Epithelial endoplasmic reticulum stress orchestrates a protective IgA response
Immunoglobulin A (IgA) is the major secretory immunoglobulin isotype found at mucosal surfaces, where it regulates microbial commensalism and excludes luminal factors from contacting intestinal epithelial cells (IECs). IgA is induced by both T cell–dependent and –independent (TI) pathways. However,...
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| Veröffentlicht in: | Science (American Association for the Advancement of Science) 2019-03, Vol.363 (6430), p.993-998 |
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| creator | Grootjans, Joep Krupka, Niklas Hosomi, Shuhei Matute, Juan D. Hanley, Thomas Saveljeva, Svetlana Gensollen, Thomas Heijmans, Jarom Li, Hai Limenitakis, Julien P. Ganal-Vonarburg, Stephanie C. Suo, Shengbao Luoma, Adrienne M. Shimodaira, Yosuke Duan, Jinzhi Shih, David Q. Conner, Margaret E. Glickman, Jonathan N. Fuhler, Gwenny M. Palm, Noah W. de Zoete, Marcel R. van der Woude, C. Janneke Yuan, Guo-Cheng Wucherpfennig, Kai W. Targan, Stephan R. Rosenstiel, Philip Flavell, Richard A. McCoy, Kathy D. Macpherson, Andrew J. Kaser, Arthur Blumberg, Richard S. |
| description | Immunoglobulin A (IgA) is the major secretory immunoglobulin isotype found at mucosal surfaces, where it regulates microbial commensalism and excludes luminal factors from contacting intestinal epithelial cells (IECs). IgA is induced by both T cell–dependent and –independent (TI) pathways. However, little is known about TI regulation. We report that IEC endoplasmic reticulum (ER) stress induces a polyreactive IgA response, which is protective against enteric inflammation. IEC ER stress causes TI and microbiota-independent expansion and activation of peritoneal B1b cells, which culminates in increased lamina propria and luminal IgA. Increased numbers of IgA-producing plasma cells were observed in healthy humans with defective autophagy, who are known to exhibit IEC ER stress. Upon ER stress, IECs communicate signals to the peritoneum that induce a barrier-protective TI IgA response. |
| doi_str_mv | 10.1126/science.aat7186 |
| format | Article |
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Janneke ; Yuan, Guo-Cheng ; Wucherpfennig, Kai W. ; Targan, Stephan R. ; Rosenstiel, Philip ; Flavell, Richard A. ; McCoy, Kathy D. ; Macpherson, Andrew J. ; Kaser, Arthur ; Blumberg, Richard S.</creator><creatorcontrib>Grootjans, Joep ; Krupka, Niklas ; Hosomi, Shuhei ; Matute, Juan D. ; Hanley, Thomas ; Saveljeva, Svetlana ; Gensollen, Thomas ; Heijmans, Jarom ; Li, Hai ; Limenitakis, Julien P. ; Ganal-Vonarburg, Stephanie C. ; Suo, Shengbao ; Luoma, Adrienne M. ; Shimodaira, Yosuke ; Duan, Jinzhi ; Shih, David Q. ; Conner, Margaret E. ; Glickman, Jonathan N. ; Fuhler, Gwenny M. ; Palm, Noah W. ; de Zoete, Marcel R. ; van der Woude, C. Janneke ; Yuan, Guo-Cheng ; Wucherpfennig, Kai W. ; Targan, Stephan R. ; Rosenstiel, Philip ; Flavell, Richard A. ; McCoy, Kathy D. ; Macpherson, Andrew J. ; Kaser, Arthur ; Blumberg, Richard S.</creatorcontrib><description>Immunoglobulin A (IgA) is the major secretory immunoglobulin isotype found at mucosal surfaces, where it regulates microbial commensalism and excludes luminal factors from contacting intestinal epithelial cells (IECs). IgA is induced by both T cell–dependent and –independent (TI) pathways. However, little is known about TI regulation. We report that IEC endoplasmic reticulum (ER) stress induces a polyreactive IgA response, which is protective against enteric inflammation. IEC ER stress causes TI and microbiota-independent expansion and activation of peritoneal B1b cells, which culminates in increased lamina propria and luminal IgA. Increased numbers of IgA-producing plasma cells were observed in healthy humans with defective autophagy, who are known to exhibit IEC ER stress. Upon ER stress, IECs communicate signals to the peritoneum that induce a barrier-protective TI IgA response.