The N6-methyladenosine writer WTAP contributes to the induction of immune tolerance post kidney transplantation by targeting regulatory T cells
N6-methyladenosine (m6A) modification is involved in diverse immunoregulation, while the relationship between m6A modification and immune tolerance post kidney transplantation remains unclear. Expression of Wilms tumor 1-associating protein (WTAP), an m6A writer, was firstly detected in tolerant kid...
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| Veröffentlicht in: | Laboratory investigation 2022-11, Vol.102 (11), p.1268-1279 |
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| creator | Wang, Zhigang Qi, Yuanbo Feng, Yonghua Xu, Hongen Wang, Junxiang Zhang, Luyu Zhang, Jie Hou, Xinyue Feng, Guiwen Shang, Wenjun |
| description | N6-methyladenosine (m6A) modification is involved in diverse immunoregulation, while the relationship between m6A modification and immune tolerance post kidney transplantation remains unclear. Expression of Wilms tumor 1-associating protein (WTAP), an m6A writer, was firstly detected in tolerant kidney transplant recipients (TOL). Then the role of WTAP on regulatory T (Treg) cell differentiation and function in CD4+ T cells from kidney transplant recipients with immune rejection (IR) was investigated. The potential target of WTAP and effect of WTAP on immune tolerance in vivo were subsequently verified. WTAP was upregulated in CD4+ T cells of TOL and positively correlated with Treg cell proportion. In vitro, WTAP overexpression promoted Treg cell differentiation and enhanced Treg cell-mediated suppression toward naïve T cells. Forkhead box other 1 (Foxo1) was identified as a target of WTAP. WTAP enhanced m6A modification of Foxo1 mRNA in coding sequence (CDS) region, leading to up-regulation of Foxo1. Overexpression of m6A demethylase removed the effect of WTAP overexpression, while Foxo1 overexpression reversed these effects. WTAP overexpression alleviated allograft rejection in model mice, as evidenced by reduced inflammatory response and increased Treg population. Our study suggests that WTAP plays a positive role in induction of immune tolerance post kidney transplant by promoting Treg cell differentiation and function. |
| doi_str_mv | 10.1038/s41374-022-00811-w |
| format | Article |
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Expression of Wilms tumor 1-associating protein (WTAP), an m6A writer, was firstly detected in tolerant kidney transplant recipients (TOL). Then the role of WTAP on regulatory T (Treg) cell differentiation and function in CD4+ T cells from kidney transplant recipients with immune rejection (IR) was investigated. The potential target of WTAP and effect of WTAP on immune tolerance in vivo were subsequently verified. WTAP was upregulated in CD4+ T cells of TOL and positively correlated with Treg cell proportion. In vitro, WTAP overexpression promoted Treg cell differentiation and enhanced Treg cell-mediated suppression toward naïve T cells. Forkhead box other 1 (Foxo1) was identified as a target of WTAP. WTAP enhanced m6A modification of Foxo1 mRNA in coding sequence (CDS) region, leading to up-regulation of Foxo1. Overexpression of m6A demethylase removed the effect of WTAP overexpression, while Foxo1 overexpression reversed these effects. WTAP overexpression alleviated allograft rejection in model mice, as evidenced by reduced inflammatory response and increased Treg population. Our study suggests that WTAP plays a positive role in induction of immune tolerance post kidney transplant by promoting Treg cell differentiation and function.</description><identifier>ISSN: 0023-6837</identifier><identifier>EISSN: 1530-0307</identifier><identifier>DOI: 10.1038/s41374-022-00811-w</identifier><identifier>PMID: 35864150</identifier><language>eng</language><publisher>New York: Elsevier Inc</publisher><subject>631/45 ; 631/80 ; Adenosine ; Animal models ; Animals ; CD4 antigen ; Cell differentiation ; Differentiation (biology) ; Forkhead protein ; FOXO1 protein ; Foxp3 protein ; Graft rejection ; Immune Tolerance ; Immunological tolerance ; Immunoregulation ; Inflammation ; Inflammatory response ; Kidney Transplantation ; Kidney transplants ; Laboratory Medicine ; Lymphocytes ; Lymphocytes T ; Medicine ; Medicine & Public Health ; Mice ; N6-methyladenosine ; Pathology ; Population studies ; Rejection ; RNA modification ; RNA, Messenger - metabolism ; T-Lymphocytes, Regulatory ; Tumors ; WT1 protein ; WT1 Proteins - metabolism</subject><ispartof>Laboratory investigation, 2022-11, Vol.102 (11), p.1268-1279</ispartof><rights>2022 United States & Canadian Academy of Pathology</rights><rights>The Author(s), under exclusive licence to United States and Canadian Academy of Pathology 2022</rights><rights>2022. The Author(s), under exclusive licence to United States and Canadian Academy of Pathology.</rights><rights>The Author(s), under exclusive licence to United States and Canadian Academy of Pathology 2022.