TCF1 dosage determines cell fate during T cell development
Loss-of-function studies have shown that transcription factor T cell factor-1 (TCF1), encoded by the gene, is essential for T cell development in the thymus. We discovered that the expression level is regulated by E box DNA binding proteins, independent of Notch, and regulates αβ and γδ T cell devel...
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| creator | Verma, Anjali Aylward, Bridget Ma, Fei Sherman, Cheryl A Chopp, Laura Shinton, Susan Roy, Roshni Fahl, Shawn Contreras, Alejandra Koenitzer, Byron Awasthi, Parirokh Mazan-Mamczarz, Krystyna De, Supriyo Ollikainen, Noah Qiu, Xiang Bosselut, Remy Sen, Ranjan Wiest, David L Sen, Jyoti Misra |
| description | Loss-of-function studies have shown that transcription factor T cell factor-1 (TCF1), encoded by the
gene, is essential for T cell development in the thymus. We discovered that the
expression level is regulated by E box DNA binding proteins, independent of Notch, and regulates αβ and γδ T cell development. Systematic interrogation of the five E protein binding elements (EPE1-5) in the
enhancer region showed lineage-specific utilization. Specifically, loss-of-function analysis revealed that only EPE3 plays a critical role in supporting αβ T cell development, while EPE1, 3, and 5 regulate the γδ T cell maturation and functional cell fate decision. The importance of EPE3 in supporting both lineages may stem from its unique capacity to interact with the
transcriptional start site. Together, these studies demonstrate that the precise dosage of TCF1 expression mediated by distinct EPEs generates a balanced output of T cells from the thymus. |
| doi_str_mv | 10.1126/sciadv.ado5982 |
| format | Article |
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gene, is essential for T cell development in the thymus. We discovered that the
expression level is regulated by E box DNA binding proteins, independent of Notch, and regulates αβ and γδ T cell development. Systematic interrogation of the five E protein binding elements (EPE1-5) in the
enhancer region showed lineage-specific utilization. Specifically, loss-of-function analysis revealed that only EPE3 plays a critical role in supporting αβ T cell development, while EPE1, 3, and 5 regulate the γδ T cell maturation and functional cell fate decision. The importance of EPE3 in supporting both lineages may stem from its unique capacity to interact with the
transcriptional start site. Together, these studies demonstrate that the precise dosage of TCF1 expression mediated by distinct EPEs generates a balanced output of T cells from the thymus.</description><identifier>ISSN: 2375-2548</identifier><identifier>EISSN: 2375-2548</identifier><identifier>DOI: 10.1126/sciadv.ado5982</identifier><identifier>PMID: 39602533</identifier><language>eng</language><publisher>United States: American Association for the Advancement of Science</publisher><subject>Animals ; Biomedicine and Life Sciences ; Cell Differentiation ; Cell Lineage - genetics ; Enhancer Elements, Genetic ; Gene Dosage ; Hepatocyte Nuclear Factor 1-alpha - genetics ; Hepatocyte Nuclear Factor 1-alpha - metabolism ; Immunology ; Mice ; Receptors, Antigen, T-Cell, alpha-beta - genetics ; Receptors, Antigen, T-Cell, alpha-beta - metabolism ; SciAdv r-articles ; T Cell Transcription Factor 1 - genetics ; T Cell Transcription Factor 1 - metabolism ; T-Lymphocytes - cytology ; T-Lymphocytes - metabolism ; Thymus Gland - cytology ; Thymus Gland - metabolism</subject><ispartof>Science advances, 2024-11, Vol.10 (48), p.eado5982</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. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC). 