Accumulation of Uterine CD16(−) Natural Killer (NK) Cells: Friends, Foes, or Jekyll-and-Hyde Relationship for the Conceptus?

REFERENCES

• Appenheimer M. M., Chen Q., Girard R. A., Wang W. C., Evans S. S. Impact of fever-range thermal stress on lymphocyte-endothelial adhesion and lymphocyte trafficking. Immunol. Invest. 2005; 34: 295–323
   PubMed Web of Science ®Google Scholar
• Arck P. C., Hertwig K., Hagen E., Hildebrandt M., Klapp B. F. Pregnancy as a model of controlled invasion might be attributed to the ratio of CD3/CD8 to CD56. Am. J. Reprod. Immunol. 2000; 44: 1–8
   Google Scholar
• Bulanova E., Budagian V., Duitman E., Orinska Z., Krause H., Rückert R., Reiling N., Bulfone-Paus S. Soluble Interleukin IL-15Rα is generated by alternative splicing or proteolytic cleavage and forms functional complexes with IL-15. J. Biol. Chem. 2007; 282: 13167–13179
   PubMed Web of Science ®Google Scholar
• Clifford K., Flanagan A. M., Regan L. Endometrial CD56+ natural killer cells in women with recurrent miscarriage: a histomorphometric study. Hum. Reprod. 1999; 14: 2727–2730
   PubMed Web of Science ®Google Scholar
• Croy B. A., van den Heuvel M. J., Borzychowski A. M., Tayade C. Uterine natural killer cells: a specialized differentiation regulated by ovarian hormones. Immunol. Rev. 2006; 214: 161–185
   PubMed Web of Science ®Google Scholar
• Drake P. M., Gunn M. D., Charo I. F., Tsou C. L., Zhou Y., Huang L., Fisher S. J. Human placental cytotrophoblasts attract monocytes and CD56bright natural killer cells via the actions of monocyte inflammatory protein-1α. J. Exp. Med. 2001; 193: 1199–1212
   PubMed Web of Science ®Google Scholar
• Dwir O., Solomon A., Mangan S., Kansas G. S., Schwarz U. S., Alon R. Avidity enhancement of L-selectin bonds by flow: shearpromoted rotation of leukocytes turn labile bonds into functional tethers. J. Cell. Biol. 2003; 163: 649–659
   PubMed Web of Science ®Google Scholar
• Eide I. P., Rolfseng T., Isaksen C. V., Mecsei R., Roald B., Lydersen S., Salvesen K. A., Harsem N. K., Austgulen R. Serious foetal growth restriction is associated with reduced proportions of natural killer cells in decidua basalis. Virchows. Arch. 2006; 448: 269–276
   PubMed Web of Science ®Google Scholar
• Fehniger T. A., Cooper M. A., Nuovo G. J., Cella M., Facchetti F., Colonna M., Caligiuri M. A. CD56bright natural killer cells are present in human lymph nodes and are activated by T cell-derived IL-2: a potential new link between adaptive and innate immunity. Blood 2003; 101: 3052–3057
   PubMed Web of Science ®Google Scholar
• Frey M., Packianathan N. B., Fehniger T. A., Ross M. E., Wang W. C., Stewart C. C., Caligiuri M. A., Evans S. S. Differential expression and function of L-selectin on CD56bright and CD56dim natural killer cell subsets. J. Immunol. 1998; 161: 400–408
   PubMed Web of Science ®Google Scholar
• Fukui A., Fujii S., Yamaguchi E., Kimura H., Sato S., Saito Y. Natural killer cell subpopulations and cytotoxicity for infertile patients undergoing in vitro fertilization. Am. J. Reprod. Immunol. 1999; 41: 413–422
   PubMed Web of Science ®Google Scholar
• Goldsmith H. L., Cokelet G. R., Gaehtgens P. Robin Fåhraeus: evolution of his concepts in cardiovascular physiology. Am. J. Physiol. 1989; 257: H1005–1015
   Google Scholar
