Goblet cell associated antigen passages support the induction and maintenance of oral tolerance
Tolerance to innocuous antigens from the diet and the commensal microbiota is a fundamental process essential to health. Why tolerance is efficiently induced to substances arising from the hostile environment of the gut lumen is incompletely understood but may be related to how these antigens are en...
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| Veröffentlicht in: | Mucosal immunology 2020-03, Vol.13 (2), p.271-282 |
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| creator | Kulkarni, Devesha H. Gustafsson, Jenny K. Knoop, Kathryn A. McDonald, Keely G. Bidani, Shay S. Davis, Jazmyne E. Floyd, Alexandria N. Hogan, Simon P. Hsieh, Chyi-Song Newberry, Rodney D. |
| description | Tolerance to innocuous antigens from the diet and the commensal microbiota is a fundamental process essential to health. Why tolerance is efficiently induced to substances arising from the hostile environment of the gut lumen is incompletely understood but may be related to how these antigens are encountered by the immune system. We observed that goblet cell associated antigen passages (GAPs), but not other pathways of luminal antigen capture, correlated with the acquisition of luminal substances by lamina propria (LP) antigen presenting cells (APCs) and with the sites of tolerance induction to luminal antigens. Strikingly this role extended beyond antigen delivery. The GAP function of goblet cells facilitated maintenance of pre-existing LP T regulatory cells (Tregs), imprinting LP-dendritic cells with tolerogenic properties, and facilitating LP macrophages to produce the immunomodulatory cytokine IL-10. Moreover, tolerance to dietary antigen was impaired in the absence of GAPs. Thus, by delivering luminal antigens, maintaining pre-existing LP Tregs, and imprinting tolerogenic properties on LP-APCs GAPs support tolerance to substances encountered in the hostile environment of the gut lumen. |
| doi_str_mv | 10.1038/s41385-019-0240-7 |
| format | Article |
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Why tolerance is efficiently induced to substances arising from the hostile environment of the gut lumen is incompletely understood but may be related to how these antigens are encountered by the immune system. We observed that goblet cell associated antigen passages (GAPs), but not other pathways of luminal antigen capture, correlated with the acquisition of luminal substances by lamina propria (LP) antigen presenting cells (APCs) and with the sites of tolerance induction to luminal antigens. Strikingly this role extended beyond antigen delivery. The GAP function of goblet cells facilitated maintenance of pre-existing LP T regulatory cells (Tregs), imprinting LP-dendritic cells with tolerogenic properties, and facilitating LP macrophages to produce the immunomodulatory cytokine IL-10. Moreover, tolerance to dietary antigen was impaired in the absence of GAPs. Thus, by delivering luminal antigens, maintaining pre-existing LP Tregs, and imprinting tolerogenic properties on LP-APCs GAPs support tolerance to substances encountered in the hostile environment of the gut lumen.</description><identifier>ISSN: 1933-0219</identifier><identifier>EISSN: 1935-3456</identifier><identifier>DOI: 10.1038/s41385-019-0240-7</identifier><identifier>PMID: 31819172</identifier><language>eng</language><publisher>New York: Nature Publishing Group US</publisher><subject>Administration, Oral ; Allergology ; Animals ; Antibodies ; Antigen Presentation ; Antigen-presenting cells ; Antigen-Presenting Cells - immunology ; Antigens ; Antigens - immunology ; Biomedical and Life Sciences ; Biomedicine ; Cells, Cultured ; Dendritic cells ; Dendritic Cells - immunology ; Gastroenterology ; Goblet cells ; Goblet Cells - immunology ; GTPase-Activating Proteins - metabolism ; Immune system ; Immune Tolerance ; Immunological tolerance ; Immunology ; Immunomodulation ; Immunoregulation ; Interleukin 10 ; Interleukin-10 - metabolism ; Lamina propria ; Life Sciences & Biomedicine ; Lymphocytes T ; Macrophages ; Macrophages - immunology ; Mice ; Mice, Inbred C57BL ; Mice, Transgenic ; Microbiota ; Mucous Membrane - immunology ; Science & Technology ; T-Lymphocytes, Regulatory - immunology</subject><ispartof>Mucosal immunology, 2020-03, Vol.13 (2), p.271-282</ispartof><rights>Society for Mucosal Immunology 2019</rights><rights>2019© Society for Mucosal Immunology 2019</rights><rights>Society for Mucosal Immunology 2019.