Extracellular Vesicle-Mediated Secretion of HLA-E by Trophoblasts Maintains Pregnancy by Regulating the Metabolism of Decidual NK Cells
Extracellular vesicles derived from trophoblasts (T-EVs) play an important role in pregnancy, but the mechanism is not entirely clear. In this study, we found that HLA-E, which is mostly confined to the cytoplasm of trophoblast cells, was secreted by T-EVs. The level of HLA-E in T-EVs from unexplain...
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| Veröffentlicht in: | International journal of biological sciences 2021-01, Vol.17 (15), p.4377-4395 |
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| creator | Jiang, Lingling Fei, Haiyi Jin, Xiaoying Liu, Xiu Yang, Cuiyu Li, Chao Chen, Jianmin Yang, Anran Zhu, Jiajuan Wang, Huihong Fei, Xiaoyang Zhang, Songying |
| description | Extracellular vesicles derived from trophoblasts (T-EVs) play an important role in pregnancy, but the mechanism is not entirely clear. In this study, we found that HLA-E, which is mostly confined to the cytoplasm of trophoblast cells, was secreted by T-EVs. The level of HLA-E in T-EVs from unexplained recurrent spontaneous abortion (URSA) patients was lower than that in normal pregnancy (NP) and RSA patients who had an abnormal embryo karyotype (AK-RSA). T-EVs promoted secretion of IFN-γ and VEGFα by decidual NK (dNK) cells from URSA patients via HLA-E, VEGFα was necessary for angiogenesis and trophoblast growth, and IFN-γ inhibited Th17 induction. Glycolysis and oxidative phosphorylation (OxPhos) were involved in this process. Glycolysis but not OxPhos of dNK cells facilitated by T-EVs was dependent on mTORC1 activation. Inhibition of T-EV production
increased the susceptibility of mice to embryo absorption, which was reversed by transferring exogenous T-EVs. T-EVs promoted secretion of IFN-γ and VEGFα by dNK cells to maintain pregnancy via Qa-1 in abortion-prone mouse models. This study reveals a new mechanism of pregnancy maintenance mediated by HLA-E via T-EVs. |
| doi_str_mv | 10.7150/ijbs.63390 |
| format | Article |
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increased the susceptibility of mice to embryo absorption, which was reversed by transferring exogenous T-EVs. T-EVs promoted secretion of IFN-γ and VEGFα by dNK cells to maintain pregnancy via Qa-1 in abortion-prone mouse models. This study reveals a new mechanism of pregnancy maintenance mediated by HLA-E via T-EVs.</description><identifier>ISSN: 1449-2288</identifier><identifier>EISSN: 1449-2288</identifier><identifier>DOI: 10.7150/ijbs.63390</identifier><identifier>PMID: 34803505</identifier><language>eng</language><publisher>Australia: Ivyspring International Publisher Pty Ltd</publisher><subject>Angiogenesis ; Animal models ; Animals ; Cell Line ; Cytoplasm ; Cytotoxicity ; Decidua ; Decidua - cytology ; Embryos ; Extracellular Vesicles - metabolism ; Female ; Flow cytometry ; Gestational age ; Glycolysis ; Helper cells ; Histocompatibility Antigens Class I - genetics ; Histocompatibility Antigens Class I - metabolism ; HLA-E Antigens ; Humans ; Immune system ; Interferon-gamma - genetics ; Interferon-gamma - metabolism ; Karyotypes ; Killer Cells, Natural - physiology ; Kinases ; Laboratory animals ; Ligands ; Lymphocytes T ; Metabolism ; Mice ; Mice, Nude ; Miscarriage ; Oxidative phosphorylation ; Phosphorylation ; Placenta - cytology ; Pregnancy ; Research Paper ; Secretion ; Tissue Culture Techniques ; Trophoblasts ; Trophoblasts - physiology ; Vascular Endothelial Growth Factor A - genetics ; Vascular Endothelial Growth Factor A - metabolism ; γ-Interferon</subject><ispartof>International journal of biological sciences, 2021-01, Vol.17 (15), p.4377-4395</ispartof><rights>The author(s).