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The microRNA cluster C19MC confers differentiation potential into trophoblast lineages upon human pluripotent stem cells

Author

Listed:
  • Norio Kobayashi

    (Tohoku University Graduate School of Medicine)

  • Hiroaki Okae

    (Tohoku University Graduate School of Medicine)

  • Hitoshi Hiura

    (Tokyo University of Agriculture)

  • Naoto Kubota

    (Kyushu University)

  • Eri H. Kobayashi

    (Tohoku University Graduate School of Medicine)

  • Shun Shibata

    (Tohoku University Graduate School of Medicine)

  • Akira Oike

    (Tohoku University Graduate School of Medicine)

  • Takeshi Hori

    (Tokyo Medical and Dental University)

  • Chie Kikutake

    (Kyushu University)

  • Hirotaka Hamada

    (Tohoku University Graduate School of Medicine)

  • Hirokazu Kaji

    (Tokyo Medical and Dental University)

  • Mikita Suyama

    (Kyushu University)

  • Marie-Line Bortolin-Cavaillé

    (University of Toulouse, CNRS, UPS)

  • Jérôme Cavaillé

    (University of Toulouse, CNRS, UPS)

  • Takahiro Arima

    (Tohoku University Graduate School of Medicine)

Abstract

The first cell fate commitment during mammalian development is the specification of the inner cell mass and trophectoderm. This irreversible cell fate commitment should be epigenetically regulated, but the precise mechanism is largely unknown in humans. Here, we show that naïve human embryonic stem (hES) cells can transdifferentiate into trophoblast stem (hTS) cells, but primed hES cells cannot. Our transcriptome and methylome analyses reveal that a primate-specific miRNA cluster on chromosome 19 (C19MC) is active in naïve hES cells but epigenetically silenced in primed ones. Moreover, genome and epigenome editing using CRISPR/Cas systems demonstrate that C19MC is essential for hTS cell maintenance and C19MC-reactivated primed hES cells can give rise to hTS cells. Thus, we reveal that C19MC activation confers differentiation potential into trophoblast lineages on hES cells. Our findings are fundamental to understanding the epigenetic regulation of human early development and pluripotency.

Suggested Citation

  • Norio Kobayashi & Hiroaki Okae & Hitoshi Hiura & Naoto Kubota & Eri H. Kobayashi & Shun Shibata & Akira Oike & Takeshi Hori & Chie Kikutake & Hirotaka Hamada & Hirokazu Kaji & Mikita Suyama & Marie-Li, 2022. "The microRNA cluster C19MC confers differentiation potential into trophoblast lineages upon human pluripotent stem cells," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-30775-w
    DOI: 10.1038/s41467-022-30775-w
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    References listed on IDEAS

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    1. Fan Zhou & Rui Wang & Peng Yuan & Yixin Ren & Yunuo Mao & Rong Li & Ying Lian & Junsheng Li & Lu Wen & Liying Yan & Jie Qiao & Fuchou Tang, 2019. "Reconstituting the transcriptome and DNA methylome landscapes of human implantation," Nature, Nature, vol. 572(7771), pages 660-664, August.
    2. Yi Zheng & Xufeng Xue & Yue Shao & Sicong Wang & Sajedeh Nasr Esfahani & Zida Li & Jonathon M. Muncie & Johnathon N. Lakins & Valerie M. Weaver & Deborah L. Gumucio & Jianping Fu, 2019. "Controlled modelling of human epiblast and amnion development using stem cells," Nature, Nature, vol. 573(7774), pages 421-425, September.
    3. Tomonori Nakamura & Ikuhiro Okamoto & Kotaro Sasaki & Yukihiro Yabuta & Chizuru Iwatani & Hideaki Tsuchiya & Yasunari Seita & Shinichiro Nakamura & Takuya Yamamoto & Mitinori Saitou, 2016. "A developmental coordinate of pluripotency among mice, monkeys and humans," Nature, Nature, vol. 537(7618), pages 57-62, September.
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    Cited by:

    1. Moriyah Naama & Moran Rahamim & Valery Zayat & Shulamit Sebban & Ahmed Radwan & Dana Orzech & Rachel Lasry & Annael Ifrah & Mohammad Jaber & Ofra Sabag & Hazar Yassen & Areej Khatib & Silvina Epsztejn, 2023. "Pluripotency-independent induction of human trophoblast stem cells from fibroblasts," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    2. Stewart J. Russell & Cheng Zhao & Savana Biondic & Karen Menezes & Michael Hagemann-Jensen & Clifford L. Librach & Sophie Petropoulos, 2024. "An atlas of small non-coding RNAs in human preimplantation development," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    3. Yueli Yang & Wenqi Jia & Zhiwei Luo & Yunpan Li & Hao Liu & Lixin Fu & Jinxiu Li & Yu Jiang & Junjian Lai & Haiwei Li & Babangida Jabir Saeed & Yi Zou & Yuan Lv & Liang Wu & Ting Zhou & Yongli Shan & , 2024. "VGLL1 cooperates with TEAD4 to control human trophectoderm lineage specification," Nature Communications, Nature, vol. 15(1), pages 1-18, December.

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