title: Microtubule-microtubule sliding by kinesin-1 is essential for normal cytoplasmic streaming in Drosophila oocytes.
abstract: 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.
authors: Department of Cell and Molecular Biology, Feinberg School of Medicine, Northwestern University, Chicago, IL 60611;
authors: Wen
authors: W
authors: Lu
authors: Department of Cell and Molecular Biology, Feinberg School of Medicine, Northwestern University, Chicago, IL 60611;
authors: Michael
authors: M
authors: Winding
authors: Department of Cell and Molecular Biology, Feinberg School of Medicine, Northwestern University, Chicago, IL 60611;
authors: Margot
authors: M
authors: Lakonishok
authors: Department of Biochemistry, University of Wisconsin-Madison, Madison, WI 53706.
authors: Jill
authors: J
authors: Wildonger
authors: Department of Cell and Molecular Biology, Feinberg School of Medicine, Northwestern University, Chicago, IL 60611; vgelfand@northwestern.edu.
authors: Vladimir I
authors: 0000-0002-6361-2798
authors: VI
authors: Gelfand
mesh_terms: D000595:Amino Acid Sequence; D000818:Animals; D001370:Axonal Transport / Q000235:genetics; D001665:Binding Sites; D001696:Biomechanical Phenomena; D016764:Cell Polarity; D003595:Cytoplasmic Streaming / Q000235:genetics*; D029721:Drosophila Proteins / Q000235:genetics* / Q000378:metabolism; D004331:Drosophila melanogaster / Q000235:genetics* / Q000254:growth & development / Q000378:metabolism; D005260:Female; D018507:Gene Expression Regulation, Developmental; D005816:Genetic Complementation Test; D016547:Kinesins / Q000235:genetics* / Q000378:metabolism; D008870:Microtubules / Q000378:metabolism* / Q000648:ultrastructure; D009154:Mutation; D009865:Oocytes / Q000378:metabolism* / Q000648:ultrastructure; D011485:Protein Binding; D000072417:Protein Domains; D016415:Sequence Alignment; D017386:Sequence Homology, Amino Acid
chemical_list: D029721:Drosophila Proteins; C515209:Khc protein, Drosophila; D016547:Kinesins
keywords: Drosophila; axis determination; cytoplasmic streaming; kinesin-1; microtubules