An integrin αEβ7-dependent mechanism of IgA transcytosis requires direct plasma cell contact with intestinal epithelium
Efficient IgA transcytosis is critical for the maintenance of a homeostatic microbiota. In the canonical model, locally-secreted dimeric (d)IgA reaches the polymeric immunoglobulin receptor (pIgR) on intestinal epithelium via simple diffusion. A role for integrin αE(CD103)β7 during transcytosis has...
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| Veröffentlicht in: | Mucosal immunology 2021-11, Vol.14 (6), p.1347-1357 |
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| creator | Guzman, Mauricio Lundborg, Luke R. Yeasmin, Shaila Tyler, Christopher J. Zgajnar, Nadia R. Taupin, Vanessa Dobaczewska, Katarzyna Mikulski, Zbigniew Bamias, Giorgos Rivera-Nieves, Jesús |
| description | Efficient IgA transcytosis is critical for the maintenance of a homeostatic microbiota. In the canonical model, locally-secreted dimeric (d)IgA reaches the polymeric immunoglobulin receptor (pIgR) on intestinal epithelium via simple diffusion. A role for integrin αE(CD103)β7 during transcytosis has not been described, nor its expression by intestinal B cell lineage cells. We found that αE-deficient (αE
−/−
) mice have a luminal IgA deficit, despite normal antibody-secreting cells (ASC) recruitment, local IgA production and increased pIgR expression. This deficit was not due to dendritic cell (DC)-derived retinoic acid (RA) nor class-switching defects, as stool from RAG
−/−
mice reconstituted with αE
−/−
B cells was also IgA deficient. Flow cytometric, ultrastructural and transcriptional profiling showed that αEβ7-expressing ASC represent an undescribed subset of terminally-differentiated intestinal plasma cells (PC) that establishes direct cell to cell contact with intestinal epithelium. We propose that IgA not only reaches pIgR through diffusion, but that αEβ7+ PC dock with E-cadherin-expressing intestinal epithelium to directly relay IgA for transcytosis into the intestinal lumen. |
| doi_str_mv | 10.1038/s41385-021-00439-x |
| format | Article |
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−/−
) mice have a luminal IgA deficit, despite normal antibody-secreting cells (ASC) recruitment, local IgA production and increased pIgR expression. This deficit was not due to dendritic cell (DC)-derived retinoic acid (RA) nor class-switching defects, as stool from RAG
−/−
mice reconstituted with αE
−/−
B cells was also IgA deficient. Flow cytometric, ultrastructural and transcriptional profiling showed that αEβ7-expressing ASC represent an undescribed subset of terminally-differentiated intestinal plasma cells (PC) that establishes direct cell to cell contact with intestinal epithelium. We propose that IgA not only reaches pIgR through diffusion, but that αEβ7+ PC dock with E-cadherin-expressing intestinal epithelium to directly relay IgA for transcytosis into the intestinal lumen.</description><identifier>ISSN: 1933-0219</identifier><identifier>EISSN: 1935-3456</identifier><identifier>DOI: 10.1038/s41385-021-00439-x</identifier><identifier>PMID: 34417548</identifier><language>eng</language><publisher>New York: Nature Publishing Group US</publisher><subject>Allergology ; Animals ; Antibodies ; Biomedical and Life Sciences ; Biomedicine ; CD103 antigen ; Cell adhesion & migration ; Cell differentiation ; Cell Differentiation - immunology ; Cell lineage ; Dendritic cells ; E-cadherin ; Epithelium ; Feces ; Flow cytometry ; Gastroenterology ; Gene Expression ; Gene Expression Regulation ; Immunoglobulin A ; Immunoglobulin A - immunology ; Immunoglobulin A - metabolism ; Immunoglobulin A, Secretory - immunology ; Immunoglobulins ; Immunology ; Integrins - deficiency ; Integrins - genetics ; Integrins - metabolism ; Intestinal Mucosa - immunology ; Intestinal Mucosa - metabolism ; Intestinal Mucosa - ultrastructure ; Intestine ; Lymphocyte Activation ; Lymphocytes ; Lymphocytes B ; Mice ; Mice, Knockout ; Microbiota ; Models, Biological ; Plasma ; Plasma cells ; Plasma Cells - cytology ; Plasma Cells - immunology ; Plasma Cells - metabolism ; Plasma Cells - ultrastructure ; Retinoic acid ; Transcription ; Transcytosis - immunology</subject><ispartof>Mucosal immunology, 2021-11, Vol.14 (6), p.1347-1357</ispartof><rights>This is a U.S. government work and not under copyright protection in the U.S.; foreign copyright protection may apply 2021</rights><rights>2021. This is a U.S. government work and not under copyright protection in the U.S.; foreign copyright protection may apply.