CCL22 controls immunity by promoting regulatory T cell communication with dendritic cells in lymph nodes
Chemokines have crucial roles in organ development and orchestration of leukocyte migration. The chemokine CCL22 is expressed constitutively at high levels in the lymph node, but the functional significance of this expression is so far unknown. Studying a newly established CCL22-deficient mouse, we...
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| Veröffentlicht in: | The Journal of experimental medicine 2019-05, Vol.216 (5), p.1170-1181 |
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| creator | Rapp, Moritz Wintergerst, Maximilian W M Kunz, Wolfgang G Vetter, Viola K Knott, Max M L Lisowski, Dominik Haubner, Sascha Moder, Stefan Thaler, Raffael Eiber, Stephan Meyer, Bastian Röhrle, Natascha Piseddu, Ignazio Grassmann, Simon Layritz, Patrick Kühnemuth, Benjamin Stutte, Susanne Bourquin, Carole von Andrian, Ulrich H Endres, Stefan Anz, David |
| description | Chemokines have crucial roles in organ development and orchestration of leukocyte migration. The chemokine CCL22 is expressed constitutively at high levels in the lymph node, but the functional significance of this expression is so far unknown. Studying a newly established CCL22-deficient mouse, we demonstrate that CCL22 expression by dendritic cells (DCs) promotes the formation of cell-cell contacts and interaction with regulatory T cells (T reg) through their CCR4 receptor. Vaccination of CCL22-deficient mice led to excessive T cell responses that were also observed when wild-type mice were vaccinated using CCL22-deficient DCs. Tumor-bearing mice with CCL22 deficiency showed prolonged survival upon vaccination, and further, CCL22-deficient mice had increased susceptibility to inflammatory disease. In conclusion, we identify the CCL22-CCR4 axis as an immune checkpoint that is crucial for the control of T cell immunity. |
| doi_str_mv | 10.1084/jem.20170277 |
| format | Article |
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The chemokine CCL22 is expressed constitutively at high levels in the lymph node, but the functional significance of this expression is so far unknown. Studying a newly established CCL22-deficient mouse, we demonstrate that CCL22 expression by dendritic cells (DCs) promotes the formation of cell-cell contacts and interaction with regulatory T cells (T reg) through their CCR4 receptor. Vaccination of CCL22-deficient mice led to excessive T cell responses that were also observed when wild-type mice were vaccinated using CCL22-deficient DCs. Tumor-bearing mice with CCL22 deficiency showed prolonged survival upon vaccination, and further, CCL22-deficient mice had increased susceptibility to inflammatory disease. In conclusion, we identify the CCL22-CCR4 axis as an immune checkpoint that is crucial for the control of T cell immunity.</description><identifier>ISSN: 0022-1007</identifier><identifier>EISSN: 1540-9538</identifier><identifier>DOI: 10.1084/jem.20170277</identifier><identifier>PMID: 30910796</identifier><language>eng</language><publisher>United States: Rockefeller University Press</publisher><subject>Animals ; Bone Marrow Cells - immunology ; Cell Communication - immunology ; Cell Line, Tumor ; Cell Movement ; Chemokine CCL22 - genetics ; Chemokine CCL22 - immunology ; Dendritic Cells - immunology ; HEK293 Cells ; Humans ; Lymph Nodes - cytology ; Lymph Nodes - immunology ; Mice ; Mice, Inbred BALB C ; Mice, Inbred C57BL ; Mice, Knockout ; Receptors, CCR4 - metabolism ; T-Lymphocytes, Regulatory - immunology ; Transplantation, Homologous</subject><ispartof>The Journal of experimental medicine, 2019-05, Vol.216 (5), p.1170-1181</ispartof><rights>2019 Rapp et al.