Plasticity of Foxp3+ T Cells Reflects Promiscuous Foxp3 Expression in Conventional T Cells but Not Reprogramming of Regulatory T Cells
The emerging notion of environment-induced reprogramming of Foxp3+ regulatory T (Treg) cells into helper T (Th) cells remains controversial. By genetic fate mapping or adoptive transfers, we have identified a minor population of nonregulatory Foxp3+ T cells exhibiting promiscuous and transient Foxp3...
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| Veröffentlicht in: | Immunity (Cambridge, Mass.) Mass.), 2012-02, Vol.36 (2), p.262-275 |
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| creator | Miyao, Takahisa Floess, Stefan Setoguchi, Ruka Luche, Hervé Fehling, Hans Joerg Waldmann, Herman Huehn, Jochen Hori, Shohei |
| description | The emerging notion of environment-induced reprogramming of Foxp3+ regulatory T (Treg) cells into helper T (Th) cells remains controversial. By genetic fate mapping or adoptive transfers, we have identified a minor population of nonregulatory Foxp3+ T cells exhibiting promiscuous and transient Foxp3 expression, which gave rise to Foxp3− (“exFoxp3”) Th cells and selectively accumulated in inflammatory cytokine milieus or in lymphopenic environments including those in early ontogeny. In contrast, Treg cells did not undergo reprogramming under those conditions irrespective of their thymic or peripheral origins. Moreover, although a few Treg cells transiently lose Foxp3 expression, such “latent” Treg cells retained their memory and robustly re-expressed Foxp3 and suppressive function upon activation. This study establishes that Treg cells constitute a stable cell lineage, whose committed state in a changing environment is ensured by DNA demethylation of the Foxp3 locus irrespectively of ongoing Foxp3 expression.
► Foxp3+ T cells contain a minor nonregulatory population ► Th cells can be generated from Foxp3+ non-Treg cells but not Treg cells ► A few Treg cells transiently lose Foxp3 expression but retain its memory ► The committed state of Treg cells is ensured by TSDR demethylation |
| doi_str_mv | 10.1016/j.immuni.2011.12.012 |
| format | Article |
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► Foxp3+ T cells contain a minor nonregulatory population ► Th cells can be generated from Foxp3+ non-Treg cells but not Treg cells ► A few Treg cells transiently lose Foxp3 expression but retain its memory ► The committed state of Treg cells is ensured by TSDR demethylation</description><identifier>ISSN: 1074-7613</identifier><identifier>EISSN: 1097-4180</identifier><identifier>DOI: 10.1016/j.immuni.2011.12.012</identifier><identifier>PMID: 22326580</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Animals ; Artificial chromosomes ; CD2 Antigens - genetics ; CD2 Antigens - metabolism ; CD4-Positive T-Lymphocytes - cytology ; CD4-Positive T-Lymphocytes - immunology ; CD4-Positive T-Lymphocytes - metabolism ; Cell Differentiation ; Cell division ; Cell Lineage - genetics ; Cell Lineage - immunology ; Cytokines ; Deoxyribonucleic acid ; DNA ; DNA Methylation ; Epigenesis, Genetic ; Forkhead Transcription Factors - genetics ; Forkhead Transcription Factors - metabolism ; Gene Expression ; Genotype & phenotype ; Homeostasis ; Humans ; Immunologic Memory ; In Vitro Techniques ; Inflammation - immunology ; Inflammation - metabolism ; Inflammation - pathology ; Interleukin-2 Receptor alpha Subunit - metabolism ; Lymphocyte Activation ; Lymphocytes ; Lymphopenia - immunology ; Lymphopenia - metabolism ; Lymphopenia - pathology ; Mice ; Mice, Knockout ; Mice, Transgenic ; Proteins ; Rodents ; Science ; Software ; T-Lymphocyte Subsets - cytology ; T-Lymphocyte Subsets - immunology ; T-Lymphocyte Subsets - metabolism ; T-Lymphocytes, Regulatory - cytology ; T-Lymphocytes, Regulatory - immunology ; T-Lymphocytes, Regulatory - metabolism ; Transcription factors</subject><ispartof>Immunity (Cambridge, Mass.), 2012-02, Vol.36 (2), p.262-275</ispartof><rights>2012 Elsevier Inc.</rights><rights>Copyright © 2012 Elsevier Inc. All rights reserved.