Kinetic and structural roles for the surface in guiding SAS-6 self-assembly to direct centriole architecture

Discovering mechanisms governing organelle assembly is a fundamental pursuit in biology. The centriole is an evolutionarily conserved organelle with a signature 9-fold symmetrical chiral arrangement of microtubules imparted onto the cilium it templates. The first structure in nascent centrioles is a...

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Main Authors: Banterle, Niccolò (Author) , Nievergelt, Adrian P. (Author) , Buhr, Svenja de (Author) , Hatzopoulos, Georgios N. (Author) , Brillard, Charlène (Author) , Andany, Santiago (Author) , Hübscher, Tania (Author) , Sorgenfrei, Frieda A. (Author) , Schwarz, Ulrich S. (Author) , Gräter, Frauke (Author) , Fantner, Georg E. (Author) , Gönczy, Pierre (Author)
Format: Article (Journal)
Language:English
Published: 26 October 2021
In: Nature Communications
Year: 2021, Volume: 12, Pages: 1-14
ISSN:2041-1723
DOI:10.1038/s41467-021-26329-1
Online Access:Verlag, kostenfrei, Volltext: https://doi.org/10.1038/s41467-021-26329-1
Verlag, kostenfrei, Volltext: https://www.nature.com/articles/s41467-021-26329-1
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Author Notes:Niccolò Banterle, Adrian P. Nievergelt, Svenja de Buhr, Georgios N. Hatzopoulos, Charlène Brillard, Santiago Andany, Tania Hübscher, Frieda A. Sorgenfrei, Ulrich S. Schwarz, Frauke Gräter, Georg E. Fantner & Pierre Gönczy
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Summary:Discovering mechanisms governing organelle assembly is a fundamental pursuit in biology. The centriole is an evolutionarily conserved organelle with a signature 9-fold symmetrical chiral arrangement of microtubules imparted onto the cilium it templates. The first structure in nascent centrioles is a cartwheel, which comprises stacked 9-fold symmetrical SAS-6 ring polymers emerging orthogonal to a surface surrounding each resident centriole. The mechanisms through which SAS-6 polymerization ensures centriole organelle architecture remain elusive. We deploy photothermally-actuated off-resonance tapping high-speed atomic force microscopy to decipher surface SAS-6 self-assembly mechanisms. We show that the surface shifts the reaction equilibrium by ~104 compared to solution. Moreover, coarse-grained molecular dynamics and atomic force microscopy reveal that the surface converts the inherent helical propensity of SAS-6 polymers into 9-fold rings with residual asymmetry, which may guide ring stacking and impart chiral features to centrioles and cilia. Overall, our work reveals fundamental design principles governing centriole assembly.
Item Description:Gesehen am 10.03.2022
Physical Description:Online Resource
ISSN:2041-1723
DOI:10.1038/s41467-021-26329-1