scholarly journals A mechano-osmotic feedback couples cell volume to the rate of cell deformation

2021 ◽  
Author(s):  
Larisa Venkova ◽  
Amit Singh Vishen ◽  
Sergio Lembo ◽  
Nishit Srivastava ◽  
Baptiste Duchamp ◽  
...  
Keyword(s):  
Cell Volume ◽  
Cell Shape ◽  
Cell Deformation ◽  
Volume Loss ◽  
Membrane Tension ◽  
Cellular Physiology ◽  
Central Focus ◽  
The Past ◽  
Actin Cortex ◽  
Shape Changes

Mechanics has been a central focus of physical biology in the past decade. In comparison, the osmotic and electric properties of cells are less understood. Here we show that a parameter central to both the physics and the physiology of the cell, its volume, depends on a mechano-osmotic coupling. We found that cells change their volume depending on the rate at which they change shape, when they spread, migrate or are externally deformed. Cells undergo slow deformation at constant volume, while fast deformation leads to volume loss. We propose a mechano-sensitive pump and leak model to explain this phenomenon. Our model and experiments suggest that volume modulation depends on the state of the actin cortex and the coupling of ion fluxes to membrane tension. This mechano-osmotic coupling defines a membrane tension homeostasis module constantly at work in cells, causing volume fluctuations associated with fast cell shape changes, with potential consequences on cellular physiology.

scholarly journals Cell volume changes contribute to epithelial morphogenesis in zebrafish Kupffer’s vesicle

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Agnik Dasgupta ◽  
Matthias Merkel ◽  
Madeline J Clark ◽  
Andrew E Jacob ◽  
Jonathan Edward Dawson ◽  
...  
Keyword(s):  
Cell Volume ◽  
Cell Shape ◽  
Single Cells ◽  
Ion Flux ◽  
Epithelial Morphogenesis ◽  
Volume Changes ◽  
Kupffer’S Vesicle ◽  
Kupffer's Vesicle ◽  
Cell Shape Changes ◽  
Shape Changes

How epithelial cell behaviors are coordinately regulated to sculpt tissue architecture is a fundamental question in biology. Kupffer’s vesicle (KV), a transient organ with a fluid-filled lumen, provides a simple system to investigate the interplay between intrinsic cellular mechanisms and external forces during epithelial morphogenesis. Using 3-dimensional (3D) analyses of single cells we identify asymmetric cell volume changes along the anteroposterior axis of KV that coincide with asymmetric cell shape changes. Blocking ion flux prevents these cell volume changes and cell shape changes. Vertex simulations suggest cell shape changes do not depend on lumen expansion. Consistent with this prediction, asymmetric changes in KV cell volume and shape occur normally when KV lumen growth fails due to leaky cell adhesions. These results indicate ion flux mediates cell volume changes that contribute to asymmetric cell shape changes in KV, and that these changes in epithelial morphology are separable from lumen-generated forces.

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

2021 ◽  
Vol 118 (47) ◽  
pp. e2103228118
Author(s):  
Chloé Roffay ◽  
Guillaume Molinard ◽  
Kyoohyun Kim ◽  
Marta Urbanska ◽  
Virginia Andrade ◽  
...  
Keyword(s):  
Cell Volume ◽  
Initial Response ◽  
Membrane Tension ◽  
Shock Cell ◽  
Dynamic Membrane ◽  
Osmotic Adaptation ◽  
Volume Increase ◽  
Actin Cortex ◽  
Downstream Effectors ◽  
Volume Measurements

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.

scholarly journals Asymmetric cell volume changes regulate epithelial morphogenesis in zebrafish Kupffer’s vesicle

2017 ◽  
Author(s):  
Agnik Dasgupta ◽  
Matthias Merkel ◽  
Andrew E. Jacob ◽  
Jonathan Dawson ◽  
M. Lisa Manning ◽  
...  
Keyword(s):  
Cell Volume ◽  
Cell Shape ◽  
Single Cells ◽  
Ion Flux ◽  
Epithelial Morphogenesis ◽  
Volume Changes ◽  
Kupffer’S Vesicle ◽  
Kupffer's Vesicle ◽  
Cell Shape Changes ◽  
Shape Changes

ABSTRACTHow epithelial cell behaviors are coordinately regulated to sculpt tissue architecture is a fundamental question in biology. Kupffer's vesicle (KV), a transient organ with a fluid - filled lumen, provides a simple system to investigate the interplay between intrinsic cellular mechanisms and external forces during epithelial morphogenesis. Using 3 - dimensional (3D) analyses of single cells we identify asymmetric cell volume changes along the anteroposterior axis of KV that coincide with asymmetric cell shape changes. Blocking ion flux prevents these cell volume changes and cell shape changes. Vertex simulations suggest cell shape changes do not depend on lumen expansion. Consistent with this prediction, asymmetric changes in KV cell volume and shape occur normally when KV lumen growth fails due to leaky cell adhesions. These results indicate ion flux mediates asymmetric cell volume changes that contribute to asymmetric cell shape changes in KV, and that these changes in epithelial morphology are separable from lumen - generated forces.

