Size and position dependent cytoplasm viscoelasticity through hydrodynamic interactions with the cell surface

Many studies of cytoplasm rheology have focused on small components in the sub-micrometer scale. However, the cytoplasm also baths large organelles like nuclei, microtubule asters or spindles that often take significant portions of cells and move across the cytoplasm to regulate cell division or polarization. Here, we translated passive components of sizes ranging from few up to ~50 percent of the cell diameter, through the vast cytoplasm of live sea urchin eggs, with calibrated magnetic forces. Creep and relaxation responses indicate that for objects larger than the micron size, the cytoplasm behaves as a Jeffreys material, viscoelastic at short time-scales and fluidizing at longer times. However, as components size approached that of cells, cytoplasm viscoelastic resistance increased in a non-monotonic manner. Flow analysis and simulations suggest that this size-dependent viscoelasticity emerges from hydrodynamic interactions between the moving object and the static cell surface. This effect also yields to position-dependent viscoelasticity with objects initially closer to the cell surface being harder to displace. These findings suggest that the cytoplasm hydrodynamically couples large organelles to the cell surface to restrain their motion, with important implications for cell shape sensing and cellular organization. Significance StatementLarge-sized organelles like nuclei or mitotic spindles typically translocate through the cytoplasm to regulate cell division or polarity, but their frictional interaction with the cytoplasm and the cell surface remain poorly addressed. We used in vivo magnetic tweezers, to move passive components in a range of size in the cytoplasm of living cells. We found that the mobility of objects with sizes approaching that of cells, can be largely reduced as a result of hydrodynamic interactions that couple objects and the cell surface through the cytoplasm fluid.