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Super-resolution microscopy and FIB-SEM imaging reveal parental centriole-derived, hybrid cilium in mammalian multiciliated cells

Super-resolution microscopy and FIB-SEM imaging reveal parental centriole-derived, hybrid cilium in mammalian multiciliated cells
Super-resolution microscopy and FIB-SEM imaging reveal parental centriole-derived, hybrid cilium in mammalian multiciliated cells

Motile cilia are cellular beating machines that play a critical role in mucociliary clearance, cerebrospinal fluid movement, and fertility. In the airways, hundreds of motile cilia present on the surface of a multiciliated epithelia cell beat coordinately to protect the epithelium from bacteria, viruses, and harmful particulates. During multiciliated cell differentiation, motile cilia are templated from basal bodies, each extending a basal foot-an appendage linking motile cilia together to ensure coordinated beating. Here, we demonstrate that among the many motile cilia of a multiciliated cell, a hybrid cilium with structural features of both primary and motile cilia is harbored. The hybrid cilium is conserved in mammalian multiciliated cells, originates from parental centrioles, and its cellular position is biased and dependent on ciliary beating. Furthermore, we show that the hybrid cilium emerges independently of other motile cilia and functions in regulating basal body alignment.

FIB-SEM, airway, appendages, basal bodies, basal foot, centrosome, cilia, electron microscopy, primary ciliary dyskinesia, quantitative imaging, super-resolution imaging
1534-5807
224-236.e6
Liu, Zhen
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Nguyen, Quynh P.H.
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Nanjundappa, Rashmi
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Delgehyr, Nathalie
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Megherbi, Alexandre
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Doherty, Regan
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Thompson, James
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Jackson, Claire
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Albulescu, Alexandra
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Heng, Yew
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Lucas, Jane
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Dell, Sharon
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Meunier, Alice
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Czymmek, Kirk
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Mahjoub, Moe R.
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Mennella, Vito
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Liu, Zhen
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Nguyen, Quynh P.H.
91934f77-429f-41b2-95c8-90bdcab5e39a
Nanjundappa, Rashmi
8a8d4590-836b-48fd-b0f2-494b1789d21d
Delgehyr, Nathalie
3251dffd-4327-4470-a1b2-414822386c46
Megherbi, Alexandre
8d0a0b91-0ed2-4ce7-aada-e662d010b63c
Doherty, Regan
da470b85-b358-4e8a-aec6-983ef87a89fc
Thompson, James
a0a1e940-d720-47de-81d7-ebcd48738239
Jackson, Claire
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Albulescu, Alexandra
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Heng, Yew
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Lucas, Jane
5cb3546c-87b2-4e59-af48-402076e25313
Dell, Sharon
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Meunier, Alice
6915dc82-44df-4d62-b091-790aafbc1960
Czymmek, Kirk
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Mahjoub, Moe R.
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Mennella, Vito
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Liu, Zhen, Nguyen, Quynh P.H., Nanjundappa, Rashmi, Delgehyr, Nathalie, Megherbi, Alexandre, Doherty, Regan, Thompson, James, Jackson, Claire, Albulescu, Alexandra, Heng, Yew, Lucas, Jane, Dell, Sharon, Meunier, Alice, Czymmek, Kirk, Mahjoub, Moe R. and Mennella, Vito (2020) Super-resolution microscopy and FIB-SEM imaging reveal parental centriole-derived, hybrid cilium in mammalian multiciliated cells. Developmental Cell, 55 (2), 224-236.e6. (doi:10.1016/j.devcel.2020.09.016).

Record type: Article

Abstract

Motile cilia are cellular beating machines that play a critical role in mucociliary clearance, cerebrospinal fluid movement, and fertility. In the airways, hundreds of motile cilia present on the surface of a multiciliated epithelia cell beat coordinately to protect the epithelium from bacteria, viruses, and harmful particulates. During multiciliated cell differentiation, motile cilia are templated from basal bodies, each extending a basal foot-an appendage linking motile cilia together to ensure coordinated beating. Here, we demonstrate that among the many motile cilia of a multiciliated cell, a hybrid cilium with structural features of both primary and motile cilia is harbored. The hybrid cilium is conserved in mammalian multiciliated cells, originates from parental centrioles, and its cellular position is biased and dependent on ciliary beating. Furthermore, we show that the hybrid cilium emerges independently of other motile cilia and functions in regulating basal body alignment.

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Accepted/In Press date: 6 October 2020
e-pub ahead of print date: 9 October 2020
Published date: 26 October 2020
Additional Information: Funding Information: This project is funded by CIHR program grant # 391917 to V.M. and S.D. and National Heart Lung and Blood Institute ( R01-HL128370 ) and the Children’s Discovery Institute of Washington University and St. Louis Children’s Hospital ( CDI-CORE-2019-813 ) to M.R.M. Z.L. was supported by the SickKids Restracomp Fellowship. The authors acknowledge PCD patients and volunteers for providing nasal cells for this study and Julie Avolio for help with nasal cell scraping. Jia Zhou, Cindy Fang, and Jasmine Kang assisted in data analysis. Douglas Holmyard (EM facility, The Hospital for Sick Children) prepared TEM and FIB-SEM samples and helped set up EM imaging. McGill EM facility contributed to FIB-SEM acquisition. We thank Profs Sudipto Roi’s lab, Jeremy Reiter’s lab, and Nick Berbari’s lab for experimental help. We thank Profs Bornens, Pelletier, Cheeseman, Kyung Lee, Elsasser, and Avidor-Reiss laboratories for sharing antibodies and plasmids. Publisher Copyright: © 2020 Elsevier Inc.
Keywords: FIB-SEM, airway, appendages, basal bodies, basal foot, centrosome, cilia, electron microscopy, primary ciliary dyskinesia, quantitative imaging, super-resolution imaging

Identifiers

Local EPrints ID: 444526
URI: http://eprints.soton.ac.uk/id/eprint/444526
ISSN: 1534-5807
PURE UUID: 2fc3baba-84f5-49be-ae29-bfb70c7424d3
ORCID for James Thompson: ORCID iD orcid.org/0000-0002-9285-1317
ORCID for Claire Jackson: ORCID iD orcid.org/0000-0002-1200-0935
ORCID for Jane Lucas: ORCID iD orcid.org/0000-0001-8701-9975
ORCID for Vito Mennella: ORCID iD orcid.org/0000-0002-4842-9012

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Date deposited: 22 Oct 2020 16:34
Last modified: 17 Mar 2024 05:57

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Contributors

Author: Zhen Liu
Author: Quynh P.H. Nguyen
Author: Rashmi Nanjundappa
Author: Nathalie Delgehyr
Author: Alexandre Megherbi
Author: Regan Doherty
Author: James Thompson ORCID iD
Author: Claire Jackson ORCID iD
Author: Alexandra Albulescu
Author: Yew Heng
Author: Jane Lucas ORCID iD
Author: Sharon Dell
Author: Alice Meunier
Author: Kirk Czymmek
Author: Moe R. Mahjoub
Author: Vito Mennella ORCID iD

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