Cell cycle control of centromeric repeat transcription and heterochromatin assembly
Heterochromatin in eukaryotic genomes regulates diverse chromosomal processes including transcriptional silencing. However, in Schizosaccharomyces pombe RNA polymerase II (RNAPII) transcription of centromeric repeats is essential for RNA-interference-mediated heterochromatin assembly. Here we study...
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description | Heterochromatin in eukaryotic genomes regulates diverse chromosomal processes including transcriptional silencing. However, in Schizosaccharomyces pombe RNA polymerase II (RNAPII) transcription of centromeric repeats is essential for RNA-interference-mediated heterochromatin assembly. Here we study heterochromatin dynamics during the cell cycle and its effect on RNAPII transcription. We describe a brief period during the S phase of the cell cycle in which RNAPII preferentially transcribes centromeric repeats. This period is enforced by heterochromatin, which restricts RNAPII accessibility at centromeric repeats for most of the cell cycle. RNAPII transcription during S phase is linked to loading of RNA interference and heterochromatin factors such as the Ago1 subunit of the RITS complex and the Clr4 methyltransferase complex subunit Rik1 (ref. 7). Moreover, Set2, an RNAPII-associated methyltransferase that methylates histone H3 lysine 36 at repeat loci during S phase, acts in a pathway parallel to Clr4 to promote heterochromatin assembly. We also show that phosphorylation of histone H3 serine 10 alters heterochromatin during mitosis, correlating with recruitment of condensin that affects silencing of centromeric repeats. Our analyses suggest at least two distinct modes of heterochromatin targeting to centromeric repeats, whereby RNAPII transcription of repeats and chromodomain proteins bound to methylated histone H3 lysine 9 mediate recruitment of silencing factors. Together, these processes probably facilitate heterochromatin maintenance through successive cell divisions. |
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S ; Chen, Ee Sin ; Zhang, Ke ; Nicolas, Estelle ; Cam, Hugh P ; Zofall, Martin</creator><creatorcontrib>Grewal, Shiv I. S ; Chen, Ee Sin ; Zhang, Ke ; Nicolas, Estelle ; Cam, Hugh P ; Zofall, Martin</creatorcontrib><description>Heterochromatin in eukaryotic genomes regulates diverse chromosomal processes including transcriptional silencing. However, in Schizosaccharomyces pombe RNA polymerase II (RNAPII) transcription of centromeric repeats is essential for RNA-interference-mediated heterochromatin assembly. Here we study heterochromatin dynamics during the cell cycle and its effect on RNAPII transcription. We describe a brief period during the S phase of the cell cycle in which RNAPII preferentially transcribes centromeric repeats. This period is enforced by heterochromatin, which restricts RNAPII accessibility at centromeric repeats for most of the cell cycle. RNAPII transcription during S phase is linked to loading of RNA interference and heterochromatin factors such as the Ago1 subunit of the RITS complex and the Clr4 methyltransferase complex subunit Rik1 (ref. 7). Moreover, Set2, an RNAPII-associated methyltransferase that methylates histone H3 lysine 36 at repeat loci during S phase, acts in a pathway parallel to Clr4 to promote heterochromatin assembly. We also show that phosphorylation of histone H3 serine 10 alters heterochromatin during mitosis, correlating with recruitment of condensin that affects silencing of centromeric repeats. Our analyses suggest at least two distinct modes of heterochromatin targeting to centromeric repeats, whereby RNAPII transcription of repeats and chromodomain proteins bound to methylated histone H3 lysine 9 mediate recruitment of silencing factors. Together, these processes probably facilitate heterochromatin maintenance through successive cell divisions.