Evolutionary conservation of centriole rotational asymmetry in the human centrosome
- Institut Jacques Monod, France
- Institut Pasteur, USR 3756 CNRS, France
- Institut de Génétique et de Biologie Moléculaire et Cellulaire (IGBMC), France
Abstract
Centrioles are formed by microtubule triplets in a nine-fold symmetric arrangement. In flagellated protists and in animal multiciliated cells, accessory structures tethered to specific triplets render the centrioles rotationally asymmetric, a property that is key to cytoskeletal and cellular organization in these contexts. In contrast, centrioles within the centrosome of animal cells display no conspicuous rotational asymmetry. Here, we uncover rotationally asymmetric molecular features in human centrioles. Using ultrastructure expansion microscopy, we show that LRRCC1, the ortholog of a protein originally characterized in flagellate green algae, associates preferentially to two consecutive triplets in the distal lumen of human centrioles. LRRCC1 partially co-localizes and affects the recruitment of another distal component, C2CD3, which also has an asymmetric localization pattern in the centriole lumen. Together, LRRCC1 and C2CD3 delineate a structure reminiscent of a filamentous density observed by electron microscopy in flagellates, termed the 'acorn'. Functionally, the depletion of LRRCC1 in human cells induced defects in centriole structure, ciliary assembly and ciliary signaling, supporting that LRRCC1 cooperates with C2CD3 to organizing the distal region of centrioles. Since a mutation in the LRRCC1 gene has been identified in Joubert syndrome patients, this finding is relevant in the context of human ciliopathies. Taken together, our results demonstrate that rotational asymmetry is an ancient property of centrioles that is broadly conserved in human cells. Our work also reveals that asymmetrically localized proteins are key for primary ciliogenesis and ciliary signaling in human cells.
Data availability
All data generated or analyzed during this study are included in the manuscript and supporting files. Source data files are available from the Dryad database (doi:10.5061/dryad.95x69p8m5).
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Data from: Evolutionary conservation of centriole rotational asymmetry in the human centrosomeDryad Digital Repository, doi:10.5061/dryad.95x69p8m5.
Article and author information
Author details
Catherine Pioche-Durieu
Juliette Azimzadeh
Funding
Agence Nationale de la Recherche (ANR-21-CE13-008)
- Juliette Azimzadeh
Fondation pour la Recherche Médicale (Graduate Student Fellowship)
- Noémie Gaudin
Fondation ARC pour la Recherche sur le Cancer (Dotation)
- Juliette Azimzadeh
Ligue Contre le Cancer (Dotation)
- Juliette Azimzadeh
Labex Who Am I?
- Juliette Azimzadeh
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Jens Lüders, Institute for Research in Biomedicine, Spain
Version history
- Received: July 21, 2021
- Preprint posted: July 22, 2021 (view preprint)
- Accepted: March 22, 2022
- Accepted Manuscript published: March 23, 2022 (version 1)
- Version of Record published: April 5, 2022 (version 2)
Copyright
© 2022, Gaudin et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Evolutionary conservation of centriole rotational asymmetry in the human centrosome
eLife 11:e72382.
https://doi.org/10.7554/eLife.72382
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