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Centriolar SAS-5 is required for centrosome duplication in C. elegans

Nature Cell Biology volume 6, pages 656–664 (2004)Cite this article

Abstract

Centrosomes, the major microtubule-organizing centres (MTOCs) of animal cells, are comprised of a pair of centrioles surrounded by pericentriolar material (PCM). Early in the cell cycle, there is a single centrosome, which duplicates during S-phase to direct bipolar spindle assembly during mitosis1. Although crucial for proper cell division, the mechanisms that govern centrosome duplication are not fully understood. Here, we identify the Caenorhabditis elegans gene sas-5 as essential for daughter-centriole formation. SAS-5 is a coiled-coil protein that localizes primarily to centrioles. Fluorescence recovery after photobleaching (FRAP) experiments with green fluorescent protein (GFP) fused to SAS-5 (GFP–SAS-5) demonstrated that the protein shuttles between centrioles and the cytoplasm throughout the cell cycle. Analysis of mutant alleles revealed that the presence of SAS-5 at centrioles is crucial for daughter-centriole formation and that ZYG-1, a kinase that is also essential for this process2, controls the distribution of SAS-5 to centrioles. Furthermore, partial RNA-interference (RNAi)-mediated inactivation experiments suggest that both sas-5 and zyg-1 are dose-dependent regulators of centrosome duplication.

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Figure 1: sas-5 has dual-parental requirement for centrosome duplication.
Figure 2: sas-5 is required for daughter centriole formation.
Figure 3: Distribution of SAS-5.
Figure 4: SAS-5 shuttles between the cytoplasm and both centrioles throughout the cell cycle.
Figure 5: sas-5 is a dose-dependent regulator of centrosome duplication.

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Acknowledgements

We are grateful to J.- M. Bellanger, M.- A. Félix, M. Labouesse and P. Strnad for critical reading of the manuscript, and to C. Echeverri for communicating results before publication. Some strains were obtained from the Caenorhabditis Genetics Center, which is funded by the National Center for Research Resources, National Institutes of Health. Sequencing of B. malayi at The Institute of Genomic Research is part of the International Brugia Genome Sequencing Project, which is supported by an award from the National Institute of Allergy and Infectious Diseases, National Institutes of Health. M. D. was supported by an EMBO long-term post-doctoral fellowship (ALTF 98-2001). Oncosuisse provides funding for work on centrosome duplication in the Gönczy laboratory (OCS 1100-02-2001).

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Author notes

  1. Khursheed Wani

    Present address: Massachusetts General Hospital Cancer Center, Charlestown, MA 02129, USA

  2. Heinke Schnabel

    Present address: Max Planck Institute of Neurobiology, 82152, Martinsreid, Germany

Authors and Affiliations

  1. Swiss Institute for Experimental Cancer Research (ISREC), Epalinges/Lausanne, CH-1066, Switzerland

    Marie Delattre, Sebastian Leidel, Khursheed Wani, Karine Baumer, Jeannine Bamat & Pierre Gönczy

  2. Institut für Genetik, TU Braunschweig, Braunschweig, D-38106, Germany

    Heinke Schnabel, Richard Feichtinger & Ralf Schnabel

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Correspondence to Pierre Gönczy.

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Delattre, M., Leidel, S., Wani, K. et al. Centriolar SAS-5 is required for centrosome duplication in C. elegans. Nat Cell Biol 6, 656–664 (2004). https://doi.org/10.1038/ncb1146

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