</description><identifier>ISSN: 0028-0836</identifier><identifier>EISSN: 1476-4687</identifier><identifier>EISSN: 1476-4679</identifier><identifier>DOI: 10.1038/nature06561</identifier><identifier>PMID: 18216783</identifier><identifier>CODEN: NATUAS</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>Argonaute Proteins ; Biological and medical sciences ; Cell cycle ; Cell Cycle - physiology ; Cell Cycle Proteins - metabolism ; Cell cycle, cell proliferation ; Cell physiology ; Cellular biology ; Centromere - genetics ; Centromeres ; Chemical properties ; Chromatin ; Chromatin Assembly and Disassembly ; Chromosomal Proteins, Non-Histone - metabolism ; Control ; Eukaryotes ; Fundamental and applied biological sciences. Psychology ; Gene Silencing ; Genetic aspects ; Heterochromatin - genetics ; Heterochromatin - metabolism ; Histone-Lysine N-Methyltransferase - metabolism ; Histones - chemistry ; Histones - metabolism ; Humanities and Social Sciences ; letter ; Life Sciences ; Methylation ; Methyltransferases - metabolism ; Molecular and cellular biology ; multidisciplinary ; Phosphorylation ; Ribonucleic acid ; RNA ; RNA Polymerase II - metabolism ; RNA-Binding Proteins ; S Phase ; Schizosaccharomyces - cytology ; Schizosaccharomyces - enzymology ; Schizosaccharomyces - genetics ; Schizosaccharomyces pombe ; Schizosaccharomyces pombe Proteins - metabolism ; Science ; Science (multidisciplinary) ; Structure ; Transcription, Genetic</subject><ispartof>Nature, 2008-02, Vol.451 (7179), p.734-737</ispartof><rights>Springer Nature Limited 2008</rights><rights>2008 INIST-CNRS</rights><rights>COPYRIGHT 2008 Nature Publishing Group</rights><rights>Copyright Nature Publishing Group Feb 7, 2008</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c850t-7ee213921c20cd17b876be05399f4cd10af957d88ec1958f3de7eb8d059a68ac3</citedby><cites>FETCH-LOGICAL-c850t-7ee213921c20cd17b876be05399f4cd10af957d88ec1958f3de7eb8d059a68ac3</cites><orcidid>0000-0003-0412-8477</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1038/nature06561$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1038/nature06561$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>230,314,778,782,883,27907,27908,41471,42540,51302</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=20037382$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/18216783$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-04297993$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Grewal, Shiv I. S</creatorcontrib><creatorcontrib>Chen, Ee Sin</creatorcontrib><creatorcontrib>Zhang, Ke</creatorcontrib><creatorcontrib>Nicolas, Estelle</creatorcontrib><creatorcontrib>Cam, Hugh P</creatorcontrib><creatorcontrib>Zofall, Martin</creatorcontrib><title>Cell cycle control of centromeric repeat transcription and heterochromatin assembly</title><title>Nature</title><addtitle>Nature</addtitle><addtitle>Nature</addtitle><description>Heterochromatin in eukaryotic genomes regulates diverse chromosomal processes including transcriptional silencing. However, in Schizosaccharomyces pombe RNA polymerase II (RNAPII) transcription of centromeric repeats is essential for RNA-interference-mediated heterochromatin assembly. Here we study heterochromatin dynamics during the cell cycle and its effect on RNAPII transcription. We describe a brief period during the S phase of the cell cycle in which RNAPII preferentially transcribes centromeric repeats. This period is enforced by heterochromatin, which restricts RNAPII accessibility at centromeric repeats for most of the cell cycle. RNAPII transcription during S phase is linked to loading of RNA interference and heterochromatin factors such as the Ago1 subunit of the RITS complex and the Clr4 methyltransferase complex subunit Rik1 (ref. 7). Moreover, Set2, an RNAPII-associated methyltransferase that methylates histone H3 lysine 36 at repeat loci during S phase, acts in a pathway parallel to Clr4 to promote heterochromatin assembly. We also show that phosphorylation of histone H3 serine 10 alters heterochromatin during mitosis, correlating with recruitment of condensin that affects silencing of centromeric repeats. Our analyses suggest at least two distinct modes of heterochromatin targeting to centromeric repeats, whereby RNAPII transcription of repeats and chromodomain proteins bound to methylated histone H3 lysine 9 mediate recruitment of silencing factors. Together, these processes probably facilitate heterochromatin maintenance through successive cell divisions.