Early Th1 Cell Differentiation Is Marked by a Tfh Cell-like Transition
Follicular helper T (Tfh) cells comprise an important subset of helper T cells; however, their relationship with other helper lineages is incompletely understood. Herein, we showed interleukin-12 acting via the transcription factor STAT4 induced both Il21 and Bcl6 genes, generating cells with featur...
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| Veröffentlicht in: | Immunity (Cambridge, Mass.) Mass.), 2011-12, Vol.35 (6), p.919-931 |
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| creator | Nakayamada, Shingo Kanno, Yuka Takahashi, Hayato Jankovic, Dragana Lu, Kristina T. Johnson, Thomas A. Sun, Hong-wei Vahedi, Golnaz Hakim, Ofir Handon, Robin Schwartzberg, Pamela L. Hager, Gordon L. O'Shea, John J. |
| description | Follicular helper T (Tfh) cells comprise an important subset of helper T cells; however, their relationship with other helper lineages is incompletely understood. Herein, we showed interleukin-12 acting via the transcription factor STAT4 induced both
Il21 and
Bcl6 genes, generating cells with features of both Tfh and Th1 cells. However, STAT4 also induced the transcription factor T-bet. With ChIP-seq, we defined the genome-wide targets of T-bet and found that it repressed
Bcl6 and other markers of Tfh cells, thereby attenuating the nascent Tfh cell-like phenotype in the late phase of Th1 cell specification. Tfh-like cells were rapidly generated after
Toxoplasma gondii infection in mice, but T-bet constrained Tfh cell expansion and consequent germinal center formation and antibody production. Our data argue that Tfh and Th1 cells share a transitional stage through the signal mediated by STAT4, which promotes both phenotypes. However, T-bet represses Tfh cell functionalities, promoting full Th1 cell differentiation.
[Display omitted]
► STAT4 drives
Il21 and
Bcl6 genes to create a cell with Tfh and Th1 cell features ► IFN-γ and T-bet attenuates the Tfh cell-like phenotype at later stage of the specification ► The
Bcl6 locus remains accessible in fully polarized Th1 cells ► T-bet limits Tfh and germinal center B cell generation during
T. gondii infection |
| doi_str_mv | 10.1016/j.immuni.2011.11.012 |
| format | Article |
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Il21 and
Bcl6 genes, generating cells with features of both Tfh and Th1 cells. However, STAT4 also induced the transcription factor T-bet. With ChIP-seq, we defined the genome-wide targets of T-bet and found that it repressed
Bcl6 and other markers of Tfh cells, thereby attenuating the nascent Tfh cell-like phenotype in the late phase of Th1 cell specification. Tfh-like cells were rapidly generated after
Toxoplasma gondii infection in mice, but T-bet constrained Tfh cell expansion and consequent germinal center formation and antibody production. Our data argue that Tfh and Th1 cells share a transitional stage through the signal mediated by STAT4, which promotes both phenotypes. However, T-bet represses Tfh cell functionalities, promoting full Th1 cell differentiation.
[Display omitted]
► STAT4 drives
Il21 and
Bcl6 genes to create a cell with Tfh and Th1 cell features ► IFN-γ and T-bet attenuates the Tfh cell-like phenotype at later stage of the specification ► The
Bcl6 locus remains accessible in fully polarized Th1 cells ► T-bet limits Tfh and germinal center B cell generation during
T. gondii infection</description><identifier>ISSN: 1074-7613</identifier><identifier>ISSN: 1097-4180</identifier><identifier>EISSN: 1097-4180</identifier><identifier>DOI: 10.1016/j.immuni.2011.11.012</identifier><identifier>PMID: 22195747</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Animals ; Antibodies ; Bcl-6 protein ; CD4-Positive T-Lymphocytes - immunology ; CD4-Positive T-Lymphocytes - metabolism ; CD4-Positive T-Lymphocytes - parasitology ; Cell Differentiation ; Cysts ; Cytokines ; Data processing ; Differentiation ; DNA-Binding Proteins - genetics ; Gene expression ; Gene Expression Regulation - drug effects ; Germinal centers ; Helper cells ; Immunophenotyping ; Infection ; Infrared imaging systems ; Interferon-gamma - metabolism ; Interleukin 12 ; Interleukin 21 ; Interleukin-12 - pharmacology ; Lymphocytes T ; Medical research ; Mice ; Mice, Inbred C57BL ; Mice, Transgenic ; Proto-Oncogene Proteins c-bcl-6 ; Stat4 protein ; STAT4 Transcription Factor - metabolism ; T-Box Domain Proteins - metabolism ; T-Lymphocytes, Helper-Inducer - cytology ; T-Lymphocytes, Helper-Inducer - immunology ; T-Lymphocytes, Helper-Inducer - metabolism ; Th1 Cells - cytology ; Th1 Cells - immunology ; Th1 Cells - metabolism ; Toxoplasma ; Toxoplasma gondii ; Transcription factors</subject><ispartof>Immunity (Cambridge, Mass.), 2011-12, Vol.35 (6), p.919-931</ispartof><rights>2011 Elsevier Inc.