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An autonomous oscillator times and executes centriole biogenesis

View ORCID ProfileMustafa G. Aydogan, View ORCID ProfileThomas L. Steinacker, View ORCID ProfileMohammad Mofatteh, Lisa Gartenmann, View ORCID ProfileAlan Wainman, View ORCID ProfileSaroj Saurya, Siu S. Wong, View ORCID ProfileFelix Y. Zhou, View ORCID ProfileMichael A. Boemo, View ORCID ProfileJordan W. Raff
doi: https://doi.org/10.1101/510875
Mustafa G. Aydogan
1Sir William Dunn School of Pathology, University of Oxford, Oxford, UK
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  • For correspondence: mustafa.aydogan@path.ox.ac.uk michael.boemo@path.ox.ac.uk jordan.raff@path.ox.ac.uk
Thomas L. Steinacker
1Sir William Dunn School of Pathology, University of Oxford, Oxford, UK
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Mohammad Mofatteh
1Sir William Dunn School of Pathology, University of Oxford, Oxford, UK
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Lisa Gartenmann
1Sir William Dunn School of Pathology, University of Oxford, Oxford, UK
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Alan Wainman
1Sir William Dunn School of Pathology, University of Oxford, Oxford, UK
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Saroj Saurya
1Sir William Dunn School of Pathology, University of Oxford, Oxford, UK
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Siu S. Wong
1Sir William Dunn School of Pathology, University of Oxford, Oxford, UK
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Felix Y. Zhou
2Ludwig Institute for Cancer Research, University of Oxford, Oxford, UK
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Michael A. Boemo
1Sir William Dunn School of Pathology, University of Oxford, Oxford, UK
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  • For correspondence: mustafa.aydogan@path.ox.ac.uk michael.boemo@path.ox.ac.uk jordan.raff@path.ox.ac.uk
Jordan W. Raff
1Sir William Dunn School of Pathology, University of Oxford, Oxford, UK
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  • For correspondence: mustafa.aydogan@path.ox.ac.uk michael.boemo@path.ox.ac.uk jordan.raff@path.ox.ac.uk
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Summary

The accurate timing and execution of organelle biogenesis is crucial for cell physiology. Centriole biogenesis is regulated by Polo-like kinase 4 (Plk4) and initiates in S-phase when a daughter centriole grows from the side of a preexisting mother. Here we show that Plk4 forms an adaptive oscillator at the base of the growing centriole to initiate and time centriole biogenesis, ensuring that centrioles grow at the right time and to the right size. The Plk4 oscillator is normally entrained to the cell-cycle oscillator, but can run autonomously of it – explaining how centrioles can duplicate independently of cell cycle progression under certain conditions. Mathematical modelling indicates that this autonomously oscillating system is generated by a time-delayed negative-feedback loop in which Plk4 inactivates its centriolar receptor through multiple rounds of phosphorylation. We postulate that such organelle-specific autonomous oscillators could regulate the timing and execution of organelle biogenesis more generally.

Footnotes

  • ↵4 Lead contact

  • Abbreviations and symbols

    A
    Amplitude
    T
    Full width at half maximum
    Ω
    Area under the curve
    CCO
    Cdk-cyclin oscillator
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    Posted March 18, 2019.
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    An autonomous oscillator times and executes centriole biogenesis
    Mustafa G. Aydogan, Thomas L. Steinacker, Mohammad Mofatteh, Lisa Gartenmann, Alan Wainman, Saroj Saurya, Siu S. Wong, Felix Y. Zhou, Michael A. Boemo, Jordan W. Raff
    bioRxiv 510875; doi: https://doi.org/10.1101/510875
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    An autonomous oscillator times and executes centriole biogenesis
    Mustafa G. Aydogan, Thomas L. Steinacker, Mohammad Mofatteh, Lisa Gartenmann, Alan Wainman, Saroj Saurya, Siu S. Wong, Felix Y. Zhou, Michael A. Boemo, Jordan W. Raff
    bioRxiv 510875; doi: https://doi.org/10.1101/510875

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