Mechanoreceptor cells develop a specialized cytoskeleton that plays structural and sensory roles at the site of mechanotransduction. However, little is known about how the cytoskeleton is organized and formed. Using electron tomography and live-cell imaging, we resolve the 3D structure and dynamics of the microtubule-based cytoskeleton in fly campaniform mechanosensory cilia. Investigating the formation of the cytoskeleton, we find that katanin p60-like 1 (kat-60L1), a neuronal type of microtubule-severing enzyme, serves two functions. First, it amplifies the mass of microtubules to form the dense microtubule arrays inside the sensory cilia. Second, it generates short microtubules that are required to build the nanoscopic cytoskeleton at the mechanotransduction site. Additional analyses further reveal the functional roles of Patronin and other potential factors in the local regulatory network. In all, our results characterize the specialized cytoskeleton in fly external mechanosensory cilia at near-molecular resolution and provide mechanistic insights into how it is formed.
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4 January 2021
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December 02 2020
Katanin p60-like 1 sculpts the cytoskeleton in mechanosensory cilia
Landi Sun,
1
Tsinghua-Peking Joint Center for Life Science, School of Life Sciences, Tsinghua University, Beijing, China
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Lihong Cui,
1
Tsinghua-Peking Joint Center for Life Science, School of Life Sciences, Tsinghua University, Beijing, China
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Zhen Liu,
1
Tsinghua-Peking Joint Center for Life Science, School of Life Sciences, Tsinghua University, Beijing, China
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Qixuan Wang,
Qixuan Wang
1
Tsinghua-Peking Joint Center for Life Science, School of Life Sciences, Tsinghua University, Beijing, China
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Zhaoyu Xue,
Zhaoyu Xue
1
Tsinghua-Peking Joint Center for Life Science, School of Life Sciences, Tsinghua University, Beijing, China
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Menghua Wu,
Menghua Wu
1
Tsinghua-Peking Joint Center for Life Science, School of Life Sciences, Tsinghua University, Beijing, China
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Tianhui Sun,
Tianhui Sun
1
Tsinghua-Peking Joint Center for Life Science, School of Life Sciences, Tsinghua University, Beijing, China
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Decai Mao,
Decai Mao
2
School of Medicine, Tsinghua University, Beijing, China
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Jianquan Ni,
Jianquan Ni
2
School of Medicine, Tsinghua University, Beijing, China
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José Carlos Pastor-Pareja,
José Carlos Pastor-Pareja
1
Tsinghua-Peking Joint Center for Life Science, School of Life Sciences, Tsinghua University, Beijing, China
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Xin Liang
1
Tsinghua-Peking Joint Center for Life Science, School of Life Sciences, Tsinghua University, Beijing, China
Correspondence to Xin Liang: xinliang@tsinghua.edu.cn
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Landi Sun
1
Tsinghua-Peking Joint Center for Life Science, School of Life Sciences, Tsinghua University, Beijing, China
Lihong Cui
1
Tsinghua-Peking Joint Center for Life Science, School of Life Sciences, Tsinghua University, Beijing, China
Zhen Liu
1
Tsinghua-Peking Joint Center for Life Science, School of Life Sciences, Tsinghua University, Beijing, China
Qixuan Wang
1
Tsinghua-Peking Joint Center for Life Science, School of Life Sciences, Tsinghua University, Beijing, China
Zhaoyu Xue
1
Tsinghua-Peking Joint Center for Life Science, School of Life Sciences, Tsinghua University, Beijing, China
Menghua Wu
1
Tsinghua-Peking Joint Center for Life Science, School of Life Sciences, Tsinghua University, Beijing, China
Tianhui Sun
1
Tsinghua-Peking Joint Center for Life Science, School of Life Sciences, Tsinghua University, Beijing, China
Decai Mao
2
School of Medicine, Tsinghua University, Beijing, China
Jianquan Ni
2
School of Medicine, Tsinghua University, Beijing, China
José Carlos Pastor-Pareja
1
Tsinghua-Peking Joint Center for Life Science, School of Life Sciences, Tsinghua University, Beijing, China
Xin Liang
1
Tsinghua-Peking Joint Center for Life Science, School of Life Sciences, Tsinghua University, Beijing, China
Correspondence to Xin Liang: xinliang@tsinghua.edu.cn
*
L. Sun, L. Cui, and Z. Liu contributed equally to this paper.
Received:
April 21 2020
Revision Received:
September 28 2020
Accepted:
October 20 2020
Online Issn: 1540-8140
Print Issn: 0021-9525
© 2020 Sun et al.
2020
This article is distributed under the terms of an Attribution–Noncommercial–Share Alike–No Mirror Sites license for the first six months after the publication date (see http://www.rupress.org/terms/). After six months it is available under a Creative Commons License (Attribution–Noncommercial–Share Alike 4.0 International license, as described at https://creativecommons.org/licenses/by-nc-sa/4.0/).
J Cell Biol (2021) 220 (1): e202004184.
Article history
Received:
April 21 2020
Revision Received:
September 28 2020
Accepted:
October 20 2020
Citation
Landi Sun, Lihong Cui, Zhen Liu, Qixuan Wang, Zhaoyu Xue, Menghua Wu, Tianhui Sun, Decai Mao, Jianquan Ni, José Carlos Pastor-Pareja, Xin Liang; Katanin p60-like 1 sculpts the cytoskeleton in mechanosensory cilia. J Cell Biol 4 January 2021; 220 (1): e202004184. doi: https://doi.org/10.1083/jcb.202004184
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