IL-10 promotes malignant pleural effusion by regulating T H 1 response via an miR-7116-5p/GPR55/ERK pathway in mice
IL-10, produced by a wide variety of cells, is a highly pleiotropic cytokine that plays a critical role in the control of immune responses. However, its regulatory activity in tumor immunity remains poorly understood. In this study, we report that IL-10 deficiency robustly suppressed the formation o...
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Veröffentlicht in: | European journal of immunology 2020-11, Vol.50 (11), p.1798-1809 |
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container_title | European journal of immunology |
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creator | Zhai, Kan Shi, Xin-Yu Yi, Feng-Shuang Huang, Zhong-Yin Wu, Xiu-Zhi Dong, Shu-Feng Wang, Wen Wu, Min-Ting Shi, Huan-Zhong |
description | IL-10, produced by a wide variety of cells, is a highly pleiotropic cytokine that plays a critical role in the control of immune responses. However, its regulatory activity in tumor immunity remains poorly understood. In this study, we report that IL-10 deficiency robustly suppressed the formation of malignant pleural effusion (MPE) and significantly enhanced miR-7116-5p expression in pleural CD4
T cells. We demonstrated that miR-7116-5p suppressed IL-10-mediated MPE formation by inhibiting pleural vascular permeability as well as tumor angiogenesis and tumor growth. IL-10 promoted MPE formation by suppressing miR-7116-5p that enhances T
1 response. We identified G protein-coupled receptor 55 (GPR55) as a potential target of miR-7116-5p, and miR-7116-5p promoted T
1 cell function by downregulating GPR55. Moreover, GPR55 promoted MPE formation by inhibiting T
1 cell expansion through the ERK phosphorylation pathway. These results uncover an IL-10-mediated pathway controlling T
1 cells and demonstrate a central role for miR-7116-5p/GPR55/ERK signaling in the physiological regulation of IL-10-driven pro-malignant responses. |
doi_str_mv | 10.1002/eji.202048574 |
format | Article |
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T cells. We demonstrated that miR-7116-5p suppressed IL-10-mediated MPE formation by inhibiting pleural vascular permeability as well as tumor angiogenesis and tumor growth. IL-10 promoted MPE formation by suppressing miR-7116-5p that enhances T
1 response. We identified G protein-coupled receptor 55 (GPR55) as a potential target of miR-7116-5p, and miR-7116-5p promoted T
1 cell function by downregulating GPR55. Moreover, GPR55 promoted MPE formation by inhibiting T
1 cell expansion through the ERK phosphorylation pathway. These results uncover an IL-10-mediated pathway controlling T
1 cells and demonstrate a central role for miR-7116-5p/GPR55/ERK signaling in the physiological regulation of IL-10-driven pro-malignant responses.</description><identifier>ISSN: 0014-2980</identifier><identifier>EISSN: 1521-4141</identifier><identifier>DOI: 10.1002/eji.202048574</identifier><identifier>PMID: 32506440</identifier><language>eng</language><publisher>Germany</publisher><subject>Animals ; CD4-Positive T-Lymphocytes - immunology ; Cell Line ; Cell Line, Tumor ; Down-Regulation - immunology ; HEK293 Cells ; Humans ; Interleukin-10 - immunology ; MAP Kinase Signaling System - immunology ; Mice ; MicroRNAs - immunology ; Pleural Effusion, Malignant - immunology ; Receptors, Cannabinoid - immunology ; Signal Transduction - immunology ; Th1 Cells - immunology</subject><ispartof>European journal of immunology, 2020-11, Vol.50 (11), p.1798-1809</ispartof><rights>2020 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c1050-93889bdaf1512c170298d5495569fea2097a6e15257efed4ad47fcd2bfd96bee3</citedby><cites>FETCH-LOGICAL-c1050-93889bdaf1512c170298d5495569fea2097a6e15257efed4ad47fcd2bfd96bee3</cites><orcidid>0000-0003-3168-3548 ; 