Contractile acto-myosin network on nuclear envelope remnants positions human chromosomes for mitosis

To ensure proper segregation during mitosis, chromosomes must be efficiently captured by spindle microtubules and subsequently aligned on the mitotic spindle. The efficacy of chromosome capture by the mitotic spindle can be influenced by how widely chromosomes are scattered in space. However it is unknown whether chromosome scattering is regulated, prior to the interactions with spindle microtubules, in early mitosis. Here, we quantify chromosome-scattering volume (CSV) and find that it is reduced immediately after nuclear envelope breakdown (NEBD) in human cells. The reduction of CSV occurs independently of microtubules and is therefore not an outcome of interactions between chromosomes and the spindle. We find that, prior to NEBD, an acto-myosin network is assembled in a LINC complex-dependent manner on the cytoplasmic surface of the nuclear envelope. This acto-myosin network remains on the nuclear envelope remnant soon after NEBD, and its myosin-II-mediated contraction reduces CSV and facilitates chromosome interactions with spindle microtubules. Thus we find a novel mechanism that positions chromosomes in early mitosis to ensure efficient chromosome–spindle interactions.