Liver sinusoidal endothelial cell cross-priming is supported by CD4 T cell-derived IL-2
[Display omitted] Liver sinusoidal endothelial cells (LSECs) are prominent liver-resident antigen (cross-)presenting cells. LSEC cross-priming of naïve CD8 T cells does not require CD4 T cell help in contrast to priming by dendritic cells (DC) but leads to the formation of memory T cells that is pre...
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| Veröffentlicht in: | Journal of hepatology 2017-05, Vol.66 (5), p.978-986 |
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| creator | Wittlich, Michaela Dudek, Michael Böttcher, Jan P Schanz, Oliver Hegenbarth, Silke Bopp, Tobias Schmitt, Edgar Kurts, Christian Garbers, Christoph Rose John, Stefan Knolle, Percy A Wohlleber, Dirk |
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Liver sinusoidal endothelial cells (LSECs) are prominent liver-resident antigen (cross-)presenting cells. LSEC cross-priming of naïve CD8 T cells does not require CD4 T cell help in contrast to priming by dendritic cells (DC) but leads to the formation of memory T cells that is preceded by transient Granzyme B (GzmB) expression. Here we provide evidence for a so far unrecognized CD4 T helper cell function in LSEC-induced CD8 T cell activation.
Naïve CD8 T cells and differentiated T helper 1 (Th1) cells were stimulated by antigen-presenting LSEC, and GzmB expression in CD8 T cells was determined by flow cytometry. To identify molecular pathways mediating this GzmB expression, mechanistic proof-of-concept experiments were conducted using stimulatory anti-CD3 antibody together with Hyper-IL-6.
We demonstrate that LSECs simultaneously function in antigen co-presentation to CD8 and CD4 T cells. Such co-presentation revealed a function of Th1 cells to increase GzmB expression in CD8 T cells after LSEC but not DC cross-priming. IL-2 released from Th1 cells was required but not sufficient for rapid GzmB induction in CD8 T cells. T cell receptor together with IL-6 trans-signaling was necessary for IL-2 to mediate rapid GzmB induction.
Our findings indicate that LSECs can serve as a platform to facilitate CD4–CD8 T cell crosstalk enhancing the immune function of LSECs to cross-prime CD8 T cells. IL-6 trans-signaling-mediated responsiveness for IL-2 inducing sustained GzmB expression in CD8 T cells reveals unique mechanisms of CD4 T cell help and CD8 T cell differentiation through liver-resident antigen-presenting cells.
Our findings demonstrate that LSEC co-present antigen to CD8 and CD4 T cells and thereby enable CD4 T cell help for LSEC-priming of CD8 T cells. This CD4 T cell help selectively enhances the rapid upregulation of GzmB and effector function of LSEC-primed CD8 T cells thereby enhancing functional differentiation towards CD8 effector T cells. |
| doi_str_mv | 10.1016/j.jhep.2016.12.015 |
| format | Article |
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Liver sinusoidal endothelial cells (LSECs) are prominent liver-resident antigen (cross-)presenting cells. LSEC cross-priming of naïve CD8 T cells does not require CD4 T cell help in contrast to priming by dendritic cells (DC) but leads to the formation of memory T cells that is preceded by transient Granzyme B (GzmB) expression. Here we provide evidence for a so far unrecognized CD4 T helper cell function in LSEC-induced CD8 T cell activation.
Naïve CD8 T cells and differentiated T helper 1 (Th1) cells were stimulated by antigen-presenting LSEC, and GzmB expression in CD8 T cells was determined by flow cytometry. To identify molecular pathways mediating this GzmB expression, mechanistic proof-of-concept experiments were conducted using stimulatory anti-CD3 antibody together with Hyper-IL-6.
We demonstrate that LSECs simultaneously function in antigen co-presentation to CD8 and CD4 T cells. Such co-presentation revealed a function of Th1 cells to increase GzmB expression in CD8 T cells after LSEC but not DC cross-priming. IL-2 released from Th1 cells was required but not sufficient for rapid GzmB induction in CD8 T cells. T cell receptor together with IL-6 trans-signaling was necessary for IL-2 to mediate rapid GzmB induction.
