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

Yuki Akieda, Shohei Ogamino, Hironobu Furuie, Shizuka Ishitani, Ryutaro Akiyoshi, Jumpei Nogami, Takamasa Masuda, Nobuyuki Shimizu, Yasuyuki Ohkawa, Tohru Ishitani

Research output: Contribution to journalArticle

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.

Original languageEnglish
Article number4710
JournalNature communications
Volume10
Issue number1
DOIs
Publication statusPublished - Dec 1 2019

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embryos
Zebrafish
Embryonic Structures
Catenins
gradients
Tissue
cells
Cadherins
Reactive Oxygen Species
apoptosis
Morphogenesis
Apoptosis
Imaging techniques
Noise
elimination
Communication
communication
proteins
Proteins
oxygen

All Science Journal Classification (ASJC) codes

  • Chemistry(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Physics and Astronomy(all)

Cite this

Akieda, Y., Ogamino, S., Furuie, H., Ishitani, S., Akiyoshi, R., Nogami, J., ... Ishitani, T. (2019). Cell competition corrects noisy Wnt morphogen gradients to achieve robust patterning in the zebrafish embryo. Nature communications, 10(1), [4710]. https://doi.org/10.1038/s41467-019-12609-4

Cell competition corrects noisy Wnt morphogen gradients to achieve robust patterning in the zebrafish embryo. / Akieda, Yuki; Ogamino, Shohei; Furuie, Hironobu; Ishitani, Shizuka; Akiyoshi, Ryutaro; Nogami, Jumpei; Masuda, Takamasa; Shimizu, Nobuyuki; Ohkawa, Yasuyuki; Ishitani, Tohru.

In: Nature communications, Vol. 10, No. 1, 4710, 01.12.2019.

Research output: Contribution to journalArticle

Akieda, Y, Ogamino, S, Furuie, H, Ishitani, S, Akiyoshi, R, Nogami, J, Masuda, T, Shimizu, N, Ohkawa, Y & Ishitani, T 2019, 'Cell competition corrects noisy Wnt morphogen gradients to achieve robust patterning in the zebrafish embryo', Nature communications, vol. 10, no. 1, 4710. https://doi.org/10.1038/s41467-019-12609-4
Akieda, Yuki ; Ogamino, Shohei ; Furuie, Hironobu ; Ishitani, Shizuka ; Akiyoshi, Ryutaro ; Nogami, Jumpei ; Masuda, Takamasa ; Shimizu, Nobuyuki ; Ohkawa, Yasuyuki ; Ishitani, Tohru. / Cell competition corrects noisy Wnt morphogen gradients to achieve robust patterning in the zebrafish embryo. In: Nature communications. 2019 ; Vol. 10, No. 1.
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