</description><subject>Argonaute Proteins</subject><subject>Biological and medical sciences</subject><subject>Cell cycle</subject><subject>Cell Cycle - physiology</subject><subject>Cell Cycle Proteins - metabolism</subject><subject>Cell cycle, cell proliferation</subject><subject>Cell physiology</subject><subject>Cellular biology</subject><subject>Centromere - genetics</subject><subject>Centromeres</subject><subject>Chemical properties</subject><subject>Chromatin</subject><subject>Chromatin Assembly and Disassembly</subject><subject>Chromosomal Proteins, Non-Histone - metabolism</subject><subject>Control</subject><subject>Eukaryotes</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Gene Silencing</subject><subject>Genetic aspects</subject><subject>Heterochromatin - genetics</subject><subject>Heterochromatin - metabolism</subject><subject>Histone-Lysine N-Methyltransferase - metabolism</subject><subject>Histones - chemistry</subject><subject>Histones - metabolism</subject><subject>Humanities and Social Sciences</subject><subject>letter</subject><subject>Life Sciences</subject><subject>Methylation</subject><subject>Methyltransferases - metabolism</subject><subject>Molecular and cellular biology</subject><subject>multidisciplinary</subject><subject>Phosphorylation</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>RNA Polymerase II - metabolism</subject><subject>RNA-Binding Proteins</subject><subject>S Phase</subject><subject>Schizosaccharomyces - cytology</subject><subject>Schizosaccharomyces - enzymology</subject><subject>Schizosaccharomyces - genetics</subject><subject>Schizosaccharomyces pombe</subject><subject>Schizosaccharomyces pombe Proteins - metabolism</subject><subject>Science</subject><subject>Science (multidisciplinary)</subject><subject>Structure</subject><subject>Transcription, Genetic</subject><issn>0028-0836</issn><issn>1476-4687</issn><issn>1476-4679</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2008</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>8G5</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>GUQSH</sourceid><sourceid>M2O</sourceid><recordid>eNqN081v0zAUAPAIgdgYnLijgATSBBl2nPjjWFXAJlUgsSGOluu8tJ4Su7MTRP97XKVqU9RpUw6JXn5-tp_9kuQ1RhcYEf7Zqq73gGhJ8ZPkFBeMZgXl7GlyilDOM8QJPUlehHCLECoxK54nJ5jnmDJOTpPrKTRNqte6gVQ723nXpK5ONWw-W_BGpx5WoLq088oG7c2qM86mylbpEjrwTi8jVJ2JsRCgnTfrl8mzWjUBXm3fZ8mvr19uppfZ7Me3q-lklmleoi5jADkmIsc6R7rCbM4ZnQMqiRB1EQNI1aJkFeegsSh5TSpgMOcVKoWiXGlylpwPeZeqkStvWuXX0ikjLyczuYmhIhdMCPIHR_thsCvv7noInWxN0HHvyoLrg2QoZ1Qg-iDEIhY31jXCd__BW9d7Gzcsc1QUjJFig7IBLVQD0tjaxTLqBVjwqnEWahPDEyxIPLVC0Md6LljB8xLtF3Hg9crcyXHS-9Eo08URFJ8KWqOPLvVxA0YznB8M2Fw3-NstVB-CvLr-eZj8QTvK-_F-O7n5Pf1-mHmrtXcheKh3NwcjueknOeqnqN9sD7mft1Dt7baBIni_BSpo1dSxSbQJO5cjRBjheXSfBhfiL7sAv78tx-d9O_AhuMs3Nv8AjV48uA</recordid><startdate>20080207</startdate><enddate>20080207</enddate><creator>Grewal, Shiv I. 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S ; Chen, Ee Sin ; Zhang, Ke ; Nicolas, Estelle ; Cam, Hugh P ; Zofall, Martin</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c850t-7ee213921c20cd17b876be05399f4cd10af957d88ec1958f3de7eb8d059a68ac3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2008</creationdate><topic>Argonaute Proteins</topic><topic>Biological and medical sciences</topic><topic>Cell cycle</topic><topic>Cell Cycle - physiology</topic><topic>Cell Cycle Proteins - metabolism</topic><topic>Cell cycle, cell proliferation</topic><topic>Cell physiology</topic><topic>Cellular biology</topic><topic>Centromere - genetics</topic><topic>Centromeres</topic><topic>Chemical properties</topic><topic>Chromatin</topic><topic>Chromatin Assembly and Disassembly</topic><topic>Chromosomal Proteins, Non-Histone - metabolism</topic><topic>Control</topic><topic>Eukaryotes</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Gene Silencing</topic><topic>Genetic aspects</topic><topic>Heterochromatin - genetics</topic><topic>Heterochromatin - metabolism</topic><topic>Histone-Lysine N-Methyltransferase - metabolism</topic><topic>Histones - chemistry</topic><topic>Histones - metabolism</topic><topic>Humanities and Social Sciences</topic><topic>letter</topic><topic>Life Sciences</topic><topic>Methylation</topic><topic>Methyltransferases - metabolism</topic><topic>Molecular and cellular biology</topic><topic>multidisciplinary</topic><topic>Phosphorylation</topic><topic>Ribonucleic acid</topic><topic>RNA</topic><topic>RNA Polymerase II - metabolism</topic><topic>RNA-Binding Proteins</topic><topic>S Phase</topic><topic>Schizosaccharomyces - cytology</topic><topic>Schizosaccharomyces - enzymology</topic><topic>Schizosaccharomyces - genetics</topic><topic>Schizosaccharomyces pombe</topic><topic>Schizosaccharomyces pombe Proteins - metabolism</topic><topic>Science</topic><topic>Science (multidisciplinary)</topic><topic>Structure</topic><topic>Transcription, Genetic</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Grewal, Shiv I. 