{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,13]],"date-time":"2026-10-13T02:47:49Z","timestamp":1791859669611,"version":"4.3.4"},"reference-count":120,"publisher":"F1000 Research Ltd","license":[{"start":{"date-parts":[[2019,7,2]],"date-time":"2019-07-02T00:00:00Z","timestamp":1562025600000},"content-version":"unspecified","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100000268","name":"Biotechnology and Biological Sciences Research Council","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100000268","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Wellbeing of Women"}],"content-domain":{"domain":["f1000research.com"],"crossmark-restriction":false},"short-container-title":["F1000Res"],"abstract":"<ns4:p>\n                    The presence of unusual natural killer cells in human endometrium has been recognized for 30 years, but despite considerable research effort, the\n                    <ns4:italic>in vivo<\/ns4:italic>\n                    role of uterine natural killer (uNK) cells in both normal and pathological pregnancy remains uncertain. uNK cells may differentiate from precursors present in endometrium, but migration from peripheral blood in response to chemokine stimuli with\n                    <ns4:italic>in situ<\/ns4:italic>\n                    modification to a uNK cell phenotype is also possible. uNK cells produce a wide range of secretory products with diverse effects on trophoblast and spiral arteries which may play an important role in implantation and early placentation. Interactions with other decidual cell populations are also becoming clear. Recent evidence has demonstrated subpopulations of uNK cells and the presence of other innate lymphoid cell populations in decidua which may refine future approaches to investigation of the role of uNK cells in human pregnancy.\n                  <\/ns4:p>","DOI":"10.12688\/f1000research.19132.1","type":"journal-article","created":{"date-parts":[[2019,7,2]],"date-time":"2019-07-02T05:20:09Z","timestamp":1562044809000},"page":"999","update-policy":"https:\/\/doi.org\/10.12688\/f1000research.crossmark-policy","source":"Crossref","is-referenced-by-count":45,"title":["Uterine natural killer cells: Time for a re-appraisal?"],"prefix":"10.12688","volume":"8","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-0001-1004","authenticated-orcid":false,"given":"Judith N.","family":"Bulmer","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3606-1361","authenticated-orcid":false,"given":"Gendie 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Tissue Res."},{"key":"ref-4","first-page":"687-96","article-title":"The fine structure of the rat metrial gland in relation to the origin of the granulated cells.","volume":"123","author":"S Peel","year":"1977","journal-title":"J Anat."},{"key":"ref-5","first-page":"329-31","article-title":"Endometrial granulocytes in human decidua react with a natural-killer (NK) cell marker, NKH1.","volume":"62","author":"A Ritson","year":"1987","journal-title":"Immunology."},{"key":"ref-6","first-page":"129-34","article-title":"Cell populations in human early pregnancy decidua: characterization and isolation of large granular lymphocytes by flow cytometry.","volume":"65","author":"P Starkey","year":"1988","journal-title":"Immunology."},{"key":"ref-7","doi-asserted-by":"publisher","first-page":"195-205","DOI":"10.1016\/0198-8859(89)90060-8","article-title":"Immunocytochemical characterization of the unusual large granular lymphocytes in human endometrium throughout the menstrual 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Pathol."},{"key":"ref-11","doi-asserted-by":"publisher","first-page":"1027-34","DOI":"10.1016\/j.placenta.2014.09.018","article-title":"Dynamic changes in maternal decidual leukocyte populations from first to second trimester gestation.","volume":"35","author":"M Kwan","year":"2014","journal-title":"Placenta."},{"key":"ref-12","doi-asserted-by":"publisher","first-page":"24-31","DOI":"10.1016\/j.jri.2009.08.001","article-title":"Decidual leucocyte populations in early to late gestation normal human pregnancy.","volume":"82","author":"P Williams","year":"2009","journal-title":"J Reprod Immunol."},{"key":"ref-13","doi-asserted-by":"publisher","first-page":"281-94","DOI":"10.1387\/ijdb.082763jb","article-title":"Immune cells in the placental bed.","volume":"54","author":"J Bulmer","year":"2010","journal-title":"Int J Dev Biol."},{"key":"ref-14","doi-asserted-by":"publisher","first-page":"347-53","DOI":"10.1038\/s41586-018-0698-6","article-title":"Single-cell reconstruction of the early 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Immunol."},{"key":"ref-18","doi-asserted-by":"publisher","first-page":"1201-12","DOI":"10.1084\/jem.20030305","article-title":"Human decidual natural killer cells are a unique NK cell subset with immunomodulatory potential.","volume":"198","author":"L Koopman","year":"2003","journal-title":"J Exp Med."},{"key":"ref-19","doi-asserted-by":"publisher","first-page":"919-26","DOI":"10.1093\/humrep\/del456","article-title":"Cells with haematopoietic stem cell phenotype in adult human endometrium: relevance to infertility?","volume":"22","author":"L Lynch","year":"2007","journal-title":"Hum Reprod."},{"key":"ref-20","doi-asserted-by":"publisher","first-page":"3378-83","DOI":"10.1073\/pnas.0611098104","article-title":"TGFbeta promotes conversion of CD16+ peripheral blood NK cells into CD16- NK cells with similarities to decidual NK cells.","volume":"104","author":"D Keskin","year":"2007","journal-title":"Proc Natl Acad Sci U S 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Reprod."