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Control of daughter centriole formation by the pericentriolar material

Nature Cell Biology volume 10, pages 322–328 (2008)Cite this article

Abstract

Controlling the number of its centrioles is vital for the cell, as supernumerary centrioles cause multipolar mitosis and genomic instability1,2. Normally, one daughter centriole forms on each mature (mother) centriole3,4; however, a mother centriole can produce multiple daughters within a single cell cycle5,6. The mechanisms that prevent centriole 'overduplication' are poorly understood. Here we use laser microsurgery to test the hypothesis that attachment of the daughter centriole to the wall of the mother inhibits formation of additional daughters7,8. We show that physical removal of the daughter induces reduplication of the mother in S-phase-arrested cells. Under conditions when multiple daughters form simultaneously on a single mother, all of these daughters must be removed to induce reduplication. The number of daughter centrioles that form during reduplication does not always match the number of ablated daughter centrioles. We also find that exaggeration of the pericentriolar material (PCM) by overexpression of the PCM protein pericentrin9 in S-phase-arrested CHO cells induces formation of numerous daughter centrioles. We propose that that the size of the PCM cloud associated with the mother centriole restricts the number of daughters that can form simultaneously.

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Figure 1: Laser ablation of daughter centrioles induces reduplication of the remaining mothers in S-phase-arrested HeLa cells.
Figure 2: Examples of centriolar configurations in S-phase-arrested CHO cells.
Figure 3: Ablation of all daughter centrioles within a centrosome induces reduplication of the mother in S-phase-arrested CHO cells.
Figure 4: Effects of PCM exaggeration on the number of daughter centrioles.

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Acknowledgements

We thank the members of our lab for fruitful discussions. Special thanks to Brian M. Davis and Igor B. Roninson for their help with construction of the centrin–GFP lentivirus and Yimin Dong for assistance with 3D reconstructions. We also thank Kip Sluder, Conly Rieder and Michael Koonce for critical comments on the manuscript. This work was supported by grants from the National Institutes of Health (GM GM59363) and the Human Frontiers Science Program (RGP0064). Construction of our laser microsurgery workstation was supported in part by a fellowship from Nikon/Marine Biological Laboratory (A. K.). We acknowledge use of the Wadsworth Center's Electron Microscopy Core Facility.

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Authors and Affiliations

  1. Division of Molecular Medicine, New York State Department of Health, Wadsworth Center, Albany, Albany, 12201-0509, New York, USA

    Jadranka Loncarek, Polla Hergert, Valentin Magidson & Alexey Khodjakov

  2. Marine Biological Laboratory, Woods Hole, 02543, Massachusetts, USA

    Alexey Khodjakov

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  4. Alexey Khodjakov
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Contributions

Experiments were conducted by J. L.; P. H. was responsible for EM preparation and data collection; V. M. designed, assembled and maintained the laser microsurgery workstation; A. K. directed the work. Experiments were planned by J. L. and A. K.

Corresponding author

Correspondence to Alexey Khodjakov.

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Loncarek, J., Hergert, P., Magidson, V. et al. Control of daughter centriole formation by the pericentriolar material. Nat Cell Biol 10, 322–328 (2008). https://doi.org/10.1038/ncb1694

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