An atlas of transcribed enhancers across helper T cell diversity for decoding human diseases
Transcribed enhancer maps can reveal nuclear interactions underpinning each cell type and connect specific cell types to diseases. Using a 5' single-cell RNA sequencing approach, we defined transcription start sites of enhancer RNAs and other classes of coding and noncoding RNAs in human CD4 T...
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| Veröffentlicht in: | Science (American Association for the Advancement of Science) 2024-07, Vol.385 (6704), p.eadd8394 |
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| creator | Oguchi, Akiko Suzuki, Akari Komatsu, Shuichiro Yoshitomi, Hiroyuki Bhagat, Shruti Son, Raku Bonnal, Raoul Jean Pierre Kojima, Shohei Koido, Masaru Takeuchi, Kazuhiro Myouzen, Keiko Inoue, Gyo Hirai, Tomoya Sano, Hiromi Takegami, Yujiro Kanemaru, Ai Yamaguchi, Itaru Ishikawa, Yuki Tanaka, Nao Hirabayashi, Shigeki Konishi, Riyo Sekito, Sho Inoue, Takahiro Kere, Juha Takeda, Shunichi Takaori-Kondo, Akifumi Endo, Itaru Kawaoka, Shinpei Kawaji, Hideya Ishigaki, Kazuyoshi Ueno, Hideki Hayashizaki, Yoshihide Pagani, Massimiliano Carninci, Piero Yanagita, Motoko Parrish, Nicholas Terao, Chikashi Yamamoto, Kazuhiko Murakawa, Yasuhiro |
| description | Transcribed enhancer maps can reveal nuclear interactions underpinning each cell type and connect specific cell types to diseases. Using a 5' single-cell RNA sequencing approach, we defined transcription start sites of enhancer RNAs and other classes of coding and noncoding RNAs in human CD4
T cells, revealing cellular heterogeneity and differentiation trajectories. Integration of these datasets with single-cell chromatin profiles showed that active enhancers with bidirectional RNA transcription are highly cell type-specific and that disease heritability is strongly enriched in these enhancers. The resulting cell type-resolved multimodal atlas of bidirectionally transcribed enhancers, which we linked with promoters using fine-scale chromatin contact maps, enabled us to systematically interpret genetic variants associated with a range of immune-mediated diseases. |
| doi_str_mv | 10.1126/science.add8394 |
| format | Article |
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T cells, revealing cellular heterogeneity and differentiation trajectories. Integration of these datasets with single-cell chromatin profiles showed that active enhancers with bidirectional RNA transcription are highly cell type-specific and that disease heritability is strongly enriched in these enhancers. The resulting cell type-resolved multimodal atlas of bidirectionally transcribed enhancers, which we linked with promoters using fine-scale chromatin contact maps, enabled us to systematically interpret genetic variants associated with a range of immune-mediated diseases.</description><identifier>ISSN: 0036-8075</identifier><identifier>ISSN: 1095-9203</identifier><identifier>EISSN: 1095-9203</identifier><identifier>DOI: 10.1126/science.add8394</identifier><identifier>PMID: 38963856</identifier><language>eng</language><publisher>United States: The American Association for the Advancement of Science</publisher><subject>Accessibility ; Atlases as Topic ; CD4 antigen ; CD4-Positive T-Lymphocytes - immunology ; Cell activation ; Cell Differentiation ; Chromatin ; Chromatin - genetics ; Chromatin - metabolism ; CRISPR ; Disease ; Enhancer Elements, Genetic ; Enhancers ; Gene expression ; Gene mapping ; Gene regulation ; Gene sequencing ; Genes ; Genetic diversity ; Genetic Predisposition to Disease ; Genetic variance ; Genetics ; Heritability ; Humans ; Immunoregulation ; Lymphocytes ; Lymphocytes T ; Nucleotides ; Promoter Regions, Genetic ; Rare diseases ; Regulatory sequences ; Ribonucleic acid ; RNA ; Single-Cell Gene Expression Analysis ; Single-nucleotide polymorphism ; T-Lymphocytes, Helper-Inducer - immunology ; Transcription ; Transcription activation ; Transcription Initiation Site ; Transcription, Genetic ; Transposase</subject><ispartof>Science (American Association for the Advancement of Science), 