Mechanically Distinct Microtubule Arrays Determine the Length and Force Response of the Meiotic Spindle

Dev Cell. 2019 Apr 22;49(2):267-278.e5. doi: 10.1016/j.devcel.2019.03.014. Epub 2019 Apr 11.

Abstract

The microtubule-based spindle is subjected to various mechanical forces during cell division. How the structure generates and responds to forces while maintaining overall integrity is unknown because we have a poor understanding of the relationship between filament architecture and mechanics. Here, to fill this gap, we combine microneedle-based quantitative micromanipulation with high-resolution imaging, simultaneously analyzing forces and local filament motility in the Xenopus meiotic spindle. We find that microtubules exhibit a compliant, fluid-like mechanical response at the middle of the spindle half, being distinct from those near the pole and the equator. A force altering spindle length induces filament sliding at this compliant array, where parallel microtubules predominate, without influencing equatorial antiparallel filament dynamics. Molecular perturbations suggest that kinesin-5 and dynein contribute to the spindle's local mechanical difference. Together, our data establish a link between spindle architecture and mechanics and uncover the mechanical design of this essential cytoskeletal assembly.

Keywords: Xenopus; cell division; dynein; kinesin-5; mechanical force; meiosis; microtubules; mitosis; speckle microscopy; spindle assembly.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Biomechanical Phenomena / physiology
  • Cell Division
  • Dyneins / metabolism
  • Female
  • Kinesins / metabolism
  • Male
  • Metaphase / physiology
  • Microtubules / metabolism*
  • Microtubules / physiology
  • Spindle Apparatus / metabolism*
  • Spindle Apparatus / physiology
  • Xenopus Proteins / metabolism
  • Xenopus laevis / metabolism

Substances

  • KIF11 protein, Xenopus
  • Xenopus Proteins
  • Dyneins
  • Kinesins