Our findings indicate that LSECs can serve as a platform to facilitate CD4–CD8 T cell crosstalk enhancing the immune function of LSECs to cross-prime CD8 T cells. IL-6 trans-signaling-mediated responsiveness for IL-2 inducing sustained GzmB expression in CD8 T cells reveals unique mechanisms of CD4 T cell help and CD8 T cell differentiation through liver-resident antigen-presenting cells.
Our findings demonstrate that LSEC co-present antigen to CD8 and CD4 T cells and thereby enable CD4 T cell help for LSEC-priming of CD8 T cells. This CD4 T cell help selectively enhances the rapid upregulation of GzmB and effector function of LSEC-primed CD8 T cells thereby enhancing functional differentiation towards CD8 effector T cells.</description><identifier>ISSN: 0168-8278</identifier><identifier>EISSN: 1600-0641</identifier><identifier>DOI: 10.1016/j.jhep.2016.12.015</identifier><identifier>PMID: 28025060</identifier><language>eng</language><publisher>Netherlands: Elsevier B.V</publisher><subject>Animals ; Antigen presentation ; Antigen-presenting cells ; Antigen-Presenting Cells - immunology ; Antigens ; CD3 antigen ; CD4 antigen ; CD4 T cell help ; CD4-Positive T-Lymphocytes - immunology ; CD8 antigen ; CD8-Positive T-Lymphocytes - immunology ; Cell activation ; Cell Communication ; Cells ; Cells, Cultured ; Cross-Priming ; Dendritic cells ; Effector cells ; Endothelial cells ; Endothelial Cells - immunology ; Flow cytometry ; Gastroenterology and Hepatology ; Granzyme B ; Granzymes - analysis ; Helper cells ; Hepatocytes ; IL-6 trans-signaling ; Immune response ; Immunological memory ; Interleukin 2 ; Interleukin 6 ; Interleukin-2 - physiology ; Liver ; Liver - immunology ; Liver primed T cells ; LSEC ; Lymphocytes T ; Memory cells ; Mice ; Mice, Inbred C57BL ; T cell receptors</subject><ispartof>Journal of hepatology, 2017-05, Vol.66 (5), p.978-986</ispartof><rights>European Association for the Study of the Liver</rights><rights>2016 European Association for the Study of the Liver</rights><rights>Copyright © 2016 European Association for the Study of the Liver. Published by Elsevier B.V. All rights reserved.</rights><rights>Copyright Elsevier Science Ltd. May 2017</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c439t-98cebfe15d82face218fd927d167dc22803889ee13bd4f5dd2593e8d47d4c8b63</citedby><cites>FETCH-LOGICAL-c439t-98cebfe15d82face218fd927d167dc22803889ee13bd4f5dd2593e8d47d4c8b63</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S0168827816307486$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,776,780,3537,27901,27902,65534</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28025060$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Wittlich, Michaela</creatorcontrib><creatorcontrib>Dudek, Michael</creatorcontrib><creatorcontrib>Böttcher, Jan P</creatorcontrib><creatorcontrib>Schanz, Oliver</creatorcontrib><creatorcontrib>Hegenbarth, Silke</creatorcontrib><creatorcontrib>Bopp, Tobias</creatorcontrib><creatorcontrib>Schmitt, Edgar</creatorcontrib><creatorcontrib>Kurts, Christian</creatorcontrib><creatorcontrib>Garbers, Christoph</creatorcontrib><creatorcontrib>Rose John, Stefan</creatorcontrib><creatorcontrib>Knolle, Percy A</creatorcontrib><creatorcontrib>Wohlleber, Dirk</creatorcontrib><title>Liver sinusoidal endothelial cell cross-priming is supported by CD4 T cell-derived IL-2</title><title>Journal of hepatology</title><addtitle>J Hepatol</addtitle><description>[Display omitted]
Liver sinusoidal endothelial cells (LSECs) are prominent liver-resident antigen (cross-)presenting cells. LSEC cross-priming of naïve CD8 T cells does not require CD4 T cell help in contrast to priming by dendritic cells (DC) but leads to the formation of memory T cells that is preceded by transient Granzyme B (GzmB) expression. Here we provide evidence for a so far unrecognized CD4 T helper cell function in LSEC-induced CD8 T cell activation.
