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Distinct modes of cell competition shape mammalian tissue morphogenesis

Author

Listed:
  • Stephanie J. Ellis

    (The Rockefeller University)

  • Nicholas C. Gomez

    (The Rockefeller University)

  • John Levorse

    (The Rockefeller University)

  • Aaron F. Mertz

    (The Rockefeller University)

  • Yejing Ge

    (The Rockefeller University)

  • Elaine Fuchs

    (The Rockefeller University)

Abstract

Cell competition—the sensing and elimination of less fit ‘loser’ cells by neighbouring ‘winner’ cells—was first described in Drosophila. Although cell competition has been proposed as a selection mechanism to optimize tissue and organ development, its evolutionary generality remains unclear. Here, by using live imaging, lineage tracing, single-cell transcriptomics and genetics, we identify two cell competition mechanisms that sequentially shape and maintain the architecture of stratified tissue during skin development in mice. In the single-layered epithelium of the early embryonic epidermis, winner progenitors kill and subsequently clear neighbouring loser cells by engulfment. Later, as the tissue begins to stratify, the basal layer instead expels losers through upward flux of differentiating progeny. This cell competition switch is physiologically relevant: when it is perturbed, so too is barrier formation. Our findings show that cell competition is a selective force that optimizes vertebrate tissue function, and illuminate how a tissue dynamically adjusts cell competition strategies to preserve fitness as its architectural complexity increases during morphogenesis.

Suggested Citation

  • Stephanie J. Ellis & Nicholas C. Gomez & John Levorse & Aaron F. Mertz & Yejing Ge & Elaine Fuchs, 2019. "Distinct modes of cell competition shape mammalian tissue morphogenesis," Nature, Nature, vol. 569(7757), pages 497-502, May.
  • Handle: RePEc:nat:nature:v:569:y:2019:i:7757:d:10.1038_s41586-019-1199-y
    DOI: 10.1038/s41586-019-1199-y
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    Cited by:

    1. Hisato Nagano & Naoaki Mizuno & Hideyuki Sato & Eiji Mizutani & Ayaka Yanagida & Mayuko Kano & Mariko Kasai & Hiromi Yamamoto & Motoo Watanabe & Fabian Suchy & Hideki Masaki & Hiromitsu Nakauchi, 2024. "Skin graft with dermis and appendages generated in vivo by cell competition," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    2. Shilpa P. Pothapragada & Praver Gupta & Soumi Mukherjee & Tamal Das, 2022. "Matrix mechanics regulates epithelial defence against cancer by tuning dynamic localization of filamin," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    3. Marianna Yusupova & Roi Ankawa & Yahav Yosefzon & David Meiri & Ido Bachelet & Yaron Fuchs, 2023. "Apoptotic dysregulation mediates stem cell competition and tissue regeneration," Nature Communications, Nature, vol. 14(1), pages 1-20, December.

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