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Developmentally Regulated Linker Histone H1c Promotes Heterochromatin Condensation and Mediates Structural Integrity of Rod Photoreceptors in Mouse Retina
Mature rod photoreceptor cells contain very small nuclei with tightly condensed heterochromatin. We observed that during mouse rod maturation, the nucleosomal repeat length increases from 190 bp at postnatal day 1 to 206 bp in the adult retina. At the same time, the total level of linker histone H1...
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| Published in: | The Journal of biological chemistry 2013-06, Vol.288 (24), p.17895-17907 |
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| container_title | The Journal of biological chemistry |
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| creator | Popova, Evgenya Y. Grigoryev, Sergei A. Fan, Yuhong Skoultchi, Arthur I. Zhang, Samuel S. Barnstable, Colin J. |
| description | Mature rod photoreceptor cells contain very small nuclei with tightly condensed heterochromatin. We observed that during mouse rod maturation, the nucleosomal repeat length increases from 190 bp at postnatal day 1 to 206 bp in the adult retina. At the same time, the total level of linker histone H1 increased reaching the ratio of 1.3 molecules of total H1 per nucleosome, mostly via a dramatic increase in H1c. Genetic elimination of the histone H1c gene is functionally compensated by other histone variants. However, retinas in H1c/H1e/H10 triple knock-outs have photoreceptors with bigger nuclei, decreased heterochromatin area, and notable morphological changes suggesting that the process of chromatin condensation and rod cell structural integrity are partly impaired. In triple knock-outs, nuclear chromatin exposed several epigenetic histone modification marks masked in the wild type chromatin. Dramatic changes in exposure of a repressive chromatin mark, H3K9me2, indicate that during development linker histone plays a role in establishing the facultative heterochromatin territory and architecture in the nucleus. During retina development, the H1c gene and its promoter acquired epigenetic patterns typical of rod-specific genes. Our data suggest that histone H1c gene expression is developmentally up-regulated to promote facultative heterochromatin in mature rod photoreceptors.
Background: Heterochromatin condenses in the middle of rod cell nuclei during retina maturation.
Results: The level of linker histone H1c increases during retina maturation. Rod photoreceptors in triple H1 knock-out mice have less compact chromatin.
Conclusion: H1c is a key architectural factor for chromatin condensation in the rod photoreceptor.
Significance: Histone H1c expression may be genetically modified to promote rod photoreceptor maturation and retina integrity. |
| doi_str_mv | 10.1074/jbc.M113.452144 |
| format | article |
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Background: Heterochromatin condenses in the middle of rod cell nuclei during retina maturation.
Results: The level of linker histone H1c increases during retina maturation. Rod photoreceptors in triple H1 knock-out mice have less compact chromatin.
Conclusion: H1c is a key architectural factor for chromatin condensation in the rod photoreceptor.
Significance: Histone H1c expression may be genetically modified to promote rod photoreceptor maturation and retina integrity.</description><identifier>ISSN: 0021-9258</identifier><identifier>EISSN: 1083-351X</identifier><identifier>DOI: 10.1074/jbc.M113.452144</identifier><identifier>PMID: 23645681</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Animals ; Cell Nucleus - metabolism ; Chromatin Assembly and Disassembly ; Development ; Developmental Biology ; Epigenesis, Genetic ; Female ; Gene Expression Regulation, Developmental ; Gene Knockout Techniques ; Heterochromatin ; Heterochromatin - metabolism ; Histone H1c ; Histones ; Histones - genetics ; Histones - metabolism ; Mice ; Mice, Inbred C57BL ; Mice, Knockout ; Nucleosomes - metabolism ; Photoreceptors ; Repetitive Sequences, Nucleic Acid - genetics ; Retina ; Retina - cytology ; Retina - growth & development ; Retina Development ; Retinal Rod Photoreceptor Cells - metabolism ; Rod Photoreceptor ; Transcription, Genetic</subject><ispartof>The Journal of biological chemistry, 2013-06, Vol.288 (24), p.17895-17907</ispartof><rights>2013 © 2013 ASBMB. Currently published by Elsevier Inc; originally published by American Society for Biochemistry and Molecular Biology.</rights><rights>2013 by The American Society for Biochemistry and Molecular Biology, Inc. 2013</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c509t-a5288c285f6228f01aaf9bdb98409035786c6eb2e80356e2410d00d29f9458193</citedby><cites>FETCH-LOGICAL-c509t-a5288c285f6228f01aaf9bdb98409035786c6eb2e80356e2410d00d29f9458193</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/PMC3682587/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S0021925820459289$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>230,315,730,783,787,888,3556,27936,27937,45792,53804,53806</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23645681$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Popova, Evgenya Y.</creatorcontrib><creatorcontrib>Grigoryev, Sergei A.</creatorcontrib><creatorcontrib>Fan, Yuhong</creatorcontrib><creatorcontrib>Skoultchi, Arthur I.</creatorcontrib><creatorcontrib>Zhang, Samuel S.</creatorcontrib><creatorcontrib>Barnstable, Colin J.</creatorcontrib><title>Developmentally Regulated Linker Histone H1c Promotes Heterochromatin Condensation and Mediates Structural Integrity of Rod Photoreceptors in Mouse Retina</title><title>The Journal of biological chemistry</title><addtitle>J Biol Chem</addtitle><description>Mature rod photoreceptor cells contain very small nuclei with tightly condensed heterochromatin. We observed that during mouse rod maturation, the nucleosomal repeat length increases from 190 bp at postnatal day 1 to 206 bp in the adult retina. At the same time, the total level of linker histone H1 increased reaching the ratio of 1.3 molecules of total H1 per nucleosome, mostly via a dramatic increase in H1c. Genetic elimination of the histone H1c gene is functionally compensated by other histone variants. However, retinas in H1c/H1e/H10 triple knock-outs have photoreceptors with bigger nuclei, decreased heterochromatin area, and notable morphological changes suggesting that the process of chromatin condensation and rod cell structural integrity are partly impaired. In triple knock-outs, nuclear chromatin exposed several epigenetic histone modification marks masked in the wild type chromatin. Dramatic changes in exposure of a repressive chromatin mark, H3K9me2, indicate that during development linker histone plays a role in establishing the facultative heterochromatin territory and architecture in the nucleus. During retina development, the H1c gene and its promoter acquired epigenetic patterns typical of rod-specific genes. Our data suggest that histone H1c gene expression is developmentally up-regulated to promote facultative heterochromatin in mature rod photoreceptors.
