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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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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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.</description><identifier>ISSN: 1356-9597</identifier><identifier>EISSN: 1365-2443</identifier><identifier>DOI: 10.1111/gtc.12496</identifier><identifier>PMID: 28497540</identifier><language>eng</language><publisher>England: Wiley Subscription Services, Inc</publisher><subject>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</subject><ispartof>Genes to cells : devoted to molecular & cellular mechanisms, 2017-06, Vol.22 (6), p.552-567</ispartof><rights>2017 Molecular Biology Society of Japan and John Wiley & Sons Australia, Ltd</rights><rights>2017 Molecular Biology Society of Japan and John Wiley & Sons Australia, Ltd.</rights><rights>Copyright © 2017 Molecular Biology Society of Japan and John Wiley & Sons Australia, Ltd</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4546-7c643d80e666ab8dc329b051b371c2cb0836b4b36c2dc7af8af99cefb7462bd83</citedby><cites>FETCH-LOGICAL-c4546-7c643d80e666ab8dc329b051b371c2cb0836b4b36c2dc7af8af99cefb7462bd83</cites><orcidid>0000-0002-5488-4812</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fgtc.12496$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fgtc.12496$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>315,781,785,1418,1434,27925,27926,45575,45576,46410,46834</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28497540$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Miyazaki, Seira</creatorcontrib><creatorcontrib>Kim, Jihye</creatorcontrib><creatorcontrib>Yamagishi, Yuya</creatorcontrib><creatorcontrib>Ishiguro, Tadashi</creatorcontrib><creatorcontrib>Okada, Yuki</creatorcontrib><creatorcontrib>Tanno, Yuji</creatorcontrib><creatorcontrib>Sakuno, Takeshi</creatorcontrib><creatorcontrib>Watanabe, Yoshinori</creatorcontrib><title>Meikin‐associated polo‐like kinase specifies Bub1 distribution in meiosis I</title><title>Genes to cells : devoted to molecular & cellular mechanisms</title><addtitle>Genes Cells</addtitle><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.</description><subject>Anaphase</subject><subject>Animals</subject><subject>Cell Adhesion</subject><subject>Cell Cycle Proteins - metabolism</subject><subject>Cells, Cultured</subject><subject>Centromere - genetics</subject><subject>Centromere - metabolism</subject><subject>Centromeres</subject><subject>Chromatids</subject><subject>Chromatin</subject><subject>Chromosomal Proteins, Non-Histone - metabolism</subject><subject>Chromosomal Proteins, Non-Histone - physiology</subject><subject>Cohesin</subject><subject>Gene Expression Regulation, Fungal</subject><subject>Heterochromatin</subject><subject>Histone H2A</subject><subject>Kinetochores</subject><subject>Localization</subject><subject>Male</subject><subject>Meiosis</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Mice, Knockout</subject><subject>Microtubules</subject><subject>Microtubules - metabolism</subject><subject>Molecular modelling</subject><subject>Phosphorylation</subject><subject>Polo-like kinase</subject><subject>Polo-Like Kinase 1</subject><subject>Protein Serine-Threonine Kinases - metabolism</subject><subject>Proto-Oncogene Proteins - metabolism</subject><subject>Schizosaccharomyces - cytology</subject><subject>Schizosaccharomyces - growth & development</subject><subject>Schizosaccharomyces - metabolism</subject><subject>Schizosaccharomyces pombe Proteins - metabolism</subject><subject>Separase</subject><subject>Sister chromatids</subject><subject>Spermatocytes - cytology</subject><subject>Spermatocytes - metabolism</subject><issn>1356-9597</issn><issn>1365-2443</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kL9OwzAQhy0EoqUw8AIoEgsMae34T-wRKiiVQF3KbNmOg9wmcYkToW48As_Ik5CSwoDELXe6-_Tp9APgHMEx6mry0pgxSohgB2CIMKNxQgg-3M2UxYKKdABOQlhBiHAC6TEYJJyIlBI4BIsn69au-nz_UCF441Rjs2jjC99tCre2UXdUwUZhY43LnQ3RbatRlLnQ1E63jfNV5KqotM4HF6L5KTjKVRHs2b6PwPP93XL6ED8uZvPpzWNsCCUsTg0jOOPQMsaU5pnBidCQIo1TZBKjIcdME42ZSTKTqpyrXAhjc50SluiM4xG46r2b2r-2NjSydMHYolCV9W2QiAuBEBV8h17-QVe-ravuO4kE5ExwKERHXfeUqX0Itc3lpnalqrcSQblLWXYpy--UO_Zib2x1abNf8ifWDpj0wJsr7PZ_k5wtp73yC0nKh9g</recordid><startdate>201706</startdate><enddate>201706</enddate><creator>Miyazaki, Seira</creator><creator>Kim, Jihye</creator><creator>Yamagishi, Yuya</creator><creator>Ishiguro, Tadashi</creator><creator>Okada, Yuki</creator><creator>Tanno, Yuji</creator><creator>Sakuno, Takeshi</creator><creator>Watanabe, Yoshinori</creator><general>Wiley Subscription Services, Inc</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7TK</scope><scope>7TM</scope><scope>8FD</scope><scope>FR3</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-5488-4812</orcidid></search><sort><creationdate>201706</creationdate><title>Meikin‐associated polo‐like kinase specifies Bub1 distribution in meiosis I</title><author>Miyazaki, Seira ; Kim, Jihye ; Yamagishi, Yuya ; Ishiguro, Tadashi ; Okada, Yuki ; Tanno, Yuji ; Sakuno, Takeshi ; Watanabe, Yoshinori</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4546-7c643d80e666ab8dc329b051b371c2cb0836b4b36c2dc7af8af99cefb7462bd83</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Anaphase</topic><topic>Animals</topic><topic>Cell Adhesion</topic><topic>Cell Cycle Proteins - metabolism</topic><topic>Cells, Cultured</topic><topic>Centromere - genetics</topic><topic>Centromere - metabolism</topic><topic>Centromeres</topic><topic>Chromatids</topic><topic>Chromatin</topic><topic>Chromosomal Proteins, Non-Histone - metabolism</topic><topic>Chromosomal Proteins, Non-Histone - physiology</topic><topic>Cohesin</topic><topic>Gene Expression Regulation, Fungal</topic><topic>Heterochromatin</topic><topic>Histone H2A</topic><topic>Kinetochores</topic><topic>Localization</topic><topic>Male</topic><topic>Meiosis</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>Mice, Knockout</topic><topic>Microtubules</topic><topic>Microtubules - metabolism</topic><topic>Molecular modelling</topic><topic>Phosphorylation</topic><topic>Polo-like kinase</topic><topic>Polo-Like Kinase 1</topic><topic>Protein Serine-Threonine Kinases - metabolism</topic><topic>Proto-Oncogene Proteins - metabolism</topic><topic>Schizosaccharomyces - cytology</topic><topic>Schizosaccharomyces - growth & development</topic><topic>Schizosaccharomyces - metabolism</topic><topic>Schizosaccharomyces pombe Proteins - metabolism</topic><topic>Separase</topic><topic>Sister chromatids</topic><topic>Spermatocytes - cytology</topic><topic>Spermatocytes - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Miyazaki, Seira</creatorcontrib><creatorcontrib>Kim, Jihye</creatorcontrib><creatorcontrib>Yamagishi, Yuya</creatorcontrib><creatorcontrib>Ishiguro, Tadashi</creatorcontrib><creatorcontrib>Okada, Yuki</creatorcontrib><creatorcontrib>Tanno, Yuji</creatorcontrib><creatorcontrib>Sakuno, Takeshi</creatorcontrib><creatorcontrib>Watanabe, Yoshinori</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Genes to cells : devoted to molecular & cellular mechanisms</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Miyazaki, Seira</au><au>Kim, Jihye</au><au>Yamagishi, Yuya</au><au>Ishiguro, Tadashi</au><au>Okada, Yuki</au><au>Tanno, Yuji</au><au>Sakuno, Takeshi</au><au>Watanabe, Yoshinori</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Meikin‐associated polo‐like kinase specifies Bub1 distribution in meiosis I</atitle><jtitle>Genes to cells : devoted to molecular & cellular mechanisms</jtitle><addtitle>Genes Cells</addtitle><date>2017-06</date><risdate>2017</risdate><volume>22</volume><issue>6</issue><spage>552</spage><epage>567</epage><pages>552-567</pages><issn>1356-9597</issn><eissn>1365-2443</eissn><abstract>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.</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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