</rights><rights>Copyright © 2011 Elsevier Inc. All rights reserved.</rights><rights>Copyright Elsevier Limited Dec 23, 2011</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c585t-f110970f3e270c43bdeb84918a5066e6a6e876372d92b6e326e62144105cca343</citedby><cites>FETCH-LOGICAL-c585t-f110970f3e270c43bdeb84918a5066e6a6e876372d92b6e326e62144105cca343</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.2011.11.012$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>314,780,784,3550,27924,27925,45995</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/22195747$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Nakayamada, Shingo</creatorcontrib><creatorcontrib>Kanno, Yuka</creatorcontrib><creatorcontrib>Takahashi, Hayato</creatorcontrib><creatorcontrib>Jankovic, Dragana</creatorcontrib><creatorcontrib>Lu, Kristina T.</creatorcontrib><creatorcontrib>Johnson, Thomas A.</creatorcontrib><creatorcontrib>Sun, Hong-wei</creatorcontrib><creatorcontrib>Vahedi, Golnaz</creatorcontrib><creatorcontrib>Hakim, Ofir</creatorcontrib><creatorcontrib>Handon, Robin</creatorcontrib><creatorcontrib>Schwartzberg, Pamela L.</creatorcontrib><creatorcontrib>Hager, Gordon L.</creatorcontrib><creatorcontrib>O'Shea, John J.</creatorcontrib><title>Early Th1 Cell Differentiation Is Marked by a Tfh Cell-like Transition</title><title>Immunity (Cambridge, Mass.)</title><addtitle>Immunity</addtitle><description>Follicular helper T (Tfh) cells comprise an important subset of helper T cells; however, their relationship with other helper lineages is incompletely understood. Herein, we showed interleukin-12 acting via the transcription factor STAT4 induced both
Il21 and
Bcl6 genes, generating cells with features of both Tfh and Th1 cells. However, STAT4 also induced the transcription factor T-bet. With ChIP-seq, we defined the genome-wide targets of T-bet and found that it repressed
Bcl6 and other markers of Tfh cells, thereby attenuating the nascent Tfh cell-like phenotype in the late phase of Th1 cell specification. Tfh-like cells were rapidly generated after
Toxoplasma gondii infection in mice, but T-bet constrained Tfh cell expansion and consequent germinal center formation and antibody production. Our data argue that Tfh and Th1 cells share a transitional stage through the signal mediated by STAT4, which promotes both phenotypes. However, T-bet represses Tfh cell functionalities, promoting full Th1 cell differentiation.
[Display omitted]
► STAT4 drives
Il21 and
Bcl6 genes to create a cell with Tfh and Th1 cell features ► IFN-γ and T-bet attenuates the Tfh cell-like phenotype at later stage of the specification ► The
Bcl6 locus remains accessible in fully polarized Th1 cells ► T-bet limits Tfh and germinal center B cell generation during
T. gondii infection</description><subject>Animals</subject><subject>Antibodies</subject><subject>Bcl-6 protein</subject><subject>CD4-Positive T-Lymphocytes - immunology</subject><subject>CD4-Positive T-Lymphocytes - metabolism</subject><subject>CD4-Positive T-Lymphocytes - parasitology</subject><subject>Cell Differentiation</subject><subject>Cysts</subject><subject>Cytokines</subject><subject>Data processing</subject><subject>Differentiation</subject><subject>DNA-Binding Proteins - genetics</subject><subject>Gene expression</subject><subject>Gene Expression Regulation - drug effects</subject><subject>Germinal centers</subject><subject>Helper cells</subject><subject>Immunophenotyping</subject><subject>Infection</subject><subject>Infrared imaging systems</subject><subject>Interferon-gamma - metabolism</subject><subject>Interleukin 12</subject><subject>Interleukin 21</subject><subject>Interleukin-12 - pharmacology</subject><subject>Lymphocytes T</subject><subject>Medical