Trans-epithelial immune cell transfer during suckling modulates delayed-type hypersensitivity in recipients as a function of gender
Breast feeding has long term effects on the developing immune system which outlive passive immunization of the neonate. We have investigated the transfer of milk immune cells and examined the result of transfer once the recipients were adult. Non-transgenic mouse pups were foster-nursed by green flu...
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| description | Breast feeding has long term effects on the developing immune system which outlive passive immunization of the neonate. We have investigated the transfer of milk immune cells and examined the result of transfer once the recipients were adult.
Non-transgenic mouse pups were foster-nursed by green fluorescent protein (GFP) transgenic dams for 3 weeks and the fate of GFP+ cells was followed by FACS analysis, immunohistochemistry and RT-PCR for GFP and appropriate immune cell markers. Pups suckled by non-transgenic dams served as controls.
Despite a preponderance of B cells and macrophages in the stomach contents of the pups, most cells undergoing trans-epithelial migration derived from the 3-4% of milk cells positive for T lymphocyte markers. These cells homed to the spleen and thymus, with maximal accumulation at 3-4 weeks. By sensitizing dams with an antigen which elicits a T cell-mediated delayed-type-hypersensitivity (DTH) response, we determined that nursing by a sensitized dam (compared to a non-sensitized dam) amplified a subsequent DTH response in females and yet suppressed one in males.
These results suggest that clinical evaluation weighing the pros and cons of nursing male versus female children by mothers with genetically-linked hypersensitivity diseases, such as celiac disease and eczema, or those in regions of the world with endemic DTH-eliciting diseases, such as tuberculosis, may be warranted. |
| doi_str_mv | 10.1371/journal.pone.0003562 |
| format | Article |
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Non-transgenic mouse pups were foster-nursed by green fluorescent protein (GFP) transgenic dams for 3 weeks and the fate of GFP+ cells was followed by FACS analysis, immunohistochemistry and RT-PCR for GFP and appropriate immune cell markers. Pups suckled by non-transgenic dams served as controls.
Despite a preponderance of B cells and macrophages in the stomach contents of the pups, most cells undergoing trans-epithelial migration derived from the 3-4% of milk cells positive for T lymphocyte markers. These cells homed to the spleen and thymus, with maximal accumulation at 3-4 weeks. By sensitizing dams with an antigen which elicits a T cell-mediated delayed-type-hypersensitivity (DTH) response, we determined that nursing by a sensitized dam (compared to a non-sensitized dam) amplified a subsequent DTH response in females and yet suppressed one in males.
These results suggest that clinical evaluation weighing the pros and cons of nursing male versus female children by mothers with genetically-linked hypersensitivity diseases, such as celiac disease and eczema, or those in regions of the world with endemic DTH-eliciting diseases, such as tuberculosis, may be warranted.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0003562</identifier><identifier>PMID: 18958163</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Adoptive Transfer - veterinary ; Allergy ; Analysis ; Animals ; Animals, Newborn ; Animals, Suckling ; Antigen-antibody reactions ; Antigens ; Autoimmune diseases ; B cells ; Babies ; Breast feeding ; Celiac disease ; Cell migration ; Cell Movement - immunology ; Cell Movement - physiology ; Children ; Cytokines ; Dams ; Eczema ; Female ; Females ; Flow cytometry ; Fluorescence ; Gastroenterology and Hepatology/Small Intestine ; Gender ; Genetic engineering ; Green fluorescent protein ; Green Fluorescent Proteins - genetics ; Green Fluorescent Proteins - metabolism ; Hormones ; Hypersensitivity ; Hypersensitivity (delayed) ; Hypersensitivity, Delayed - immunology ; Immune system ; Immunity, Maternally-Acquired - physiology ; Immunization ; Immunization (passive) ; Immunoglobulins ; Immunohistochemistry ; Immunology ; Immunology/Allergy and Hypersensitivity ; Intestinal Mucosa - immunology ; Intestinal Mucosa - metabolism ; Intestinal Mucosa - physiology ; Laboratory animals ; Lactation - immunology ; Leukocyte migration ; Long term effects ; Lymphocytes ; Lymphocytes B ; Lymphocytes T ; Macrophages ; Male ; Males ; Mammary Glands, Animal - immunology ; Mammary Glands, Animal - physiology ; Markers ; Mice ; Mice, Inbred C57BL ; Mice, Transgenic ; Milk ; Newborn babies ; Nitrogen ; Nursing ; Pediatrics