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DSAS-6 Organizes a Tube-like Centriole Precursor, and Its Absence Suggests Modularity in Centriole Assembly

Rodrigues-Martins, Ana and Bettencourt-Dias, Mónica and Riparbelli, Maria and Ferreira, Cláudia and Ferreira, Inês and Callaini, Giuliano and Glover, David M. (2007) DSAS-6 Organizes a Tube-like Centriole Precursor, and Its Absence Suggests Modularity in Centriole Assembly. Current Biology, 17 (17). pp. 1465-1472. ISSN 0960-9822. doi:10.1016/j.cub.2007.07.034. https://resolver.caltech.edu/CaltechAUTHORS:20200928-150626070

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Abstract

Centrioles are microtubule-based cylindrical structures that exhibit 9-fold symmetry and facilitate the organization of centrosomes, flagella, and cilia [1]. Abnormalities in centrosome structure and number occur in many cancers 1, 2. Despite its importance, very little is known about centriole biogenesis. Recent studies in C. elegans have highlighted a group of molecules necessary for centriole assembly 1, 3. ZYG-1 kinase recruits a complex of two coiled-coil proteins, SAS-6 and SAS-5, which are necessary to form the C. elegans centriolar tube, a scaffold in centriole formation 4, 5. This complex also recruits SAS-4, which is required for the assembly of the centriolar microtubules that decorate that tube 4, 5. Here we show that Drosophila SAS-6 is involved in centriole assembly and cohesion. Overexpression of DSAS-6 in syncitial embryos led to the de novo formation of multiple microtubule-organizing centers (MTOCs). Strikingly, the center of these MTOCs did not contain centrioles, as described previously for SAK/PLK4 overexpression [6]. Instead, tube-like structures were present, supporting the idea that centriolar assembly starts with the formation of a tube-like scaffold, dependent on DSAS-6 [5]. In DSAS-6 loss-of-function mutants, centrioles failed to close and to elongate the structure along all axes of the 9-fold symmetry, suggesting modularity in centriole assembly. We propose that the tube is built from nine subunits fitting together laterally and longitudinally in a modular and sequential fashion, like pieces of a layered “hollow” cake.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1016/j.cub.2007.07.034DOIArticle
ORCID:
AuthorORCID
Callaini, Giuliano0000-0003-2252-0309
Glover, David M.0000-0003-0956-0103
Additional Information:© 2007 Elsevier. Under an Elsevier user license. Received 27 April 2007, Revised 17 July 2007, Accepted 17 July 2007, Available online 9 August 2007. We thank Z. Santos and C. Ott for help with experiments. We thank D. Johnston, R. Basto, and J. Raff for reagents. We thank J. Raff and R. Kuriyama for sharing unpublished data. We thank H. Ohkura for advice on female meiosis. We thank R. Martinho, P. Lourtie, J. Pereira-Leal, M. Gatt, R. Kuriyama, Z. Santos, J. Lamego, R. Linck, L. Pelletier, K. Tokuyasu, the Drosophila IGC community, and the M.B.-D. and D.M.G. groups for discussions. We thank http://www.thebestgene.com for making transgenic flies and the IGC imaging unit for help with image acquisition. We are grateful for grants from Cancer Research UK, Fundação Calouste Gulbenkian, Fundação para a Ciência e Tecnologia, and to an International Joint Project Grant from the Royal Society for collaboration between the M.B.-D. and D.M.G. groups. G.C. thanks PRIN and PAR (University of Siena) for funding.
Funders:
Funding AgencyGrant Number
Cancer Research UKUNSPECIFIED
Fundação Calouste GulbenkianUNSPECIFIED
Fundação para a Ciência e Tecnologia (FCT)UNSPECIFIED
Royal SocietyUNSPECIFIED
University of SienaUNSPECIFIED
Subject Keywords:CELLBIO; DNA
Issue or Number:17
DOI:10.1016/j.cub.2007.07.034
Record Number:CaltechAUTHORS:20200928-150626070
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20200928-150626070
Official Citation:Ana Rodrigues-Martins, Mónica Bettencourt-Dias, Maria Riparbelli, Cláudia Ferreira, Inês Ferreira, Giuliano Callaini, David M. Glover, DSAS-6 Organizes a Tube-like Centriole Precursor, and Its Absence Suggests Modularity in Centriole Assembly, Current Biology, Volume 17, Issue 17, 2007, Pages 1465-1472, ISSN 0960-9822, https://doi.org/10.1016/j.cub.2007.07.034.
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:105610
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:29 Sep 2020 14:56
Last Modified:16 Nov 2021 18:44

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