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Microtubule stabilizer reveals requirement of Ca(2+)-dependent conformational changes of microtubules for rapid coiling of haptonema in haptophyte algae

A haptonema is an elongated microtubule-based motile organelle uniquely present in haptophytes. The most notable and rapid movement of a haptonema is ‘coiling’, which occurs within a few milliseconds following mechanical stimulation in an unknown motor-independent mechanism. Here, we analyzed the co...

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Autores principales: Nomura, Mami, Atsuji, Kohei, Hirose, Keiko, Shiba, Kogiku, Yanase, Ryuji, Nakayama, Takeshi, Ishida, Ken-ichiro, Inaba, Kazuo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Company of Biologists Ltd 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6398456/
https://www.ncbi.nlm.nih.gov/pubmed/30700402
http://dx.doi.org/10.1242/bio.036590
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author Nomura, Mami
Atsuji, Kohei
Hirose, Keiko
Shiba, Kogiku
Yanase, Ryuji
Nakayama, Takeshi
Ishida, Ken-ichiro
Inaba, Kazuo
author_facet Nomura, Mami
Atsuji, Kohei
Hirose, Keiko
Shiba, Kogiku
Yanase, Ryuji
Nakayama, Takeshi
Ishida, Ken-ichiro
Inaba, Kazuo
author_sort Nomura, Mami
collection PubMed
description A haptonema is an elongated microtubule-based motile organelle uniquely present in haptophytes. The most notable and rapid movement of a haptonema is ‘coiling’, which occurs within a few milliseconds following mechanical stimulation in an unknown motor-independent mechanism. Here, we analyzed the coiling process in detail by high-speed filming and showed that haptonema coiling was initiated by left-handed twisting of the haptonema, followed by writhing to form a helix from the distal tip. On recovery from a mechanical stimulus, the helix slowly uncoiled from the proximal region. Electron microscopy showed that the seven microtubules in a haptonema were arranged mostly in parallel but that one of the microtubules often wound around the others in the extended state. A microtubule stabilizer, paclitaxel, inhibited coiling and induced right-handed twisting of the haptonema in the absence of Ca(2+), suggesting changes in the mechanical properties of microtubules. Addition of Ca(2+) resulted in the conversion of haptonematal twist into the planar bends near the proximal region. These results indicate that switching microtubule conformation, possibly with the aid of Ca(2+)-binding microtubule-associated proteins is responsible for rapid haptonematal coiling.
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spelling pubmed-63984562019-03-05 Microtubule stabilizer reveals requirement of Ca(2+)-dependent conformational changes of microtubules for rapid coiling of haptonema in haptophyte algae Nomura, Mami Atsuji, Kohei Hirose, Keiko Shiba, Kogiku Yanase, Ryuji Nakayama, Takeshi Ishida, Ken-ichiro Inaba, Kazuo Biol Open Research Article A haptonema is an elongated microtubule-based motile organelle uniquely present in haptophytes. The most notable and rapid movement of a haptonema is ‘coiling’, which occurs within a few milliseconds following mechanical stimulation in an unknown motor-independent mechanism. Here, we analyzed the coiling process in detail by high-speed filming and showed that haptonema coiling was initiated by left-handed twisting of the haptonema, followed by writhing to form a helix from the distal tip. On recovery from a mechanical stimulus, the helix slowly uncoiled from the proximal region. Electron microscopy showed that the seven microtubules in a haptonema were arranged mostly in parallel but that one of the microtubules often wound around the others in the extended state. A microtubule stabilizer, paclitaxel, inhibited coiling and induced right-handed twisting of the haptonema in the absence of Ca(2+), suggesting changes in the mechanical properties of microtubules. Addition of Ca(2+) resulted in the conversion of haptonematal twist into the planar bends near the proximal region. These results indicate that switching microtubule conformation, possibly with the aid of Ca(2+)-binding microtubule-associated proteins is responsible for rapid haptonematal coiling. The Company of Biologists Ltd 2019-01-30 /pmc/articles/PMC6398456/ /pubmed/30700402 http://dx.doi.org/10.1242/bio.036590 Text en © 2019. Published by The Company of Biologists Ltd http://creativecommons.org/licenses/by/4.0This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Article
Nomura, Mami
Atsuji, Kohei
Hirose, Keiko
Shiba, Kogiku
Yanase, Ryuji
Nakayama, Takeshi
Ishida, Ken-ichiro
Inaba, Kazuo
Microtubule stabilizer reveals requirement of Ca(2+)-dependent conformational changes of microtubules for rapid coiling of haptonema in haptophyte algae
title Microtubule stabilizer reveals requirement of Ca(2+)-dependent conformational changes of microtubules for rapid coiling of haptonema in haptophyte algae
title_full Microtubule stabilizer reveals requirement of Ca(2+)-dependent conformational changes of microtubules for rapid coiling of haptonema in haptophyte algae
title_fullStr Microtubule stabilizer reveals requirement of Ca(2+)-dependent conformational changes of microtubules for rapid coiling of haptonema in haptophyte algae
title_full_unstemmed Microtubule stabilizer reveals requirement of Ca(2+)-dependent conformational changes of microtubules for rapid coiling of haptonema in haptophyte algae
title_short Microtubule stabilizer reveals requirement of Ca(2+)-dependent conformational changes of microtubules for rapid coiling of haptonema in haptophyte algae
title_sort microtubule stabilizer reveals requirement of ca(2+)-dependent conformational changes of microtubules for rapid coiling of haptonema in haptophyte algae
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6398456/
https://www.ncbi.nlm.nih.gov/pubmed/30700402
http://dx.doi.org/10.1242/bio.036590
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