</rights><rights>2019 Rapp et al. 2019</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c384t-1b6132b045a28f5fed2275cdd532ea917772b30e0f8767b72a8173044c5103a3</citedby><cites>FETCH-LOGICAL-c384t-1b6132b045a28f5fed2275cdd532ea917772b30e0f8767b72a8173044c5103a3</cites><orcidid>0000-0002-5348-1456 ; 0000-0001-5767-3386 ; 0000-0001-5104-7683 ; 0000-0002-4703-537X ; 0000-0002-8336-3418 ; 0000-0003-3862-4583</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,776,780,881,27903,27904</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30910796$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Rapp, Moritz</creatorcontrib><creatorcontrib>Wintergerst, Maximilian W M</creatorcontrib><creatorcontrib>Kunz, Wolfgang G</creatorcontrib><creatorcontrib>Vetter, Viola K</creatorcontrib><creatorcontrib>Knott, Max M L</creatorcontrib><creatorcontrib>Lisowski, Dominik</creatorcontrib><creatorcontrib>Haubner, Sascha</creatorcontrib><creatorcontrib>Moder, Stefan</creatorcontrib><creatorcontrib>Thaler, Raffael</creatorcontrib><creatorcontrib>Eiber, Stephan</creatorcontrib><creatorcontrib>Meyer, Bastian</creatorcontrib><creatorcontrib>Röhrle, Natascha</creatorcontrib><creatorcontrib>Piseddu, Ignazio</creatorcontrib><creatorcontrib>Grassmann, Simon</creatorcontrib><creatorcontrib>Layritz, Patrick</creatorcontrib><creatorcontrib>Kühnemuth, Benjamin</creatorcontrib><creatorcontrib>Stutte, Susanne</creatorcontrib><creatorcontrib>Bourquin, Carole</creatorcontrib><creatorcontrib>von Andrian, Ulrich H</creatorcontrib><creatorcontrib>Endres, Stefan</creatorcontrib><creatorcontrib>Anz, David</creatorcontrib><title>CCL22 controls immunity by promoting regulatory T cell communication with dendritic cells in lymph nodes</title><title>The Journal of experimental medicine</title><addtitle>J Exp Med</addtitle><description>Chemokines have crucial roles in organ development and orchestration of leukocyte migration. The chemokine CCL22 is expressed constitutively at high levels in the lymph node, but the functional significance of this expression is so far unknown. Studying a newly established CCL22-deficient mouse, we demonstrate that CCL22 expression by dendritic cells (DCs) promotes the formation of cell-cell contacts and interaction with regulatory T cells (T reg) through their CCR4 receptor. Vaccination of CCL22-deficient mice led to excessive T cell responses that were also observed when wild-type mice were vaccinated using CCL22-deficient DCs. Tumor-bearing mice with CCL22 deficiency showed prolonged survival upon vaccination, and further, CCL22-deficient mice had increased susceptibility to inflammatory disease. In conclusion, we identify the CCL22-CCR4 axis as an immune checkpoint that is crucial for the control of T cell immunity.</description><subject>Animals</subject><subject>Bone Marrow Cells - immunology</subject><subject>Cell Communication - immunology</subject><subject>Cell Line, Tumor</subject><subject>Cell Movement</subject><subject>Chemokine CCL22 - genetics</subject><subject>Chemokine CCL22 - immunology</subject><subject>Dendritic Cells - immunology</subject><subject>HEK293 Cells</subject><subject>Humans</subject><subject>Lymph Nodes - cytology</subject><subject>Lymph Nodes - immunology</subject><subject>Mice</subject><subject>Mice, Inbred BALB C</subject><subject>Mice, Inbred C57BL</subject><subject>Mice, Knockout</subject><subject>Receptors, CCR4 - metabolism</subject><subject>T-Lymphocytes, Regulatory - immunology</subject><subject>Transplantation, Homologous</subject><issn>0022-1007</issn><issn>1540-9538</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpVkT1v2zAQhomiQe2k3ToXHDtEzvFLlJYChdEkBQx08U5QFGUzkEiXpBLo31dObKOZbrjn3rvDg9BXAisCFb97ssOKApFApfyAlkRwKGrBqo9oCUBpQQDkAl2n9ARAOBflJ7RgUBOQdblE-_V6Qyk2wecY-oTdMIze5Qk3Ez7EMITs_A5Huxt7nUOc8BYb2_fzwCtodHbB4xeX97i1vo0uO_NKzFEe99Nw2GMfWps-o6tO98l-OdUbtL3_tV0_Fps_D7_XPzeFYRXPBWlKwmgDXGhadaKzLaVSmLYVjFpdEyklbRhY6CpZykZSXRHJgHMjCDDNbtCPt9jD2Ay2NXb-S_fqEN2g46SCdup9x7u92oVnVQrglFRzwPdTQAx_R5uyGlw6PqS9DWNSlNSyqokoj-jtG2piSCna7rKGgDq6UbMbdXYz49_-P-0Cn2Wwf9sxi9I</recordid><startdate>20190506</startdate><enddate>20190506</enddate><creator>Rapp, Moritz</creator><creator>Wintergerst, Maximilian W M</creator><creator>Kunz, Wolfgang G</creator><creator>Vetter, Viola K</creator><creator>Knott, Max M L</creator><creator>Lisowski, Dominik</creator><creator>Haubner, Sascha</creator><creator>Moder, Stefan</creator><creator>Thaler, Raffael</creator><creator>Eiber, Stephan</creator><creator>Meyer, Bastian</creator><creator>Röhrle, Natascha</creator><creator>Piseddu, Ignazio</creator><creator>Grassmann, Simon</creator><creator>Layritz, Patrick</creator><creator>Kühnemuth, Benjamin</creator><creator>Stutte, Susanne</creator><creator>Bourquin, Carole</creator><creator>von Andrian, Ulrich H</creator><creator>Endres, Stefan</creator><creator>Anz, David</creator><general>Rockefeller University Press</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/0000-0002-5348-1456</orcidid><orcidid>https://orcid.org/0000-0001-5767-3386</orcidid><orcidid>https://orcid.org/0000-0001-5104-7683</orcidid><orcidid>https://orcid.org/0000-0002-4703-537X</orcidid><orcidid>https://orcid.org/0000-0002-8336-3418</orcidid><orcidid>https://orcid.org/0000-0003-3862-4583</orcidid></search><sort><creationdate>20190506</creationdate><title>CCL22 controls immunity by promoting regulatory T cell communication with dendritic cells in lymph nodes</title><author>Rapp, Moritz ; Wintergerst, Maximilian W M ; Kunz, Wolfgang G ; Vetter, Viola K ; Knott, Max M L ; Lisowski, Dominik ; Haubner, Sascha ; Moder, Stefan ; Thaler, Raffael ; Eiber, Stephan ; Meyer, Bastian ; Röhrle, Natascha ; Piseddu, Ignazio ; Grassmann, Simon ; Layritz, Patrick ; Kühnemuth, Benjamin ; Stutte, Susanne ; Bourquin, Carole ; von Andrian, Ulrich H ; Endres, Stefan ; Anz, David</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c384t-1b6132b045a28f5fed2275cdd532ea917772b30e0f8767b72a8173044c5103a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Animals</topic><topic>Bone Marrow Cells - immunology</topic><topic>Cell Communication - immunology</topic><topic>Cell Line, Tumor</topic><topic>Cell Movement</topic><topic>Chemokine CCL22 - genetics</topic><topic>Chemokine CCL22 - immunology</topic><topic>Dendritic Cells - immunology</topic><topic>HEK293 Cells</topic><topic>Humans</topic><topic>Lymph Nodes - cytology</topic><topic>Lymph Nodes - immunology</topic><topic>Mice</topic><topic>Mice, Inbred BALB C</topic><topic>Mice, Inbred C57BL</topic><topic>Mice, Knockout</topic><topic>Receptors, CCR4 - metabolism</topic><topic>T-Lymphocytes, Regulatory - immunology</topic><topic>Transplantation, Homologous</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Rapp, Moritz</creatorcontrib><creatorcontrib>Wintergerst, Maximilian W M</creatorcontrib><creatorcontrib>Kunz, Wolfgang G</creatorcontrib><creatorcontrib>Vetter, Viola K</creatorcontrib><creatorcontrib>Knott, Max M