Podocytes present antigen to activate specific T cell immune responses in inflammatory renal disease
Infiltration of activated T cells into renal tissue plays an essential role in inflammatory nephropathy. However, the mechanism enabling the renal recruitment and activation of T cells remains elusive. Here we report that inflammatory cytokine‐promoted antigen presentation by podocytes is a key for...
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| Veröffentlicht in: | The Journal of pathology 2020-10, Vol.252 (2), p.165-177 |
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| creator | Li, Shan Liu, Ying He, Yueqin Rong, Weiwei Zhang, Mingchao Li, Limin Liu, Zhihong Zen, Ke |
| description | Infiltration of activated T cells into renal tissue plays an essential role in inflammatory nephropathy. However, the mechanism enabling the renal recruitment and activation of T cells remains elusive. Here we report that inflammatory cytokine‐promoted antigen presentation by podocytes is a key for recruiting and activating specific T cells. Our results showed that diabetes‐associated inflammatory cytokines IFNγ and IL‐17 all upregulated expression of MHC‐I, MHC‐II, CD80 and CD86 on the podocyte surface. Both IFNγ and IL‐17 stimulated the uptake and processing of ovalbumin (OVA) by mouse podocytes, resulting in presentation of OVA antigen peptide on the cell surface. OVA antigen presentation by podocytes was also validated using human podocytes. Furthermore, OVA antigen‐presenting mouse podocytes were able to activate OT‐I mouse T cell proliferation and inflammatory cytokine secretion, which in turn caused podocyte injury and apoptosis. Finally, OT‐I mice subjected to direct renal injection of OVA plus IFNγ/IL‐17 but not OVA alone exhibited OVA antigen presentation by podocytes and developed nephropathy in 4 weeks. In conclusion, antigen presentation by podocytes under inflammatory conditions plays an important role in activating T cell immune responses and facilitating immune‐mediated glomerular disease development. © 2020 Pathological Society of Great Britain and Ireland. Published by John Wiley & Sons, Ltd. |
| doi_str_mv | 10.1002/path.5508 |
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However, the mechanism enabling the renal recruitment and activation of T cells remains elusive. Here we report that inflammatory cytokine‐promoted antigen presentation by podocytes is a key for recruiting and activating specific T cells. Our results showed that diabetes‐associated inflammatory cytokines IFNγ and IL‐17 all upregulated expression of MHC‐I, MHC‐II, CD80 and CD86 on the podocyte surface. Both IFNγ and IL‐17 stimulated the uptake and processing of ovalbumin (OVA) by mouse podocytes, resulting in presentation of OVA antigen peptide on the cell surface. OVA antigen presentation by podocytes was also validated using human podocytes. Furthermore, OVA antigen‐presenting mouse podocytes were able to activate OT‐I mouse T cell proliferation and inflammatory cytokine secretion, which in turn caused podocyte injury and apoptosis. Finally, OT‐I mice subjected to direct renal injection of OVA plus IFNγ/IL‐17 but not OVA alone exhibited OVA antigen presentation by podocytes and developed nephropathy in 4 weeks. In conclusion, antigen presentation by podocytes under inflammatory conditions plays an important role in activating T cell immune responses and facilitating immune‐mediated glomerular disease development. © 2020 Pathological Society of Great Britain and Ireland. Published by John Wiley & Sons, Ltd.</description><identifier>ISSN: 0022-3417</identifier><identifier>EISSN: 1096-9896</identifier><identifier>DOI: 10.1002/path.5508</identifier><identifier>PMID: 32686090</identifier><language>eng</language><publisher>Chichester, UK: John Wiley & Sons, Ltd</publisher><subject>Animals ; Antigen presentation ; Antigen Presentation - immunology ; Antigen-Presenting Cells - immunology ; Apoptosis ; CD80 antigen ; CD86 antigen ; Cell activation ; Cell proliferation ; Cell surface ; cytokine ; Cytokines ; Diabetes mellitus ; Humans ; Immune response (cell-mediated) ; inflammatory renal disease ; Kidney diseases ; Lymphocyte Activation - immunology ; Lymphocytes ; Lymphocytes T ; Major histocompatibility complex ; Mice ; Nephritis - immunology ; Nephropathy ; Ovalbumin ; podocyte ; Podocytes - immunology ; T cell ; T-Lymphocytes - immunology ; γ-Interferon</subject><ispartof>The Journal of pathology, 2020-10, Vol.252 (2), p.165-177</ispartof><rights>2020 Pathological Society of Great Britain and Ireland. Published by John Wiley & Sons, Ltd.