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A developmental coordinate of pluripotency among mice, monkeys and humans

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  • Tomonori Nakamura

    (Graduate School of Medicine, Kyoto University, Yoshida-Konoe-cho
    JST, ERATO, Yoshida-Konoe-cho)

  • Ikuhiro Okamoto

    (Graduate School of Medicine, Kyoto University, Yoshida-Konoe-cho
    JST, ERATO, Yoshida-Konoe-cho)

  • Kotaro Sasaki

    (Graduate School of Medicine, Kyoto University, Yoshida-Konoe-cho
    JST, ERATO, Yoshida-Konoe-cho)

  • Yukihiro Yabuta

    (Graduate School of Medicine, Kyoto University, Yoshida-Konoe-cho
    JST, ERATO, Yoshida-Konoe-cho)

  • Chizuru Iwatani

    (Research Center for Animal Life Science, Shiga University of Medical Science, Seta-Tsukinowa-cho)

  • Hideaki Tsuchiya

    (Research Center for Animal Life Science, Shiga University of Medical Science, Seta-Tsukinowa-cho)

  • Yasunari Seita

    (Research Center for Animal Life Science, Shiga University of Medical Science, Seta-Tsukinowa-cho)

  • Shinichiro Nakamura

    (Research Center for Animal Life Science, Shiga University of Medical Science, Seta-Tsukinowa-cho)

  • Takuya Yamamoto

    (Center for iPS Cell Research and Application, Kyoto University, 53 Kawahara-cho, Shogoin
    Institute for Integrated Cell-Material Sciences, Kyoto University, Yoshida-Ushinomiya-cho
    AMED-CREST, AMED, 1-7-1 Otemachi)

  • Mitinori Saitou

    (Graduate School of Medicine, Kyoto University, Yoshida-Konoe-cho
    JST, ERATO, Yoshida-Konoe-cho
    Center for iPS Cell Research and Application, Kyoto University, 53 Kawahara-cho, Shogoin
    Institute for Integrated Cell-Material Sciences, Kyoto University, Yoshida-Ushinomiya-cho)

Abstract

The epiblast (EPI) is the origin of all somatic and germ cells in mammals, and of pluripotent stem cells in vitro. To explore the ontogeny of human and primate pluripotency, here we perform comprehensive single-cell RNA sequencing for pre- and post-implantation EPI development in cynomolgus monkeys (Macaca fascicularis). We show that after specification in the blastocysts, EPI from cynomolgus monkeys (cyEPI) undergoes major transcriptome changes on implantation. Thereafter, while generating gastrulating cells, cyEPI stably maintains its transcriptome over a week, retains a unique set of pluripotency genes and acquires properties for ‘neuron differentiation’. Human and monkey pluripotent stem cells show the highest similarity to post-implantation late cyEPI, which, despite co-existing with gastrulating cells, bears characteristics of pre-gastrulating mouse EPI and epiblast-like cells in vitro. These findings not only reveal the divergence and coherence of EPI development, but also identify a developmental coordinate of the spectrum of pluripotency among key species, providing a basis for better regulation of human pluripotency in vitro.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:nature:v:537:y:2016:i:7618:d:10.1038_nature19096
    DOI: 10.1038/nature19096
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    Cited by:

    1. Sajedeh Nasr Esfahani & Yi Zheng & Auriana Arabpour & Agnes M. Resto Irizarry & Norio Kobayashi & Xufeng Xue & Yue Shao & Cheng Zhao & Nicole L. Agranonik & Megan Sparrow & Timothy J. Hunt & Jared Fai, 2024. "Derivation of human primordial germ cell-like cells in an embryonic-like culture," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    2. 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.
    3. Anna Malkowska & Christopher Penfold & Sophie Bergmann & Thorsten E. Boroviak, 2022. "A hexa-species transcriptome atlas of mammalian embryogenesis delineates metabolic regulation across three different implantation modes," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    4. Luke Simpson & Andrew Strange & Doris Klisch & Sophie Kraunsoe & Takuya Azami & Daniel Goszczynski & Triet Minh & Benjamin Planells & Nadine Holmes & Fei Sang & Sonal Henson & Matthew Loose & Jennifer, 2024. "A single-cell atlas of pig gastrulation as a resource for comparative embryology," Nature Communications, Nature, vol. 15(1), pages 1-16, December.

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