Meikin‐associated polo‐like kinase specifies Bub1 distribution in meiosis I

• Published in: Genes to cells : devoted to molecular & cellular mechanisms 2017-06, Vol.22 (6), p.552-567
• Main Authors: Miyazaki, Seira, Kim, Jihye, Yamagishi, Yuya, Ishiguro, Tadashi, Okada, Yuki, Tanno, Yuji, Sakuno, Takeshi, Watanabe, Yoshinori
• Format: Article
• Language: English
• Subjects: Anaphase; Animals; Cell Adhesion; Cell Cycle Proteins - metabolism; Cells, Cultured; Centromere - genetics; Centromere - metabolism; Centromeres; Chromatids; Chromatin; Chromosomal Proteins, Non-Histone - metabolism; Chromosomal Proteins, Non-Histone - physiology; Cohesin; Gene Expression Regulation, Fungal; Heterochromatin; Histone H2A; Kinetochores; Localization; Male; Meiosis; Mice; Mice, Inbred C57BL; Mice, Knockout; Microtubules; Microtubules - metabolism; Molecular modelling; Phosphorylation; Polo-like kinase; Polo-Like Kinase 1; Protein Serine-Threonine Kinases - metabolism; Proto-Oncogene Proteins - metabolism; Schizosaccharomyces - cytology; Schizosaccharomyces - growth & development; Schizosaccharomyces - metabolism; Schizosaccharomyces pombe Proteins - metabolism; Separase; Sister chromatids; Spermatocytes - cytology; Spermatocytes - metabolism
• ISSN: 1356-9597; 1365-2443
• DOI: 10.1111/gtc.12496

In meiosis I, sister chromatids are captured by microtubules emanating from the same pole (mono‐orientation), and centromeric cohesion is protected throughout anaphase. Shugoshin, which is localized to centromeres depending on the phosphorylation of histone H2A by Bub1 kinase, plays a central role in protecting meiotic cohesin Rec8 from separase cleavage. Another key meiotic kinetochore factor, meikin, may regulate cohesion protection, although the underlying molecular mechanisms remain elusive. Here, we show that fission yeast Moa1 (meikin), which associates stably with CENP‐C during meiosis I, recruits Plo1 (polo‐like kinase) to the kinetochores and phosphorylates Spc7 (KNL1) to accumulate Bub1. Consequently, in contrast to the transient kinetochore localization of mitotic Bub1, meiotic Bub1 persists at kinetochores until anaphase I. The meiotic Bub1 pool ensures robust Sgo1 (shugoshin) localization and cohesion protection at centromeres by cooperating with heterochromatin protein Swi6, which binds and stabilizes Sgo1. Furthermore, molecular genetic analyses show a hierarchical regulation of centromeric cohesion protection by meikin and shugoshin that is important for establishing meiosis‐specific chromosome segregation. We provide evidence that the meiosis‐specific Bub1 regulation is conserved in mouse. Fission yeast Moa1 (meikin) recruits Plo1 (polo‐like kinase) to the kinetochores and phosphorylates Spc7 (KNL1) to accumulate Bub1 in meiosis. The meiotic Bub1 pool ensures robust Sgo1 (shugoshin) localization and cohesion protection at centromeres by cooperating with heterochromatin protein Swi6, which binds and stabilizes Sgo1.