2024-07, Vol.385 (6704), p.eadd8394</ispartof><rights>Copyright © 2024 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c317t-dbaf61e9c879f6af1a119bf608dd9ba721259657f0abb705e1d1001cc7196c0c3</cites><orcidid>0000-0002-2123-6536 ; 0000-0002-6971-8016 ; 0000-0003-1974-0271 ; 0000-0002-1646-9167 ; 0000-0002-5343-3681 ; 0000-0003-2881-0657 ; 0000-0002-0561-2802 ; 0000-0002-2085-4682 ; 0000-0002-6452-4095 ; 0000-0001-8082-6301 ; 0000-0002-0575-0308 ; 0000-0002-9948-6295 ; 0000-0002-0339-9008 ; 0000-0001-5520-8114 ; 0000-0002-2457-5824 ; 0000-0002-5415-1352 ; 0000-0002-6514-8239 ; 0000-0001-7747-0738 ; 0000-0002-9250-9474 ; 0000-0001-7678-4284 ; 0000-0003-4064-6781 ; 0000-0001-7339-9030 ; 0000-0002-7017-9304 ; 0000-0002-6764-4818 ; 0000-0002-7918-2403 ; 0000-0001-8586-784X ; 0000-0001-7202-7243 ; 0000-0002-0348-0666 ; 0000-0002-6684-9432 ; 0000-0001-9037-3625</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,776,780,881,2871,2872,27901,27902</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38963856$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttp://kipublications.ki.se/Default.aspx?queryparsed=id:159938013$$DView record from Swedish Publication Index$$Hfree_for_read</backlink></links><search><creatorcontrib>Oguchi, Akiko</creatorcontrib><creatorcontrib>Suzuki, Akari</creatorcontrib><creatorcontrib>Komatsu, Shuichiro</creatorcontrib><creatorcontrib>Yoshitomi, Hiroyuki</creatorcontrib><creatorcontrib>Bhagat, Shruti</creatorcontrib><creatorcontrib>Son, Raku</creatorcontrib><creatorcontrib>Bonnal, Raoul Jean Pierre</creatorcontrib><creatorcontrib>Kojima, Shohei</creatorcontrib><creatorcontrib>Koido, Masaru</creatorcontrib><creatorcontrib>Takeuchi, Kazuhiro</creatorcontrib><creatorcontrib>Myouzen, Keiko</creatorcontrib><creatorcontrib>Inoue, Gyo</creatorcontrib><creatorcontrib>Hirai, Tomoya</creatorcontrib><creatorcontrib>Sano, Hiromi</creatorcontrib><creatorcontrib>Takegami, Yujiro</creatorcontrib><creatorcontrib>Kanemaru, Ai</creatorcontrib><creatorcontrib>Yamaguchi, Itaru</creatorcontrib><creatorcontrib>Ishikawa, Yuki</creatorcontrib><creatorcontrib>Tanaka, Nao</creatorcontrib><creatorcontrib>Hirabayashi, Shigeki</creatorcontrib><creatorcontrib>Konishi, Riyo</creatorcontrib><creatorcontrib>Sekito, Sho</creatorcontrib><creatorcontrib>Inoue, Takahiro</creatorcontrib><creatorcontrib>Kere, Juha</creatorcontrib><creatorcontrib>Takeda, Shunichi</creatorcontrib><creatorcontrib>Takaori-Kondo, Akifumi</creatorcontrib><creatorcontrib>Endo, Itaru</creatorcontrib><creatorcontrib>Kawaoka, Shinpei</creatorcontrib><creatorcontrib>Kawaji, Hideya</creatorcontrib><creatorcontrib>Ishigaki, Kazuyoshi</creatorcontrib><creatorcontrib>Ueno, Hideki</creatorcontrib><creatorcontrib>Hayashizaki, Yoshihide</creatorcontrib><creatorcontrib>Pagani, Massimiliano</creatorcontrib><creatorcontrib>Carninci, Piero</creatorcontrib><creatorcontrib>Yanagita, Motoko</creatorcontrib><creatorcontrib>Parrish, Nicholas</creatorcontrib><creatorcontrib>Terao, Chikashi</creatorcontrib><creatorcontrib>Yamamoto, Kazuhiko</creatorcontrib><creatorcontrib>Murakawa, Yasuhiro</creatorcontrib><creatorcontrib>ITEC Consortium</creatorcontrib><creatorcontrib>ITEC Consortium Members</creatorcontrib><title>An atlas of transcribed enhancers across helper T cell diversity for decoding human diseases</title><title>Science (American Association for the Advancement of Science)</title><addtitle>Science</addtitle><description>Transcribed enhancer maps can reveal nuclear interactions underpinning each cell type and connect specific cell types to diseases. Using a 5' single-cell RNA sequencing approach, we defined transcription start sites of enhancer RNAs and other classes of coding and noncoding RNAs in human CD4