</description><identifier>ISSN: 0036-8075</identifier><identifier>ISSN: 1095-9203</identifier><identifier>EISSN: 1095-9203</identifier><identifier>DOI: 10.1126/science.aat7186</identifier><identifier>PMID: 30819965</identifier><language>eng</language><publisher>United States: American Association for the Advancement of Science</publisher><subject>Animals ; Autophagy ; Autophagy-Related Proteins - genetics ; Commensalism ; Endoplasmic reticulum ; Endoplasmic Reticulum Stress ; Epithelial cells ; Epithelial Cells - immunology ; Epithelium ; Gastrointestinal tract ; Humans ; Immunity, Mucosal ; Immunoglobulin A ; Immunoglobulin A - immunology ; Immunoglobulins ; Inflammation ; Intestinal Mucosa - immunology ; Lamina propria ; Lymphocytes ; Lymphocytes T ; Mice ; Mice, Inbred C57BL ; Mice, Knockout ; Microbiota ; Microorganisms ; Mucosa ; Peritoneum ; Phagocytosis ; Plasma cells ; Plasma Cells - immunology ; Stress ; Tissue Culture Techniques ; X-Box Binding Protein 1 - genetics</subject><ispartof>Science (American Association for the Advancement of Science), 2019-03, Vol.363 (6430), p.993-998</ispartof><rights>Copyright © 2019 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works.</rights><rights>Copyright © 2019 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c509t-e6268cad8aa3858785f4e32be594e800cd047339edc846675bbaf877ac4ccc753</citedby><cites>FETCH-LOGICAL-c509t-e6268cad8aa3858785f4e32be594e800cd047339edc846675bbaf877ac4ccc753</cites><orcidid>0000-0002-1829-302X ; 0000-0002-0644-9752 ; 0000-0003-1335-7044 ; 0000-0002-2548-7754 ; 0000-0001-7262-9455 ; 0000-0002-8808-5672 ; 0000-0002-2805-4831 ; 0000-0003-4461-0778 ; 0000-0003-0314-9196 ; 0000-0002-3900-9227 ; 0000-0002-7146-8159 ; 0000-0003-1419-3344 ; 0000-0002-9704-248X ; 0000-0001-5948-7536 ; 0000-0003-3875-6957 ; 0000-0002-4270-8299 ; 0000-0002-7192-0184 ; 0000-0001-9351-4956 ; 0000-0001-9615-7851 ; 0000-0002-9834-5490 ; 0000-0002-6785-3492 ; 0000-0003-0910-2655</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,776,780,881,2871,2872,27901,27902</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30819965$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Grootjans, Joep</creatorcontrib><creatorcontrib>Krupka, Niklas</creatorcontrib><creatorcontrib>Hosomi, Shuhei</creatorcontrib><creatorcontrib>Matute, Juan D.</creatorcontrib><creatorcontrib>Hanley, Thomas</creatorcontrib><creatorcontrib>Saveljeva, Svetlana</creatorcontrib><creatorcontrib>Gensollen, Thomas</creatorcontrib><creatorcontrib>Heijmans, Jarom</creatorcontrib><creatorcontrib>Li, Hai</creatorcontrib><creatorcontrib>Limenitakis, Julien P.</creatorcontrib><creatorcontrib>Ganal-Vonarburg, Stephanie C.</creatorcontrib><creatorcontrib>Suo, Shengbao</creatorcontrib><creatorcontrib>Luoma, Adrienne M.</creatorcontrib><creatorcontrib>Shimodaira, Yosuke</creatorcontrib><creatorcontrib>Duan, Jinzhi</creatorcontrib><creatorcontrib>Shih, David Q.</creatorcontrib><creatorcontrib>Conner, Margaret E.</creatorcontrib><creatorcontrib>Glickman, Jonathan N.</creatorcontrib><creatorcontrib>Fuhler, Gwenny M.</creatorcontrib><creatorcontrib>Palm, Noah W.</creatorcontrib><creatorcontrib>de Zoete, Marcel R.</creatorcontrib><creatorcontrib>van der Woude, C. Janneke</creatorcontrib><creatorcontrib>Yuan, Guo-Cheng</creatorcontrib><creatorcontrib>Wucherpfennig, Kai W.</creatorcontrib><creatorcontrib>Targan, Stephan R.</creatorcontrib><creatorcontrib>Rosenstiel, Philip</creatorcontrib><creatorcontrib>Flavell, Richard A.</creatorcontrib><creatorcontrib>McCoy, Kathy D.</creatorcontrib><creatorcontrib>Macpherson, Andrew J.</creatorcontrib><creatorcontrib>Kaser, Arthur</creatorcontrib><creatorcontrib>Blumberg, Richard S.