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Dri1 mediates heterochromatin assembly via RNAi and histone deacetylation

Abstract Heterochromatin, a transcriptionally silenced chromatin domain, is important for genome stability and gene expression. Histone 3 lysine 9 methylation (H3K9me) and histone hypoacetylation are conserved epigenetic hallmarks of heterochromatin. In fission yeast, RNA interference (RNAi) plays a...

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Published in:Genetics (Austin) 2021-05, Vol.218 (1)
Main Authors: Ban, Hyoju, Sun, Wenqi, Chen, Yu-hang, Chen, Yong, Li, Fei
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description Abstract Heterochromatin, a transcriptionally silenced chromatin domain, is important for genome stability and gene expression. Histone 3 lysine 9 methylation (H3K9me) and histone hypoacetylation are conserved epigenetic hallmarks of heterochromatin. In fission yeast, RNA interference (RNAi) plays a key role in H3K9 methylation and heterochromatin silencing. However, how RNAi machinery and histone deacetylases (HDACs) are coordinated to ensure proper heterochromatin assembly is still unclear. Previously, we showed that Dpb4, a conserved DNA polymerase epsilon subunit, plays a key role in the recruitment of HDACs to heterochromatin during S phase. Here, we identified a novel RNA-binding protein Dri1 that interacts with Dpb4. GFP-tagged Dri1 forms distinct foci mostly in the nucleus, showing a high degree of colocalization with Swi6/Heterochromatin Protein 1. Deletion of dri1+ leads to defects in silencing, H3K9me, and heterochromatic siRNA generation. We also showed that Dri1 physically associates with heterochromatic transcripts, and is required for the recruitment of the RNA-induced transcriptional silencing (RITS) complex via interacting with the complex. Furthermore, loss of Dri1 decreases the association of the Sir2 HDAC with heterochromatin. We further demonstrated that the C-terminus of Dri1 that includes an intrinsically disordered (IDR) region and three zinc fingers is crucial for its role in silencing. Together, our evidences suggest that Dri1 facilitates heterochromatin assembly via the RNAi pathway and HDAC.
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Histone 3 lysine 9 methylation (H3K9me) and histone hypoacetylation are conserved epigenetic hallmarks of heterochromatin. In fission yeast, RNA interference (RNAi) plays a key role in H3K9 methylation and heterochromatin silencing. However, how RNAi machinery and histone deacetylases (HDACs) are coordinated to ensure proper heterochromatin assembly is still unclear. Previously, we showed that Dpb4, a conserved DNA polymerase epsilon subunit, plays a key role in the recruitment of HDACs to heterochromatin during S phase. Here, we identified a novel RNA-binding protein Dri1 that interacts with Dpb4. GFP-tagged Dri1 forms distinct foci mostly in the nucleus, showing a high degree of colocalization with Swi6/Heterochromatin Protein 1. Deletion of dri1+ leads to defects in silencing, H3K9me, and heterochromatic siRNA generation. We also showed that Dri1 physically associates with heterochromatic transcripts, and is required for the recruitment of the RNA-induced transcriptional silencing (RITS) complex via interacting with the complex. Furthermore, loss of Dri1 decreases the association of the Sir2 HDAC with heterochromatin. We further demonstrated that the C-terminus of Dri1 that includes an intrinsically disordered (IDR) region and three zinc fingers is crucial for its role in silencing. Together, our evidences suggest that Dri1 facilitates heterochromatin assembly via the RNAi pathway and HDAC.