• Goodell M. A., Brose K., Paradis G., Conner A. S., Mulligan R. C. Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J. Exp. Med. 1996; 183: 1797–1806
   PubMed Web of Science ®Google Scholar
• Guimond M. J., Wang B., Croy B. A. Engraftment of bone marrow from severe combined immunodeficient (SCID) mice reverses the reproductive deficits in natural killer cell-deficient tgε26 mice. J. Exp. Med. 1998; 187: 217–223
   PubMed Web of Science ®Google Scholar
• Hameed A., Fox W. M., Kurman R. J., Hruban R. H., Podack E. R. Perforin expression in endometrium during the menstrual cycle. In.t J. Gynecol. Pathol. 1995; 14: 143–150
   Google Scholar
• Hanna J., Wald O., Goldman-Wohl D., Prus D., Markel G., Gazit R., Katz G., Haimov-Kochman R., Fujii N., Yagel S., Peled A., Mandelboim O. CXCL12 expression by invasive trophoblasts induces the specific migration of CD16- human natural killer cells. Blood 2003; 102: 1569–1577
   PubMed Web of Science ®Google Scholar
• Hickey M., Crewe J., Goodridge J. P., Witt C. S., Fraser I. S., Doherty D., Christiansen F. T., Salamonsen L. A. Menopausal hormone therapy and irregular endometrial bleeding: a potential role for uterine natural killer cells?. J. Clin. Endocrinol. Metab. 2005; 90: 5528–5535
   Google Scholar
• Jones R. K., Bulmer J. N., Searle R. F. Cytotoxic activity of endometrial granulated lymphocytes during the menstrual cycle in humans. Biol. Reprod. 1997; 57: 1217–1222
   Google Scholar
• Jones R. L., Morison N. B., Hannan N. J., Critchley H. O., Salamonsen L. A. Chemokine expression is dysregulated in the endometrium of women using progestin-only contraceptives and correlates to elevated recruitment of distinct leukocyte populations. Hum. Reprod. 2005; 20: 2724–2735
   Google Scholar
• Kämmerer U., Marzusch K., Kröber S., Ruck P., Handgretinger R., Dietl J. A subset of CD56+ large granular lymphocytes in first-trimester human decidua are proliferating cells. Fertil. Steril. 1999; 71: 74–79
   Google Scholar
• Kämmerer U., Rieger L., Kapp M., Dietl J., Ruck P. Immunocompetent cells in the endometrium of fetuses and children. Hum. Reprod. 2003; 18: 969–975
   Google Scholar
• Kato K., Yoshimoto M., Kato K., Adachi S., Yamayoshi A., Arima T., Asanoma K., Kyo S., Nakahata T., Wake N. Characterization of side-population cells in human normal endometrium. Hum. Reprod. 2007; 22: 1214–1223
   PubMed Web of Science ®Google Scholar
• Keskin D. B., Allan D. S., Rybalov B., Andzelm M. M., Stern J. N., Kopcow H. D., Koopman L. A., Strominger J. L. TGFβ promotes conversion of CD16+ peripheral blood NK cells into CD16- NK cells with similarities to decidual NK cells. Proc. Natl. Acad. Sci. USA 2007; 104: 3378–3383
   PubMed Web of Science ®Google Scholar
• Khan A. I., Landis R. C., Malhotra R. L-selectin ligands in lymphoid tissues and models of inflammation. Inflammation 2003; 27: 265–280
   PubMedGoogle Scholar
• King A., Balendran N., Wooding P., Carter N. P., Loke Y. W. CD3- leukocytes present in the human uterus during early placentation: phenotypic and morphologic characterization of the CD56++ population. Dev. Immunol. 1991; 1: 169–190
   PubMedGoogle Scholar
• Kitaya K., Yasuda J., Nakayama T., Fushiki S., Honjo H. Effect of female sex steroids on human endometrial CD16neg CD56bright natural killer cells. Fertil. Steril. 2003; 79(Suppl 1)730–734
   PubMedGoogle Scholar