research</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Mice, Transgenic</subject><subject>Proto-Oncogene Proteins c-bcl-6</subject><subject>Stat4 protein</subject><subject>STAT4 Transcription Factor - metabolism</subject><subject>T-Box Domain Proteins - metabolism</subject><subject>T-Lymphocytes, Helper-Inducer - cytology</subject><subject>T-Lymphocytes, Helper-Inducer - immunology</subject><subject>T-Lymphocytes, Helper-Inducer - metabolism</subject><subject>Th1 Cells - cytology</subject><subject>Th1 Cells - immunology</subject><subject>Th1 Cells - metabolism</subject><subject>Toxoplasma</subject><subject>Toxoplasma gondii</subject><subject>Transcription factors</subject><issn>1074-7613</issn><issn>1097-4180</issn><issn>1097-4180</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2011</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kU1r3DAQhkVpSDZp_kEpgh6aizcaWR_2pRA2SRtIyGV7FrI8ZrXxx1ayC_vvI--mPfQQGJAQz7wa6SHkM7AlMFDX26Xvuqn3S84AlqkY8A9kAazUmYCCfZz3WmRaQX5GzmPcMgZCluyUnHEOpdRCL8j9nQ3tnq43QFfYtvTWNw0G7EdvRz_09CHSJxtesKbVnlq6bjYHLmv9C9J1sH30M_eJnDS2jXj5tl6QX_d369XP7PH5x8Pq5jFzspBj1sA8Hmty5Jo5kVc1VoUoobCSKYXKKiy0yjWvS14pzHk64yAEMOmczUV-Qb4dc3dh-D1hHE3no0sD2R6HKZoSuC61UCqRV--SwDiXSnMpE_r1P3Q7TKFP7zAgmeCqlIdAcaRcGGIM2Jhd8J0N-xRlZiNma45GzGzEpEpGUtuXt_Cp6rD-1_RXQQK-HwFM__bHYzDReewd1j6gG009-PdveAWaVJpB</recordid><startdate>20111223</startdate><enddate>20111223</enddate><creator>Nakayamada, Shingo</creator><creator>Kanno, Yuka</creator><creator>Takahashi, Hayato</creator><creator>Jankovic, Dragana</creator><creator>Lu, Kristina T.</creator><creator>Johnson, Thomas A.</creator><creator>Sun, Hong-wei</creator><creator>Vahedi, Golnaz</creator><creator>Hakim, Ofir</creator><creator>Handon, Robin</creator><creator>Schwartzberg, Pamela L.</creator><creator>Hager, Gordon L.</creator><creator>O'Shea, John J.</creator><general>Elsevier Inc</general><general>Elsevier Limited</general><scope>6I.</scope><scope>AAFTH</scope><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></search><sort><creationdate>20111223</creationdate><title>Early Th1 Cell Differentiation Is Marked by a Tfh Cell-like Transition</title><author>Nakayamada, Shingo ; Kanno, Yuka ; Takahashi, Hayato ; Jankovic, Dragana ; Lu, Kristina T. ; Johnson, Thomas A. ; Sun, Hong-wei ; Vahedi, Golnaz ; Hakim, Ofir ; Handon, Robin ; Schwartzberg, Pamela L. ; Hager, Gordon L. ; O'Shea, John J.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c585t-f110970f3e270c43bdeb84918a5066e6a6e876372d92b6e326e62144105cca343</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2011</creationdate><topic>Animals</topic><topic>Antibodies</topic><topic>Bcl-6 protein</topic><topic>CD4-Positive T-Lymphocytes - immunology</topic><topic>CD4-Positive T-Lymphocytes - metabolism</topic><topic>CD4-Positive T-Lymphocytes - parasitology</topic><topic>Cell Differentiation</topic><topic>Cysts</topic><topic>Cytokines</topic><topic>Data processing</topic><topic>Differentiation</topic><topic>DNA-Binding Proteins - genetics</topic><topic>Gene expression</topic><topic>Gene Expression Regulation - drug effects</topic><topic>Germinal centers</topic><topic>Helper cells</topic><topic>Immunophenotyping</topic><topic>Infection</topic><topic>Infrared imaging systems</topic><topic>Interferon-gamma - metabolism</topic><topic>Interleukin 12</topic><topic>Interleukin 21</topic><topic>Interleukin-12 - pharmacology</topic><topic>Lymphocytes T</topic><topic>Medical research</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>Mice, Transgenic</topic><topic>Proto-Oncogene Proteins c-bcl-6</topic><topic>Stat4 protein</topic><topic>STAT4 Transcription Factor - metabolism</topic><topic>T-Box Domain Proteins - metabolism</topic><topic>T-Lymphocytes, Helper-Inducer - cytology</topic><topic>T-Lymphocytes, Helper-Inducer - immunology</topic><topic>T-Lymphocytes, Helper-Inducer - metabolism</topic><topic>Th1 Cells - cytology</topic><topic>Th1 Cells - immunology</topic><topic>Th1 Cells - metabolism</topic><topic>Toxoplasma</topic><topic>Toxoplasma gondii</topic><topic>Transcription factors</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Nakayamada, Shingo</creatorcontrib><creatorcontrib>Kanno, Yuka</creatorcontrib><creatorcontrib>Takahashi, Hayato</creatorcontrib><creatorcontrib>Jankovic, Dragana</creatorcontrib><creatorcontrib>Lu, Kristina T.