</rights><rights>This is a U.S. government work and not under copyright protection in the U.S.; foreign copyright protection may apply 2021. This work is published under http://creativecommons.org/licenses/by/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-c389x-39de988ff728b3c10673da322eb92c9cd3f94497b49e2de3b8a880ba0e6e506f3</citedby><cites>FETCH-LOGICAL-c389x-39de988ff728b3c10673da322eb92c9cd3f94497b49e2de3b8a880ba0e6e506f3</cites><orcidid>0000-0002-7887-7959</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.proquest.com/docview/2583709179?pq-origsite=primo$$EHTML$$P50$$Gproquest$$H</linktohtml><link.rule.ids>230,314,780,784,885,27922,27923,64383,64385,64387,72239</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34417548$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Guzman, Mauricio</creatorcontrib><creatorcontrib>Lundborg, Luke R.</creatorcontrib><creatorcontrib>Yeasmin, Shaila</creatorcontrib><creatorcontrib>Tyler, Christopher J.</creatorcontrib><creatorcontrib>Zgajnar, Nadia R.</creatorcontrib><creatorcontrib>Taupin, Vanessa</creatorcontrib><creatorcontrib>Dobaczewska, Katarzyna</creatorcontrib><creatorcontrib>Mikulski, Zbigniew</creatorcontrib><creatorcontrib>Bamias, Giorgos</creatorcontrib><creatorcontrib>Rivera-Nieves, Jesús</creatorcontrib><title>An integrin αEβ7-dependent mechanism of IgA transcytosis requires direct plasma cell contact with intestinal epithelium</title><title>Mucosal immunology</title><addtitle>Mucosal Immunol</addtitle><addtitle>Mucosal Immunol</addtitle><description>Efficient IgA transcytosis is critical for the maintenance of a homeostatic microbiota. In the canonical model, locally-secreted dimeric (d)IgA reaches the polymeric immunoglobulin receptor (pIgR) on intestinal epithelium via simple diffusion. A role for integrin αE(CD103)β7 during transcytosis has not been described, nor its expression by intestinal B cell lineage cells. We found that αE-deficient (αE
−/−
) mice have a luminal IgA deficit, despite normal antibody-secreting cells (ASC) recruitment, local IgA production and increased pIgR expression. This deficit was not due to dendritic cell (DC)-derived retinoic acid (RA) nor class-switching defects, as stool from RAG
−/−
mice reconstituted with αE
−/−
B cells was also IgA deficient. Flow cytometric, ultrastructural and transcriptional profiling showed that αEβ7-expressing ASC represent an undescribed subset of terminally-differentiated intestinal plasma cells (PC) that establishes direct cell to cell contact with intestinal epithelium. We propose that IgA not only reaches pIgR through diffusion, but that αEβ7+ PC dock with E-cadherin-expressing intestinal epithelium to directly relay IgA for transcytosis into the intestinal lumen.</description><subject>Allergology</subject><subject>Animals</subject><subject>Antibodies</subject><subject>Biomedical and Life Sciences</subject><subject>Biomedicine</subject><subject>CD103 antigen</subject><subject>Cell adhesion & migration</subject><subject>Cell differentiation</subject><subject>Cell Differentiation - immunology</subject><subject>Cell lineage</subject><subject>Dendritic cells</subject><subject>E-cadherin</subject><subject>Epithelium</subject><subject>Feces</subject><subject>Flow cytometry</subject><subject>Gastroenterology</subject><subject>Gene Expression</subject><subject>Gene Expression Regulation</subject><subject>Immunoglobulin A</subject><subject>Immunoglobulin A - immunology</subject><subject>Immunoglobulin A - metabolism</subject><subject>Immunoglobulin A, Secretory - immunology</subject><subject>Immunoglobulins</subject><subject>Immunology</subject><subject>Integrins - deficiency</subject><subject>Integrins - genetics</subject><subject>Integrins - metabolism</subject><subject>Intestinal Mucosa - immunology</subject><subject>Intestinal Mucosa - metabolism</subject><subject>Intestinal Mucosa - ultrastructure</subject><subject>Intestine</subject><subject>Lymphocyte