The Role of Uterine NK Cells in Normal Reproduction and Reproductive Disorders




Blois SM, Klapp BF, Barrientos G (2011) Decidualization and angiogenesis in early pregnancy: unravelling the functions of DC and NK cells. J Reprod Immunol 88:86–92PubMed


Broudy VC (1997) Stem cell factor and hematopoiesis. Blood 90:1345–1364PubMed


Bulmer JN, Lash GE (2005) Human uterine natural killer cells: a reappraisal. Mol Immunol 42:511–521PubMed


Bulmer JN, Lunny DP, Hagin SV (1988a) Immunohistochemical characterization of stromal leucocytes in nonpregnant human endometrium. Am J Reprod Immunol Microbiol 17:83–90PubMed


Bulmer JN, Smith J, Morrison L, Wells M (1988b) Maternal and fetal cellular relationships in the human placental basal plate. Placenta 9:237–246PubMed


Bulmer JN, Morrison L, Longfellow M, Ritson A, Pace D (1991) Granulated lymphocytes in human endometrium: histochemical and immunohistochemical studies. Hum Reprod 6:791–798PubMed


Bulmer JN, Williams PJ, Lash GE (2010) Immune cells in the placental bed. Int J Dev Biol 54:281–294PubMed


Castriconi R, Cantoni C, Della Chiesa M, Vitale M, Marcenaro E, Conte R, Biassoni R, Bottino C, Moretta L, Moretta A (2003) Transforming growth factor beta 1 inhibits expression of NKp30 and NKG2D receptors: consequences for the NK-mediated killing of dendritic cells. Proc Natl Acad Sci USA 100:4120–4125PubMedCentralPubMed


Champion H, Innes BA, Robson SC, Lash GE, Bulmer JN (2012) Effects of interleukin-6 on extravillous trophoblast invasion in early human pregnancy. Mol Hum Reprod 18:391–400PubMed


Chao KH, Yang YS, Ho HN, Chen SU, Chen HF, Dai HJ, Huang SC, Gill TJ 3rd (1995) Decidual natural killer cytotoxicity decreased in normal pregnancy but not in anembryonic pregnancy and recurrent spontaneous abortion. Am J Reprod Immunol 34:274–280PubMed


Chazara O, Xiong S, Moffett A (2011) Maternal KIR and fetal HLA-C: a fine balance. J Leukoc Biol 90:703–716PubMed


Chen LJ, Han ZQ, Zhou H, Zou L, Zou P (2010) Inhibition of HLA-G expression via RNAi abolishes resistance of Extravillous trophoblast cell line TEV-1 to NK lysis. Placenta 31:519–527PubMed


Chumbly G, King A, Robertson K, Holmes N, Loke YW (1994) Resistance of HLA-G and HLA-A2 transfectants to lysis by decidual NK cells. Cell Immunol 155:312–322


Clark DA (2014) Popular myths in reproductive immunology. J Reprod Immunol 104–105:54–62PubMed


Clifford K, Flanagan AM, Regan L (1999) Endometrial CD56+ natural killer cells in women with recurrent miscarriage: a histomorphometric study. Hum Reprod 14:2727–2730PubMed


Cooper MA, Fehniger TA, Caligiuri MA (2001) The biology of human natural killer-cell subsets. Trends Immunol 22:633–640PubMed


Craven CM, Morgan T, Ward K (1998) Decidual spiral artery remodelling begins before cellular interaction with cytotrophoblasts. Placenta 19:241–252PubMed


De Oliveira LG, Lash GE, Murray-Dunning C, Bulmer JN, Innes BA, Searle RF, Sass N, Robson SC (2010) Role of interleukin 8 in uterine natural killer cell regulation of extravillous trophoblast cell invasion. Placenta 31:595–601PubMed


Dietl J, Hönig A, Kämmerer U, Rieger L (2006) Natural killer cells and dendritic cells at the human feto-maternal interface: an effective cooperation? Placenta 27:341–347PubMed


Dimitriadis E, White CA, Jones RL, Salamonsen LA (2005) Cytokines, chemokines and growth factors in endometrium related to implantation. Hum Reprod Update 11:613–630


Disep B, Innes BA, Cochrane HR, Tijani S, Bulmer JN (2004) Immunohistochemical characterization of endometrial leucocytes in endometritis. Histopathology 45:625–632PubMed


Dunn CL, Critchley HO, Kelly RW (2002) IL-15 regulation in human endometrial stromal cells. J Clin Endocrinol Metab 87:1898–1901


Eide IP, Rolfseng T, Isaksen CV, Mecsei R, Roald B, Lydersen S, Salvesen KA, Harsem NK, Austgulen R (2006) Serious foetal growth restriction is associated with reduced proportions of natural killer cells in decidua basalis. Virchows Arch 448:269–276PubMed