Naïve CD8 T cells and differentiated T helper 1 (Th1) cells were stimulated by antigen-presenting LSEC, and GzmB expression in CD8 T cells was determined by flow cytometry. To identify molecular pathways mediating this GzmB expression, mechanistic proof-of-concept experiments were conducted using stimulatory anti-CD3 antibody together with Hyper-IL-6.
We demonstrate that LSECs simultaneously function in antigen co-presentation to CD8 and CD4 T cells. Such co-presentation revealed a function of Th1 cells to increase GzmB expression in CD8 T cells after LSEC but not DC cross-priming. IL-2 released from Th1 cells was required but not sufficient for rapid GzmB induction in CD8 T cells. T cell receptor together with IL-6 trans-signaling was necessary for IL-2 to mediate rapid GzmB induction.
Our findings indicate that LSECs can serve as a platform to facilitate CD4–CD8 T cell crosstalk enhancing the immune function of LSECs to cross-prime CD8 T cells. IL-6 trans-signaling-mediated responsiveness for IL-2 inducing sustained GzmB expression in CD8 T cells reveals unique mechanisms of CD4 T cell help and CD8 T cell differentiation through liver-resident antigen-presenting cells.
Our findings demonstrate that LSEC co-present antigen to CD8 and CD4 T cells and thereby enable CD4 T cell help for LSEC-priming of CD8 T cells. This CD4 T cell help selectively enhances the rapid upregulation of GzmB and effector function of LSEC-primed CD8 T cells thereby enhancing functional differentiation towards CD8 effector T cells.</description><subject>Animals</subject><subject>Antigen presentation</subject><subject>Antigen-presenting cells</subject><subject>Antigen-Presenting Cells - immunology</subject><subject>Antigens</subject><subject>CD3 antigen</subject><subject>CD4 antigen</subject><subject>CD4 T cell help</subject><subject>CD4-Positive T-Lymphocytes - immunology</subject><subject>CD8 antigen</subject><subject>CD8-Positive T-Lymphocytes - immunology</subject><subject>Cell activation</subject><subject>Cell Communication</subject><subject>Cells</subject><subject>Cells, Cultured</subject><subject>Cross-Priming</subject><subject>Dendritic cells</subject><subject>Effector cells</subject><subject>Endothelial cells</subject><subject>Endothelial Cells - immunology</subject><subject>Flow cytometry</subject><subject>Gastroenterology and Hepatology</subject><subject>Granzyme B</subject><subject>Granzymes - analysis</subject><subject>Helper cells</subject><subject>Hepatocytes</subject><subject>IL-6 trans-signaling</subject><subject>Immune response</subject><subject>Immunological memory</subject><subject>Interleukin 2</subject><subject>Interleukin 6</subject><subject>Interleukin-2 - physiology</subject><subject>Liver</subject><subject>Liver - immunology</subject><subject>Liver primed T cells</subject><subject>LSEC</subject><subject>Lymphocytes T</subject><subject>Memory cells</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>T cell receptors</subject><issn>0168-8278</issn><issn>1600-0641</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9UU1r3DAUFKEh2aT9Az0UQy-92NGHJcsQCmXzCQs9NKVHYes9N3K8tivZgf33kbNpDjnkIj14M8PMPEI-M5oxytRZm7X3OGY8zhnjGWXygKyYojSlKmcfyCoudKp5oY_JSQgtpVTQMj8ix1xTLqmiK_Jn4x7RJ8H1cxgcVF2CPQzTPXYuzha7-PghhHT0buv6v4kLSZjHcfATQlLvkvVFntw9A1NAH8Ugud2k_CM5bKou4KeX_5T8vrq8W9-km5_Xt-sfm9TmopzSUlusG2QSNG8qi5zpBkpeAFMFWB59Cq1LRCZqyBsJwGUpUENeQG51rcQp-bbXHf3wb8Ywma0Li5uqx2EOhmkphJKykBH69Q20HWbfR3eG00JrJkS5CPI96jm2x8YsySu_M4yapXbTmqV2s9RuGDex9kj68iI911uEV8r_niPgfA_A2MWjQ2-CddhbBOfRTgYG977-9zd027ne2ap7wB2G1xzMhEgwv5bDL3dnStAi10o8AdVgpyI</recordid><startdate>20170501</startdate><enddate>20170501</enddate><creator>Wittlich, Michaela</creator><creator>Dudek, Michael</creator><creator>Böttcher, Jan P</creator><creator>Schanz, Oliver</creator><creator>Hegenbarth, Silke</creator><creator>Bopp, Tobias</creator><creator>Schmitt, Edgar</creator><creator>Kurts, Christian</creator><creator>Garbers, Christoph</creator><creator>Rose John, Stefan</creator><creator>Knolle, Percy