Spatial coin-tossing by kinesin-1 head and tail binding collectively drives microtubule patterns

Abstract

Intracellular microtubule-based transport depends on an essential plus-ended molecular motor, kinesin-1. The N-terminal ATP-dependent head driving motility and a C-terminal cargo interacting tail, both bind microtubules. Previously, the interplay of both domains were hypothesized to play a role in collective microtubule sliding patterns, but the mechanisms remained unclear. Here, we show that full-length Drosophila kinesin-1 results in spontaneous spatiotemporal patterns in gliding assays including bending, looping, and oscillations as well as stop-and-go motion of microtubules. We demonstrate that presence of the motor domain alone cannot produce these patterns. The tail itself can bind microtubules passively, acting as a static “anchor.” An equimolar mixture of these two domain constructs reproduces the spatiotemporal patterns both in terms of increased bending with length and velocity distributions. Based on a simple “coin-toss” model, where either the head or tail bind microtubules with equal probability, we test the effect of increasing proportions of motor and tail and find antagonistic interactions drive velocity distributions with coexistence of bimodal distributions when the two tendencies are balanced. This mechanical effect of the kinesin head-tail competition suggests it could explain the emergence of self-organized patterns inside cells, beyond regulation or cargo binding alone.