Interleukin‐27 signalling induces stem cell antigen‐1 expression in T lymphocytes in vivo
Summary Stem cell antigen‐1 (Sca‐1/Ly6A/E) is a cell surface glycoprotein that is often used as a biomarker for stem cells and cell stemness. However, it is not clear what factors can directly induce the expression of Sca‐1/Ly6A/E in T lymphocytes in vivo, and if induction of Sca‐1 is associated wit...
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| Veröffentlicht in: | Immunology 2017-12, Vol.152 (4), p.638-647 |
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| creator | Liu, Zhihao Wu, Lisha Zhu, Jing Zhu, Xiaotong Zhu, Jianmin Liu, Jin‐Qing Zhang, Jianchao Davis, Jonathan P. Varikuti, Sanjay Satoskar, Abhay R. Zhou, Jie Li, Ming‐Song Bai, Xue‐Feng |
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Stem cell antigen‐1 (Sca‐1/Ly6A/E) is a cell surface glycoprotein that is often used as a biomarker for stem cells and cell stemness. However, it is not clear what factors can directly induce the expression of Sca‐1/Ly6A/E in T lymphocytes in vivo, and if induction of Sca‐1 is associated with T cell stemness. In this study, we show that interleukin‐27 (IL‐27), a member of the IL‐12 family of cytokines, directly induces Sca‐1 expression in T cells in vivo. We found that mice‐deficient for IL‐27 (either P28 or EBI3) or its signalling (IL‐27Rα) had profound reduction of Sca‐1 expression in naive (CD62L+ CD44−), memory (CD62L+ CD44+) and effector (CD62L− CD44+) T cells. In contrast, in vivo delivery of IL‐27 using adeno‐associated viral vectors strongly induced the expression of Sca‐1 in naive and memory/effector T‐cell populations in an IL‐27 receptor‐ or signal transducer and activator of transcription 1‐dependent manner. Interestingly, IL‐27‐induced Sca‐1+ T cells do not express or up‐regulate classic stem cell‐associated genes such as Nanog, Oct4, Sox2 and Ctnnb1. However, IL‐27‐induced Sca‐1+ T cells had increased expression of effector/memory‐associated transcription factor T‐bet, Eomes and Blimp1. Hence, IL‐27 signalling directly induces the expression of Sca‐1/Ly6A/E expression in T cells. Direct expansion of Sca‐1+ CD62L+ CD44− T memory stem cells may explain why IL‐27 enhances T‐cell memory.
Interleukin‐27 signalling induces the expression of stem cell antigen‐1 in mature T lymphocytes in vivo, which leads to the expansion of the T memory stem cell population. |
| doi_str_mv | 10.1111/imm.12805 |
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Stem cell antigen‐1 (Sca‐1/Ly6A/E) is a cell surface glycoprotein that is often used as a biomarker for stem cells and cell stemness. However, it is not clear what factors can directly induce the expression of Sca‐1/Ly6A/E in T lymphocytes in vivo, and if induction of Sca‐1 is associated with T cell stemness. In this study, we show that interleukin‐27 (IL‐27), a member of the IL‐12 family of cytokines, directly induces Sca‐1 expression in T cells in vivo. We found that mice‐deficient for IL‐27 (either P28 or EBI3) or its signalling (IL‐27Rα) had profound reduction of Sca‐1 expression in naive (CD62L+ CD44−), memory (CD62L+ CD44+) and effector (CD62L− CD44+) T cells. In contrast, in vivo delivery of IL‐27 using adeno‐associated viral vectors strongly induced the expression of Sca‐1 in naive and memory/effector T‐cell populations in an IL‐27 receptor‐ or signal transducer and activator of transcription 1‐dependent manner. Interestingly, IL‐27‐induced Sca‐1+ T cells do not express or up‐regulate classic stem cell‐associated genes such as Nanog, Oct4, Sox2 and Ctnnb1. However, IL‐27‐induced Sca‐1+ T cells had increased expression of effector/memory‐associated transcription factor T‐bet, Eomes and Blimp1. Hence, IL‐27 signalling directly induces the expression of Sca‐1/Ly6A/E expression in T cells. Direct expansion of Sca‐1+ CD62L+ CD44− T memory stem cells may explain why IL‐27 enhances T‐cell memory.
