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Research Article
Polo-like kinase phosphorylation determines Caenorhabditis elegans centrosome size and density by biasing SPD-5 toward an assembly-competent conformation
Oliver Wueseke, David Zwicker, Anne Schwager, Yao Liang Wong, Karen Oegema, Frank Jülicher, Anthony A. Hyman, Jeffrey B. Woodruff
Biology Open 2016 5: 1431-1440; doi: 10.1242/bio.020990
Oliver Wueseke
1Institute of Molecular Biotechnology, Dr. Bohr-Gasse 3, Wien 1030, Austria
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David Zwicker
2School of Engineering and Applied Sciences, Harvard University, 29 Oxford Street, Cambridge, MA 02138, USA
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Anne Schwager
3Max Planck Institute of Molecular Cell Biology and Genetics, Pfotenhauerstrasse 108, Dresden 01307, Germany
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Yao Liang Wong
4Dept. of Cellular and Molecular Medicine, Ludwig Institute for Cancer Research, University of California, San Diego, La Jolla, CA 92093, USA
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Karen Oegema
4Dept. of Cellular and Molecular Medicine, Ludwig Institute for Cancer Research, University of California, San Diego, La Jolla, CA 92093, USA
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Frank Jülicher
5Max Planck Institute for the Physics of Complex Systems, Nöthnitzer Str. 38, Dresden 01187, Germany
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Anthony A. Hyman
3Max Planck Institute of Molecular Cell Biology and Genetics, Pfotenhauerstrasse 108, Dresden 01307, Germany
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Jeffrey B. Woodruff
3Max Planck Institute of Molecular Cell Biology and Genetics, Pfotenhauerstrasse 108, Dresden 01307, Germany
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  • For correspondence: woodruff@mpi-cbg.de
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ABSTRACT

Centrosomes are major microtubule-organizing centers composed of centrioles surrounded by an extensive proteinacious layer called the pericentriolar material (PCM). In Caenorhabditis elegans embryos, the mitotic PCM expands by Polo-like kinase 1 (PLK-1) phosphorylation-accelerated assembly of SPD-5 molecules into supramolecular scaffolds. However, how PLK-1 phosphorylation regulates SPD-5 assembly is not known. We found that a mutant version of SPD-5 that is insensitive to PLK-1 phosphorylation (SPD-54A) could localize to PCM but was unable to rescue the reduction in PCM size and density when wild-type SPD-5 levels were decreased. In vitro, purified SPD-54A self-assembled into functional supramolecular scaffolds over long time scales, suggesting that phosphorylation only controls the rate of SPD-5 scaffold assembly. Furthermore, the SPD-5 scaffold, once assembled, remained intact and supported microtubule nucleation in the absence of PLK-1 activity in vivo. We conclude that PLK-1 is required for rapid assembly of the PCM scaffold but not for scaffold maintenance or function. Based on this idea, we developed a theoretical model that adequately predicted PCM growth rates in different mutant conditions in vivo. We propose that PLK-1 phosphorylation-dependent conversion of SPD-5 into an assembly-competent form underlies PCM formation in vivo and that the rate of this conversion determines final PCM size and density.

Footnotes

  • Competing interests

    The authors declare no competing or financial interests.

  • Author contributions

    O.W., J.B.W., and D.Z. designed the experiments and wrote the manuscript. O.W. performed the in vivo experiments and quantifications of centrosome size and density as well as protein levels from western blots and stainings. D.Z. developed and tested the model with help from F.J. J.B.W. performed the in vitro experiments and in vivo analysis of centrosome size in the plk-1as embryos. Y.L.W. and K.O. created the plk-1as gfp::spd-5 strain. A.S. immunostained embryos. A.A.H. assisted with experimental design.

  • Funding

    This project was funded by the Max-Planck-Gesellschaft (Max Planck Society) and the European Commission's Seventh Framework Programme [grant number FP7-HEALTH-2009-241548/MitoSys] and a Max Planck Research Network in Synthetic Biology (MaxSynBio) grant to A.A.H. and F.J. J.B.W. was supported by an EMBO fellowship [no. ALTF 759-2012] and MaxSynBio.

  • Supplementary information

    Supplementary information available online at http://bio.biologists.org/lookup/doi/10.1242/bio.020990.supplemental

  • Received July 29, 2016.
  • Accepted August 25, 2016.
  • © 2016. Published by The Company of Biologists Ltd

This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

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Keywords

  • C. elegans
  • PCM
  • Polo-like kinase
  • SPD-5
  • Centrosome
  • Microtubule

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Research Article
Polo-like kinase phosphorylation determines Caenorhabditis elegans centrosome size and density by biasing SPD-5 toward an assembly-competent conformation
Oliver Wueseke, David Zwicker, Anne Schwager, Yao Liang Wong, Karen Oegema, Frank Jülicher, Anthony A. Hyman, Jeffrey B. Woodruff
Biology Open 2016 5: 1431-1440; doi: 10.1242/bio.020990
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Research Article
Polo-like kinase phosphorylation determines Caenorhabditis elegans centrosome size and density by biasing SPD-5 toward an assembly-competent conformation
Oliver Wueseke, David Zwicker, Anne Schwager, Yao Liang Wong, Karen Oegema, Frank Jülicher, Anthony A. Hyman, Jeffrey B. Woodruff
Biology Open 2016 5: 1431-1440; doi: 10.1242/bio.020990

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