Asymmetric unwrapping of nucleosomal DNA propagates asymmetric opening and dissociation of the histone core
The nucleosome core particle (NCP) is the basic structural unit for genome packaging in eukaryotic cells and consists of DNA wound around a core of eight histone proteins. DNA access is modulated through dynamic processes of NCP disassembly. Partly disassembled structures, such as the hexasome (cont...
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| Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 2017-01, Vol.114 (2), p.334-339 |
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| creator | Chen, Yujie Tokuda, Joshua M. Topping, Traci Meisburger, Steve P. Pabit, Suzette A. Gloss, Lisa M. Pollack, Lois |
| description | The nucleosome core particle (NCP) is the basic structural unit for genome packaging in eukaryotic cells and consists of DNA wound around a core of eight histone proteins. DNA access is modulated through dynamic processes of NCP disassembly. Partly disassembled structures, such as the hexasome (containing six histones) and the tetrasome (four histones), are important for transcription regulation in vivo. However, the pathways for their formation have been difficult to characterize. We combine time-resolved (TR) small-angle X-ray scattering and TR-FRET to correlate changes in the DNA conformations with composition of the histone core during salt-induced disassembly of canonical NCPs. We find that H2A–H2B histone dimers are released sequentially, with the first dimer being released after the DNA has formed an asymmetrically unwrapped, teardrop-shape DNA structure. This finding suggests that the octasome-to-hexasome transition is guided by the asymmetric unwrapping of the DNA. The link between DNA structure and histone composition suggests a potential mechanism for the action of proteins that alter nucleosome configurations such as histone chaperones and chromatin remodeling complexes. |
| doi_str_mv | 10.1073/pnas.1611118114 |
| format | Article |
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DNA access is modulated through dynamic processes of NCP disassembly. Partly disassembled structures, such as the hexasome (containing six histones) and the tetrasome (four histones), are important for transcription regulation in vivo. However, the pathways for their formation have been difficult to characterize. We combine time-resolved (TR) small-angle X-ray scattering and TR-FRET to correlate changes in the DNA conformations with composition of the histone core during salt-induced disassembly of canonical NCPs. We find that H2A–H2B histone dimers are released sequentially, with the first dimer being released after the DNA has formed an asymmetrically unwrapped, teardrop-shape DNA structure. This finding suggests that the octasome-to-hexasome transition is guided by the asymmetric unwrapping of the DNA. The link between DNA structure and histone composition suggests a potential mechanism for the action of proteins that alter nucleosome configurations such as histone chaperones and chromatin remodeling complexes.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.1611118114</identifier><identifier>PMID: 28028239</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>BASIC BIOLOGICAL SCIENCES ; Biological Sciences ; Chromatin ; contrast variation SAXS ; Correlation analysis ; Deoxyribonucleic acid ; DNA ; Eukaryotes ; FRET ; Genomes ; hexasome ; nucleosomes ; Proteins ; time resolved</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2017-01, Vol.114 (2), p.334-339</ispartof><rights>Volumes 1–89 and 106–113, copyright as a collective work only; author(s) retains copyright to individual articles</rights><rights>Copyright National Academy of Sciences Jan 10, 2017</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c639t-d0d17a4ff59e77b717f85c271335a4cabb65fb607a16faa61dd97b7f5d5500ef3</citedby><cites>FETCH-LOGICAL-c639t-d0d17a4ff59e77b717f85c271335a4cabb65fb607a16faa61dd97b7f5d5500ef3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/26478714$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/26478714$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,723,776,780,799,881,27901,27902,53766,53768,57992,58225</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28028239$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://www.osti.gov/servlets/purl/1340704$$D View this record in Osti.gov$$Hfree_for_read</backlink></links><search><creatorcontrib>Chen, Yujie</creatorcontrib><creatorcontrib>Tokuda, Joshua M.</creatorcontrib><creatorcontrib>Topping, Traci</creatorcontrib><creatorcontrib>Meisburger, Steve P.</creatorcontrib><creatorcontrib>Pabit, Suzette A.</creatorcontrib><creatorcontrib>Gloss, Lisa M.</creatorcontrib><creatorcontrib>Pollack, Lois</creatorcontrib><creatorcontrib>Argonne National Laboratory (ANL), Argonne, IL (United States)</creatorcontrib><title>Asymmetric unwrapping of nucleosomal DNA propagates asymmetric opening and dissociation of the histone core</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>The nucleosome core particle (NCP) is the basic structural unit for genome packaging in eukaryotic cells and consists of DNA wound around a core of eight histone proteins. 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The link between DNA structure and histone composition suggests a potential mechanism for the action of proteins that alter nucleosome configurations such as histone chaperones and chromatin remodeling complexes.</description><subject>BASIC BIOLOGICAL SCIENCES</subject><subject>Biological Sciences</subject><subject>Chromatin</subject><subject>contrast variation SAXS</subject><subject>Correlation analysis</subject><subject>Deoxyribonucleic acid</subject><subject>DNA</subject><subject>Eukaryotes</subject><subject>FRET</subject><subject>Genomes</subject><subject>hexasome</subject><subject>nucleosomes</subject><subject>Proteins</subject><subject>time resolved</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><recordid>eNqNkj2P1DAQhi0E4paDmgoUQUOTu3H8lTRIq-NTOkEDteU49q6XxA62A7p_j6M9boEKNy7mmcea8YvQUwwXGAS5nL1KF5jjclqM6T20wdDhmtMO7qMNQCPqljb0DD1K6QAAHWvhITprWmjahnQb9G2bbqbJ5Oh0tfifUc2z87sq2MovejQhhUmN1ZtP22qOYVY7lU2q1KknzMavDcoP1eBSCtqp7IJfDXlvqr1LOXhT6RDNY_TAqjGZJ7f3Ofr67u2Xqw_19ef3H6-217XmpMv1AAMWilrLOiNEL7CwLdONwIQwRbXqe85sz0EozK1SHA9DVzDLBsYAjCXn6PXROy_9ZAZtfI5qlHN0k4o3Mign_654t5e78EOyhoJo2iJ4cRSElJ1M2mWj9zp4b3SWmBQIaIFe3b4Sw_fFpCwnl7QZR-VNWJLE7aoCSsl_oIwISrngBX35D3oIS_RlXSvVcgDCVuHlkdIxpBSNvRsOg1yDIddgyFMwSsfzP3dyx_9OQgGeHYFD-bB4qnMqWlEEvwA0R7-m</recordid><startdate>20170110</startdate><enddate>20170110</enddate><creator>Chen, Yujie</creator><creator>Tokuda, Joshua M.</creator><creator>Topping, Traci</creator><creator>Meisburger, Steve P.</creator><creator>Pabit, Suzette A.</creator><creator>Gloss, Lisa M.</creator><creator>Pollack, Lois</creator><general>National Academy of Sciences</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>OIOZB</scope><scope>OTOTI</scope><scope>5PM</scope></search><sort><creationdate>20170110</creationdate><title>Asymmetric unwrapping of nucleosomal DNA propagates asymmetric opening and dissociation of the histone core</title><author>Chen, Yujie ; 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| subjects | BASIC BIOLOGICAL SCIENCES Biological Sciences Chromatin contrast variation SAXS Correlation analysis Deoxyribonucleic acid DNA Eukaryotes FRET Genomes hexasome nucleosomes Proteins time resolved |
| title | Asymmetric unwrapping of nucleosomal DNA propagates asymmetric opening and dissociation of the histone core |
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