A</creator><creator>Wohlleber, Dirk</creator><general>Elsevier B.V</general><general>Elsevier Science Ltd</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>7T5</scope><scope>H94</scope><scope>7X8</scope></search><sort><creationdate>20170501</creationdate><title>Liver sinusoidal endothelial cell cross-priming is supported by CD4 T cell-derived IL-2</title><author>Wittlich, Michaela ; Dudek, Michael ; Böttcher, Jan P ; Schanz, Oliver ; Hegenbarth, Silke ; Bopp, Tobias ; Schmitt, Edgar ; Kurts, Christian ; Garbers, Christoph ; Rose John, Stefan ; Knolle, Percy A ; Wohlleber, Dirk</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c439t-98cebfe15d82face218fd927d167dc22803889ee13bd4f5dd2593e8d47d4c8b63</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Animals</topic><topic>Antigen presentation</topic><topic>Antigen-presenting cells</topic><topic>Antigen-Presenting Cells - immunology</topic><topic>Antigens</topic><topic>CD3 antigen</topic><topic>CD4 antigen</topic><topic>CD4 T cell help</topic><topic>CD4-Positive T-Lymphocytes - immunology</topic><topic>CD8 antigen</topic><topic>CD8-Positive T-Lymphocytes - immunology</topic><topic>Cell activation</topic><topic>Cell Communication</topic><topic>Cells</topic><topic>Cells, Cultured</topic><topic>Cross-Priming</topic><topic>Dendritic cells</topic><topic>Effector cells</topic><topic>Endothelial cells</topic><topic>Endothelial Cells - immunology</topic><topic>Flow cytometry</topic><topic>Gastroenterology and Hepatology</topic><topic>Granzyme B</topic><topic>Granzymes - analysis</topic><topic>Helper cells</topic><topic>Hepatocytes</topic><topic>IL-6 trans-signaling</topic><topic>Immune response</topic><topic>Immunological memory</topic><topic>Interleukin 2</topic><topic>Interleukin 6</topic><topic>Interleukin-2 - physiology</topic><topic>Liver</topic><topic>Liver - immunology</topic><topic>Liver primed T cells</topic><topic>LSEC</topic><topic>Lymphocytes T</topic><topic>Memory cells</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>T cell receptors</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Wittlich, Michaela</creatorcontrib><creatorcontrib>Dudek, Michael</creatorcontrib><creatorcontrib>Böttcher, Jan P</creatorcontrib><creatorcontrib>Schanz, Oliver</creatorcontrib><creatorcontrib>Hegenbarth, Silke</creatorcontrib><creatorcontrib>Bopp, Tobias</creatorcontrib><creatorcontrib>Schmitt, Edgar</creatorcontrib><creatorcontrib>Kurts, Christian</creatorcontrib><creatorcontrib>Garbers, Christoph</creatorcontrib><creatorcontrib>Rose John, Stefan</creatorcontrib><creatorcontrib>Knolle, Percy A</creatorcontrib><creatorcontrib>Wohlleber, Dirk</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Immunology Abstracts</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Journal of hepatology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wittlich, Michaela</au><au>Dudek, Michael</au><au>Böttcher, Jan P</au><au>Schanz, Oliver</au><au>Hegenbarth, Silke</au><au>Bopp, Tobias</au><au>Schmitt, Edgar</au><au>Kurts, Christian</au><au>Garbers, Christoph</au><au>Rose John, Stefan</au><au>Knolle, Percy A</au><au>Wohlleber, Dirk</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Liver sinusoidal endothelial cell cross-priming is supported by CD4 T cell-derived IL-2</atitle><jtitle>Journal of hepatology</jtitle><addtitle>J Hepatol</addtitle><date>2017-05-01</date><risdate>2017</risdate><volume>66</volume><issue>5</issue><spage>978</spage><epage>986</epage><pages>978-986</pages><issn>0168-8278</issn><eissn>1600-0641</eissn><abstract>[Display omitted]
Liver sinusoidal endothelial cells (LSECs) are prominent liver-resident antigen (cross-)presenting cells. LSEC cross-priming of naïve CD8 T cells does not require CD4 T cell help in contrast to priming by dendritic cells (DC) but leads to the formation of memory T cells that is preceded by transient Granzyme B (GzmB) expression. Here we provide evidence for a so far unrecognized CD4 T helper cell function in LSEC-induced CD8 T cell activation.
