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Fetal exposure to intact immunoglobulin E occurs via the gastrointestinal tract

Summary Background Consideration of the evolutionary significance of IgE might provide insight into the immunological interactions occurring in utero and during early post‐natal life that regulate later atopic disease. Objective We postulated that the fetal gut is exposed to intact amniotic fluid Ig...

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Published in:Clinical and experimental allergy 2003-03, Vol.33 (3), p.306-311
Main Authors: Thornton, C. A., Holloway, J. A., Popplewell, E. J., Shute, J. K., Boughton, J., Warner, J. O.
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container_title Clinical and experimental allergy
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creator Thornton, C. A.
Holloway, J. A.
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Warner, J. O.
description Summary Background Consideration of the evolutionary significance of IgE might provide insight into the immunological interactions occurring in utero and during early post‐natal life that regulate later atopic disease. Objective We postulated that the fetal gut is exposed to intact amniotic fluid IgE that might interact with local IgE receptors. Methods IgE levels in matched maternal blood and amniotic fluid (n = 47) or breast milk (n = 15) collected from pregnant women in the UK (Southampton) and Brazil (Sao Paulo) were studied. Expression of IgE receptors, FcɛRI and FcɛRII (CD23), in fetal gastrointestinal tract (n = 19) and skin (n = 11) was examined immunohistochemically. Results Human amniotic fluid at 16–18 weeks' gestation contained intact IgE at levels that increased as maternal circulating levels increased (Spearman's ρ = 0.897; P  37 weeks' gestation) amniotic fluid (ρ = 0.993; P 
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A. ; Holloway, J. A. ; Popplewell, E. J. ; Shute, J. K. ; Boughton, J. ; Warner, J. O.</creator><creatorcontrib>Thornton, C. A. ; Holloway, J. A. ; Popplewell, E. J. ; Shute, J. K. ; Boughton, J. ; Warner, J. O.</creatorcontrib><description>Summary Background Consideration of the evolutionary significance of IgE might provide insight into the immunological interactions occurring in utero and during early post‐natal life that regulate later atopic disease. Objective We postulated that the fetal gut is exposed to intact amniotic fluid IgE that might interact with local IgE receptors. Methods IgE levels in matched maternal blood and amniotic fluid (n = 47) or breast milk (n = 15) collected from pregnant women in the UK (Southampton) and Brazil (Sao Paulo) were studied. Expression of IgE receptors, FcɛRI and FcɛRII (CD23), in fetal gastrointestinal tract (n = 19) and skin (n = 11) was examined immunohistochemically. Results Human amniotic fluid at 16–18 weeks' gestation contained intact IgE at levels that increased as maternal circulating levels increased (Spearman's ρ = 0.897; P &lt; 0.001). Circulating IgE levels from women in Sao Paulo, Brazil, associated positively not only with term (&gt; 37 weeks' gestation) amniotic fluid (ρ = 0.993; P &lt; 0.001) but also breast milk IgE levels (ρ = 0.785; P = 0.001). Maternal levels of IgE did not change significantly over pregnancy and fetal circulating levels of IgE were very low (&lt; 0.6 IU/mL). Low‐affinity IgE receptors (CD23) were expressed in lymphoid follicles of the fetal gut from 16 weeks of gestation (6/8), but not from 11 to 16 weeks (0/11) or in the skin. Conclusion Amniotic fluid contains intact IgE that might bind to CD23+ cells within the lymphoid follicles of the fetal gastrointestinal tract. The evolutionary significance of these interactions might be to prepare the immune system for helminthic parasite exposure at birth via IgE‐mediated antigen focusing, or ‘education’ of the developing immune system about the prevailing extrauterine environment. However, at present in societies where helminthosis is not a significant health issue, this pathway may still be operational and associated with the development of atopic disease.