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Oscillatory movement of a dynein-microtubule complex crosslinked with DNA origami

Bending of cilia and flagella occurs when axonemal dynein molecules on one side of the axoneme produce force and move toward the microtubule (MT) minus end. These dyneins are then pulled back when the axoneme bends in the other direction, meaning oscillatory back and forth movement of dynein during...

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Autores principales: Abdellatef, Shimaa A, Tadakuma, Hisashi, Yan, Kangmin, Fujiwara, Takashi, Fukumoto, Kodai, Kondo, Yuichi, Takazaki, Hiroko, Boudria, Rofia, Yasunaga, Takuo, Higuchi, Hideo, Hirose, Keiko
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9232216/
https://www.ncbi.nlm.nih.gov/pubmed/35749159
http://dx.doi.org/10.7554/eLife.76357
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author Abdellatef, Shimaa A
Tadakuma, Hisashi
Yan, Kangmin
Fujiwara, Takashi
Fukumoto, Kodai
Kondo, Yuichi
Takazaki, Hiroko
Boudria, Rofia
Yasunaga, Takuo
Higuchi, Hideo
Hirose, Keiko
author_facet Abdellatef, Shimaa A
Tadakuma, Hisashi
Yan, Kangmin
Fujiwara, Takashi
Fukumoto, Kodai
Kondo, Yuichi
Takazaki, Hiroko
Boudria, Rofia
Yasunaga, Takuo
Higuchi, Hideo
Hirose, Keiko
author_sort Abdellatef, Shimaa A
collection PubMed
description Bending of cilia and flagella occurs when axonemal dynein molecules on one side of the axoneme produce force and move toward the microtubule (MT) minus end. These dyneins are then pulled back when the axoneme bends in the other direction, meaning oscillatory back and forth movement of dynein during repetitive bending of cilia/flagella. There are various factors that may regulate the dynein activity, e.g. the nexin-dynein regulatory complex, radial spokes, and central apparatus. In order to understand the basic mechanism of dynein’s oscillatory movement, we constructed a simple model system composed of MTs, outer-arm dyneins, and crosslinks between the MTs made of DNA origami. Electron microscopy (EM) showed pairs of parallel MTs crossbridged by patches of regularly arranged dynein molecules bound in two different orientations, depending on which of the MTs their tails bind to. The oppositely oriented dyneins are expected to produce opposing forces when the pair of MTs have the same polarity. Optical trapping experiments showed that the dynein-MT-DNA-origami complex actually oscillates back and forth after photolysis of caged ATP. Intriguingly, the complex, when held at one end, showed repetitive bending motions. The results show that a simple system composed of ensembles of oppositely oriented dyneins, MTs, and inter-MT crosslinkers, without any additional regulatory structures, has an intrinsic ability to cause oscillation and repetitive bending motions.
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spelling pubmed-92322162022-06-25 Oscillatory movement of a dynein-microtubule complex crosslinked with DNA origami Abdellatef, Shimaa A Tadakuma, Hisashi Yan, Kangmin Fujiwara, Takashi Fukumoto, Kodai Kondo, Yuichi Takazaki, Hiroko Boudria, Rofia Yasunaga, Takuo Higuchi, Hideo Hirose, Keiko eLife Cell Biology Bending of cilia and flagella occurs when axonemal dynein molecules on one side of the axoneme produce force and move toward the microtubule (MT) minus end. These dyneins are then pulled back when the axoneme bends in the other direction, meaning oscillatory back and forth movement of dynein during repetitive bending of cilia/flagella. There are various factors that may regulate the dynein activity, e.g. the nexin-dynein regulatory complex, radial spokes, and central apparatus. In order to understand the basic mechanism of dynein’s oscillatory movement, we constructed a simple model system composed of MTs, outer-arm dyneins, and crosslinks between the MTs made of DNA origami. Electron microscopy (EM) showed pairs of parallel MTs crossbridged by patches of regularly arranged dynein molecules bound in two different orientations, depending on which of the MTs their tails bind to. The oppositely oriented dyneins are expected to produce opposing forces when the pair of MTs have the same polarity. Optical trapping experiments showed that the dynein-MT-DNA-origami complex actually oscillates back and forth after photolysis of caged ATP. Intriguingly, the complex, when held at one end, showed repetitive bending motions. The results show that a simple system composed of ensembles of oppositely oriented dyneins, MTs, and inter-MT crosslinkers, without any additional regulatory structures, has an intrinsic ability to cause oscillation and repetitive bending motions. eLife Sciences Publications, Ltd 2022-06-24 /pmc/articles/PMC9232216/ /pubmed/35749159 http://dx.doi.org/10.7554/eLife.76357 Text en © 2022, Abdellatef et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Cell Biology
Abdellatef, Shimaa A
Tadakuma, Hisashi
Yan, Kangmin
Fujiwara, Takashi
Fukumoto, Kodai
Kondo, Yuichi
Takazaki, Hiroko
Boudria, Rofia
Yasunaga, Takuo
Higuchi, Hideo
Hirose, Keiko
Oscillatory movement of a dynein-microtubule complex crosslinked with DNA origami
title Oscillatory movement of a dynein-microtubule complex crosslinked with DNA origami
title_full Oscillatory movement of a dynein-microtubule complex crosslinked with DNA origami
title_fullStr Oscillatory movement of a dynein-microtubule complex crosslinked with DNA origami
title_full_unstemmed Oscillatory movement of a dynein-microtubule complex crosslinked with DNA origami
title_short Oscillatory movement of a dynein-microtubule complex crosslinked with DNA origami
title_sort oscillatory movement of a dynein-microtubule complex crosslinked with dna origami
topic Cell Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9232216/
https://www.ncbi.nlm.nih.gov/pubmed/35749159
http://dx.doi.org/10.7554/eLife.76357
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