</description><identifier>ISSN: 1943-2631</identifier><identifier>ISSN: 0016-6731</identifier><identifier>EISSN: 1943-2631</identifier><identifier>DOI: 10.1093/genetics/iyab032</identifier><identifier>PMID: 33693625</identifier><language>eng</language><publisher>United States: Oxford University Press</publisher><subject>Acetylation ; Assembly ; C-Terminus ; Cell Nucleus - metabolism ; Chromatin ; Chromatin - metabolism ; Chromatin Assembly and Disassembly - genetics ; Chromosomal Proteins, Non-Histone - genetics ; Deacetylation ; DNA methylation ; DNA polymerase ; DNA Polymerase II - metabolism ; DNA-directed DNA polymerase ; Epigenetics ; Gene expression ; Gene silencing ; Genetics ; Genomes ; Heterochromatin ; Heterochromatin - genetics ; Heterochromatin - metabolism ; Heterochromatin protein 1 ; Histone deacetylase ; Histone-Lysine N-Methyltransferase - metabolism ; Histones ; Histones - genetics ; Investigation ; Lysine ; Methylation ; Proteins ; Recruitment ; Ribonucleic acid ; RNA ; RNA Interference ; RNA, Small Interfering - genetics ; RNA-binding protein ; RNA-mediated interference ; S phase ; Schizosaccharomyces - genetics ; Schizosaccharomyces pombe Proteins - genetics ; Schizosaccharomyces pombe Proteins - metabolism ; siRNA ; Yeasts ; Zinc finger proteins</subject><ispartof>Genetics (Austin), 2021-05, Vol.218 (1)</ispartof><rights>The Author(s) 2021. Published by Oxford University Press on behalf of Genetics Society of America. All rights reserved. For permissions, please email: journals.permissions@oup.com 2021</rights><rights>The Author(s) 2021. Published by Oxford University Press on behalf of Genetics Society of America. All rights reserved. For permissions, please email: journals.permissions@oup.com.</rights><rights>The Author(s) 2021. Published by Oxford University Press on behalf of Genetics Society of America. All rights reserved. For permissions, please email: journals.permissions@oup.com</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c526t-b627951a87f055e5b2d341dbc08bc63bb49fb5d3b7093ecd7c4d631f974a39eb3</citedby><cites>FETCH-LOGICAL-c526t-b627951a87f055e5b2d341dbc08bc63bb49fb5d3b7093ecd7c4d631f974a39eb3</cites><orcidid>0000-0001-5857-6086</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33693625$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Freitag, M</contributor><creatorcontrib>Ban, Hyoju</creatorcontrib><creatorcontrib>Sun, Wenqi</creatorcontrib><creatorcontrib>Chen, Yu-hang</creatorcontrib><creatorcontrib>Chen, Yong</creatorcontrib><creatorcontrib>Li, Fei</creatorcontrib><title>Dri1 mediates heterochromatin assembly via RNAi and histone deacetylation</title><title>Genetics (Austin)</title><addtitle>Genetics</addtitle><description>Abstract Heterochromatin, a transcriptionally silenced chromatin domain, is important for genome stability and gene expression. Histone 3 lysine 9 methylation (H3K9me) and histone hypoacetylation are conserved epigenetic hallmarks of heterochromatin. In fission yeast, RNA interference (RNAi) plays a key role in H3K9 methylation and heterochromatin silencing. However, how RNAi machinery and histone deacetylases (HDACs) are coordinated to ensure proper heterochromatin assembly is still unclear. Previously, we showed that Dpb4, a conserved DNA polymerase epsilon subunit, plays a key role in the recruitment of HDACs to heterochromatin during S phase. Here, we identified a novel RNA-binding protein Dri1 that interacts with Dpb4. GFP-tagged Dri1 forms distinct foci mostly in the nucleus, showing a high degree of colocalization with Swi6/Heterochromatin Protein 1. Deletion of dri1+ leads to defects in silencing, H3K9me, and heterochromatic siRNA generation. We also showed that Dri1 physically associates with heterochromatic transcripts, and is required for the recruitment of the RNA-induced transcriptional silencing (RITS) complex via interacting with the complex. Furthermore, loss of Dri1 decreases the association of the Sir2 HDAC with heterochromatin. We further demonstrated that the C-terminus of Dri1 that includes an intrinsically disordered (IDR) region and three zinc fingers is crucial for its role in silencing. Together, our evidences suggest that Dri1 facilitates heterochromatin assembly via the RNAi pathway and HDAC.