Journal
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
Volume 118, Issue 47, Pages -Publisher
NATL ACAD SCIENCES
DOI: 10.1073/pnas.2103228118
Keywords
plasma membrane tension; cell volume; flipper-TR; osmotic shocks; mechanobiology
Categories
Funding
- Human Frontier Science Program Young Investigator Grant [RGY0076/2009-C]
- Swiss National Fund [31003A_149975, 31003A_173087]
- Synergia Grant [CRSII5_189996]
- European Research Council Consolidator Grant [311536]
- Synergy Grant [951324-R2-TENSION]
- Institut Pasteur
- CNRS
- ANR (SeptScort)
- Doctoral School Complexite du Vivant [ED515]
- La Ligue Contre le Cancer
- ANR [ANR-15-CE13-0004-03]
- European Research Council [677532]
- Swiss National Science Foundation (SNF) [31003A_149975, 31003A_173087, CRSII5_189996] Funding Source: Swiss National Science Foundation (SNF)
- European Research Council (ERC) [311536] Funding Source: European Research Council (ERC)
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This study investigated the coupling between membrane tension and cell volume during osmotic shocks. It was found that membrane tension dynamically followed changes in cell volume as it equilibrated osmotic pressures inside and outside the cell. While tension and volume recovered from hypoosmotic shocks, they did not fully recover from hyperosmotic shocks, with mTORC2 potentially playing a key role in regulating the response to osmotic shocks.
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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