T cells, revealing cellular heterogeneity and differentiation trajectories. Integration of these datasets with single-cell chromatin profiles showed that active enhancers with bidirectional RNA transcription are highly cell type-specific and that disease heritability is strongly enriched in these enhancers. The resulting cell type-resolved multimodal atlas of bidirectionally transcribed enhancers, which we linked with promoters using fine-scale chromatin contact maps, enabled us to systematically interpret genetic variants associated with a range of immune-mediated diseases.</description><subject>Accessibility</subject><subject>Atlases as Topic</subject><subject>CD4 antigen</subject><subject>CD4-Positive T-Lymphocytes - immunology</subject><subject>Cell activation</subject><subject>Cell Differentiation</subject><subject>Chromatin</subject><subject>Chromatin - genetics</subject><subject>Chromatin - metabolism</subject><subject>CRISPR</subject><subject>Disease</subject><subject>Enhancer Elements, Genetic</subject><subject>Enhancers</subject><subject>Gene expression</subject><subject>Gene mapping</subject><subject>Gene regulation</subject><subject>Gene sequencing</subject><subject>Genes</subject><subject>Genetic diversity</subject><subject>Genetic Predisposition to Disease</subject><subject>Genetic variance</subject><subject>Genetics</subject><subject>Heritability</subject><subject>Humans</subject><subject>Immunoregulation</subject><subject>Lymphocytes</subject><subject>Lymphocytes T</subject><subject>Nucleotides</subject><subject>Promoter Regions, Genetic</subject><subject>Rare diseases</subject><subject>Regulatory sequences</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>Single-Cell Gene Expression Analysis</subject><subject>Single-nucleotide polymorphism</subject><subject>T-Lymphocytes, Helper-Inducer - immunology</subject><subject>Transcription</subject><subject>Transcription activation</subject><subject>Transcription Initiation Site</subject><subject>Transcription, 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Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Solid State and Superconductivity Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>METADEX</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ANTE: Abstracts in New Technology & Engineering</collection><collection>Engineering Research Database</collection><collection>Aerospace Database</collection><collection>Copper Technical Reference Library</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Materials Research Database</collection><collection>ProQuest Computer Science Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Civil Engineering Abstracts</collection><collection>Advanced Technologies Database with Aerospace</collection><collection>Computer and Information Systems Abstracts Academic</collection><collection>Computer and Information Systems Abstracts Professional</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>SwePub</collection><collection>SwePub Articles</collection><jtitle>Science (American Association for the Advancement of Science)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Oguchi, Akiko</au><au>Suzuki, Akari</au><au>Komatsu, Shuichiro</au><au>Yoshitomi, Hiroyuki</au><au>Bhagat, Shruti</au><au>Son, Raku</au><au>Bonnal, Raoul Jean Pierre</au><au>Kojima, Shohei</au><au>Koido, Masaru</au><au>Takeuchi, Kazuhiro</au><au>Myouzen, Keiko</au><au>Inoue, Gyo</au><au>Hirai, Tomoya</au><au>Sano, Hiromi</au><au>Takegami, Yujiro</au><au>Kanemaru, Ai</au><au>Yamaguchi, Itaru</au><au>Ishikawa, Yuki</au><au>Tanaka, Nao</au><au>Hirabayashi, Shigeki</au><au>Konishi, Riyo</au><au>Sekito, Sho</au><au>Inoue, Takahiro</au><au>Kere, Juha</au><au>Takeda, Shunichi</au><au>Takaori-Kondo, Akifumi</au><au>Endo, Itaru</au><au>Kawaoka, Shinpei</au><au>Kawaji, Hideya</au><au>Ishigaki, Kazuyoshi</au><au>Ueno, Hideki</au><au>Hayashizaki, Yoshihide</au><au>Pagani, Massimiliano</au><au>Carninci, Piero</au><au>Yanagita, Motoko</au><au>Parrish, Nicholas</au><au>Terao, Chikashi</au><au>Yamamoto, Kazuhiko</au><au>Murakawa, Yasuhiro</au><aucorp>ITEC Consortium</aucorp><aucorp>ITEC Consortium Members</aucorp><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>An atlas of transcribed enhancers across helper T cell diversity for decoding human diseases</atitle><jtitle>Science (American Association for the Advancement of Science)</jtitle><addtitle>Science</addtitle><date>2024-07-05</date><risdate>2024</risdate><volume>385</volume><issue>6704</issue><spage>eadd8394</spage><pages>eadd8394-</pages><issn>0036-8075</issn><issn>1095-9203</issn><eissn>1095-9203</eissn><abstract>Transcribed enhancer maps can reveal nuclear interactions underpinning each cell type and connect specific cell types to diseases. Using a 5' single-cell RNA sequencing approach, we defined transcription start sites of enhancer RNAs and other classes of coding and noncoding RNAs in human CD4
