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

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 i...

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Veröffentlicht in:Genes to cells : devoted to molecular & cellular mechanisms 2017-06, Vol.22 (6), p.552-567
Hauptverfasser: Miyazaki, Seira, Kim, Jihye, Yamagishi, Yuya, Ishiguro, Tadashi, Okada, Yuki, Tanno, Yuji, Sakuno, Takeshi, Watanabe, Yoshinori
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container_title Genes to cells : devoted to molecular & cellular mechanisms
container_volume 22
creator Miyazaki, Seira
Kim, Jihye
Yamagishi, Yuya
Ishiguro, Tadashi
Okada, Yuki
Tanno, Yuji
Sakuno, Takeshi
Watanabe, Yoshinori
description 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.
doi_str_mv 10.1111/gtc.12496
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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. 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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.</abstract><cop>England</cop><pub>Wiley Subscription Services, Inc</pub><pmid>28497540</pmid><doi>10.1111/gtc.12496</doi><tpages>16</tpages><orcidid>https://orcid.org/0000-0002-5488-4812</orcidid><oa>free_for_read</oa></addata></record>
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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
title Meikin‐associated polo‐like kinase specifies Bub1 distribution in meiosis I
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