</rights><rights>Copyright Elsevier Limited Feb 24, 2012</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c435t-3237b7f625955317b8fa4918e7bf4cfd8e97c9e381c1912be4f47b1fd5d077ab3</citedby><cites>FETCH-LOGICAL-c435t-3237b7f625955317b8fa4918e7bf4cfd8e97c9e381c1912be4f47b1fd5d077ab3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S1074761312000404$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>314,776,780,3537,27901,27902,65306</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/22326580$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Miyao, Takahisa</creatorcontrib><creatorcontrib>Floess, Stefan</creatorcontrib><creatorcontrib>Setoguchi, Ruka</creatorcontrib><creatorcontrib>Luche, Hervé</creatorcontrib><creatorcontrib>Fehling, Hans Joerg</creatorcontrib><creatorcontrib>Waldmann, Herman</creatorcontrib><creatorcontrib>Huehn, Jochen</creatorcontrib><creatorcontrib>Hori, Shohei</creatorcontrib><title>Plasticity of Foxp3+ T Cells Reflects Promiscuous Foxp3 Expression in Conventional T Cells but Not Reprogramming of Regulatory T Cells</title><title>Immunity (Cambridge, Mass.)</title><addtitle>Immunity</addtitle><description>The emerging notion of environment-induced reprogramming of Foxp3+ regulatory T (Treg) cells into helper T (Th) cells remains controversial. By genetic fate mapping or adoptive transfers, we have identified a minor population of nonregulatory Foxp3+ T cells exhibiting promiscuous and transient Foxp3 expression, which gave rise to Foxp3− (“exFoxp3”) Th cells and selectively accumulated in inflammatory cytokine milieus or in lymphopenic environments including those in early ontogeny. In contrast, Treg cells did not undergo reprogramming under those conditions irrespective of their thymic or peripheral origins. Moreover, although a few Treg cells transiently lose Foxp3 expression, such “latent” Treg cells retained their memory and robustly re-expressed Foxp3 and suppressive function upon activation. This study establishes that Treg cells constitute a stable cell lineage, whose committed state in a changing environment is ensured by DNA demethylation of the Foxp3 locus irrespectively of ongoing Foxp3 expression.
► Foxp3+ T cells contain a minor nonregulatory population ► Th cells can be generated from Foxp3+ non-Treg cells but not Treg cells ► A few Treg cells transiently lose Foxp3 expression but retain its memory ► The committed state of Treg cells is ensured by TSDR demethylation</description><subject>Animals</subject><subject>Artificial chromosomes</subject><subject>CD2 Antigens - genetics</subject><subject>CD2 Antigens - metabolism</subject><subject>CD4-Positive T-Lymphocytes - cytology</subject><subject>CD4-Positive T-Lymphocytes - immunology</subject><subject>CD4-Positive T-Lymphocytes - metabolism</subject><subject>Cell Differentiation</subject><subject>Cell division</subject><subject>Cell Lineage - genetics</subject><subject>Cell Lineage - immunology</subject><subject>Cytokines</subject><subject>Deoxyribonucleic acid</subject><subject>DNA</subject><subject>DNA Methylation</subject><subject>Epigenesis, Genetic</subject><subject>Forkhead Transcription Factors - genetics</subject><subject>Forkhead Transcription Factors - metabolism</subject><subject>Gene Expression</subject><subject>Genotype & phenotype</subject><subject>Homeostasis</subject><subject>Humans</subject><subject>Immunologic Memory</subject><subject>In Vitro Techniques</subject><subject>Inflammation - immunology</subject><subject>Inflammation - metabolism</subject><subject>Inflammation - pathology</subject><subject>Interleukin-2 Receptor alpha Subunit - metabolism</subject><subject>Lymphocyte Activation</subject><subject>Lymphocytes</subject><subject>Lymphopenia - immunology</subject><subject>Lymphopenia - metabolism</subject><subject>Lymphopenia - pathology</subject><subject>Mice</subject><subject>Mice, Knockout</subject><subject>Mice, Transgenic</subject><subject>Proteins</subject><subject>Rodents</subject><subject>Science</subject><subject>Software</subject><subject>T-Lymphocyte Subsets - cytology</subject><subject>T-Lymphocyte Subsets - immunology</subject><subject>T-Lymphocyte Subsets - metabolism</subject><subject>T-Lymphocytes, Regulatory - cytology</subject><subject>T-Lymphocytes, Regulatory - immunology</subject><subject>T-Lymphocytes, Regulatory - metabolism</subject><subject>Transcription factors</subject><issn>1074-7613</issn><issn>1097-4180</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2012</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kc1q3DAUhU1padK0b1CKoIsuil1dSbasTaEM-SmEJIR0LWz5atBgW1PJDpkXyHNHxkkWXXQlCb5z7j06WfYZaAEUqh-7wg3DPLqCUYACWEGBvcmOgSqZC6jp2-UuRS4r4EfZhxh3lIIoFX2fHTHGWVXW9Dh7vOmbODnjpgPxlpz5hz3_Tu7IBvs-klu0PZopkpvgBxfN7Oe4MuT0YR8wRudH4kay8eM9jlN6Nf2rup0ncuWn5LIPfhuaYXDjdplyi9u5byYfDi_sx-ydbfqIn57Pk-zP2end5iK_vD7_vfl1mRvByynnjMtW2oqVqiw5yLa2jVBQo2ytMLarUUmjkNdgQAFrUVghW7Bd2VEpm5afZN9W37TR3xnjpJdYaYNmxJRNK8aTMwiWyK__kDs_hxQvaqiEkFxIpRIlVsoEH2NAq_fBDU04aKB6qUnv9FqTXmrSwHSqKcm-PJvP7YDdq-illwT8XAFMn3HvMOhoHI4GOxdSIbrz7v8TngDngqXF</recordid><startdate>20120224</startdate><enddate>20120224</enddate><creator>Miyao, Takahisa</creator><creator>Floess, Stefan</creator><creator>Setoguchi, Ruka</creator><creator>Luche, Hervé</creator><creator>Fehling, Hans Joerg</creator><creator>Waldmann, Herman</creator><creator>Huehn, Jochen</creator><creator>Hori, Shohei</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>20120224</creationdate><title>Plasticity of Foxp3+ T Cells Reflects Promiscuous Foxp3 Expression in Conventional T Cells but Not Reprogramming of Regulatory T Cells</title><author>Miyao, Takahisa ; 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By genetic fate mapping or adoptive transfers, we have identified a minor population of nonregulatory Foxp3+ T cells exhibiting promiscuous and transient Foxp3 expression, which gave rise to Foxp3− (“exFoxp3”) Th cells and selectively accumulated in inflammatory cytokine milieus or in lymphopenic environments including those in early ontogeny. In contrast, Treg cells did not undergo reprogramming under those conditions irrespective of their thymic or peripheral origins. Moreover, although a few Treg cells transiently lose Foxp3 expression, such “latent” Treg cells retained their memory and robustly re-expressed Foxp3 and suppressive function upon activation. This study establishes that Treg cells constitute a stable cell lineage, whose committed state in a changing environment is ensured by DNA demethylation of the Foxp3 locus irrespectively of ongoing Foxp3 expression.
► Foxp3+ T cells contain a minor nonregulatory population ► Th cells can be generated from Foxp3+ non-Treg cells but not Treg cells ► A few Treg cells transiently lose Foxp3 expression but retain its memory ► The committed state of Treg cells is ensured by TSDR demethylation</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>22326580</pmid><doi>10.1016/j.immuni.2011.12.012</doi><tpages>14</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Animals Artificial chromosomes CD2 Antigens - genetics CD2 Antigens - metabolism CD4-Positive T-Lymphocytes - cytology CD4-Positive T-Lymphocytes - immunology CD4-Positive T-Lymphocytes - metabolism Cell Differentiation Cell division Cell Lineage - genetics Cell Lineage - immunology Cytokines Deoxyribonucleic acid DNA DNA Methylation Epigenesis, Genetic Forkhead Transcription Factors - genetics Forkhead Transcription Factors - metabolism Gene Expression Genotype & phenotype Homeostasis Humans Immunologic Memory In Vitro Techniques Inflammation - immunology Inflammation - metabolism Inflammation - pathology Interleukin-2 Receptor alpha Subunit - metabolism Lymphocyte Activation Lymphocytes Lymphopenia - immunology Lymphopenia - metabolism Lymphopenia - pathology Mice Mice, Knockout Mice, Transgenic Proteins Rodents Science Software T-Lymphocyte Subsets - cytology T-Lymphocyte Subsets - immunology T-Lymphocyte Subsets - metabolism T-Lymphocytes, Regulatory - cytology T-Lymphocytes, Regulatory - immunology T-Lymphocytes, Regulatory - metabolism Transcription factors |
| title | Plasticity of Foxp3+ T Cells Reflects Promiscuous Foxp3 Expression in Conventional T Cells but Not Reprogramming of Regulatory T Cells |
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