Interleukin-10 and its receptors at the maternal–conceptus interface: expression, regulation, and implication for T helper 2 cytokine predominance and maternal immune tolerance in the pig, a true epitheliochorial placentation species
The appropriate balance between pro-inflammatory and anti-inflammatory cytokines is important for the maternal immune tolerance during pregnancy in mammals. Among the various cytokines, interleukin (IL)-10 (IL10) plays an essential role in anti-inflammatory responses, while IL12 is involved in pro-i...
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| Veröffentlicht in: | Biology of reproduction 2022-06, Vol.106 (6), p.1159-1174 |
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| creator | Han, Jisoo Yoo, Inkyu Lee, Soohyung Cheon, Yugyeong Yun, Cheol-Heui Ka, Hakhyun |
| description | The appropriate balance between pro-inflammatory and anti-inflammatory cytokines is important for the maternal immune tolerance during pregnancy in mammals. Among the various cytokines, interleukin (IL)-10 (IL10) plays an essential role in anti-inflammatory responses, while IL12 is involved in pro-inflammatory responses during pregnancy. However, the roles of IL10 and IL12 in the endometrium during pregnancy have not been studied in pigs. Thus, we investigated the expression of IL10, IL12 (IL12A and IL12B), and their receptors (IL10RA, IL10RB, IL12RB1, and IL12RB2) at the maternal–conceptus interface. IL10, IL12, and their receptors were expressed in the endometrium during the estrous cycle and pregnancy in a pregnancy stage-specific manner. During pregnancy, IL10 expression increased on Day 15, whereas the expression of IL12A and IL12B decreased after the implantation period. IL10 protein was localized to luminal epithelial (LE), stromal cells, and macrophages; IL10RA protein to LE, endothelial, stromal, and T cells; and IL10RB mRNA to LE cells in the endometrium. IL10 and IL10RA proteins and IL10RB mRNA were also localized to chorionic epithelial (CE) cells. In endometrial explants, the expression of IL10RA and IL10RB was induced by estradiol-17β, IL-1β, and/or interferon-γ . Heme oxygenase 1, an IL10-inducible factor, was expressed in the endometrium with the highest levels on Day 30 of pregnancy and was localized to LE and CE cells. These results in pigs suggest that conceptus-derived signals change the endometrial immune environment by regulating the expression of IL10 and IL10 receptors at the maternal–conceptus interface and that IL10 may provide anti-inflammatory conditions for the maternal immune tolerance. Summary Sentence IL10 expression increases at the maternal–conceptus interface in pigs. |
| doi_str_mv | 10.1093/biolre/ioac058 |
| format | Article |
| fullrecord | <record><control><sourceid>proquest_cross</sourceid><recordid>TN_cdi_proquest_miscellaneous_2644942197</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><oup_id>10.1093/biolre/ioac058</oup_id><sourcerecordid>2644942197</sourcerecordid><originalsourceid>FETCH-LOGICAL-b324t-19d24956ddee9d9d8119bfc9abc224c462cd99c538d317162717084927fad3b93</originalsourceid><addsrcrecordid>eNqFkrtuFTEQhlcIRA6BlhJZogEpm_iyN9OhiEukSDShXnnt2RwHr21sr0S6vEPekJaXwLt7QkGTytbM9___WJ6ieE3wKcGcnQ3amQBn2gmJ6-5JsSM15WVLm-5pscMYNyVjDTsqXsR4gzGpGGXPiyNWs6prGN0Vfy5sgmBg_qFtSTASViGdIgogwScXIhIJpT2gSWTOCvP77l46uzTniPQiHoWEDwh--QAxamdPsvh6NiKt99Vw8kbLtYBGF9AV2oPxEBBF8ja5HA0oq5WbtBXZexU9BGb1NGcgOQNh7Wq7TuT1dbZHKcyAwOtcMtrJvQs6i7zJU9m0ZUYPUkN8WTwbhYnw6nAeF98_f7o6_1pefvtycf7xshwYrVJJuKIVrxulALjiqiOED6PkYpCUVrJqqFScy5p1ipGWNLQlLe4qTttRKDZwdly823x9cD9niKmfdJRgjLDg5tjTpqp4RQlvM_r2P_TGzcurF6rtCOOENpk63SgZXIwBxt4HPYlw2xPcL2vQb2vQH9YgC94cbOdhAvUPf_j3DLzfADf7x81ONjbXnYXH8L8UMtRc</addsrcrecordid><sourcetype>Aggregation Database</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2678139126</pqid></control><display><type>article</type><title>Interleukin-10 and its receptors at the maternal–conceptus interface: expression, regulation, and implication for T helper 2 cytokine predominance and maternal immune tolerance in the pig, a true epitheliochorial placentation species</title><source>Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals</source><source>Oxford University Press Journals All Titles (1996-Current)</source><source>Alma/SFX Local Collection</source><creator>Han, Jisoo ; Yoo, Inkyu ; Lee, Soohyung ; Cheon, Yugyeong ; Yun, Cheol-Heui ; Ka, Hakhyun</creator><creatorcontrib>Han, Jisoo ; Yoo, Inkyu ; Lee, Soohyung ; Cheon, Yugyeong ; Yun, Cheol-Heui ; Ka, Hakhyun</creatorcontrib><description>The