Dynactin-dependent cortical dynein and spherical spindle shape correlate temporally with meiotic spindle rotation in Caenorhabditis elegans

Mol Biol Cell. 2015 Sep 1;26(17):3030-46. doi: 10.1091/mbc.E15-05-0290. Epub 2015 Jul 1.

Abstract

Oocyte meiotic spindles orient with one pole juxtaposed to the cortex to facilitate extrusion of chromosomes into polar bodies. In Caenorhabditis elegans, these acentriolar spindles initially orient parallel to the cortex and then rotate to the perpendicular orientation. To understand the mechanism of spindle rotation, we characterized events that correlated temporally with rotation, including shortening of the spindle in the pole-to pole axis, which resulted in a nearly spherical spindle at rotation. By analyzing large spindles of polyploid C. elegans and a related nematode species, we found that spindle rotation initiated at a defined spherical shape rather than at a defined spindle length. In addition, dynein accumulated on the cortex just before rotation, and microtubules grew from the spindle with plus ends outward during rotation. Dynactin depletion prevented accumulation of dynein on the cortex and prevented spindle rotation independently of effects on spindle shape. These results support a cortical pulling model in which spindle shape might facilitate rotation because a sphere can rotate without deforming the adjacent elastic cytoplasm. We also present evidence that activation of spindle rotation is promoted by dephosphorylation of the basic domain of p150 dynactin.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Caenorhabditis elegans / cytology
  • Caenorhabditis elegans / metabolism*
  • Cell Shape / physiology
  • Dynactin Complex
  • Dyneins / metabolism*
  • Female
  • Meiosis / physiology
  • Microtubule-Associated Proteins / metabolism*
  • Microtubules / metabolism
  • Oocytes / cytology
  • Oocytes / metabolism*
  • Rotation
  • Spatio-Temporal Analysis
  • Spindle Apparatus / metabolism*
  • Statistics as Topic

Substances

  • Dynactin Complex
  • Microtubule-Associated Proteins
  • Dyneins