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Architecture of the centriole cartwheel‐containing region revealed by cryo‐electron tomography

Centrioles are evolutionarily conserved barrels of microtubule triplets that form the core of the centrosome and the base of the cilium. While the crucial role of the proximal region in centriole biogenesis has been well documented, its native architecture and evolutionary conservation remain relati...

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Autores principales: Klena, Nikolai, Le Guennec, Maeva, Tassin, Anne‐Marie, van den Hoek, Hugo, Erdmann, Philipp S, Schaffer, Miroslava, Geimer, Stefan, Aeschlimann, Gabriel, Kovacik, Lubomir, Sadian, Yashar, Goldie, Kenneth N, Stahlberg, Henning, Engel, Benjamin D, Hamel, Virginie, Guichard, Paul
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7667884/
https://www.ncbi.nlm.nih.gov/pubmed/32954513
http://dx.doi.org/10.15252/embj.2020106246
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author Klena, Nikolai
Le Guennec, Maeva
Tassin, Anne‐Marie
van den Hoek, Hugo
Erdmann, Philipp S
Schaffer, Miroslava
Geimer, Stefan
Aeschlimann, Gabriel
Kovacik, Lubomir
Sadian, Yashar
Goldie, Kenneth N
Stahlberg, Henning
Engel, Benjamin D
Hamel, Virginie
Guichard, Paul
author_facet Klena, Nikolai
Le Guennec, Maeva
Tassin, Anne‐Marie
van den Hoek, Hugo
Erdmann, Philipp S
Schaffer, Miroslava
Geimer, Stefan
Aeschlimann, Gabriel
Kovacik, Lubomir
Sadian, Yashar
Goldie, Kenneth N
Stahlberg, Henning
Engel, Benjamin D
Hamel, Virginie
Guichard, Paul
author_sort Klena, Nikolai
collection PubMed
description Centrioles are evolutionarily conserved barrels of microtubule triplets that form the core of the centrosome and the base of the cilium. While the crucial role of the proximal region in centriole biogenesis has been well documented, its native architecture and evolutionary conservation remain relatively unexplored. Here, using cryo‐electron tomography of centrioles from four evolutionarily distant species, we report on the architectural diversity of the centriole's proximal cartwheel‐bearing region. Our work reveals that the cartwheel central hub is constructed from a stack of paired rings with cartwheel inner densities inside. In both Paramecium and Chlamydomonas, the repeating structural unit of the cartwheel has a periodicity of 25 nm and consists of three ring pairs, with 6 radial spokes emanating and merging into a single bundle that connects to the microtubule triplet via the D2‐rod and the pinhead. Finally, we identified that the cartwheel is indirectly connected to the A‐C linker through the triplet base structure extending from the pinhead. Together, our work provides unprecedented evolutionary insights into the architecture of the centriole proximal region, which underlies centriole biogenesis.
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spelling pubmed-76678842020-11-20 Architecture of the centriole cartwheel‐containing region revealed by cryo‐electron tomography Klena, Nikolai Le Guennec, Maeva Tassin, Anne‐Marie van den Hoek, Hugo Erdmann, Philipp S Schaffer, Miroslava Geimer, Stefan Aeschlimann, Gabriel Kovacik, Lubomir Sadian, Yashar Goldie, Kenneth N Stahlberg, Henning Engel, Benjamin D Hamel, Virginie Guichard, Paul EMBO J Articles Centrioles are evolutionarily conserved barrels of microtubule triplets that form the core of the centrosome and the base of the cilium. While the crucial role of the proximal region in centriole biogenesis has been well documented, its native architecture and evolutionary conservation remain relatively unexplored. Here, using cryo‐electron tomography of centrioles from four evolutionarily distant species, we report on the architectural diversity of the centriole's proximal cartwheel‐bearing region. Our work reveals that the cartwheel central hub is constructed from a stack of paired rings with cartwheel inner densities inside. In both Paramecium and Chlamydomonas, the repeating structural unit of the cartwheel has a periodicity of 25 nm and consists of three ring pairs, with 6 radial spokes emanating and merging into a single bundle that connects to the microtubule triplet via the D2‐rod and the pinhead. Finally, we identified that the cartwheel is indirectly connected to the A‐C linker through the triplet base structure extending from the pinhead. Together, our work provides unprecedented evolutionary insights into the architecture of the centriole proximal region, which underlies centriole biogenesis. John Wiley and Sons Inc. 2020-09-20 2020-11-16 /pmc/articles/PMC7667884/ /pubmed/32954513 http://dx.doi.org/10.15252/embj.2020106246 Text en © 2020 The Authors. Published under the terms of the CC BY 4.0 license This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Articles
Klena, Nikolai
Le Guennec, Maeva
Tassin, Anne‐Marie
van den Hoek, Hugo
Erdmann, Philipp S
Schaffer, Miroslava
Geimer, Stefan
Aeschlimann, Gabriel
Kovacik, Lubomir
Sadian, Yashar
Goldie, Kenneth N
Stahlberg, Henning
Engel, Benjamin D
Hamel, Virginie
Guichard, Paul
Architecture of the centriole cartwheel‐containing region revealed by cryo‐electron tomography
title Architecture of the centriole cartwheel‐containing region revealed by cryo‐electron tomography
title_full Architecture of the centriole cartwheel‐containing region revealed by cryo‐electron tomography
title_fullStr Architecture of the centriole cartwheel‐containing region revealed by cryo‐electron tomography
title_full_unstemmed Architecture of the centriole cartwheel‐containing region revealed by cryo‐electron tomography
title_short Architecture of the centriole cartwheel‐containing region revealed by cryo‐electron tomography
title_sort architecture of the centriole cartwheel‐containing region revealed by cryo‐electron tomography
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7667884/
https://www.ncbi.nlm.nih.gov/pubmed/32954513
http://dx.doi.org/10.15252/embj.2020106246
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