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Impaired histone inheritance promotes tumor progression

Author

Listed:
  • Congcong Tian

    (Chinese Academy of Sciences)

  • Jiaqi Zhou

    (Chinese Academy of Sciences)

  • Xinran Li

    (Chinese Academy of Sciences)

  • Yuan Gao

    (Cold Spring Harbor Laboratory)

  • Qing Wen

    (Chinese Academy of Sciences)

  • Xing Kang

    (Chinese Academy of Sciences)

  • Nan Wang

    (Chinese Academy of Sciences)

  • Yuan Yao

    (Chinese Academy of Sciences)

  • Jiuhang Jiang

    (Chinese Academy of Sciences
    South China Agricultural University)

  • Guibing Song

    (Chinese Academy of Sciences
    Northwest A&F University)

  • Tianjun Zhang

    (Chinese Academy of Sciences
    The University of Adelaide)

  • Suili Hu

    (Chinese Academy of Sciences
    South China Agricultural University)

  • JingYi Liao

    (Chinese Academy of Sciences)

  • Chuanhe Yu

    (University of Minnesota)

  • Zhiquan Wang

    (Mayo Clinic)

  • Xiangyu Liu

    (Shenzhen University Health Science Center)

  • Xinhai Pei

    (Shenzhen University Health Science Center)

  • Kuiming Chan

    (City University of Hong Kong
    Shenzhen Research Institute of City University of Hong Kong)

  • Zichuan Liu

    (Tianjin University)

  • Haiyun Gan

    (Chinese Academy of Sciences)

Abstract

Faithful inheritance of parental histones is essential to maintain epigenetic information and cellular identity during cell division. Parental histones are evenly deposited onto the replicating DNA of sister chromatids in a process dependent on the MCM2 subunit of DNA helicase. However, the impact of aberrant parental histone partition on human disease such as cancer is largely unknown. In this study, we construct a model of impaired histone inheritance by introducing MCM2-2A mutation (defective in parental histone binding) in MCF-7 breast cancer cells. The resulting impaired histone inheritance reprograms the histone modification landscapes of progeny cells, especially the repressive histone mark H3K27me3. Lower H3K27me3 levels derepress the expression of genes associated with development, cell proliferation, and epithelial to mesenchymal transition. These epigenetic changes confer fitness advantages to some newly emerged subclones and consequently promote tumor growth and metastasis after orthotopic implantation. In summary, our results indicate that impaired inheritance of parental histones can drive tumor progression.

Suggested Citation

  • Congcong Tian & Jiaqi Zhou & Xinran Li & Yuan Gao & Qing Wen & Xing Kang & Nan Wang & Yuan Yao & Jiuhang Jiang & Guibing Song & Tianjun Zhang & Suili Hu & JingYi Liao & Chuanhe Yu & Zhiquan Wang & Xia, 2023. "Impaired histone inheritance promotes tumor progression," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-39185-y
    DOI: 10.1038/s41467-023-39185-y
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