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Patterned apoptosis has an instructive role for local growth and tissue shape regulation in a fast-growing epithelium

Alexis Matamoro-Vidal, Tom Cumming, Anđela Davidović, View ORCID ProfileRomain Levayer
doi: https://doi.org/10.1101/2022.03.11.484029
Alexis Matamoro-Vidal
1Department of Developmental and Stem Cell Biology, Institut Pasteur, CNRS UMR 3738, Université Paris Cité, Cell Death and Epithelial Homeostasis Unit, F-75015 Paris, France
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Tom Cumming
1Department of Developmental and Stem Cell Biology, Institut Pasteur, CNRS UMR 3738, Université Paris Cité, Cell Death and Epithelial Homeostasis Unit, F-75015 Paris, France
2PPU program Institut Pasteur, Sorbonne Université, Collège Doctoral, F75005 Paris, France
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Anđela Davidović
3Institut Pasteur, Université Paris Cité, Bioinformatics and Biostatistics Hub, F-75015 Paris, France
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Romain Levayer
1Department of Developmental and Stem Cell Biology, Institut Pasteur, CNRS UMR 3738, Université Paris Cité, Cell Death and Epithelial Homeostasis Unit, F-75015 Paris, France
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  • ORCID record for Romain Levayer
  • For correspondence: romain.levayer@pasteur.fr
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Abstract

What regulates organ size and shape remains one of the fundamental mysteries of modern biology. So far, research in this area has primarily focused on deciphering the regulation in time and space of growth and cell division, while the contribution of cell death has been much more neglected. This includes studies of the Drosophila wing imaginal disc, the prospective fly wing which undergoes massive growth during larval stage, and represents one of the best characterised systems for the study of growth and patterning. So far, it has been assumed that cell death was relatively neglectable in this tissue and as a result the pattern of growth was usually attributed to the distribution of cell division. Here, using systematic mapping and registration combined with quantitative assessment of clone size and disappearance, we show for the first time that cell death is not neglectable, and outline a persistent pattern of cell death and clone elimination in the disc. Local variation of cell death is associated with local variation of clone size, pointing to an impact of cell death on local growth which is not fully compensated by proliferation. Using morphometric analyses of adult wing shape and genetic perturbations, we provide evidence that patterned death affects locally and globally adult wing shape and size. This study describes a roadmap for accurate assessment of the contribution of cell death to tissue shape, and outlines for the first time an important instructive role of cell death in modulating quantitatively local growth and the morphogenesis of a fast-growing tissue.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • ↵§ Lead contact

  • We have corrected some of the maps of clone size after changing one protocol of quantification/segmentation. We have also updated the map of hid expression using now local z projection instead of large scale z projection

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted April 20, 2022.
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Patterned apoptosis has an instructive role for local growth and tissue shape regulation in a fast-growing epithelium
Alexis Matamoro-Vidal, Tom Cumming, Anđela Davidović, Romain Levayer
bioRxiv 2022.03.11.484029; doi: https://doi.org/10.1101/2022.03.11.484029
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Patterned apoptosis has an instructive role for local growth and tissue shape regulation in a fast-growing epithelium
Alexis Matamoro-Vidal, Tom Cumming, Anđela Davidović, Romain Levayer
bioRxiv 2022.03.11.484029; doi: https://doi.org/10.1101/2022.03.11.484029

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