The Fission Yeast TACC Protein Mia1p Stabilizes Microtubule Arrays by Length-Independent Crosslinking

Microtubule (MT) arrays are mechanistic effectors of polarity specification and cell division. Linear bundles in which MTs are bridged laterally [1, 2] are dynamically assembled in systems ranging from differentiated metazoan cells to fungi in a process that remains poorly understood. Often, bundled MTs slide with respect to each other via molecular motors [3, 4]. In interphase cells of the fission yeast Schizosaccharomyces pombe, MT nucleation frequently occurs at preexisting arrays [5,6]. As the nascent MT lengthens, stable antiparallel MT overlaps are thought to form through competition between motion of the minus-end-directed kinesin K1p2p [4] and braking force exerted by the accumulating lateral crosslinker Ase1p [7-9]. Here we show that Mia1p/A1p7p, a transforming acidic coiled-coil (TACC) protein [10, 11], functions as a length-independent MT crosslinker. In cells lacking Mia1p MT-bundling activity, linear arrays frequently disassemble, accompanied by a marked increase in Ase1p off rate and erratic motion of sliding MTs. We propose that the combined action of lateral length-dependent (Ase1p) and terminal length-independent (Mia1p) crosslinkers is crucial for robust assembly and stability of linear MT arrays. Such use of qualitatively distinct crosslinking mechanisms in tandem may point to a general design principle in the engineering of stable cytoskeletal assemblies.