A quantitative biophysical principle to explain the 3D cellular connectivity in curved epithelia.

bioimage analysis computational geometry developmental systems biology mathematical/biophysical modeling tissue/cellular biophysics

Journal

Cell systems
ISSN: 2405-4720
Titre abrégé: Cell Syst
Pays: United States
ID NLM: 101656080

Informations de publication

Date de publication:
17 08 2022
Historique:
received: 13 04 2021
revised: 15 02 2022
accepted: 15 06 2022
pubmed: 15 7 2022
medline: 23 8 2022
entrez: 14 7 2022
Statut: ppublish

Résumé

Epithelial cell organization and the mechanical stability of tissues are closely related. In this context, it has been recently shown that packing optimization in bended or folded epithelia is achieved by an energy minimization mechanism that leads to a complex cellular shape: the "scutoid". Here, we focus on the relationship between this shape and the connectivity between cells. We use a combination of computational, experimental, and biophysical approaches to examine how energy drivers affect the three-dimensional (3D) packing of tubular epithelia. We propose an energy-based stochastic model that explains the 3D cellular connectivity. Then, we challenge it by experimentally reducing the cell adhesion. As a result, we observed an increment in the appearance of scutoids that correlated with a decrease in the energy barrier necessary to connect with new cells. We conclude that tubular epithelia satisfy a quantitative biophysical principle that links tissue geometry and energetics with the average cellular connectivity.

Identifiants

pubmed: 35835108
pii: S2405-4712(22)00273-3
doi: 10.1016/j.cels.2022.06.003
pii:
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

631-643.e8

Informations de copyright

Copyright © 2022. Published by Elsevier Inc.

Déclaration de conflit d'intérêts

Declaration of interests The authors declare no competing interests.

Auteurs

Pedro Gómez-Gálvez (P)

Instituto de Biomedicina de Sevilla (IBiS), Hospital Universitario Virgen del Rocío/CSIC/Universidad de Sevilla and Departamento de Biología Celular, Universidad de Sevilla, 41013 Seville, Spain; Biomedical Network Research Centre on Neurodegenerative Diseases (CIBERNED), Madrid, Spain. Electronic address: pgg@mrc-lmb.cam.ac.uk.

Pablo Vicente-Munuera (P)

Instituto de Biomedicina de Sevilla (IBiS), Hospital Universitario Virgen del Rocío/CSIC/Universidad de Sevilla and Departamento de Biología Celular, Universidad de Sevilla, 41013 Seville, Spain; Biomedical Network Research Centre on Neurodegenerative Diseases (CIBERNED), Madrid, Spain.

Samira Anbari (S)

Chemical and Biomolecular Engineering Department, Lehigh University, Bethlehem, PA 18018, USA.

Antonio Tagua (A)

Instituto de Biomedicina de Sevilla (IBiS), Hospital Universitario Virgen del Rocío/CSIC/Universidad de Sevilla and Departamento de Biología Celular, Universidad de Sevilla, 41013 Seville, Spain; Biomedical Network Research Centre on Neurodegenerative Diseases (CIBERNED), Madrid, Spain.

Carmen Gordillo-Vázquez (C)

Instituto de Biomedicina de Sevilla (IBiS), Hospital Universitario Virgen del Rocío/CSIC/Universidad de Sevilla and Departamento de Biología Celular, Universidad de Sevilla, 41013 Seville, Spain; Biomedical Network Research Centre on Neurodegenerative Diseases (CIBERNED), Madrid, Spain.

Jesús A Andrés-San Román (JA)

Instituto de Biomedicina de Sevilla (IBiS), Hospital Universitario Virgen del Rocío/CSIC/Universidad de Sevilla and Departamento de Biología Celular, Universidad de Sevilla, 41013 Seville, Spain; Biomedical Network Research Centre on Neurodegenerative Diseases (CIBERNED), Madrid, Spain.

Daniel Franco-Barranco (D)

Department of Computer Science and Artificial Intelligence, University of the Basque Country (UPV/EHU), San Sebastian, Spain; Donostia International Physics Center (DIPC), San Sebastian, Spain.

Ana M Palacios (AM)

Instituto de Biomedicina de Sevilla (IBiS), Hospital Universitario Virgen del Rocío/CSIC/Universidad de Sevilla and Departamento de Biología Celular, Universidad de Sevilla, 41013 Seville, Spain; Biomedical Network Research Centre on Neurodegenerative Diseases (CIBERNED), Madrid, Spain.

Antonio Velasco (A)

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

Carlos Capitán-Agudo (C)

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

Clara Grima (C)

Departamento de Matemática Aplicada I, Universidad de Sevilla, Seville 41012, Spain.

Valentina Annese (V)

Instituto de Biomedicina de Sevilla (IBiS), Hospital Universitario Virgen del Rocío/CSIC/Universidad de Sevilla and Departamento de Biología Celular, Universidad de Sevilla, 41013 Seville, Spain; Biomedical Network Research Centre on Neurodegenerative Diseases (CIBERNED), Madrid, Spain.

Ignacio Arganda-Carreras (I)

Department of Computer Science and Artificial Intelligence, University of the Basque Country (UPV/EHU), San Sebastian, Spain; Donostia International Physics Center (DIPC), San Sebastian, Spain; Ikerbasque, Basque Foundation for Science, Bilbao, Spain.

Rafael Robles (R)

Departamento de Matemática Aplicada I, Universidad de Sevilla, Seville 41012, Spain.

Alberto Márquez (A)

Departamento de Matemática Aplicada I, Universidad de Sevilla, Seville 41012, Spain.

Javier Buceta (J)

Institute for Integrative Systems Biology (I2SysBio), CSIC-UV, Paterna 46980, Spain. Electronic address: javier.buceta@csic.es.

Luis M Escudero (LM)

Instituto de Biomedicina de Sevilla (IBiS), Hospital Universitario Virgen del Rocío/CSIC/Universidad de Sevilla and Departamento de Biología Celular, Universidad de Sevilla, 41013 Seville, Spain; Biomedical Network Research Centre on Neurodegenerative Diseases (CIBERNED), Madrid, Spain. Electronic address: lmescudero-ibis@us.es.

Articles similaires

High-throughput Bronchus-on-a-Chip system for modeling the human bronchus.

Akina Mori, Marjolein Vermeer, Lenie J van den Broek et al.
1.00
Humans Bronchi Lab-On-A-Chip Devices Epithelial Cells Goblet Cells
Respiratory Syncytial Virus Infections Humans Animals Mice STAT3 Transcription Factor
Humans Deep Learning Mouth Neoplasms Drug Resistance, Neoplasm Cell Line, Tumor
1.00
Algorithms Computer Simulation Models, Biological Programming Languages Humans

Classifications MeSH