appropriate balance between pro-inflammatory and anti-inflammatory cytokines is important for the maternal immune tolerance during pregnancy in mammals. Among the various cytokines, interleukin (IL)-10 (IL10) plays an essential role in anti-inflammatory responses, while IL12 is involved in pro-inflammatory responses during pregnancy. However, the roles of IL10 and IL12 in the endometrium during pregnancy have not been studied in pigs. Thus, we investigated the expression of IL10, IL12 (IL12A and IL12B), and their receptors (IL10RA, IL10RB, IL12RB1, and IL12RB2) at the maternal–conceptus interface. IL10, IL12, and their receptors were expressed in the endometrium during the estrous cycle and pregnancy in a pregnancy stage-specific manner. During pregnancy, IL10 expression increased on Day 15, whereas the expression of IL12A and IL12B decreased after the implantation period. IL10 protein was localized to luminal epithelial (LE), stromal cells, and macrophages; IL10RA protein to LE, endothelial, stromal, and T cells; and IL10RB mRNA to LE cells in the endometrium. IL10 and IL10RA proteins and IL10RB mRNA were also localized to chorionic epithelial (CE) cells. In endometrial explants, the expression of IL10RA and IL10RB was induced by estradiol-17β, IL-1β, and/or interferon-γ . Heme oxygenase 1, an IL10-inducible factor, was expressed in the endometrium with the highest levels on Day 30 of pregnancy and was localized to LE and CE cells. These results in pigs suggest that conceptus-derived signals change the endometrial immune environment by regulating the expression of IL10 and IL10 receptors at the maternal–conceptus interface and that IL10 may provide anti-inflammatory conditions for the maternal immune tolerance. Summary Sentence IL10 expression increases at the maternal–conceptus interface in pigs.</description><identifier>ISSN: 0006-3363</identifier><identifier>EISSN: 1529-7268</identifier><identifier>DOI: 10.1093/biolre/ioac058</identifier><identifier>PMID: 35348632</identifier><language>eng</language><publisher>United States: Society for the Study of Reproduction</publisher><subject>17β-Estradiol ; Cytokines ; Endometrium ; Estrus cycle ; Explants ; Heme ; IL-1β ; immune tolerance ; Immunological tolerance ; Implantation ; Inflammation ; Interleukin 1 ; Interleukin 10 ; Interleukin 12 ; Leukocytes (neutrophilic) ; Lymphocytes T ; Macrophages ; mRNA ; Oxygenase ; pig ; Pregnancy ; RESEARCH ARTICLE ; Stromal cells ; γ-Interferon</subject><ispartof>Biology of reproduction, 2022-06, Vol.106 (6), p.1159-1174</ispartof><rights>The Author(s) 2022. Published by Oxford University Press on behalf of Society for the Study of Reproduction. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com journals.permissions@oup.com</rights><rights>The Author(s) 2022. Published by Oxford University Press on behalf of Society for the Study of Reproduction. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com 2022</rights><rights>The Author(s) 2022. Published by Oxford University Press on behalf of Society for the Study of Reproduction. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.</rights><rights>The Author(s) 2022. Published by Oxford University Press on behalf of Society for the Study of Reproduction. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-b324t-19d24956ddee9d9d8119bfc9abc224c462cd99c538d317162717084927fad3b93</citedby><cites>FETCH-LOGICAL-b324t-19d24956ddee9d9d8119bfc9abc224c462cd99c538d317162717084927fad3b93</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>315,781,785,1585,27929,27930</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/35348632$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Han, Jisoo</creatorcontrib><creatorcontrib>Yoo, Inkyu</creatorcontrib><creatorcontrib>Lee, Soohyung</creatorcontrib><creatorcontrib>Cheon, Yugyeong</creatorcontrib><creatorcontrib>Yun, Cheol-Heui</creatorcontrib><creatorcontrib>Ka, Hakhyun</creatorcontrib><title>Interleukin-10 and its receptors at the maternal–conceptus interface: expression, regulation, and implication for T helper 2 cytokine predominance and maternal immune tolerance in the pig, a true epitheliochorial placentation species</title><title>Biology of reproduction</title><addtitle>Biol Reprod</addtitle><description>The appropriate balance between pro-inflammatory and anti-inflammatory cytokines is important for the maternal immune tolerance during pregnancy in mammals. Among the various cytokines, interleukin (IL)-10 (IL10) plays an essential role in anti-inflammatory