</creatorcontrib><title>Epithelial endoplasmic reticulum stress orchestrates a protective IgA response</title><title>Science (American Association for the Advancement of Science)</title><addtitle>Science</addtitle><description>Immunoglobulin A (IgA) is the major secretory immunoglobulin isotype found at mucosal surfaces, where it regulates microbial commensalism and excludes luminal factors from contacting intestinal epithelial cells (IECs). IgA is induced by both T cell–dependent and –independent (TI) pathways. However, little is known about TI regulation. We report that IEC endoplasmic reticulum (ER) stress induces a polyreactive IgA response, which is protective against enteric inflammation. IEC ER stress causes TI and microbiota-independent expansion and activation of peritoneal B1b cells, which culminates in increased lamina propria and luminal IgA. Increased numbers of IgA-producing plasma cells were observed in healthy humans with defective autophagy, who are known to exhibit IEC ER stress. 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Janneke ; Yuan, Guo-Cheng ; Wucherpfennig, Kai W. ; Targan, Stephan R. ; Rosenstiel, Philip ; Flavell, Richard A. ; McCoy, Kathy D. ; Macpherson, Andrew J. ; Kaser, Arthur ; Blumberg, Richard S.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c509t-e6268cad8aa3858785f4e32be594e800cd047339edc846675bbaf877ac4ccc753</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Animals</topic><topic>Autophagy</topic><topic>Autophagy-Related Proteins - genetics</topic><topic>Commensalism</topic><topic>Endoplasmic reticulum</topic><topic>Endoplasmic Reticulum Stress</topic><topic>Epithelial cells</topic><topic>Epithelial Cells - immunology</topic><topic>Epithelium</topic><topic>Gastrointestinal tract</topic><topic>Humans</topic><topic>Immunity, Mucosal</topic><topic>Immunoglobulin A</topic><topic>Immunoglobulin A - immunology</topic><topic>Immunoglobulins</topic><topic>Inflammation</topic><topic>Intestinal Mucosa - immunology</topic><topic>Lamina propria</topic><topic>Lymphocytes</topic><topic>Lymphocytes T</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>Mice, Knockout</topic><topic>Microbiota</topic><topic>Microorganisms</topic><topic>Mucosa</topic><topic>Peritoneum</topic><topic>Phagocytosis</topic><topic>Plasma cells</topic><topic>Plasma Cells - immunology</topic><topic>Stress</topic><topic>Tissue Culture Techniques</topic><topic>X-Box Binding Protein 1 - genetics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Grootjans, Joep</creatorcontrib><creatorcontrib>Krupka, Niklas</creatorcontrib><creatorcontrib>Hosomi, Shuhei</creatorcontrib><creatorcontrib>Matute, Juan D.</creatorcontrib><creatorcontrib>Hanley, Thomas</creatorcontrib><creatorcontrib>Saveljeva, Svetlana</creatorcontrib><creatorcontrib>Gensollen, Thomas</creatorcontrib><creatorcontrib>Heijmans, Jarom</creatorcontrib><creatorcontrib>Li, Hai</creatorcontrib><creatorcontrib>Limenitakis, Julien P.</creatorcontrib><creatorcontrib>Ganal-Vonarburg, Stephanie C.</creatorcontrib><creatorcontrib>Suo, Shengbao</creatorcontrib><creatorcontrib>Luoma, Adrienne M.</creatorcontrib><creatorcontrib>Shimodaira, Yosuke</creatorcontrib><creatorcontrib>Duan, Jinzhi</creatorcontrib><creatorcontrib>Shih, David Q.</creatorcontrib><creatorcontrib>Conner, Margaret E.</creatorcontrib><creatorcontrib>Glickman, Jonathan N.</creatorcontrib><creatorcontrib>Fuhler, Gwenny M.</creatorcontrib><creatorcontrib>Palm, Noah W.</creatorcontrib><creatorcontrib>de Zoete, Marcel R.</creatorcontrib><creatorcontrib>van der Woude, C. 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Janneke</au><au>Yuan, Guo-Cheng</au><au>Wucherpfennig, Kai W.</au><au>Targan, Stephan R.</au><au>Rosenstiel, Philip</au><au>Flavell, Richard A.</au><au>McCoy, Kathy D.</au><au>Macpherson, Andrew J.</au><au>Kaser, Arthur</au><au>Blumberg, Richard S.