Ana1/CEP295 is an essential player in the centrosome maintenance program regulated by Polo kinase and the PCM
Pimenta-Marques A, Perestrelo T, Dos Reis Rodrigues P, Duarte P, Ferreira-Silva A, Lince-Faria M, Bettencourt-Dias M. 2024. Ana1/CEP295 is an essential player in the centrosome maintenance program regulated by Polo kinase and the PCM. EMBO reports. 25(1), 102–127.
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Author
Pimenta-Marques, Ana;
Perestrelo, Tania;
Rodrigues, PatriciaISTA ;
Duarte, Paulo;
Ferreira-Silva, Ana;
Lince-Faria, Mariana;
Bettencourt-Dias, Mónica
Department
Abstract
Centrioles are part of centrosomes and cilia, which are microtubule organising centres (MTOC) with diverse functions. Despite their stability, centrioles can disappear during differentiation, such as in oocytes, but little is known about the regulation of their structural integrity. Our previous research revealed that the pericentriolar material (PCM) that surrounds centrioles and its recruiter, Polo kinase, are downregulated in oogenesis and sufficient for maintaining both centrosome structural integrity and MTOC activity. We now show that the expression of specific components of the centriole cartwheel and wall, including ANA1/CEP295, is essential for maintaining centrosome integrity. We find that Polo kinase requires ANA1 to promote centriole stability in cultured cells and eggs. In addition, ANA1 expression prevents the loss of centrioles observed upon PCM-downregulation. However, the centrioles maintained by overexpressing and tethering ANA1 are inactive, unlike the MTOCs observed upon tethering Polo kinase. These findings demonstrate that several centriole components are needed to maintain centrosome structure. Our study also highlights that centrioles are more dynamic than previously believed, with their structural stability relying on the continuous expression of multiple components.
Publishing Year
Date Published
2024-01-10
Journal Title
EMBO reports
Publisher
Embo Press
Acknowledgement
We thank all members of the Cell Cycle and Regulation Lab for the discussions and for the critical reading of the manuscript. We thank Tomer Avidor-Reiss (University of Toledo, Toledo, OH), Daniel St. Johnston (The Gurdon Institute, Cambridge, UK), David Glover (University of Cambridge, Cambridge, UK), Jingyan Fu (Agricultural University, Beijing, China) Jordan Raff (University of Oxford, Oxford, UK) and Timothy Megraw (Florida State University, Tallahassee, FL) for sharing tools. We acknowledge the technical support of Instituto Gulbenkian de Ciência (IGC)‘s Advanced Imaging Facility, in particular Gabriel Martins, Nuno Pimpão Martins and José Marques. We also thank Tiago Paixão from the IGC’s Quantitative & Digital Science Unit and Marco Louro from the CCR lab for the support provided on statistical analysis. IGC’s Advanced Imaging Facility (AIF-UIC) is supported by the national Portuguese funding ref# PPBI-POCI-01-0145-FEDER -022122. We thank the IGC’s Fly Facility, supported by CONGENTO (LISBOA-01-0145-FEDER-022170). This work was supported by an ERC grant (ERC-2015-CoG-683258) awarded to MBD and a grant from the Portuguese Research Council (FCT) awarded to APM (PTDC/BIA-BID/32225/2017).
Volume
25
Issue
1
Page
102-127
eISSN
IST-REx-ID
Cite this
Pimenta-Marques A, Perestrelo T, Dos Reis Rodrigues P, et al. Ana1/CEP295 is an essential player in the centrosome maintenance program regulated by Polo kinase and the PCM. EMBO reports. 2024;25(1):102-127. doi:10.1038/s44319-023-00020-6
Pimenta-Marques, A., Perestrelo, T., Dos Reis Rodrigues, P., Duarte, P., Ferreira-Silva, A., Lince-Faria, M., & Bettencourt-Dias, M. (2024). Ana1/CEP295 is an essential player in the centrosome maintenance program regulated by Polo kinase and the PCM. EMBO Reports. Embo Press. https://doi.org/10.1038/s44319-023-00020-6
Pimenta-Marques, Ana, Tania Perestrelo, Patricia Dos Reis Rodrigues, Paulo Duarte, Ana Ferreira-Silva, Mariana Lince-Faria, and Mónica Bettencourt-Dias. “Ana1/CEP295 Is an Essential Player in the Centrosome Maintenance Program Regulated by Polo Kinase and the PCM.” EMBO Reports. Embo Press, 2024. https://doi.org/10.1038/s44319-023-00020-6.
A. Pimenta-Marques et al., “Ana1/CEP295 is an essential player in the centrosome maintenance program regulated by Polo kinase and the PCM,” EMBO reports, vol. 25, no. 1. Embo Press, pp. 102–127, 2024.
Pimenta-Marques A, Perestrelo T, Dos Reis Rodrigues P, Duarte P, Ferreira-Silva A, Lince-Faria M, Bettencourt-Dias M. 2024. Ana1/CEP295 is an essential player in the centrosome maintenance program regulated by Polo kinase and the PCM. EMBO reports. 25(1), 102–127.
Pimenta-Marques, Ana, et al. “Ana1/CEP295 Is an Essential Player in the Centrosome Maintenance Program Regulated by Polo Kinase and the PCM.” EMBO Reports, vol. 25, no. 1, Embo Press, 2024, pp. 102–27, doi:10.1038/s44319-023-00020-6.
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