CCR4+CD8+ T cells clonally expand to differentiated effectors in murine psoriasis and in human psoriatic arthritis
Psoriasis is a chronic inflammatory skin disease with an autoimmune component and associated with joint inflammation in up to 30% of cases. To investigate autoreactive T cells, we developed an imiquimod‐induced psoriasis‐like inflammation model in K5‐mOVA.tg C57BL/6 mice expressing ovalbumin (OVA) o...
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| Veröffentlicht in: | European journal of immunology 2023-04, Vol.53 (4), p.e2149702-n/a |
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| creator | Montico, Guendalina Mingozzi, Francesca Casciano, Fabio Protti, Giulia Gornati, Laura Marzola, Erika Banfi, Giuseppe Guerrini, Remo Secchiero, Paola Volinia, Stefano Granucci, Francesca Reali, Eva |
| description | Psoriasis is a chronic inflammatory skin disease with an autoimmune component and associated with joint inflammation in up to 30% of cases. To investigate autoreactive T cells, we developed an imiquimod‐induced psoriasis‐like inflammation model in K5‐mOVA.tg C57BL/6 mice expressing ovalbumin (OVA) on the keratinocyte membrane, adoptively transferred with OT‐I OVA‐specific CD8+ T cells. We evaluated the expansion of OT‐I CD8+ T cells and their localization in skin, blood, and spleen. scRNA‐seq and TCR sequencing data from patients with psoriatic arthritis were also analyzed. In the imiquimod‐treated K5‐mOVA.tg mouse model, OT‐I T cells were markedly expanded in the skin and blood at early time points. OT‐I T cells in the skin showed mainly CXCR3+ effector memory phenotype, whereas in peripheral blood there was an expansion of CCR4+CXCR3+ OT‐I cells. At a later time point, expanded OVA‐specific T‐cell population was found in the spleen. In patients with psoriatic arthritis, scRNA‐seq and TCR sequencing data showed clonal expansion of CCR4+ TCM cells in the circulation and further expansion in the synovial fluid. Importantly, there was a clonotype overlap between CCR4+ TCM in the peripheral blood and CD8+ T‐cell effectors in the synovial fluid. This mechanism could play a role in the generation and spreading of autoreactive T cells to the synovioentheseal tissues in psoriasis patients at risk of developing psoriatic arthritis.
Skin‐primed self‐reactive T cells egressing to the blood cloud localize and clonally expand at distant organs. This mechanism could represent a link between skin and joint manifestations in psoriasis patients at risk of developing psoriatic arthritis. |
| doi_str_mv | 10.1002/eji.202149702 |
| format | Article |
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Skin‐primed self‐reactive T cells egressing to the blood cloud localize and clonally expand at distant organs. This mechanism could represent a link between skin and joint manifestations in psoriasis patients at risk of developing psoriatic arthritis.</description><identifier>ISSN: 0014-2980</identifier><identifier>EISSN: 1521-4141</identifier><identifier>DOI: 10.1002/eji.202149702</identifier><identifier>PMID: 36722608</identifier><language>eng</language><publisher>Germany: Wiley Subscription Services, Inc</publisher><subject>Animals ; Arthritis, Psoriatic ; CD8 antigen ; CD8-Positive T-Lymphocytes ; Cell differentiation ; Chemokine receptors ; Clonal expansion ; CXCR3 protein ; Humans ; Imiquimod ; Inflammation ; Localization ; Lymphocytes ; Lymphocytes T ; Memory cells ; Mice ; Mice, Inbred C57BL ; Ovalbumin ; Peripheral blood ; Phenotypes ; Psoriasis ; Psoriasis and psoriatic arthritis ; Psoriatic arthritis ; Receptors, Antigen, T-Cell - genetics ; Receptors, CCR4 ; Self‐reactive CD8 T cells ; Skin Diseases ; Spleen ; Synovial fluid ; T cell receptors ; T‐cell recirculation</subject><ispartof>European journal of immunology, 2023-04, Vol.53 (4), p.e2149702-n/a</ispartof><rights>2023 The Authors. published by Wiley‐VCH GmbH</rights><rights>2023 The Authors. European Journal of Immunology published by Wiley-VCH GmbH.