</description><subject>Acetylation</subject><subject>Assembly</subject><subject>C-Terminus</subject><subject>Cell Nucleus - metabolism</subject><subject>Chromatin</subject><subject>Chromatin - metabolism</subject><subject>Chromatin Assembly and Disassembly - genetics</subject><subject>Chromosomal Proteins, Non-Histone - genetics</subject><subject>Deacetylation</subject><subject>DNA methylation</subject><subject>DNA polymerase</subject><subject>DNA Polymerase II - metabolism</subject><subject>DNA-directed DNA polymerase</subject><subject>Epigenetics</subject><subject>Gene expression</subject><subject>Gene silencing</subject><subject>Genetics</subject><subject>Genomes</subject><subject>Heterochromatin</subject><subject>Heterochromatin - genetics</subject><subject>Heterochromatin - metabolism</subject><subject>Heterochromatin protein 1</subject><subject>Histone deacetylase</subject><subject>Histone-Lysine N-Methyltransferase - metabolism</subject><subject>Histones</subject><subject>Histones - genetics</subject><subject>Investigation</subject><subject>Lysine</subject><subject>Methylation</subject><subject>Proteins</subject><subject>Recruitment</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>RNA Interference</subject><subject>RNA, Small Interfering - genetics</subject><subject>RNA-binding protein</subject><subject>RNA-mediated interference</subject><subject>S phase</subject><subject>Schizosaccharomyces - genetics</subject><subject>Schizosaccharomyces pombe Proteins - genetics</subject><subject>Schizosaccharomyces pombe Proteins - metabolism</subject><subject>siRNA</subject><subject>Yeasts</subject><subject>Zinc finger proteins</subject><issn>1943-2631</issn><issn>0016-6731</issn><issn>1943-2631</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><recordid>eNqFkUtLxDAUhYMovveupOBGkNE8mrbZCOIbREF0HZL01om0yZikwvx7IzOKunF1L9zvHO7hILRH8DHBgp28gINkTTyxc6Uxoytok4iSTWjFyOqPfQNtxfiKMa4Eb9bRBmOVYBXlm-j2IlhSDNBalSAWU0gQvJkGP6hkXaFihEH38-LdquLx_swWyrXF1MbkHRQtKANp3mfUux201qk-wu5ybqPnq8un85vJ3cP17fnZ3cRwWqWJrmgtOFFN3WHOgWvaspK02uBGm4ppXYpO85bpOgcE09ambHOCTtSlYgI020anC9_ZqPPfBlwKqpezYAcV5tIrK39fnJ3KF_8uG0KbEvNscLg0CP5thJjkYKOBvlcO_Bgl5RizmnJCMnrwB331Y3A5XqZqUdOGVThTeEGZ4GMM0H0_Q7D87El-9SSXPWXJ_s8Q34KvYjJwtAD8OPvf7gMOOKHT</recordid><startdate>20210517</startdate><enddate>20210517</enddate><creator>Ban, Hyoju</creator><creator>Sun, Wenqi</creator><creator>Chen, Yu-hang</creator><creator>Chen, Yong</creator><creator>Li, Fei</creator><general>Oxford University Press</general><general>Genetics Society of America</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>4T-</scope><scope>4U-</scope><scope>7QP</scope><scope>7SS</scope><scope>7TK</scope><scope>7TM</scope><scope>8FD</scope><scope>FR3</scope><scope>K9.</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-5857-6086</orcidid></search><sort><creationdate>20210517</creationdate><title>Dri1 mediates heterochromatin assembly via RNAi and histone deacetylation</title><author>Ban, Hyoju ; Sun, Wenqi ; Chen, Yu-hang ; Chen, Yong ; Li, Fei</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c526t-b627951a87f055e5b2d341dbc08bc63bb49fb5d3b7093ecd7c4d631f974a39eb3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Acetylation</topic><topic>Assembly</topic><topic>C-Terminus</topic><topic>Cell Nucleus - metabolism</topic><topic>Chromatin</topic><topic>Chromatin - metabolism</topic><topic>Chromatin Assembly and Disassembly - genetics</topic><topic>Chromosomal Proteins, Non-Histone - genetics</topic><topic>Deacetylation</topic><topic>DNA methylation</topic><topic>DNA polymerase</topic><topic>DNA Polymerase II - metabolism</topic><topic>DNA-directed DNA polymerase</topic><topic>Epigenetics</topic><topic>Gene expression</topic><topic>Gene silencing</topic><topic>Genetics</topic><topic>Genomes</topic><topic>Heterochromatin</topic><topic>Heterochromatin - genetics</topic><topic>Heterochromatin - metabolism</topic><topic>Heterochromatin protein 1</topic><topic>Histone deacetylase</topic><topic>Histone-Lysine N-Methyltransferase - metabolism</topic><topic>Histones</topic><topic>Histones - genetics</topic><topic>Investigation</topic><topic>Lysine</topic><topic>Methylation</topic><topic>Proteins</topic><topic>Recruitment</topic><topic>Ribonucleic acid</topic><topic>RNA</topic><topic>RNA Interference</topic><topic>RNA, Small Interfering - genetics</topic><topic>RNA-binding protein</topic><topic>RNA-mediated interference</topic><topic>S phase</topic><topic>Schizosaccharomyces - genetics</topic><topic>Schizosaccharomyces pombe Proteins - genetics</topic><topic>Schizosaccharomyces pombe Proteins - metabolism</topic><topic>siRNA</topic><topic>Yeasts</topic><topic>Zinc finger proteins</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Ban, Hyoju</creatorcontrib><creatorcontrib>Sun, Wenqi</creatorcontrib><creatorcontrib>Chen, Yu-hang</creatorcontrib><creatorcontrib>Chen, Yong</creatorcontrib><creatorcontrib>Li, Fei</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Docstoc</collection><collection>University Readers</collection><collection>Calcium &amp; 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We also showed that Dri1 physically associates with heterochromatic transcripts, and is required for the recruitment of the RNA-induced transcriptional silencing (RITS) complex via interacting with the complex. Furthermore, loss of Dri1 decreases the association of the Sir2 HDAC with heterochromatin. We further demonstrated that the C-terminus of Dri1 that includes an intrinsically disordered (IDR) region and three zinc fingers is crucial for its role in silencing. Together, our evidences suggest that Dri1 facilitates heterochromatin assembly via the RNAi pathway and HDAC.</abstract><cop>United States</cop><pub>Oxford University Press</pub><pmid>33693625</pmid><doi>10.1093/genetics/iyab032</doi><orcidid>https://orcid.org/0000-0001-5857-6086</orcidid><oa>free_for_read</oa></addata></record>
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source Freely Accessible Science Journals - check A-Z of ejournals; Oxford Journals Online; Alma/SFX Local Collection
subjects Acetylation
Assembly
C-Terminus
Cell Nucleus - metabolism
Chromatin
Chromatin - metabolism
Chromatin Assembly and Disassembly - genetics
Chromosomal Proteins, Non-Histone - genetics
Deacetylation
DNA methylation
DNA polymerase
DNA Polymerase II - metabolism
DNA-directed DNA polymerase
Epigenetics
Gene expression
Gene silencing
Genetics
Genomes
Heterochromatin
Heterochromatin - genetics
Heterochromatin - metabolism
Heterochromatin protein 1
Histone deacetylase
Histone-Lysine N-Methyltransferase - metabolism
Histones
Histones - genetics
Investigation
Lysine
Methylation
Proteins
Recruitment
Ribonucleic acid
RNA
RNA Interference
RNA, Small Interfering - genetics
RNA-binding protein
RNA-mediated interference
S phase
Schizosaccharomyces - genetics
Schizosaccharomyces pombe Proteins - genetics
Schizosaccharomyces pombe Proteins - metabolism
siRNA
Yeasts
Zinc finger proteins
title Dri1 mediates heterochromatin assembly via RNAi and histone deacetylation
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