Differential Expression of the Transcription Factor GATA3 Specifies Lineage and Functions of Innate Lymphoid Cells
Lymphoid tissue inducer (LTi) cells are regarded as a subset of innate lymphoid cells (ILCs). However, these cells are not derived from the ILC common progenitor, which generates other ILC subsets and is defined by the expression of the transcription factor PLZF. Here, we examined transcription fact...
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| creator | Zhong, Chao Zheng, Mingzhu Cui, Kairong Martins, Andrew J. Hu, Gangqing Li, Dan Tessarollo, Lino Kozlov, Serguei Keller, Jonathan R. Tsang, John S. Zhao, Keji Zhu, Jinfang |
| description | Lymphoid tissue inducer (LTi) cells are regarded as a subset of innate lymphoid cells (ILCs). However, these cells are not derived from the ILC common progenitor, which generates other ILC subsets and is defined by the expression of the transcription factor PLZF. Here, we examined transcription factor(s) determining the fate of LTi progenitors versus non-LTi ILC progenitors. Conditional deletion of Gata3 resulted in the loss of PLZF+ non-LTi progenitors but not the LTi progenitors that expressed the transcription factor RORγt. Consistently, PLZF+ non-LTi progenitors expressed high amounts of GATA3, whereas GATA3 expression was low in RORγt+ LTi progenitors. The generation of both progenitors required the transcriptional regulator Id2, which defines the common helper-like innate lymphoid progenitor (ChILP), but not cytokine signaling. Nevertheless, low GATA3 expression was necessary for the generation of functionally mature LTi cells. Thus, differential expression of GATA3 determines the fates and functions of distinct ILC progenitors.
[Display omitted]
•High GATA3 expression is required for the development of non-LTi ILC progenitors•GATA3 is dispensable for the development of RORγt-expressing LTi progenitors•Low GATA3 expression is essential for the acquisition of LTi cell function•GATA3 and Id2 determine ILC lineage fates before cytokine-mediated ILC maturation
Lymphoid tissue inducer (LTi) cells are regarded as a subset of innate lymphoid cells (ILCs). Zhong et al. show that the generation of both non-LTi and LTi progenitors requires the transcriptional regulator Id2, but is distinguished by the differential requirement for the transcription factor GATA3. Their findings suggest that non-LTi ILCs are the bona fide innate counterparts of CD4+ T effector cells. |
| doi_str_mv | 10.1016/j.immuni.2019.12.001 |
| format | Article |
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[Display omitted]
•High GATA3 expression is required for the development of non-LTi ILC progenitors•GATA3 is dispensable for the development of RORγt-expressing LTi progenitors•Low GATA3 expression is essential for the acquisition of LTi cell function•GATA3 and Id2 determine ILC lineage fates before cytokine-mediated ILC maturation
Lymphoid tissue inducer (LTi) cells are regarded as a subset of innate lymphoid cells (ILCs). Zhong et al. show that the generation of both non-LTi and LTi progenitors requires the transcriptional regulator Id2, but is distinguished by the differential requirement for the transcription factor GATA3. Their findings suggest that non-LTi ILCs are the bona fide innate counterparts of CD4+ T effector cells.</description><identifier>ISSN: 1074-7613</identifier><identifier>ISSN: 1097-4180</identifier><identifier>EISSN: 1097-4180</identifier><identifier>DOI: 10.1016/j.immuni.2019.12.001</identifier><identifier>PMID: 31882362</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Animals ; Bone marrow ; cell fate bifurcation ; Cell Lineage - immunology ; Cells, Cultured ; Clonal deletion ; Cytokines ; GATA-3 protein ; GATA3 Transcription Factor - biosynthesis ; GATA3 Transcription Factor - genetics ; Gene expression ; Inhibitor of Differentiation Protein 2 - metabolism ; innate lymphoid cell ; Interleukin Receptor Common gamma Subunit - genetics ; lineage commitment ; lymphocyte development ; Lymphocytes ; Lymphoid cells ; Lymphoid tissue ; lymphoid tissue inducer ; lymphopoiesis ; Mice ; Mice, Inbred C57BL ; Mice, Knockout ; Nuclear Receptor Subfamily 1, Group F, Member 3 - biosynthesis ; progenitor heterogeneity ; Programmed Cell Death 1 Receptor - biosynthesis ; Promyelocytic Leukemia Zinc Finger Protein - biosynthesis ; Small intestine ; Stem Cells - cytology ; Stem Cells - immunology ; T-Lymphocyte Subsets - cytology ; T-Lymphocyte Subsets - immunology ; T-Lymphocytes, Helper-Inducer - cytology ; T-Lymphocytes, Helper-Inducer - immunology ; transcription factor ; Transcription factors ; transcriptional regulation</subject><ispartof>Immunity (Cambridge, Mass.), 2020-01, Vol.52 (1), p.83-95.e4</ispartof><rights>2019 Elsevier Inc.