</rights><rights>2021. This work is published under https://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><rights>The author(s) 2021</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c406t-8abd71ec5a45c8507ada068897e44ee267df0bc2994aeec08551c33351cabf443</citedby></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8579460/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8579460/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34803505$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Jiang, Lingling</creatorcontrib><creatorcontrib>Fei, Haiyi</creatorcontrib><creatorcontrib>Jin, Xiaoying</creatorcontrib><creatorcontrib>Liu, Xiu</creatorcontrib><creatorcontrib>Yang, Cuiyu</creatorcontrib><creatorcontrib>Li, Chao</creatorcontrib><creatorcontrib>Chen, Jianmin</creatorcontrib><creatorcontrib>Yang, Anran</creatorcontrib><creatorcontrib>Zhu, Jiajuan</creatorcontrib><creatorcontrib>Wang, Huihong</creatorcontrib><creatorcontrib>Fei, Xiaoyang</creatorcontrib><creatorcontrib>Zhang, Songying</creatorcontrib><title>Extracellular Vesicle-Mediated Secretion of HLA-E by Trophoblasts Maintains Pregnancy by Regulating the Metabolism of Decidual NK Cells</title><title>International journal of biological sciences</title><addtitle>Int J Biol Sci</addtitle><description>Extracellular vesicles derived from trophoblasts (T-EVs) play an important role in pregnancy, but the mechanism is not entirely clear. In this study, we found that HLA-E, which is mostly confined to the cytoplasm of trophoblast cells, was secreted by T-EVs. The level of HLA-E in T-EVs from unexplained recurrent spontaneous abortion (URSA) patients was lower than that in normal pregnancy (NP) and RSA patients who had an abnormal embryo karyotype (AK-RSA). T-EVs promoted secretion of IFN-γ and VEGFα by decidual NK (dNK) cells from URSA patients via HLA-E, VEGFα was necessary for angiogenesis and trophoblast growth, and IFN-γ inhibited Th17 induction. Glycolysis and oxidative phosphorylation (OxPhos) were involved in this process. Glycolysis but not OxPhos of dNK cells facilitated by T-EVs was dependent on mTORC1 activation. Inhibition of T-EV production
increased the susceptibility of mice to embryo absorption, which was reversed by transferring exogenous T-EVs. T-EVs promoted secretion of IFN-γ and VEGFα by dNK cells to maintain pregnancy via Qa-1 in abortion-prone mouse models. This study reveals a new mechanism of pregnancy maintenance mediated by HLA-E via T-EVs.</description><subject>Angiogenesis</subject><subject>Animal models</subject><subject>Animals</subject><subject>Cell Line</subject><subject>Cytoplasm</subject><subject>Cytotoxicity</subject><subject>Decidua</subject><subject>Decidua - cytology</subject><subject>Embryos</subject><subject>Extracellular Vesicles - metabolism</subject><subject>Female</subject><subject>Flow cytometry</subject><subject>Gestational age</subject><subject>Glycolysis</subject><subject>Helper cells</subject><subject>Histocompatibility Antigens Class I - genetics</subject><subject>Histocompatibility Antigens Class I - metabolism</subject><subject>HLA-E Antigens</subject><subject>Humans</subject><subject>Immune system</subject><subject>Interferon-gamma - genetics</subject><subject>Interferon-gamma - metabolism</subject><subject>Karyotypes</subject><subject>Killer Cells, Natural - physiology</subject><subject>Kinases</subject><subject>Laboratory