A force-sensitive mutation reveals a non-canonical role for dynein in anaphase progression

J Cell Biol. 2024 Oct 7;223(10):e202310022. doi: 10.1083/jcb.202310022. Epub 2024 Jul 1.

Abstract

The diverse roles of the dynein motor in shaping microtubule networks and cargo transport complicate in vivo analysis of its functions significantly. To address this issue, we have generated a series of missense mutations in Drosophila Dynein heavy chain. We show that mutations associated with human neurological disease cause a range of defects, including impaired cargo trafficking in neurons. We also describe a novel microtubule-binding domain mutation that specifically blocks the metaphase-anaphase transition during mitosis in the embryo. This effect is independent from dynein's canonical role in silencing the spindle assembly checkpoint. Optical trapping of purified dynein complexes reveals that this mutation only compromises motor performance under load, a finding rationalized by the results of all-atom molecular dynamics simulations. We propose that dynein has a novel function in anaphase progression that depends on it operating in a specific load regime. More broadly, our work illustrates how in vivo functions of motors can be dissected by manipulating their mechanical properties.

MeSH terms

  • Anaphase*
  • Animals
  • Drosophila Proteins* / genetics
  • Drosophila Proteins* / metabolism
  • Drosophila melanogaster* / genetics
  • Drosophila melanogaster* / metabolism
  • Dyneins* / genetics
  • Dyneins* / metabolism
  • Humans
  • Microtubules* / genetics
  • Microtubules* / metabolism
  • Molecular Dynamics Simulation
  • Mutation / genetics
  • Mutation, Missense
  • Spindle Apparatus / genetics
  • Spindle Apparatus / metabolism

Substances

  • Dyneins
  • Drosophila Proteins