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Genome accessibility is widely preserved and locally modulated during mitosis
Mitosis entails global alterations to chromosome structure and nuclear architecture, concomitant with transient silencing of transcription. How cells transmit transcriptional states through mitosis remains incompletely understood. While many nuclear factors dissociate from mitotic chromosomes, the o...
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Published in: | Genome research 2015-02, Vol.25 (2), p.213-225 |
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creator | Hsiung, Chris C-S Morrissey, Christapher S Udugama, Maheshi Frank, Christopher L Keller, Cheryl A Baek, Songjoon Giardine, Belinda Crawford, Gregory E Sung, Myong-Hee Hardison, Ross C Blobel, Gerd A |
description | Mitosis entails global alterations to chromosome structure and nuclear architecture, concomitant with transient silencing of transcription. How cells transmit transcriptional states through mitosis remains incompletely understood. While many nuclear factors dissociate from mitotic chromosomes, the observation that certain nuclear factors and chromatin features remain associated with individual loci during mitosis originated the hypothesis that such mitotically retained molecular signatures could provide transcriptional memory through mitosis. To understand the role of chromatin structure in mitotic memory, we performed the first genome-wide comparison of DNase I sensitivity of chromatin in mitosis and interphase, using a murine erythroblast model. Despite chromosome condensation during mitosis visible by microscopy, the landscape of chromatin accessibility at the macromolecular level is largely unaltered. However, mitotic chromatin accessibility is locally dynamic, with individual loci maintaining none, some, or all of their interphase accessibility. Mitotic reduction in accessibility occurs primarily within narrow, highly DNase hypersensitive sites that frequently coincide with transcription factor binding sites, whereas broader domains of moderate accessibility tend to be more stable. In mitosis, proximal promoters generally maintain their accessibility more strongly, whereas distal regulatory elements tend to lose accessibility. Large domains of DNA hypomethylation mark a subset of promoters that retain accessibility during mitosis and across many cell types in interphase. Erythroid transcription factor GATA1 exerts site-specific changes in interphase accessibility that are most pronounced at distal regulatory elements, but has little influence on mitotic accessibility. We conclude that features of open chromatin are remarkably stable through mitosis, but are modulated at the level of individual genes and regulatory elements. |
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How cells transmit transcriptional states through mitosis remains incompletely understood. While many nuclear factors dissociate from mitotic chromosomes, the observation that certain nuclear factors and chromatin features remain associated with individual loci during mitosis originated the hypothesis that such mitotically retained molecular signatures could provide transcriptional memory through mitosis. To understand the role of chromatin structure in mitotic memory, we performed the first genome-wide comparison of DNase I sensitivity of chromatin in mitosis and interphase, using a murine erythroblast model. Despite chromosome condensation during mitosis visible by microscopy, the landscape of chromatin accessibility at the macromolecular level is largely unaltered. However, mitotic chromatin accessibility is locally dynamic, with individual loci maintaining none, some, or all of their interphase accessibility. Mitotic reduction in accessibility occurs primarily within narrow, highly DNase hypersensitive sites that frequently coincide with transcription factor binding sites, whereas broader domains of moderate accessibility tend to be more stable. In mitosis, proximal promoters generally maintain their accessibility more strongly, whereas distal regulatory elements tend to lose accessibility. Large domains of DNA hypomethylation mark a subset of promoters that retain accessibility during mitosis and across many cell types in interphase. Erythroid transcription factor GATA1 exerts site-specific changes in interphase accessibility that are most pronounced at distal regulatory elements, but has little influence on mitotic accessibility. We conclude that features of open chromatin are remarkably stable through mitosis, but are modulated at the level of individual genes and regulatory elements.