Diversification of human plasmacytoid predendritic cells in response to a single stimulus
Innate immune cells adjust to microbial and inflammatory stimuli through a process termed environmental plasticity, which links a given individual stimulus to a unique activated state. Here, we report that activation of human plasmacytoid predendritic cells (pDCs) with a single microbial or cytokine...
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| Veröffentlicht in: | Nature immunology 2018-01, Vol.19 (1), p.63-75 |
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| creator | Alculumbre, Solana G. Saint-André, Violaine Di Domizio, Jeremy Vargas, Pablo Sirven, Philemon Bost, Pierre Maurin, Mathieu Maiuri, Paolo Wery, Maxime Roman, Mabel San Savey, Léa Touzot, Maxime Terrier, Benjamin Saadoun, David Conrad, Curdin Gilliet, Michel Morillon, Antonin Soumelis, Vassili |
| description | Innate immune cells adjust to microbial and inflammatory stimuli through a process termed environmental plasticity, which links a given individual stimulus to a unique activated state. Here, we report that activation of human plasmacytoid predendritic cells (pDCs) with a single microbial or cytokine stimulus triggers cell diversification into three stable subpopulations (P1–P3). P1-pDCs (PD-L1
+
CD80
–
) displayed a plasmacytoid morphology and specialization for type I interferon production. P3-pDCs (PD-L1
–
CD80
+
) adopted a dendritic morphology and adaptive immune functions. P2-pDCs (PD-L1
+
CD80
+
) displayed both innate and adaptive functions. Each subpopulation expressed a specific coding- and long-noncoding-RNA signature and was stable after secondary stimulation. P1-pDCs were detected in samples from patients with lupus or psoriasis. pDC diversification was independent of cell divisions or preexisting heterogeneity within steady-state pDCs but was controlled by a TNF autocrine and/or paracrine communication loop. Our findings reveal a novel mechanism for diversity and division of labor in innate immune cells.
Plasmacytoid dendritic cells (pDCs) are known for their copious IFN-I production. Soumelis and colleagues show that functionally and transcriptomically distinct human pDC populations can be generated from a single microbial or cytokine stimulus. |
| doi_str_mv | 10.1038/s41590-017-0012-z |
| format | Article |
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+
CD80
–
) displayed a plasmacytoid morphology and specialization for type I interferon production. P3-pDCs (PD-L1
–
CD80
+
) adopted a dendritic morphology and adaptive immune functions. P2-pDCs (PD-L1
+
CD80
+
) displayed both innate and adaptive functions. Each subpopulation expressed a specific coding- and long-noncoding-RNA signature and was stable after secondary stimulation. P1-pDCs were detected in samples from patients with lupus or psoriasis. pDC diversification was independent of cell divisions or preexisting heterogeneity within steady-state pDCs but was controlled by a TNF autocrine and/or paracrine communication loop. Our findings reveal a novel mechanism for diversity and division of labor in innate immune cells.
Plasmacytoid dendritic cells (pDCs) are known for their copious IFN-I production. Soumelis and colleagues show that functionally and transcriptomically distinct human pDC populations can be generated from a single microbial or cytokine stimulus.</description><identifier>ISSN: 1529-2908</identifier><identifier>EISSN: 1529-2916</identifier><identifier>DOI: 10.1038/s41590-017-0012-z</identifier><identifier>PMID: 29203862</identifier><language>eng</language><publisher>New York: Nature Publishing Group US</publisher><subject>Adaptive Immunity - immunology ; Autocrine signalling ; B7-1 Antigen - immunology ; B7-1 Antigen - metabolism ; B7-H1 Antigen - immunology ; B7-H1 Antigen - metabolism ; Biodiversity ; Biological response modifiers ; Biomedical and Life Sciences ; Biomedicine ; CD80 antigen ; Cells, Cultured ; Cytokines - genetics ; Cytokines - immunology ; Cytokines - metabolism ; Dendritic cells ; Dendritic Cells - immunology ; Dendritic Cells - metabolism ; Dendritic Cells - ultrastructure ; Diversification ; Division of labor ; Gene Expression - immunology ; Gene Expression Profiling - methods ; Heterogeneity ; Humans ; Immunity, Innate - immunology ; Immunology ; Infectious Diseases ; Inflammation ; Innate immunity ; Interferon ; Interferon Type I - genetics ; Interferon Type I - immunology ; Interferon Type I - metabolism ; Life Sciences ; Lupus ; Lupus Erythematosus, Systemic - immunology ; Microscopy, Electron, Transmission ; Morphology ; Orthomyxoviridae - immunology ; Paracrine signalling ; PD-L1 protein ; Psoriasis ; Psoriasis - immunology ; Ribonucleic acid ; RNA ; Skin diseases ; Specialization ; Subpopulations ; Tumor necrosis factor</subject><ispartof>Nature immunology, 2018-01, Vol.19 (1), p.63-75</ispartof><rights>The Author(s) 2017</rights><rights>COPYRIGHT 2018 Nature Publishing Group</rights><rights>Copyright Nature Publishing Group Jan 2018</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c503t-d1b7c03f2e12f9dddb35cfb3fabc052111a66aa3c937d122f0e4bed7fb517dad3</citedby><cites>FETCH-LOGICAL-c503t-d1b7c03f2e12f9dddb35cfb3fabc052111a66aa3c937d122f0e4bed7fb517dad3</cites><orcidid>0000-0001-5079-445X ; 0000-0002-6281-3918 ; 0000-0002-6475-494X ; 0000-0003-1849-9834 ; 0000-0002-2162-0909 ; 0000-0001-6612-7336 ; 0000-0003-3628-9996 ; 0000-0002-0575-5264</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1038/s41590-017-0012-z$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1038/s41590-017-0012-z$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>230,314,776,780,881,27901,27902,41464,42533,51294</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/29203862$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-02349815$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Alculumbre, Solana G.</creatorcontrib><creatorcontrib>Saint-André, Violaine</creatorcontrib><creatorcontrib>Di Domizio, Jeremy</creatorcontrib><creatorcontrib>Vargas, Pablo</creatorcontrib><creatorcontrib>Sirven, Philemon</creatorcontrib><creatorcontrib>Bost, Pierre</creatorcontrib><creatorcontrib>Maurin, Mathieu</creatorcontrib><creatorcontrib>Maiuri, Paolo</creatorcontrib><creatorcontrib>Wery, Maxime</creatorcontrib><creatorcontrib>Roman, Mabel San</creatorcontrib><creatorcontrib>Savey, Léa</creatorcontrib><creatorcontrib>Touzot, Maxime</creatorcontrib><creatorcontrib>Terrier, Benjamin</creatorcontrib><creatorcontrib>Saadoun, David</creatorcontrib><creatorcontrib>Conrad, Curdin</creatorcontrib><creatorcontrib>Gilliet, Michel</creatorcontrib><creatorcontrib>Morillon, Antonin</creatorcontrib><creatorcontrib>Soumelis, Vassili</creatorcontrib><title>Diversification of human plasmacytoid predendritic cells in response to a single stimulus</title><title>Nature immunology</title><addtitle>Nat Immunol</addtitle><addtitle>Nat Immunol</addtitle><description>Innate immune cells adjust to microbial and inflammatory stimuli through a process termed environmental plasticity, which links a given individual stimulus to a unique activated state. Here, we report that activation of human plasmacytoid predendritic cells (pDCs) with a single microbial or cytokine stimulus triggers cell diversification into three stable subpopulations (P1–P3). P1-pDCs (PD-L1
+
CD80
–
) displayed a plasmacytoid morphology and specialization for type I interferon production. P3-pDCs (PD-L1
–
CD80
+
) adopted a dendritic morphology and adaptive immune functions. P2-pDCs (PD-L1
+
CD80
+
) displayed both innate and adaptive functions. Each subpopulation expressed a specific coding- and long-noncoding-RNA signature and was stable after secondary stimulation. P1-pDCs were detected in samples from patients with lupus or psoriasis. pDC diversification was independent of cell divisions or preexisting heterogeneity within steady-state pDCs but was controlled by a TNF autocrine and/or paracrine communication loop. Our findings reveal a novel mechanism for diversity and division of labor in innate immune cells.
