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

Drosophila apoptosis clone dynamics geometric morphometrics growth morphogenesis quantitative mapping wing imaginal disc

Journal

Current biology : CB
ISSN: 1879-0445
Titre abrégé: Curr Biol
Pays: England
ID NLM: 9107782

Informations de publication

Date de publication:
09 Jan 2024
Historique:
received: 21 04 2022
revised: 13 07 2023
accepted: 11 12 2023
medline: 13 1 2024
pubmed: 13 1 2024
entrez: 12 1 2024
Statut: aheadofprint

Résumé

What regulates organ size and shape remains one fundamental mystery of modern biology. 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 overall neglected. This includes studies of the Drosophila wing, one of the best-characterized systems for the study of growth and patterning, undergoing massive growth during larval stage and important morphogenetic remodeling during pupal stage. So far, it has been assumed that cell death was relatively neglectable in this tissue both during larval stage and pupal stage, 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 as well as live imaging, we outline a persistent pattern of cell death and clone elimination emerging in the larval wing disc and persisting during pupal wing morphogenesis. Local variation of cell death is associated with local variation of clone size, pointing to an impact of cell death on local growth that is not fully compensated by proliferation. Using morphometric analyses of adult wing shape and genetic perturbations, we provide evidence that patterned death locally and globally affects adult wing shape and size. This study describes a roadmap for precise assessment of the contribution of cell death to tissue shape and outlines an important instructive role of cell death in modulating quantitatively local growth and morphogenesis of a fast-growing tissue.

Identifiants

pubmed: 38215743
pii: S0960-9822(23)01687-1
doi: 10.1016/j.cub.2023.12.031
pii:
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

Copyright © 2023 The Author(s). Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests The authors declare no competing interests.

Auteurs

Alexis Matamoro-Vidal (A)

Department of Developmental and Stem Cell Biology, Institut Pasteur, CNRS UMR 3738, Université Paris Cité, Cell Death and Epithelial Homeostasis Unit, 75015 Paris, France.

Tom Cumming (T)

Department of Developmental and Stem Cell Biology, Institut Pasteur, CNRS UMR 3738, Université Paris Cité, Cell Death and Epithelial Homeostasis Unit, 75015 Paris, France; PPU program Institut Pasteur, Sorbonne Université, Collège Doctoral, 75005 Paris, France.

Anđela Davidović (A)

Institut Pasteur, Université Paris Cité, Bioinformatics and Biostatistics Hub, 75015 Paris, France.

Florence Levillayer (F)

Department of Developmental and Stem Cell Biology, Institut Pasteur, CNRS UMR 3738, Université Paris Cité, Cell Death and Epithelial Homeostasis Unit, 75015 Paris, France.

Romain Levayer (R)

Department of Developmental and Stem Cell Biology, Institut Pasteur, CNRS UMR 3738, Université Paris Cité, Cell Death and Epithelial Homeostasis Unit, 75015 Paris, France. Electronic address: romain.levayer@pasteur.fr.

Classifications MeSH