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Phospho-regulation of the Shugoshin - Condensin interaction at the centromere in budding yeast

View ORCID ProfileGalal Yahya Metwaly, View ORCID ProfileYehui Wu, Karolina Peplowska, View ORCID ProfileJennifer Röhrl, View ORCID ProfileYoung-Min Soh, View ORCID ProfileFrank Bürmann, View ORCID ProfileStephan Gruber, View ORCID ProfileZuzana Storchova
doi: https://doi.org/10.1101/2019.12.16.877894
Galal Yahya Metwaly
1Department of Molecular Genetics, TU Kaiserlautern, Paul-Ehrlich Str. 24, 67663 Kaiserslautern, Germany
2Department of Microbiology and Immunology School of Pharmacy, Zagazig University, Egypt
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Yehui Wu
3Max Planck Institute of Biochemistry, Am Klopferspitz 18, 82152 Martinsried, Germany
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Karolina Peplowska
3Max Planck Institute of Biochemistry, Am Klopferspitz 18, 82152 Martinsried, Germany
4Genomics and Bioinformatics Shared Resource, University of Hawaii Cancer Center, 701 Ilalo St., Honolulu, HI 96813, USA
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Jennifer Röhrl
3Max Planck Institute of Biochemistry, Am Klopferspitz 18, 82152 Martinsried, Germany
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Young-Min Soh
5Department of Fundamental Microbiology, UNIL-Sorge District, Lausanne, Switzerland
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Frank Bürmann
6MRC Laboratory of Molecular Biology, Francis Crick Avenue, Cambridge CB2 0QH, United Kingdom
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Stephan Gruber
5Department of Fundamental Microbiology, UNIL-Sorge District, Lausanne, Switzerland
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Zuzana Storchova
1Department of Molecular Genetics, TU Kaiserlautern, Paul-Ehrlich Str. 24, 67663 Kaiserslautern, Germany
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  • For correspondence: storchova@bio.uni-kl.de
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Abstract

Correct bioriented attachment of sister chromatids to mitotic spindle is essential for chromosome segregation. The conserved protein shugoshin (Sgo1) contributes in budding yeast to biorientation by recruiting the protein phosphatase PP2A-Rts1 and the condensin complex to centromeres. Using peptide prints, we identified a Serine-Rich Motif (SRM) of Sgo1 that mediates the interaction with condensin and is essential for centromeric condensin recruitment and the establishment of biorientation. We show that the interaction is regulated via phosphorylation within the SRM and we determined the phospho-sites using mass spectrometry. Analysis of the phosphomimicking and phosphoresistant mutants revealed that SRM phosphorylation disrupts the shugoshin – condensin interaction. We present an evidence that Mps1, a central kinase in the spindle assembly checkpoint, directly phosphorylates Sgo1 within the SRM to regulate the interaction with condensin and thereby condensin localization to centromeres. Our findings identify novel mechanisms that control shugoshin activity at the centromere in budding yeast.

Author summary Proper chromosome segregation in eukaryotes is ensured through correct attachment of the spindle microtubules to the centromeric chromosomal regions. The attachment is mediated via the multimolecular proteinaceous complex called kinetochore and precisely regulated. This enables the establishment of so called bioirentation, when each sister chromatid is attached to microtubules emanating from opposite spindle poles. Shugoshin (Sgo1) is a conserved centromeric protein that facilitates biorientation through its interactions with the protein phosphatase PP2A/Rts1, chromosome passanger complex and centromeric condensin. Here, we identified a serin-rich motif that is required for the interaction of shugoshin with the condensin complex. We show that loss of this region impairs condensin enrichment at the centromere, chromosome biorientation, segregation as well as the function of the chromosome passanger complex in the error correction. Moreover, the interaction is phosphoregulated, as phosphorylation of the serin-rich motif on Sgo1 disrupts its interaction with condensin. Finally, we show that the conserved spindle assembly checkpoint kinase Mps1 is responsible for this phosphorylation. Our findings uncover novel regulatory mechanisms that facilitate proper chromosome segregation.

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Posted December 16, 2019.
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Phospho-regulation of the Shugoshin - Condensin interaction at the centromere in budding yeast
Galal Yahya Metwaly, Yehui Wu, Karolina Peplowska, Jennifer Röhrl, Young-Min Soh, Frank Bürmann, Stephan Gruber, Zuzana Storchova
bioRxiv 2019.12.16.877894; doi: https://doi.org/10.1101/2019.12.16.877894
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Phospho-regulation of the Shugoshin - Condensin interaction at the centromere in budding yeast
Galal Yahya Metwaly, Yehui Wu, Karolina Peplowska, Jennifer Röhrl, Young-Min Soh, Frank Bürmann, Stephan Gruber, Zuzana Storchova
bioRxiv 2019.12.16.877894; doi: https://doi.org/10.1101/2019.12.16.877894

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