Antigen‐presenting cell‐derived IL‐6 restricts the expression of GATA3 and IL‐4 by follicular helper T cells
Follicular helper T cells (Tfh) support high‐affinity Ab production by germinal center B cells through both membrane interactions and secretion of IL‐4 and ‐21, two major cytokines implicated in B‐cell survival and Ab class switch. Tfh‐2 cells recently emerged in humans as a strong IL‐4 producer Tfh...
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| creator | Hercor, Mélanie Anciaux, Maelle Denanglaire, Sébastien Debuisson, Delphine Leo, Oberdan Andris, Fabienne |
| description | Follicular helper T cells (Tfh) support high‐affinity Ab production by germinal center B cells through both membrane interactions and secretion of IL‐4 and ‐21, two major cytokines implicated in B‐cell survival and Ab class switch. Tfh‐2 cells recently emerged in humans as a strong IL‐4 producer Tfh cell subset implicated in both autoimmune and allergic diseases. Although the molecular mechanisms governing Tfh cell differentiation from naive T cells have been widely described, much less is known about the regulation of cytokine secretion by mouse Tfh‐2 cells. The purpose of our study was to evaluate the role of dendritic cell–derived IL‐6 in fine‐tuning cytokine secretion by Tfh cells. Our results demonstrate that priming of Th cells by IL‐6‐deficient antigen‐presenting dendritic cells preferentially leads to accumulation of a subset of Tfh cells characterized by high expression of GATA3 and IL‐4, associated with reduced production of IL‐21. STAT3‐deficient Tfh cells also overexpress GATA3, suggesting that early IL‐6/STAT3 signaling during Tfh cell development inhibits the expression of a set of genes associated with the Th2 differentiation program. Overall, our data indicate that IL‐6/STAT3 signaling restrains the expression of Th2‐like genes in Tfh cells, thus contributing to the control of IgE secretion in vivo.
IL‐6/STAT3 signaling modulates the cytokine and transcription factor pattern of Tfh cells and controls IgE secretion in vivo. |
| doi_str_mv | 10.1189/jlb.1HI1115-511R |
| format | Article |
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IL‐6/STAT3 signaling modulates the cytokine and transcription factor pattern of Tfh cells and controls IgE secretion in vivo.</description><identifier>ISSN: 0741-5400</identifier><identifier>EISSN: 1938-3673</identifier><identifier>DOI: 10.1189/jlb.1HI1115-511R</identifier><identifier>PMID: 27474166</identifier><language>eng</language><publisher>United States: Oxford University Press</publisher><subject>Allergic diseases ; Animals ; Antigen-presenting cells ; Antigen-Presenting Cells - metabolism ; Antigens ; Antigens - immunology ; B-Lymphocytes - immunology ; Bone Marrow Cells - metabolism ; Cell Differentiation ; Cell survival ; Class switching ; Cytokines ; Dendritic cells ; Dendritic Cells - metabolism ; Differentiation (biology) ; GATA-3 protein ; GATA3 Transcription Factor - metabolism ; Gene expression ; Gene Expression Profiling ; Genes ; Helper cells ; humoral response ; Immunization ; Immunoglobulin Class Switching ; Immunoglobulin E ; Immunoglobulin E - metabolism ; Interleukin 21 ; Interleukin 4 ; Interleukin 6 ; Interleukin-12 - metabolism ; Interleukin-4 - metabolism ; Interleukin-6 - metabolism ; Lymphocytes ; Lymphocytes B ; Lymphocytes T ; Mice, Inbred C57BL ; Molecular modelling ; Priming ; RNA, Messenger - genetics ; RNA, Messenger - metabolism ; Signal Transduction ; Signaling ; Spotlight on Leading Edge Research ; STAT3 ; Stat3 protein ; STAT3 Transcription Factor - metabolism ; T cell receptors ; T-Lymphocytes, Helper-Inducer - metabolism ; Tfh‐2 ; Transcription Factors - genetics ; Transcription Factors - metabolism</subject><ispartof>Journal of leukocyte biology, 2017-01, Vol.101 (1), p.5-14</ispartof><rights>2017 Society for Leukocyte Biology</rights><rights>Society for Leukocyte Biology.