Evolution of a confluent gut epithelium under on-chip cyclic stretching

The progress of food in the gastrointestinal (GI) tract is driven by a peristaltic motion generated by the muscle belt surrounding the GI tract. In turn, the response of the intestinal epithelial cells to the peristaltic stresses affects the dynamics of the epithelial structure. In this work, we stu...

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Main Authors: Lauriane Gérémie, Efe Ilker, Moencopi Bernheim-Dennery, Charles Cavaniol, Jean-Louis Viovy, Danijela Matic Vignjevic, Jean-François Joanny, Stéphanie Descroix
Format: Article
Language:English
Published: American Physical Society 2022-04-01
Series:Physical Review Research
Online Access:http://doi.org/10.1103/PhysRevResearch.4.023032
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author Lauriane Gérémie
Efe Ilker
Moencopi Bernheim-Dennery
Charles Cavaniol
Jean-Louis Viovy
Danijela Matic Vignjevic
Jean-François Joanny
Stéphanie Descroix
author_facet Lauriane Gérémie
Efe Ilker
Moencopi Bernheim-Dennery
Charles Cavaniol
Jean-Louis Viovy
Danijela Matic Vignjevic
Jean-François Joanny
Stéphanie Descroix
author_sort Lauriane Gérémie
collection DOAJ
description The progress of food in the gastrointestinal (GI) tract is driven by a peristaltic motion generated by the muscle belt surrounding the GI tract. In turn, the response of the intestinal epithelial cells to the peristaltic stresses affects the dynamics of the epithelial structure. In this work, we study the effect of cyclic stretching (0.125 Hz, 10% strain) on the spatial organization of the intestinal epithelium using intestinal cells deposited on a flat elastomeric substrate to mimic the peristaltic motion in vitro. A confluent monolayer of Caco-2 cells is grown on a PDMS chip to probe the morphological and orientational response of the tissue to cyclic stretching. The PDMS chips are either covalently or noncovalently coated with laminin to recapitulate the basement membrane. We observe a significant orientational response where the cells rearrange their long axes perpendicular to the stretching direction for both coating conditions. The experiment is modeled by a vertex model where the cells store elastic energy with varying strain and effectively have a rotational diffusive motion of their long axes through rearrangements of their shapes. The model also predicts a transition between the perpendicular orientation and the orientation at an oblique angle determined by the level of the cell elastic anisotropy. It provides a general framework to study cell response and relaxation dynamics under cyclic stretching across different cell types. We also discuss potential relevance of peristalsis in determining planar cell polarity in three-dimensional architectures.
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spelling doaj.art-e1e6864b360a4f5cb035be1f6e447bd42024-04-12T17:19:46ZengAmerican Physical SocietyPhysical Review Research2643-15642022-04-014202303210.1103/PhysRevResearch.4.023032Evolution of a confluent gut epithelium under on-chip cyclic stretchingLauriane GérémieEfe IlkerMoencopi Bernheim-DenneryCharles CavaniolJean-Louis ViovyDanijela Matic VignjevicJean-François JoannyStéphanie DescroixThe progress of food in the gastrointestinal (GI) tract is driven by a peristaltic motion generated by the muscle belt surrounding the GI tract. In turn, the response of the intestinal epithelial cells to the peristaltic stresses affects the dynamics of the epithelial structure. In this work, we study the effect of cyclic stretching (0.125 Hz, 10% strain) on the spatial organization of the intestinal epithelium using intestinal cells deposited on a flat elastomeric substrate to mimic the peristaltic motion in vitro. A confluent monolayer of Caco-2 cells is grown on a PDMS chip to probe the morphological and orientational response of the tissue to cyclic stretching. The PDMS chips are either covalently or noncovalently coated with laminin to recapitulate the basement membrane. We observe a significant orientational response where the cells rearrange their long axes perpendicular to the stretching direction for both coating conditions. The experiment is modeled by a vertex model where the cells store elastic energy with varying strain and effectively have a rotational diffusive motion of their long axes through rearrangements of their shapes. The model also predicts a transition between the perpendicular orientation and the orientation at an oblique angle determined by the level of the cell elastic anisotropy. It provides a general framework to study cell response and relaxation dynamics under cyclic stretching across different cell types. We also discuss potential relevance of peristalsis in determining planar cell polarity in three-dimensional architectures.http://doi.org/10.1103/PhysRevResearch.4.023032
spellingShingle Lauriane Gérémie
Efe Ilker
Moencopi Bernheim-Dennery
Charles Cavaniol
Jean-Louis Viovy
Danijela Matic Vignjevic
Jean-François Joanny
Stéphanie Descroix
Evolution of a confluent gut epithelium under on-chip cyclic stretching
Physical Review Research
title Evolution of a confluent gut epithelium under on-chip cyclic stretching
title_full Evolution of a confluent gut epithelium under on-chip cyclic stretching
title_fullStr Evolution of a confluent gut epithelium under on-chip cyclic stretching
title_full_unstemmed Evolution of a confluent gut epithelium under on-chip cyclic stretching
title_short Evolution of a confluent gut epithelium under on-chip cyclic stretching
title_sort evolution of a confluent gut epithelium under on chip cyclic stretching
url http://doi.org/10.1103/PhysRevResearch.4.023032
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