scholarly journals Getting in shape and swimming: the role of cortical forces and membrane heterogeneity in eukaryotic cells

2017 ◽  
Author(s):  
Hao Wu ◽  
Marco Avila Ponce de León ◽  
Hans G. Othmer
Keyword(s):  
Cell Movement ◽  
Membrane Properties ◽  
Membrane Tension ◽  
Actin Cortex ◽  
Bending Modulus ◽  
Motile Cells ◽  
Cell Shapes ◽  
Direction Of Movement ◽  
Shape Changes

AbstractRecent research has shown that motile cells can adapt their mode of propulsion to the mechanical properties of the environment in which they find themselves – crawling in some environments while swimming in others. The latter can involve movement by blebbing or other cyclic shape changes, and both highly-simplified and more realistic models of these modes have been studied previously. Herein we study swimming that is driven by membrane tension gradients that arise from flows in the actin cortex underlying the membrane, and does not involve imposed cyclic shape changes. Such gradients can lead to a number of different characteristic cell shapes, and our first objective is to understand how different distributions of membrane tension influence the shape of cells in a quiescent fluid. We then analyze the effects of spatial variation in other membrane properties, and how they interact with tension gradients to determine the shape. We also study the effect of fluid-cell interactions and show how tension leads to cell movement, how the balance between tension gradients and a variable bending modulus determine the shape and direction of movement, and how the efficiency of movement depends on the properties of the fluid and the distribution of tension and bending modulus in the membrane.Dedicated to the memory of Karl P. Hadeler, a pioneer in the field of Mathematical Biology and a friend and mentor to many.

scholarly journals Quantitative coupling of cell volume and membrane tension during osmotic shocks

2021 ◽  
Author(s):  
Chloé Roffay ◽  
Guillaume Molinard ◽  
Kyoohyun Kim ◽  
Victoria Barbarassa ◽  
Marta Urbanska ◽  
...  
Keyword(s):  
Cell Volume ◽  
Initial Response ◽  
Membrane Tension ◽  
Shock Cell ◽  
Dynamic Membrane ◽  
Osmotic Adaptation ◽  
Volume Increase ◽  
Actin Cortex ◽  
Passive Mechanism ◽  
Volume Measurements

ABSTRACTDuring 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 a 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. During these asymmetric recoveries, tension and volume remained coupled. Pharmacological disruption of the cytoskeleton and functional inhibition of ion channels and mTOR all affected tension and volume responses, proving that a passive mechanism is necessary and critical for the cell to adapt fast. The coupling between them was, nonetheless, maintained for a few exceptions suggesting that volume and tension regulations are independent from the regulation of their coupling.

scholarly journals A genetic screen for temperature-sensitive morphogenesis-defectiveCaenorhabditis elegansmutants

2021 ◽  
Vol 11 (4) ◽  
Author(s):  
Molly C Jud ◽  
Josh Lowry ◽  
Thalia Padilla ◽  
Erin Clifford ◽  
Yuqi Yang ◽  
...  
Keyword(s):  
Cell Shape ◽  
The Body ◽  
Temperature Sensitive ◽  
Restrictive Temperature ◽  
Fundamental Biological Process ◽  
Embryonic Morphogenesis ◽  
Cell Shape Changes ◽  
Development Temperature ◽  
Multicellular Organisms ◽  
Shape Changes

AbstractMorphogenesis involves coordinated cell migrations and cell shape changes that generate tissues and organs, and organize the body plan. Cell adhesion and the cytoskeleton are important for executing morphogenesis, but their regulation remains poorly understood. As genes required for embryonic morphogenesis may have earlier roles in development, temperature-sensitive embryonic-lethal mutations are useful tools for investigating this process. From a collection of ∼200 such Caenorhabditis elegans mutants, we have identified 17 that have highly penetrant embryonic morphogenesis defects after upshifts from the permissive to the restrictive temperature, just prior to the cell shape changes that mediate elongation of the ovoid embryo into a vermiform larva. Using whole genome sequencing, we identified the causal mutations in seven affected genes. These include three genes that have roles in producing the extracellular matrix, which is known to affect the morphogenesis of epithelial tissues in multicellular organisms: the rib-1 and rib-2 genes encode glycosyltransferases, and the emb-9 gene encodes a collagen subunit. We also used live imaging to characterize epidermal cell shape dynamics in one mutant, or1219ts, and observed cell elongation defects during dorsal intercalation and ventral enclosure that may be responsible for the body elongation defects. These results indicate that our screen has identified factors that influence morphogenesis and provides a platform for advancing our understanding of this fundamental biological process.

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