</creatorcontrib><creatorcontrib>Johnson, Thomas A.</creatorcontrib><creatorcontrib>Sun, Hong-wei</creatorcontrib><creatorcontrib>Vahedi, Golnaz</creatorcontrib><creatorcontrib>Hakim, Ofir</creatorcontrib><creatorcontrib>Handon, Robin</creatorcontrib><creatorcontrib>Schwartzberg, Pamela L.</creatorcontrib><creatorcontrib>Hager, Gordon L.</creatorcontrib><creatorcontrib>O'Shea, John J.</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><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><jtitle>Immunity (Cambridge, Mass.)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Nakayamada, Shingo</au><au>Kanno, Yuka</au><au>Takahashi, Hayato</au><au>Jankovic, Dragana</au><au>Lu, Kristina T.</au><au>Johnson, Thomas A.</au><au>Sun, Hong-wei</au><au>Vahedi, Golnaz</au><au>Hakim, Ofir</au><au>Handon, Robin</au><au>Schwartzberg, Pamela L.</au><au>Hager, Gordon L.</au><au>O'Shea, John J.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Early Th1 Cell Differentiation Is Marked by a Tfh Cell-like Transition</atitle><jtitle>Immunity (Cambridge, Mass.)</jtitle><addtitle>Immunity</addtitle><date>2011-12-23</date><risdate>2011</risdate><volume>35</volume><issue>6</issue><spage>919</spage><epage>931</epage><pages>919-931</pages><issn>1074-7613</issn><issn>1097-4180</issn><eissn>1097-4180</eissn><abstract>Follicular helper T (Tfh) cells comprise an important subset of helper T cells; however, their relationship with other helper lineages is incompletely understood. Herein, we showed interleukin-12 acting via the transcription factor STAT4 induced both
Il21 and
Bcl6 genes, generating cells with features of both Tfh and Th1 cells. However, STAT4 also induced the transcription factor T-bet. With ChIP-seq, we defined the genome-wide targets of T-bet and found that it repressed
Bcl6 and other markers of Tfh cells, thereby attenuating the nascent Tfh cell-like phenotype in the late phase of Th1 cell specification. Tfh-like cells were rapidly generated after
Toxoplasma gondii infection in mice, but T-bet constrained Tfh cell expansion and consequent germinal center formation and antibody production. Our data argue that Tfh and Th1 cells share a transitional stage through the signal mediated by STAT4, which promotes both phenotypes. However, T-bet represses Tfh cell functionalities, promoting full Th1 cell differentiation.
[Display omitted]
► STAT4 drives
Il21 and
Bcl6 genes to create a cell with Tfh and Th1 cell features ► IFN-γ and T-bet attenuates the Tfh cell-like phenotype at later stage of the specification ► The
Bcl6 locus remains accessible in fully polarized Th1 cells ► T-bet limits Tfh and germinal center B cell generation during
T. gondii infection</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>22195747</pmid><doi>10.1016/j.immuni.2011.11.012</doi><tpages>13</tpages><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1074-7613 |
| ispartof | Immunity (Cambridge, Mass.), 2011-12, Vol.35 (6), p.919-931 |
| issn | 1074-7613 1097-4180 1097-4180 |
| language | eng |
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| source | MEDLINE; Cell Press Free Archives; Access via ScienceDirect (Elsevier); EZB-FREE-00999 freely available EZB journals |
| subjects | Animals Antibodies Bcl-6 protein CD4-Positive T-Lymphocytes - immunology CD4-Positive T-Lymphocytes - metabolism CD4-Positive T-Lymphocytes - parasitology Cell Differentiation Cysts Cytokines Data processing Differentiation DNA-Binding Proteins - genetics Gene expression Gene Expression Regulation - drug effects Germinal centers Helper cells Immunophenotyping Infection Infrared imaging systems Interferon-gamma - metabolism Interleukin 12 Interleukin 21 Interleukin-12 - pharmacology Lymphocytes T Medical research Mice Mice, Inbred C57BL Mice, Transgenic Proto-Oncogene Proteins c-bcl-6 Stat4 protein STAT4 Transcription Factor - metabolism T-Box Domain Proteins - metabolism T-Lymphocytes, Helper-Inducer - cytology T-Lymphocytes, Helper-Inducer - immunology T-Lymphocytes, Helper-Inducer - metabolism Th1 Cells - cytology Th1 Cells - immunology Th1 Cells - metabolism Toxoplasma Toxoplasma gondii Transcription factors |
| title | Early Th1 Cell Differentiation Is Marked by a Tfh Cell-like Transition |
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