Cargando…

Surface tension of model tissues during malignant transformation and epithelial–mesenchymal transition

Epithelial–mesenchymal transition is associated with migration, invasion, and metastasis. The translation at the tissue scale of these changes has not yet been enlightened while being essential in the understanding of tumor progression. Thus, biophysical tools dedicated to measurements on model tumo...

Descripción completa

Detalles Bibliográficos
Autores principales: Nagle, Irène, Richert, Alain, Quinteros, Michael, Janel, Sébastien, Buysschaert, Edgar, Luciani, Nathalie, Debost, Henry, Thevenet, Véronique, Wilhelm, Claire, Prunier, Céline, Lafont, Frank, Padilla-Benavides, Teresita, Boissan, Mathieu, Reffay, Myriam
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9468677/
https://www.ncbi.nlm.nih.gov/pubmed/36111347
http://dx.doi.org/10.3389/fcell.2022.926322
_version_ 1784788467248529408
author Nagle, Irène
Richert, Alain
Quinteros, Michael
Janel, Sébastien
Buysschaert, Edgar
Luciani, Nathalie
Debost, Henry
Thevenet, Véronique
Wilhelm, Claire
Prunier, Céline
Lafont, Frank
Padilla-Benavides, Teresita
Boissan, Mathieu
Reffay, Myriam
author_facet Nagle, Irène
Richert, Alain
Quinteros, Michael
Janel, Sébastien
Buysschaert, Edgar
Luciani, Nathalie
Debost, Henry
Thevenet, Véronique
Wilhelm, Claire
Prunier, Céline
Lafont, Frank
Padilla-Benavides, Teresita
Boissan, Mathieu
Reffay, Myriam
author_sort Nagle, Irène
collection PubMed
description Epithelial–mesenchymal transition is associated with migration, invasion, and metastasis. The translation at the tissue scale of these changes has not yet been enlightened while being essential in the understanding of tumor progression. Thus, biophysical tools dedicated to measurements on model tumor systems are needed to reveal the impact of epithelial–mesenchymal transition at the collective cell scale. Herein, using an original biophysical approach based on magnetic nanoparticle insertion inside cells, we formed and flattened multicellular aggregates to explore the consequences of the loss of the metastasis suppressor NME1 on the mechanical properties at the tissue scale. Multicellular spheroids behave as viscoelastic fluids, and their equilibrium shape is driven by surface tension as measured by their deformation upon magnetic field application. In a model of breast tumor cells genetically modified for NME1, we correlated tumor invasion, migration, and adhesion modifications with shape maintenance properties by measuring surface tension and exploring both invasive and migratory potential as well as adhesion characteristics.
format Online
Article
Text
id pubmed-9468677
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-94686772022-09-14 Surface tension of model tissues during malignant transformation and epithelial–mesenchymal transition Nagle, Irène Richert, Alain Quinteros, Michael Janel, Sébastien Buysschaert, Edgar Luciani, Nathalie Debost, Henry Thevenet, Véronique Wilhelm, Claire Prunier, Céline Lafont, Frank Padilla-Benavides, Teresita Boissan, Mathieu Reffay, Myriam Front Cell Dev Biol Cell and Developmental Biology Epithelial–mesenchymal transition is associated with migration, invasion, and metastasis. The translation at the tissue scale of these changes has not yet been enlightened while being essential in the understanding of tumor progression. Thus, biophysical tools dedicated to measurements on model tumor systems are needed to reveal the impact of epithelial–mesenchymal transition at the collective cell scale. Herein, using an original biophysical approach based on magnetic nanoparticle insertion inside cells, we formed and flattened multicellular aggregates to explore the consequences of the loss of the metastasis suppressor NME1 on the mechanical properties at the tissue scale. Multicellular spheroids behave as viscoelastic fluids, and their equilibrium shape is driven by surface tension as measured by their deformation upon magnetic field application. In a model of breast tumor cells genetically modified for NME1, we correlated tumor invasion, migration, and adhesion modifications with shape maintenance properties by measuring surface tension and exploring both invasive and migratory potential as well as adhesion characteristics. Frontiers Media S.A. 2022-08-30 /pmc/articles/PMC9468677/ /pubmed/36111347 http://dx.doi.org/10.3389/fcell.2022.926322 Text en Copyright © 2022 Nagle, Richert, Quinteros, Janel, Buysschaert, Luciani, Debost, Thevenet, Wilhelm, Prunier, Lafont, Padilla-Benavides, Boissan and Reffay. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Cell and Developmental Biology
Nagle, Irène
Richert, Alain
Quinteros, Michael
Janel, Sébastien
Buysschaert, Edgar
Luciani, Nathalie
Debost, Henry
Thevenet, Véronique
Wilhelm, Claire
Prunier, Céline
Lafont, Frank
Padilla-Benavides, Teresita
Boissan, Mathieu
Reffay, Myriam
Surface tension of model tissues during malignant transformation and epithelial–mesenchymal transition
title Surface tension of model tissues during malignant transformation and epithelial–mesenchymal transition
title_full Surface tension of model tissues during malignant transformation and epithelial–mesenchymal transition
title_fullStr Surface tension of model tissues during malignant transformation and epithelial–mesenchymal transition
title_full_unstemmed Surface tension of model tissues during malignant transformation and epithelial–mesenchymal transition
title_short Surface tension of model tissues during malignant transformation and epithelial–mesenchymal transition
title_sort surface tension of model tissues during malignant transformation and epithelial–mesenchymal transition
topic Cell and Developmental Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9468677/
https://www.ncbi.nlm.nih.gov/pubmed/36111347
http://dx.doi.org/10.3389/fcell.2022.926322
work_keys_str_mv AT nagleirene surfacetensionofmodeltissuesduringmalignanttransformationandepithelialmesenchymaltransition
AT richertalain surfacetensionofmodeltissuesduringmalignanttransformationandepithelialmesenchymaltransition
AT quinterosmichael surfacetensionofmodeltissuesduringmalignanttransformationandepithelialmesenchymaltransition
AT janelsebastien surfacetensionofmodeltissuesduringmalignanttransformationandepithelialmesenchymaltransition
AT buysschaertedgar surfacetensionofmodeltissuesduringmalignanttransformationandepithelialmesenchymaltransition
AT lucianinathalie surfacetensionofmodeltissuesduringmalignanttransformationandepithelialmesenchymaltransition
AT debosthenry surfacetensionofmodeltissuesduringmalignanttransformationandepithelialmesenchymaltransition
AT thevenetveronique surfacetensionofmodeltissuesduringmalignanttransformationandepithelialmesenchymaltransition
AT wilhelmclaire surfacetensionofmodeltissuesduringmalignanttransformationandepithelialmesenchymaltransition
AT prunierceline surfacetensionofmodeltissuesduringmalignanttransformationandepithelialmesenchymaltransition
AT lafontfrank surfacetensionofmodeltissuesduringmalignanttransformationandepithelialmesenchymaltransition
AT padillabenavidesteresita surfacetensionofmodeltissuesduringmalignanttransformationandepithelialmesenchymaltransition
AT boissanmathieu surfacetensionofmodeltissuesduringmalignanttransformationandepithelialmesenchymaltransition
AT reffaymyriam surfacetensionofmodeltissuesduringmalignanttransformationandepithelialmesenchymaltransition