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>true</woscitedreferencessubscribed><woscitedreferencescount>88</woscitedreferencescount><woscitedreferencesoriginalsourcerecordid>wos000518456900008</woscitedreferencesoriginalsourcerecordid><cites>FETCH-LOGICAL-p262t-6b5db77cda51eed5ae13d17ec856cb1fb8235e0f359d106406a576a30d919b273</cites><orcidid>0000-0003-2007-3066</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.proquest.com/docview/2362200588?pq-origsite=primo$$EHTML$$P50$$Gproquest$$H</linktohtml><link.rule.ids>230,315,782,786,887,27931,27932,28255,64392,64396,72476</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31819172$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Kulkarni, Devesha H.</creatorcontrib><creatorcontrib>Gustafsson, Jenny K.</creatorcontrib><creatorcontrib>Knoop, Kathryn A.</creatorcontrib><creatorcontrib>McDonald, Keely G.</creatorcontrib><creatorcontrib>Bidani, Shay S.</creatorcontrib><creatorcontrib>Davis, Jazmyne E.</creatorcontrib><creatorcontrib>Floyd, Alexandria N.</creatorcontrib><creatorcontrib>Hogan, Simon P.</creatorcontrib><creatorcontrib>Hsieh, Chyi-Song</creatorcontrib><creatorcontrib>Newberry, Rodney D.</creatorcontrib><title>Goblet cell associated antigen passages support the induction and maintenance of oral tolerance</title><title>Mucosal immunology</title><addtitle>Mucosal Immunol</addtitle><addtitle>MUCOSAL IMMUNOL</addtitle><addtitle>Mucosal Immunol</addtitle><description>Tolerance to innocuous antigens from the diet and the commensal microbiota is a fundamental process essential to health. Why tolerance is efficiently induced to substances arising from the hostile environment of the gut lumen is incompletely understood but may be related to how these antigens are encountered by the immune system. We observed that goblet cell associated antigen passages (GAPs), but not other pathways of luminal antigen capture, correlated with the acquisition of luminal substances by lamina propria (LP) antigen presenting cells (APCs) and with the sites of tolerance induction to luminal antigens. Strikingly this role extended beyond antigen delivery. The GAP function of goblet cells facilitated maintenance of pre-existing LP T regulatory cells (Tregs), imprinting LP-dendritic cells with tolerogenic properties, and facilitating LP macrophages to produce the immunomodulatory cytokine IL-10. Moreover, tolerance to dietary antigen was impaired in the absence of GAPs. Thus, by delivering luminal antigens, maintaining pre-existing LP Tregs, and imprinting tolerogenic properties on LP-APCs GAPs support tolerance to substances encountered in the hostile environment of the gut lumen.</description><subject>Administration, Oral</subject><subject>Allergology</subject><subject>Animals</subject><subject>Antibodies</subject><subject>Antigen Presentation</subject><subject>Antigen-presenting cells</subject><subject>Antigen-Presenting Cells - immunology</subject><subject>Antigens</subject><subject>Antigens - immunology</subject><subject>Biomedical and Life Sciences</subject><subject>Biomedicine</subject><subject>Cells, Cultured</subject><subject>Dendritic cells</subject><subject>Dendritic Cells - immunology</subject><subject>Gastroenterology</subject><subject>Goblet cells</subject><subject>Goblet Cells - immunology</subject><subject>GTPase-Activating Proteins - metabolism</subject><subject>Immune system</subject><subject>Immune Tolerance</subject><subject>Immunological