The importance of intermediate filaments in the shape maintenance of myoblast model tissues

Liquid and elastic behaviours of tissues drive their morphology and response to the environment. They appear as the first insight into tissue mechanics. We explore the role of individual cell properties on spheroids of mouse muscle precursor cells and investigate the role of intermediate filaments o...

Full description

Bibliographic Details
Main Authors: Irène Nagle, Florence Delort, Sylvie Hénon, Claire Wilhelm, Sabrina Batonnet-Pichon, Myriam Reffay
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2022-12-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/76409
_version_ 1811292943295709184
author Irène Nagle
Florence Delort
Sylvie Hénon
Claire Wilhelm
Sabrina Batonnet-Pichon
Myriam Reffay
author_facet Irène Nagle
Florence Delort
Sylvie Hénon
Claire Wilhelm
Sabrina Batonnet-Pichon
Myriam Reffay
author_sort Irène Nagle
collection DOAJ
description Liquid and elastic behaviours of tissues drive their morphology and response to the environment. They appear as the first insight into tissue mechanics. We explore the role of individual cell properties on spheroids of mouse muscle precursor cells and investigate the role of intermediate filaments on surface tension and Young’s modulus. By flattening multicellular myoblast aggregates under magnetic constraint, we measure their rigidity and surface tension and show that they act as highly sensitive macroscopic reporters closely related to microscopic local tension and effective adhesion. Shedding light on the major contributions of acto-myosin contractility, actin organization, and intercellular adhesions, we reveal the role of a major component of intermediate filaments in the muscle, desmin and its organization, on the macroscopic mechanics of these tissue models. Implicated in the mechanical and shape integrity of cells, intermediate filaments are found to be crucial to the mechanics of unorganized muscle tissue models even at an early stage of differentiation both in terms of elasticity and surface tension.
first_indexed 2024-04-13T04:53:59Z
format Article
id doaj.art-06e70ba60be3489bace48b304fbf7cec
institution Directory Open Access Journal
issn 2050-084X
language English
last_indexed 2024-04-13T04:53:59Z
publishDate 2022-12-01
publisher eLife Sciences Publications Ltd
record_format Article
series eLife
spelling doaj.art-06e70ba60be3489bace48b304fbf7cec2022-12-22T03:01:34ZengeLife Sciences Publications LtdeLife2050-084X2022-12-011110.7554/eLife.76409The importance of intermediate filaments in the shape maintenance of myoblast model tissuesIrène Nagle0Florence Delort1Sylvie Hénon2Claire Wilhelm3Sabrina Batonnet-Pichon4Myriam Reffay5https://orcid.org/0000-0002-3695-2789Laboratoire Matière et Systèmes Complexes, UMR 7057, Université Paris Cité and CNRS, Paris, FranceLaboratoire Biologie Fonctionnelle et Adaptative, UMR 8251, Université Paris Cité and CNRS, Paris, FranceLaboratoire Matière et Systèmes Complexes, UMR 7057, Université Paris Cité and CNRS, Paris, FranceLaboratoire Matière et Systèmes Complexes, UMR 7057, Université Paris Cité and CNRS, Paris, FranceLaboratoire Biologie Fonctionnelle et Adaptative, UMR 8251, Université Paris Cité and CNRS, Paris, FranceLaboratoire Matière et Systèmes Complexes, UMR 7057, Université Paris Cité and CNRS, Paris, FranceLiquid and elastic behaviours of tissues drive their morphology and response to the environment. They appear as the first insight into tissue mechanics. We explore the role of individual cell properties on spheroids of mouse muscle precursor cells and investigate the role of intermediate filaments on surface tension and Young’s modulus. By flattening multicellular myoblast aggregates under magnetic constraint, we measure their rigidity and surface tension and show that they act as highly sensitive macroscopic reporters closely related to microscopic local tension and effective adhesion. Shedding light on the major contributions of acto-myosin contractility, actin organization, and intercellular adhesions, we reveal the role of a major component of intermediate filaments in the muscle, desmin and its organization, on the macroscopic mechanics of these tissue models. Implicated in the mechanical and shape integrity of cells, intermediate filaments are found to be crucial to the mechanics of unorganized muscle tissue models even at an early stage of differentiation both in terms of elasticity and surface tension.https://elifesciences.org/articles/76409mechanobiologysurface tensionelasticitymagnetic nanoparticlesintermediate filamentmyoblasts
spellingShingle Irène Nagle
Florence Delort
Sylvie Hénon
Claire Wilhelm
Sabrina Batonnet-Pichon
Myriam Reffay
The importance of intermediate filaments in the shape maintenance of myoblast model tissues
eLife
mechanobiology
surface tension
elasticity
magnetic nanoparticles
intermediate filament
myoblasts
title The importance of intermediate filaments in the shape maintenance of myoblast model tissues
title_full The importance of intermediate filaments in the shape maintenance of myoblast model tissues
title_fullStr The importance of intermediate filaments in the shape maintenance of myoblast model tissues
title_full_unstemmed The importance of intermediate filaments in the shape maintenance of myoblast model tissues
title_short The importance of intermediate filaments in the shape maintenance of myoblast model tissues
title_sort importance of intermediate filaments in the shape maintenance of myoblast model tissues
topic mechanobiology
surface tension
elasticity
magnetic nanoparticles
intermediate filament
myoblasts
url https://elifesciences.org/articles/76409
work_keys_str_mv AT irenenagle theimportanceofintermediatefilamentsintheshapemaintenanceofmyoblastmodeltissues
AT florencedelort theimportanceofintermediatefilamentsintheshapemaintenanceofmyoblastmodeltissues
AT sylviehenon theimportanceofintermediatefilamentsintheshapemaintenanceofmyoblastmodeltissues
AT clairewilhelm theimportanceofintermediatefilamentsintheshapemaintenanceofmyoblastmodeltissues
AT sabrinabatonnetpichon theimportanceofintermediatefilamentsintheshapemaintenanceofmyoblastmodeltissues
AT myriamreffay theimportanceofintermediatefilamentsintheshapemaintenanceofmyoblastmodeltissues
AT irenenagle importanceofintermediatefilamentsintheshapemaintenanceofmyoblastmodeltissues
AT florencedelort importanceofintermediatefilamentsintheshapemaintenanceofmyoblastmodeltissues
AT sylviehenon importanceofintermediatefilamentsintheshapemaintenanceofmyoblastmodeltissues
AT clairewilhelm importanceofintermediatefilamentsintheshapemaintenanceofmyoblastmodeltissues
AT sabrinabatonnetpichon importanceofintermediatefilamentsintheshapemaintenanceofmyoblastmodeltissues
AT myriamreffay importanceofintermediatefilamentsintheshapemaintenanceofmyoblastmodeltissues