The cytoplasm of living cells can sustain transient and steady intracellular pressure gradients

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Abstract

Understanding the physical basis of cellular shape change in response to both internal and external mechanical stresses requires characterisation of cytoplasmic rheology. At subsecond time-scales and micron length-scales, cells behave as fluid-filled sponges in which shape changes necessitate intracellular fluid redistribution. However, whether these cytoplasmic poroelastic properties play an important role in cellular mechanical response over length- scales and time-scales relevant to cell physiology remains unclear. Here, we investigated whether and how a localised deformation of the cell surface gives rise to transient intracellular flows spanning several microns and lasting seconds. Next, we showed that pressure gradients induced in the cytoplasm can be sustained over several minutes. We found that stable pressure gradients can arise from the combination of cortical tension, cytoplasmic poroelasticity and water flows across the membrane. Overall our data indicate that intracellular cytosolic flows and pressure gradients may play a much greater role than currently appreciated, acting over time- and length-scales relevant to mechanotransduction and cell migration, signifying that poroelastic properties need to be accounted for in models of the cell.

Significance statement

Understanding how cells change shape dynamically under the influence of external and internal forces requires characterisation of the mechanical response of the cytoplasm, the viscous material that fills their interior. The cytoplasm consists of a porous solid phase bathed in a fluid, the cytosol. As the cytoplasm is incompressible, any cellular shape change necessitates redistribution of the cytosol within the cell and its flow rate sets the time-scale for deformation. How the cytoplasmic mechanical response affects cell physiology remains poorly understood. We show that the unique physical properties of the cytoplasm allow cells to sustain cellular-scale pressure gradients over minute time-scales. As a consequence, pressure-driven mechanisms may play a much greater role in cell physiology than currently appreciated.

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