tolerance</subject><subject>Immunology</subject><subject>Immunomodulation</subject><subject>Immunoregulation</subject><subject>Interleukin 10</subject><subject>Interleukin-10 - metabolism</subject><subject>Lamina propria</subject><subject>Life Sciences & Biomedicine</subject><subject>Lymphocytes T</subject><subject>Macrophages</subject><subject>Macrophages - immunology</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Mice, Transgenic</subject><subject>Microbiota</subject><subject>Mucous Membrane - immunology</subject><subject>Science & Technology</subject><subject>T-Lymphocytes, Regulatory - immunology</subject><issn>1933-0219</issn><issn>1935-3456</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>AOWDO</sourceid><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNqNkk-LFDEQxYMo7rr6AbxIwKO0VpLOn74IMugqLHjRc0gn1bNZepK2k1b89macddWLeEpR9avi8fIIecrgJQNhXpWeCSM7YEMHvIdO3yPnbBCyE71U93_Wok3YcEYelXIDoACkeEjOBDNsYJqfE3uZxxkr9TjP1JWSfXQVA3Wpxj0murSe22OhZVuWvFZar5HGFDZfY04NC_TgYqqYXPJI80Tz6mZa84zrsfOYPJjcXPDJ7XtBPr97-2n3vrv6ePlh9-aqW7jitVOjDKPWPjjJEIN0yERgGr2Ryo9sGg0XEmEScggMVA_KSa2cgDCwYeRaXJDXp7vLNh4weEy16bDLGg9u_W6zi_bvSYrXdp-_Wg19DxLagee3B9b8ZcNS7U3e1tQ0W95rCZJJLv5JCcV589eYRj37U8ydil-2N8CcgG845qn4iM2qOwzaFWbaFw6tArOL1R3N3uUt1bb64v9XG81PdGlE2uP6Wy8DewyRPYXIthDZY4isFj8A6be2aw</recordid><startdate>20200301</startdate><enddate>20200301</enddate><creator>Kulkarni, Devesha H.</creator><creator>Gustafsson, Jenny K.</creator><creator>Knoop, Kathryn A.</creator><creator>McDonald, Keely G.</creator><creator>Bidani, Shay S.</creator><creator>Davis, Jazmyne E.</creator><creator>Floyd, Alexandria N.</creator><creator>Hogan, Simon P.</creator><creator>Hsieh, Chyi-Song</creator><creator>Newberry, Rodney D.</creator><general>Nature Publishing Group US</general><general>Springer Nature</general><general>Elsevier Limited</general><scope>AOWDO</scope><scope>BLEPL</scope><scope>DTL</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>3V.</scope><scope>7T5</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</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>M7P</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-2007-3066</orcidid></search><sort><creationdate>20200301</creationdate><title>Goblet cell associated antigen passages support the induction and maintenance of oral tolerance</title><author>Kulkarni, Devesha H. ; Gustafsson, Jenny K. ; Knoop, Kathryn A. ; McDonald, Keely G. ; Bidani, Shay S. ; Davis, Jazmyne E. ; Floyd, Alexandria N. ; Hogan, Simon P. ; Hsieh, Chyi-Song ; Newberry, Rodney D.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-p262t-6b5db77cda51eed5ae13d17ec856cb1fb8235e0f359d106406a576a30d919b273</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Administration, Oral</topic><topic>Allergology</topic><topic>Animals</topic><topic>Antibodies</topic><topic>Antigen Presentation</topic><topic>Antigen-presenting cells</topic><topic>Antigen-Presenting Cells - immunology</topic><topic>Antigens</topic><topic>Antigens - immunology</topic><topic>Biomedical and Life Sciences</topic><topic>Biomedicine</topic><topic>Cells, Cultured</topic><topic>Dendritic cells</topic><topic>Dendritic Cells - immunology</topic><topic>Gastroenterology</topic><topic>Goblet cells</topic><topic>Goblet Cells - immunology</topic><topic>GTPase-Activating Proteins - metabolism</topic><topic>Immune system</topic><topic>Immune Tolerance</topic><topic>Immunological tolerance</topic><topic>Immunology</topic><topic>Immunomodulation</topic><topic>Immunoregulation</topic><topic>Interleukin 10</topic><topic>Interleukin-10 - metabolism</topic><topic>Lamina propria</topic><topic>Life Sciences & Biomedicine</topic><topic>Lymphocytes T</topic><topic>Macrophages</topic><topic>Macrophages - immunology</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>Mice, Transgenic</topic><topic>Microbiota</topic><topic>Mucous Membrane - immunology</topic><topic>Science & Technology</topic><topic>T-Lymphocytes, Regulatory - immunology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kulkarni, Devesha H.</creatorcontrib><creatorcontrib>Gustafsson, Jenny K.