and Child Health/Neonatology ; Polymerase chain reaction ; Public Health and Epidemiology/Epidemiology ; Rodents ; Sensitizing ; Sex Characteristics ; Skin diseases ; Spleen ; Stomach ; Stomach - cytology ; Stomach - metabolism ; Suckling behavior ; T cells ; Thymus ; Transgenic mice ; Tuberculosis</subject><ispartof>PloS one, 2008-10, Vol.3 (10), p.e3562-e3562</ispartof><rights>COPYRIGHT 2008 Public Library of Science</rights><rights>2008 Ma et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>Ma et al. 2008</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c662t-4d45a0565b9cd61c5204e5fea174caf6fedc763e1cad9320b1023dbb7b6a70d43</citedby><cites>FETCH-LOGICAL-c662t-4d45a0565b9cd61c5204e5fea174caf6fedc763e1cad9320b1023dbb7b6a70d43</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC2569205/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC2569205/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2102,2928,23866,27924,27925,53791,53793,79600,79601</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/18958163$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Zimmer, Jacques</contributor><creatorcontrib>Ma, Lisa J</creatorcontrib><creatorcontrib>Walter, Barbara</creatorcontrib><creatorcontrib>Deguzman, Ariel</creatorcontrib><creatorcontrib>Muller, H Konrad</creatorcontrib><creatorcontrib>Walker, Ameae M</creatorcontrib><title>Trans-epithelial immune cell transfer during suckling modulates delayed-type hypersensitivity in recipients as a function of gender</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Breast feeding has long term effects on the developing immune system which outlive passive immunization of the neonate. We have investigated the transfer of milk immune cells and examined the result of transfer once the recipients were adult.
Non-transgenic mouse pups were foster-nursed by green fluorescent protein (GFP) transgenic dams for 3 weeks and the fate of GFP+ cells was followed by FACS analysis, immunohistochemistry and RT-PCR for GFP and appropriate immune cell markers. Pups suckled by non-transgenic dams served as controls.
Despite a preponderance of B cells and macrophages in the stomach contents of the pups, most cells undergoing trans-epithelial migration derived from the 3-4% of milk cells positive for T lymphocyte markers. These cells homed to the spleen and thymus, with maximal accumulation at 3-4 weeks. By sensitizing dams with an antigen which elicits a T cell-mediated delayed-type-hypersensitivity (DTH) response, we determined that nursing by a sensitized dam (compared to a non-sensitized dam) amplified a subsequent DTH response in females and yet suppressed one in males.
These results suggest that clinical evaluation weighing the pros and cons of nursing male versus female children by mothers with genetically-linked hypersensitivity diseases, such as celiac disease and eczema, or those in regions of the world with endemic DTH-eliciting diseases, such as tuberculosis, may be warranted.</description><subject>Adoptive Transfer - veterinary</subject><subject>Allergy</subject><subject>Analysis</subject><subject>Animals</subject><subject>Animals, Newborn</subject><subject>Animals, Suckling</subject><subject>Antigen-antibody reactions</subject><subject>Antigens</subject><subject>Autoimmune diseases</subject><subject>B cells</subject><subject>Babies</subject><subject>Breast feeding</subject><subject>Celiac disease</subject><subject>Cell migration</subject><subject>Cell Movement - immunology</subject><subject>Cell Movement - physiology</subject><subject>Children</subject><subject>Cytokines</subject><subject>Dams</subject><subject>Eczema</subject><subject>Female</subject><subject>Females</subject><subject>Flow cytometry</subject><subject>Fluorescence</subject><subject>Gastroenterology and Hepatology/Small Intestine</subject><subject>Gender</subject><subject>Genetic engineering</subject><subject>Green fluorescent protein</subject><subject>Green Fluorescent Proteins - genetics</subject><subject>Green Fluorescent Proteins - metabolism</subject><subject>Hormones</subject><subject>Hypersensitivity</subject><subject>Hypersensitivity (delayed)</subject><subject>Hypersensitivity, Delayed - immunology</subject><subject>Immune system</subject><subject>Immunity, Maternally-Acquired - physiology</subject><subject>Immunization</subject><subject>Immunization (passive)</subject><subject>Immunoglobulins</subject><subject>Immunohistochemistry</subject><subject>Immunology</subject><subject>Immunology/Allergy and Hypersensitivity</subject><subject>Intestinal Mucosa - immunology</subject><subject>Intestinal Mucosa - metabolism</subject><subject>Intestinal Mucosa - physiology</subject><subject>Laboratory