2024 The Authors</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c1519-fd677c0d69d3185d264f6345ac5afa8fe6e514f013b92938e8ad96d3a805e2903</cites><orcidid>0000-0002-0489-2048 ; 0000-0002-0377-2028 ; 0000-0003-3653-5958 ; 0000-0002-2075-7655 ; 0000-0001-7977-4698 ; 0009-0005-1545-0500 ; 0000-0001-9161-9033 ; 0000-0003-2033-1790 ; 0000-0002-1174-2400 ; 0000-0002-0792-3188 ; 0000-0001-6494-4439 ; 0000-0002-6365-0866 ; 0009-0007-3039-1945 ; 0000-0003-2649-1904 ; 0000-0003-0401-0954 ; 0009-0004-1861-8711 ; 0000-0002-1916-3905 ; 0000-0002-5831-9781</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC11601199/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC11601199/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,27923,27924,53790,53792</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39602533$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Verma, Anjali</creatorcontrib><creatorcontrib>Aylward, Bridget</creatorcontrib><creatorcontrib>Ma, Fei</creatorcontrib><creatorcontrib>Sherman, Cheryl A</creatorcontrib><creatorcontrib>Chopp, Laura</creatorcontrib><creatorcontrib>Shinton, Susan</creatorcontrib><creatorcontrib>Roy, Roshni</creatorcontrib><creatorcontrib>Fahl, Shawn</creatorcontrib><creatorcontrib>Contreras, Alejandra</creatorcontrib><creatorcontrib>Koenitzer, Byron</creatorcontrib><creatorcontrib>Awasthi, Parirokh</creatorcontrib><creatorcontrib>Mazan-Mamczarz, Krystyna</creatorcontrib><creatorcontrib>De, Supriyo</creatorcontrib><creatorcontrib>Ollikainen, Noah</creatorcontrib><creatorcontrib>Qiu, Xiang</creatorcontrib><creatorcontrib>Bosselut, Remy</creatorcontrib><creatorcontrib>Sen, Ranjan</creatorcontrib><creatorcontrib>Wiest, David L</creatorcontrib><creatorcontrib>Sen, Jyoti Misra</creatorcontrib><title>TCF1 dosage determines cell fate during T cell development</title><title>Science advances</title><addtitle>Sci Adv</addtitle><description>Loss-of-function studies have shown that transcription factor T cell factor-1 (TCF1), encoded by the
gene, is essential for T cell development in the thymus. We discovered that the
expression level is regulated by E box DNA binding proteins, independent of Notch, and regulates αβ and γδ T cell development. Systematic interrogation of the five E protein binding elements (EPE1-5) in the
enhancer region showed lineage-specific utilization. Specifically, loss-of-function analysis revealed that only EPE3 plays a critical role in supporting αβ T cell development, while EPE1, 3, and 5 regulate the γδ T cell maturation and functional cell fate decision. The importance of EPE3 in supporting both lineages may stem from its unique capacity to interact with the
transcriptional start site. Together, these studies demonstrate that the precise dosage of TCF1 expression mediated by distinct EPEs generates a balanced output of T cells from the thymus.</description><subject>Animals</subject><subject>Biomedicine and Life Sciences</subject><subject>Cell Differentiation</subject><subject>Cell Lineage - genetics</subject><subject>Enhancer Elements, Genetic</subject><subject>Gene Dosage</subject><subject>Hepatocyte Nuclear Factor 1-alpha - genetics</subject><subject>Hepatocyte Nuclear Factor 1-alpha - metabolism</subject><subject>Immunology</subject><subject>Mice</subject><subject>Receptors, Antigen, T-Cell, alpha-beta - genetics</subject><subject>Receptors, Antigen, T-Cell, alpha-beta - metabolism</subject><subject>SciAdv r-articles</subject><subject>T Cell Transcription Factor 1 - genetics</subject><subject>T Cell Transcription Factor 1 - metabolism</subject><subject>T-Lymphocytes - cytology</subject><subject>T-Lymphocytes - metabolism</subject><subject>Thymus Gland - cytology</subject><subject>Thymus Gland - metabolism</subject><issn>2375-2548</issn><issn>2375-2548</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpVULFOwzAQtRCIVqUrI8rIkuKzYydmQaiigFSJpcyWG59LUBIXO63E35MqBZXpTu_evXf3CLkGOgNg8i6WlbH7mbFeqIKdkTHjuUiZyIrzk35EpjF-Ukohk1KAuiQjriRlgvMxuV_NF5BYH80GE4sdhqZqMSYl1nXiTNeDu1C1m2Q1QBb3WPttg213RS6cqSNOj3VC3hdPq_lLunx7fp0_LtMSerfUWZnnJbVSWQ6FsExmTvJMmFIYZwqHEgVkjgJfK6Z4gYWxSlpuCiqQKcon5GHQ3e7WDdqytw6m1ttQNSZ8a28q_X_SVh964_caQFIApXqF26NC8F87jJ1uqnh4x7Tod1Fz4DznWc5ZT50N1DL4GAO6Px-g-hC6HkLXx9D7hZvT6_7ovxHzH7Y2fsk</recordid><startdate>20241129</startdate><enddate>20241129</enddate><creator>Verma, Anjali</creator><creator>Aylward, Bridget</creator><creator>Ma, Fei</creator><creator>Sherman, Cheryl A</creator><creator>Chopp, Laura</creator><creator>Shinton, Susan</creator><creator>Roy, Roshni</creator><creator>Fahl, Shawn</creator><creator>Contreras, Alejandra</creator><creator>Koenitzer, Byron</creator><creator>Awasthi, Parirokh</creator><creator>Mazan-Mamczarz, Krystyna</creator><creator>De, Supriyo</creator><creator>Ollikainen, Noah</creator><creator>Qiu, Xiang</creator><creator>Bosselut, Remy</creator><creator>Sen, Ranjan</creator><creator>Wiest, David L</creator><creator>Sen, Jyoti Misra</creator><general>American Association for the Advancement of Science</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>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-0489-2048</orcidid><orcidid>https://orcid.org/0000-0002-0377-2028</orcidid><orcidid>https://orcid.org/0000-0003-3653-5958</orcidid><orcidid>https://orcid.org/0000-0002-2075-7655</orcidid><orcidid>https://orcid.org/0000-0001-7977-4698</orcidid><orcidid>https://orcid.org/0009-0005-1545-0500</orcidid><orcidid>https://orcid.org/0000-0001-9161-9033</orcidid><orcidid>https://orcid.org/0000-0003-2033-1790</orcidid><orcidid>https://orcid.org/0000-0002-1174-2400</orcidid><orcidid>https://orcid.org/0000-0002-0792-3188</orcidid><orcidid>https://orcid.org/0000-0001-6494-4439</orcidid><orcidid>https://orcid.org/0000-0002-6365-0866</orcidid><orcidid>https://orcid.org/0009-0007-3039-1945</orcidid><orcidid>https://orcid.org/0000-0003-2649-1904</orcidid><orcidid>https://orcid.org/0000-0003-0401-0954</orcidid><orcidid>https://orcid.org/0009-0004-1861-8711</orcidid><orcidid>https://orcid.org/0000-0002-1916-3905</orcidid><orcidid>https://orcid.org/0000-0002-5831-9781</orcidid></search><sort><creationdate>20241129</creationdate><title>TCF1 dosage determines cell fate during T cell development</title><author>Verma, Anjali ; 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gene, is essential for T cell development in the thymus. We discovered that the
expression level is regulated by E box DNA binding proteins, independent of Notch, and regulates αβ and γδ T cell development. Systematic interrogation of the five E protein binding elements (EPE1-5) in the
enhancer region showed lineage-specific utilization. Specifically, loss-of-function analysis revealed that only EPE3 plays a critical role in supporting αβ T cell development, while EPE1, 3, and 5 regulate the γδ T cell maturation and functional cell fate decision. The importance of EPE3 in supporting both lineages may stem from its unique capacity to interact with the
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| subjects | Animals Biomedicine and Life Sciences Cell Differentiation Cell Lineage - genetics Enhancer Elements, Genetic Gene Dosage Hepatocyte Nuclear Factor 1-alpha - genetics Hepatocyte Nuclear Factor 1-alpha - metabolism Immunology Mice Receptors, Antigen, T-Cell, alpha-beta - genetics Receptors, Antigen, T-Cell, alpha-beta - metabolism SciAdv r-articles T Cell Transcription Factor 1 - genetics T Cell Transcription Factor 1 - metabolism T-Lymphocytes - cytology T-Lymphocytes - metabolism Thymus Gland - cytology Thymus Gland - metabolism |
| title | TCF1 dosage determines cell fate during T cell development |
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