Wilson To & Chiara Prodani & Gráinne McNamara & Ludovica Bruno & Alessandro Sardini & Zoe Webster & James McGinty & Paul M. W., 2022. "Epigenetic changes induced by in utero dietary challenge result in phenotypic variability in successive generations of mice," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    3. Jorge Mata-Garrido & Yao Xiang & Yunhua Chang-Marchand & Caroline Reisacher & Elisabeth Ageron & Ida Chiara Guerrera & Iñigo Casafont & Aurelia Bruneau & Claire Cherbuy & Xavier Treton & Anne Dumay & , 2022. "The Heterochromatin protein 1 is a regulator in RNA splicing precision deficient in ulcerative colitis," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    4. Lidice González & Daniel Kolbin & Christian Trahan & Célia Jeronimo & François Robert & Marlene Oeffinger & Kerry Bloom & Stephen W. Michnick, 2023. "Adaptive partitioning of a gene locus to the nuclear envelope in Saccharomyces cerevisiae is driven by polymer-polymer phase separation," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    5. Hua Yu & Zhen Sun & Tianyu Tan & Hongru Pan & Jing Zhao & Ling Zhang & Jiayu Chen & Anhua Lei & Yuqing Zhu & Lang Chen & Yuyan Xu & Yaxin Liu & Ming Chen & Jinghao Sheng & Zhengping Xu & Pengxu Qian &, 2021. "rRNA biogenesis regulates mouse 2C-like state by 3D structure reorganization of peri-nucleolar heterochromatin," Nature Communications, Nature, vol. 12(1), pages 1-21, December.
    6. Seiichi Yano & Takashi Ishiuchi & Shusaku Abe & Satoshi H. Namekawa & Gang Huang & Yoshihiro Ogawa & Hiroyuki Sasaki, 2022. "Histone H3K36me2 and H3K36me3 form a chromatin platform essential for DNMT3A-dependent DNA methylation in mouse oocytes," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    7. Naohiro Kuwayama & Tomoya Kujirai & Yusuke Kishi & Rina Hirano & Kenta Echigoya & Lingyan Fang & Sugiko Watanabe & Mitsuyoshi Nakao & Yutaka Suzuki & Kei-ichiro Ishiguro & Hitoshi Kurumizaka & Yukiko , 2023. "HMGA2 directly mediates chromatin condensation in association with neuronal fate regulation," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    8. Beatriz del Blanco & Sergio Niñerola & Ana M. Martín-González & Juan Paraíso-Luna & Minji Kim & Rafael Muñoz-Viana & Carina Racovac & Jose V. Sanchez-Mut & Yijun Ruan & Ángel Barco, 2024. "Kdm1a safeguards the topological boundaries of PRC2-repressed genes and prevents aging-related euchromatinization in neurons," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    9. Xiaoqing Nie & Qianhua Xu & Chengpeng Xu & Fengling Chen & Qizhi Wang & Dandan Qin & Rui Wang & Zheng Gao & Xukun Lu & Xinai Yang & Yu Wu & Chen Gu & Wei Xie & Lei Li, 2023. "Maternal TDP-43 interacts with RNA Pol II and regulates zygotic genome activation," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    10. Gayan I. Balasooriya & David L. Spector, 2022. "Allele-specific differential regulation of monoallelically expressed autosomal genes in the cardiac lineage," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    11. Xiaowen Lyu & M. Jordan Rowley & Michael J. Kulik & Stephen Dalton & Victor G. Corces, 2023. "Regulation of CTCF loop formation during pancreatic cell differentiation," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    12. Tao Zhang & Na Zhang & Jing Xing & Shuhua Zhang & Yulu Chen & Daichao Xu & Jinyang Gu, 2023. "UDP-glucuronate metabolism controls RIPK1-driven liver damage in nonalcoholic steatohepatitis," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    13. Natalia Benetti & Quentin Gouil & Andres Tapia del Fierro & Tamara Beck & Kelsey Breslin & Andrew Keniry & Edwina McGlinn & Marnie E. Blewitt, 2022. "Maternal SMCHD1 regulates Hox gene expression and patterning in the mouse embryo," Nature Communications, Nature, vol. 13(1), pages 1-13, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-36584-z. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.