Local and global changes in cell density induce reorganisation of 3D packing in a proliferating epithelium

Author:

Barone Vanessa12ORCID,Tagua Antonio34,Román Jesus Á. Andrés-San34,Hamdoun Amro1ORCID,Garrido-García Juan34,Lyons Deirdre C.1,Escudero Luis M.345ORCID

Affiliation:

1. Center for Marine Biotechnology and Biomedicine, University of California San Diego 1 , La Jolla, CA 92093 , USA

2. Stanford University 2 Hopkins Marine Station, Department of Biology , , Pacific Grove, CA 93950 , USA

3. Instituto de Biomedicina de Sevilla (IBiS), Hospital Universitario Virgen del Rocío/CSIC/Universidad de Sevilla 3 and Departamento de Biología Celular, Facultad de Biología , , 41013 Seville , Spain

4. Universidad de Sevilla 3 and Departamento de Biología Celular, Facultad de Biología , , 41013 Seville , Spain

5. Biomedical Network Research Centre on Neurodegenerative Diseases (CIBERNED) 4 , 28029 Madrid , Spain

Abstract

ABSTRACT Tissue morphogenesis is intimately linked to the changes in shape and organisation of individual cells. In curved epithelia, cells can intercalate along their own apicobasal axes, adopting a shape named ‘scutoid’ that allows energy minimization in the tissue. Although several geometric and biophysical factors have been associated with this 3D reorganisation, the dynamic changes underlying scutoid formation in 3D epithelial packing remain poorly understood. Here, we use live imaging of the sea star embryo coupled with deep learning-based segmentation to dissect the relative contributions of cell density, tissue compaction and cell proliferation on epithelial architecture. We find that tissue compaction, which naturally occurs in the embryo, is necessary for the appearance of scutoids. Physical compression experiments identify cell density as the factor promoting scutoid formation at a global level. Finally, the comparison of the developing embryo with computational models indicates that the increase in the proportion of scutoids is directly associated with cell divisions. Our results suggest that apico-basal intercalations appearing immediately after mitosis may help accommodate the new cells within the tissue. We propose that proliferation in a compact epithelium induces 3D cell rearrangements during development.

Funder

Human Frontier Science Program

National Institutes of Health

Ministerio de Ciencia e Innovacion

Junta de Andalucia

Universidad de Sevilla

Publisher

The Company of Biologists

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