</rights><rights>2023. This article is published under http://creativecommons.org/licenses/by-nc/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3339-663ddd84ac38165f0630c29d5f1aad41309a66d9c5b54e13b36f9ed9296d11ff3</citedby><cites>FETCH-LOGICAL-c3339-663ddd84ac38165f0630c29d5f1aad41309a66d9c5b54e13b36f9ed9296d11ff3</cites><orcidid>0000-0003-1900-1356 ; 0000-0002-7046-4914 ; 0000-0002-6431-3335</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%2Feji.202149702$$EPDF$$P50$$Gwiley$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1002%2Feji.202149702$$EHTML$$P50$$Gwiley$$Hfree_for_read</linktohtml><link.rule.ids>314,780,784,1416,1432,27922,27923,45572,45573,46407,46831</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/36722608$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Montico, Guendalina</creatorcontrib><creatorcontrib>Mingozzi, Francesca</creatorcontrib><creatorcontrib>Casciano, Fabio</creatorcontrib><creatorcontrib>Protti, Giulia</creatorcontrib><creatorcontrib>Gornati, Laura</creatorcontrib><creatorcontrib>Marzola, Erika</creatorcontrib><creatorcontrib>Banfi, Giuseppe</creatorcontrib><creatorcontrib>Guerrini, Remo</creatorcontrib><creatorcontrib>Secchiero, Paola</creatorcontrib><creatorcontrib>Volinia, Stefano</creatorcontrib><creatorcontrib>Granucci, Francesca</creatorcontrib><creatorcontrib>Reali, Eva</creatorcontrib><title>CCR4+CD8+ T cells clonally expand to differentiated effectors in murine psoriasis and in human psoriatic arthritis</title><title>European journal of immunology</title><addtitle>Eur J Immunol</addtitle><description>Psoriasis is a chronic inflammatory skin disease with an autoimmune component and associated with joint inflammation in up to 30% of cases. To investigate autoreactive T cells, we developed an imiquimod‐induced psoriasis‐like inflammation model in K5‐mOVA.tg C57BL/6 mice expressing ovalbumin (OVA) on the keratinocyte membrane, adoptively transferred with OT‐I OVA‐specific CD8+ T cells. We evaluated the expansion of OT‐I CD8+ T cells and their localization in skin, blood, and spleen. scRNA‐seq and TCR sequencing data from patients with psoriatic arthritis were also analyzed. In the imiquimod‐treated K5‐mOVA.tg mouse model, OT‐I T cells were markedly expanded in the skin and blood at early time points. OT‐I T cells in the skin showed mainly CXCR3+ effector memory phenotype, whereas in peripheral blood there was an expansion of CCR4+CXCR3+ OT‐I cells. At a later time point, expanded OVA‐specific T‐cell population was found in the spleen. In patients with psoriatic arthritis, scRNA‐seq and TCR sequencing data showed clonal expansion of CCR4+ TCM cells in the circulation and further expansion in the synovial fluid. Importantly, there was a clonotype overlap between CCR4+ TCM in the peripheral blood and CD8+ T‐cell effectors in the synovial fluid. This mechanism could play a role in the generation and spreading of autoreactive T cells to the synovioentheseal tissues in psoriasis patients at risk of developing psoriatic arthritis.