animals</subject><subject>Ligands</subject><subject>Lymphocytes T</subject><subject>Metabolism</subject><subject>Mice</subject><subject>Mice, Nude</subject><subject>Miscarriage</subject><subject>Oxidative phosphorylation</subject><subject>Phosphorylation</subject><subject>Placenta - cytology</subject><subject>Pregnancy</subject><subject>Research Paper</subject><subject>Secretion</subject><subject>Tissue Culture Techniques</subject><subject>Trophoblasts</subject><subject>Trophoblasts - physiology</subject><subject>Vascular Endothelial Growth Factor A - genetics</subject><subject>Vascular Endothelial Growth Factor A - metabolism</subject><subject>γ-Interferon</subject><issn>1449-2288</issn><issn>1449-2288</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</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><recordid>eNpdkctu1DAUhi0EoqWw4QGQJTYIKa0TX-JskKphaBEzgKCwtRznZMajjD21narzBLx2HXpRYeGL5E_fOcc_Qq9LclyXnJzYTRuPBaUNeYIOS8aaoqqkfProfoBexLghhAouyXN0QJkklBN-iP7Mr1PQBoZhHHTAvyFaM0CxhM7qBB3-CSZAst5h3-PzxWkxx-0eXwS_W_t20DFFvNTWpbwi_h5g5bQz-4n5AausTNatcFoDXkLSrR9s3E6mj2BsN-oBf_2CZ7l4fIme9XqI8OruPEK_Ps0vZufF4tvZ59npojCMiFRI3XZ1CYZrxo3kpNadJkLKpgbGACpRdz1pTdU0TAMYIjkvDaU077rtGaNH6MOtdze2W-gMuDz-oHbBbnXYK6-t-vfF2bVa-Ssled0wQbLg3Z0g-MsRYlJbG6f_0w78GFUlCJEVy3RG3_6HbvwYXB5PVbzhQhBRiky9v6VM8DEG6B-aKYma8lVTvupvvhl-87j9B_Q-UHoDOASjFw</recordid><startdate>20210101</startdate><enddate>20210101</enddate><creator>Jiang, Lingling</creator><creator>Fei, Haiyi</creator><creator>Jin, Xiaoying</creator><creator>Liu, Xiu</creator><creator>Yang, Cuiyu</creator><creator>Li, Chao</creator><creator>Chen, Jianmin</creator><creator>Yang, Anran</creator><creator>Zhu, Jiajuan</creator><creator>Wang, Huihong</creator><creator>Fei, Xiaoyang</creator><creator>Zhang, Songying</creator><general>Ivyspring International Publisher Pty Ltd</general><general>Ivyspring International Publisher</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>7QL</scope><scope>7QO</scope><scope>7U9</scope><scope>8FD</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BENPR</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20210101</creationdate><title>Extracellular Vesicle-Mediated Secretion of HLA-E by Trophoblasts Maintains Pregnancy by Regulating the Metabolism of Decidual NK Cells</title><author>Jiang, Lingling ; Fei, Haiyi ; Jin, Xiaoying ; Liu, Xiu ; Yang, Cuiyu ; Li, Chao ; Chen, Jianmin ; Yang, Anran ; Zhu, Jiajuan ; Wang, Huihong ; Fei, Xiaoyang ; Zhang, Songying</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c406t-8abd71ec5a45c8507ada068897e44ee267df0bc2994aeec08551c33351cabf443</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Angiogenesis</topic><topic>Animal models</topic><topic>Animals</topic><topic>Cell Line</topic><topic>Cytoplasm</topic><topic>Cytotoxicity</topic><topic>Decidua</topic><topic>Decidua - cytology</topic><topic>Embryos</topic><topic>Extracellular Vesicles - metabolism</topic><topic>Female</topic><topic>Flow cytometry</topic><topic>Gestational age</topic><topic>Glycolysis</topic><topic>Helper cells</topic><topic>Histocompatibility Antigens Class I - genetics</topic><topic>Histocompatibility Antigens Class I - metabolism</topic><topic>HLA-E Antigens</topic><topic>Humans</topic><topic>Immune system</topic><topic>Interferon-gamma - genetics</topic><topic>Interferon-gamma - metabolism</topic><topic>Karyotypes</topic><topic>Killer Cells, Natural - physiology</topic><topic>Kinases</topic><topic>Laboratory animals</topic><topic>Ligands</topic><topic>Lymphocytes T</topic><topic>Metabolism</topic><topic>Mice</topic><topic>Mice, Nude</topic><topic>Miscarriage</topic><topic>Oxidative