Recent advances in understanding immunology of reproductive failure

Journal of Reproductive Immunology

Volumn 90, Issue 1, 2011, Pages 96-104

  Makrigiannakis, Antonis ^a   Petsas, George ^a   Toth, Bettina ^b   Relakis, Konstantinos ^a   Jeschke, Udo ^c  

^a UNIVERSITY OF CRETE   (Greece)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c UNIVERSITY OF MUNICH   (Germany)

Author keywords

Cytokines; Fetomaternal interface; HLA; Immunology; Implantation; IVF; NK cells; Recurrent spontaneous abortion; Repeated implantation failure

Indexed keywords

CORTICOTROPIN RELEASING FACTOR; CYTOKINE;

ANTIGEN EXPRESSION; ARTICLE; FERTILIZATION IN VITRO; HLA SYSTEM; HUMAN; IMMUNOLOGICAL PARAMETERS; IMMUNOLOGY; IMPLANTATION; NATURAL KILLER CELL; PRIORITY JOURNAL; REPRODUCTION; SPONTANEOUS ABORTION; TH1 TH2 BALANCE;

ANIMALS; EMBRYO IMPLANTATION; FEMALE; FERTILIZATION IN VITRO; HUMANS; INFERTILITY; PREGNANCY; PREGNANCY COMPLICATIONS; PREGNANCY OUTCOME; REPRODUCTION;

EID: 79960022988     PISSN: 01650378     EISSN: 18727603     Source Type: Journal    
DOI: 10.1016/j.jri.2011.03.006     Document Type: Article

References (104)