Background: Heterochromatin condenses in the middle of rod cell nuclei during retina maturation.
Results: The level of linker histone H1c increases during retina maturation. Rod photoreceptors in triple H1 knock-out mice have less compact chromatin.
Conclusion: H1c is a key architectural factor for chromatin condensation in the rod photoreceptor.
Significance: Histone H1c expression may be genetically modified to promote rod photoreceptor maturation and retina integrity.</description><subject>Animals</subject><subject>Cell Nucleus - metabolism</subject><subject>Chromatin Assembly and Disassembly</subject><subject>Development</subject><subject>Developmental Biology</subject><subject>Epigenesis, Genetic</subject><subject>Female</subject><subject>Gene Expression Regulation, Developmental</subject><subject>Gene Knockout Techniques</subject><subject>Heterochromatin</subject><subject>Heterochromatin - metabolism</subject><subject>Histone H1c</subject><subject>Histones</subject><subject>Histones - genetics</subject><subject>Histones - metabolism</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Mice, Knockout</subject><subject>Nucleosomes - metabolism</subject><subject>Photoreceptors</subject><subject>Repetitive Sequences, Nucleic Acid - genetics</subject><subject>Retina</subject><subject>Retina - cytology</subject><subject>Retina - growth & development</subject><subject>Retina Development</subject><subject>Retinal Rod Photoreceptor Cells - metabolism</subject><subject>Rod Photoreceptor</subject><subject>Transcription, Genetic</subject><issn>0021-9258</issn><issn>1083-351X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><recordid>eNp1kU-PEyEYxonRuHX17M1w9DJdYJgpXExM_dNN2rhZNfFGGHinZZ2BLjBN-lX8tNJ03ehBLi9v-PHw8jwIvaZkTsmCX911Zr6htJ7zhlHOn6AZJaKu6ob-eIpmhDBaSdaIC_QipTtSFpf0ObpgdcubVtAZ-vUBDjCE_Qg-62E44lvYToPOYPHa-Z8Q8cqlHDzgFTX4JoYxZEh4BRliMLvS6-w8XgZvwaeyDx5rb_EGrNMn8muOk8lT1AO-9hm20eUjDj2-DRbf7EIOEQzsS0m46GzClKDMUDT1S_Ss10OCVw_1En3_9PHbclWtv3y-Xr5fV6YhMle6YUIYJpq-ZUz0hGrdy852UnAiSd0sRGta6BiI0rTAOCWWEMtkL3kjqKwv0buz7n7qRrCmOFGmVfvoRh2PKmin_j3xbqe24aDqVhRvF0Xg7YNADPcTpKxGlwwMg_ZQ_qNo3UpW84bTgl6dURNDShH6x2coUadEVUlUnRJV50TLjTd_T_fI_4mwAPIMQPHo4CCqZBx4UwIo1mZlg_uv-G_ukLO3</recordid><startdate>20130614</startdate><enddate>20130614</enddate><creator>Popova, Evgenya Y.</creator><creator>Grigoryev, Sergei A.</creator><creator>Fan, Yuhong</creator><creator>Skoultchi, Arthur I.</creator><creator>Zhang, Samuel S.</creator><creator>Barnstable, Colin J.</creator><general>Elsevier Inc</general><general>American Society for Biochemistry and Molecular Biology</general><scope>6I.</scope><scope>AAFTH</scope><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>7X8</scope><scope>5PM</scope></search><sort><creationdate>20130614</creationdate><title>Developmentally Regulated Linker Histone H1c Promotes Heterochromatin Condensation and Mediates Structural Integrity of Rod Photoreceptors in Mouse Retina</title><author>Popova, Evgenya Y. ; Grigoryev, Sergei A. ; Fan, Yuhong ; Skoultchi, Arthur I. ; Zhang, Samuel S. ; Barnstable, Colin J.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c509t-a5288c285f6228f01aaf9bdb98409035786c6eb2e80356e2410d00d29f9458193</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Animals</topic><topic>Cell Nucleus - metabolism</topic><topic>Chromatin Assembly and Disassembly</topic><topic>Development</topic><topic>Developmental Biology</topic><topic>Epigenesis, Genetic</topic><topic>Female</topic><topic>Gene Expression Regulation, Developmental</topic><topic>Gene Knockout Techniques</topic><topic>Heterochromatin</topic><topic>Heterochromatin - metabolism</topic><topic>Histone H1c</topic><topic>Histones</topic><topic>Histones - genetics</topic><topic>Histones - metabolism</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>Mice, Knockout</topic><topic>Nucleosomes - metabolism</topic><topic>Photoreceptors</topic><topic>Repetitive Sequences, Nucleic Acid - genetics</topic><topic>Retina</topic><topic>Retina - cytology</topic><topic>Retina - growth & development</topic><topic>Retina Development</topic><topic>Retinal Rod Photoreceptor Cells - metabolism</topic><topic>Rod Photoreceptor</topic><topic>Transcription, Genetic</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Popova, Evgenya Y.