Emmer PM, Steegers EA, Kerstens HM, Bulten J, Nelen WL, Boer K, Joosten I (2002) Altered phenotype of HLA-G expressing trophoblast and decidual natural killer cells in pathological pregnancies. Hum Reprod 17:1072–1080PubMed


Eriksson M, Meadows SK, Wira CR, Sentman CL (2004) Unique phenotype of human uterine NK cells and their regulation by endogenous TGF-beta. J Leukoc Biol 76:667–675PubMed


Evans J, Salamonsen LA (2012) Inflammation, leukocytes and menstruation. Rev Endocr Metab Disord 13:277–288PubMed


Everett C (1997) Incidence and outcome of bleeding before the 20th week of pregnancy: prospective study from general practice. BMJ 315:32–34PubMedCentralPubMed


Fraser R, Whitley GS, Johnstone AP et al (2012) Impaired decidual natural killer cell regulation of vascular remodelling in early human pregnancies with high uterine artery resistance. J Pathol 228:322–332PubMedCentralPubMed


Freud AG, Yokohama A, Becknell B, Lee MT, Mao HC, Ferketich AK, Caligiuri MA (2006) Evidence for discrete stages of human natural killer cell differentiation in vivo. J Exp Med 203:1033–1043PubMedCentralPubMed


Fu B, Wang F, Sun R, Ling B, Tian Z, Wei H (2011) CD11b and CD27 reflect distinct population and functional specialization in human natural killer cells. Immunology 133:350–359PubMedCentralPubMed


Fu B, Li X, Sun R, Tong X, Ling B, Tian Z, Wei H (2013) Natural killer cells promote immune tolerance by regulating inflammatory TH17 cells at the human maternal-fetal interface. Proc Natl Acad Sci USA 110:E231–240PubMedCentralPubMed


Fukui A, Fujii S, Yamaguchi E, Kimura H, Sato S, Saito Y (1999) Natural killer cell subpopulations and cytotoxicity for infertile patients undergoing in vitro fertilization. Am J Reprod Immunol 41:413–422PubMed


Gardner L, Moffett A (2003) Dendritic cells in the human decidua. Biol Reprod 69:1438–1446PubMed


Gargett CE, Masuda H (2010) Adult stem cells in the endometrium. Mol Hum Reprod 16:818–834PubMed


Gibson DA, McInnes KJ, Critchley HO, Saunders PT (2013) Endometrial Intracrinology—generation of an estrogen-dominated microenvironment in the secretory phase of women. J Clin Endocrinol Metab 98:E1802–1806PubMed


Guerin LR, Moldenhauer LM, Prins JR, Bromfield JJ, Hayball JD, Robertson SA (2011) Seminal fluid regulates accumulation of FOXP3+ regulatory T cells in the preimplantation mouse uterus through expanding the FOXP3+ cell pool and CCL19-mediated recruitment. Biol Reprod 85:397–408PubMed


Gustafsson C, Mjösberg J, Matussek A, Geffers R, Matthiesen L, Berg G, Sharma S, Buer J, Ernerudh J (2008) Gene expression profiling of human decidual macrophages: evidence for immunosuppressive phenotype. PLoS One 3, e2078PubMedCentralPubMed


Hamperl H, Hellweg G (1958) Granular endometrial stroma cells. Obstet Gynecol 11:379–387PubMed


Hanna J, Goldman-Wohl D, Hamani Y, Avraham I, Greenfield C, Natanson-Yaron S, Prus D, Cohen-Daniel L, Arnon TI, Manaster I, Gazit R, Yutkin V, Benharroch D, Porgador A, Keshet E, Yagel S, Mandelboim O (2006) Decidual NK cells regulate key developmental processes at the human fetal-maternal interface. Nat Med 12:1065–1074PubMed


Hannan NJ, Paiva P, Meehan KL, Rombauts LJ, Gardner DK, Salamonsen LA (2011) Analysis of fertility-related soluble mediators in human uterine fluid identifies VEGF as a key regulator of embryo implantation. Endocrinology 152:4948–4956PubMed


Hannon T, Innes BA, Lash GE, Bulmer JN, Robson SC (2012) Effects of local decidua on trophoblast invasion and spiral artery remodeling in focal placenta creta—an immunohistochemical study. Placenta 33:998–1004PubMed


Heikkinen J, Mottonen M, Komi J, Alanen A, Lassila O (2003) Phenotypic characterization of human decidual macrophages. Clin Exp Immunol 131:498–505PubMedCentralPubMed


Helige C, Ahammer H, Moser G, Hammer A, Dohr G, Huppertz B, Sedlmayr P (2014) Distribution of decidual natural killer cells and macrophages in the neighbourhood of the trophoblast invasion front: a quantitative evaluation. Hum Reprod 29:8–17PubMed


Henderson TA, Saunders PTK, Moffett-King A, Groome NP, Critchley HOD (2003) Steroid receptor expression in uterine natural killer cells. J Clin Endocrinol Metab 88:440–449PubMed


