Pivot-and-bond model explains microtubule bundle formation.

Marcel Prelogović,Ana Milas,Nenad Pavin,Lora Winters,Iva M Tolić

doi:10.1103/physreve.100.012403

Abstract

During mitosis, microtubules form a spindle, which is responsible for proper segregation of the genetic material. A common structural element in a mitotic spindle is a parallel bundle, consisting of two or more microtubules growing from the same origin and held together by cross-linking proteins. An interesting question is what are the physical principles underlying the formation and stability of such microtubule bundles. Here we show, by introducing the pivot-and-bond model, that random angular movement of microtubules around the spindle pole and forces exerted by cross-linking proteins can explain the formation of microtubule bundles as observed in our experiments. The model predicts that stable parallel bundles can form in the presence of either passive crosslinkers or plus-end directed motors, but not minus-end directed motors. In the cases where bundles form, the time needed for their formation depends mainly on the concentration of cross-linking proteins and the angular diffusion of the microtubule. In conclusion, the angular motion drives the alignment of microtubules, which in turn allows the cross-linking proteins to connect the microtubules into a stable bundle.

Highlights

During mitosis the cell forms a spindle, a complex selforganized molecular machine composed of bundles of microtubules (MTs), which segregates the chromosomes into two daughter cells [1]
Some MTs growing from one spindle pole come into contact with an MT growing from the same spindle pole, thereby forming a parallel bundle (Fig. 1(a), Supplemental Material Movie 1 [38])
MTs can form antiparallel bundles, which was studied in our recent work [26], and MTs growing at an angle with respect to this antiparallel bundle can eventually join it in a manner similar to the parallel bundle formation (Fig. 1(c), Supplemental Material Movie 2 [38])

Summary

Introduction

During mitosis the cell forms a spindle, a complex selforganized molecular machine composed of bundles of microtubules (MTs), which segregates the chromosomes into two daughter cells [1]. MTs are thin stiff filaments that typically extend in random directions from two spindle poles [2]. Stability of MT bundles is ensured by cross-linking proteins, which bind along the MT lattice, connecting neighboring MTs. Cross-linking occurs only if the distance between the MTs is comparable with the size of a cross-linking protein. Cross-linking occurs only if the distance between the MTs is comparable with the size of a cross-linking protein These proteins can be divided into two classes: (i) proteins that cross-link MTs without directed movement along the MT, such as Ase1/PRC1 [6]; (ii) motor proteins that walk along the MT either toward the plus end of the MT, such as Cut7/Eg5 [7,8], or toward the minus end, such as Ncd [9,10]

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Conclusion