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Passive coupling of membrane tension and cell volume during active response of cells to osmosis

During osmotic changes of their environment, cells actively regulate their volume and plasma membrane tension that can passively change through osmosis. How tension and volume are coupled during osmotic adaptation remains unknown, as their quantitative characterization is lacking. Here, we performed...

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Autores principales: Roffay, Chloé, Molinard, Guillaume, Kim, Kyoohyun, Urbanska, Marta, Andrade, Virginia, Barbarasa, Victoria, Nowak, Paulina, Mercier, Vincent, García-Calvo, José, Matile, Stefan, Loewith, Robbie, Echard, Arnaud, Guck, Jochen, Lenz, Martin, Roux, Aurélien
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8617515/
https://www.ncbi.nlm.nih.gov/pubmed/34785592
http://dx.doi.org/10.1073/pnas.2103228118
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author Roffay, Chloé
Molinard, Guillaume
Kim, Kyoohyun
Urbanska, Marta
Andrade, Virginia
Barbarasa, Victoria
Nowak, Paulina
Mercier, Vincent
García-Calvo, José
Matile, Stefan
Loewith, Robbie
Echard, Arnaud
Guck, Jochen
Lenz, Martin
Roux, Aurélien
author_facet Roffay, Chloé
Molinard, Guillaume
Kim, Kyoohyun
Urbanska, Marta
Andrade, Virginia
Barbarasa, Victoria
Nowak, Paulina
Mercier, Vincent
García-Calvo, José
Matile, Stefan
Loewith, Robbie
Echard, Arnaud
Guck, Jochen
Lenz, Martin
Roux, Aurélien
author_sort Roffay, Chloé
collection PubMed
description During osmotic changes of their environment, cells actively regulate their volume and plasma membrane tension that can passively change through osmosis. How tension and volume are coupled during osmotic adaptation remains unknown, as their quantitative characterization is lacking. Here, we performed dynamic membrane tension and cell volume measurements during osmotic shocks. During the first few seconds following the shock, cell volume varied to equilibrate osmotic pressures inside and outside the cell, and membrane tension dynamically followed these changes. A theoretical model based on the passive, reversible unfolding of the membrane as it detaches from the actin cortex during volume increase quantitatively describes our data. After the initial response, tension and volume recovered from hypoosmotic shocks but not from hyperosmotic shocks. Using a fluorescent membrane tension probe (fluorescent lipid tension reporter [Flipper-TR]), we investigated the coupling between tension and volume during these asymmetric recoveries. Caveolae depletion and pharmacological inhibition of ion transporters and channels, mTORCs, and the cytoskeleton all affected tension and volume responses. Treatments targeting mTORC2 and specific downstream effectors caused identical changes to both tension and volume responses, their coupling remaining the same. This supports that the coupling of tension and volume responses to osmotic shocks is primarily regulated by mTORC2.
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spelling pubmed-86175152021-12-09 Passive coupling of membrane tension and cell volume during active response of cells to osmosis Roffay, Chloé Molinard, Guillaume Kim, Kyoohyun Urbanska, Marta Andrade, Virginia Barbarasa, Victoria Nowak, Paulina Mercier, Vincent García-Calvo, José Matile, Stefan Loewith, Robbie Echard, Arnaud Guck, Jochen Lenz, Martin Roux, Aurélien Proc Natl Acad Sci U S A Physical Sciences During osmotic changes of their environment, cells actively regulate their volume and plasma membrane tension that can passively change through osmosis. How tension and volume are coupled during osmotic adaptation remains unknown, as their quantitative characterization is lacking. Here, we performed dynamic membrane tension and cell volume measurements during osmotic shocks. During the first few seconds following the shock, cell volume varied to equilibrate osmotic pressures inside and outside the cell, and membrane tension dynamically followed these changes. A theoretical model based on the passive, reversible unfolding of the membrane as it detaches from the actin cortex during volume increase quantitatively describes our data. After the initial response, tension and volume recovered from hypoosmotic shocks but not from hyperosmotic shocks. Using a fluorescent membrane tension probe (fluorescent lipid tension reporter [Flipper-TR]), we investigated the coupling between tension and volume during these asymmetric recoveries. Caveolae depletion and pharmacological inhibition of ion transporters and channels, mTORCs, and the cytoskeleton all affected tension and volume responses. Treatments targeting mTORC2 and specific downstream effectors caused identical changes to both tension and volume responses, their coupling remaining the same. This supports that the coupling of tension and volume responses to osmotic shocks is primarily regulated by mTORC2. National Academy of Sciences 2021-11-16 2021-11-23 /pmc/articles/PMC8617515/ /pubmed/34785592 http://dx.doi.org/10.1073/pnas.2103228118 Text en Copyright © 2021 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Physical Sciences
Roffay, Chloé
Molinard, Guillaume
Kim, Kyoohyun
Urbanska, Marta
Andrade, Virginia
Barbarasa, Victoria
Nowak, Paulina
Mercier, Vincent
García-Calvo, José
Matile, Stefan
Loewith, Robbie
Echard, Arnaud
Guck, Jochen
Lenz, Martin
Roux, Aurélien
Passive coupling of membrane tension and cell volume during active response of cells to osmosis
title Passive coupling of membrane tension and cell volume during active response of cells to osmosis
title_full Passive coupling of membrane tension and cell volume during active response of cells to osmosis
title_fullStr Passive coupling of membrane tension and cell volume during active response of cells to osmosis
title_full_unstemmed Passive coupling of membrane tension and cell volume during active response of cells to osmosis
title_short Passive coupling of membrane tension and cell volume during active response of cells to osmosis
title_sort passive coupling of membrane tension and cell volume during active response of cells to osmosis
topic Physical Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8617515/
https://www.ncbi.nlm.nih.gov/pubmed/34785592
http://dx.doi.org/10.1073/pnas.2103228118
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