Hiby SE, Walker JJ, O’shaughnessy KM, Redman CW, Carrington M, Trowsdale J, Moffett A (2004) Combinations of maternal KIR and fetal HLA-C genes influence the risk of preeclampsia and reproductive success. J Exp Med 200:957–965PubMedCentralPubMed


Hiby SE, Apps R, Sharkey AM, Farrell LE, Gardner L, Mulder A, Claas FH, Walker JJ, Redman CC, Morgan L, Tower C, Regan L, Moore GE, Carrington M, Moffett A (2010) Maternal activating KIRs protect against human reproductive failure mediated by fetal HLA-C2. J Clin Invest 120:4102–4110PubMedCentralPubMed


Houser BL (2012) Decidual macrophages and their roles at the maternal-fetal interface. Yale J Biol Med 85:105–118PubMedCentralPubMed


Houser BL, Tilburgs T, Hill J, Nicotra ML, Strominger JL (2011) Two unique human decidual macrophage populations. J Immunol 186:2633–2642PubMedCentralPubMed


Hu Y, Dutz JP, Maccalman CD, Yong P, Tan R, Von Dadelszen P (2006) Decidual NK cells alter in vitro first trimester extravillous cytotrophoblast migration: a role for IFN-gamma. J Immunol 177:8522–8530PubMed


Hutter H, Dohr G (1998) HLA expression on immature and mature human germ cells. J Reprod Immunol 38:101–122PubMed


Jokhi PP, King A, Loke YW (1994) Production of granulocyte-macrophage colony-stimulating factor by human trophoblast cells and by decidual large granular lymphocytes. Hum Reprod 9:1660–1669PubMed


Jones RK, Bulmer JN, Searle RF (1997) Cytotoxic activity of endometrial granulated lymphocytes during the menstrual cycle in humans. Biol Reprod 57:1217–1222PubMed


Jones RK, Searle RF, Stewart JA, Turner S, Bulmer JN (1998) Apoptosis, bcl-2 expression, and proliferative activity in human endometrial stroma and endometrial granulated lymphocytes. Biol Reprod 58:995–1002PubMed


Jones RL, Stoikos C, Findlay JK, Salamonsen LA (2006) TGF-beta superfamily expression and actions in the endometrium and placenta. Reproduction 132:217–232PubMed


Kalkunte SS, Mselle TF, Norris WE, Wira CR, Sentman CL, Sharma S (2009) Vascular endothelial growth factor C facilitates immune tolerance and endovascular activity of human uterine NK cells at the maternal-fetal interface. J Immunol 182:4085–4092PubMedCentralPubMed


Kam EP, Gardner L, Loke YW, King A (1999) The role of trophoblast in the physiological change in decidual spiral arteries. Hum Reprod 14:2131–2138PubMed


Kämmerer U, Marzusch K, Kröber S, Ruck P, Handgretinger R, Dietl J (1999) A subset of CD56+ large granular lymphocytes in first-trimester human decidua are proliferating cells. Fertil Steril 71:74–79PubMed


Kammerer U, Eggert AO, Kapp M, McLellan AD, Geijtenbeek TB, Dietl J, van Kooyk Y, Kampgen E (2003) Unique appearance of proliferating antigen-presenting cells expressing DC-SIGN (CD209) in the decidua of early human pregnancy. Am J Pathol 162:887–896PubMedCentralPubMed


Kauma S, Huff T, Krystal G, Ryan J, Takacs P, Turner T (1996) The expression of stem cell factor and its receptor, c-kit in human endometrium and placental tissues during pregnancy. J Clin Endocrinol Metab 81:1261–1266PubMed


Kelly RW, Critchley HO (1997) Immunomodulation by human seminal plasma: a benefit for spermatozoon and pathogen? Hum Reprod 12:2200–2207PubMed


Keskin DB, Allan DSJ, Rybalov B, Andzelm MM, Stern JNH, Kopcow HD, Koopman LA, Strominger JL (2007) TGFβ promotes conversion of CD16+ peripheral blood NK cells into CD16- NK cells with similarities to decidual NK cells. Proc Natl Acad Sci USA 104:3378–3383PubMedCentralPubMed


King A, Loke YW (1990) Human trophoblast and JEG choriocarcinoma cells are sensitive to lysis by IL-2-stimulated decidual NK cells. Cell Immunol 129:435–448PubMed


King A, Wooding P, Gardner L, Loke YW (1993) Expression of perforin, granzyme A and TIA-1 by human uterine CD56+ NK cells implies they are activated and capable of effector functions. Hum Reprod 8:2061–2067PubMed


Kitaya K, Yasuo T (2010) Leukocyte density and composition in human cycling endometrium with uterine fibroids. Hum Immunol 71:158–163PubMed

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Oct 18, 2016 | Posted by in EMBRYOLOGY | Comments Off on The Role of Uterine NK Cells in Normal Reproduction and Reproductive Disorders
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