</rights><rights>Copyright © 2019 Elsevier Inc. All rights reserved.</rights><rights>2019. Elsevier Inc.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c557t-94d86472a507a4f8b405c9d1bcb5ed2533b48c2b40afd103c02d84b1388c1bcd3</citedby><cites>FETCH-LOGICAL-c557t-94d86472a507a4f8b405c9d1bcb5ed2533b48c2b40afd103c02d84b1388c1bcd3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.immuni.2019.12.001$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>230,314,780,784,885,3550,27924,27925,45995</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31882362$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Zhong, Chao</creatorcontrib><creatorcontrib>Zheng, Mingzhu</creatorcontrib><creatorcontrib>Cui, Kairong</creatorcontrib><creatorcontrib>Martins, Andrew J.</creatorcontrib><creatorcontrib>Hu, Gangqing</creatorcontrib><creatorcontrib>Li, Dan</creatorcontrib><creatorcontrib>Tessarollo, Lino</creatorcontrib><creatorcontrib>Kozlov, Serguei</creatorcontrib><creatorcontrib>Keller, Jonathan R.</creatorcontrib><creatorcontrib>Tsang, John S.</creatorcontrib><creatorcontrib>Zhao, Keji</creatorcontrib><creatorcontrib>Zhu, Jinfang</creatorcontrib><title>Differential Expression of the Transcription Factor GATA3 Specifies Lineage and Functions of Innate Lymphoid Cells</title><title>Immunity (Cambridge, Mass.)</title><addtitle>Immunity</addtitle><description>Lymphoid tissue inducer (LTi) cells are regarded as a subset of innate lymphoid cells (ILCs). However, these cells are not derived from the ILC common progenitor, which generates other ILC subsets and is defined by the expression of the transcription factor PLZF. Here, we examined transcription factor(s) determining the fate of LTi progenitors versus non-LTi ILC progenitors. Conditional deletion of Gata3 resulted in the loss of PLZF+ non-LTi progenitors but not the LTi progenitors that expressed the transcription factor RORγt. Consistently, PLZF+ non-LTi progenitors expressed high amounts of GATA3, whereas GATA3 expression was low in RORγt+ LTi progenitors. The generation of both progenitors required the transcriptional regulator Id2, which defines the common helper-like innate lymphoid progenitor (ChILP), but not cytokine signaling. Nevertheless, low GATA3 expression was necessary for the generation of functionally mature LTi cells. Thus, differential expression of GATA3 determines the fates and functions of distinct ILC progenitors.
[Display omitted]
•High GATA3 expression is required for the development of non-LTi ILC progenitors•GATA3 is dispensable for the development of RORγt-expressing LTi progenitors•Low GATA3 expression is essential for the acquisition of LTi cell function•GATA3 and Id2 determine ILC lineage fates before cytokine-mediated ILC maturation
Lymphoid tissue inducer (LTi) cells are regarded as a subset of innate lymphoid cells (ILCs). Zhong et al. show that the generation of both non-LTi and LTi progenitors requires the transcriptional regulator Id2, but is distinguished by the differential requirement for the transcription factor GATA3. Their findings suggest that non-LTi ILCs are the bona fide innate counterparts of CD4+ T effector cells.</description><subject>Animals</subject><subject>Bone marrow</subject><subject>cell fate bifurcation</subject><subject>Cell Lineage - immunology</subject><subject>Cells, Cultured</subject><subject>Clonal deletion</subject><subject>Cytokines</subject><subject>GATA-3 protein</subject><subject>GATA3 Transcription Factor - biosynthesis</subject><subject>GATA3 Transcription Factor - genetics</subject><subject>Gene expression</subject><subject>Inhibitor of Differentiation Protein 2 - metabolism</subject><subject>innate lymphoid cell</subject><subject>Interleukin Receptor Common gamma Subunit - genetics</subject><subject>lineage commitment</subject><subject>lymphocyte development</subject><subject>Lymphocytes</subject><subject>Lymphoid cells</subject><subject>Lymphoid tissue</subject><subject>lymphoid tissue inducer</subject><subject>lymphopoiesis</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Mice, Knockout</subject><subject>Nuclear Receptor Subfamily 1, Group F, Member 3 - biosynthesis</subject><subject>progenitor