</description><identifier>ISSN: 1088-9051</identifier><identifier>EISSN: 1549-5469</identifier><identifier>DOI: 10.1101/gr.180646.114</identifier><identifier>PMID: 25373146</identifier><language>eng</language><publisher>United States: Cold Spring Harbor Laboratory Press</publisher><subject>Animals ; Binding Sites ; Cell Cycle - genetics ; Cell Differentiation - genetics ; Chromatin Assembly and Disassembly ; Chromatin Immunoprecipitation ; Chromosomes ; Computational Biology ; Deoxyribonuclease I - metabolism ; DNA Methylation ; Erythroid Cells - cytology ; Erythroid Cells - metabolism ; GATA1 Transcription Factor - metabolism ; Genome ; High-Throughput Nucleotide Sequencing ; Interphase - genetics ; Mice ; Mitosis - drug effects ; Mitosis - genetics ; Promoter Regions, Genetic ; Protein Binding ; Regulatory Sequences, Nucleic Acid ; Transcription Factors - metabolism ; Transcription, Genetic</subject><ispartof>Genome research, 2015-02, Vol.25 (2), p.213-225</ispartof><rights>2015 Hsiung et al.; Published by Cold Spring Harbor Laboratory Press.</rights><rights>2015</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c420t-989f5584d556e4e2607d7259266520044e857a35e207a359eb919afe046979793</citedby><cites>FETCH-LOGICAL-c420t-989f5584d556e4e2607d7259266520044e857a35e207a359eb919afe046979793</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4315295/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4315295/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25373146$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Hsiung, Chris C-S</creatorcontrib><creatorcontrib>Morrissey, Christapher S</creatorcontrib><creatorcontrib>Udugama, Maheshi</creatorcontrib><creatorcontrib>Frank, Christopher L</creatorcontrib><creatorcontrib>Keller, Cheryl A</creatorcontrib><creatorcontrib>Baek, Songjoon</creatorcontrib><creatorcontrib>Giardine, Belinda</creatorcontrib><creatorcontrib>Crawford, Gregory E</creatorcontrib><creatorcontrib>Sung, Myong-Hee</creatorcontrib><creatorcontrib>Hardison, Ross C</creatorcontrib><creatorcontrib>Blobel, Gerd A</creatorcontrib><title>Genome accessibility is widely preserved and locally modulated during mitosis</title><title>Genome research</title><addtitle>Genome Res</addtitle><description>Mitosis entails global alterations to chromosome structure and nuclear architecture, concomitant with transient silencing of transcription. How cells transmit transcriptional states through mitosis remains incompletely understood. While many nuclear factors dissociate from mitotic chromosomes, the observation that certain nuclear factors and chromatin features remain associated with individual loci during mitosis originated the hypothesis that such mitotically retained molecular signatures could provide transcriptional memory through mitosis. To understand the role of chromatin structure in mitotic memory, we performed the first genome-wide comparison of DNase I sensitivity of chromatin in mitosis and interphase, using a murine erythroblast model. Despite chromosome condensation during mitosis visible by microscopy, the landscape of chromatin accessibility at the macromolecular level is largely unaltered. However, mitotic chromatin accessibility is locally dynamic, with individual loci maintaining none, some, or all of their interphase accessibility. Mitotic reduction in accessibility occurs primarily within narrow, highly DNase hypersensitive sites that frequently coincide with transcription factor binding sites, whereas broader domains of moderate accessibility tend to be more stable. In mitosis, proximal promoters generally maintain their accessibility more strongly, whereas distal regulatory elements tend to lose accessibility. Large domains of DNA hypomethylation mark a subset of promoters that retain accessibility during mitosis and across many cell types in interphase. Erythroid transcription factor GATA1 exerts site-specific changes in interphase accessibility that are most pronounced at distal regulatory elements, but has little influence on mitotic accessibility. We conclude that features of open chromatin are remarkably stable through mitosis, but are modulated at the level of individual genes and regulatory elements.