</rights><rights>Copyright Federation of American Societies for Experimental Biology (FASEB) Jan 2017</rights><rights>Society for Leukocyte Biology 2016 Society for Leukocyte Biology</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5035-3625a1335968e49faa2dc3682e8445a956b6e2efbe99621d9e6b4b8cbd2d5b923</citedby><cites>FETCH-LOGICAL-c5035-3625a1335968e49faa2dc3682e8445a956b6e2efbe99621d9e6b4b8cbd2d5b923</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1189%2Fjlb.1HI1115-511R$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1189%2Fjlb.1HI1115-511R$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>230,314,776,780,881,1411,27901,27902,45550,45551</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/27474166$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Hercor, Mélanie</creatorcontrib><creatorcontrib>Anciaux, Maelle</creatorcontrib><creatorcontrib>Denanglaire, Sébastien</creatorcontrib><creatorcontrib>Debuisson, Delphine</creatorcontrib><creatorcontrib>Leo, Oberdan</creatorcontrib><creatorcontrib>Andris, Fabienne</creatorcontrib><title>Antigen‐presenting cell‐derived IL‐6 restricts the expression of GATA3 and IL‐4 by follicular helper T cells</title><title>Journal of leukocyte biology</title><addtitle>J Leukoc Biol</addtitle><description>Follicular helper T cells (Tfh) support high‐affinity Ab production by germinal center B cells through both membrane interactions and secretion of IL‐4 and ‐21, two major cytokines implicated in B‐cell survival and Ab class switch. Tfh‐2 cells recently emerged in humans as a strong IL‐4 producer Tfh cell subset implicated in both autoimmune and allergic diseases. Although the molecular mechanisms governing Tfh cell differentiation from naive T cells have been widely described, much less is known about the regulation of cytokine secretion by mouse Tfh‐2 cells. The purpose of our study was to evaluate the role of dendritic cell–derived IL‐6 in fine‐tuning cytokine secretion by Tfh cells. Our results demonstrate that priming of Th cells by IL‐6‐deficient antigen‐presenting dendritic cells preferentially leads to accumulation of a subset of Tfh cells characterized by high expression of GATA3 and IL‐4, associated with reduced production of IL‐21. STAT3‐deficient Tfh cells also overexpress GATA3, suggesting that early IL‐6/STAT3 signaling during Tfh cell development inhibits the expression of a set of genes associated with the Th2 differentiation program. Overall, our data indicate that IL‐6/STAT3 signaling restrains the expression of Th2‐like genes in Tfh cells, thus contributing to the control of IgE secretion in vivo.
IL‐6/STAT3 signaling modulates the cytokine and transcription factor pattern of Tfh cells and controls IgE secretion in vivo.</description><subject>Allergic diseases</subject><subject>Animals</subject><subject>Antigen-presenting cells</subject><subject>Antigen-Presenting Cells - metabolism</subject><subject>Antigens</subject><subject>Antigens - immunology</subject><subject>B-Lymphocytes - immunology</subject><subject>Bone Marrow Cells - metabolism</subject><subject>Cell Differentiation</subject><subject>Cell survival</subject><subject>Class switching</subject><subject>Cytokines</subject><subject>Dendritic cells</subject><subject>Dendritic Cells - metabolism</subject><subject>Differentiation (biology)</subject><subject>GATA-3 protein</subject><subject>GATA3 Transcription Factor - metabolism</subject><subject>Gene expression</subject><subject>Gene Expression Profiling</subject><subject>Genes</subject><subject>Helper cells</subject><subject>humoral response</subject><subject>Immunization</subject><subject>Immunoglobulin Class Switching</subject><subject>Immunoglobulin E</subject><subject>Immunoglobulin E - metabolism</subject><subject>Interleukin 21</subject><subject>Interleukin 4</subject><subject>Interleukin 6</subject><subject>Interleukin-12 - metabolism</subject><subject>Interleukin-4 - metabolism</subject><subject>Interleukin-6 - metabolism</subject><subject>Lymphocytes</subject><subject>Lymphocytes B</subject><subject>Lymphocytes T</subject><subject>Mice, Inbred C57BL</subject><subject>Molecular modelling</subject><subject>Priming</subject><subject>RNA, Messenger - genetics</subject><subject>RNA, Messenger - metabolism</subject><subject>Signal Transduction</subject><subject>Signaling</subject><subject>Spotlight on Leading Edge Research</subject><subject>STAT3</subject><subject>Stat3 protein</subject><subject>STAT3 Transcription Factor - metabolism</subject><subject>T cell receptors</subject><subject>T-Lymphocytes, Helper-Inducer - metabolism</subject><subject>Tfh‐2</subject><subject>Transcription Factors - genetics</subject><subject>Transcription Factors - metabolism</subject><issn>0741-5400</issn><issn>1938-3673</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNks1uEzEUhS0EoqGwZ4Usselmiv_H3iCFqrRBkZBQWFuemTuJI2cm2DOl2fUReEaeBIeEqnQDK-v6fvfYx8cIvabknFJt3q1DdU6vZ5RSWUhKvzxBE2q4Lrgq-VM0IaWghRSEnKAXKa0JIZwp8hydsFLkllITNEy7wS-h-3n3YxshQa66Ja4hhLzTQPQ30ODZPBcK5_4QfT0kPKwAw-1-IPm-w32Lr6aLKceuO8ICVzvc9iH4egwu4hWELUS8-K2cXqJnrQsJXh3XU_T14-Xi4rqYf76aXUznRS0Jl9kFk45yLo3SIEzrHGtqrjQDLYR0RqpKAYO2AmMUo40BVYlK11XDGlkZxk_R-4Pudqw20NTZXXTBbqPfuLizvfP2707nV3bZ31iZ30ZwkQXOjgKx_zZm-3bj096C66Afk6VaGqGNKNl_oCyHUkopM_r2Ebrux9jll7DU6Hys1IRnihyoOvYpRWjv702J3advc_r2mL7dp59H3jz0ez_wJ-4MyAPw3QfY_VPQfpp_yJ9G8l8-4b9u</recordid><startdate>201701</startdate><enddate>201701</enddate><creator>Hercor, Mélanie</creator><creator>Anciaux, Maelle</creator><creator>Denanglaire, Sébastien</creator><creator>Debuisson, Delphine</creator><creator>Leo, Oberdan</creator><creator>Andris, Fabienne</creator><general>Oxford University Press</general><general>Society for Leukocyte Biology</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>7T5</scope><scope>7T7</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>201701</creationdate><title>Antigen‐presenting cell‐derived IL‐6 restricts the expression of GATA3 and IL‐4 by follicular helper T cells</title><author>Hercor, Mélanie ; Anciaux, Maelle ; Denanglaire, Sébastien ; Debuisson, Delphine ; Leo, Oberdan ; Andris, Fabienne</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5035-3625a1335968e49faa2dc3682e8445a956b6e2efbe99621d9e6b4b8cbd2d5b923</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Allergic diseases</topic><topic>Animals</topic><topic>Antigen-presenting cells</topic><topic>Antigen-Presenting Cells - metabolism</topic><topic>Antigens</topic><topic>Antigens - immunology</topic><topic>B-Lymphocytes - immunology</topic><topic>Bone Marrow Cells - metabolism</topic><topic>Cell Differentiation</topic><topic>Cell survival</topic><topic>Class switching</topic><topic>Cytokines</topic><topic>Dendritic cells</topic><topic>Dendritic Cells - metabolism</topic><topic>Differentiation (biology)</topic><topic>GATA-3 protein</topic><topic>GATA3 Transcription Factor - metabolism</topic><topic>Gene expression</topic><topic>Gene Expression Profiling</topic><topic>Genes</topic><topic>Helper cells</topic><topic>humoral response</topic><topic>Immunization</topic><topic>Immunoglobulin Class Switching</topic><topic>Immunoglobulin E</topic><topic>Immunoglobulin E - metabolism</topic><topic>Interleukin 21</topic><topic>Interleukin 4</topic><topic>Interleukin 6</topic><topic>Interleukin-12 - metabolism</topic><topic>Interleukin-4 - metabolism</topic><topic>Interleukin-6 - metabolism</topic><topic>Lymphocytes</topic><topic>Lymphocytes B</topic><topic>Lymphocytes T</topic><topic>Mice, Inbred C57BL</topic><topic>Molecular modelling</topic><topic>Priming</topic><topic>RNA, Messenger - genetics</topic><topic>RNA, Messenger - metabolism</topic><topic>Signal Transduction</topic><topic>Signaling</topic><topic>Spotlight on Leading Edge Research</topic><topic>STAT3</topic><topic>Stat3 protein</topic><topic>STAT3 Transcription Factor - metabolism</topic><topic>T cell receptors</topic><topic>T-Lymphocytes, Helper-Inducer - metabolism</topic><topic>Tfh‐2</topic><topic>Transcription Factors - genetics</topic><topic>Transcription Factors - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Hercor, Mélanie</creatorcontrib><creatorcontrib>Anciaux, Maelle</creatorcontrib><creatorcontrib>Denanglaire, Sébastien</creatorcontrib><creatorcontrib>Debuisson, Delphine</creatorcontrib><creatorcontrib>Leo, Oberdan</creatorcontrib><creatorcontrib>Andris, Fabienne</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>Immunology Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</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>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Journal of leukocyte biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Hercor, Mélanie</au><au>Anciaux, Maelle</au><au>Denanglaire, Sébastien</au><au>Debuisson, Delphine</au><au>Leo, Oberdan</au><au>Andris, Fabienne</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Antigen‐presenting cell‐derived IL‐6 restricts the expression of GATA3 and IL‐4 by follicular helper T cells</atitle><jtitle>Journal of leukocyte biology</jtitle><addtitle>J Leukoc Biol</addtitle><date>2017-01</date><risdate>2017</risdate><volume>101</volume><issue>1</issue><spage>5</spage><epage>14</epage><pages>5-14</pages><issn>0741-5400</issn><eissn>1938-3673</eissn><abstract>Follicular helper T cells (Tfh) support high‐affinity Ab production by germinal center B cells through both membrane interactions and secretion of IL‐4 and ‐21, two major cytokines implicated in B‐cell survival and Ab class switch. Tfh‐2 cells recently emerged in humans as a strong IL‐4 producer Tfh cell subset implicated in both autoimmune and allergic diseases. Although the molecular mechanisms governing Tfh cell differentiation from naive T cells have been widely described, much less is known about the regulation of cytokine secretion by mouse Tfh‐2 cells. The purpose of our study was to evaluate the role of dendritic cell–derived IL‐6 in fine‐tuning cytokine secretion by Tfh cells. Our results demonstrate that priming of Th cells by IL‐6‐deficient antigen‐presenting dendritic cells preferentially leads to accumulation of a subset of Tfh cells characterized by high expression of GATA3 and IL‐4, associated with reduced production of IL‐21. STAT3‐deficient Tfh cells also overexpress GATA3, suggesting that early IL‐6/STAT3 signaling during Tfh cell development inhibits the expression of a set of genes associated with the Th2 differentiation program. Overall, our data indicate that IL‐6/STAT3 signaling restrains the expression of Th2‐like genes in Tfh cells, thus contributing to the control of IgE secretion in vivo.
IL‐6/STAT3 signaling modulates the cytokine and transcription factor pattern of Tfh cells and controls IgE secretion in vivo.</abstract><cop>United States</cop><pub>Oxford University Press</pub><pmid>27474166</pmid><doi>10.1189/jlb.1HI1115-511R</doi><tpages>10</tpages><oa>free_for_read</oa></addata></record> |
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| source | Oxford University Press Journals All Titles (1996-Current); MEDLINE; Wiley Online Library Journals Frontfile Complete; EZB-FREE-00999 freely available EZB journals; Alma/SFX Local Collection |
| subjects | Allergic diseases Animals Antigen-presenting cells Antigen-Presenting Cells - metabolism Antigens Antigens - immunology B-Lymphocytes - immunology Bone Marrow Cells - metabolism Cell Differentiation Cell survival Class switching Cytokines Dendritic cells Dendritic Cells - metabolism Differentiation (biology) GATA-3 protein GATA3 Transcription Factor - metabolism Gene expression Gene Expression Profiling Genes Helper cells humoral response Immunization Immunoglobulin Class Switching Immunoglobulin E Immunoglobulin E - metabolism Interleukin 21 Interleukin 4 Interleukin 6 Interleukin-12 - metabolism Interleukin-4 - metabolism Interleukin-6 - metabolism Lymphocytes Lymphocytes B Lymphocytes T Mice, Inbred C57BL Molecular modelling Priming RNA, Messenger - genetics RNA, Messenger - metabolism Signal Transduction Signaling Spotlight on Leading Edge Research STAT3 Stat3 protein STAT3 Transcription Factor - metabolism T cell receptors T-Lymphocytes, Helper-Inducer - metabolism Tfh‐2 Transcription Factors - genetics Transcription Factors - metabolism |
| title | Antigen‐presenting cell‐derived IL‐6 restricts the expression of GATA3 and IL‐4 by follicular helper T cells |
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