heterogeneity</subject><subject>Programmed Cell Death 1 Receptor - biosynthesis</subject><subject>Promyelocytic Leukemia Zinc Finger Protein - biosynthesis</subject><subject>Small intestine</subject><subject>Stem Cells - cytology</subject><subject>Stem Cells - immunology</subject><subject>T-Lymphocyte Subsets - cytology</subject><subject>T-Lymphocyte Subsets - immunology</subject><subject>T-Lymphocytes, Helper-Inducer - cytology</subject><subject>T-Lymphocytes, Helper-Inducer - immunology</subject><subject>transcription factor</subject><subject>Transcription factors</subject><subject>transcriptional regulation</subject><issn>1074-7613</issn><issn>1097-4180</issn><issn>1097-4180</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kUtv1DAUhSMEakvpP0DIEhs2CX4lcTZIo6FTKo3URYe15dg3HY8SO9hJ1f57HE0fwILVvbr-7rGPT5Z9JLggmFRfD4UdhtnZgmLSFIQWGJM32RnBTZ1zIvDbpa95XleEnWbvYzwkgJcNPslOGRGCsoqeZeG77ToI4CarenT5MAaI0XqHfIemPaBdUC7qYMdpGW6UnnxAV6vdiqHbEbTtLES0tQ7UHSDlDNrMTi9sXBSunVMToO3jMO69NWgNfR8_ZO861Ue4eKrn2c_N5W79I9_eXF2vV9tcl2U95Q03ouI1VSWuFe9Ey3GpG0Na3ZZgaMlYy4Wmaaw6QzDTmBrBW8KE0Aky7Dz7dtQd53YAo5PHoHo5Bjuo8Ci9svLvE2f38s7fy6qpknyTBL48CQT_a4Y4ycFGnSwoB36OkjJGaClYzRL6-R_04Ofgkr2FqhsqcMkTxY-UDj7GAN3LYwiWS6jyII-hyiVUSahMmaW1T38aeVl6TvHVKaTvvLcQZNQWnAZjA-hJGm__f8NvdRG2NQ</recordid><startdate>20200114</startdate><enddate>20200114</enddate><creator>Zhong, Chao</creator><creator>Zheng, Mingzhu</creator><creator>Cui, Kairong</creator><creator>Martins, Andrew J.</creator><creator>Hu, Gangqing</creator><creator>Li, Dan</creator><creator>Tessarollo, Lino</creator><creator>Kozlov, Serguei</creator><creator>Keller, Jonathan R.</creator><creator>Tsang, John S.</creator><creator>Zhao, Keji</creator><creator>Zhu, Jinfang</creator><general>Elsevier Inc</general><general>Elsevier Limited</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>7T5</scope><scope>7T7</scope><scope>7TK</scope><scope>7TM</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>K9.</scope><scope>M7N</scope><scope>NAPCQ</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20200114</creationdate><title>Differential Expression of the Transcription Factor GATA3 Specifies Lineage and Functions of Innate Lymphoid Cells</title><author>Zhong, Chao ; Zheng, Mingzhu ; Cui, Kairong ; Martins, Andrew J. ; Hu, Gangqing ; Li, Dan ; Tessarollo, Lino ; Kozlov, Serguei ; Keller, Jonathan R. ; Tsang, John S. ; Zhao, Keji ; Zhu, Jinfang</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c557t-94d86472a507a4f8b405c9d1bcb5ed2533b48c2b40afd103c02d84b1388c1bcd3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Animals</topic><topic>Bone marrow</topic><topic>cell fate bifurcation</topic><topic>Cell Lineage - immunology</topic><topic>Cells, Cultured</topic><topic>Clonal deletion</topic><topic>Cytokines</topic><topic>GATA-3 protein</topic><topic>GATA3 Transcription Factor - biosynthesis</topic><topic>GATA3 Transcription Factor - genetics</topic><topic>Gene expression</topic><topic>Inhibitor of Differentiation Protein 2 - metabolism</topic><topic>innate lymphoid cell</topic><topic>Interleukin Receptor Common gamma Subunit - genetics</topic><topic>lineage commitment</topic><topic>lymphocyte development</topic><topic>Lymphocytes</topic><topic>Lymphoid cells</topic><topic>Lymphoid tissue</topic><topic>lymphoid tissue inducer</topic><topic>lymphopoiesis</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>Mice, Knockout</topic><topic>Nuclear Receptor Subfamily 1, Group F, Member 3 - biosynthesis</topic><topic>progenitor heterogeneity</topic><topic>Programmed Cell Death 1 Receptor - biosynthesis</topic><topic>Promyelocytic Leukemia Zinc Finger Protein - biosynthesis</topic><topic>Small intestine</topic><topic>Stem Cells - cytology</topic><topic>Stem Cells - immunology</topic><topic>T-Lymphocyte Subsets - cytology</topic><topic>T-Lymphocyte Subsets - immunology</topic><topic>T-Lymphocytes, Helper-Inducer - cytology</topic><topic>T-Lymphocytes, Helper-Inducer - immunology</topic><topic>transcription factor</topic><topic>Transcription factors</topic><topic>transcriptional regulation</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Zhong, Chao</creatorcontrib><creatorcontrib>Zheng, Mingzhu</creatorcontrib><creatorcontrib>Cui, Kairong</creatorcontrib><creatorcontrib>Martins, Andrew J.</creatorcontrib><creatorcontrib>Hu, Gangqing</creatorcontrib><creatorcontrib>Li, Dan</creatorcontrib><creatorcontrib>Tessarollo, Lino</creatorcontrib><creatorcontrib>Kozlov, Serguei</creatorcontrib><creatorcontrib>Keller, Jonathan R.