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Spatial distribution of cell–cell and cell–ECM adhesions regulates force balance while main­taining E-cadherin molecular tension in cell pairs

Mechanical linkage between cell–cell and cell–extracellular matrix (ECM) adhesions regulates cell shape changes during embryonic development and tissue homoeostasis. We examined how the force balance between cell–cell and cell–ECM adhesions changes with cell spread area and aspect ratio in pairs of...

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Autores principales: Sim, Joo Yong, Moeller, Jens, Hart, Kevin C., Ramallo, Diego, Vogel, Viola, Dunn, Alex R., Nelson, W. James, Pruitt, Beth L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The American Society for Cell Biology 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4571300/
https://www.ncbi.nlm.nih.gov/pubmed/25971797
http://dx.doi.org/10.1091/mbc.E14-12-1618
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author Sim, Joo Yong
Moeller, Jens
Hart, Kevin C.
Ramallo, Diego
Vogel, Viola
Dunn, Alex R.
Nelson, W. James
Pruitt, Beth L.
author_facet Sim, Joo Yong
Moeller, Jens
Hart, Kevin C.
Ramallo, Diego
Vogel, Viola
Dunn, Alex R.
Nelson, W. James
Pruitt, Beth L.
author_sort Sim, Joo Yong
collection PubMed
description Mechanical linkage between cell–cell and cell–extracellular matrix (ECM) adhesions regulates cell shape changes during embryonic development and tissue homoeostasis. We examined how the force balance between cell–cell and cell–ECM adhesions changes with cell spread area and aspect ratio in pairs of MDCK cells. We used ECM micropatterning to drive different cytoskeleton strain energy states and cell-generated traction forces and used a Förster resonance energy transfer tension biosensor to ask whether changes in forces across cell–cell junctions correlated with E-cadherin molecular tension. We found that continuous peripheral ECM adhesions resulted in increased cell–cell and cell–ECM forces with increasing spread area. In contrast, confining ECM adhesions to the distal ends of cell–cell pairs resulted in shorter junction lengths and constant cell–cell forces. Of interest, each cell within a cell pair generated higher strain energies than isolated single cells of the same spread area. Surprisingly, E-cadherin molecular tension remained constant regardless of changes in cell–cell forces and was evenly distributed along cell–cell junctions independent of cell spread area and total traction forces. Taken together, our results showed that cell pairs maintained constant E-cadherin molecular tension and regulated total forces relative to cell spread area and shape but independently of total focal adhesion area.
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spelling pubmed-45713002015-09-29 Spatial distribution of cell–cell and cell–ECM adhesions regulates force balance while main­taining E-cadherin molecular tension in cell pairs Sim, Joo Yong Moeller, Jens Hart, Kevin C. Ramallo, Diego Vogel, Viola Dunn, Alex R. Nelson, W. James Pruitt, Beth L. Mol Biol Cell Articles Mechanical linkage between cell–cell and cell–extracellular matrix (ECM) adhesions regulates cell shape changes during embryonic development and tissue homoeostasis. We examined how the force balance between cell–cell and cell–ECM adhesions changes with cell spread area and aspect ratio in pairs of MDCK cells. We used ECM micropatterning to drive different cytoskeleton strain energy states and cell-generated traction forces and used a Förster resonance energy transfer tension biosensor to ask whether changes in forces across cell–cell junctions correlated with E-cadherin molecular tension. We found that continuous peripheral ECM adhesions resulted in increased cell–cell and cell–ECM forces with increasing spread area. In contrast, confining ECM adhesions to the distal ends of cell–cell pairs resulted in shorter junction lengths and constant cell–cell forces. Of interest, each cell within a cell pair generated higher strain energies than isolated single cells of the same spread area. Surprisingly, E-cadherin molecular tension remained constant regardless of changes in cell–cell forces and was evenly distributed along cell–cell junctions independent of cell spread area and total traction forces. Taken together, our results showed that cell pairs maintained constant E-cadherin molecular tension and regulated total forces relative to cell spread area and shape but independently of total focal adhesion area. The American Society for Cell Biology 2015-07-01 /pmc/articles/PMC4571300/ /pubmed/25971797 http://dx.doi.org/10.1091/mbc.E14-12-1618 Text en © 2015 Sim, Moeller, et al. This article is distributed by The American Society for Cell Biology under license from the author(s). Two months after publication it is available to the public under an Attribution–Noncommercial–Share Alike 3.0 Unported Creative Commons License (http://creativecommons.org/licenses/by-nc-sa/3.0). “ASCB®,” “The American Society for Cell Biology®,” and “Molecular Biology of the Cell®” are registered trademarks of The American Society for Cell Biology.
spellingShingle Articles
Sim, Joo Yong
Moeller, Jens
Hart, Kevin C.
Ramallo, Diego
Vogel, Viola
Dunn, Alex R.
Nelson, W. James
Pruitt, Beth L.
Spatial distribution of cell–cell and cell–ECM adhesions regulates force balance while main­taining E-cadherin molecular tension in cell pairs
title Spatial distribution of cell–cell and cell–ECM adhesions regulates force balance while main­taining E-cadherin molecular tension in cell pairs
title_full Spatial distribution of cell–cell and cell–ECM adhesions regulates force balance while main­taining E-cadherin molecular tension in cell pairs
title_fullStr Spatial distribution of cell–cell and cell–ECM adhesions regulates force balance while main­taining E-cadherin molecular tension in cell pairs
title_full_unstemmed Spatial distribution of cell–cell and cell–ECM adhesions regulates force balance while main­taining E-cadherin molecular tension in cell pairs
title_short Spatial distribution of cell–cell and cell–ECM adhesions regulates force balance while main­taining E-cadherin molecular tension in cell pairs
title_sort spatial distribution of cell–cell and cell–ecm adhesions regulates force balance while main­taining e-cadherin molecular tension in cell pairs
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4571300/
https://www.ncbi.nlm.nih.gov/pubmed/25971797
http://dx.doi.org/10.1091/mbc.E14-12-1618
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