Activation</subject><subject>Lymphocytes</subject><subject>Lymphocytes B</subject><subject>Mice</subject><subject>Mice, Knockout</subject><subject>Microbiota</subject><subject>Models, Biological</subject><subject>Plasma</subject><subject>Plasma cells</subject><subject>Plasma Cells - cytology</subject><subject>Plasma Cells - immunology</subject><subject>Plasma Cells - metabolism</subject><subject>Plasma Cells - ultrastructure</subject><subject>Retinoic acid</subject><subject>Transcription</subject><subject>Transcytosis - immunology</subject><issn>1933-0219</issn><issn>1935-3456</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>C6C</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>eNp9kc1u1DAUhS0EoqXwAiyQJTZsAravk9gbpFFVoFIlNrC2HOdmxlXipHZCZx4LHqTPhGemlJ8FG9u69_O5Pj6EvOTsLWeg3iXJQZUFE7xgTIIuto_IKddQFiDL6vHhDPu2PiHPUrpmrGKshKfkBKTkdSnVKdmtAvVhxnX0gd59v7j7URctThhaDDMd0G1s8GmgY0cv1ys6RxuS281j8olGvFl8xETbvLqZTr1Ng6UO-566Mcw21279vDkMSLMPtqc45QL2fhmekyed7RO-uN_PyNcPF1_OPxVXnz9enq-uCgdKbwvQLWqluq4WqgHHWVVDa0EIbLRw2rXQaSl13UiNokVolFWKNZZhhSWrOjgj74-609IM2LrsK9reTNEPNu7MaL35uxP8xqzHb0aVQtVcZoE39wJxvFmyETP4tDdpA45LMqKsQAqe_zSjr_9Br8clZt97SkHNNK91psSRcnFMKWL38BjOzD5Zc0zW5OjMIVmzzZde_Wnj4cqvKDMARyDlVlhj_D37P7I_AW4Ws9o</recordid><startdate>20211101</startdate><enddate>20211101</enddate><creator>Guzman, Mauricio</creator><creator>Lundborg, Luke R.</creator><creator>Yeasmin, Shaila</creator><creator>Tyler, Christopher J.</creator><creator>Zgajnar, Nadia R.</creator><creator>Taupin, Vanessa</creator><creator>Dobaczewska, Katarzyna</creator><creator>Mikulski, Zbigniew</creator><creator>Bamias, Giorgos</creator><creator>Rivera-Nieves, Jesús</creator><general>Nature Publishing Group US</general><general>Elsevier Limited</general><scope>C6C</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>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>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-7887-7959</orcidid></search><sort><creationdate>20211101</creationdate><title>An integrin αEβ7-dependent mechanism of IgA transcytosis requires direct plasma cell contact with intestinal epithelium</title><author>Guzman, Mauricio ; Lundborg, Luke R. ; Yeasmin, Shaila ; Tyler, Christopher J. ; Zgajnar, Nadia R. ; Taupin, Vanessa ; Dobaczewska, Katarzyna ; Mikulski, Zbigniew ; Bamias, Giorgos ; Rivera-Nieves, Jesús</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c389x-39de988ff728b3c10673da322eb92c9cd3f94497b49e2de3b8a880ba0e6e506f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Allergology</topic><topic>Animals</topic><topic>Antibodies</topic><topic>Biomedical and Life Sciences</topic><topic>Biomedicine</topic><topic>CD103 antigen</topic><topic>Cell adhesion & migration</topic><topic>Cell differentiation</topic><topic>Cell Differentiation - immunology</topic><topic>Cell lineage</topic><topic>Dendritic cells</topic><topic>E-cadherin</topic><topic>Epithelium</topic><topic>Feces</topic><topic>Flow cytometry</topic><topic>Gastroenterology</topic><topic>Gene Expression</topic><topic>Gene Expression Regulation</topic><topic>Immunoglobulin A</topic><topic>Immunoglobulin A - immunology</topic><topic>Immunoglobulin A - metabolism</topic><topic>Immunoglobulin A, Secretory - immunology</topic><topic>Immunoglobulins</topic><topic>Immunology</topic><topic>Integrins - deficiency</topic><topic>Integrins - genetics</topic><topic>Integrins - metabolism</topic><topic>Intestinal Mucosa - immunology</topic><topic>Intestinal Mucosa - metabolism</topic><topic>Intestinal Mucosa - ultrastructure</topic><topic>Intestine</topic><topic>Lymphocyte Activation</topic><topic>Lymphocytes</topic><topic>Lymphocytes B</topic><topic>Mice</topic><topic>Mice, Knockout</topic><topic>Microbiota</topic><topic>Models, Biological</topic><topic>Plasma</topic><topic>Plasma cells</topic><topic>Plasma Cells - cytology</topic><topic>Plasma Cells - immunology</topic><topic>Plasma Cells - metabolism</topic><topic>Plasma Cells - ultrastructure</topic><topic>Retinoic acid</topic><topic>Transcription</topic><topic>Transcytosis - immunology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Guzman, Mauricio</creatorcontrib><creatorcontrib>Lundborg, Luke R.</creatorcontrib><creatorcontrib>Yeasmin, Shaila</creatorcontrib><creatorcontrib>Tyler, Christopher J.