Plasmacytoid dendritic cells (pDCs) are known for their copious IFN-I production. Soumelis and colleagues show that functionally and transcriptomically distinct human pDC populations can be generated from a single microbial or cytokine stimulus.</description><subject>Adaptive Immunity - immunology</subject><subject>Autocrine signalling</subject><subject>B7-1 Antigen - immunology</subject><subject>B7-1 Antigen - metabolism</subject><subject>B7-H1 Antigen - immunology</subject><subject>B7-H1 Antigen - metabolism</subject><subject>Biodiversity</subject><subject>Biological response modifiers</subject><subject>Biomedical and Life Sciences</subject><subject>Biomedicine</subject><subject>CD80 antigen</subject><subject>Cells, Cultured</subject><subject>Cytokines - genetics</subject><subject>Cytokines - immunology</subject><subject>Cytokines - metabolism</subject><subject>Dendritic cells</subject><subject>Dendritic Cells - immunology</subject><subject>Dendritic Cells - metabolism</subject><subject>Dendritic Cells - ultrastructure</subject><subject>Diversification</subject><subject>Division of labor</subject><subject>Gene Expression - immunology</subject><subject>Gene Expression Profiling - methods</subject><subject>Heterogeneity</subject><subject>Humans</subject><subject>Immunity, Innate - immunology</subject><subject>Immunology</subject><subject>Infectious Diseases</subject><subject>Inflammation</subject><subject>Innate immunity</subject><subject>Interferon</subject><subject>Interferon Type I - genetics</subject><subject>Interferon Type I - immunology</subject><subject>Interferon Type I - metabolism</subject><subject>Life Sciences</subject><subject>Lupus</subject><subject>Lupus Erythematosus, Systemic - immunology</subject><subject>Microscopy, Electron, Transmission</subject><subject>Morphology</subject><subject>Orthomyxoviridae - immunology</subject><subject>Paracrine signalling</subject><subject>PD-L1 protein</subject><subject>Psoriasis</subject><subject>Psoriasis - immunology</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>Skin diseases</subject><subject>Specialization</subject><subject>Subpopulations</subject><subject>Tumor necrosis factor</subject><issn>1529-2908</issn><issn>1529-2916</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><recordid>eNp1kktv1DAUhSMEoqXwA9ggS2zoIsXXzmOyHLVAK42ExGPBynLs66mrxB5sp6L99ThKGRgE8sLW9XeOdaxTFC-BngHlq7exgrqjJYW2pBRYef-oOIaadSXroHm8P9PVUfEsxpvMVG1TPS2OWMeyvmHHxbcLe4shWmOVTNY74g25nkbpyG6QcZTqLnmryS6gRqeDTVYRhcMQiXUkYNx5F5EkTySJ1m0HJDHZcRqm-Lx4YuQQ8cXDflJ8ff_uy_llufn44ep8vSlVTXkqNfStotwwBGY6rXXPa2V6bmSvaM0AQDaNlFx1vNXAmKFY9ahb09fQaqn5SXG6-F7LQeyCHWW4E15acbneiHlGGa-6FdS3kNk3C7sL_vuEMYnRxjmOdOinKKBrOWWs4U1GX_-F3vgpuJxkplrGWlbz39RWDiisMz4FqWZTsa4z0cAK5mfP_kHlpXG0yjs0Ns8PBKcHgswk_JG2copRXH3-dMjCwqrgYwxo9p8AVMw1EUtNRK6JmGsi7rPm1UO4qR9R7xW_epEBtgAxX7kthj_S_9f1J6_TxmA</recordid><startdate>20180101</startdate><enddate>20180101</enddate><creator>Alculumbre, Solana G.</creator><creator>Saint-André, Violaine</creator><creator>Di Domizio, Jeremy</creator><creator>Vargas, Pablo</creator><creator>Sirven, Philemon</creator><creator>Bost, Pierre</creator><creator>Maurin, Mathieu</creator><creator>Maiuri, Paolo</creator><creator>Wery, Maxime</creator><creator>Roman, Mabel San</creator><creator>Savey, Léa</creator><creator>Touzot, Maxime</creator><creator>Terrier, Benjamin</creator><creator>Saadoun, David</creator><creator>Conrad, Curdin</creator><creator>Gilliet, Michel</creator><creator>Morillon, Antonin</creator><creator>Soumelis, Vassili</creator><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>ISR</scope><scope>3V.