responses, while IL12 is involved in pro-inflammatory responses during pregnancy. However, the roles of IL10 and IL12 in the endometrium during pregnancy have not been studied in pigs. Thus, we investigated the expression of IL10, IL12 (IL12A and IL12B), and their receptors (IL10RA, IL10RB, IL12RB1, and IL12RB2) at the maternal–conceptus interface. IL10, IL12, and their receptors were expressed in the endometrium during the estrous cycle and pregnancy in a pregnancy stage-specific manner. During pregnancy, IL10 expression increased on Day 15, whereas the expression of IL12A and IL12B decreased after the implantation period. IL10 protein was localized to luminal epithelial (LE), stromal cells, and macrophages; IL10RA protein to LE, endothelial, stromal, and T cells; and IL10RB mRNA to LE cells in the endometrium. IL10 and IL10RA proteins and IL10RB mRNA were also localized to chorionic epithelial (CE) cells. In endometrial explants, the expression of IL10RA and IL10RB was induced by estradiol-17β, IL-1β, and/or interferon-γ . Heme oxygenase 1, an IL10-inducible factor, was expressed in the endometrium with the highest levels on Day 30 of pregnancy and was localized to LE and CE cells. These results in pigs suggest that conceptus-derived signals change the endometrial immune environment by regulating the expression of IL10 and IL10 receptors at the maternal–conceptus interface and that IL10 may provide anti-inflammatory conditions for the maternal immune tolerance. Summary Sentence IL10 expression increases at the maternal–conceptus interface in pigs.</description><subject>17β-Estradiol</subject><subject>Cytokines</subject><subject>Endometrium</subject><subject>Estrus cycle</subject><subject>Explants</subject><subject>Heme</subject><subject>IL-1β</subject><subject>immune tolerance</subject><subject>Immunological tolerance</subject><subject>Implantation</subject><subject>Inflammation</subject><subject>Interleukin 1</subject><subject>Interleukin 10</subject><subject>Interleukin 12</subject><subject>Leukocytes (neutrophilic)</subject><subject>Lymphocytes T</subject><subject>Macrophages</subject><subject>mRNA</subject><subject>Oxygenase</subject><subject>pig</subject><subject>Pregnancy</subject><subject>RESEARCH ARTICLE</subject><subject>Stromal cells</subject><subject>γ-Interferon</subject><issn>0006-3363</issn><issn>1529-7268</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNqFkrtuFTEQhlcIRA6BlhJZogEpm_iyN9OhiEukSDShXnnt2RwHr21sr0S6vEPekJaXwLt7QkGTytbM9___WJ6ieE3wKcGcnQ3amQBn2gmJ6-5JsSM15WVLm-5pscMYNyVjDTsqXsR4gzGpGGXPiyNWs6prGN0Vfy5sgmBg_qFtSTASViGdIgogwScXIhIJpT2gSWTOCvP77l46uzTniPQiHoWEDwh--QAxamdPsvh6NiKt99Vw8kbLtYBGF9AV2oPxEBBF8ja5HA0oq5WbtBXZexU9BGb1NGcgOQNh7Wq7TuT1dbZHKcyAwOtcMtrJvQs6i7zJU9m0ZUYPUkN8WTwbhYnw6nAeF98_f7o6_1pefvtycf7xshwYrVJJuKIVrxulALjiqiOED6PkYpCUVrJqqFScy5p1ipGWNLQlLe4qTttRKDZwdly823x9cD9niKmfdJRgjLDg5tjTpqp4RQlvM_r2P_TGzcurF6rtCOOENpk63SgZXIwBxt4HPYlw2xPcL2vQb2vQH9YgC94cbOdhAvUPf_j3DLzfADf7x81ONjbXnYXH8L8UMtRc</recordid><startdate>20220613</startdate><enddate>20220613</enddate><creator>Han, Jisoo</creator><creator>Yoo, Inkyu</creator><creator>Lee, Soohyung</creator><creator>Cheon, Yugyeong</creator><creator>Yun, Cheol-Heui</creator><creator>Ka, Hakhyun</creator><general>Society for the Study of Reproduction</general><general>Oxford University Press</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FD</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>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>P64</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>RC3</scope><scope>7X8</scope></search><sort><creationdate>20220613</creationdate><title>Interleukin-10 and its receptors at the maternal–conceptus interface: expression, regulation, and implication for T helper 2 cytokine predominance and maternal immune tolerance in the pig, a true epitheliochorial placentation species</title><author>Han, Jisoo ; Yoo, Inkyu ; Lee, Soohyung ; Cheon, Yugyeong ; Yun, Cheol-Heui ; Ka, Hakhyun</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-b324t-19d24956ddee9d9d8119bfc9abc224c462cd99c538d317162717084927fad3b93</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>17β-Estradiol</topic><topic>Cytokines</topic><topic>Endometrium</topic><topic>Estrus cycle</topic><topic>Explants</topic><topic>Heme</topic><topic>IL-1β</topic><topic>immune tolerance</topic><topic>Immunological tolerance</topic><topic>Implantation</topic><topic>Inflammation</topic><topic>Interleukin 1</topic><topic>Interleukin 10</topic><topic>Interleukin 12</topic><topic>Leukocytes (neutrophilic)</topic><topic>Lymphocytes T</topic><topic>Macrophages</topic><topic>mRNA</topic><topic>Oxygenase</topic><topic>pig</topic><topic>Pregnancy</topic><topic>RESEARCH ARTICLE</topic><topic>Stromal cells</topic><topic>γ-Interferon</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Han, Jisoo</creatorcontrib><creatorcontrib>Yoo, Inkyu</creatorcontrib><creatorcontrib>Lee, Soohyung</creatorcontrib><creatorcontrib>Cheon, Yugyeong</creatorcontrib><creatorcontrib>Yun, Cheol-Heui</creatorcontrib><creatorcontrib>Ka, Hakhyun</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Technology Research Database</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>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</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>Biotechnology and BioEngineering Abstracts</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>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Biology of reproduction</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Han, Jisoo</au><au>Yoo, Inkyu</au><au>Lee, Soohyung</au><au>Cheon, Yugyeong</au><au>Yun, Cheol-Heui</au><au>Ka, Hakhyun</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Interleukin-10 and its receptors at the maternal–conceptus interface: expression, regulation, and implication for T helper 2 cytokine predominance and maternal immune tolerance in the pig, a true epitheliochorial placentation species</atitle><jtitle>Biology of reproduction</jtitle><addtitle>Biol Reprod</addtitle><date>2022-06-13</date><risdate>2022</risdate><volume>106</volume><issue>6</issue><spage>1159</spage><epage>1174</epage><pages>1159-1174</pages><issn>0006-3363</issn><eissn>1529-7268</eissn><abstract>The appropriate balance between pro-inflammatory and anti-inflammatory cytokines is important for the maternal immune tolerance during pregnancy in mammals. Among the various cytokines, interleukin (IL)-10 (IL10) plays an essential role in anti-inflammatory responses, while IL12 is involved in pro-inflammatory responses during pregnancy. However, the roles of IL10 and IL12 in the endometrium during pregnancy have not been studied in pigs. Thus, we investigated the expression of IL10, IL12 (IL12A and IL12B), and their receptors (IL10RA, IL10RB, IL12RB1, and IL12RB2) at the maternal–conceptus interface. IL10, IL12, and their receptors were expressed in the endometrium during the estrous cycle and pregnancy in a pregnancy stage-specific manner. During pregnancy, IL10 expression increased on Day 15, whereas the expression of IL12A and IL12B decreased after the implantation period. IL10 protein was localized to luminal epithelial (LE), stromal cells, and macrophages; IL10RA protein to LE, endothelial, stromal, and T cells; and IL10RB mRNA to LE cells in the endometrium. IL10 and IL10RA proteins and IL10RB mRNA were also localized to chorionic epithelial (CE) cells. In endometrial explants, the expression of IL10RA and IL10RB was induced by estradiol-17β, IL-1β, and/or interferon-γ . Heme oxygenase 1, an IL10-inducible factor, was expressed in the endometrium with the highest levels on Day 30 of pregnancy and was localized to LE and CE cells. These results in pigs suggest that conceptus-derived signals change the endometrial immune environment by regulating the expression of IL10 and IL10 receptors at the maternal–conceptus interface and that IL10 may provide anti-inflammatory conditions for the maternal immune tolerance. Summary Sentence IL10 expression increases at the maternal–conceptus interface in pigs.</abstract><cop>United States</cop><pub>Society for the Study of Reproduction</pub><pmid>35348632</pmid><doi>10.1093/biolre/ioac058</doi><tpages>16</tpages></addata></record> |
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| source | Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Oxford University Press Journals All Titles (1996-Current); Alma/SFX Local Collection |
| subjects | 17β-Estradiol Cytokines Endometrium Estrus cycle Explants Heme IL-1β immune tolerance Immunological tolerance Implantation Inflammation Interleukin 1 Interleukin 10 Interleukin 12 Leukocytes (neutrophilic) Lymphocytes T Macrophages mRNA Oxygenase pig Pregnancy RESEARCH ARTICLE Stromal cells γ-Interferon |
| title | Interleukin-10 and its receptors at the maternal–conceptus interface: expression, regulation, and implication for T helper 2 cytokine predominance and maternal immune tolerance in the pig, a true epitheliochorial placentation species |
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