</description><identifier>ISSN: 0954-7894</identifier><identifier>EISSN: 1365-2222</identifier><identifier>DOI: 10.1046/j.1365-2222.2003.01614.x</identifier><identifier>PMID: 12614443</identifier><language>eng</language><publisher>Oxford, UK: Blackwell Science Ltd</publisher><subject>Allergic diseases ; amniotic fluid ; Amniotic Fluid - immunology ; Biological and medical sciences ; breast milk ; CD23 ; Enzyme-Linked Immunosorbent Assay ; Female ; Fetal Blood - immunology ; fetal gut ; Fetus - immunology ; General aspects ; Gestational Age ; Humans ; Hypersensitivity - etiology ; IgE ; Immunoglobulin E - blood ; Immunopathology ; in utero ; Intestines - immunology ; Medical sciences ; Milk, Human - immunology ; Pregnancy ; Receptors, IgE - analysis ; Skin - immunology ; Statistics, Nonparametric</subject><ispartof>Clinical and experimental allergy, 2003-03, Vol.33 (3), p.306-311</ispartof><rights>2003 INIST-CNRS</rights><rights>Copyright Blackwell Scientific Publications Ltd. Mar 2003</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5414-d650d24ee5e35244a560d9657a5abaf8eaf26d40073af8a781bbb87bb19122d03</citedby><cites>FETCH-LOGICAL-c5414-d650d24ee5e35244a560d9657a5abaf8eaf26d40073af8a781bbb87bb19122d03</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,776,780,27901,27902</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&amp;idt=14599057$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/12614443$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Thornton, C. A.</creatorcontrib><creatorcontrib>Holloway, J. A.</creatorcontrib><creatorcontrib>Popplewell, E. J.</creatorcontrib><creatorcontrib>Shute, J. K.</creatorcontrib><creatorcontrib>Boughton, J.</creatorcontrib><creatorcontrib>Warner, J. O.</creatorcontrib><title>Fetal exposure to intact immunoglobulin E occurs via the gastrointestinal tract</title><title>Clinical and experimental allergy</title><addtitle>Clin Exp Allergy</addtitle><description>Summary Background Consideration of the evolutionary significance of IgE might provide insight into the immunological interactions occurring in utero and during early post‐natal life that regulate later atopic disease. Objective We postulated that the fetal gut is exposed to intact amniotic fluid IgE that might interact with local IgE receptors. Methods IgE levels in matched maternal blood and amniotic fluid (n = 47) or breast milk (n = 15) collected from pregnant women in the UK (Southampton) and Brazil (Sao Paulo) were studied. Expression of IgE receptors, FcɛRI and FcɛRII (CD23), in fetal gastrointestinal tract (n = 19) and skin (n = 11) was examined immunohistochemically. Results Human amniotic fluid at 16–18 weeks' gestation contained intact IgE at levels that increased as maternal circulating levels increased (Spearman's ρ = 0.897; P &lt; 0.001). Circulating IgE levels from women in Sao Paulo, Brazil, associated positively not only with term (&gt; 37 weeks' gestation) amniotic fluid (ρ = 0.993; P &lt; 0.001) but also breast milk IgE levels (ρ = 0.785; P = 0.001). Maternal levels of IgE did not change significantly over pregnancy and fetal circulating levels of IgE were very low (&lt; 0.6 IU/mL). Low‐affinity IgE receptors (CD23) were expressed in lymphoid follicles of the fetal gut from 16 weeks of gestation (6/8), but not from 11 to 16 weeks (0/11) or in the skin. Conclusion Amniotic fluid contains intact IgE that might bind to CD23+ cells within the lymphoid follicles of the fetal gastrointestinal tract. The evolutionary significance of these interactions might be to prepare the immune system for helminthic parasite exposure at birth via IgE‐mediated antigen focusing, or ‘education’ of the developing immune system about the prevailing extrauterine environment. However, at present in societies where helminthosis is not a significant health issue, this pathway may still be operational and associated with the development of atopic disease.