</scope><scope>7QP</scope><scope>7QR</scope><scope>7T5</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>AEUYN</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</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>RC3</scope><scope>7X8</scope><scope>1XC</scope><orcidid>https://orcid.org/0000-0001-5079-445X</orcidid><orcidid>https://orcid.org/0000-0002-6281-3918</orcidid><orcidid>https://orcid.org/0000-0002-6475-494X</orcidid><orcidid>https://orcid.org/0000-0003-1849-9834</orcidid><orcidid>https://orcid.org/0000-0002-2162-0909</orcidid><orcidid>https://orcid.org/0000-0001-6612-7336</orcidid><orcidid>https://orcid.org/0000-0003-3628-9996</orcidid><orcidid>https://orcid.org/0000-0002-0575-5264</orcidid></search><sort><creationdate>20180101</creationdate><title>Diversification of human plasmacytoid predendritic cells in response to a single stimulus</title><author>Alculumbre, Solana G. ; Saint-André, Violaine ; Di Domizio, Jeremy ; Vargas, Pablo ; Sirven, Philemon ; Bost, Pierre ; Maurin, Mathieu ; Maiuri, Paolo ; Wery, Maxime ; Roman, Mabel San ; Savey, Léa ; Touzot, Maxime ; Terrier, Benjamin ; Saadoun, David ; Conrad, Curdin ; Gilliet, Michel ; Morillon, Antonin ; Soumelis, Vassili</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c503t-d1b7c03f2e12f9dddb35cfb3fabc052111a66aa3c937d122f0e4bed7fb517dad3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>Adaptive Immunity - immunology</topic><topic>Autocrine signalling</topic><topic>B7-1 Antigen - immunology</topic><topic>B7-1 Antigen - metabolism</topic><topic>B7-H1 Antigen - immunology</topic><topic>B7-H1 Antigen - metabolism</topic><topic>Biodiversity</topic><topic>Biological response modifiers</topic><topic>Biomedical and Life Sciences</topic><topic>Biomedicine</topic><topic>CD80 antigen</topic><topic>Cells, Cultured</topic><topic>Cytokines - genetics</topic><topic>Cytokines - immunology</topic><topic>Cytokines - metabolism</topic><topic>Dendritic cells</topic><topic>Dendritic Cells - immunology</topic><topic>Dendritic Cells - metabolism</topic><topic>Dendritic Cells - ultrastructure</topic><topic>Diversification</topic><topic>Division of labor</topic><topic>Gene Expression - immunology</topic><topic>Gene Expression Profiling - methods</topic><topic>Heterogeneity</topic><topic>Humans</topic><topic>Immunity, Innate - immunology</topic><topic>Immunology</topic><topic>Infectious Diseases</topic><topic>Inflammation</topic><topic>Innate immunity</topic><topic>Interferon</topic><topic>Interferon Type I - 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Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><jtitle>Nature immunology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Alculumbre, Solana G.</au><au>Saint-André, Violaine</au><au>Di Domizio, Jeremy</au><au>Vargas, Pablo</au><au>Sirven, Philemon</au><au>Bost, Pierre</au><au>Maurin, Mathieu</au><au>Maiuri, Paolo</au><au>Wery, Maxime</au><au>Roman, Mabel San</au><au>Savey, Léa</au><au>Touzot, Maxime</au><au>Terrier, Benjamin</au><au>Saadoun, David</au><au>Conrad, Curdin</au><au>Gilliet, Michel</au><au>Morillon, Antonin</au><au>Soumelis, Vassili</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Diversification of human plasmacytoid predendritic cells in response to a single stimulus</atitle><jtitle>Nature immunology</jtitle><stitle>Nat Immunol</stitle><addtitle>Nat Immunol</addtitle><date>2018-01-01</date><risdate>2018</risdate><volume>19</volume><issue>1</issue><spage>63</spage><epage>75</epage><pages>63-75</pages><issn>1529-2908</issn><eissn>1529-2916</eissn><abstract>Innate immune cells adjust to microbial and inflammatory stimuli through a process termed environmental plasticity, which links a given individual stimulus to a unique activated state. Here, we report that activation of human plasmacytoid predendritic cells (pDCs) with a single microbial or cytokine stimulus triggers cell diversification into three stable subpopulations (P1–P3). P1-pDCs (PD-L1
+
CD80
–
) displayed a plasmacytoid morphology and specialization for type I interferon production. P3-pDCs (PD-L1
–
CD80
+
) adopted a dendritic morphology and adaptive immune functions. P2-pDCs (PD-L1
+
CD80
+
) displayed both innate and adaptive functions. Each subpopulation expressed a specific coding- and long-noncoding-RNA signature and was stable after secondary stimulation. P1-pDCs were detected in samples from patients with lupus or psoriasis. pDC diversification was independent of cell divisions or preexisting heterogeneity within steady-state pDCs but was controlled by a TNF autocrine and/or paracrine communication loop. Our findings reveal a novel mechanism for diversity and division of labor in innate immune cells.
