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Cell competition corrects noisy Wnt morphogen gradients to achieve robust patterning in the zebrafish embryo

Author

Listed:
  • Yuki Akieda

    (Gunma University
    Osaka University)

  • Shohei Ogamino

    (Gunma University)

  • Hironobu Furuie

    (Kyushu University
    Kyushu University)

  • Shizuka Ishitani

    (Gunma University)

  • Ryutaro Akiyoshi

    (Research and Development, Olympus Corp.)

  • Jumpei Nogami

    (Kyushu University)

  • Takamasa Masuda

    (Kyushu University)

  • Nobuyuki Shimizu

    (Kyushu University)

  • Yasuyuki Ohkawa

    (Kyushu University)

  • Tohru Ishitani

    (Gunma University
    Osaka University
    Kyushu University)

Abstract

Morphogen signalling forms an activity gradient and instructs cell identities in a signalling strength-dependent manner to pattern developing tissues. However, developing tissues also undergo dynamic morphogenesis, which may produce cells with unfit morphogen signalling and consequent noisy morphogen gradients. Here we show that a cell competition-related system corrects such noisy morphogen gradients. Zebrafish imaging analyses of the Wnt/β-catenin signalling gradient, which acts as a morphogen to establish embryonic anterior-posterior patterning, identify that unfit cells with abnormal Wnt/β-catenin activity spontaneously appear and produce noise in the gradient. Communication between unfit and neighbouring fit cells via cadherin proteins stimulates apoptosis of the unfit cells by activating Smad signalling and reactive oxygen species production. This unfit cell elimination is required for proper Wnt/β-catenin gradient formation and consequent anterior-posterior patterning. Because this gradient controls patterning not only in the embryo but also in adult tissues, this system may support tissue robustness and disease prevention.

Suggested Citation

  • Yuki Akieda & Shohei Ogamino & Hironobu Furuie & Shizuka Ishitani & Ryutaro Akiyoshi & Jumpei Nogami & Takamasa Masuda & Nobuyuki Shimizu & Yasuyuki Ohkawa & Tohru Ishitani, 2019. "Cell competition corrects noisy Wnt morphogen gradients to achieve robust patterning in the zebrafish embryo," Nature Communications, Nature, vol. 10(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:10:y:2019:i:1:d:10.1038_s41467-019-12609-4
    DOI: 10.1038/s41467-019-12609-4
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    Cited by:

    1. Kazuki Nakai & Hancheng Lin & Shotaro Yamano & Shinya Tanaka & Sho Kitamoto & Hitoshi Saitoh & Kenta Sakuma & Junpei Kurauchi & Eilma Akter & Masamitsu Konno & Kojiro Ishibashi & Ryo Kamata & Akihiro , 2023. "Wnt activation disturbs cell competition and causes diffuse invasion of transformed cells through NF-κB-MMP21 pathway," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    2. Yukinari Haraoka & Yuki Akieda & Yuri Nagai & Chihiro Mogi & Tohru Ishitani, 2022. "Zebrafish imaging reveals TP53 mutation switching oncogene-induced senescence from suppressor to driver in primary tumorigenesis," Nature Communications, Nature, vol. 13(1), pages 1-15, December.

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