</description><subject>Animals</subject><subject>Binding Sites</subject><subject>Cell Cycle - genetics</subject><subject>Cell Differentiation - genetics</subject><subject>Chromatin Assembly and Disassembly</subject><subject>Chromatin Immunoprecipitation</subject><subject>Chromosomes</subject><subject>Computational Biology</subject><subject>Deoxyribonuclease I - metabolism</subject><subject>DNA Methylation</subject><subject>Erythroid Cells - cytology</subject><subject>Erythroid Cells - metabolism</subject><subject>GATA1 Transcription Factor - metabolism</subject><subject>Genome</subject><subject>High-Throughput Nucleotide Sequencing</subject><subject>Interphase - genetics</subject><subject>Mice</subject><subject>Mitosis - drug effects</subject><subject>Mitosis - genetics</subject><subject>Promoter Regions, Genetic</subject><subject>Protein Binding</subject><subject>Regulatory Sequences, Nucleic Acid</subject><subject>Transcription Factors - metabolism</subject><subject>Transcription, Genetic</subject><issn>1088-9051</issn><issn>1549-5469</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><recordid>eNpVUT1PwzAQtRCIlsLIijKypNiO7cQLEqqgIBWxwGy5ySUYOXGxk6L-exwVKtAN9_X03n0gdEnwnBBMbho_JwUWTMSUHaEp4UymnAl5HGNcFKnEnEzQWQgfGOOMFcUpmlCe5RlhYoqel9C5FhJdlhCCWRtr-l1iQvJlKrC7ZOMhgN9CleiuSqwrtY3V1lWD1X2sVoM3XZO0pnfBhHN0Umsb4OLHz9Dbw_3r4jFdvSyfFnertGQU96ksZM15wSrOBTCgAudVTrmkQnCKMWNQ8FxnHCgenYS1JFLXgONaebRshm73vJth3UJVQtd7bdXGm1b7nXLaqP-dzryrxm0VywinkkeC6x8C7z4HCL1qTSjBWt2BG4IiIhfZOMuole6hpXcheKgPMgSr8QWq8Wr_gpiyiL_6O9sB_Xvz7BuMAIH_</recordid><startdate>201502</startdate><enddate>201502</enddate><creator>Hsiung, Chris C-S</creator><creator>Morrissey, Christapher S</creator><creator>Udugama, Maheshi</creator><creator>Frank, Christopher L</creator><creator>Keller, Cheryl A</creator><creator>Baek, Songjoon</creator><creator>Giardine, Belinda</creator><creator>Crawford, Gregory E</creator><creator>Sung, Myong-Hee</creator><creator>Hardison, Ross C</creator><creator>Blobel, Gerd A</creator><general>Cold Spring Harbor Laboratory Press</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>7TM</scope><scope>8FD</scope><scope>FR3</scope><scope>P64</scope><scope>RC3</scope><scope>5PM</scope></search><sort><creationdate>201502</creationdate><title>Genome accessibility is widely preserved and locally modulated during mitosis</title><author>Hsiung, Chris C-S ; Morrissey, Christapher S ; Udugama, Maheshi ; Frank, Christopher L ; Keller, Cheryl A ; Baek, Songjoon ; Giardine, Belinda ; Crawford, Gregory E ; Sung, Myong-Hee ; Hardison, Ross C ; Blobel, Gerd A</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c420t-989f5584d556e4e2607d7259266520044e857a35e207a359eb919afe046979793</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Animals</topic><topic>Binding Sites</topic><topic>Cell Cycle - genetics</topic><topic>Cell Differentiation - genetics</topic><topic>Chromatin Assembly and Disassembly</topic><topic>Chromatin Immunoprecipitation</topic><topic>Chromosomes</topic><topic>Computational Biology</topic><topic>Deoxyribonuclease I - metabolism</topic><topic>DNA Methylation</topic><topic>Erythroid Cells - cytology</topic><topic>Erythroid Cells - metabolism</topic><topic>GATA1 Transcription Factor - metabolism</topic><topic>Genome</topic><topic>High-Throughput Nucleotide Sequencing</topic><topic>Interphase - genetics</topic><topic>Mice</topic><topic>Mitosis - drug effects</topic><topic>Mitosis - genetics</topic><topic>Promoter Regions, Genetic</topic><topic>Protein Binding</topic><topic>Regulatory Sequences, Nucleic Acid</topic><topic>Transcription Factors - metabolism</topic><topic>Transcription, Genetic</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Hsiung, Chris C-S</creatorcontrib><creatorcontrib>Morrissey, Christapher