0000-0002-1154-7920</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32506440$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Zhai, Kan</creatorcontrib><creatorcontrib>Shi, Xin-Yu</creatorcontrib><creatorcontrib>Yi, Feng-Shuang</creatorcontrib><creatorcontrib>Huang, Zhong-Yin</creatorcontrib><creatorcontrib>Wu, Xiu-Zhi</creatorcontrib><creatorcontrib>Dong, Shu-Feng</creatorcontrib><creatorcontrib>Wang, Wen</creatorcontrib><creatorcontrib>Wu, Min-Ting</creatorcontrib><creatorcontrib>Shi, Huan-Zhong</creatorcontrib><title>IL-10 promotes malignant pleural effusion by regulating T H 1 response via an miR-7116-5p/GPR55/ERK pathway in mice</title><title>European journal of immunology</title><addtitle>Eur J Immunol</addtitle><description>IL-10, produced by a wide variety of cells, is a highly pleiotropic cytokine that plays a critical role in the control of immune responses. However, its regulatory activity in tumor immunity remains poorly understood. In this study, we report that IL-10 deficiency robustly suppressed the formation of malignant pleural effusion (MPE) and significantly enhanced miR-7116-5p expression in pleural CD4
T cells. We demonstrated that miR-7116-5p suppressed IL-10-mediated MPE formation by inhibiting pleural vascular permeability as well as tumor angiogenesis and tumor growth. IL-10 promoted MPE formation by suppressing miR-7116-5p that enhances T
1 response. We identified G protein-coupled receptor 55 (GPR55) as a potential target of miR-7116-5p, and miR-7116-5p promoted T
1 cell function by downregulating GPR55. Moreover, GPR55 promoted MPE formation by inhibiting T
1 cell expansion through the ERK phosphorylation pathway. These results uncover an IL-10-mediated pathway controlling T
1 cells and demonstrate a central role for miR-7116-5p/GPR55/ERK signaling in the physiological regulation of IL-10-driven pro-malignant responses.</description><subject>Animals</subject><subject>CD4-Positive T-Lymphocytes - immunology</subject><subject>Cell Line</subject><subject>Cell Line, Tumor</subject><subject>Down-Regulation - immunology</subject><subject>HEK293 Cells</subject><subject>Humans</subject><subject>Interleukin-10 - immunology</subject><subject>MAP Kinase Signaling System - immunology</subject><subject>Mice</subject><subject>MicroRNAs - immunology</subject><subject>Pleural Effusion, Malignant - immunology</subject><subject>Receptors, Cannabinoid - immunology</subject><subject>Signal Transduction - immunology</subject><subject>Th1 Cells - immunology</subject><issn>0014-2980</issn><issn>1521-4141</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNo9kE1Lw0AURQdRbK0u3cr8gWnfm8wkmaWU2hYLSqnrMEne1JR8kUmV_ntT1K4uXA4X7mHsEWGKAHJGh2IqQYKKdaSu2Bi1RKFQ4TUbA6AS0sQwYnfeHwDAhNrcslEgNYRKwZj59UYg8LZrqqYnzytbFvva1j1vSzp2tuTk3NEXTc3TE-9ofyxtX9R7vuMrjkPh26b2xL8Ky23Nq2IrIsRQ6Ha2fN9qPVtsX3lr-89ve-LFGcjont04W3p6-MsJ-3hZ7OYrsXlbrufPG5EhaBAmiGOT5tahRplhBMOTXCujdWgcWQkmsiENf3VEjnJlcxW5LJepy02YEgUTJn53s67xviOXtF1R2e6UICRneckgL7nIG_inX749phXlF_rfVvADF_xofg</recordid><startdate>202011</startdate><enddate>202011</enddate><creator>Zhai, Kan</creator><creator>Shi, Xin-Yu</creator><creator>Yi, Feng-Shuang</creator><creator>Huang, Zhong-Yin</creator><creator>Wu, Xiu-Zhi</creator><creator>Dong, Shu-Feng</creator><creator>Wang, Wen</creator><creator>Wu, Min-Ting</creator><creator>Shi, Huan-Zhong</creator><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><orcidid>https://orcid.org/0000-0003-3168-3548</orcidid><orcidid>https://orcid.org/0000-0002-1154-7920</orcidid></search><sort><creationdate>202011</creationdate><title>IL-10 promotes malignant pleural effusion by regulating T H 1 response via an miR-7116-5p/GPR55/ERK pathway in mice</title><author>Zhai, Kan ; Shi, Xin-Yu ; Yi, Feng-Shuang ; Huang, Zhong-Yin ; Wu, Xiu-Zhi ; Dong, Shu-Feng ; Wang, Wen ; Wu, Min-Ting ; Shi, Huan-Zhong</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c1050-93889bdaf1512c170298d5495569fea2097a6e15257efed4ad47fcd2bfd96bee3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Animals</topic><topic>CD4-Positive T-Lymphocytes - immunology</topic><topic>Cell Line</topic><topic>Cell Line, Tumor</topic><topic>Down-Regulation - immunology</topic><topic>HEK293 Cells</topic><topic>Humans</topic><topic>Interleukin-10 - immunology</topic><topic>MAP Kinase Signaling System - immunology</topic><topic>Mice</topic><topic>MicroRNAs - immunology</topic><topic>Pleural Effusion, Malignant - immunology</topic><topic>Receptors, Cannabinoid - immunology</topic><topic>Signal Transduction - immunology</topic><topic>Th1 Cells - immunology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Zhai, Kan</creatorcontrib><creatorcontrib>Shi, Xin-Yu</creatorcontrib><creatorcontrib>Yi, Feng-Shuang</creatorcontrib><creatorcontrib>Huang, Zhong-Yin</creatorcontrib><creatorcontrib>Wu, Xiu-Zhi</creatorcontrib><creatorcontrib>Dong, Shu-Feng</creatorcontrib><creatorcontrib>Wang, Wen</creatorcontrib><creatorcontrib>Wu, Min-Ting</creatorcontrib><creatorcontrib>Shi, Huan-Zhong</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><jtitle>European journal of immunology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Zhai, Kan</au><au>Shi, Xin-Yu</au><au>Yi, Feng-Shuang</au><au>Huang, Zhong-Yin</au><au>Wu, Xiu-Zhi</au><au>Dong, Shu-Feng</au><au>Wang, Wen</au><au>Wu, Min-Ting</au><au>Shi, Huan-Zhong</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>IL-10 promotes malignant pleural effusion by regulating T H 1 response via an miR-7116-5p/GPR55/ERK pathway in mice</atitle><jtitle>European journal of immunology</jtitle><addtitle>Eur J Immunol</addtitle><date>2020-11</date><risdate>2020</risdate><volume>50</volume><issue>11</issue><spage>1798</spage><epage>1809</epage><pages>1798-1809</pages><issn>0014-2980</issn><eissn>1521-4141</eissn><abstract>IL-10, produced by a wide variety of cells, is a highly pleiotropic cytokine that plays a critical role in the control of immune responses. However, its regulatory activity in tumor immunity remains poorly understood. In this study, we report that IL-10 deficiency robustly suppressed the formation of malignant pleural effusion (MPE) and significantly enhanced miR-7116-5p expression in pleural CD4
T cells. We demonstrated that miR-7116-5p suppressed IL-10-mediated MPE formation by inhibiting pleural vascular permeability as well as tumor angiogenesis and tumor growth. IL-10 promoted MPE formation by suppressing miR-7116-5p that enhances T
1 response. We identified G protein-coupled receptor 55 (GPR55) as a potential target of miR-7116-5p, and miR-7116-5p promoted T
1 cell function by downregulating GPR55. Moreover, GPR55 promoted MPE formation by inhibiting T
1 cell expansion through the ERK phosphorylation pathway. These results uncover an IL-10-mediated pathway controlling T
1 cells and demonstrate a central role for miR-7116-5p/GPR55/ERK signaling in the physiological regulation of IL-10-driven pro-malignant responses.</abstract><cop>Germany</cop><pmid>32506440</pmid><doi>10.1002/eji.202048574</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0003-3168-3548</orcidid><orcidid>https://orcid.org/0000-0002-1154-7920</orcidid></addata></record> |
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subjects | Animals CD4-Positive T-Lymphocytes - immunology Cell Line Cell Line, Tumor Down-Regulation - immunology HEK293 Cells Humans Interleukin-10 - immunology MAP Kinase Signaling System - immunology Mice MicroRNAs - immunology Pleural Effusion, Malignant - immunology Receptors, Cannabinoid - immunology Signal Transduction - immunology Th1 Cells - immunology |
title | IL-10 promotes malignant pleural effusion by regulating T H 1 response via an miR-7116-5p/GPR55/ERK pathway in mice |
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