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c472t-ea601237bf3d54f56b486da8062ef50983b9ac92f4ae1bcea55fcc40adfc024b3</citedby><cites>FETCH-LOGICAL-c472t-ea601237bf3d54f56b486da8062ef50983b9ac92f4ae1bcea55fcc40adfc024b3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,777,781,27905,27906</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/35864150$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Wang, Zhigang</creatorcontrib><creatorcontrib>Qi, Yuanbo</creatorcontrib><creatorcontrib>Feng, Yonghua</creatorcontrib><creatorcontrib>Xu, Hongen</creatorcontrib><creatorcontrib>Wang, Junxiang</creatorcontrib><creatorcontrib>Zhang, Luyu</creatorcontrib><creatorcontrib>Zhang, Jie</creatorcontrib><creatorcontrib>Hou, Xinyue</creatorcontrib><creatorcontrib>Feng, Guiwen</creatorcontrib><creatorcontrib>Shang, Wenjun</creatorcontrib><title>The N6-methyladenosine writer WTAP contributes to the induction of immune tolerance post kidney transplantation by targeting regulatory T cells</title><title>Laboratory investigation</title><addtitle>Lab Invest</addtitle><addtitle>Lab Invest</addtitle><description>N6-methyladenosine (m6A) modification is involved in diverse immunoregulation, while the relationship between m6A modification and immune tolerance post kidney transplantation remains unclear. Expression of Wilms tumor 1-associating protein (WTAP), an m6A writer, was firstly detected in tolerant kidney transplant recipients (TOL). Then the role of WTAP on regulatory T (Treg) cell differentiation and function in CD4+ T cells from kidney transplant recipients with immune rejection (IR) was investigated. The potential target of WTAP and effect of WTAP on immune tolerance in vivo were subsequently verified. WTAP was upregulated in CD4+ T cells of TOL and positively correlated with Treg cell proportion. In vitro, WTAP overexpression promoted Treg cell differentiation and enhanced Treg cell-mediated suppression toward naïve T cells. Forkhead box other 1 (Foxo1) was identified as a target of WTAP. WTAP enhanced m6A modification of Foxo1 mRNA in coding sequence (CDS) region, leading to up-regulation of Foxo1. Overexpression of m6A demethylase removed the effect of WTAP overexpression, while Foxo1 overexpression reversed these effects. WTAP overexpression alleviated allograft rejection in model mice, as evidenced by reduced inflammatory response and increased Treg population. Our study suggests that WTAP plays a positive role in induction of immune tolerance post kidney transplant by promoting Treg cell differentiation and function.</description><subject>631/45</subject><subject>631/80</subject><subject>Adenosine</subject><subject>Animal models</subject><subject>Animals</subject><subject>CD4 antigen</subject><subject>Cell differentiation</subject><subject>Differentiation (biology)</subject><subject>Forkhead protein</subject><subject>FOXO1 protein</subject><subject>Foxp3 protein</subject><subject>Graft rejection</subject><subject>Immune Tolerance</subject><subject>Immunological tolerance</subject><subject>Immunoregulation</subject><subject>Inflammation</subject><subject>Inflammatory response</subject><subject>Kidney Transplantation</subject><subject>Kidney transplants</subject><subject>Laboratory Medicine</subject><subject>Lymphocytes</subject><subject>Lymphocytes T</subject><subject>Medicine</subject><subject>Medicine & Public Health</subject><subject>Mice</subject><subject>N6-methyladenosine</subject><subject>Pathology</subject><subject>Population studies</subject><subject>Rejection</subject><subject>RNA modification</subject><subject>RNA, Messenger - metabolism</subject><subject>T-Lymphocytes, Regulatory</subject><subject>Tumors</subject><subject>WT1 protein</subject><subject>WT1 Proteins - metabolism</subject><issn>0023-6837</issn><issn>1530-0307</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNp9kctu1DAUhi0EokPhBVggS2zYBI4vcRKJTVVxkypgMYil5TgnU5fEHmyno3kKXhm3KSCx6MrS8ff9PvJPyHMGrxmI9k2STDSyAs4rgJax6vCAbFgtoAIBzUOyAeCiUq1oTsiTlK4AmJSqfkxORN0qyWrYkF_bS6SfVTVjvjxOZkAfkvNID9FljPT79uwrtcHn6PolY6I50FwM54fFZhc8DSN187wUJYcJo_EW6T6kTH-4weOR5jJK-8n4bG75voxM3GF2fkcj7pbJ5BCPdEstTlN6Sh6NZkr47O48Jd_ev9uef6wuvnz4dH52UVnZ8FyhUcC4aPpRDLUca9XLVg2mBcVxrKFrRd8Z2_FRGmS9RVPXo7USzDBa4LIXp-TVmruP4eeCKevZpZsNjMewJM1VJ5qGi5YX9OV_6FVYoi_bad7wRnZdYQvFV8rGkFLEUe-jm008agb6pi691qVLXfq2Ln0o0ou76KWfcfir_OmnAGIFUrnyO4z_3r439u1qYfnBa1esZB2WZgYX0WY9BHef_hvWw7en</recordid><startdate>20221101</startdate><enddate>20221101</enddate><creator>Wang, Zhigang</creator><creator>Qi, Yuanbo</creator><creator>Feng, Yonghua</creator><creator>Xu, Hongen</creator><creator>Wang, Junxiang</creator><creator>Zhang, Luyu</creator><creator>Zhang, Jie</creator><creator>Hou, Xinyue</creator><creator>Feng, Guiwen</creator><creator>Shang, Wenjun</creator><general>Elsevier Inc</general><general>Nature Publishing Group US</general><general>Nature Publishing Group</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>3V.