S</creatorcontrib><creatorcontrib>Udugama, Maheshi</creatorcontrib><creatorcontrib>Frank, Christopher L</creatorcontrib><creatorcontrib>Keller, Cheryl A</creatorcontrib><creatorcontrib>Baek, Songjoon</creatorcontrib><creatorcontrib>Giardine, Belinda</creatorcontrib><creatorcontrib>Crawford, Gregory E</creatorcontrib><creatorcontrib>Sung, Myong-Hee</creatorcontrib><creatorcontrib>Hardison, Ross C</creatorcontrib><creatorcontrib>Blobel, Gerd A</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Nucleic Acids Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Genome research</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Hsiung, Chris C-S</au><au>Morrissey, Christapher S</au><au>Udugama, Maheshi</au><au>Frank, Christopher L</au><au>Keller, Cheryl A</au><au>Baek, Songjoon</au><au>Giardine, Belinda</au><au>Crawford, Gregory E</au><au>Sung, Myong-Hee</au><au>Hardison, Ross C</au><au>Blobel, Gerd A</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Genome accessibility is widely preserved and locally modulated during mitosis</atitle><jtitle>Genome research</jtitle><addtitle>Genome Res</addtitle><date>2015-02</date><risdate>2015</risdate><volume>25</volume><issue>2</issue><spage>213</spage><epage>225</epage><pages>213-225</pages><issn>1088-9051</issn><eissn>1549-5469</eissn><abstract>Mitosis entails global alterations to chromosome structure and nuclear architecture, concomitant with transient silencing of transcription. How cells transmit transcriptional states through mitosis remains incompletely understood. While many nuclear factors dissociate from mitotic chromosomes, the observation that certain nuclear factors and chromatin features remain associated with individual loci during mitosis originated the hypothesis that such mitotically retained molecular signatures could provide transcriptional memory through mitosis. To understand the role of chromatin structure in mitotic memory, we performed the first genome-wide comparison of DNase I sensitivity of chromatin in mitosis and interphase, using a murine erythroblast model. Despite chromosome condensation during mitosis visible by microscopy, the landscape of chromatin accessibility at the macromolecular level is largely unaltered. However, mitotic chromatin accessibility is locally dynamic, with individual loci maintaining none, some, or all of their interphase accessibility. Mitotic reduction in accessibility occurs primarily within narrow, highly DNase hypersensitive sites that frequently coincide with transcription factor binding sites, whereas broader domains of moderate accessibility tend to be more stable. In mitosis, proximal promoters generally maintain their accessibility more strongly, whereas distal regulatory elements tend to lose accessibility. Large domains of DNA hypomethylation mark a subset of promoters that retain accessibility during mitosis and across many cell types in interphase. Erythroid transcription factor GATA1 exerts site-specific changes in interphase accessibility that are most pronounced at distal regulatory elements, but has little influence on mitotic accessibility. We conclude that features of open chromatin are remarkably stable through mitosis, but are modulated at the level of individual genes and regulatory elements.</abstract><cop>United States</cop><pub>Cold Spring Harbor Laboratory Press</pub><pmid>25373146</pmid><doi>10.1101/gr.180646.114</doi><tpages>13</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Animals Binding Sites Cell Cycle - genetics Cell Differentiation - genetics Chromatin Assembly and Disassembly Chromatin Immunoprecipitation Chromosomes Computational Biology Deoxyribonuclease I - metabolism DNA Methylation Erythroid Cells - cytology Erythroid Cells - metabolism GATA1 Transcription Factor - metabolism Genome High-Throughput Nucleotide Sequencing Interphase - genetics Mice Mitosis - drug effects Mitosis - genetics Promoter Regions, Genetic Protein Binding Regulatory Sequences, Nucleic Acid Transcription Factors - metabolism Transcription, Genetic |
title | Genome accessibility is widely preserved and locally modulated during mitosis |
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