</creatorcontrib><creatorcontrib>Grigoryev, Sergei A.</creatorcontrib><creatorcontrib>Fan, Yuhong</creatorcontrib><creatorcontrib>Skoultchi, Arthur I.</creatorcontrib><creatorcontrib>Zhang, Samuel S.</creatorcontrib><creatorcontrib>Barnstable, Colin J.</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Journal of biological chemistry</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Popova, Evgenya Y.</au><au>Grigoryev, Sergei A.</au><au>Fan, Yuhong</au><au>Skoultchi, Arthur I.</au><au>Zhang, Samuel S.</au><au>Barnstable, Colin J.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Developmentally Regulated Linker Histone H1c Promotes Heterochromatin Condensation and Mediates Structural Integrity of Rod Photoreceptors in Mouse Retina</atitle><jtitle>The Journal of biological chemistry</jtitle><addtitle>J Biol Chem</addtitle><date>2013-06-14</date><risdate>2013</risdate><volume>288</volume><issue>24</issue><spage>17895</spage><epage>17907</epage><pages>17895-17907</pages><issn>0021-9258</issn><eissn>1083-351X</eissn><abstract>Mature rod photoreceptor cells contain very small nuclei with tightly condensed heterochromatin. We observed that during mouse rod maturation, the nucleosomal repeat length increases from 190 bp at postnatal day 1 to 206 bp in the adult retina. At the same time, the total level of linker histone H1 increased reaching the ratio of 1.3 molecules of total H1 per nucleosome, mostly via a dramatic increase in H1c. Genetic elimination of the histone H1c gene is functionally compensated by other histone variants. However, retinas in H1c/H1e/H10 triple knock-outs have photoreceptors with bigger nuclei, decreased heterochromatin area, and notable morphological changes suggesting that the process of chromatin condensation and rod cell structural integrity are partly impaired. In triple knock-outs, nuclear chromatin exposed several epigenetic histone modification marks masked in the wild type chromatin. Dramatic changes in exposure of a repressive chromatin mark, H3K9me2, indicate that during development linker histone plays a role in establishing the facultative heterochromatin territory and architecture in the nucleus. During retina development, the H1c gene and its promoter acquired epigenetic patterns typical of rod-specific genes. Our data suggest that histone H1c gene expression is developmentally up-regulated to promote facultative heterochromatin in mature rod photoreceptors.
Background: Heterochromatin condenses in the middle of rod cell nuclei during retina maturation.
Results: The level of linker histone H1c increases during retina maturation. Rod photoreceptors in triple H1 knock-out mice have less compact chromatin.
Conclusion: H1c is a key architectural factor for chromatin condensation in the rod photoreceptor.
Significance: Histone H1c expression may be genetically modified to promote rod photoreceptor maturation and retina integrity.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>23645681</pmid><doi>10.1074/jbc.M113.452144</doi><tpages>13</tpages><oa>free_for_read</oa></addata></record> |
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| source | ScienceDirect; Open Access: PubMed Central |
| subjects | Animals Cell Nucleus - metabolism Chromatin Assembly and Disassembly Development Developmental Biology Epigenesis, Genetic Female Gene Expression Regulation, Developmental Gene Knockout Techniques Heterochromatin Heterochromatin - metabolism Histone H1c Histones Histones - genetics Histones - metabolism Mice Mice, Inbred C57BL Mice, Knockout Nucleosomes - metabolism Photoreceptors Repetitive Sequences, Nucleic Acid - genetics Retina Retina - cytology Retina - growth & development Retina Development Retinal Rod Photoreceptor Cells - metabolism Rod Photoreceptor Transcription, Genetic |
| title | Developmentally Regulated Linker Histone H1c Promotes Heterochromatin Condensation and Mediates Structural Integrity of Rod Photoreceptors in Mouse Retina |
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