Passive coupling of membrane tension and cell volume during active response of cells to osmosis – Archive ouverte HAL

Chloé Roffay ¹ Guillaume Molinard ¹ Kyoohyun Kim ^{2, 3} Marta Urbanska ^{2, 3} Virginia Andrade ^{4, 5} Victoria Barbarasa ¹ Paulina Nowak ¹ Vincent Mercier ¹ José García-Calvo ¹ Stefan Matile ¹ Robbie Loewith ¹ Arnaud Echard ⁴ Jochen Guck ^{2, 3} Martin Lenz ^{6, 7} Aurélien Roux ^{1, *}

Chloé Roffay, Guillaume Molinard, Kyoohyun Kim, Marta Urbanska, Virginia Andrade, et al.. Passive coupling of membrane tension and cell volume during active response of cells to osmosis. Proceedings of the National Academy of Sciences of the United States of America , National Academy of Sciences, 2021, 118 (47), pp.e2103228118. ⟨10.1073/pnas.2103228118⟩. ⟨hal-03451662⟩

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.

• 1. University of Geneva [Switzerland]
• 2. Max Planck Institute for the Science of Light
• 3. TU Dresden – Technische Universität Dresden = Dresden University of Technology
• 4. Trafic membranaire et Division cellulaire – Membrane Traffic and Cell Division
• 5. Collège doctoral [Sorbonne universités]
• 6. LPTMS – Laboratoire de Physique Théorique et Modèles Statistiques
• 7. PMMH – Physique et mécanique des milieux hétérogenes (UMR 7636)