L</creatorcontrib><creatorcontrib>Lisowski, Dominik</creatorcontrib><creatorcontrib>Haubner, Sascha</creatorcontrib><creatorcontrib>Moder, Stefan</creatorcontrib><creatorcontrib>Thaler, Raffael</creatorcontrib><creatorcontrib>Eiber, Stephan</creatorcontrib><creatorcontrib>Meyer, Bastian</creatorcontrib><creatorcontrib>Röhrle, Natascha</creatorcontrib><creatorcontrib>Piseddu, Ignazio</creatorcontrib><creatorcontrib>Grassmann, Simon</creatorcontrib><creatorcontrib>Layritz, Patrick</creatorcontrib><creatorcontrib>Kühnemuth, Benjamin</creatorcontrib><creatorcontrib>Stutte, Susanne</creatorcontrib><creatorcontrib>Bourquin, Carole</creatorcontrib><creatorcontrib>von Andrian, Ulrich H</creatorcontrib><creatorcontrib>Endres, Stefan</creatorcontrib><creatorcontrib>Anz, David</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Journal of experimental medicine</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Rapp, Moritz</au><au>Wintergerst, Maximilian W M</au><au>Kunz, Wolfgang G</au><au>Vetter, Viola K</au><au>Knott, Max M L</au><au>Lisowski, Dominik</au><au>Haubner, Sascha</au><au>Moder, Stefan</au><au>Thaler, Raffael</au><au>Eiber, Stephan</au><au>Meyer, Bastian</au><au>Röhrle, Natascha</au><au>Piseddu, Ignazio</au><au>Grassmann, Simon</au><au>Layritz, Patrick</au><au>Kühnemuth, Benjamin</au><au>Stutte, Susanne</au><au>Bourquin, Carole</au><au>von Andrian, Ulrich H</au><au>Endres, Stefan</au><au>Anz, David</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>CCL22 controls immunity by promoting regulatory T cell communication with dendritic cells in lymph nodes</atitle><jtitle>The Journal of experimental medicine</jtitle><addtitle>J Exp Med</addtitle><date>2019-05-06</date><risdate>2019</risdate><volume>216</volume><issue>5</issue><spage>1170</spage><epage>1181</epage><pages>1170-1181</pages><issn>0022-1007</issn><eissn>1540-9538</eissn><abstract>Chemokines have crucial roles in organ development and orchestration of leukocyte migration. The chemokine CCL22 is expressed constitutively at high levels in the lymph node, but the functional significance of this expression is so far unknown. Studying a newly established CCL22-deficient mouse, we demonstrate that CCL22 expression by dendritic cells (DCs) promotes the formation of cell-cell contacts and interaction with regulatory T cells (T reg) through their CCR4 receptor. Vaccination of CCL22-deficient mice led to excessive T cell responses that were also observed when wild-type mice were vaccinated using CCL22-deficient DCs. Tumor-bearing mice with CCL22 deficiency showed prolonged survival upon vaccination, and further, CCL22-deficient mice had increased susceptibility to inflammatory disease. In conclusion, we identify the CCL22-CCR4 axis as an immune checkpoint that is crucial for the control of T cell immunity.</abstract><cop>United States</cop><pub>Rockefeller University Press</pub><pmid>30910796</pmid><doi>10.1084/jem.20170277</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0002-5348-1456</orcidid><orcidid>https://orcid.org/0000-0001-5767-3386</orcidid><orcidid>https://orcid.org/0000-0001-5104-7683</orcidid><orcidid>https://orcid.org/0000-0002-4703-537X</orcidid><orcidid>https://orcid.org/0000-0002-8336-3418</orcidid><orcidid>https://orcid.org/0000-0003-3862-4583</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Animals Bone Marrow Cells - immunology Cell Communication - immunology Cell Line, Tumor Cell Movement Chemokine CCL22 - genetics Chemokine CCL22 - immunology Dendritic Cells - immunology HEK293 Cells Humans Lymph Nodes - cytology Lymph Nodes - immunology Mice Mice, Inbred BALB C Mice, Inbred C57BL Mice, Knockout Receptors, CCR4 - metabolism T-Lymphocytes, Regulatory - immunology Transplantation, Homologous |
| title | CCL22 controls immunity by promoting regulatory T cell communication with dendritic cells in lymph nodes |
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