phosphorylation</topic><topic>Phosphorylation</topic><topic>Placenta - cytology</topic><topic>Pregnancy</topic><topic>Research Paper</topic><topic>Secretion</topic><topic>Tissue Culture Techniques</topic><topic>Trophoblasts</topic><topic>Trophoblasts - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>International journal of biological sciences</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Jiang, Lingling</au><au>Fei, Haiyi</au><au>Jin, Xiaoying</au><au>Liu, Xiu</au><au>Yang, Cuiyu</au><au>Li, Chao</au><au>Chen, Jianmin</au><au>Yang, Anran</au><au>Zhu, Jiajuan</au><au>Wang, Huihong</au><au>Fei, Xiaoyang</au><au>Zhang, Songying</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Extracellular Vesicle-Mediated Secretion of HLA-E by Trophoblasts Maintains Pregnancy by Regulating the Metabolism of Decidual NK Cells</atitle><jtitle>International journal of biological sciences</jtitle><addtitle>Int J Biol Sci</addtitle><date>2021-01-01</date><risdate>2021</risdate><volume>17</volume><issue>15</issue><spage>4377</spage><epage>4395</epage><pages>4377-4395</pages><issn>1449-2288</issn><eissn>1449-2288</eissn><abstract>Extracellular vesicles derived from trophoblasts (T-EVs) play an important role in pregnancy, but the mechanism is not entirely clear. In this study, we found that HLA-E, which is mostly confined to the cytoplasm of trophoblast cells, was secreted by T-EVs. The level of HLA-E in T-EVs from unexplained recurrent spontaneous abortion (URSA) patients was lower than that in normal pregnancy (NP) and RSA patients who had an abnormal embryo karyotype (AK-RSA). T-EVs promoted secretion of IFN-γ and VEGFα by decidual NK (dNK) cells from URSA patients via HLA-E, VEGFα was necessary for angiogenesis and trophoblast growth, and IFN-γ inhibited Th17 induction. Glycolysis and oxidative phosphorylation (OxPhos) were involved in this process. Glycolysis but not OxPhos of dNK cells facilitated by T-EVs was dependent on mTORC1 activation. Inhibition of T-EV production
increased the susceptibility of mice to embryo absorption, which was reversed by transferring exogenous T-EVs. T-EVs promoted secretion of IFN-γ and VEGFα by dNK cells to maintain pregnancy via Qa-1 in abortion-prone mouse models. This study reveals a new mechanism of pregnancy maintenance mediated by HLA-E via T-EVs.</abstract><cop>Australia</cop><pub>Ivyspring International Publisher Pty Ltd</pub><pmid>34803505</pmid><doi>10.7150/ijbs.63390</doi><tpages>19</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Angiogenesis Animal models Animals Cell Line Cytoplasm Cytotoxicity Decidua Decidua - cytology Embryos Extracellular Vesicles - metabolism Female Flow cytometry Gestational age Glycolysis Helper cells Histocompatibility Antigens Class I - genetics Histocompatibility Antigens Class I - metabolism HLA-E Antigens Humans Immune system Interferon-gamma - genetics Interferon-gamma - metabolism Karyotypes Killer Cells, Natural - physiology Kinases Laboratory animals Ligands Lymphocytes T Metabolism Mice Mice, Nude Miscarriage Oxidative phosphorylation Phosphorylation Placenta - cytology Pregnancy Research Paper Secretion Tissue Culture Techniques Trophoblasts Trophoblasts - physiology Vascular Endothelial Growth Factor A - genetics Vascular Endothelial Growth Factor A - metabolism γ-Interferon |
| title | Extracellular Vesicle-Mediated Secretion of HLA-E by Trophoblasts Maintains Pregnancy by Regulating the Metabolism of Decidual NK Cells |
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