1. Abbondanzo S.J., Cullinan E.B., McIntyre K., Labow M.A., Stewart C.L. Reproduction in mice lacking a functional type 1 IL1 receptor. Endocrinology 1996, 137:3598-3601.
2. Ashkar A.A., Black G.P., Wei Q., He H., Liang L., Head J.R., Croy B.A. Assessment of requirements for IL15 and IFN regulatory factors in uterine NK cell differentiation and function during pregnancy. J. Immunol. 2003, 171:2937-2944.
3. Bashirova A.A., Martin M.P., McVicar D.W., Carrington M. The killer immunoglobulin-like receptor gene cluster: tuning the genome for defense. Annu. Rev. Genomics Hum. Genet. 2006, 7:277-300.
4. Bates M.D., Quenby S., Takakuwa K., Johnson P.M., Vince G.S. Aberrant cytokine production by peripheral blood mononuclear cells in recurrent pregnancy loss?. Hum. Reprod. 2002, 17:2439-2444.
5. Beydoun H., Saftlas A.F. Association of human leucocyte antigen sharing with recurrent spontaneous abortions. Tissue Antigens 2005, 65:123-135.
6. Billington W.D. Influence of immunological dissimilarity of mother and foetus on size of placenta in mice. Nature 1964, 202:317-318.
7. Boomsma C.M., Kavelaars A., Eijkemans M.J., Lentjes E.G., Fauser B.C., Heijnen C.J., Macklon N.S. Endometrial secretion analysis identifies a cytokine profile predictive of pregnancy in IVF. Hum. Reprod. 2009, 24:1427-1435.
8. Borrego F., Ulbrecht M., Weiss E.H., Coligan J.E., Brooks A.G. Recognition of human histocompatibility leukocyte antigen (HLA)-E complexed with HLA class I signal sequence-derived peptides by CD94/NKG2 confers protection from natural killer cell-mediated lysis. J. Exp. Med. 1998, 187:813-818.
9. Bulmer J.N., Lash G.E. Human uterine natural killer cells: a reappraisal. Mol. Immunol. 2005, 42:511-521.
10. Chaouat G., Ledee-Bataille N., Dubanchet S., Zourbas S., Sandra O., Martal J. TH1/TH2 paradigm in pregnancy: paradigm lost? Cytokines in pregnancy/early abortion: reexamining the TH1/TH2 paradigm. Int. Arch. Allergy Immunol. 2004, 134:93-119.
11. Chen J.R., Cheng J.G., Shatzer T., Sewell L., Hernandez L., Stewart C.L. Leukemia inhibitory factor can substitute for nidatory estrogen and is essential to inducing a receptive uterus for implantation but is not essential for subsequent embryogenesis. Endocrinology 2000, 141:4365-4372.
12. 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.
13. Colonna M., Borsellino G., Falco M., Ferrara G.B., Strominger J.L. HLA-C is the inhibitory ligand that determines dominant resistance to lysis by NK1- and NK2-specific natural killer cells. Proc. Natl. Acad. Sci. U.S.A. 1993, 90:12000-12004.
14. Colonna M., Nakajima H., Cella M. Inhibitory and activating receptors involved in immune surveillance by human NK and myeloid cells. J. Leukoc. Biol. 1999, 66:718-722.
15. Cooper M.A., Fehniger T.A., Caligiuri M.A. The biology of human natural killer-cell subsets. Trends Immunol. 2001, 22:633-640.
16. Creus M., Balasch J., Fabregues F., Martorell J., Boada M., Penarrubia J., et al. Parental human leukocyte antigens and implantation failure after in-vitro fertilization. Hum. Reprod. 1998, 13:39-43.
17. Crncic T.B., Laskarin G., Frankovic K.J., Tokmadzic V.S., Strbo N., Bedenicki I., et al. Early pregnancy decidual lymphocytes beside perforin use Fas ligand (FasL) mediated cytotoxicity. J. Reprod. Immunol. 2007, 73:108-117.
18. Dey S.K., Lim H., Das S.K., Reese J., Paria B.C., Daikoku T., Wang H. Molecular cues to implantation. Endocr. Rev. 2004, 25:341-373.
19. Ernst M., Inglese M., Waring P., Campbell I.K., Bao S., Clay F.J., et al. Defective gp130-mediated signal transducer and activator of transcription (STAT) signaling results in degenerative joint disease, gastrointestinal ulceration, and failure of uterine implantation. J. Exp. Med. 2001, 194:189-203.
20. Faridi R.M., Das V., Tripthi G., Talwar S., Parveen F., Agrawal S. Influence of activating and inhibitory killer immunoglobulin-like receptors on predisposition to recurrent miscarriages. Hum. Reprod. 2009, 24:1758-1764.