Interleukin‐27 signalling induces the expression of stem cell antigen‐1 in mature T lymphocytes in vivo, which leads to the expansion of the T memory stem cell population.</description><identifier>ISSN: 0019-2805</identifier><identifier>EISSN: 1365-2567</identifier><identifier>DOI: 10.1111/imm.12805</identifier><identifier>PMID: 28758191</identifier><language>eng</language><publisher>England: John Wiley and Sons Inc</publisher><subject>Animals ; Antigens, CD - genetics ; Antigens, CD - immunology ; Antigens, Ly - genetics ; Antigens, Ly - immunology ; Gene Expression Regulation - immunology ; Immunologic Memory ; Interleukins - genetics ; Interleukins - immunology ; interleukin‐27 ; Membrane Proteins - genetics ; Membrane Proteins - immunology ; Mice ; Mice, Knockout ; Original ; Receptors, Cytokine - genetics ; Receptors, Cytokine - immunology ; Signal Transduction - genetics ; Signal Transduction - immunology ; stem cell antigen‐1 ; T-Lymphocytes - immunology ; T‐cell memory</subject><ispartof>Immunology, 2017-12, Vol.152 (4), p.638-647</ispartof><rights>2017 John Wiley & Sons Ltd</rights><rights>2017 John Wiley & Sons Ltd.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3305-e8814f391f45def2b53c9aca467409abb6c2584475aa1ef57209ed5e64be58d93</citedby><cites>FETCH-LOGICAL-c3305-e8814f391f45def2b53c9aca467409abb6c2584475aa1ef57209ed5e64be58d93</cites><orcidid>0000-0001-9476-8376</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5680066/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5680066/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,1417,1433,27924,27925,45574,45575,46409,46833,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28758191$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Liu, Zhihao</creatorcontrib><creatorcontrib>Wu, Lisha</creatorcontrib><creatorcontrib>Zhu, Jing</creatorcontrib><creatorcontrib>Zhu, Xiaotong</creatorcontrib><creatorcontrib>Zhu, Jianmin</creatorcontrib><creatorcontrib>Liu, Jin‐Qing</creatorcontrib><creatorcontrib>Zhang, Jianchao</creatorcontrib><creatorcontrib>Davis, Jonathan P.</creatorcontrib><creatorcontrib>Varikuti, Sanjay</creatorcontrib><creatorcontrib>Satoskar, Abhay R.</creatorcontrib><creatorcontrib>Zhou, Jie</creatorcontrib><creatorcontrib>Li, Ming‐Song</creatorcontrib><creatorcontrib>Bai, Xue‐Feng</creatorcontrib><title>Interleukin‐27 signalling induces stem cell antigen‐1 expression in T lymphocytes in vivo</title><title>Immunology</title><addtitle>Immunology</addtitle><description>Summary
Stem cell antigen‐1 (Sca‐1/Ly6A/E) is a cell surface glycoprotein that is often used as a biomarker for stem cells and cell stemness. However, it is not clear what factors can directly induce the expression of Sca‐1/Ly6A/E in T lymphocytes in vivo, and if induction of Sca‐1 is associated with T cell stemness. In this study, we show that interleukin‐27 (IL‐27), a member of the IL‐12 family of cytokines, directly induces Sca‐1 expression in T cells in vivo. We found that mice‐deficient for IL‐27 (either P28 or EBI3) or its signalling (IL‐27Rα) had profound reduction of Sca‐1 expression in naive (CD62L+ CD44−), memory (CD62L+ CD44+) and effector (CD62L− CD44+) T cells. In contrast, in vivo delivery of IL‐27 using adeno‐associated viral vectors strongly induced the expression of Sca‐1 in naive and memory/effector T‐cell populations in an IL‐27 receptor‐ or signal transducer and activator of transcription 1‐dependent manner. Interestingly, IL‐27‐induced Sca‐1+ T cells do not express or up‐regulate classic stem cell‐associated genes such as Nanog, Oct4, Sox2 and Ctnnb1. However, IL‐27‐induced Sca‐1+ T cells had increased expression of effector/memory‐associated transcription factor T‐bet, Eomes and Blimp1. Hence, IL‐27 signalling directly induces the expression of Sca‐1/Ly6A/E expression in T cells. Direct expansion of Sca‐1+ CD62L+ CD44− T memory stem cells may explain why IL‐27 enhances T‐cell memory.
