The Mitotic Crosslinking Protein PRC1 Acts Like a Mechanical Dashpot to Resist Microtubule Sliding

Cell division in eukaryotes requires the regulated assembly of the spindle apparatus. The proper organization of microtubules within the spindle is driven by motor proteins that exert forces to slide filaments, whereas non-motor proteins crosslink filaments into higher-order motifs, such as overlapping bundles. It is not clear how active and passive forces are integrated to produce regulated mechanical outputs within spindles. Here, we employ simultaneous optical trapping and total internal reflection fluorescence (TIRF) microscopy to directly measure the frictional forces produced by the mitotic crosslinking protein PRC1 that resist microtubule sliding. These forces scale with microtubule sliding velocity and the number of PRC1 crosslinks but do not depend on overlap length or PRC1 density within overlaps. Our results suggest that PRC1 ensembles act similarly to a mechanical dashpot, producing significant resistance against fast motions but minimal resistance against slow motions, allowing for the integration of diverse motor activities into a single mechanical outcome. [Display omitted] •Ensembles of the mitotic crosslinking protein PRC1 generate frictional forces•Resistance to microtubule sliding scales linearly with filament velocity•Frictional forces scale with PRC1 number but not overlap length or PRC1 density•PRC1 acts as a viscous dashpot to regulate microtubule velocities in dividing cells Successful cell division requires the precisely timed positioning of chromosomes. Gaska et al. demonstrate that the essential mitotic crosslinking protein PRC1 generates viscous forces that resist microtubule sliding. PRC1 behaves like a damper that inhibits fast motions while permitting slow motions, thereby regulating microtubule speeds and positions within the spindle.