An F-actin shell ruptures the nuclear envelope by sorting pore-dense and pore-free membranes in meiosis of starfish oocytes

In metazoa, the nuclear envelope (NE), composed of nuclear membranes, pores (NPCs) and the underlying network of lamin filaments, disassembles and reassembles in every division. A phase of sudden rupture is a conserved feature of NE breakdown (NEBD), a key cell-cycle event essential for timely spindle assembly and faithful chromosome segregation. This rupture involves mechanical forces generated by microtubules in somatic cells, and by the actin cytoskeleton in starfish oocytes. How cytoskeletal forces disrupt the NE remained unknown. Here, by live-cell and super-resolution light microscopy we show that at NEBD a transient cortex-like F-actin structure assembles within the lamina. This F-actin shell sprouts filopodia-like protrusions forcing apart the lamina and nuclear membranes. By correlated light and electron microscopy, we visualize that these F-actin spikes protrude pore-free nuclear membranes, while adjoining stretches accumulate packed NPCs. These NPC conglomerates sort into distinct membrane tubules and vesicles, while breaks appear in pore-free regions. We propose that the F-actin shell destabilizes the NE by forcing apart the lamina and nuclear membranes, providing the first mechanistic explanation for the sudden collapse of the NE during its breakdown.