</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>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>P64</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>7X8</scope></search><sort><creationdate>20221101</creationdate><title>The N6-methyladenosine writer WTAP contributes to the induction of immune tolerance post kidney transplantation by targeting regulatory T cells</title><author>Wang, Zhigang ; Qi, Yuanbo ; Feng, Yonghua ; Xu, Hongen ; Wang, Junxiang ; Zhang, Luyu ; Zhang, Jie ; Hou, Xinyue ; Feng, Guiwen ; Shang, Wenjun</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c472t-ea601237bf3d54f56b486da8062ef50983b9ac92f4ae1bcea55fcc40adfc024b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>631/45</topic><topic>631/80</topic><topic>Adenosine</topic><topic>Animal models</topic><topic>Animals</topic><topic>CD4 antigen</topic><topic>Cell differentiation</topic><topic>Differentiation (biology)</topic><topic>Forkhead protein</topic><topic>FOXO1 protein</topic><topic>Foxp3 protein</topic><topic>Graft rejection</topic><topic>Immune Tolerance</topic><topic>Immunological tolerance</topic><topic>Immunoregulation</topic><topic>Inflammation</topic><topic>Inflammatory response</topic><topic>Kidney Transplantation</topic><topic>Kidney transplants</topic><topic>Laboratory Medicine</topic><topic>Lymphocytes</topic><topic>Lymphocytes T</topic><topic>Medicine</topic><topic>Medicine & Public Health</topic><topic>Mice</topic><topic>N6-methyladenosine</topic><topic>Pathology</topic><topic>Population studies</topic><topic>Rejection</topic><topic>RNA modification</topic><topic>RNA, Messenger - 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Academic</collection><jtitle>Laboratory investigation</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wang, Zhigang</au><au>Qi, Yuanbo</au><au>Feng, Yonghua</au><au>Xu, Hongen</au><au>Wang, Junxiang</au><au>Zhang, Luyu</au><au>Zhang, Jie</au><au>Hou, Xinyue</au><au>Feng, Guiwen</au><au>Shang, Wenjun</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The N6-methyladenosine writer WTAP contributes to the induction of immune tolerance post kidney transplantation by targeting regulatory T cells</atitle><jtitle>Laboratory investigation</jtitle><stitle>Lab Invest</stitle><addtitle>Lab Invest</addtitle><date>2022-11-01</date><risdate>2022</risdate><volume>102</volume><issue>11</issue><spage>1268</spage><epage>1279</epage><pages>1268-1279</pages><issn>0023-6837</issn><eissn>1530-0307</eissn><abstract>N6-methyladenosine (m6A) modification is involved in diverse immunoregulation, while the relationship between m6A modification and immune tolerance post kidney transplantation remains unclear. Expression of Wilms tumor 1-associating protein (WTAP), an m6A writer, was firstly detected in tolerant kidney transplant recipients (TOL). Then the role of WTAP on regulatory T (Treg) cell differentiation and function in CD4+ T cells from kidney transplant recipients with immune rejection (IR) was investigated. The potential target of WTAP and effect of WTAP on immune tolerance in vivo were subsequently verified. WTAP was upregulated in CD4+ T cells of TOL and positively correlated with Treg cell proportion. In vitro, WTAP overexpression promoted Treg cell differentiation and enhanced Treg cell-mediated suppression toward naïve T cells. Forkhead box other 1 (Foxo1) was identified as a target of WTAP. WTAP enhanced m6A modification of Foxo1 mRNA in coding sequence (CDS) region, leading to up-regulation of Foxo1. Overexpression of m6A demethylase removed the effect of WTAP overexpression, while Foxo1 overexpression reversed these effects. WTAP overexpression alleviated allograft rejection in model mice, as evidenced by reduced inflammatory response and increased Treg population. Our study suggests that WTAP plays a positive role in induction of immune tolerance post kidney transplant by promoting Treg cell differentiation and function.</abstract><cop>New York</cop><pub>Elsevier Inc</pub><pmid>35864150</pmid><doi>10.1038/s41374-022-00811-w</doi><tpages>12</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | 631/45 631/80 Adenosine Animal models Animals CD4 antigen Cell differentiation Differentiation (biology) Forkhead protein FOXO1 protein Foxp3 protein Graft rejection Immune Tolerance Immunological tolerance Immunoregulation Inflammation Inflammatory response Kidney Transplantation Kidney transplants Laboratory Medicine Lymphocytes Lymphocytes T Medicine Medicine & Public Health Mice N6-methyladenosine Pathology Population studies Rejection RNA modification RNA, Messenger - metabolism T-Lymphocytes, Regulatory Tumors WT1 protein WT1 Proteins - metabolism |
| title | The N6-methyladenosine writer WTAP contributes to the induction of immune tolerance post kidney transplantation by targeting regulatory T cells |
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