Plasmacytoid dendritic cells (pDCs) are known for their copious IFN-I production. Soumelis and colleagues show that functionally and transcriptomically distinct human pDC populations can be generated from a single microbial or cytokine stimulus.</abstract><cop>New York</cop><pub>Nature Publishing Group US</pub><pmid>29203862</pmid><doi>10.1038/s41590-017-0012-z</doi><tpages>13</tpages><orcidid>https://orcid.org/0000-0001-5079-445X</orcidid><orcidid>https://orcid.org/0000-0002-6281-3918</orcidid><orcidid>https://orcid.org/0000-0002-6475-494X</orcidid><orcidid>https://orcid.org/0000-0003-1849-9834</orcidid><orcidid>https://orcid.org/0000-0002-2162-0909</orcidid><orcidid>https://orcid.org/0000-0001-6612-7336</orcidid><orcidid>https://orcid.org/0000-0003-3628-9996</orcidid><orcidid>https://orcid.org/0000-0002-0575-5264</orcidid></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1529-2908 |
| ispartof | Nature immunology, 2018-01, Vol.19 (1), p.63-75 |
| issn | 1529-2908 1529-2916 |
| language | eng |
| recordid | cdi_hal_primary_oai_HAL_hal_02349815v1 |
| source | MEDLINE; SpringerLink Journals; Nature |
| subjects | Adaptive Immunity - immunology Autocrine signalling B7-1 Antigen - immunology B7-1 Antigen - metabolism B7-H1 Antigen - immunology B7-H1 Antigen - metabolism Biodiversity Biological response modifiers Biomedical and Life Sciences Biomedicine CD80 antigen Cells, Cultured Cytokines - genetics Cytokines - immunology Cytokines - metabolism Dendritic cells Dendritic Cells - immunology Dendritic Cells - metabolism Dendritic Cells - ultrastructure Diversification Division of labor Gene Expression - immunology Gene Expression Profiling - methods Heterogeneity Humans Immunity, Innate - immunology Immunology Infectious Diseases Inflammation Innate immunity Interferon Interferon Type I - genetics Interferon Type I - immunology Interferon Type I - metabolism Life Sciences Lupus Lupus Erythematosus, Systemic - immunology Microscopy, Electron, Transmission Morphology Orthomyxoviridae - immunology Paracrine signalling PD-L1 protein Psoriasis Psoriasis - immunology Ribonucleic acid RNA Skin diseases Specialization Subpopulations Tumor necrosis factor |
| title | Diversification of human plasmacytoid predendritic cells in response to a single stimulus |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-09T08%3A47%3A48IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_hal_p&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Diversification%20of%20human%20plasmacytoid%20predendritic%20cells%20in%20response%20to%20a%20single%20stimulus&rft.jtitle=Nature%20immunology&rft.au=Alculumbre,%20Solana%20G.&rft.date=2018-01-01&rft.volume=19&rft.issue=1&rft.spage=63&rft.epage=75&rft.pages=63-75&rft.issn=1529-2908&rft.eissn=1529-2916&rft_id=info:doi/10.1038/s41590-017-0012-z&rft_dat=%3Cgale_hal_p%3EA572561811%3C/gale_hal_p%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1977227253&rft_id=info:pmid/29203862&rft_galeid=A572561811&rfr_iscdi=true |