animals</subject><subject>Lactation - immunology</subject><subject>Leukocyte migration</subject><subject>Long term effects</subject><subject>Lymphocytes</subject><subject>Lymphocytes B</subject><subject>Lymphocytes T</subject><subject>Macrophages</subject><subject>Male</subject><subject>Males</subject><subject>Mammary Glands, Animal - immunology</subject><subject>Mammary Glands, Animal - physiology</subject><subject>Markers</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Mice, Transgenic</subject><subject>Milk</subject><subject>Newborn babies</subject><subject>Nitrogen</subject><subject>Nursing</subject><subject>Pediatrics and Child Health/Neonatology</subject><subject>Polymerase chain reaction</subject><subject>Public Health and Epidemiology/Epidemiology</subject><subject>Rodents</subject><subject>Sensitizing</subject><subject>Sex Characteristics</subject><subject>Skin diseases</subject><subject>Spleen</subject><subject>Stomach</subject><subject>Stomach - cytology</subject><subject>Stomach - metabolism</subject><subject>Suckling behavior</subject><subject>T cells</subject><subject>Thymus</subject><subject>Transgenic mice</subject><subject>Tuberculosis</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2008</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNqNk12PEyEUhidG467Vf2CUxGQTL1r5GJjOjclm40eTTTbR1VvCwJmWlYEKzMZe-8dlbNWt8cJAgMDzHjiHc6rqKcELwhry6iaM0Su32AYPC4wx44Leq05Jy-hcUMzu31mfVI9SusGYs6UQD6sTsmz5kgh2Wn2_jsqnOWxt3oCzyiE7DKMHpME5lKfDHiIyY7R-jdKov7hpMQQzOpUhIQNO7cDM824LaFOGmMAnm-2tzTtkPYqg7daCzwmp0lE_ep1t8Cj0aA3eQHxcPeiVS_DkMM-qT2_fXF-8n19evVtdnF_OtRA0z2tTc4W54F2rjSCaU1wD70GRptaqFz0Y3QgGRCtTHMcdwZSZrms6oRpsajarnu_tbl1I8hC_JAkjlOG2bSditSdMUDdyG-2g4k4GZeXPjRDXUsVstQPZAuWqYaqrmaqXGJTqa85NUy9pt6RcFFuvD7eN3VCeViIQlTsyenzi7Uauw60s4paWr5pVZwcDMXwdIWU52DR9i_IQxiRF29C6LT7Oqhd_gf_2bbGn1qo83_o-lFt1aQYGq0sS9bbsn9cN5Q0hHBfByyNBYTJ8y2s1piRXHz_8P3v1-Zg9u8NuQLm8ScGNU1KkY7DegzqGlCL0v4NHsJxq4JefcqoBeaiBInt2N_B_RIekZz8A4xIF2g</recordid><startdate>20081029</startdate><enddate>20081029</enddate><creator>Ma, Lisa J</creator><creator>Walter, Barbara</creator><creator>Deguzman, Ariel</creator><creator>Muller, H Konrad</creator><creator>Walker, Ameae M</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><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>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20081029</creationdate><title>Trans-epithelial immune cell transfer during suckling modulates delayed-type hypersensitivity in recipients as a function of gender</title><author>Ma, Lisa J ; Walter, Barbara ; Deguzman, Ariel ; Muller, H Konrad ; Walker, Ameae M</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c662t-4d45a0565b9cd61c5204e5fea174caf6fedc763e1cad9320b1023dbb7b6a70d43</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2008</creationdate><topic>Adoptive Transfer - veterinary</topic><topic>Allergy</topic><topic>Analysis</topic><topic>Animals</topic><topic>Animals, Newborn</topic><topic>Animals, Suckling</topic><topic>Antigen-antibody reactions</topic><topic>Antigens</topic><topic>Autoimmune diseases</topic><topic>B cells</topic><topic>Babies</topic><topic>Breast feeding</topic><topic>Celiac disease</topic><topic>Cell migration</topic><topic>Cell Movement - immunology</topic><topic>Cell Movement - physiology</topic><topic>Children</topic><topic>Cytokines</topic><topic>Dams</topic><topic>Eczema</topic><topic>Female</topic><topic>Females</topic><topic>Flow cytometry</topic><topic>Fluorescence</topic><topic>Gastroenterology and Hepatology/Small Intestine</topic><topic>Gender</topic><topic>Genetic engineering</topic><topic>Green fluorescent protein</topic><topic>Green Fluorescent Proteins - genetics</topic><topic>Green Fluorescent Proteins - metabolism</topic><topic>Hormones</topic><topic>Hypersensitivity</topic><topic>Hypersensitivity (delayed)</topic><topic>Hypersensitivity, Delayed - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Ma, Lisa J</au><au>Walter, Barbara</au><au>Deguzman, Ariel</au><au>Muller, H Konrad</au><au>Walker, Ameae M</au><au>Zimmer, Jacques</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Trans-epithelial immune cell transfer during suckling modulates delayed-type hypersensitivity in recipients as a function of gender</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2008-10-29</date><risdate>2008</risdate><volume>3</volume><issue>10</issue><spage>e3562</spage><epage>e3562</epage><pages>e3562-e3562</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Breast feeding has long term effects on the developing immune system which outlive passive immunization of the neonate. We have investigated the transfer of milk immune cells and examined the result of transfer once the recipients were adult.
