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Kinesin-3 and dynein cooperate in long-range retrograde endosome motility along a nonuniform microtubule array

The polarity of microtubules (MTs) determines the motors for intracellular motility, with kinesins moving to plus ends and dynein to minus ends. In elongated cells of Ustilago maydis, dynein is thought to move early endosomes (EEs) toward the septum (retrograde), whereas kinesin-3 transports them to...

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Autores principales: Schuster, Martin, Kilaru, Sreedhar, Fink, Gero, Collemare, Jérôme, Roger, Yvonne, Steinberg, Gero
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The American Society for Cell Biology 2011
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3183019/
https://www.ncbi.nlm.nih.gov/pubmed/21832152
http://dx.doi.org/10.1091/mbc.E11-03-0217
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author Schuster, Martin
Kilaru, Sreedhar
Fink, Gero
Collemare, Jérôme
Roger, Yvonne
Steinberg, Gero
author_facet Schuster, Martin
Kilaru, Sreedhar
Fink, Gero
Collemare, Jérôme
Roger, Yvonne
Steinberg, Gero
author_sort Schuster, Martin
collection PubMed
description The polarity of microtubules (MTs) determines the motors for intracellular motility, with kinesins moving to plus ends and dynein to minus ends. In elongated cells of Ustilago maydis, dynein is thought to move early endosomes (EEs) toward the septum (retrograde), whereas kinesin-3 transports them to the growing cell tip (anterograde). Occasionally, EEs run up to 90 μm in one direction. The underlying MT array consists of unipolar MTs at both cell ends and antipolar bundles in the middle region of the cell. Cytoplasmic MT-organizing centers, labeled with a γ-tubulin ring complex protein, are distributed along the antipolar MTs but are absent from the unipolar regions. Dynein colocalizes with EEs for 10–20 μm after they have left the cell tip. Inactivation of temperature-sensitive dynein abolishes EE motility within the unipolar MT array, whereas long-range motility is not impaired. In contrast, kinesin-3 is continuously present, and its inactivation stops long-range EE motility. This indicates that both motors participate in EE motility, with dynein transporting the organelles through the unipolar MT array near the cell ends, and kinesin-3 taking over at the beginning of the medial antipolar MT array. The cooperation of both motors mediates EE movements over the length of the entire cell.
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spelling pubmed-31830192011-12-16 Kinesin-3 and dynein cooperate in long-range retrograde endosome motility along a nonuniform microtubule array Schuster, Martin Kilaru, Sreedhar Fink, Gero Collemare, Jérôme Roger, Yvonne Steinberg, Gero Mol Biol Cell Articles The polarity of microtubules (MTs) determines the motors for intracellular motility, with kinesins moving to plus ends and dynein to minus ends. In elongated cells of Ustilago maydis, dynein is thought to move early endosomes (EEs) toward the septum (retrograde), whereas kinesin-3 transports them to the growing cell tip (anterograde). Occasionally, EEs run up to 90 μm in one direction. The underlying MT array consists of unipolar MTs at both cell ends and antipolar bundles in the middle region of the cell. Cytoplasmic MT-organizing centers, labeled with a γ-tubulin ring complex protein, are distributed along the antipolar MTs but are absent from the unipolar regions. Dynein colocalizes with EEs for 10–20 μm after they have left the cell tip. Inactivation of temperature-sensitive dynein abolishes EE motility within the unipolar MT array, whereas long-range motility is not impaired. In contrast, kinesin-3 is continuously present, and its inactivation stops long-range EE motility. This indicates that both motors participate in EE motility, with dynein transporting the organelles through the unipolar MT array near the cell ends, and kinesin-3 taking over at the beginning of the medial antipolar MT array. The cooperation of both motors mediates EE movements over the length of the entire cell. The American Society for Cell Biology 2011-10-01 /pmc/articles/PMC3183019/ /pubmed/21832152 http://dx.doi.org/10.1091/mbc.E11-03-0217 Text en © 2011 Schuster et al. This article is distributed by The American Society for Cell Biology under license from the author(s). Two months after publication it is available to the public under an Attribution–Noncommercial–Share Alike 3.0 Unported Creative Commons License (http://creativecommons.org/licenses/by-nc-sa/3.0). “ASCB®,” “The American Society for Cell Biology®,” and “Molecular Biology of the Cell®” are registered trademarks of The American Society of Cell Biology.
spellingShingle Articles
Schuster, Martin
Kilaru, Sreedhar
Fink, Gero
Collemare, Jérôme
Roger, Yvonne
Steinberg, Gero
Kinesin-3 and dynein cooperate in long-range retrograde endosome motility along a nonuniform microtubule array
title Kinesin-3 and dynein cooperate in long-range retrograde endosome motility along a nonuniform microtubule array
title_full Kinesin-3 and dynein cooperate in long-range retrograde endosome motility along a nonuniform microtubule array
title_fullStr Kinesin-3 and dynein cooperate in long-range retrograde endosome motility along a nonuniform microtubule array
title_full_unstemmed Kinesin-3 and dynein cooperate in long-range retrograde endosome motility along a nonuniform microtubule array
title_short Kinesin-3 and dynein cooperate in long-range retrograde endosome motility along a nonuniform microtubule array
title_sort kinesin-3 and dynein cooperate in long-range retrograde endosome motility along a nonuniform microtubule array
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3183019/
https://www.ncbi.nlm.nih.gov/pubmed/21832152
http://dx.doi.org/10.1091/mbc.E11-03-0217
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