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Cell cycle arrest determines adult neural stem cell ontogeny by an embryonic Notch-nonoscillatory Hey1 module

Author

Listed:
  • Yujin Harada

    (The University of Tokyo)

  • Mayumi Yamada

    (Institute for Frontier Life and Medical Sciences, Kyoto University
    Kyoto University)

  • Itaru Imayoshi

    (Institute for Frontier Life and Medical Sciences, Kyoto University
    Kyoto University)

  • Ryoichiro Kageyama

    (Institute for Frontier Life and Medical Sciences, Kyoto University
    2-1 Hirosawa)

  • Yutaka Suzuki

    (The University of Tokyo)

  • Takaaki Kuniya

    (The University of Tokyo)

  • Shohei Furutachi

    (The University of Tokyo
    University College London)

  • Daichi Kawaguchi

    (The University of Tokyo)

  • Yukiko Gotoh

    (The University of Tokyo
    The University of Tokyo)

Abstract

Quiescent neural stem cells (NSCs) in the adult mouse brain are the source of neurogenesis that regulates innate and adaptive behaviors. Adult NSCs in the subventricular zone are derived from a subpopulation of embryonic neural stem-progenitor cells (NPCs) that is characterized by a slower cell cycle relative to the more abundant rapid cycling NPCs that build the brain. Yet, how slow cell cycle can cause the establishment of adult NSCs remains largely unknown. Here, we demonstrate that Notch and an effector Hey1 form a module that is upregulated by cell cycle arrest in slowly dividing NPCs. In contrast to the oscillatory expression of the Notch effectors Hes1 and Hes5 in fast cycling progenitors, Hey1 displays a non-oscillatory stationary expression pattern and contributes to the long-term maintenance of NSCs. These findings reveal a novel division of labor in Notch effectors where cell cycle rate biases effector selection and cell fate.

Suggested Citation

  • Yujin Harada & Mayumi Yamada & Itaru Imayoshi & Ryoichiro Kageyama & Yutaka Suzuki & Takaaki Kuniya & Shohei Furutachi & Daichi Kawaguchi & Yukiko Gotoh, 2021. "Cell cycle arrest determines adult neural stem cell ontogeny by an embryonic Notch-nonoscillatory Hey1 module," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-26605-0
    DOI: 10.1038/s41467-021-26605-0
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    References listed on IDEAS

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    1. Cerys S. Manning & Veronica Biga & James Boyd & Jochen Kursawe & Bodvar Ymisson & David G. Spiller & Christopher M. Sanderson & Tobias Galla & Magnus Rattray & Nancy Papalopulu, 2019. "Quantitative single-cell live imaging links HES5 dynamics with cell-state and fate in murine neurogenesis," Nature Communications, Nature, vol. 10(1), pages 1-19, December.
    2. Marc Goodfellow & Nicholas E. Phillips & Cerys Manning & Tobias Galla & Nancy Papalopulu, 2014. "microRNA input into a neural ultradian oscillator controls emergence and timing of alternative cell states," Nature Communications, Nature, vol. 5(1), pages 1-10, May.
    3. Naoya Hirata & Shigeru Yamada & Takuji Shoda & Masaaki Kurihara & Yuko Sekino & Yasunari Kanda, 2014. "Sphingosine-1-phosphate promotes expansion of cancer stem cells via S1PR3 by a ligand-independent Notch activation," Nature Communications, Nature, vol. 5(1), pages 1-14, December.
    4. Daichi Kawaguchi & Shohei Furutachi & Hiroki Kawai & Katsuto Hozumi & Yukiko Gotoh, 2013. "Dll1 maintains quiescence of adult neural stem cells and segregates asymmetrically during mitosis," Nature Communications, Nature, vol. 4(1), pages 1-12, October.
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    Cited by:

    1. Naohiro Kuwayama & Tomoya Kujirai & Yusuke Kishi & Rina Hirano & Kenta Echigoya & Lingyan Fang & Sugiko Watanabe & Mitsuyoshi Nakao & Yutaka Suzuki & Kei-ichiro Ishiguro & Hitoshi Kurumizaka & Yukiko , 2023. "HMGA2 directly mediates chromatin condensation in association with neuronal fate regulation," Nature Communications, Nature, vol. 14(1), pages 1-18, December.

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