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An ordered pattern of Ana2 phosphorylation by Plk4 is required for centriole assembly

Tiffany A. McLamarrah, Daniel W. Buster, Brian J. Galletta, Cody J. Boese, John M. Ryniawec, Natalie A. Hollingsworth, Amy E. Byrnes, Christopher W. Brownlee, Kevin C. Slep, Nasser M. Rusan, Gregory C. Rogers
doi: https://doi.org/10.1101/240374
Tiffany A. McLamarrah
1Department of Cellular and Molecular Medicine, University of Arizona Cancer Center, University of Arizona, Tucson, AZ 85724 USA
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Daniel W. Buster
1Department of Cellular and Molecular Medicine, University of Arizona Cancer Center, University of Arizona, Tucson, AZ 85724 USA
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Brian J. Galletta
2National Heart, Lung, and Blood Institute (NHLBI), National Institutes of Health, Bethesda, MD 20892 USA
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Cody J. Boese
1Department of Cellular and Molecular Medicine, University of Arizona Cancer Center, University of Arizona, Tucson, AZ 85724 USA
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John M. Ryniawec
1Department of Cellular and Molecular Medicine, University of Arizona Cancer Center, University of Arizona, Tucson, AZ 85724 USA
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Natalie A. Hollingsworth
1Department of Cellular and Molecular Medicine, University of Arizona Cancer Center, University of Arizona, Tucson, AZ 85724 USA
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Amy E. Byrnes
3Department of Biochemistry and Biophysics, Program in Molecular and Cellular Biophysics, University of North Carolina, Chapel Hill, NC 27599 USA
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Christopher W. Brownlee
1Department of Cellular and Molecular Medicine, University of Arizona Cancer Center, University of Arizona, Tucson, AZ 85724 USA
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Kevin C. Slep
4Department of Biology, CB3280, University of North Carolina, Chapel Hill, NC 27599 USA
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Nasser M. Rusan
2National Heart, Lung, and Blood Institute (NHLBI), National Institutes of Health, Bethesda, MD 20892 USA
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Gregory C. Rogers
1Department of Cellular and Molecular Medicine, University of Arizona Cancer Center, University of Arizona, Tucson, AZ 85724 USA
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  • For correspondence: gcrogers@email.arizona.edu
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Abstract

Polo-like kinase 4 (Plk4) initiates an early step in centriole assembly by phosphorylating Ana2/STIL, a structural component of the procentriole. Here, we show that Plk4 binding to the central coiled-coil (CC) of Ana2 is a conserved event, involving Polo-box 3 and a previously unidentified putative CC located adjacent to the kinase domain. Ana2 binding stimulates Plk4 kinase activity in vitro, and, in turn, is phosphorylated along its length. Previous studies showed that Plk4 phosphorylates the C-terminal STAN domain of Ana2/STIL, triggering binding and recruitment of the cartwheel protein Sas6 to the procentriole assembly site. However, the physiological relevance of N-terminal phosphorylation was unknown. We found that Plk4 first phosphorylates the extreme N–terminus of Ana2 which is critical for subsequent STAN domain modification. Phosphorylation of the central region then breaks the Plk4-Ana2 interaction. This phosphorylation pattern is important for centriole assembly and integrity because replacement of endogenous Ana2 with phospho-Ana2 mutants disrupts distinct steps in Ana2 function and inhibits centriole duplication.

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Posted December 28, 2017.
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An ordered pattern of Ana2 phosphorylation by Plk4 is required for centriole assembly
Tiffany A. McLamarrah, Daniel W. Buster, Brian J. Galletta, Cody J. Boese, John M. Ryniawec, Natalie A. Hollingsworth, Amy E. Byrnes, Christopher W. Brownlee, Kevin C. Slep, Nasser M. Rusan, Gregory C. Rogers
bioRxiv 240374; doi: https://doi.org/10.1101/240374
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An ordered pattern of Ana2 phosphorylation by Plk4 is required for centriole assembly
Tiffany A. McLamarrah, Daniel W. Buster, Brian J. Galletta, Cody J. Boese, John M. Ryniawec, Natalie A. Hollingsworth, Amy E. Byrnes, Christopher W. Brownlee, Kevin C. Slep, Nasser M. Rusan, Gregory C. Rogers
bioRxiv 240374; doi: https://doi.org/10.1101/240374

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