Active diffusion in oocytes nonspecifically centers large objects during prophase I and meiosis I

Abstract

Nucleus centering in mouse oocytes results from a gradient of actin-positive vesicle activity and is essential for developmental success. Here, we analyze 3D model simulations to demonstrate how a gradient in the persistence of actin-positive vesicles can center objects of different sizes. We test model predictions by tracking the transport of exogenous passive tracers. The gradient of activity induces a centering force, akin to an effective pressure gradient, leading to the centering of oil droplets with velocities comparable to nuclear ones. Simulations and experimental measurements show that passive particles subjected to the gradient exhibit biased diffusion toward the center. Strikingly, we observe that the centering mechanism is maintained in meiosis I despite chromosome movement in the opposite direction; thus, it can counteract a process that specifically off-centers the spindle. In conclusion, our findings reconcile how common molecular players can participate in the two opposing functions of chromosome centering versus off-centering.

Calcium-vesicles perform active diffusion in the sea urchin embryo during larval biomineralization

“…Our analyses, in the light of previous studies, point toward cytoskeleton remodeling as an important effector of vesicle motion and deposition. Active diffusion depends on the dynamics of cytoskeleton remodeling and is affected by the strength and activity of the actomyosin network [ 37 – 40 ]. Furthermore, vesicle deposition was shown to be regulated by a network of cytoskeleton remodeling proteins that controls f-actin assembly and myosin contractility [ 64 ].…”

“…This mechanism could, in principle, be used in calcifying cells, to direct the mineral-bearing vesicles into the biomineralizing compartment. Alternatively, the vesicles can perform a diffusive motion that is constrained by the cellular organelles and affected by the dynamic remodeling of the cytoskeleton network within the cell [ 35 – 40 ]. This mode of vesicle diffusion within the cells is called “active diffusion” to distinguish it from thermal diffusion [ 35 – 40 ].…”

“…Alternatively, the vesicles can perform a diffusive motion that is constrained by the cellular organelles and affected by the dynamic remodeling of the cytoskeleton network within the cell [ 35 – 40 ]. This mode of vesicle diffusion within the cells is called “active diffusion” to distinguish it from thermal diffusion [ 35 – 40 ]. Deciphering the mode of motion of the calcium vesicles within the skeletogenic cells and specifically, distinguishing between motor guided motion and diffusion, is essential for understanding the cellular regulation of mineral transport into the biomineralization compartment.…”

Robustness of the microtubule network self-organization in epithelia

“…The correct positioning of intracellular components such as proteins and organelles is critical for correct cellular function ( St Johnston and Ahringer, 2010 ; Ryder and Lerit, 2018 ). These components are transported to their biologically relevant locations by motor proteins moving along the cytoskeleton ( Gagnon and Mowry, 2011 ; Kapitein and Hoogenraad, 2011 ; Franker and Hoogenraad, 2013 ), or through active diffusion often dependent on these motors ( Drechsler et al, 2017 ; Colin et al, 2020 ). Therefore, the direction of cytoskeleton filaments guides the direction and efficiency of intracellular transport.…”

Escape from mitotic catastrophe by actin-dependent nuclear displacement in fission yeast

“…In budding yeast, the nucleus that originally locates within the mother cell translocates toward the bud neck in an actin- and MT-dependent manner, thereby ensuring equal partition of the nuclei to each mother and daughter cell ( Xiang, 2018 ). In early embryos of C. elegans , pushing forces generated by astral MTs play a pivotal role in spindle centering and movement ( Garzon-Coral et al., 2016 ), whereas in mouse oocytes, the actin cytoskeleton, which forms a meshlike network, is required for centering the nucleus/chromosomes ( Colin et al., 2020 ).…”