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


Journal

The EMBO journal
ISSN: 1460-2075
Titre abrégé: EMBO J
Pays: England
ID NLM: 8208664

Informations de publication

Date de publication:
16 11 2020
Historique:
received: 15 07 2020
revised: 20 08 2020
accepted: 24 08 2020
pubmed: 22 9 2020
medline: 15 4 2021
entrez: 21 9 2020
Statut: ppublish

Résumé

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.

Identifiants

pubmed: 32954513
doi: 10.15252/embj.2020106246
pmc: PMC7667884
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e106246

Subventions

Organisme : EC|H2020|H2020 Priority Excellent Science|H2020 European Research Council ERC
ID : StG 715289
Organisme : Swiss National Science Foundation
ID : PP00P3_187198, PP00P3_157517
Pays : Switzerland

Informations de copyright

© 2020 The Authors. Published under the terms of the CC BY 4.0 license.

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Auteurs

Nikolai Klena (N)

Department of Cell Biology, University of Geneva, Sciences III, Geneva, Switzerland.

Maeva Le Guennec (M)

Department of Cell Biology, University of Geneva, Sciences III, Geneva, Switzerland.

Anne-Marie Tassin (AM)

Institute for Integrative Biology of the Cell (I2BC), CEA, CNRS, Univ. Paris Sud, Université Paris-Saclay, Gif sur Yvette, France.

Hugo van den Hoek (H)

Helmholtz Pioneer Campus, Helmholtz Zentrum München, Neuherberg, Germany.
Department of Molecular Structural Biology, Max Planck Institute of Biochemistry, Martinsried, Germany.

Philipp S Erdmann (PS)

Department of Molecular Structural Biology, Max Planck Institute of Biochemistry, Martinsried, Germany.

Miroslava Schaffer (M)

Department of Molecular Structural Biology, Max Planck Institute of Biochemistry, Martinsried, Germany.

Stefan Geimer (S)

Department of Cell Biology and Electron Microscopy, Universität Bayreuth, Bayreuth, Germany.

Gabriel Aeschlimann (G)

Ribosome Studio Aeschlimann, Oberrieden, Switzerland.

Lubomir Kovacik (L)

Center for Cellular Imaging and NanoAnalytics (C-CINA), Biozentrum, University of Basel, Basel, Switzerland.

Yashar Sadian (Y)

Bioimaging and Cryogenic Center, University of Geneva, Geneva, Switzerland.

Kenneth N Goldie (KN)

Center for Cellular Imaging and NanoAnalytics (C-CINA), Biozentrum, University of Basel, Basel, Switzerland.

Henning Stahlberg (H)

Center for Cellular Imaging and NanoAnalytics (C-CINA), Biozentrum, University of Basel, Basel, Switzerland.

Benjamin D Engel (BD)

Helmholtz Pioneer Campus, Helmholtz Zentrum München, Neuherberg, Germany.
Department of Molecular Structural Biology, Max Planck Institute of Biochemistry, Martinsried, Germany.
Department of Chemistry, Technical University of Munich, Garching, Germany.

Virginie Hamel (V)

Department of Cell Biology, University of Geneva, Sciences III, Geneva, Switzerland.

Paul Guichard (P)

Department of Cell Biology, University of Geneva, Sciences III, Geneva, Switzerland.

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Classifications MeSH