Determinants of Polar versus Nematic Organization in Networks of Dynamic Microtubules and Mitotic Motors

During cell division, mitotic motors organize microtubules in the bipolar spindle into either polar arrays at the spindle poles or a “nematic” network of aligned microtubules at the spindle center. The reasons for the distinct self-organizing capacities of dynamic microtubules and different motors are not understood. Using in vitro reconstitution experiments and computer simulations, we show that the human mitotic motors kinesin-5 KIF11 and kinesin-14 HSET, despite opposite directionalities, can both organize dynamic microtubules into either polar or nematic networks. We show that in addition to the motor properties the natural asymmetry between microtubule plus- and minus-end growth critically contributes to the organizational potential of the motors. We identify two control parameters that capture system composition and kinetic properties and predict the outcome of microtubule network organization. These results elucidate a fundamental design principle of spindle bipolarity and establish general rules for active filament network organization. [Display omitted] •Kinesin-5 and kinesin-14 can produce nematic and polar microtubule networks•Self-organizing network architecture depends on both motor and microtubule properties•Two system-level control parameters determine which cytoskeletal network forms•General rules explain the organizational capacities of mitotic motors in the spindle In vitro reconstitutions and computer simulations identify rules that govern microtubule network organization and reveal a design principle underlying bipolar spindle formation.