TY - JOUR
T1 - A novel mechanism of bulk cytoplasmic transport by cortical dynein in Drosophila ovary
AU - Lu, Wen
AU - Lakonishok, Margot
AU - Serpinskaya, Anna S.
AU - Gelfand, Vladimir I.
N1 - Funding Information:
We thank many colleagues who generously contributed reagents for this work: Dr. Thomas Hays (University of Minnesota); Dr. Graydon Gonsalvez (Augusta University); Dr. Uri Abdu (Ben-Gurion University of the Negev, Israel); Dr. David Glover (Caltech); Dr. Gohta Goshima (Nagoya University, Japan); Dr. Klaus Hahn (University of North Carolina Chapel Hill); Dr. Andrew Carter (MRC Laboratory of Molecular Biology, Cambridge); Dr. Edwin Ferguson (the University of Chicago); Dr. Yu-Chiun Wang (RIKEN Center for Biosystems Dynamics Research, Japan); Bloomington Drosophila Stock Center (supported by National Institutes of Health grant P40OD018537) and Drosophila Genomics Resource Center (supported by NIH grant 2P40OD010949). The anti-Orb 4H8 monoclonal antibody developed by Dr. Paul D Schedl’s group at Princeton University, anti-DHC 2C11-2 antibody developed by Dr. Jonathan M Scholey’s group at University of California, Davis, and anti-BicD 4C2 antibody developed by Dr. Ruth Steward group at Waksman Institute Rutgers University, were obtained from the Developmental Studies Hybridoma Bank, created by the NICHD of the NIH and maintained at The University of Iowa, Department of Biology, Iowa City, IA 52242. We also thank all the Gelfand laboratory members for support, discussions, and suggestions. Research reported in this study was supported by the National Institute of General Medical Sciences grant R35GM131752 to VI Gelfand.
Funding Information:
We thank many colleagues who generously contributed reagents for this work: Dr. Thomas Hays (University of Minnesota); Dr. Graydon Gonsalvez (Augusta University); Dr. Uri Abdu (Ben-Gurion University of the Negev, Israel); Dr. David Glover (Caltech); Dr. Gohta Goshima (Nagoya University, Japan); Dr. Klaus Hahn (University of North Carolina Chapel Hill); Dr. Andrew Carter (MRC Laboratory of Molecular Biology, Cambridge); Dr. Edwin Ferguson (the University of Chicago); Dr. Yu-Chiun Wang (RIKEN Center for Biosystems Dynamics Research, Japan); Bloomington Drosophila Stock Center (supported by National Institutes of Health grant P40OD018537) and Drosophila Genomics Resource Center (supported by NIH grant 2P40OD010949). The anti-Orb 4H8 monoclonal antibody developed by Dr. Paul D Schedl?s group at Princeton University, anti-DHC 2C11-2 antibody developed by Dr. Jonathan M Scholey?s group at University of California, Davis, and anti-BicD 4C2 antibody developed by Dr. Ruth Steward group at Waksman Institute Rutgers University, were obtained from the Developmental Studies Hybridoma Bank, created by the NICHD of the NIH and maintained at The University of Iowa, Department of Biology, Iowa City, IA 52242. We also thank all the Gelfand laboratory members for support, discussions, and suggestions. Research reported in this study was supported by the National Institute of General Medical Sciences grant R35GM131752 to VI Gelfand.
Publisher Copyright:
© Lu et al.
PY - 2022/2
Y1 - 2022/2
N2 - Cytoplasmic dynein, a major minus-end directed microtubule motor, plays essential roles in eukaryotic cells. Drosophila oocyte growth is mainly dependent on the contribution of cytoplasmic contents from the interconnected sister cells, nurse cells. We have previously shown that cytoplasmic dynein is required for Drosophila oocyte growth and assumed that it simply trans-ports cargoes along microtubule tracks from nurse cells to the oocyte. Here, we report that instead of transporting individual cargoes along stationary microtubules into the oocyte, cortical dynein actively moves microtubules within nurse cells and from nurse cells to the oocyte via the cyto-plasmic bridges, the ring canals. This robust microtubule movement is sufficient to drag even inert cytoplasmic particles through the ring canals to the oocyte. Furthermore, replacing dynein with a minus-end directed plant kinesin linked to the actin cortex is sufficient for transporting organelles and cytoplasm to the oocyte and driving its growth. These experiments show that cortical dynein performs bulk cytoplasmic transport by gliding microtubules along the cell cortex and through the ring canals to the oocyte. We propose that the dynein-driven microtubule flow could serve as a novel mode of fast cytoplasmic transport.
AB - Cytoplasmic dynein, a major minus-end directed microtubule motor, plays essential roles in eukaryotic cells. Drosophila oocyte growth is mainly dependent on the contribution of cytoplasmic contents from the interconnected sister cells, nurse cells. We have previously shown that cytoplasmic dynein is required for Drosophila oocyte growth and assumed that it simply trans-ports cargoes along microtubule tracks from nurse cells to the oocyte. Here, we report that instead of transporting individual cargoes along stationary microtubules into the oocyte, cortical dynein actively moves microtubules within nurse cells and from nurse cells to the oocyte via the cyto-plasmic bridges, the ring canals. This robust microtubule movement is sufficient to drag even inert cytoplasmic particles through the ring canals to the oocyte. Furthermore, replacing dynein with a minus-end directed plant kinesin linked to the actin cortex is sufficient for transporting organelles and cytoplasm to the oocyte and driving its growth. These experiments show that cortical dynein performs bulk cytoplasmic transport by gliding microtubules along the cell cortex and through the ring canals to the oocyte. We propose that the dynein-driven microtubule flow could serve as a novel mode of fast cytoplasmic transport.
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U2 - 10.7554/ELIFE.75538
DO - 10.7554/ELIFE.75538
M3 - Article
C2 - 35170428
AN - SCOPUS:85125599607
SN - 2050-084X
VL - 11
JO - eLife
JF - eLife
M1 - e75538
ER -