21. Fasouliotis S.J., Spandorfer S.D., Witkin S.S., Schattman G., Liu H.C., Roberts J.E., Rosenwaks Z. Maternal serum levels of interferon-gamma and interleukin-2 soluble receptor-alpha predict the outcome of early IVF pregnancies. Hum. Reprod. 2004, 19:1357-1363.
22. Ferry B.L., Sargent I.L., Starkey P.M., Redman C.W. Cytotoxic activity against trophoblast and choriocarcinoma cells of large granular lymphocytes from human early pregnancy decidua. Cell. Immunol. 1991, 132:140-149.
23. 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.
24. Fukui A., Kwak-Kim J., Ntrivalas E., Gilman-Sachs A., Lee S.K., Beaman K. Intracellular cytokine expression of peripheral blood natural killer cell subsets in women with recurrent spontaneous abortions and implantation failures. Fertil. Steril. 2008, 89:157-165.
25. Fuzzi B., Rizzo R., Criscuoli L., Noci I., Melchiorri L., Scarselli B., et al. HLA-G expression in early embryos is a fundamental prerequisite for the obtainment of pregnancy. Eur. J. Immunol. 2002, 32:311-315.
26. Ginsburg E.S., Xiao L., Gargiulo A.R., Kung F.T., Politch J.A., Schust D.J., Hill J.A. T-helper 2 and 3 type immunity to trophoblast in successful in vitro fertilization-embryo transfer. Fertil. Steril. 2005, 83:1659-1664.
27. Hiby S.E., Regan L., Lo W., Farrell L., Carrington M., Moffett A. Association of maternal killer-cell immunoglobulin-like receptors and parental HLA-C genotypes with recurrent miscarriage. Hum. Reprod. 2008, 23:972-976.
28. Hill J.A., Polgar K., Anderson D.J. T-helper 1-type immunity to trophoblast in women with recurrent spontaneous abortion. J. Am. Med. Assoc. 1995, 273:1933-1936.
29. Hong Y., Wang X., Lu P., Song Y., Lin Q. Killer immunoglobulin-like receptor repertoire on uterine natural killer cell subsets in women with recurrent spontaneous abortions. Eur. J. Obstet. Gynecol. Reprod. Biol. 2008, 140:218-223.
30. Hunt J.S., Andrews G.K., Wood G.W. Normal trophoblasts resist induction of class I HLA. J. Immunol. 1987, 138:2481-2487.
31. Hunt J.S., Jadhav L., Chu W., Geraghty D.E., Ober C. Soluble HLA-G circulates in maternal blood during pregnancy. Am. J. Obstet. Gynecol. 2000, 183:682-688.
32. Hunt J.S., Petroff M.G., McIntire R.H., Ober C. HLA-G and immune tolerance in pregnancy. FASEB J. 2005, 19:681-693.
33. Inagaki N., Stern C., McBain J., Lopata A., Kornman L., Wilkinson D. Analysis of intra-uterine cytokine concentration and matrix-metalloproteinase activity in women with recurrent failed embryo transfer. Hum. Reprod. 2003, 18:608-615.
34. Ishitani A., Sageshima N., Lee N., Dorofeeva N., Hatake K., Marquardt H., Geraghty D.E. Protein expression and peptide binding suggest unique and interacting functional roles for HLA-E, F, and G in maternal-placental immune recognition. J. Immunol. 2003, 171:1376-1384.
35. Kalu E., Bhaskaran S., Thum M.Y., Vishwanatha R., Croucher C., Sherriff E., et al. Serial estimation of Th1:th2 cytokines profile in women undergoing in-vitro fertilization-embryo transfer. Am. J. Reprod. Immunol. 2008, 59:206-211.
36. King A., Burrows T.D., Hiby S.E., Bowen J.M., Joseph S., Verma S., et al. Surface expression of HLA-C antigen by human extravillous trophoblast. Placenta 2000, 21:376-387.
37. Kirby D.R. The egg and immunology. Proc. R. Soc. Med. 1970, 63:59-61.
38. Kulkarni A.B., Karlsson S. Transforming growth factor-beta 1 knockout mice. A mutation in one cytokine gene causes a dramatic inflammatory disease. Am. J. Pathol. 1993, 143:3-9.
39. Kwak-Kim J.Y., Chung-Bang H.S., Ng S.C., Ntrivalas E.I., Mangubat C.P., Beaman K.D., et al. Increased T helper 1 cytokine responses by circulating T cells are present in women with recurrent pregnancy losses and in infertile women with multiple implantation failures after IVF. Hum. Reprod. 2003, 18:767-773.
40. 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.
41. Le Bouteiller P. Commentary. Major breakthrough in the HLA-G debate: occurrence of pregnancy in human depends on the HLA-G status of preimplantation embryos. Eur. J. Immunol. 2002, 32:309-310.