</rights><rights>Copyright © 2020 Pathological Society of Great Britain and Ireland</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c2688-a62b78dd69d1ea73f1e41b5ba7e102d3d59b1bb1701247364ccacac859d3695d3</citedby><cites>FETCH-LOGICAL-c2688-a62b78dd69d1ea73f1e41b5ba7e102d3d59b1bb1701247364ccacac859d3695d3</cites><orcidid>0000-0002-7382-6810</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1002%2Fpath.5508$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1002%2Fpath.5508$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,780,784,1417,27924,27925,45574,45575</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32686090$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Li, Shan</creatorcontrib><creatorcontrib>Liu, Ying</creatorcontrib><creatorcontrib>He, Yueqin</creatorcontrib><creatorcontrib>Rong, Weiwei</creatorcontrib><creatorcontrib>Zhang, Mingchao</creatorcontrib><creatorcontrib>Li, Limin</creatorcontrib><creatorcontrib>Liu, Zhihong</creatorcontrib><creatorcontrib>Zen, Ke</creatorcontrib><title>Podocytes present antigen to activate specific T cell immune responses in inflammatory renal disease</title><title>The Journal of pathology</title><addtitle>J Pathol</addtitle><description>Infiltration of activated T cells into renal tissue plays an essential role in inflammatory nephropathy. However, the mechanism enabling the renal recruitment and activation of T cells remains elusive. Here we report that inflammatory cytokine‐promoted antigen presentation by podocytes is a key for recruiting and activating specific T cells. Our results showed that diabetes‐associated inflammatory cytokines IFNγ and IL‐17 all upregulated expression of MHC‐I, MHC‐II, CD80 and CD86 on the podocyte surface. Both IFNγ and IL‐17 stimulated the uptake and processing of ovalbumin (OVA) by mouse podocytes, resulting in presentation of OVA antigen peptide on the cell surface. OVA antigen presentation by podocytes was also validated using human podocytes. Furthermore, OVA antigen‐presenting mouse podocytes were able to activate OT‐I mouse T cell proliferation and inflammatory cytokine secretion, which in turn caused podocyte injury and apoptosis. Finally, OT‐I mice subjected to direct renal injection of OVA plus IFNγ/IL‐17 but not OVA alone exhibited OVA antigen presentation by podocytes and developed nephropathy in 4 weeks. In conclusion, antigen presentation by podocytes under inflammatory conditions plays an important role in activating T cell immune responses and facilitating immune‐mediated glomerular disease development. © 2020 Pathological Society of Great Britain and Ireland. Published by John Wiley & Sons, Ltd.</description><subject>Animals</subject><subject>Antigen presentation</subject><subject>Antigen Presentation - immunology</subject><subject>Antigen-Presenting Cells - immunology</subject><subject>Apoptosis</subject><subject>CD80 antigen</subject><subject>CD86 antigen</subject><subject>Cell activation</subject><subject>Cell proliferation</subject><subject>Cell surface</subject><subject>cytokine</subject><subject>Cytokines</subject><subject>Diabetes mellitus</subject><subject>Humans</subject><subject>Immune response (cell-mediated)</subject><subject>inflammatory renal disease</subject><subject>Kidney diseases</subject><subject>Lymphocyte Activation - immunology</subject><subject>Lymphocytes</subject><subject>Lymphocytes T</subject><subject>Major histocompatibility complex</subject><subject>Mice</subject><subject>Nephritis - immunology</subject><subject>Nephropathy</subject><subject>Ovalbumin</subject><subject>podocyte</subject><subject>Podocytes - immunology</subject><subject>T cell</subject><subject>T-Lymphocytes - immunology</subject><subject>γ-Interferon</subject><issn>0022-3417</issn><issn>1096-9896</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kM1KxDAURoMozji68AUk4EYX1aRp0mYpg38g6GJclzS51QxtU5tUmbc3ddSFILmQxT334-MgdEzJBSUkvexVeL3gnBQ7aE6JFIkspNhF87hLE5bRfIYOvF8TQqTkfB_NWCoKQSSZI_PkjNObAB73A3joAlZdsC_Q4eCw0sG-qwDY96BtbTVeYQ1Ng23bjh3geNG7zsdj28WpG9W2KrhhEzedarCxHpSHQ7RXq8bD0fe_QM8316vlXfLweHu_vHpIdOxTJEqkVV4YI6ShoHJWU8hoxSuVAyWpYYbLilYVzQlNs5yJTGsVX8GlYUJywxbobJvbD-5tBB_K1vqpr-rAjb5Ms5RzyaOdiJ7-QdduHGLnicoyzqhgeaTOt5QenPcD1GU_2FYNm5KSclJfTurLSX1kT74Tx6oF80v-uI7A5Rb4sA1s_k8qn65Wd1-RnxR2juM</recordid><startdate>202010</startdate><enddate>202010</enddate><creator>Li, Shan</creator><creator>Liu, Ying</creator><creator>He, Yueqin</creator><creator>Rong, Weiwei</creator><creator>Zhang, Mingchao</creator><creator>Li, Limin</creator><creator>Liu, Zhihong</creator><creator>Zen, Ke</creator><general>John Wiley & Sons, Ltd</general><general>Wiley Subscription Services, 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>7QP</scope><scope>7QR</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>8FD</scope><scope>FR3</scope><scope>H94</scope><scope>K9.