Interleukin‐27 signalling induces the expression of stem cell antigen‐1 in mature T lymphocytes in vivo, which leads to the expansion of the T memory stem cell population.</description><subject>Animals</subject><subject>Antigens, CD - genetics</subject><subject>Antigens, CD - immunology</subject><subject>Antigens, Ly - genetics</subject><subject>Antigens, Ly - immunology</subject><subject>Gene Expression Regulation - immunology</subject><subject>Immunologic Memory</subject><subject>Interleukins - genetics</subject><subject>Interleukins - immunology</subject><subject>interleukin‐27</subject><subject>Membrane Proteins - genetics</subject><subject>Membrane Proteins - immunology</subject><subject>Mice</subject><subject>Mice, Knockout</subject><subject>Original</subject><subject>Receptors, Cytokine - genetics</subject><subject>Receptors, Cytokine - immunology</subject><subject>Signal Transduction - genetics</subject><subject>Signal Transduction - immunology</subject><subject>stem cell antigen‐1</subject><subject>T-Lymphocytes - immunology</subject><subject>T‐cell memory</subject><issn>0019-2805</issn><issn>1365-2567</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kT9OwzAUhy0EoqUwcAGUEYZQO4kTZ0FCFX8qgVhgxXKcl9bgOCVOCt04AkfgLByFk-DQUsGAlyf7ff78rB9C-wQfE7eGqiyPScAw3UB9EsbUD2icbKI-xiT1u_Me2rH2wW1DTOk26gUsoYykpI_ux6aBWkP7qMzn61uQeFZNjNBamYmnTN5KsJ5toPQkaO0J06gJdCTx4GVWg7WqMg70bj29KGfTSi4ad0OZj_e5mle7aKsQ2sLeqg7Q3fnZ7ejSv7q5GI9Or3wZupF8YIxERZiSIqI5FEFGQ5kKKaI4iXAqsiyWAWVRlFAhCBQ0CXAKOYU4yoCyPA0H6GTpnbVZCbkE09RC81mtSlEveCUU_9sxason1ZzTmGEcx05wuBLU1VMLtuGlst2XhYGqtZykQcSYgzv0aInKurK2hmL9DMG8y4O7PPh3Ho49-D3XmvwJwAHDJfCsNCz-N_Hx9fVS-QVIZ5lp</recordid><startdate>201712</startdate><enddate>201712</enddate><creator>Liu, Zhihao</creator><creator>Wu, Lisha</creator><creator>Zhu, Jing</creator><creator>Zhu, Xiaotong</creator><creator>Zhu, Jianmin</creator><creator>Liu, Jin‐Qing</creator><creator>Zhang, Jianchao</creator><creator>Davis, Jonathan P.</creator><creator>Varikuti, Sanjay</creator><creator>Satoskar, Abhay R.</creator><creator>Zhou, Jie</creator><creator>Li, Ming‐Song</creator><creator>Bai, Xue‐Feng</creator><general>John Wiley and Sons Inc</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/0000-0001-9476-8376</orcidid></search><sort><creationdate>201712</creationdate><title>Interleukin‐27 signalling induces stem cell antigen‐1 expression in T lymphocytes in vivo</title><author>Liu, Zhihao ; Wu, Lisha ; Zhu, Jing ; Zhu, Xiaotong ; Zhu, Jianmin ; Liu, Jin‐Qing ; Zhang, Jianchao ; Davis, Jonathan P. ; Varikuti, Sanjay ; Satoskar, Abhay R. ; Zhou, Jie ; Li, Ming‐Song ; Bai, Xue‐Feng</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3305-e8814f391f45def2b53c9aca467409abb6c2584475aa1ef57209ed5e64be58d93</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Animals</topic><topic>Antigens, CD - genetics</topic><topic>Antigens, CD - immunology</topic><topic>Antigens, Ly - genetics</topic><topic>Antigens, Ly - immunology</topic><topic>Gene Expression Regulation - immunology</topic><topic>Immunologic Memory</topic><topic>Interleukins - genetics</topic><topic>Interleukins - immunology</topic><topic>interleukin‐27</topic><topic>Membrane Proteins - genetics</topic><topic>Membrane Proteins - immunology</topic><topic>Mice</topic><topic>Mice, Knockout</topic><topic>Original</topic><topic>Receptors, Cytokine - genetics</topic><topic>Receptors, Cytokine - immunology</topic><topic>Signal Transduction - genetics</topic><topic>Signal Transduction - immunology</topic><topic>stem cell antigen‐1</topic><topic>T-Lymphocytes - immunology</topic><topic>T‐cell memory</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Liu, Zhihao</creatorcontrib><creatorcontrib>Wu, Lisha</creatorcontrib><creatorcontrib>Zhu, Jing</creatorcontrib><creatorcontrib>Zhu, Xiaotong</creatorcontrib><creatorcontrib>Zhu, Jianmin</creatorcontrib><creatorcontrib>Liu, Jin‐Qing</creatorcontrib><creatorcontrib>Zhang, Jianchao</creatorcontrib><creatorcontrib>Davis, Jonathan P.