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Allelic reprogramming of the histone modification H3K4me3 in early mammalian development

机译：组蛋白修饰H3K4me3在哺乳动物早期发育中的等位基因重编程

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摘要

Histone modifications are fundamental epigenetic regulators that control many crucial cellular processes(1) . However, whether these marks can be passed on from mammalian gametes to the next generation is a long-standing question that remains unanswered. Here, by developing a highly sensitive approach, STAR ChIP-seq, we provide a panoramic view of the landscape of H3K4me3, a histone hallmark for transcription initiation(2), from developing gametes to post-implantation embryos. We find that upon fertilization, extensive reprogramming occurs on the paternal genome, as H3K4me3 peaks are depleted in zygotes but are readily observed after major zygotic genome activation at the late two-cell stage. On the maternal genome, we unexpectedly find a non-canonical form of H3K4me3 (ncH3K4me3) in full-grown and mature oocytes, which exists as broad peaks at promoters and a large number of distal loci. Such broad H3K4me3 peaks are in contrast to the typical sharp H3K4me3 peaks restricted to CpG-rich regions of promoters. Notably, ncH3K4me3 in oocytes overlaps almost exclusively with partially methylated DNA domains. It is then inherited in preimplantation embryos, before being erased in the late two-cell embryos, when canonical H3K4me3 starts to be established. The removal of ncH3K4me3 requires zygotic transcription but is independent of DNA replication-mediated passive dilution. Finally, downregulation of H3K4me3 in full-grown oocytes by overexpression of the H3K4me3 demethylase KDM5B is associated with defects in genome silencing. Taken together, these data unveil inheritance and highly dynamic reprogramming of the epigenome in early mammalian development.
机译：组蛋白修饰是控制许多关键细胞过程的基本表观遗传调节剂（1）。但是，这些标记是否可以从哺乳动物配子传给下一代，这是一个长期存在的问题，至今尚未得到解答。在这里，通过开发高度敏感的方法STAR ChIP-seq，我们提供了H3K4me3的全景图，H3K4me3是转录起始的组蛋白标志（2），从发育配子到植入后的胚胎。我们发现受精后，在父本基因组上发生大量的重编程，因为H3K4me3峰在受精卵中被耗尽，但是在主要的合子基因组激活后在两细胞晚期才很容易观察到。在母体基因组上，我们意外地在成熟和成熟的卵母细胞中发现了H3K4me3（ncH3K4me3）的非规范形式，其在启动子和大量远端基因座处均以宽峰存在。如此宽的H3K4me3峰与限制在启动子富含CpG区域的典型的尖锐的H3K4me3峰相反。值得注意的是，卵母细胞中的ncH3K4me3几乎只与部分甲基化的DNA结构域重叠。然后，在规范的H3K4me3开始建立之初，它就在植入前的胚胎中遗传，然后在晚期的两细胞胚胎中消失。 ncH3K4me3的去除需要合子转录，但与DNA复制介导的被动稀释无关。最后，通过过度表达H3K4me3脱甲基酶KDM5B，在成年卵母细胞中H3K4me3的下调与基因组沉默的缺陷有关。综上所述，这些数据揭示了早期哺乳动物发育中表观基因组的遗传和高度动态的重编程。

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  • 来源
    《Nature》 |2016年第7621期|553-557|共5页
  • 作者

    Zhang Bingjie; Zheng Hui; Huang Bo; Li Wenzhi; Xiang Yunlong; Peng Xu; Ming Jia; Wu Xiaotong; Zhang Yu; Xu Qianhua; Liu Wenqiang; Kou Xiaochen; Zhao Yanhong; He Wenteng; Li Chong; Chen Bo; Li Yuanyuan; Wang Qiujun; Ma Jing; Yin Qiangzong; Kee Kehkooi; Meng Anming; Gao Shaorong; Xu Feng; Na Jie; Xie Wei;

  • 作者单位

    Tsinghua Univ, Sch Life Sci, Ctr Stem Cell Biol & Regenerat Med, MOE Key Lab Bioinformat,THU PKU Ctr Life Sci, Beijing 100084, Peoples R China;

    Tsinghua Univ, Sch Life Sci, Ctr Stem Cell Biol & Regenerat Med, MOE Key Lab Bioinformat,THU PKU Ctr Life Sci, Beijing 100084, Peoples R China;