42. Le Bouteiller P., Lenfant F. Antigen-presenting function(s) of the non-classical HLA-E-F and -G class I molecules: the beginning of a story. Res. Immunol. 1996, 147:301-313.
43. Le Bouteiller P., Legrand-Abravanel F., Solier C. Soluble HLA-G1 at the materno-foetal interface-a review. Placenta 2003, 24(Suppl. A):S10-S15.
44. Ledee-Bataille N., Bonnet-Chea K., Hosny G., Dubanchet S., Frydman R., Chaouat G. Role of the endometrial tripod interleukin-18-15, and -12 in inadequate uterine receptivity in patients with a history of repeated in vitro fertilization-embryo transfer failure. Fertil. Steril. 2005, 83:598-605.
45. Lee N., Llano M., Carretero M., Ishitani A., Navarro F., Lopez-Botet M., Geraghty D.E. HLA-E is a major ligand for the natural killer inhibitory receptor CD94/NKG2A. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:5199-5204.
46. Li X.F., Charnock-Jones D.S., Zhang E., Hiby S., Malik S., Day K., et al. Angiogenic growth factor messenger ribonucleic acids in uterine natural killer cells. J. Clin. Endocrinol. Metab. 2001, 86:1823-1834.
47. Lim K.J., Odukoya O.A., Ajjan R.A., Li T.C., Weetman A.P., Cooke I.D. Profile of cytokine mRNA expression in peri-implantation human endometrium. Mol. Hum. Reprod. 1998, 4:77-81.
48. Ljunggren H.G., Karre K. In search of the 'missing self': MHC molecules and NK cell recognition. Immunol. Today 1990, 11:237-244.
49. Loke Y.W., King A. Decidual natural-killer-cell interaction with trophoblast: cytolysis or cytokine production?. Biochem. Soc. Trans. 2000, 28:196-198.
50. Macklon N.S., Geraedts J.P., Fauser B.C. Conception to ongoing pregnancy: the 'black box' of early pregnancy loss. Hum. Reprod. Update 2002, 8:333-343.
51. Madhappan B., Kempuraj D., Christodoulou S., Tsapikidis S., Boucher W., Karagiannis V., et al. High levels of intrauterine corticotropin-releasing hormone, urocortin, tryptase, and interleukin-8 in spontaneous abortions. Endocrinology 2003, 144:2285-2290.
52. Makrigiannakis A., Margioris A.N., Le Goascogne C., Zoumakis E., Nikas G., Stournaras C., et al. Corticotropin-releasing hormone (CRH) is expressed at the implantation sites of early pregnant rat uterus. Life Sci. 1995, 57:1869-1875.
53. Makrigiannakis A., Zoumakis E., Margioris A.N., Stournaras C., Chrousos G.P., Gravanis A. Regulation of the promoter of the human corticotropin-releasing hormone gene in transfected human endometrial cells. Neuroendocrinology 1996, 64:85-92.
54. Makrigiannakis A., Margioris A.N., Chatzaki E., Zoumakis E., Chrousos G.P., Gravanis A. The decidualizing effect of progesterone may involve direct transcriptional activation of corticotrophin-releasing hormone from human endometrial stromal cells. Mol. Hum. Reprod. 1999, 5:789-796.
55. Makrigiannakis A., Margioris A.N., Zoumakis E., Stournaras C., Gravanis A. The transcription of corticotropin-releasing hormone in human endometrial cells is regulated by cytokines. Neuroendocrinology 1999, 70:451-459.
56. Makrigiannakis A., Zoumakis E., Kalantaridou S., Coutifaris C., Margioris A.N., Coukos G., et al. Corticotropin-releasing hormone promotes blastocyst implantation and early maternal tolerance. Nat. Immunol. 2001, 2:1018-1024.
57. Matteo M.G., Greco P., Rosenberg P., Mestice A., Baldini D., Falagario T., et al. Normal percentage of CD56bright natural killer cells in young patients with a history of repeated unexplained implantation failure after in vitro fertilization cycles. Fertil. Steril. 2007, 88:990-993.
58. Michimata T., Ogasawara M.S., Tsuda H., Suzumori K., Aoki K., Sakai M., et al. Distributions of endometrial NK cells, B cells, T cells, and Th2/Tc2 cells fail to predict pregnancy outcome following recurrent abortion. Am. J. Reprod. Immunol. 2002, 47:196-202.
