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Microtubule-microtubule sliding by kinesin-1 is essential for normal cytoplasmic streaming in Drosophila oocytes.

Proc Natl Acad Sci U S A. 2016 Aug 23;113(34):E4995-5004. Epub 2016 Aug 10
Wen Lu 1 , Michael Winding 1 , Margot Lakonishok 1 , Jill Wildonger 2 , Vladimir I Gelfand 3
Wen Lu 1 , Michael Winding 1 , Margot Lakonishok 1 , Jill Wildonger 2 , Vladimir I Gelfand 3

[No authors listed]

Author information
  • 1 Department of Cell and Molecular Biology, Feinberg School of Medicine, Northwestern University, Chicago, IL 60611;
  • 2 Department of Biochemistry, University of Wisconsin-Madison, Madison, WI 53706.
  • 3 Department of Cell and Molecular Biology, Feinberg School of Medicine, Northwestern University, Chicago, IL 60611; vgelfand@northwestern.edu.

摘要


Cytoplasmic streaming in Drosophila oocytes is a microtubule-based bulk cytoplasmic movement. Streaming efficiently circulates and localizes mRNAs and proteins deposited by the nurse cells across the oocyte. This movement is driven by kinesin-1, a major microtubule motor. Recently, we have shown that kinesin-1 heavy chain (KHC) can transport one microtubule on another microtubule, thus driving microtubule-microtubule sliding in multiple cell types. To study the role of microtubule sliding in oocyte cytoplasmic streaming, we used a Khc mutant that is deficient in microtubule sliding but able to transport a majority of cargoes. We demonstrated that streaming is reduced by genomic replacement of wild-type Khc with this sliding-deficient mutant. Streaming can be fully rescued by wild-type KHC and partially rescued by a chimeric motor that cannot move organelles but is active in microtubule sliding. Consistent with these data, we identified two populations of microtubules in fast-streaming oocytes: a network of stable microtubules anchored to the actin cortex and free cytoplasmic microtubules that moved in the ooplasm. We further demonstrated that the reduced streaming in sliding-deficient oocytes resulted in posterior determination defects. Together, we propose that kinesin-1 slides free cytoplasmic microtubules against cortically immobilized microtubules, generating forces that contribute to cytoplasmic streaming and are essential for the refinement of posterior determinants.

KEYWORDS: Drosophila, axis determination, cytoplasmic streaming, kinesin-1, microtubules