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Epithelial endoplasmic reticulum stress orchestrates a protective IgA response</atitle><jtitle>Science (American Association for the Advancement of Science)</jtitle><addtitle>Science</addtitle><date>2019-03-01</date><risdate>2019</risdate><volume>363</volume><issue>6430</issue><spage>993</spage><epage>998</epage><pages>993-998</pages><issn>0036-8075</issn><issn>1095-9203</issn><eissn>1095-9203</eissn><abstract>Immunoglobulin A (IgA) is the major secretory immunoglobulin isotype found at mucosal surfaces, where it regulates microbial commensalism and excludes luminal factors from contacting intestinal epithelial cells (IECs). IgA is induced by both T cell–dependent and –independent (TI) pathways. However, little is known about TI regulation. We report that IEC endoplasmic reticulum (ER) stress induces a polyreactive IgA response, which is protective against enteric inflammation. IEC ER stress causes TI and microbiota-independent expansion and activation of peritoneal B1b cells, which culminates in increased lamina propria and luminal IgA. Increased numbers of IgA-producing plasma cells were observed in healthy humans with defective autophagy, who are known to exhibit IEC ER stress. Upon ER stress, IECs communicate signals to the peritoneum that induce a barrier-protective TI IgA response.</abstract><cop>United States</cop><pub>American Association for the Advancement of Science</pub><pmid>30819965</pmid><doi>10.1126/science.aat7186</doi><tpages>6</tpages><orcidid>https://orcid.org/0000-0002-1829-302X</orcidid><orcidid>https://orcid.org/0000-0002-0644-9752</orcidid><orcidid>https://orcid.org/0000-0003-1335-7044</orcidid><orcidid>https://orcid.org/0000-0002-2548-7754</orcidid><orcidid>https://orcid.org/0000-0001-7262-9455</orcidid><orcidid>https://orcid.org/0000-0002-8808-5672</orcidid><orcidid>https://orcid.org/0000-0002-2805-4831</orcidid><orcidid>https://orcid.org/0000-0003-4461-0778</orcidid><orcidid>https://orcid.org/0000-0003-0314-9196</orcidid><orcidid>https://orcid.org/0000-0002-3900-9227</orcidid><orcidid>https://orcid.org/0000-0002-7146-8159</orcidid><orcidid>https://orcid.org/0000-0003-1419-3344</orcidid><orcidid>https://orcid.org/0000-0002-9704-248X</orcidid><orcidid>https://orcid.org/0000-0001-5948-7536</orcidid><orcidid>https://orcid.org/0000-0003-3875-6957</orcidid><orcidid>https://orcid.org/0000-0002-4270-8299</orcidid><orcidid>https://orcid.org/0000-0002-7192-0184</orcidid><orcidid>https://orcid.org/0000-0001-9351-4956</orcidid><orcidid>https://orcid.org/0000-0001-9615-7851</orcidid><orcidid>https://orcid.org/0000-0002-9834-5490</orcidid><orcidid>https://orcid.org/0000-0002-6785-3492</orcidid><orcidid>https://orcid.org/0000-0003-0910-2655</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 0036-8075 |
| ispartof | Science (American Association for the Advancement of Science), 2019-03, Vol.363 (6430), p.993-998 |
| issn | 0036-8075 1095-9203 1095-9203 |
| language | eng |
| recordid | cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_6637967 |
| source | American Association for the Advancement of Science; MEDLINE |
| subjects | Animals Autophagy Autophagy-Related Proteins - genetics Commensalism Endoplasmic reticulum Endoplasmic Reticulum Stress Epithelial cells Epithelial Cells - immunology Epithelium Gastrointestinal tract Humans Immunity, Mucosal Immunoglobulin A Immunoglobulin A - immunology Immunoglobulins Inflammation Intestinal Mucosa - immunology Lamina propria Lymphocytes Lymphocytes T Mice Mice, Inbred C57BL Mice, Knockout Microbiota Microorganisms Mucosa Peritoneum Phagocytosis Plasma cells Plasma Cells - immunology Stress Tissue Culture Techniques X-Box Binding Protein 1 - genetics |
| title | Epithelial endoplasmic reticulum stress orchestrates a protective IgA response |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-08T06%3A18%3A02IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-jstor_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Epithelial%20endoplasmic%20reticulum%20stress%20orchestrates%20a%20protective%20IgA%20response&rft.jtitle=Science%20(American%20Association%20for%20the%20Advancement%20of%20Science)&rft.au=Grootjans,%20Joep&rft.date=2019-03-01&rft.volume=363&rft.issue=6430&rft.spage=993&rft.epage=998&rft.pages=993-998&rft.issn=0036-8075&rft.eissn=1095-9203&rft_id=info:doi/10.1126/science.aat7186&rft_dat=%3Cjstor_pubme%3E26611649%3C/jstor_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2187118810&rft_id=info:pmid/30819965&rft_jstor_id=26611649&rfr_iscdi=true |