</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-7382-6810</orcidid></search><sort><creationdate>202010</creationdate><title>Podocytes present antigen to activate specific T cell immune responses in inflammatory renal disease</title><author>Li, Shan ; Liu, Ying ; He, Yueqin ; Rong, Weiwei ; Zhang, Mingchao ; Li, Limin ; Liu, Zhihong ; Zen, Ke</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c2688-a62b78dd69d1ea73f1e41b5ba7e102d3d59b1bb1701247364ccacac859d3695d3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Animals</topic><topic>Antigen presentation</topic><topic>Antigen Presentation - immunology</topic><topic>Antigen-Presenting Cells - immunology</topic><topic>Apoptosis</topic><topic>CD80 antigen</topic><topic>CD86 antigen</topic><topic>Cell activation</topic><topic>Cell proliferation</topic><topic>Cell surface</topic><topic>cytokine</topic><topic>Cytokines</topic><topic>Diabetes mellitus</topic><topic>Humans</topic><topic>Immune response (cell-mediated)</topic><topic>inflammatory renal disease</topic><topic>Kidney diseases</topic><topic>Lymphocyte Activation - immunology</topic><topic>Lymphocytes</topic><topic>Lymphocytes T</topic><topic>Major histocompatibility complex</topic><topic>Mice</topic><topic>Nephritis - immunology</topic><topic>Nephropathy</topic><topic>Ovalbumin</topic><topic>podocyte</topic><topic>Podocytes - immunology</topic><topic>T cell</topic><topic>T-Lymphocytes - immunology</topic><topic>γ-Interferon</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Li, Shan</creatorcontrib><creatorcontrib>Liu, Ying</creatorcontrib><creatorcontrib>He, Yueqin</creatorcontrib><creatorcontrib>Rong, Weiwei</creatorcontrib><creatorcontrib>Zhang, Mingchao</creatorcontrib><creatorcontrib>Li, Limin</creatorcontrib><creatorcontrib>Liu, Zhihong</creatorcontrib><creatorcontrib>Zen, Ke</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Immunology Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>The Journal of pathology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Li, Shan</au><au>Liu, Ying</au><au>He, Yueqin</au><au>Rong, Weiwei</au><au>Zhang, Mingchao</au><au>Li, Limin</au><au>Liu, Zhihong</au><au>Zen, Ke</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Podocytes present antigen to activate specific T cell immune responses in inflammatory renal disease</atitle><jtitle>The Journal of pathology</jtitle><addtitle>J Pathol</addtitle><date>2020-10</date><risdate>2020</risdate><volume>252</volume><issue>2</issue><spage>165</spage><epage>177</epage><pages>165-177</pages><issn>0022-3417</issn><eissn>1096-9896</eissn><abstract>Infiltration of activated T cells into renal tissue plays an essential role in inflammatory nephropathy. However, the mechanism enabling the renal recruitment and activation of T cells remains elusive. Here we report that inflammatory cytokine‐promoted antigen presentation by podocytes is a key for recruiting and activating specific T cells. Our results showed that diabetes‐associated inflammatory cytokines IFNγ and IL‐17 all upregulated expression of MHC‐I, MHC‐II, CD80 and CD86 on the podocyte surface. Both IFNγ and IL‐17 stimulated the uptake and processing of ovalbumin (OVA) by mouse podocytes, resulting in presentation of OVA antigen peptide on the cell surface. OVA antigen presentation by podocytes was also validated using human podocytes. Furthermore, OVA antigen‐presenting mouse podocytes were able to activate OT‐I mouse T cell proliferation and inflammatory cytokine secretion, which in turn caused podocyte injury and apoptosis. Finally, OT‐I mice subjected to direct renal injection of OVA plus IFNγ/IL‐17 but not OVA alone exhibited OVA antigen presentation by podocytes and developed nephropathy in 4 weeks. In conclusion, antigen presentation by podocytes under inflammatory conditions plays an important role in activating T cell immune responses and facilitating immune‐mediated glomerular disease development. © 2020 Pathological Society of Great Britain and Ireland. Published by John Wiley & Sons, Ltd.</abstract><cop>Chichester, UK</cop><pub>John Wiley & Sons, Ltd</pub><pmid>32686090</pmid><doi>10.1002/path.5508</doi><tpages>13</tpages><orcidid>https://orcid.org/0000-0002-7382-6810</orcidid></addata></record> |
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| subjects | Animals Antigen presentation Antigen Presentation - immunology Antigen-Presenting Cells - immunology Apoptosis CD80 antigen CD86 antigen Cell activation Cell proliferation Cell surface cytokine Cytokines Diabetes mellitus Humans Immune response (cell-mediated) inflammatory renal disease Kidney diseases Lymphocyte Activation - immunology Lymphocytes Lymphocytes T Major histocompatibility complex Mice Nephritis - immunology Nephropathy Ovalbumin podocyte Podocytes - immunology T cell T-Lymphocytes - immunology γ-Interferon |
| title | Podocytes present antigen to activate specific T cell immune responses in inflammatory renal disease |
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