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Cell-cycle-independent transitions in temporal identity of mammalian neural progenitor cells

Author

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  • Mayumi Okamoto

    (Nagoya University Graduate School of Medicine
    Present address: Department of Anatomy and Neurobiology, Boston University School of Medicine, 72 East Concord St, Boston, Massachusetts 02115, USA)

  • Takaki Miyata

    (Nagoya University Graduate School of Medicine)

  • Daijiro Konno

    (Laboratory for Cell Asymmetry, Center for Developmental Biology, RIKEN Kobe Institute)

  • Hiroki R. Ueda

    (Laboratory for Systems Biology, Center for Developmental Biology, RIKEN Kobe Institute
    Functional Genomics Unit, Center for Developmental Biology, RIKEN Kobe Institute
    Present address: Laboratory for Synthetic Biology, RIKEN Quantitative Biology Center, 2-2-3 Minatojima-minamimachi, Chuo-ku, Kobe, Hyogo 650-0047, Japan)

  • Takeya Kasukawa

    (Functional Genomics Unit, Center for Developmental Biology, RIKEN Kobe Institute
    Large Scale Data Managing Unit, Center for Life Science Technologies, RIKEN Yokohama Institute)

  • Mitsuhiro Hashimoto

    (Nagoya University Graduate School of Medicine
    Fukushima Medical University)

  • Fumio Matsuzaki

    (Laboratory for Cell Asymmetry, Center for Developmental Biology, RIKEN Kobe Institute)

  • Ayano Kawaguchi

    (Nagoya University Graduate School of Medicine)

Abstract

During cerebral development, many types of neurons are sequentially generated by self-renewing progenitor cells called apical progenitors (APs). Temporal changes in AP identity are thought to be responsible for neuronal diversity; however, the mechanisms underlying such changes remain largely unknown. Here we perform single-cell transcriptome analysis of individual progenitors at different developmental stages, and identify a subset of genes whose expression changes over time but is independent of differentiation status. Surprisingly, the pattern of changes in the expression of such temporal-axis genes in APs is unaffected by cell-cycle arrest. Consistent with this, transient cell-cycle arrest of APs in vivo does not prevent descendant neurons from acquiring their correct laminar fates. Analysis of cultured APs reveals that transitions in AP gene expression are driven by both cell-intrinsic and -extrinsic mechanisms. These results suggest that the timing mechanisms controlling AP temporal identity function independently of cell-cycle progression and Notch activation mode.

Suggested Citation

  • Mayumi Okamoto & Takaki Miyata & Daijiro Konno & Hiroki R. Ueda & Takeya Kasukawa & Mitsuhiro Hashimoto & Fumio Matsuzaki & Ayano Kawaguchi, 2016. "Cell-cycle-independent transitions in temporal identity of mammalian neural progenitor cells," Nature Communications, Nature, vol. 7(1), pages 1-16, September.
  • Handle: RePEc:nat:natcom:v:7:y:2016:i:1:d:10.1038_ncomms11349
    DOI: 10.1038/ncomms11349
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    Cited by:

    1. Hailun Zhu & Sihai Dave Zhao & Alokananda Ray & Yu Zhang & Xin Li, 2022. "A comprehensive temporal patterning gene network in Drosophila medulla neuroblasts revealed by single-cell RNA sequencing," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    2. Hans-Juergen Schulten & Deema Hussein, 2019. "Array expression meta-analysis of cancer stem cell genes identifies upregulation of PODXL especially in DCC low expression meningiomas," PLOS ONE, Public Library of Science, vol. 14(5), pages 1-20, May.

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