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Conserved molecular interactions in centriole-to-centrosome conversion

Fu, Jingyan and Lipinszki, Zoltan and Rangone, Hélène and Min, Mingwei and Mykura, Charlotte and Chao-Chu, Jennifer and Schneider, Sandra and Dzhindzhev, Nikola S. and Gottardo, Marco and Riparbelli, Maria Giovanna and Callaini, Giuliano and Glover, David M. (2016) Conserved molecular interactions in centriole-to-centrosome conversion. Nature Cell Biology, 18 (1). pp. 87-99. ISSN 1465-7392. PMCID PMC4719191. doi:10.1038/ncb3274. https://resolver.caltech.edu/CaltechAUTHORS:20200807-170349570

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Abstract

Centrioles are required to assemble centrosomes for cell division and cilia for motility and signalling. New centrioles assemble perpendicularly to pre-existing ones in G1–S and elongate throughout S and G2. Fully elongated daughter centrioles are converted into centrosomes during mitosis to be able to duplicate and organize pericentriolar material in the next cell cycle. Here we show that centriole-to-centrosome conversion requires sequential loading of Cep135, Ana1 (Cep295) and Asterless (Cep152) onto daughter centrioles during mitotic progression in both Drosophila melanogaster and human. This generates a molecular network spanning from the inner- to outermost parts of the centriole. Ana1 forms a molecular strut within the network, and its essential role can be substituted by an engineered fragment providing an alternative linkage between Asterless and Cep135. This conserved architectural framework is essential for loading Asterless or Cep152, the partner of the master regulator of centriole duplication, Plk4. Our study thus uncovers the molecular basis for centriole-to-centrosome conversion that renders daughter centrioles competent for motherhood.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1038/ncb3274DOIArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4719191/PubMed CentralArticle
https://rdcu.be/b6a4ZPublisherFree ReadCube access
ORCID:
AuthorORCID
Fu, Jingyan0000-0002-5896-8132
Lipinszki, Zoltan0000-0002-2067-0832
Chao-Chu, Jennifer0000-0001-6740-8797
Dzhindzhev, Nikola S.0000-0001-9866-3600
Gottardo, Marco0000-0001-8649-7799
Callaini, Giuliano0000-0003-2252-0309
Glover, David M.0000-0003-0956-0103
Additional Information:© 2016 Nature Publishing Group. Received 25 February 2015. Accepted 21 October 2015. Published 23 November 2015. J.F., Z.L., S.S. and N.S.D. are supported by a Programme Grant to D.M.G. from Cancer Research UK. H.R. is supported by an MRC Programme Grant to D.M.G. J.F. thanks the British Academy and the Royal Society for the Newton International Fellowship and Z.L. thanks the Federation of European Biochemical Societies for the Long-Term postdoctoral Fellowship. The authors thank N. Lawrence and A. Sossick for assistance with 3D-SIM. Author Contributions: J.F. designed and performed experiments; Z.L. carried out biochemical analysis; H.R. carried out studies on mutant Drosophila; M.G., M.G.R. and G.C. performed electron microscopy; M.M., C.M., J.C.-C., S.S. and N.S.D. contributed material support; J.F. and D.M.G. analysed results and wrote manuscript. Z.L. and H.R. commented on the manuscript. The authors declare no competing financial interests.
Funders:
Funding AgencyGrant Number
Cancer Research UKUNSPECIFIED
Medical Research Council (UK)UNSPECIFIED
British AcademyUNSPECIFIED
Royal SocietyUNSPECIFIED
Federation of European Biochemical SocietiesUNSPECIFIED
Issue or Number:1
PubMed Central ID:PMC4719191
DOI:10.1038/ncb3274
Record Number:CaltechAUTHORS:20200807-170349570
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20200807-170349570
Official Citation:Fu, J., Lipinszki, Z., Rangone, H. et al. Conserved molecular interactions in centriole-to-centrosome conversion. Nat Cell Biol 18, 87–99 (2016). https://doi.org/10.1038/ncb3274
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:104837
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:11 Aug 2020 14:11
Last Modified:16 Nov 2021 18:36

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