},{"key":"ref-45","doi-asserted-by":"publisher","first-page":"3009-17","DOI":"10.4049\/jimmunol.181.5.3009","article-title":"Critical and differential roles of nkp46- and nkp30-activating receptors expressed by uterine NK cells in early pregnancy.","volume":"181","author":"H El Costa","year":"2008","journal-title":"J Immunol."},{"key":"ref-46","doi-asserted-by":"publisher","first-page":"3017-27","DOI":"10.1002\/eji.201141445","article-title":"The effect of pregnancy on the uterine NK cell KIR repertoire.","volume":"41","author":"V Male","year":"2011","journal-title":"Eur J Immunol."},{"key":"ref-47","doi-asserted-by":"publisher","first-page":"322-31","DOI":"10.1038\/mi.2016.50","article-title":"Composition and dynamics of the uterine NK cell KIR repertoire in menstrual blood.","volume":"10","author":"M Ivarsson","year":"2017","journal-title":"Mucosal 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Reprod."},{"key":"ref-51","doi-asserted-by":"publisher","first-page":"4102-10","DOI":"10.1172\/JCI43998","article-title":"Maternal activating KIRs protect against human reproductive failure mediated by fetal HLA-C2.","volume":"120","author":"S Hiby","year":"2010","journal-title":"J Clin Invest."},{"key":"ref-52","doi-asserted-by":"publisher","first-page":"2593-601","DOI":"10.4049\/jimmunol.1800860","article-title":"High-Resolution Genetic and Phenotypic Analysis of KIR2DL1 Alleles and Their Association with Pre-Eclampsia.","volume":"201","author":"O Huhn","year":"2018","journal-title":"J Immunol."},{"key":"ref-53","doi-asserted-by":"publisher","first-page":"93-8","DOI":"10.1016\/j.jri.2005.12.005","article-title":"The incidence of pre-eclampsia among couples consisting of Japanese women and Caucasian men.","volume":"70","author":"S Saito","year":"2006","journal-title":"J Reprod Immunol."},{"key":"ref-54","doi-asserted-by":"publisher","first-page":"27-33","DOI":"10.1016\/j.placenta.2018.11.008","article-title":"Fetal human leukocyte antigen-C and maternal killer-cell immunoglobulin-like receptors in cases of severe preeclampsia.","volume":"75","author":"T Larsen","year":"2019","journal-title":"Placenta."},{"key":"ref-55","doi-asserted-by":"publisher","first-page":"653-64","DOI":"10.2353\/ajpath.2008.071169","article-title":"Granulysin produced by uterine natural killer cells induces apoptosis of extravillous trophoblasts in spontaneous abortion.","volume":"173","author":"A Nakashima","year":"2008","journal-title":"Am J Pathol."},{"key":"ref-56","doi-asserted-by":"publisher","first-page":"155","DOI":"10.1095\/biolreprod.112.099465","article-title":"Maternal decidual macrophages inhibit nk cell killing of invasive cytotrophoblasts during human pregnancy.","volume":"88","author":"E Co","year":"2013","journal-title":"Biol 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Med."},{"key":"ref-67","doi-asserted-by":"publisher","first-page":"595-601","DOI":"10.1016\/j.placenta.2010.04.012","article-title":"Role of interleukin 8 in uterine natural killer cell regulation of extravillous trophoblast cell invasion.","volume":"31","author":"L De Oliveira","year":"2010","journal-title":"Placenta."},{"key":"ref-68","doi-asserted-by":"publisher","first-page":"2512-8","DOI":"10.1096\/fj.06-6616com","article-title":"Interferon-gamma inhibits extravillous trophoblast cell invasion by a mechanism that involves both changes in apoptosis and protease levels.","volume":"20","author":"G Lash","year":"2006","journal-title":"FASEB J."},{"key":"ref-69","doi-asserted-by":"publisher","first-page":"1-11","DOI":"10.1016\/j.jri.2010.10.003","article-title":"Effect of tumour necrosis factor-\u03b1 in combination with interferon-\u03b3 on first trimester extravillous trophoblast invasion.","volume":"88","author":"H Otun","year":"2011","journal-title":"J Reprod Immunol."},{"key":"ref-70","doi-asserted-by":"publisher","first-page":"1137-45","DOI":"10.1093\/humrep\/deq050","article-title":"Regulation of extravillous trophoblast invasion by uterine natural killer cells is dependent on gestational age.","volume":"25","author":"G Lash","year":"2010","journal-title":"Hum Reprod."},{"key":"ref-71","doi-asserted-by":"publisher","first-page":"8522-30","DOI":"10.4049\/jimmunol.177.12.8522","article-title":"Decidual NK cells alter in vitro first trimester extravillous cytotrophoblast migration: a role for IFN-gamma.","volume":"177","author":"Y Hu","year":"2006","journal-title":"J Immunol."},{"key":"ref-72","doi-asserted-by":"publisher","first-page":"939-58","DOI":"10.1016\/j.placenta.2005.12.006","article-title":"The uterine spiral arteries in human pregnancy: facts and controversies.","volume":"27","author":"R Pijnenborg","year":"2006","journal-title":"Placenta."},{"key":"ref-73","doi-asserted-by":"publisher","first-page":"998-1004","DOI":"10.1016\/j.placenta.2012.09.004","article-title":"Effects of local decidua on trophoblast invasion and spiral artery remodeling in focal placenta creta - an immunohistochemical study.","volume":"33","author":"T Hannon","year":"2012","journal-title":"Placenta."},{"key":"ref-74","doi-asserted-by":"publisher","first-page":"1412-8","DOI":"10.1016\/j.placenta.2015.10.013","article-title":"Differentiation of first trimester cytotrophoblast to extravillous trophoblast involves an epithelial-mesenchymal transition.","volume":"36","author":"S DaSilva-Arnold","year":"2015","journal-title":"Placenta."},{"key":"ref-75","doi-asserted-by":"publisher","first-page":"310-21","DOI":"10.1080\/19336918.2016.1170258","article-title":"Epithelial-mesenchymal transition during extravillous trophoblast differentiation.","volume":"10","author":"J E 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