A stable microtubule bundle formed through an orchestrated multistep process controls quiescence exit

Abstract

Cells fine-tune microtubule assembly in both space and time, to give rise to distinct edifices with specific cellular functions. In proliferating cells, microtubules are highly dynamics, yet, proliferation cessation often lead to their stabilization. One of the most stable microtubule structures identified to date is the nuclear bundle assembled in yeast quiescent cells. In this report, we characterize the original multistep process driving the assembly of this structure in an AuroraB/Ipl1-dependent mechanism. This process follows a precise temporality that relies on the sequential actions of kinesin-14, kinesins-5 and involves both microtubule-kinetochore and kinetochore-kinetochore interactions. Upon quiescence exit, the microtubule bundle disassembles via a cooperative process involving the Kinesin-8 and its full disassembly is required to authorize cells re-entry into proliferation. Overall, our study not only provides the first description, at the molecular scale, of the entire life cycle of a stable microtubule structure in vivo, but also sheds light on its function as a sort of “checkpoint” for cell cycle resumption.