Kinesin-1 and cytoplasmic dynein act sequentially to move the meiotic spindle to the oocyte cortex in Caenorhabditis elegans

Mol Biol Cell. 2009 Jun;20(11):2722-30. doi: 10.1091/mbc.e08-12-1253. Epub 2009 Apr 8.

Abstract

During female meiosis in animals, the meiotic spindle is attached to the egg cortex by one pole during anaphase to allow selective disposal of half the chromosomes in a polar body. In Caenorhabditis elegans, this anaphase spindle position is achieved sequentially through kinesin-1-dependent early translocation followed by anaphase-promoting complex (APC)-dependent spindle rotation. Partial depletion of cytoplasmic dynein heavy chain by RNA interference blocked spindle rotation without affecting early translocation. Dynein depletion also blocked the APC-dependent late translocation that occurs in kinesin-1-depleted embryos. Time-lapse imaging of green fluorescent protein-tagged dynein heavy chain as well as immunofluorescence with dynein-specific antibodies revealed that dynein starts to accumulate at spindle poles just before the initiation of rotation or late translocation. Accumulation of dynein at poles was kinesin-1 independent and APC dependent, just like dynein driven spindle movements. This represents a case of kinesin-1/dynein coordination in which these two motors of opposite polarity act sequentially and independently on a cargo to move it in the same direction.

Publication types

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

MeSH terms

  • Anaphase-Promoting Complex-Cyclosome
  • Animals
  • Caenorhabditis elegans / embryology
  • Caenorhabditis elegans / genetics
  • Caenorhabditis elegans / metabolism*
  • Caenorhabditis elegans Proteins / genetics
  • Caenorhabditis elegans Proteins / metabolism*
  • Cell Cycle Proteins / genetics
  • Cell Cycle Proteins / metabolism
  • Cytoplasm / metabolism
  • Cytoplasmic Dyneins
  • Dyneins / genetics
  • Dyneins / metabolism*
  • Embryo, Nonmammalian / metabolism
  • Female
  • Fluorescent Antibody Technique
  • Green Fluorescent Proteins / genetics
  • Green Fluorescent Proteins / metabolism
  • Immunohistochemistry
  • Kinesins / genetics
  • Kinesins / metabolism*
  • Meiosis / genetics
  • Microscopy, Fluorescence
  • Microtubules / metabolism
  • Models, Biological
  • Mutation
  • Oocytes / cytology
  • Oocytes / metabolism*
  • RNA Interference
  • Recombinant Fusion Proteins / genetics
  • Recombinant Fusion Proteins / metabolism
  • Spindle Apparatus / metabolism*
  • Tubulin / genetics
  • Tubulin / metabolism
  • Ubiquitin-Protein Ligase Complexes / genetics
  • Ubiquitin-Protein Ligase Complexes / metabolism

Substances

  • Caenorhabditis elegans Proteins
  • Cell Cycle Proteins
  • Recombinant Fusion Proteins
  • Tubulin
  • UNC-116 protein, C elegans
  • Green Fluorescent Proteins
  • Ubiquitin-Protein Ligase Complexes
  • Anaphase-Promoting Complex-Cyclosome
  • Cytoplasmic Dyneins
  • DHC-1 protein, C elegans
  • Dyneins
  • Kinesins