Non-transgenic mouse pups were foster-nursed by green fluorescent protein (GFP) transgenic dams for 3 weeks and the fate of GFP+ cells was followed by FACS analysis, immunohistochemistry and RT-PCR for GFP and appropriate immune cell markers. Pups suckled by non-transgenic dams served as controls.
Despite a preponderance of B cells and macrophages in the stomach contents of the pups, most cells undergoing trans-epithelial migration derived from the 3-4% of milk cells positive for T lymphocyte markers. These cells homed to the spleen and thymus, with maximal accumulation at 3-4 weeks. By sensitizing dams with an antigen which elicits a T cell-mediated delayed-type-hypersensitivity (DTH) response, we determined that nursing by a sensitized dam (compared to a non-sensitized dam) amplified a subsequent DTH response in females and yet suppressed one in males.
These results suggest that clinical evaluation weighing the pros and cons of nursing male versus female children by mothers with genetically-linked hypersensitivity diseases, such as celiac disease and eczema, or those in regions of the world with endemic DTH-eliciting diseases, such as tuberculosis, may be warranted.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>18958163</pmid><doi>10.1371/journal.pone.0003562</doi><tpages>e3562</tpages><oa>free_for_read</oa></addata></record> |
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| recordid | cdi_plos_journals_1312309994 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Public Library of Science (PLoS); EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Adoptive Transfer - veterinary Allergy Analysis Animals Animals, Newborn Animals, Suckling Antigen-antibody reactions Antigens Autoimmune diseases B cells Babies Breast feeding Celiac disease Cell migration Cell Movement - immunology Cell Movement - physiology Children Cytokines Dams Eczema Female Females Flow cytometry Fluorescence Gastroenterology and Hepatology/Small Intestine Gender Genetic engineering Green fluorescent protein Green Fluorescent Proteins - genetics Green Fluorescent Proteins - metabolism Hormones Hypersensitivity Hypersensitivity (delayed) Hypersensitivity, Delayed - immunology Immune system Immunity, Maternally-Acquired - physiology Immunization Immunization (passive) Immunoglobulins Immunohistochemistry Immunology Immunology/Allergy and Hypersensitivity Intestinal Mucosa - immunology Intestinal Mucosa - metabolism Intestinal Mucosa - physiology Laboratory animals Lactation - immunology Leukocyte migration Long term effects Lymphocytes Lymphocytes B Lymphocytes T Macrophages Male Males Mammary Glands, Animal - immunology Mammary Glands, Animal - physiology Markers Mice Mice, Inbred C57BL Mice, Transgenic Milk Newborn babies Nitrogen Nursing Pediatrics and Child Health/Neonatology Polymerase chain reaction Public Health and Epidemiology/Epidemiology Rodents Sensitizing Sex Characteristics Skin diseases Spleen Stomach Stomach - cytology Stomach - metabolism Suckling behavior T cells Thymus Transgenic mice Tuberculosis |
| title | Trans-epithelial immune cell transfer during suckling modulates delayed-type hypersensitivity in recipients as a function of gender |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-06T09%3A10%3A17IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Trans-epithelial%20immune%20cell%20transfer%20during%20suckling%20modulates%20delayed-type%20hypersensitivity%20in%20recipients%20as%20a%20function%20of%20gender&rft.jtitle=PloS%20one&rft.au=Ma,%20Lisa%20J&rft.date=2008-10-29&rft.volume=3&rft.issue=10&rft.spage=e3562&rft.epage=e3562&rft.pages=e3562-e3562&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0003562&rft_dat=%3Cgale_plos_%3EA472571150%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1312309994&rft_id=info:pmid/18958163&rft_galeid=A472571150&rft_doaj_id=oai_doaj_org_article_9e25a73ab43a480eaaf455d7482b8256&rfr_iscdi=true |