</creatorcontrib><creatorcontrib>Knoop, Kathryn A.</creatorcontrib><creatorcontrib>McDonald, Keely G.</creatorcontrib><creatorcontrib>Bidani, Shay S.</creatorcontrib><creatorcontrib>Davis, Jazmyne E.</creatorcontrib><creatorcontrib>Floyd, Alexandria N.</creatorcontrib><creatorcontrib>Hogan, Simon P.</creatorcontrib><creatorcontrib>Hsieh, Chyi-Song</creatorcontrib><creatorcontrib>Newberry, Rodney D.</creatorcontrib><collection>Web of Science - Science Citation Index Expanded - 2020</collection><collection>Web of Science Core Collection</collection><collection>Science Citation Index Expanded</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>ProQuest Central (Corporate)</collection><collection>Immunology Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Biological Science Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Mucosal immunology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kulkarni, Devesha H.</au><au>Gustafsson, Jenny K.</au><au>Knoop, Kathryn A.</au><au>McDonald, Keely G.</au><au>Bidani, Shay S.</au><au>Davis, Jazmyne E.</au><au>Floyd, Alexandria N.</au><au>Hogan, Simon P.</au><au>Hsieh, Chyi-Song</au><au>Newberry, Rodney D.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Goblet cell associated antigen passages support the induction and maintenance of oral tolerance</atitle><jtitle>Mucosal immunology</jtitle><stitle>Mucosal Immunol</stitle><stitle>MUCOSAL IMMUNOL</stitle><addtitle>Mucosal Immunol</addtitle><date>2020-03-01</date><risdate>2020</risdate><volume>13</volume><issue>2</issue><spage>271</spage><epage>282</epage><pages>271-282</pages><issn>1933-0219</issn><eissn>1935-3456</eissn><abstract>Tolerance to innocuous antigens from the diet and the commensal microbiota is a fundamental process essential to health. Why tolerance is efficiently induced to substances arising from the hostile environment of the gut lumen is incompletely understood but may be related to how these antigens are encountered by the immune system. We observed that goblet cell associated antigen passages (GAPs), but not other pathways of luminal antigen capture, correlated with the acquisition of luminal substances by lamina propria (LP) antigen presenting cells (APCs) and with the sites of tolerance induction to luminal antigens. Strikingly this role extended beyond antigen delivery. The GAP function of goblet cells facilitated maintenance of pre-existing LP T regulatory cells (Tregs), imprinting LP-dendritic cells with tolerogenic properties, and facilitating LP macrophages to produce the immunomodulatory cytokine IL-10. Moreover, tolerance to dietary antigen was impaired in the absence of GAPs. Thus, by delivering luminal antigens, maintaining pre-existing LP Tregs, and imprinting tolerogenic properties on LP-APCs GAPs support tolerance to substances encountered in the hostile environment of the gut lumen.</abstract><cop>New York</cop><pub>Nature Publishing Group US</pub><pmid>31819172</pmid><doi>10.1038/s41385-019-0240-7</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0003-2007-3066</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Administration, Oral Allergology Animals Antibodies Antigen Presentation Antigen-presenting cells Antigen-Presenting Cells - immunology Antigens Antigens - immunology Biomedical and Life Sciences Biomedicine Cells, Cultured Dendritic cells Dendritic Cells - immunology Gastroenterology Goblet cells Goblet Cells - immunology GTPase-Activating Proteins - metabolism Immune system Immune Tolerance Immunological tolerance Immunology Immunomodulation Immunoregulation Interleukin 10 Interleukin-10 - metabolism Lamina propria Life Sciences & Biomedicine Lymphocytes T Macrophages Macrophages - immunology Mice Mice, Inbred C57BL Mice, Transgenic Microbiota Mucous Membrane - immunology Science & Technology T-Lymphocytes, Regulatory - immunology |
| title | Goblet cell associated antigen passages support the induction and maintenance of oral tolerance |
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