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S</au><au>Chen, Ee Sin</au><au>Zhang, Ke</au><au>Nicolas, Estelle</au><au>Cam, Hugh P</au><au>Zofall, Martin</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Cell cycle control of centromeric repeat transcription and heterochromatin assembly</atitle><jtitle>Nature</jtitle><stitle>Nature</stitle><addtitle>Nature</addtitle><date>2008-02-07</date><risdate>2008</risdate><volume>451</volume><issue>7179</issue><spage>734</spage><epage>737</epage><pages>734-737</pages><issn>0028-0836</issn><eissn>1476-4687</eissn><eissn>1476-4679</eissn><coden>NATUAS</coden><abstract>Heterochromatin in eukaryotic genomes regulates diverse chromosomal processes including transcriptional silencing. However, in Schizosaccharomyces pombe RNA polymerase II (RNAPII) transcription of centromeric repeats is essential for RNA-interference-mediated heterochromatin assembly. Here we study heterochromatin dynamics during the cell cycle and its effect on RNAPII transcription. We describe a brief period during the S phase of the cell cycle in which RNAPII preferentially transcribes centromeric repeats. This period is enforced by heterochromatin, which restricts RNAPII accessibility at centromeric repeats for most of the cell cycle. RNAPII transcription during S phase is linked to loading of RNA interference and heterochromatin factors such as the Ago1 subunit of the RITS complex and the Clr4 methyltransferase complex subunit Rik1 (ref. 7). Moreover, Set2, an RNAPII-associated methyltransferase that methylates histone H3 lysine 36 at repeat loci during S phase, acts in a pathway parallel to Clr4 to promote heterochromatin assembly. We also show that phosphorylation of histone H3 serine 10 alters heterochromatin during mitosis, correlating with recruitment of condensin that affects silencing of centromeric repeats. Our analyses suggest at least two distinct modes of heterochromatin targeting to centromeric repeats, whereby RNAPII transcription of repeats and chromodomain proteins bound to methylated histone H3 lysine 9 mediate recruitment of silencing factors. Together, these processes probably facilitate heterochromatin maintenance through successive cell divisions.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>18216783</pmid><doi>10.1038/nature06561</doi><tpages>4</tpages><orcidid>https://orcid.org/0000-0003-0412-8477</orcidid></addata></record> |
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source | MEDLINE; Nature Journals Online; SpringerLink Journals - AutoHoldings |
subjects | Argonaute Proteins Biological and medical sciences Cell cycle Cell Cycle - physiology Cell Cycle Proteins - metabolism Cell cycle, cell proliferation Cell physiology Cellular biology Centromere - genetics Centromeres Chemical properties Chromatin Chromatin Assembly and Disassembly Chromosomal Proteins, Non-Histone - metabolism Control Eukaryotes Fundamental and applied biological sciences. Psychology Gene Silencing Genetic aspects Heterochromatin - genetics Heterochromatin - metabolism Histone-Lysine N-Methyltransferase - metabolism Histones - chemistry Histones - metabolism Humanities and Social Sciences letter Life Sciences Methylation Methyltransferases - metabolism Molecular and cellular biology multidisciplinary Phosphorylation Ribonucleic acid RNA RNA Polymerase II - metabolism RNA-Binding Proteins S Phase Schizosaccharomyces - cytology Schizosaccharomyces - enzymology Schizosaccharomyces - genetics Schizosaccharomyces pombe Schizosaccharomyces pombe Proteins - metabolism Science Science (multidisciplinary) Structure Transcription, Genetic |
title | Cell cycle control of centromeric repeat transcription and heterochromatin assembly |
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