T cells, revealing cellular heterogeneity and differentiation trajectories. Integration of these datasets with single-cell chromatin profiles showed that active enhancers with bidirectional RNA transcription are highly cell type-specific and that disease heritability is strongly enriched in these enhancers. The resulting cell type-resolved multimodal atlas of bidirectionally transcribed enhancers, which we linked with promoters using fine-scale chromatin contact maps, enabled us to systematically interpret genetic variants associated with a range of immune-mediated diseases.</abstract><cop>United States</cop><pub>The American Association for the Advancement of Science</pub><pmid>38963856</pmid><doi>10.1126/science.add8394</doi><orcidid>https://orcid.org/0000-0002-2123-6536</orcidid><orcidid>https://orcid.org/0000-0002-6971-8016</orcidid><orcidid>https://orcid.org/0000-0003-1974-0271</orcidid><orcidid>https://orcid.org/0000-0002-1646-9167</orcidid><orcidid>https://orcid.org/0000-0002-5343-3681</orcidid><orcidid>https://orcid.org/0000-0003-2881-0657</orcidid><orcidid>https://orcid.org/0000-0002-0561-2802</orcidid><orcidid>https://orcid.org/0000-0002-2085-4682</orcidid><orcidid>https://orcid.org/0000-0002-6452-4095</orcidid><orcidid>https://orcid.org/0000-0001-8082-6301</orcidid><orcidid>https://orcid.org/0000-0002-0575-0308</orcidid><orcidid>https://orcid.org/0000-0002-9948-6295</orcidid><orcidid>https://orcid.org/0000-0002-0339-9008</orcidid><orcidid>https://orcid.org/0000-0001-5520-8114</orcidid><orcidid>https://orcid.org/0000-0002-2457-5824</orcidid><orcidid>https://orcid.org/0000-0002-5415-1352</orcidid><orcidid>https://orcid.org/0000-0002-6514-8239</orcidid><orcidid>https://orcid.org/0000-0001-7747-0738</orcidid><orcidid>https://orcid.org/0000-0002-9250-9474</orcidid><orcidid>https://orcid.org/0000-0001-7678-4284</orcidid><orcidid>https://orcid.org/0000-0003-4064-6781</orcidid><orcidid>https://orcid.org/0000-0001-7339-9030</orcidid><orcidid>https://orcid.org/0000-0002-7017-9304</orcidid><orcidid>https://orcid.org/0000-0002-6764-4818</orcidid><orcidid>https://orcid.org/0000-0002-7918-2403</orcidid><orcidid>https://orcid.org/0000-0001-8586-784X</orcidid><orcidid>https://orcid.org/0000-0001-7202-7243</orcidid><orcidid>https://orcid.org/0000-0002-0348-0666</orcidid><orcidid>https://orcid.org/0000-0002-6684-9432</orcidid><orcidid>https://orcid.org/0000-0001-9037-3625</orcidid></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 0036-8075 |
| ispartof | Science (American Association for the Advancement of Science), 2024-07, Vol.385 (6704), p.eadd8394 |
| issn | 0036-8075 1095-9203 1095-9203 |
| language | eng |
| recordid | cdi_swepub_primary_oai_swepub_ki_se_876004 |
| source | MEDLINE; Science Online科学在线 |
| subjects | Accessibility Atlases as Topic CD4 antigen CD4-Positive T-Lymphocytes - immunology Cell activation Cell Differentiation Chromatin Chromatin - genetics Chromatin - metabolism CRISPR Disease Enhancer Elements, Genetic Enhancers Gene expression Gene mapping Gene regulation Gene sequencing Genes Genetic diversity Genetic Predisposition to Disease Genetic variance Genetics Heritability Humans Immunoregulation Lymphocytes Lymphocytes T Nucleotides Promoter Regions, Genetic Rare diseases Regulatory sequences Ribonucleic acid RNA Single-Cell Gene Expression Analysis Single-nucleotide polymorphism T-Lymphocytes, Helper-Inducer - immunology Transcription Transcription activation Transcription Initiation Site Transcription, Genetic Transposase |
| title | An atlas of transcribed enhancers across helper T cell diversity for decoding human diseases |
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