• Kitaya K., Yamaguchi T., Honjo H. Central role of interleukin-15 in postovulatory recruitment of peripheral blood CD16(−) natural killer cells into human endometrium. J. Clin. Endocrinol. Metab. 2005; 90: 2932–2940
   PubMed Web of Science ®Google Scholar
• Kitaya K., Yasuo T., Yamaguchi T., Fushiki S., Honjo H. Genes regulated by interferon-γ in human uterine microvascular endothelial cells. Int. J. Mol. Med. 2007a; 20: 689–697
   Google Scholar
• Kitaya K., Yamaguchi T., Yasuo T., Okubo T., Honjo H. Post-ovulatory rise of endometrial CD16(−) natural killer cells: in situ proliferation of residual cells or selective recruitment from circulating peripheral blood?. J. Reprod. Immunol. 2007b; 76: 45–53
   Google Scholar
• Knoeller S., Lim E., Aleta L., Hertwig K., Dudenhausen J. W., Arck P. C. Distribution of immunocompetent cells in decidua of controlled and uncontrolled (choriocarcinoma/hydatidiform mole) trophoblast invasion. Am. J. Reprod. Immunol. 2003; 50: 41–47
   PubMed Web of Science ®Google Scholar
• Kopcow H. D., Allan D. S. J., Chen X., Rybalov B., Andzelm M. M., Ge B., Strominger J.L. Human decidual NK cells form immature activating synapses and are not cytotoxic. Proc. Natl. Acad. Sci. USA 2005; 102: 15563–15568
   PubMedGoogle Scholar
• Kopcow H. D., Karumanchi S. A. Angiogenic factors and natural killer (NK) cells in the pathogenesis of preeclampsia. J. Reprod. Immunol. 2007; 76: 23–29
   PubMed Web of Science ®Google Scholar
• Lachapelle M. H., Miron P., Hemmings R., Roy D. C. Endometrial T, B and NK cells in patients with recurrent spontaneous abortion: altered profile and pregnancy outcome. J. Immunol. 1996; 156: 4027–4034
   PubMed Web of Science ®Google Scholar
• Lima M., Teixeira M. A., Queirós M. L., Leite M., Santos A. H., Justiça B., Orfão A. Immunophenotypic characterization of normal blood CD56+lo versus CD56+hi NK-cell subsets and its impact on the understanding of their tissue distribution and functional properties. Blood Cells Mol. Dis. 2001; 27: 731–743
   PubMed Web of Science ®Google Scholar
• Manastera I., Mandelboim O. The unique properties of human NK cells in the uterine mucosa. Placenta 2008, Suppl A: S60–S66
   Google Scholar
• Pijnenborg R., Vercruysse L., Hanssens M. The uterine spiral arteries in human pregnancy: facts and controversies. Placenta 2006; 27: 939–958
   PubMed Web of Science ®Google Scholar
• Pröll J., Bensussan A., Goffin F., Foidart J. M., Berrebi A., Le Bouteiller P. Tubal versus uterine placentation: similar HLA-G expressing extravillous cytotrophoblast invasion but different maternal leukocyte recruitment. Tissue Antigens 2000; 56: 479–491
   PubMed Web of Science ®Google Scholar
• Quenby S., Bates M., Doig T., Brewster J., Lewis-Jones D. I., Johnson P. M., Vince G. Pre-implantation endometrial leukocytes in women with recurrent miscarriage. Hum. Reprod. 1999; 14: 2386–2391
   PubMed Web of Science ®Google Scholar
• Quenby S., Kalumbi C., Bates M., Farquharson R., Vince G. Prednisolone reduces preconceptual endometrial natural killer cells in women with recurrent miscarriage. Fertil. Steril. 2005; 84: 980–984
   PubMed Web of Science ®Google Scholar
• Rieger L., Hofmeister V., Probe C., Dietl J., Weiss E. H., Steck T., Kämmerer U. Th1- and Th2-like cytokine production by first trimester decidual large granular lymphocytes is influenced by HLA-G and HLA-E. Mol. Hum. Reprod. 2002; 8: 255–261
