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

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-Line Bortolin-Cavaillé, Jérôme Cavaillé and Takahiro Arima ()
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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

Nature Communications, 2022, vol. 13, issue 1, 1-14

Abstract: 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.

Date: 2022
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DOI: 10.1038/s41467-022-30775-w

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