    Tsinghua Univ, Sch Life Sci, Ctr Stem Cell Biol & Regenerat Med, MOE Key Lab Bioinformat,THU PKU Ctr Life Sci, Beijing 100084, Peoples R China|Peking Univ, Acad Adv Interdisciplinary Studies, PKU THU Ctr Life Sci, Beijing 100871, Peoples R China;

    Tsinghua Univ, Sch Med, Ctr Stem Cell Biol & Regenerat Med, Beijing 100084, Peoples R China;

    Tsinghua Univ, Sch Life Sci, Ctr Stem Cell Biol & Regenerat Med, MOE Key Lab Bioinformat,THU PKU Ctr Life Sci, Beijing 100084, Peoples R China;

    ASTAR, Singapore Inst Clin Sci, Singapore 117609, Singapore;

    Tsinghua Univ, Sch Med, Ctr Stem Cell Biol & Regenerat Med, Beijing 100084, Peoples R China;

    Tsinghua Univ, Sch Life Sci, State Key Lab Biomembrane & Membrane Engn, Beijing 100084, Peoples R China;

    Tsinghua Univ, Sch Life Sci, Ctr Stem Cell Biol & Regenerat Med, MOE Key Lab Bioinformat,THU PKU Ctr Life Sci, Beijing 100084, Peoples R China;

    Tsinghua Univ, Sch Life Sci, Ctr Stem Cell Biol & Regenerat Med, MOE Key Lab Bioinformat,THU PKU Ctr Life Sci, Beijing 100084, Peoples R China;

    Tongji Univ, Clin & Translat Res Ctr, Sch Life Sci & Technol, Shanghai Matern & Infant Hosp 1, Shanghai 200092, Peoples R China;

    Tongji Univ, Clin & Translat Res Ctr, Sch Life Sci & Technol, Shanghai Matern & Infant Hosp 1, Shanghai 200092, Peoples R China;

    Tongji Univ, Clin & Translat Res Ctr, Sch Life Sci & Technol, Shanghai Matern & Infant Hosp 1, Shanghai 200092, Peoples R China;

    Tongji Univ, Clin & Translat Res Ctr, Sch Life Sci & Technol, Shanghai Matern & Infant Hosp 1, Shanghai 200092, Peoples R China;

    Tongji Univ, Clin & Translat Res Ctr, Sch Life Sci & Technol, Shanghai Matern & Infant Hosp 1, Shanghai 200092, Peoples R China;

    Tsinghua Univ, Sch Med, Ctr Stem Cell Biol & Regenerat Med, Beijing 100084, Peoples R China;

    Tsinghua Univ, Sch Life Sci, Ctr Stem Cell Biol & Regenerat Med, MOE Key Lab Bioinformat,THU PKU Ctr Life Sci, Beijing 100084, Peoples R China;

    Tsinghua Univ, Sch Life Sci, Ctr Stem Cell Biol & Regenerat Med, MOE Key Lab Bioinformat,THU PKU Ctr Life Sci, Beijing 100084, Peoples R China;

    Tsinghua Univ, Sch Life Sci, Ctr Stem Cell Biol & Regenerat Med, MOE Key Lab Bioinformat,THU PKU Ctr Life Sci, Beijing 100084, Peoples R China;

    Tsinghua Univ, Sch Life Sci, Ctr Stem Cell Biol & Regenerat Med, MOE Key Lab Bioinformat,THU PKU Ctr Life Sci, Beijing 100084, Peoples R China;

    Tsinghua Univ, Sch Med, Ctr Stem Cell Biol & Regenerat Med, Beijing 100084, Peoples R China;

    Tsinghua Univ, Sch Life Sci, State Key Lab Biomembrane & Membrane Engn, Beijing 100084, Peoples R China;

    Tongji Univ, Clin & Translat Res Ctr, Sch Life Sci & Technol, Shanghai Matern & Infant Hosp 1, Shanghai 200092, Peoples R China;

    ASTAR, Singapore Inst Clin Sci, Singapore 117609, Singapore|ASTAR, Inst Mol & Cell Biol, Singapore 138673, Singapore;

    Tsinghua Univ, Sch Med, Ctr Stem Cell Biol & Regenerat Med, Beijing 100084, Peoples R China;

    Tsinghua Univ, Sch Life Sci, Ctr Stem Cell Biol & Regenerat Med, MOE Key Lab Bioinformat,THU PKU Ctr Life Sci, Beijing 100084, Peoples R China;

  • 收录信息 美国《科学引文索引》(SCI);美国《工程索引》(EI);美国《生物学医学文摘》(MEDLINE);美国《化学文摘》(CA);
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