</creatorcontrib><creatorcontrib>Tsang, John S.</creatorcontrib><creatorcontrib>Zhao, Keji</creatorcontrib><creatorcontrib>Zhu, Jinfang</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>Immunology Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</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>ProQuest Health & Medical Complete (Alumni)</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Nursing & Allied Health Premium</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Immunity (Cambridge, Mass.)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Zhong, Chao</au><au>Zheng, Mingzhu</au><au>Cui, Kairong</au><au>Martins, Andrew J.</au><au>Hu, Gangqing</au><au>Li, Dan</au><au>Tessarollo, Lino</au><au>Kozlov, Serguei</au><au>Keller, Jonathan R.</au><au>Tsang, John S.</au><au>Zhao, Keji</au><au>Zhu, Jinfang</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Differential Expression of the Transcription Factor GATA3 Specifies Lineage and Functions of Innate Lymphoid Cells</atitle><jtitle>Immunity (Cambridge, Mass.)</jtitle><addtitle>Immunity</addtitle><date>2020-01-14</date><risdate>2020</risdate><volume>52</volume><issue>1</issue><spage>83</spage><epage>95.e4</epage><pages>83-95.e4</pages><issn>1074-7613</issn><issn>1097-4180</issn><eissn>1097-4180</eissn><abstract>Lymphoid tissue inducer (LTi) cells are regarded as a subset of innate lymphoid cells (ILCs). However, these cells are not derived from the ILC common progenitor, which generates other ILC subsets and is defined by the expression of the transcription factor PLZF. Here, we examined transcription factor(s) determining the fate of LTi progenitors versus non-LTi ILC progenitors. Conditional deletion of Gata3 resulted in the loss of PLZF+ non-LTi progenitors but not the LTi progenitors that expressed the transcription factor RORγt. Consistently, PLZF+ non-LTi progenitors expressed high amounts of GATA3, whereas GATA3 expression was low in RORγt+ LTi progenitors. The generation of both progenitors required the transcriptional regulator Id2, which defines the common helper-like innate lymphoid progenitor (ChILP), but not cytokine signaling. Nevertheless, low GATA3 expression was necessary for the generation of functionally mature LTi cells. Thus, differential expression of GATA3 determines the fates and functions of distinct ILC progenitors.
[Display omitted]
•High GATA3 expression is required for the development of non-LTi ILC progenitors•GATA3 is dispensable for the development of RORγt-expressing LTi progenitors•Low GATA3 expression is essential for the acquisition of LTi cell function•GATA3 and Id2 determine ILC lineage fates before cytokine-mediated ILC maturation
Lymphoid tissue inducer (LTi) cells are regarded as a subset of innate lymphoid cells (ILCs). Zhong et al. show that the generation of both non-LTi and LTi progenitors requires the transcriptional regulator Id2, but is distinguished by the differential requirement for the transcription factor GATA3. Their findings suggest that non-LTi ILCs are the bona fide innate counterparts of CD4+ T effector cells.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>31882362</pmid><doi>10.1016/j.immuni.2019.12.001</doi><oa>free_for_read</oa></addata></record> |
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| subjects | Animals Bone marrow cell fate bifurcation Cell Lineage - immunology Cells, Cultured Clonal deletion Cytokines GATA-3 protein GATA3 Transcription Factor - biosynthesis GATA3 Transcription Factor - genetics Gene expression Inhibitor of Differentiation Protein 2 - metabolism innate lymphoid cell Interleukin Receptor Common gamma Subunit - genetics lineage commitment lymphocyte development Lymphocytes Lymphoid cells Lymphoid tissue lymphoid tissue inducer lymphopoiesis Mice Mice, Inbred C57BL Mice, Knockout Nuclear Receptor Subfamily 1, Group F, Member 3 - biosynthesis progenitor heterogeneity Programmed Cell Death 1 Receptor - biosynthesis Promyelocytic Leukemia Zinc Finger Protein - biosynthesis Small intestine Stem Cells - cytology Stem Cells - immunology T-Lymphocyte Subsets - cytology T-Lymphocyte Subsets - immunology T-Lymphocytes, Helper-Inducer - cytology T-Lymphocytes, Helper-Inducer - immunology transcription factor Transcription factors transcriptional regulation |
| title | Differential Expression of the Transcription Factor GATA3 Specifies Lineage and Functions of Innate Lymphoid Cells |
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