Midzone bundles of the mammalian anaphase spindle are mechanically coupled both locally and globally

Abstract

Robust chromosome segregation requires the anaphase spindle to both preserve and remodel its structure under force. How it does so remains unclear as probing mechanics during anaphases short lifetime is challenging. Here, we use microneedles to pull on mammalian anaphase midzone bundles and ask how they respond to and transmit force across space and time. We find that midzone bundles locally transmit force to each other in the spindles short axis over multiple timescales. Along the spindles long axis, midzone bundles globally transmit force: rather than bundles sliding apart or detaching under force, the spindle shortens. This reveals strong anchorage and resistance to outward sliding, and that spindle elongation requires all midzone bundles to elongate. This global force transmission is stronger for short-lived forces and is strictly PRC1-dependent, indicating limited mechanistic redundancy. In sum, the anaphase spindle acts as a single mechanical unit over short timescales to resist and transmit force, while remodeling over long timescales to segregate chromosomes. SummaryUsing microneedle manipulation, Mullin-Bernstein et al. show that microtubule bundles of the mammalian anaphase spindle are mechanically coupled, transmitting force both laterally and between spindle poles. These strong connections may help ensure coordinated and error-free chromosome segregation.