Skin‐primed self‐reactive T cells egressing to the blood cloud localize and clonally expand at distant organs. This mechanism could represent a link between skin and joint manifestations in psoriasis patients at risk of developing psoriatic arthritis.</description><subject>Animals</subject><subject>Arthritis, Psoriatic</subject><subject>CD8 antigen</subject><subject>CD8-Positive T-Lymphocytes</subject><subject>Cell differentiation</subject><subject>Chemokine receptors</subject><subject>Clonal expansion</subject><subject>CXCR3 protein</subject><subject>Humans</subject><subject>Imiquimod</subject><subject>Inflammation</subject><subject>Localization</subject><subject>Lymphocytes</subject><subject>Lymphocytes T</subject><subject>Memory cells</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Ovalbumin</subject><subject>Peripheral blood</subject><subject>Phenotypes</subject><subject>Psoriasis</subject><subject>Psoriasis and psoriatic arthritis</subject><subject>Psoriatic arthritis</subject><subject>Receptors, Antigen, T-Cell - genetics</subject><subject>Receptors, CCR4</subject><subject>Self‐reactive CD8 T cells</subject><subject>Skin Diseases</subject><subject>Spleen</subject><subject>Synovial fluid</subject><subject>T cell receptors</subject><subject>T‐cell recirculation</subject><issn>0014-2980</issn><issn>1521-4141</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>WIN</sourceid><sourceid>EIF</sourceid><recordid>eNp9kctLAzEQxoMoWqtHrxLwIpStee_mKGvViiCInpc0D0zZR0120f73prT24MHDMMzHbz6Y-QC4wGiKESI3dumnBBHMZI7IARhhTnDGMMOHYIQQZhmRBToBpzEuEUJScHkMTqjICRGoGIFQlq9sUt4VE_gGta3rCHXdtaqu19B-r1RrYN9B452zwba9V7010KZJ912I0LewGYJvLVzFLngVfYSbnaR_DI1qd3LvNVSh_wi-9_EMHDlVR3u-62Pwfj97Kx-z55eHeXn7nGlKqcyEoMaYgilNCyy4Q4IiTaThDitlGKZIKiGM1HzBmcV0QYWT1kgihcHYOToG11vfVeg-Bxv7qvFxc6JqbTfEiuQ5FjRVntCrP-iyG0L6woaSheCF5EWisi2lQxdjsK5aBd-osK4wqjZhVCmMah9G4i93rsOisWZP_34_AWQLfPnarv93q2ZPc86opD9HaZOg</recordid><startdate>202304</startdate><enddate>202304</enddate><creator>Montico, Guendalina</creator><creator>Mingozzi, Francesca</creator><creator>Casciano, Fabio</creator><creator>Protti, Giulia</creator><creator>Gornati, Laura</creator><creator>Marzola, Erika</creator><creator>Banfi, Giuseppe</creator><creator>Guerrini, Remo</creator><creator>Secchiero, Paola</creator><creator>Volinia, Stefano</creator><creator>Granucci, Francesca</creator><creator>Reali, Eva</creator><general>Wiley Subscription Services, Inc</general><scope>24P</scope><scope>WIN</scope><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>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>8FD</scope><scope>FR3</scope><scope>H94</scope><scope>K9.</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0003-1900-1356</orcidid><orcidid>https://orcid.org/0000-0002-7046-4914</orcidid><orcidid>https://orcid.org/0000-0002-6431-3335</orcidid></search><sort><creationdate>202304</creationdate><title>CCR4+CD8+ T cells clonally expand to differentiated effectors in murine psoriasis and in human psoriatic arthritis</title><author>Montico, Guendalina ; Mingozzi, Francesca ; Casciano, Fabio ; Protti, Giulia ; Gornati, Laura ; Marzola, Erika ; Banfi, Giuseppe ; Guerrini, Remo ; Secchiero, Paola ; Volinia, Stefano ; Granucci, Francesca ; Reali, Eva</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3339-663ddd84ac38165f0630c29d5f1aad41309a66d9c5b54e13b36f9ed9296d11ff3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Animals</topic><topic>Arthritis, Psoriatic</topic><topic>CD8 antigen</topic><topic>CD8-Positive T-Lymphocytes</topic><topic>Cell differentiation</topic><topic>Chemokine receptors</topic><topic>Clonal expansion</topic><topic>CXCR3 protein</topic><topic>Humans</topic><topic>Imiquimod</topic><topic>Inflammation</topic><topic>Localization</topic><topic>Lymphocytes</topic><topic>Lymphocytes T</topic><topic>Memory cells</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>Ovalbumin</topic><topic>Peripheral blood</topic><topic>Phenotypes</topic><topic>Psoriasis</topic><topic>Psoriasis and psoriatic arthritis</topic><topic>Psoriatic arthritis</topic><topic>Receptors, Antigen, T-Cell - genetics</topic><topic>Receptors, CCR4</topic><topic>Self‐reactive CD8 T cells</topic><topic>Skin Diseases</topic><topic>Spleen</topic><topic>Synovial fluid</topic><topic>T cell receptors</topic><topic>T‐cell