</description><subject>Allergic diseases</subject><subject>amniotic fluid</subject><subject>Amniotic Fluid - immunology</subject><subject>Biological and medical sciences</subject><subject>breast milk</subject><subject>CD23</subject><subject>Enzyme-Linked Immunosorbent Assay</subject><subject>Female</subject><subject>Fetal Blood - immunology</subject><subject>fetal gut</subject><subject>Fetus - immunology</subject><subject>General aspects</subject><subject>Gestational Age</subject><subject>Humans</subject><subject>Hypersensitivity - etiology</subject><subject>IgE</subject><subject>Immunoglobulin E - blood</subject><subject>Immunopathology</subject><subject>in utero</subject><subject>Intestines - immunology</subject><subject>Medical sciences</subject><subject>Milk, Human - immunology</subject><subject>Pregnancy</subject><subject>Receptors, IgE - analysis</subject><subject>Skin - immunology</subject><subject>Statistics, Nonparametric</subject><issn>0954-7894</issn><issn>1365-2222</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2003</creationdate><recordtype>article</recordtype><recordid>eNqN0c1u1DAUBWALUdGh5RWQhQS7pP53vGBRRtMWVLVILUJiYzmJUzwk8WA7MH17HGbUSt1ANk7k71zd6AAAMSoxYuJkXWIqeEHyUxKEaImwwKzcPgOLh4vnYIEUZ4WsFDsEL2Ncoyy5ql6AQ0wyZ4wuwPWZTaaHdrvxcQoWJg_dmEyToBuGafR3va-n3o1wBX3TTCHCX87A9N3COxNT8BnbmNyYZ6SQY8fgoDN9tK_25xH4cra6XV4Ul9fnH5enl0XDGWZFKzhqCbOWW8oJY4YL1CrBpeGmNl1lTUdEyxCSNH8ZWeG6ritZ11hhQlpEj8C73dxN8D-nvIIeXGxs35vR-ilqSZGUGJF_QlxlxiqR4ZsncO2nkH8sG6UUQgqxjKodaoKPMdhOb4IbTLjXGOm5Gr3WcwN6bkDP1ei_1ehtjr7ez5_qwbaPwX0XGbzdAxMb03fBjI2Lj47xvAWX2b3fud-ut_f_vYBerk7nt5wvdnkXk90-5E34oYWkkuuvV-f69hvlnz5c3OjP9A_RurgQ</recordid><startdate>200303</startdate><enddate>200303</enddate><creator>Thornton, C. A.</creator><creator>Holloway, J. A.</creator><creator>Popplewell, E. J.</creator><creator>Shute, J. K.</creator><creator>Boughton, J.</creator><creator>Warner, J. O.</creator><general>Blackwell Science Ltd</general><general>Blackwell</general><general>Wiley Subscription Services, Inc</general><scope>BSCLL</scope><scope>IQODW</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>7T5</scope><scope>H94</scope><scope>K9.</scope><scope>7X8</scope></search><sort><creationdate>200303</creationdate><title>Fetal exposure to intact immunoglobulin E occurs via the gastrointestinal tract</title><author>Thornton, C. A. ; Holloway, J. A. ; Popplewell, E. J. ; Shute, J. K. ; Boughton, J. ; Warner, J. O.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5414-d650d24ee5e35244a560d9657a5abaf8eaf26d40073af8a781bbb87bb19122d03</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2003</creationdate><topic>Allergic diseases</topic><topic>amniotic fluid</topic><topic>Amniotic Fluid - immunology</topic><topic>Biological and medical sciences</topic><topic>breast milk</topic><topic>CD23</topic><topic>Enzyme-Linked Immunosorbent Assay</topic><topic>Female</topic><topic>Fetal Blood - immunology</topic><topic>fetal gut</topic><topic>Fetus - immunology</topic><topic>General aspects</topic><topic>Gestational Age</topic><topic>Humans</topic><topic>Hypersensitivity - etiology</topic><topic>IgE</topic><topic>Immunoglobulin E - blood</topic><topic>Immunopathology</topic><topic>in utero</topic><topic>Intestines - immunology</topic><topic>Medical sciences</topic><topic>Milk, Human - immunology</topic><topic>Pregnancy</topic><topic>Receptors, IgE - analysis</topic><topic>Skin - immunology</topic><topic>Statistics, Nonparametric</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Thornton, C. A.</creatorcontrib><creatorcontrib>Holloway, J. A.</creatorcontrib><creatorcontrib>Popplewell, E. J.</creatorcontrib><creatorcontrib>Shute, J. K.