</creatorcontrib><creatorcontrib>Varikuti, Sanjay</creatorcontrib><creatorcontrib>Satoskar, Abhay R.</creatorcontrib><creatorcontrib>Zhou, Jie</creatorcontrib><creatorcontrib>Li, Ming‐Song</creatorcontrib><creatorcontrib>Bai, Xue‐Feng</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>Immunology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Liu, Zhihao</au><au>Wu, Lisha</au><au>Zhu, Jing</au><au>Zhu, Xiaotong</au><au>Zhu, Jianmin</au><au>Liu, Jin‐Qing</au><au>Zhang, Jianchao</au><au>Davis, Jonathan P.</au><au>Varikuti, Sanjay</au><au>Satoskar, Abhay R.</au><au>Zhou, Jie</au><au>Li, Ming‐Song</au><au>Bai, Xue‐Feng</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Interleukin‐27 signalling induces stem cell antigen‐1 expression in T lymphocytes in vivo</atitle><jtitle>Immunology</jtitle><addtitle>Immunology</addtitle><date>2017-12</date><risdate>2017</risdate><volume>152</volume><issue>4</issue><spage>638</spage><epage>647</epage><pages>638-647</pages><issn>0019-2805</issn><eissn>1365-2567</eissn><abstract>Summary
Stem cell antigen‐1 (Sca‐1/Ly6A/E) is a cell surface glycoprotein that is often used as a biomarker for stem cells and cell stemness. However, it is not clear what factors can directly induce the expression of Sca‐1/Ly6A/E in T lymphocytes in vivo, and if induction of Sca‐1 is associated with T cell stemness. In this study, we show that interleukin‐27 (IL‐27), a member of the IL‐12 family of cytokines, directly induces Sca‐1 expression in T cells in vivo. We found that mice‐deficient for IL‐27 (either P28 or EBI3) or its signalling (IL‐27Rα) had profound reduction of Sca‐1 expression in naive (CD62L+ CD44−), memory (CD62L+ CD44+) and effector (CD62L− CD44+) T cells. In contrast, in vivo delivery of IL‐27 using adeno‐associated viral vectors strongly induced the expression of Sca‐1 in naive and memory/effector T‐cell populations in an IL‐27 receptor‐ or signal transducer and activator of transcription 1‐dependent manner. Interestingly, IL‐27‐induced Sca‐1+ T cells do not express or up‐regulate classic stem cell‐associated genes such as Nanog, Oct4, Sox2 and Ctnnb1. However, IL‐27‐induced Sca‐1+ T cells had increased expression of effector/memory‐associated transcription factor T‐bet, Eomes and Blimp1. Hence, IL‐27 signalling directly induces the expression of Sca‐1/Ly6A/E expression in T cells. Direct expansion of Sca‐1+ CD62L+ CD44− T memory stem cells may explain why IL‐27 enhances T‐cell memory.
Interleukin‐27 signalling induces the expression of stem cell antigen‐1 in mature T lymphocytes in vivo, which leads to the expansion of the T memory stem cell population.</abstract><cop>England</cop><pub>John Wiley and Sons Inc</pub><pmid>28758191</pmid><doi>10.1111/imm.12805</doi><tpages>10</tpages><orcidid>https://orcid.org/0000-0001-9476-8376</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Animals Antigens, CD - genetics Antigens, CD - immunology Antigens, Ly - genetics Antigens, Ly - immunology Gene Expression Regulation - immunology Immunologic Memory Interleukins - genetics Interleukins - immunology interleukin‐27 Membrane Proteins - genetics Membrane Proteins - immunology Mice Mice, Knockout Original Receptors, Cytokine - genetics Receptors, Cytokine - immunology Signal Transduction - genetics Signal Transduction - immunology stem cell antigen‐1 T-Lymphocytes - immunology T‐cell memory |
| title | Interleukin‐27 signalling induces stem cell antigen‐1 expression in T lymphocytes in vivo |
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