recirculation</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Montico, Guendalina</creatorcontrib><creatorcontrib>Mingozzi, Francesca</creatorcontrib><creatorcontrib>Casciano, Fabio</creatorcontrib><creatorcontrib>Protti, Giulia</creatorcontrib><creatorcontrib>Gornati, Laura</creatorcontrib><creatorcontrib>Marzola, Erika</creatorcontrib><creatorcontrib>Banfi, Giuseppe</creatorcontrib><creatorcontrib>Guerrini, Remo</creatorcontrib><creatorcontrib>Secchiero, Paola</creatorcontrib><creatorcontrib>Volinia, Stefano</creatorcontrib><creatorcontrib>Granucci, Francesca</creatorcontrib><creatorcontrib>Reali, Eva</creatorcontrib><collection>Wiley-Blackwell Open Access Titles</collection><collection>Wiley Free Content</collection><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>Immunology Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids 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>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>European journal of immunology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Montico, Guendalina</au><au>Mingozzi, Francesca</au><au>Casciano, Fabio</au><au>Protti, Giulia</au><au>Gornati, Laura</au><au>Marzola, Erika</au><au>Banfi, Giuseppe</au><au>Guerrini, Remo</au><au>Secchiero, Paola</au><au>Volinia, Stefano</au><au>Granucci, Francesca</au><au>Reali, Eva</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>CCR4+CD8+ T cells clonally expand to differentiated effectors in murine psoriasis and in human psoriatic arthritis</atitle><jtitle>European journal of immunology</jtitle><addtitle>Eur J Immunol</addtitle><date>2023-04</date><risdate>2023</risdate><volume>53</volume><issue>4</issue><spage>e2149702</spage><epage>n/a</epage><pages>e2149702-n/a</pages><issn>0014-2980</issn><eissn>1521-4141</eissn><abstract>Psoriasis is a chronic inflammatory skin disease with an autoimmune component and associated with joint inflammation in up to 30% of cases. To investigate autoreactive T cells, we developed an imiquimod‐induced psoriasis‐like inflammation model in K5‐mOVA.tg C57BL/6 mice expressing ovalbumin (OVA) on the keratinocyte membrane, adoptively transferred with OT‐I OVA‐specific CD8+ T cells. We evaluated the expansion of OT‐I CD8+ T cells and their localization in skin, blood, and spleen. scRNA‐seq and TCR sequencing data from patients with psoriatic arthritis were also analyzed. In the imiquimod‐treated K5‐mOVA.tg mouse model, OT‐I T cells were markedly expanded in the skin and blood at early time points. OT‐I T cells in the skin showed mainly CXCR3+ effector memory phenotype, whereas in peripheral blood there was an expansion of CCR4+CXCR3+ OT‐I cells. At a later time point, expanded OVA‐specific T‐cell population was found in the spleen. In patients with psoriatic arthritis, scRNA‐seq and TCR sequencing data showed clonal expansion of CCR4+ TCM cells in the circulation and further expansion in the synovial fluid. Importantly, there was a clonotype overlap between CCR4+ TCM in the peripheral blood and CD8+ T‐cell effectors in the synovial fluid. This mechanism could play a role in the generation and spreading of autoreactive T cells to the synovioentheseal tissues in psoriasis patients at risk of developing psoriatic arthritis.
Skin‐primed self‐reactive T cells egressing to the blood cloud localize and clonally expand at distant organs. This mechanism could represent a link between skin and joint manifestations in psoriasis patients at risk of developing psoriatic arthritis.</abstract><cop>Germany</cop><pub>Wiley Subscription Services, Inc</pub><pmid>36722608</pmid><doi>10.1002/eji.202149702</doi><tpages>13</tpages><orcidid>https://orcid.org/0000-0003-1900-1356</orcidid><orcidid>https://orcid.org/0000-0002-7046-4914</orcidid><orcidid>https://orcid.org/0000-0002-6431-3335</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Animals Arthritis, Psoriatic CD8 antigen CD8-Positive T-Lymphocytes Cell differentiation Chemokine receptors Clonal expansion CXCR3 protein Humans Imiquimod Inflammation Localization Lymphocytes Lymphocytes T Memory cells Mice Mice, Inbred C57BL Ovalbumin Peripheral blood Phenotypes Psoriasis Psoriasis and psoriatic arthritis Psoriatic arthritis Receptors, Antigen, T-Cell - genetics Receptors, CCR4 Self‐reactive CD8 T cells Skin Diseases Spleen Synovial fluid T cell receptors T‐cell recirculation |
| title | CCR4+CD8+ T cells clonally expand to differentiated effectors in murine psoriasis and in human psoriatic arthritis |
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