Epithelial colonies in vitro elongate through collective effects

Autor: S.S. Soumya, Frank Jülicher, Guillaume Salbreux, S Anvitha, Daniel Riveline, Jordi Comelles, Linjie Lu, Mandar M. Inamdar, Emilie Le Maout
Přispěvatelé: Riveline, Daniel, Institut de Génétique et de Biologie Moléculaire et Cellulaire (IGBMC), Université de Strasbourg (UNISTRA)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Institut de Science et d'ingénierie supramoléculaires (ISIS), Université de Strasbourg (UNISTRA)-Institut de Chimie du CNRS (INC)-Centre National de la Recherche Scientifique (CNRS)-Matériaux et Nanosciences Grand-Est (MNGE), Université de Strasbourg (UNISTRA)-Université de Haute-Alsace (UHA) Mulhouse - Colmar (Université de Haute-Alsace (UHA))-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut de Chimie du CNRS (INC)-Centre National de la Recherche Scientifique (CNRS)-Université de Strasbourg (UNISTRA)-Université de Haute-Alsace (UHA) Mulhouse - Colmar (Université de Haute-Alsace (UHA))-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Réseau nanophotonique et optique, Université de Strasbourg (UNISTRA)-Université de Haute-Alsace (UHA) Mulhouse - Colmar (Université de Haute-Alsace (UHA))-Centre National de la Recherche Scientifique (CNRS)-Université de Strasbourg (UNISTRA)-Centre National de la Recherche Scientifique (CNRS), Indian Institute of Technology Bombay (IIT Bombay), The Francis Crick Institute [London], Max Planck Institute for the Physics of Complex Systems (MPI-PKS), Max-Planck-Gesellschaft, Réseau nanophotonique et optique, Centre National de la Recherche Scientifique (CNRS)-Université de Strasbourg (UNISTRA)-Université de Haute-Alsace (UHA) Mulhouse - Colmar (Université de Haute-Alsace (UHA))-Centre National de la Recherche Scientifique (CNRS)-Université de Strasbourg (UNISTRA)-Université de Haute-Alsace (UHA) Mulhouse - Colmar (Université de Haute-Alsace (UHA))-Centre National de la Recherche Scientifique (CNRS)-Institut de Chimie du CNRS (INC)-Matériaux et nanosciences d'Alsace (FMNGE), Institut de Chimie du CNRS (INC)-Université de Strasbourg (UNISTRA)-Université de Haute-Alsace (UHA) Mulhouse - Colmar (Université de Haute-Alsace (UHA))-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Université de Strasbourg (UNISTRA)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Université de Strasbourg (UNISTRA)
Jazyk: angličtina
Rok vydání: 2021
Předmět:
0301 basic medicine
Cell division
[SDV]Life Sciences [q-bio]
Cell
01 natural sciences
symmetry breaking
Epithelium
Madin Darby Canine Kidney Cells
[PHYS] Physics [physics]
Cell elongation
physics of living systems
Morphogenesis
Biology (General)
Physics
[PHYS]Physics [physics]
0303 health sciences
Chemistry
General Neuroscience
030302 biochemistry & molecular biology
General Medicine
Biomechanical Phenomena
[SDV] Life Sciences [q-bio]
medicine.anatomical_structure
Medicine
Elongation
Cell Division
Research Article
Morphogen
vertex model
QH301-705.5
[PHYS.PHYS.PHYS-BIO-PH]Physics [physics]/Physics [physics]/Biological Physics [physics.bio-ph]
Science
General Biochemistry
Genetics and Molecular Biology

Adherens junction
03 medical and health sciences
Dogs
tissue elongation
0103 physical sciences
medicine
Animals
Humans
Symmetry breaking
010306 general physics
Process (anatomy)
030304 developmental biology
Boundary cell
General Immunology and Microbiology
Epithelial Cells
Global symmetry
In vitro
030104 developmental biology
Biophysics
Other
Caco-2 Cells
Zdroj: eLife
eLife, 2021, 10, ⟨10.7554/eLife.57730⟩
eLife, Vol 10 (2021)
eLife, eLife Sciences Publication, 2021, 10, ⟨10.7554/eLife.57730⟩
eLife, eLife Sciences Publication, 2020, ⟨10.7554/eLife.57730⟩
ISSN: 2050-084X
DOI: 10.7554/eLife.57730
Popis: Tissue elongation is a central morphogenetic event occurring in all organisms in development1,2. During this process, symmetry of cells and tissues is broken by different mechanisms, such as neighbor exchange3,4, cell elongation5,6 and oriented cell division7. While the phenomenon is known to involve remodeling of adherens junctions4 and acto-myosin4,8 at the molecular level, mesoscopic mechanisms leading to distinct morphogenesis processes are poorly understood. This is partly because inputs from morphogen gradients9 or from neighboring tissues10,11 can affect tissue autonomous self-organization in vivo. It is therefore difficult to disentangle cell intrinsic from externally mediated behaviors. Here we use in vitro experiments and numerical simulations to characterize the spontaneous behavior of a growing cell colony in vitro. We show that in vitro tissue elongation arises from anisotropy in the average cell elongation. This anisotropy sets the direction along which boundary cells migrate radially resulting in a non-isotropic elongation that arises primarily through cell elongation. For colonies submitted to a time periodic stretch, the axis of global symmetry breaking can be imposed by external force, and tissue elongation arises through oriented neighbor exchange. Emergence of radially migrating cells and the interplay between cell elongation and cell rearrangements are confirmed by numerical simulations based on a vertex model. Our results suggest that spontaneous shape deformation is related to the mean orientation of the nematic cell elongation field in the absence of any external input. This provides a framework to explain autonomous tissue elongation and how contributions from different mesoscopic mechanisms can be modulated by external forces.
Databáze: OpenAIRE