3D genomic architecture reveals that neocentromeres associate with heterochromatin regions
The centromere is an important genomic locus for chromosomal segregation. Although the centromere is specified by sequence-independent epigenetic mechanisms in most organisms, it is usually composed of highly repetitive sequences, which associate with heterochromatin. We have previously generated va...
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Veröffentlicht in: | The Journal of cell biology 2019-01, Vol.218 (1), p.134-149 |
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creator | Nishimura, Kohei Komiya, Masataka Hori, Tetsuya Itoh, Takehiko Fukagawa, Tatsuo |
description | The centromere is an important genomic locus for chromosomal segregation. Although the centromere is specified by sequence-independent epigenetic mechanisms in most organisms, it is usually composed of highly repetitive sequences, which associate with heterochromatin. We have previously generated various chicken DT40 cell lines containing differently positioned neocentromeres, which do not contain repetitive sequences and do not associate with heterochromatin. In this study, we performed systematic 4C analysis using three cell lines containing differently positioned neocentromeres to identify neocentromere-associated regions at the 3D level. This analysis reveals that these neocentromeres commonly associate with specific heterochromatin-rich regions, which were distantly located from neocentromeres. In addition, we demonstrate that centromeric chromatin adopts a compact structure, and centromere clustering also occurs in vertebrate interphase nuclei. Interestingly, the occurrence of centromere-heterochromatin associations depend on CENP-H, but not CENP-C. Our analyses provide an insight into understanding the 3D architecture of the genome, including the centromeres. |
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Although the centromere is specified by sequence-independent epigenetic mechanisms in most organisms, it is usually composed of highly repetitive sequences, which associate with heterochromatin. We have previously generated various chicken DT40 cell lines containing differently positioned neocentromeres, which do not contain repetitive sequences and do not associate with heterochromatin. In this study, we performed systematic 4C analysis using three cell lines containing differently positioned neocentromeres to identify neocentromere-associated regions at the 3D level. This analysis reveals that these neocentromeres commonly associate with specific heterochromatin-rich regions, which were distantly located from neocentromeres. In addition, we demonstrate that centromeric chromatin adopts a compact structure, and centromere clustering also occurs in vertebrate interphase nuclei. Interestingly, the occurrence of centromere-heterochromatin associations depend on CENP-H, but not CENP-C. Our analyses provide an insight into understanding the 3D architecture of the genome, including the centromeres.</description><identifier>ISSN: 0021-9525</identifier><identifier>EISSN: 1540-8140</identifier><identifier>DOI: 10.1083/jcb.201805003</identifier><identifier>PMID: 30396998</identifier><language>eng</language><publisher>United States: Rockefeller University Press</publisher><subject>Animals ; Architecture ; Biotechnology ; Cell Line, Tumor ; Cell lines ; Cellular biology ; Centromere - drug effects ; Centromere - metabolism ; Centromere - ultrastructure ; Centromeres ; Chickens ; Chromatin ; Chromosomal Proteins, Non-Histone - genetics ; Chromosomal Proteins, Non-Histone - metabolism ; Chromosome Segregation - drug effects ; Clustering ; Epigenesis, Genetic ; Epigenetics ; Flow Cytometry ; Genome ; Genomes ; Genomics ; Heterochromatin ; Heterochromatin - drug effects ; Heterochromatin - metabolism ; Heterochromatin - ultrastructure ; Indoleacetic Acids - pharmacology ; Lymphocytes - drug effects ; Lymphocytes - metabolism ; Lymphocytes - ultrastructure ; Methyltransferases - genetics ; Methyltransferases - metabolism ; Poultry ; Protein Isoforms - genetics ; Protein Isoforms - metabolism ; Vertebrates</subject><ispartof>The Journal of cell biology, 2019-01, Vol.218 (1), p.134-149</ispartof><rights>2018 Nishimura et al.