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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...
Autores principales: | , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
The Company of Biologists Ltd
2019
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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. |
format | Online Article Text |
id | pubmed-6398456 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2019 |
publisher | The Company of Biologists Ltd |
record_format | MEDLINE/PubMed |
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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