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Evolutionary conservation of centriole rotational asymmetry in the human centrosome

Centrioles are formed by microtubule triplets in a ninefold symmetric arrangement. In flagellated protists and animal multiciliated cells, accessory structures tethered to specific triplets render the centrioles rotationally asymmetric, a property that is key to cytoskeletal and cellular organizatio...

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Autores principales: Gaudin, Noémie, Martin Gil, Paula, Boumendjel, Meriem, Ershov, Dmitry, Pioche-Durieu, Catherine, Bouix, Manon, Delobelle, Quentin, Maniscalco, Lucia, Phan, Than Bich Ngan, Heyer, Vincent, Reina-San-Martin, Bernardo, Azimzadeh, Juliette
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8983040/
https://www.ncbi.nlm.nih.gov/pubmed/35319462
http://dx.doi.org/10.7554/eLife.72382
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author Gaudin, Noémie
Martin Gil, Paula
Boumendjel, Meriem
Ershov, Dmitry
Pioche-Durieu, Catherine
Bouix, Manon
Delobelle, Quentin
Maniscalco, Lucia
Phan, Than Bich Ngan
Heyer, Vincent
Reina-San-Martin, Bernardo
Azimzadeh, Juliette
author_facet Gaudin, Noémie
Martin Gil, Paula
Boumendjel, Meriem
Ershov, Dmitry
Pioche-Durieu, Catherine
Bouix, Manon
Delobelle, Quentin
Maniscalco, Lucia
Phan, Than Bich Ngan
Heyer, Vincent
Reina-San-Martin, Bernardo
Azimzadeh, Juliette
author_sort Gaudin, Noémie
collection PubMed
description Centrioles are formed by microtubule triplets in a ninefold symmetric arrangement. In flagellated protists and 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.
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spelling pubmed-89830402022-04-06 Evolutionary conservation of centriole rotational asymmetry in the human centrosome Gaudin, Noémie Martin Gil, Paula Boumendjel, Meriem Ershov, Dmitry Pioche-Durieu, Catherine Bouix, Manon Delobelle, Quentin Maniscalco, Lucia Phan, Than Bich Ngan Heyer, Vincent Reina-San-Martin, Bernardo Azimzadeh, Juliette eLife Cell Biology Centrioles are formed by microtubule triplets in a ninefold symmetric arrangement. In flagellated protists and 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. eLife Sciences Publications, Ltd 2022-03-23 /pmc/articles/PMC8983040/ /pubmed/35319462 http://dx.doi.org/10.7554/eLife.72382 Text en © 2022, Gaudin et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Cell Biology
Gaudin, Noémie
Martin Gil, Paula
Boumendjel, Meriem
Ershov, Dmitry
Pioche-Durieu, Catherine
Bouix, Manon
Delobelle, Quentin
Maniscalco, Lucia
Phan, Than Bich Ngan
Heyer, Vincent
Reina-San-Martin, Bernardo
Azimzadeh, Juliette
Evolutionary conservation of centriole rotational asymmetry in the human centrosome
title Evolutionary conservation of centriole rotational asymmetry in the human centrosome
title_full Evolutionary conservation of centriole rotational asymmetry in the human centrosome
title_fullStr Evolutionary conservation of centriole rotational asymmetry in the human centrosome
title_full_unstemmed Evolutionary conservation of centriole rotational asymmetry in the human centrosome
title_short Evolutionary conservation of centriole rotational asymmetry in the human centrosome
title_sort evolutionary conservation of centriole rotational asymmetry in the human centrosome
topic Cell Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8983040/
https://www.ncbi.nlm.nih.gov/pubmed/35319462
http://dx.doi.org/10.7554/eLife.72382
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