</rights><rights>Copyright Rockefeller University Press Jan 2019</rights><rights>2018 Nishimura et al. 2018</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c415t-5ed6171f186e376646b12a9dfad3d50f45577e81b2d1e464ccdbfe6a49774af83</citedby><cites>FETCH-LOGICAL-c415t-5ed6171f186e376646b12a9dfad3d50f45577e81b2d1e464ccdbfe6a49774af83</cites><orcidid>0000-0002-0363-4688 ; 0000-0001-8564-6852</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/30396998$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Nishimura, Kohei</creatorcontrib><creatorcontrib>Komiya, Masataka</creatorcontrib><creatorcontrib>Hori, Tetsuya</creatorcontrib><creatorcontrib>Itoh, Takehiko</creatorcontrib><creatorcontrib>Fukagawa, Tatsuo</creatorcontrib><title>3D genomic architecture reveals that neocentromeres associate with heterochromatin regions</title><title>The Journal of cell biology</title><addtitle>J Cell Biol</addtitle><description>The centromere is an important genomic locus for chromosomal segregation. Although the centromere is specified by sequence-independent epigenetic mechanisms in most organisms, it is usually composed of highly repetitive sequences, which associate with heterochromatin. We have previously generated various chicken DT40 cell lines containing differently positioned neocentromeres, which do not contain repetitive sequences and do not associate with heterochromatin. In this study, we performed systematic 4C analysis using three cell lines containing differently positioned neocentromeres to identify neocentromere-associated regions at the 3D level. This analysis reveals that these neocentromeres commonly associate with specific heterochromatin-rich regions, which were distantly located from neocentromeres. In addition, we demonstrate that centromeric chromatin adopts a compact structure, and centromere clustering also occurs in vertebrate interphase nuclei. Interestingly, the occurrence of centromere-heterochromatin associations depend on CENP-H, but not CENP-C. Our analyses provide an insight into understanding the 3D architecture of the genome, including the centromeres.</description><subject>Animals</subject><subject>Architecture</subject><subject>Biotechnology</subject><subject>Cell Line, Tumor</subject><subject>Cell lines</subject><subject>Cellular biology</subject><subject>Centromere - drug effects</subject><subject>Centromere - metabolism</subject><subject>Centromere - ultrastructure</subject><subject>Centromeres</subject><subject>Chickens</subject><subject>Chromatin</subject><subject>Chromosomal Proteins, Non-Histone - genetics</subject><subject>Chromosomal Proteins, Non-Histone - metabolism</subject><subject>Chromosome Segregation - drug effects</subject><subject>Clustering</subject><subject>Epigenesis, Genetic</subject><subject>Epigenetics</subject><subject>Flow Cytometry</subject><subject>Genome</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Heterochromatin</subject><subject>Heterochromatin - drug effects</subject><subject>Heterochromatin - metabolism</subject><subject>Heterochromatin - ultrastructure</subject><subject>Indoleacetic Acids - pharmacology</subject><subject>Lymphocytes - drug effects</subject><subject>Lymphocytes - metabolism</subject><subject>Lymphocytes - ultrastructure</subject><subject>Methyltransferases - genetics</subject><subject>Methyltransferases - metabolism</subject><subject>Poultry</subject><subject>Protein Isoforms - genetics</subject><subject>Protein Isoforms - metabolism</subject><subject>Vertebrates</subject><issn>0021-9525</issn><issn>1540-8140</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkc1P3DAQxa2qFSwfx16rSL30Ehh_JrkgoaUFJKRe4MLFcpzJxqtNTG0HxH-PKbACTnOY3zy9N4-Q7xSOKNT8eG3bIwa0BgnAv5AFlQLKmgr4ShYAjJaNZHKX7MW4BgBRCb5DdjnwRjVNvSC3_KxY4eRHZwsT7OAS2jQHLALeo9nEIg0mFRN6i1MKfsSAsTAxeutMwuLBpaEYMGHwdshrk9yUT1fOT_GAfOuzAh6-zn1y8-f39fKivPp7frk8vSqtoDKVEjtFK9rTWiGvlBKqpcw0XW863knohZRVhTVtWUdRKGFt1_aojGiqSpi-5vvk5EX3bm5H7P4bNRt9F9xowqP2xumPm8kNeuXvteJUSMGzwK9XgeD_zRiTHl20uNmYnHuOmtH8L1CMVRn9-Qld-zlMOV6mVMOk4vWzo_KFssHHGLDfmqGgn1vTuTW9bS3zP94n2NJvNfEn-VCU8w</recordid><startdate>20190107</startdate><enddate>20190107</enddate><creator>Nishimura, Kohei</creator><creator>Komiya, Masataka</creator><creator>Hori, Tetsuya</creator><creator>Itoh, Takehiko</creator><creator>Fukagawa, Tatsuo</creator><general>Rockefeller University 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>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7TK</scope><scope>7TM</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>5PM</scope><orcidid>https://orcid.org/0000-0002-0363-4688</orcidid><orcidid>https://orcid.org/0000-0001-8564-6852</orcidid></search><sort><creationdate>20190107</creationdate><title>3D genomic architecture reveals that neocentromeres associate with heterochromatin regions</title><author>Nishimura, Kohei ; Komiya, Masataka ; Hori, Tetsuya ; Itoh, Takehiko ; Fukagawa, Tatsuo</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c415t-5ed6171f186e376646b12a9dfad3d50f45577e81b2d1e464ccdbfe6a49774af83</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Animals</topic><topic>Architecture</topic><topic>Biotechnology</topic><topic>Cell Line, Tumor</topic><topic>Cell lines</topic><topic>Cellular biology</topic><topic>Centromere - drug effects</topic><topic>Centromere - metabolism</topic><topic>Centromere - ultrastructure</topic><topic>Centromeres</topic><topic>Chickens</topic><topic>Chromatin</topic><topic>Chromosomal Proteins, Non-Histone - genetics</topic><topic>Chromosomal Proteins, Non-Histone - metabolism</topic><topic>Chromosome Segregation - drug effects</topic><topic>Clustering</topic><topic>Epigenesis, Genetic</topic><topic>Epigenetics</topic><topic>Flow Cytometry</topic><topic>Genome</topic><topic>Genomes</topic><topic>Genomics</topic><topic>Heterochromatin</topic><topic>Heterochromatin - drug effects</topic><topic>Heterochromatin - metabolism</topic><topic>Heterochromatin - ultrastructure</topic><topic>Indoleacetic Acids - pharmacology</topic><topic>Lymphocytes - drug effects</topic><topic>Lymphocytes - metabolism</topic><topic>Lymphocytes - ultrastructure</topic><topic>Methyltransferases - genetics</topic><topic>Methyltransferases - metabolism</topic><topic>Poultry</topic><topic>Protein Isoforms - genetics</topic><topic>Protein Isoforms - metabolism</topic><topic>Vertebrates</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Nishimura, Kohei</creatorcontrib><creatorcontrib>Komiya, Masataka</creatorcontrib><creatorcontrib>Hori, Tetsuya</creatorcontrib><creatorcontrib>Itoh, Takehiko</creatorcontrib><creatorcontrib>Fukagawa, Tatsuo</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Journal of cell biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Nishimura, Kohei</au><au>Komiya, Masataka</au><au>Hori, Tetsuya</au><au>Itoh, Takehiko</au><au>Fukagawa, Tatsuo</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>3D genomic architecture reveals that neocentromeres associate with heterochromatin regions</atitle><jtitle>The Journal of cell biology</jtitle><addtitle>J Cell Biol</addtitle><date>2019-01-07</date><risdate>2019</risdate><volume>218</volume><issue>1</issue><spage>134</spage><epage>149</epage><pages>134-149</pages><issn>0021-9525</issn><eissn>1540-8140</eissn><abstract>The centromere is an important genomic locus for chromosomal segregation. Although the centromere is specified by sequence-independent epigenetic mechanisms in most organisms, it is usually composed of highly repetitive sequences, which associate with heterochromatin. We have previously generated various chicken DT40 cell lines containing differently positioned neocentromeres, which do not contain repetitive sequences and do not associate with heterochromatin. In this study, we performed systematic 4C analysis using three cell lines containing differently positioned neocentromeres to identify neocentromere-associated regions at the 3D level. This analysis reveals that these neocentromeres commonly associate with specific heterochromatin-rich regions, which were distantly located from neocentromeres. In addition, we demonstrate that centromeric chromatin adopts a compact structure, and centromere clustering also occurs in vertebrate interphase nuclei. Interestingly, the occurrence of centromere-heterochromatin associations depend on CENP-H, but not CENP-C. Our analyses provide an insight into understanding the 3D architecture of the genome, including the centromeres.</abstract><cop>United States</cop><pub>Rockefeller University Press</pub><pmid>30396998</pmid><doi>10.1083/jcb.201805003</doi><tpages>16</tpages><orcidid>https://orcid.org/0000-0002-0363-4688</orcidid><orcidid>https://orcid.org/0000-0001-8564-6852</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Animals Architecture Biotechnology Cell Line, Tumor Cell lines Cellular biology Centromere - drug effects Centromere - metabolism Centromere - ultrastructure Centromeres Chickens Chromatin Chromosomal Proteins, Non-Histone - genetics Chromosomal Proteins, Non-Histone - metabolism Chromosome Segregation - drug effects Clustering Epigenesis, Genetic Epigenetics Flow Cytometry Genome Genomes Genomics Heterochromatin Heterochromatin - drug effects Heterochromatin - metabolism Heterochromatin - ultrastructure Indoleacetic Acids - pharmacology Lymphocytes - drug effects Lymphocytes - metabolism Lymphocytes - ultrastructure Methyltransferases - genetics Methyltransferases - metabolism Poultry Protein Isoforms - genetics Protein Isoforms - metabolism Vertebrates |
title | 3D genomic architecture reveals that neocentromeres associate with heterochromatin regions |
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