</creatorcontrib><creatorcontrib>Zgajnar, Nadia R.</creatorcontrib><creatorcontrib>Taupin, Vanessa</creatorcontrib><creatorcontrib>Dobaczewska, Katarzyna</creatorcontrib><creatorcontrib>Mikulski, Zbigniew</creatorcontrib><creatorcontrib>Bamias, Giorgos</creatorcontrib><creatorcontrib>Rivera-Nieves, Jesús</creatorcontrib><collection>Springer Nature OA Free Journals</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</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>MEDLINE - Academic</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>Guzman, Mauricio</au><au>Lundborg, Luke R.</au><au>Yeasmin, Shaila</au><au>Tyler, Christopher J.</au><au>Zgajnar, Nadia R.</au><au>Taupin, Vanessa</au><au>Dobaczewska, Katarzyna</au><au>Mikulski, Zbigniew</au><au>Bamias, Giorgos</au><au>Rivera-Nieves, Jesús</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>An integrin αEβ7-dependent mechanism of IgA transcytosis requires direct plasma cell contact with intestinal epithelium</atitle><jtitle>Mucosal immunology</jtitle><stitle>Mucosal Immunol</stitle><addtitle>Mucosal Immunol</addtitle><date>2021-11-01</date><risdate>2021</risdate><volume>14</volume><issue>6</issue><spage>1347</spage><epage>1357</epage><pages>1347-1357</pages><issn>1933-0219</issn><eissn>1935-3456</eissn><abstract>Efficient IgA transcytosis is critical for the maintenance of a homeostatic microbiota. In the canonical model, locally-secreted dimeric (d)IgA reaches the polymeric immunoglobulin receptor (pIgR) on intestinal epithelium via simple diffusion. A role for integrin αE(CD103)β7 during transcytosis has not been described, nor its expression by intestinal B cell lineage cells. We found that αE-deficient (αE
−/−
) mice have a luminal IgA deficit, despite normal antibody-secreting cells (ASC) recruitment, local IgA production and increased pIgR expression. This deficit was not due to dendritic cell (DC)-derived retinoic acid (RA) nor class-switching defects, as stool from RAG
−/−
mice reconstituted with αE
−/−
B cells was also IgA deficient. Flow cytometric, ultrastructural and transcriptional profiling showed that αEβ7-expressing ASC represent an undescribed subset of terminally-differentiated intestinal plasma cells (PC) that establishes direct cell to cell contact with intestinal epithelium. We propose that IgA not only reaches pIgR through diffusion, but that αEβ7+ PC dock with E-cadherin-expressing intestinal epithelium to directly relay IgA for transcytosis into the intestinal lumen.</abstract><cop>New York</cop><pub>Nature Publishing Group US</pub><pmid>34417548</pmid><doi>10.1038/s41385-021-00439-x</doi><tpages>11</tpages><orcidid>https://orcid.org/0000-0002-7887-7959</orcidid><oa>free_for_read</oa></addata></record> |
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| ispartof | Mucosal immunology, 2021-11, Vol.14 (6), p.1347-1357 |
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| language | eng |
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| source | MEDLINE; EZB-FREE-00999 freely available EZB journals; ProQuest Central UK/Ireland; Alma/SFX Local Collection |
| subjects | Allergology Animals Antibodies Biomedical and Life Sciences Biomedicine CD103 antigen Cell adhesion & migration Cell differentiation Cell Differentiation - immunology Cell lineage Dendritic cells E-cadherin Epithelium Feces Flow cytometry Gastroenterology Gene Expression Gene Expression Regulation Immunoglobulin A Immunoglobulin A - immunology Immunoglobulin A - metabolism Immunoglobulin A, Secretory - immunology Immunoglobulins Immunology Integrins - deficiency Integrins - genetics Integrins - metabolism Intestinal Mucosa - immunology Intestinal Mucosa - metabolism Intestinal Mucosa - ultrastructure Intestine Lymphocyte Activation Lymphocytes Lymphocytes B Mice Mice, Knockout Microbiota Models, Biological Plasma Plasma cells Plasma Cells - cytology Plasma Cells - immunology Plasma Cells - metabolism Plasma Cells - ultrastructure Retinoic acid Transcription Transcytosis - immunology |
| title | An integrin αEβ7-dependent mechanism of IgA transcytosis requires direct plasma cell contact with intestinal epithelium |
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