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The conserved kinetochore protein shugoshin protects centromeric cohesion during meiosis

Naturevolume 427, pages510–517 (2004)Cite this article

Abstract

Meiosis comprises a pair of specialized nuclear divisions that produce haploid germ cells. To accomplish this, sister chromatids must segregate together during the first meiotic division (meiosis I), which requires that sister chromatid cohesion persists at centromeres. The factors that protect centromeric cohesion during meiosis I have remained elusive. Here we identify Sgo1 (shugoshin), a protector of the centromeric cohesin Rec8 in fission yeast. We also identify a homologue of Sgo1 in budding yeast. We provide evidence that shugoshin is widely conserved among eukaryotes. Moreover, we identify Sgo2, a paralogue of shugoshin in fission yeast, which is required for faithful mitotic chromosome segregation. Localization of Sgo1 and Sgo2 at centromeres requires the kinase Bub1, identifying shugoshin as a crucial target for the kinetochore function of Bub1. These findings provide insights into the evolution of meiosis and kinetochore regulation during mitosis and meiosis.

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Figure 1: Co-expression of Sgo1 and Rec8 causes failure of sister chromatid separation during mitosis.
Figure 2: Sgo1 is required to protect Rec8 and thereby cohesion at centromeres during anaphase of meiosis I.
Figure 3: Sgo1 localizes at pericentromeric regions during meiosis I.
Figure 4: Sgo2 has a crucial role in mitotic division at the kinetochore.
Figure 5: Analysis of budding yeast shugoshin ScSgo1.
Figure 6: Alignment of the amino-terminal coiled-coil regions and C-terminal basic regions of shugoshin-like proteins in various organisms.

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Acknowledgements

We thank J. P. Cooper for critical reading of the manuscript; S. Hauf, M. Ohsugi and R. Watanabe for suggestions; J. P. Javerzat, F. Chang, T. Toda, M. Yanagida and P. Nurse for strains and plasmids of fission yeast; and F. Klein, K. P. Rabitsch, K. Nasmyth, M. Longtine, A. Shinohara and T. Maeda for strains and methods of budding yeast. We appreciate the support of M. Yamamoto and all members of his laboratory for their help. This work was supported in part by grants from the Ministry of Education, Science and Culture of Japan.

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Authors and Affiliations

  1. Department of Biophysics and Biochemistry, Graduate School of Science, University of Tokyo, 113-0033, Hongo, Tokyo, Japan

    Tomoya S. Kitajima, Shigehiro A. Kawashima & Yoshinori Watanabe

  2. SORST, Japan Science and Technology Agency, 113-0033, Hongo, Tokyo, Japan

    Yoshinori Watanabe

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  1. Tomoya S. Kitajima

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  2. Shigehiro A. Kawashima

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Correspondence toYoshinori Watanabe.

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Kitajima, T., Kawashima, S. & Watanabe, Y. The conserved kinetochore protein shugoshin protects centromeric cohesion during meiosis.Nature427, 510–517 (2004). https://doi.org/10.1038/nature02312

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