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

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Abstract

Liquid and elastic behaviors of tissues drives their morphology and their 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 attening 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.

Data availability

Data supporting the findings of this study are available within the article and its Supplementary information files. Computing resources should be found on Github (https://github.com/mreffay/INagle-MReffay).

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Irène Nagle

Laboratoire Matière et Systèmes Complexes, Université de Paris, CNRS, Paris, France

Competing interests
The authors declare that no competing interests exist.
Florence Delort

Laboratoire Biologie Fonctionnelle et Adaptative, Université de Paris, CNRS, Paris, France

Competing interests
The authors declare that no competing interests exist.
Sylvie Hénon

Laboratoire Matière et Systèmes Complexes, Université de Paris, CNRS, Paris, France

Competing interests
The authors declare that no competing interests exist.
Claire Wilhelm

Laboratoire Physico-Chimie Curie, Institute Curie, Paris, France

Competing interests
The authors declare that no competing interests exist.
Sabrina Batonnet-Pichon

Laboratoire Biologie Fonctionnelle et Adaptative, Université de Paris, CNRS, Paris, France

Competing interests
The authors declare that no competing interests exist.
Myriam Reffay

Laboratoire Matiere et Systemes Complexes, Université de Paris, CNRS, Paris, France

For correspondence
myriam.reffay@u-paris.fr

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-3695-2789

Funding

Emergence Ville de Paris (MAGIC)

Myriam Reffay

AFM (AFM-22956)

Sabrina Batonnet-Pichon

French Defense Procurement Agency

Myriam Reffay

Labex Who Am I? (Labex ANR-11-LABX-0071)

Myriam Reffay

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.