Naïve CD8 T cells and differentiated T helper 1 (Th1) cells were stimulated by antigen-presenting LSEC, and GzmB expression in CD8 T cells was determined by flow cytometry. To identify molecular pathways mediating this GzmB expression, mechanistic proof-of-concept experiments were conducted using stimulatory anti-CD3 antibody together with Hyper-IL-6.
We demonstrate that LSECs simultaneously function in antigen co-presentation to CD8 and CD4 T cells. Such co-presentation revealed a function of Th1 cells to increase GzmB expression in CD8 T cells after LSEC but not DC cross-priming. IL-2 released from Th1 cells was required but not sufficient for rapid GzmB induction in CD8 T cells. T cell receptor together with IL-6 trans-signaling was necessary for IL-2 to mediate rapid GzmB induction.
Our findings indicate that LSECs can serve as a platform to facilitate CD4–CD8 T cell crosstalk enhancing the immune function of LSECs to cross-prime CD8 T cells. IL-6 trans-signaling-mediated responsiveness for IL-2 inducing sustained GzmB expression in CD8 T cells reveals unique mechanisms of CD4 T cell help and CD8 T cell differentiation through liver-resident antigen-presenting cells.
Our findings demonstrate that LSEC co-present antigen to CD8 and CD4 T cells and thereby enable CD4 T cell help for LSEC-priming of CD8 T cells. This CD4 T cell help selectively enhances the rapid upregulation of GzmB and effector function of LSEC-primed CD8 T cells thereby enhancing functional differentiation towards CD8 effector T cells.</abstract><cop>Netherlands</cop><pub>Elsevier B.V</pub><pmid>28025060</pmid><doi>10.1016/j.jhep.2016.12.015</doi><tpages>9</tpages></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 0168-8278 |
| ispartof | Journal of hepatology, 2017-05, Vol.66 (5), p.978-986 |
| issn | 0168-8278 1600-0641 |
| language | eng |
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| subjects | Animals Antigen presentation Antigen-presenting cells Antigen-Presenting Cells - immunology Antigens CD3 antigen CD4 antigen CD4 T cell help CD4-Positive T-Lymphocytes - immunology CD8 antigen CD8-Positive T-Lymphocytes - immunology Cell activation Cell Communication Cells Cells, Cultured Cross-Priming Dendritic cells Effector cells Endothelial cells Endothelial Cells - immunology Flow cytometry Gastroenterology and Hepatology Granzyme B Granzymes - analysis Helper cells Hepatocytes IL-6 trans-signaling Immune response Immunological memory Interleukin 2 Interleukin 6 Interleukin-2 - physiology Liver Liver - immunology Liver primed T cells LSEC Lymphocytes T Memory cells Mice Mice, Inbred C57BL T cell receptors |
| title | Liver sinusoidal endothelial cell cross-priming is supported by CD4 T cell-derived IL-2 |
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