</creatorcontrib><creatorcontrib>Boughton, J.</creatorcontrib><creatorcontrib>Warner, J. O.</creatorcontrib><collection>Istex</collection><collection>Pascal-Francis</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Immunology Abstracts</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>ProQuest Health &amp; Medical Complete (Alumni)</collection><collection>MEDLINE - Academic</collection><jtitle>Clinical and experimental allergy</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Thornton, C. A.</au><au>Holloway, J. A.</au><au>Popplewell, E. J.</au><au>Shute, J. K.</au><au>Boughton, J.</au><au>Warner, J. O.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Fetal exposure to intact immunoglobulin E occurs via the gastrointestinal tract</atitle><jtitle>Clinical and experimental allergy</jtitle><addtitle>Clin Exp Allergy</addtitle><date>2003-03</date><risdate>2003</risdate><volume>33</volume><issue>3</issue><spage>306</spage><epage>311</epage><pages>306-311</pages><issn>0954-7894</issn><eissn>1365-2222</eissn><abstract>Summary Background Consideration of the evolutionary significance of IgE might provide insight into the immunological interactions occurring in utero and during early post‐natal life that regulate later atopic disease. Objective We postulated that the fetal gut is exposed to intact amniotic fluid IgE that might interact with local IgE receptors. Methods IgE levels in matched maternal blood and amniotic fluid (n = 47) or breast milk (n = 15) collected from pregnant women in the UK (Southampton) and Brazil (Sao Paulo) were studied. Expression of IgE receptors, FcɛRI and FcɛRII (CD23), in fetal gastrointestinal tract (n = 19) and skin (n = 11) was examined immunohistochemically. Results Human amniotic fluid at 16–18 weeks' gestation contained intact IgE at levels that increased as maternal circulating levels increased (Spearman's ρ = 0.897; P &lt; 0.001). Circulating IgE levels from women in Sao Paulo, Brazil, associated positively not only with term (&gt; 37 weeks' gestation) amniotic fluid (ρ = 0.993; P &lt; 0.001) but also breast milk IgE levels (ρ = 0.785; P = 0.001). Maternal levels of IgE did not change significantly over pregnancy and fetal circulating levels of IgE were very low (&lt; 0.6 IU/mL). Low‐affinity IgE receptors (CD23) were expressed in lymphoid follicles of the fetal gut from 16 weeks of gestation (6/8), but not from 11 to 16 weeks (0/11) or in the skin. Conclusion Amniotic fluid contains intact IgE that might bind to CD23+ cells within the lymphoid follicles of the fetal gastrointestinal tract. The evolutionary significance of these interactions might be to prepare the immune system for helminthic parasite exposure at birth via IgE‐mediated antigen focusing, or ‘education’ of the developing immune system about the prevailing extrauterine environment. However, at present in societies where helminthosis is not a significant health issue, this pathway may still be operational and associated with the development of atopic disease.</abstract><cop>Oxford, UK</cop><pub>Blackwell Science Ltd</pub><pmid>12614443</pmid><doi>10.1046/j.1365-2222.2003.01614.x</doi><tpages>6</tpages><oa>free_for_read</oa></addata></record>
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subjects Allergic diseases
amniotic fluid
Amniotic Fluid - immunology
Biological and medical sciences
breast milk
CD23
Enzyme-Linked Immunosorbent Assay
Female
Fetal Blood - immunology
fetal gut
Fetus - immunology
General aspects
Gestational Age
Humans
Hypersensitivity - etiology
IgE
Immunoglobulin E - blood
Immunopathology
in utero
Intestines - immunology
Medical sciences
Milk, Human - immunology
Pregnancy
Receptors, IgE - analysis
Skin - immunology
Statistics, Nonparametric
title Fetal exposure to intact immunoglobulin E occurs via the gastrointestinal tract
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