Epithelial damage and tissue γδ T cells promote a unique tumor-protective IgE response
IgE is an ancient and conserved immunoglobulin isotype with potent immunological function. Nevertheless, the regulation of IgE responses remains an enigma, and evidence of a role for IgE in host defense is limited. Here we report that topical exposure to a common environmental DNA-damaging xenobioti...
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| Veröffentlicht in: | Nature immunology 2018-08, Vol.19 (8), p.859-870 |
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| creator | Crawford, Greg Hayes, Mark David Seoane, Rocio Castro Ward, Sophie Dalessandri, Tim Lai, Chester Healy, Eugene Kipling, David Proby, Charlotte Moyes, Colin Green, Kile Best, Katie Haniffa, Muzlifah Botto, Marina Dunn-Walters, Deborah Strid, Jessica |
| description | IgE is an ancient and conserved immunoglobulin isotype with potent immunological function. Nevertheless, the regulation of IgE responses remains an enigma, and evidence of a role for IgE in host defense is limited. Here we report that topical exposure to a common environmental DNA-damaging xenobiotic initiated stress surveillance by γδTCR
+
intraepithelial lymphocytes that resulted in class switching to IgE in B cells and the accumulation of autoreactive IgE. High-throughput antibody sequencing revealed that γδ T cells shaped the IgE repertoire by supporting specific variable-diversity-joining (VDJ) rearrangements with unique characteristics of the complementarity-determining region CDRH3. This endogenous IgE response, via the IgE receptor FcεRI, provided protection against epithelial carcinogenesis, and expression of the gene encoding FcεRI in human squamous-cell carcinoma correlated with good disease prognosis. These data indicate a joint role for immunosurveillance by T cells and by B cells in epithelial tissues and suggest that IgE is part of the host defense against epithelial damage and tumor development.
Evidence of protective and homeostatic roles for IgE is relatively limited. Strid and colleagues demonstrate that γδ T cells induce switching to IgE that provides protection against experimentally induced epithelial cancer. |
| doi_str_mv | 10.1038/s41590-018-0161-8 |
| format | Article |
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+
intraepithelial lymphocytes that resulted in class switching to IgE in B cells and the accumulation of autoreactive IgE. High-throughput antibody sequencing revealed that γδ T cells shaped the IgE repertoire by supporting specific variable-diversity-joining (VDJ) rearrangements with unique characteristics of the complementarity-determining region CDRH3. This endogenous IgE response, via the IgE receptor FcεRI, provided protection against epithelial carcinogenesis, and expression of the gene encoding FcεRI in human squamous-cell carcinoma correlated with good disease prognosis. These data indicate a joint role for immunosurveillance by T cells and by B cells in epithelial tissues and suggest that IgE is part of the host defense against epithelial damage and tumor development.
Evidence of protective and homeostatic roles for IgE is relatively limited. Strid and colleagues demonstrate that γδ T cells induce switching to IgE that provides protection against experimentally induced epithelial cancer.</description><identifier>ISSN: 1529-2908</identifier><identifier>EISSN: 1529-2916</identifier><identifier>DOI: 10.1038/s41590-018-0161-8</identifier><identifier>PMID: 30013146</identifier><language>eng</language><publisher>New York: Nature Publishing Group US</publisher><subject>631/250 ; 631/250/580/1884 ; Animals ; Anthracenes - toxicity ; B-Lymphocytes - physiology ; Biomedical and Life Sciences ; Biomedicine ; Carcinogenesis ; Carcinoma, Squamous Cell - diagnosis ; Carcinoma, Squamous Cell - immunology ; Cell Death ; Cells, Cultured ; Class switching ; Complementarity Determining Regions - genetics ; Complementarity-determining region ; DNA Damage ; Environmental DNA ; Epithelial Cells - physiology ; Female ; High-Throughput Nucleotide Sequencing ; Immunoglobulin Class Switching ; Immunoglobulin E ; Immunoglobulin E - genetics ; Immunoglobulin E - metabolism ; Immunologic Surveillance ; Immunology ; Immunosurveillance ; Infectious Diseases ; Intraepithelial Lymphocytes - physiology ; Lymphocytes ; Lymphocytes B ; Lymphocytes T ; Mice ; Mice, Inbred C57BL ; Mice, Knockout ; Neoplasms, Experimental - chemically induced ; Neoplasms, Experimental - immunology ; Piperidines - toxicity ; Prognosis ; Receptors, Antigen, T-Cell, gamma-delta - genetics ; Receptors, Antigen, T-Cell, gamma-delta - metabolism ; Receptors, IgE - metabolism ; Squamous cell carcinoma</subject><ispartof>Nature immunology, 2018-08, Vol.19 (8), p.859-870</ispartof><rights>The Author(s) 2018</rights><rights>Copyright Nature Publishing Group Aug 2018</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4238-a4af6b07460ccb000650d84a1a13b7a2e16baad68983218936f5b70831b497563</citedby><cites>FETCH-LOGICAL-c4238-a4af6b07460ccb000650d84a1a13b7a2e16baad68983218936f5b70831b497563</cites><orcidid>0000-0003-3690-2201 ; 0000-0002-0927-5954 ; 0000-0002-3927-2084 ; 0000-0003-2282-5655 ; 0000-0001-5591-6970</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/s41590-018-0161-8$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1038/s41590-018-0161-8$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>230,314,550,776,780,881,27901,27902,41464,42533,51294</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30013146$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttp://kipublications.ki.se/Default.aspx?queryparsed=id:138798778$$DView record from Swedish Publication Index$$Hfree_for_read</backlink></links><search><creatorcontrib>Crawford, Greg</creatorcontrib><creatorcontrib>Hayes, Mark David</creatorcontrib><creatorcontrib>Seoane, Rocio Castro</creatorcontrib><creatorcontrib>Ward, Sophie</creatorcontrib><creatorcontrib>Dalessandri, Tim</creatorcontrib><creatorcontrib>Lai, Chester</creatorcontrib><creatorcontrib>Healy, Eugene</creatorcontrib><creatorcontrib>Kipling, David</creatorcontrib><creatorcontrib>Proby, Charlotte</creatorcontrib><creatorcontrib>Moyes, Colin</creatorcontrib><creatorcontrib>Green, Kile</creatorcontrib><creatorcontrib>Best, Katie</creatorcontrib><creatorcontrib>Haniffa, Muzlifah</creatorcontrib><creatorcontrib>Botto, Marina</creatorcontrib><creatorcontrib>Dunn-Walters, Deborah</creatorcontrib><creatorcontrib>Strid, Jessica</creatorcontrib><title>Epithelial damage and tissue γδ T cells promote a unique tumor-protective IgE response</title><title>Nature immunology</title><addtitle>Nat Immunol</addtitle><addtitle>Nat Immunol</addtitle><description>IgE is an ancient and conserved immunoglobulin isotype with potent immunological function. Nevertheless, the regulation of IgE responses remains an enigma, and evidence of a role for IgE in host defense is limited. Here we report that topical exposure to a common environmental DNA-damaging xenobiotic initiated stress surveillance by γδTCR
+
intraepithelial lymphocytes that resulted in class switching to IgE in B cells and the accumulation of autoreactive IgE. High-throughput antibody sequencing revealed that γδ T cells shaped the IgE repertoire by supporting specific variable-diversity-joining (VDJ) rearrangements with unique characteristics of the complementarity-determining region CDRH3. This endogenous IgE response, via the IgE receptor FcεRI, provided protection against epithelial carcinogenesis, and expression of the gene encoding FcεRI in human squamous-cell carcinoma correlated with good disease prognosis. These data indicate a joint role for immunosurveillance by T cells and by B cells in epithelial tissues and suggest that IgE is part of the host defense against epithelial damage and tumor development.
Evidence of protective and homeostatic roles for IgE is relatively limited. Strid and colleagues demonstrate that γδ T cells induce switching to IgE that provides protection against experimentally induced epithelial cancer.</description><subject>631/250</subject><subject>631/250/580/1884</subject><subject>Animals</subject><subject>Anthracenes - toxicity</subject><subject>B-Lymphocytes - physiology</subject><subject>Biomedical and Life Sciences</subject><subject>Biomedicine</subject><subject>Carcinogenesis</subject><subject>Carcinoma, Squamous Cell - diagnosis</subject><subject>Carcinoma, Squamous Cell - immunology</subject><subject>Cell Death</subject><subject>Cells, Cultured</subject><subject>Class switching</subject><subject>Complementarity Determining Regions - genetics</subject><subject>Complementarity-determining region</subject><subject>DNA Damage</subject><subject>Environmental DNA</subject><subject>Epithelial Cells - physiology</subject><subject>Female</subject><subject>High-Throughput Nucleotide Sequencing</subject><subject>Immunoglobulin Class 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damage and tissue γδ T cells promote a unique tumor-protective IgE response</title><author>Crawford, Greg ; Hayes, Mark David ; Seoane, Rocio Castro ; Ward, Sophie ; Dalessandri, Tim ; Lai, Chester ; Healy, Eugene ; Kipling, David ; Proby, Charlotte ; Moyes, Colin ; Green, Kile ; Best, Katie ; Haniffa, Muzlifah ; Botto, Marina ; Dunn-Walters, Deborah ; Strid, Jessica</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4238-a4af6b07460ccb000650d84a1a13b7a2e16baad68983218936f5b70831b497563</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>631/250</topic><topic>631/250/580/1884</topic><topic>Animals</topic><topic>Anthracenes - toxicity</topic><topic>B-Lymphocytes - physiology</topic><topic>Biomedical and Life Sciences</topic><topic>Biomedicine</topic><topic>Carcinogenesis</topic><topic>Carcinoma, Squamous Cell - diagnosis</topic><topic>Carcinoma, Squamous Cell - 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Marina</au><au>Dunn-Walters, Deborah</au><au>Strid, Jessica</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Epithelial damage and tissue γδ T cells promote a unique tumor-protective IgE response</atitle><jtitle>Nature immunology</jtitle><stitle>Nat Immunol</stitle><addtitle>Nat Immunol</addtitle><date>2018-08-01</date><risdate>2018</risdate><volume>19</volume><issue>8</issue><spage>859</spage><epage>870</epage><pages>859-870</pages><issn>1529-2908</issn><eissn>1529-2916</eissn><abstract>IgE is an ancient and conserved immunoglobulin isotype with potent immunological function. Nevertheless, the regulation of IgE responses remains an enigma, and evidence of a role for IgE in host defense is limited. Here we report that topical exposure to a common environmental DNA-damaging xenobiotic initiated stress surveillance by γδTCR
+
intraepithelial lymphocytes that resulted in class switching to IgE in B cells and the accumulation of autoreactive IgE. High-throughput antibody sequencing revealed that γδ T cells shaped the IgE repertoire by supporting specific variable-diversity-joining (VDJ) rearrangements with unique characteristics of the complementarity-determining region CDRH3. This endogenous IgE response, via the IgE receptor FcεRI, provided protection against epithelial carcinogenesis, and expression of the gene encoding FcεRI in human squamous-cell carcinoma correlated with good disease prognosis. These data indicate a joint role for immunosurveillance by T cells and by B cells in epithelial tissues and suggest that IgE is part of the host defense against epithelial damage and tumor development.
Evidence of protective and homeostatic roles for IgE is relatively limited. Strid and colleagues demonstrate that γδ T cells induce switching to IgE that provides protection against experimentally induced epithelial cancer.</abstract><cop>New York</cop><pub>Nature Publishing Group US</pub><pmid>30013146</pmid><doi>10.1038/s41590-018-0161-8</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0003-3690-2201</orcidid><orcidid>https://orcid.org/0000-0002-0927-5954</orcidid><orcidid>https://orcid.org/0000-0002-3927-2084</orcidid><orcidid>https://orcid.org/0000-0003-2282-5655</orcidid><orcidid>https://orcid.org/0000-0001-5591-6970</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1529-2908 |
| ispartof | Nature immunology, 2018-08, Vol.19 (8), p.859-870 |
| issn | 1529-2908 1529-2916 |
| language | eng |
| recordid | cdi_swepub_primary_oai_swepub_ki_se_486942 |
| source | MEDLINE; SpringerLink Journals; Nature Journals Online; SWEPUB Freely available online |
| subjects | 631/250 631/250/580/1884 Animals Anthracenes - toxicity B-Lymphocytes - physiology Biomedical and Life Sciences Biomedicine Carcinogenesis Carcinoma, Squamous Cell - diagnosis Carcinoma, Squamous Cell - immunology Cell Death Cells, Cultured Class switching Complementarity Determining Regions - genetics Complementarity-determining region DNA Damage Environmental DNA Epithelial Cells - physiology Female High-Throughput Nucleotide Sequencing Immunoglobulin Class Switching Immunoglobulin E Immunoglobulin E - genetics Immunoglobulin E - metabolism Immunologic Surveillance Immunology Immunosurveillance Infectious Diseases Intraepithelial Lymphocytes - physiology Lymphocytes Lymphocytes B Lymphocytes T Mice Mice, Inbred C57BL Mice, Knockout Neoplasms, Experimental - chemically induced Neoplasms, Experimental - immunology Piperidines - toxicity Prognosis Receptors, Antigen, T-Cell, gamma-delta - genetics Receptors, Antigen, T-Cell, gamma-delta - metabolism Receptors, IgE - metabolism Squamous cell carcinoma |
| title | Epithelial damage and tissue γδ T cells promote a unique tumor-protective IgE response |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-19T08%3A04%3A25IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_swepu&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Epithelial%20damage%20and%20tissue%20%CE%B3%CE%B4%20T%20cells%20promote%20a%20unique%20tumor-protective%20IgE%20response&rft.jtitle=Nature%20immunology&rft.au=Crawford,%20Greg&rft.date=2018-08-01&rft.volume=19&rft.issue=8&rft.spage=859&rft.epage=870&rft.pages=859-870&rft.issn=1529-2908&rft.eissn=1529-2916&rft_id=info:doi/10.1038/s41590-018-0161-8&rft_dat=%3Cproquest_swepu%3E2074114991%3C/proquest_swepu%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2074114991&rft_id=info:pmid/30013146&rfr_iscdi=true |