   Google Scholar
• Saito S., Sakai M., Sasaki Y., Nakashima A., Shiozaki A. Inadequate tolerance induction may induce pre-eclampsia. J. Reprod. Immunol. 2007; 76: 30–39
   PubMed Web of Science ®Google Scholar
• Sargent I. L., Borzychowski A. M., Redman C. W. G. NK cells and pre-eclampsia. J. Reprod. Immunol. 2007; 76: 40–44
   PubMed Web of Science ®Google Scholar
• Taylor H. S. Endometrial cells derived from donor stem cells in bone marrow transplant recipients. JAMA 2004; 292: 81–85
   PubMed Web of Science ®Google Scholar
• Thathiah A., Blobel C. P., Carson D. D. Tumor necrosis factor-α converting enzyme/ADAM 17 mediates MUC1 shedding. J. Biol. Chem. 2003; 278: 3386–3394
   PubMed Web of Science ®Google Scholar
• van den Heuvel M. J., Chantakru S., Xie X., Evans S. S., Tekpetey F., Mote P. A., Clarke C. L., Croy B. A. Trafficking of circulating pro-NK cells to the decidualizing uterus: regulatory mechanisms in the mouse and human. Immunol. Invest. 2005; 34: 273–293
   PubMed Web of Science ®Google Scholar
• Verma S., Hiby S. E., Loke Y. W., King A. Human decidual natural killer cells express the receptor for and respond to the cytokine interleukin 15. Biol. Reprod. 2000; 62: 959–968
   PubMed Web of Science ®Google Scholar
• von Rango U., Classen-Linke I., Kertschanska S., Kemp B., Beier H. M. Effects of trophoblast invasion on the distribution of leukocytes in uterine and tubal implantation sites. Fertil Steril. 2001; 76: 116–124
   PubMed Web of Science ®Google Scholar
• Wilczyński J. R., Tchórzewski H., Banasik M., Głowacka E., Wieczorek A., Lewkowicz P., Malinowski A., Szpakowski M., Wilczynski J. Lymphocyte subset distribution and cytokine secretion in third trimester decidua in normal pregnancy and preeclampsia. Eur. J. Obstet. Gynecol. Reprod. Biol. 2003; 109: 8–15
   PubMed Web of Science ®Google Scholar
• Yamaguchi T., Kitaya K., Daikoku N., Yasuo T., Fushiki S., Honjo H. Potential selectin L ligands involved in selective recruitment of peripheral blood CD16(-) natural killer cells into human endometrium. Biol. Reprod. 2006; 74: 35–40
   Google Scholar
• Yasuo T., Kitaya K., Yamaguchi T., Fushiki S., Honjo H. Possible role of hematopoietic CD44/chondroitin sulfate interaction in extravasation of peripheral blood CD16(-) natural killer cells into human endometrium. J. Reprod. Immunol. 2008; 78: 1–10
   Google Scholar
• Yeaman GR., Collins J. E., Currie J. K., Guyre P. M., Wira C. R., Fanger M. W. IFN-γ is produced by polymorphonuclear neutrophils in human uterine endometrium and by cultured peripheral blood polymorphonuclear neutrophils. J. Immunol. 1998; 160: 5145–5153
   Google Scholar
• Zhou S., Schuetz J. D., Bunting K. D., Colapietro A. M., Sampath J., Morris J. J., Lagutina I., Grosveld G. C., Osawa M., Nakauchi H., Sorrentino B. P. The ABC transporter Bcrp1/ABCG2 is expressed in a wide variety of stem cells and is a molecular determinant of the side-population phenotype. Nat. Med. 2001; 7: 1028–1034
   PubMed Web of Science ®Google Scholar
• Zhou Y., Fisher S. J., Janatpour M., Genbacev O., Dejana E., Wheelock M., Damsky C. H. Human cytotrophoblasts adopt a vascular phenotype as they differentiate. A strategy for successful endovascular invasion?. J. Clin. Invest. 1997; 99: 2139–2151
   PubMed Web of Science ®Google Scholar