59. Minas V., Jeschke U., Kalantaridou S.N., Richter D.U., Reimer T., Mylonas I., et al. Abortion is associated with increased expression of FasL in decidual leukocytes and apoptosis of extravillous trophoblasts: a role for CRH and urocortin. Mol. Hum. Reprod. 2007, 13:663-673.
60. Moffett A., Regan L., Braude P. Natural killer cells, miscarriage, and infertility. BMJ 2004, 329:1283-1285.
61. Moretta A., Vitale M., Bottino C., Orengo A.M., Morelli L., Augugliaro R., et al. P58 molecules as putative receptors for major histocompatibility complex (MHC) class I molecules in human natural killer (NK) cells. Anti-p58 antibodies reconstitute lysis of MHC class I-protected cells in NK clones displaying different specificities. J. Exp. Med. 1993, 178:597-604.
62. Navarro F., Llano M., Bellon T., Colonna M., Geraghty D.E., Lopez-Botet M. The ILT2(LIR1) and CD94/NKG2A NK cell receptors respectively recognize HLA-G1 and HLA-E molecules co-expressed on target cells. Eur. J. Immunol. 1999, 29:277-283.
63. Ng S.C., Gilman-Sachs A., Thaker P., Beaman K.D., Beer A.E., Kwak-Kim J. Expression of intracellular Th1 and Th2 cytokines in women with recurrent spontaneous abortion, implantation failures after IVF/ET or normal pregnancy. Am. J. Reprod. Immunol. 2002, 48:77-86.
64. Noci I., Fuzzi B., Rizzo R., Melchiorri L., Criscuoli L., Dabizzi S., et al. Embryonic soluble HLA-G as a marker of developmental potential in embryos. Hum. Reprod. 2005, 20:138-146.
65. Ntrivalas E.I., Bowser C.R., Kwak-Kim J., Beaman K.D., Gilman-Sachs A. Expression of killer immunoglobulin-like receptors on peripheral blood NK cell subsets of women with recurrent spontaneous abortions or implantation failures. Am. J. Reprod. Immunol. 2005, 53:215-221.
66. O'Callaghan C.A., Bell J.I. Structure and function of the human MHC class Ib molecules HLA-E, HLA-F and HLA-G. Immunol. Rev. 1998, 163:129-138.
67. Parham P. MHC class I molecules and KIRs in human history, health and survival. Nat. Rev. Immunol. 2005, 5:201-214.
68. Pazmany L., Mandelboim O., Vales-Gomez M., Davis D.M., Reyburn H.T., Strominger J.L. Protection from natural killer cell-mediated lysis by HLA-G expression on target cells. Science 1996, 274:792-795.
69. Piccinni M.P., Beloni L., Livi C., Maggi E., Scarselli G., Romagnani S. Defective production of both leukemia inhibitory factor and type 2 T-helper cytokines by decidual T cells in unexplained recurrent abortions. Nat. Med. 1998, 4:1020-1024.
70. Piccinni M.P., Scaletti C., Mavilia C., Lazzeri E., Romagnani P., Natali I., et al. Production of IL4 and leukemia inhibitory factor by T cells of the cumulus oophorus: a favorable microenvironment for pre-implantation embryo development. Eur. J. Immunol. 2001, 31:2431-2437.
71. Pietra G., Romagnani C., Falco M., Vitale M., Castriconi R., Pende D., et al. The analysis of the natural killer-like activity of human cytolytic T lymphocytes revealed HLA-E as a novel target for TCR alpha/beta-mediated recognition. Eur. J. Immunol. 2001, 31:3687-3693.
72. Pollard J.W., Hunt J.S., Wiktor-Jedrzejczak W., Stanley E.R. A pregnancy defect in the osteopetrotic (op/op) mouse demonstrates the requirement for CSF-1 in female fertility. Dev. Biol. 1991, 148:273-283.
73. Potts W.K., Manning C.J., Wakeland E.K. Mating patterns in seminatural populations of mice influenced by MHC genotype. Nature 1991, 352:619-621.
74. 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.
75. Quenby S., Nik H., Innes B., Lash G., Turner M., Drury J., Bulmer J. Uterine natural killer cells and angiogenesis in recurrent reproductive failure. Hum. Reprod. 2009, 24:45-54.
76. Raghupathy R., Makhseed M., Azizieh F., Hassan N., Al-Azemi M., Al-Shamali E. Maternal Th1- and Th2-type reactivity to placental antigens in normal human pregnancy and unexplained recurrent spontaneous abortions. Cell. Immunol. 1999, 196:122-130.
77. Raghupathy R., Makhseed M., Azizieh F., Omu A., Gupta M., Farhat R. Cytokine production by maternal lymphocytes during normal human pregnancy and in unexplained recurrent spontaneous abortion. Hum. Reprod. 2000, 15:713-718.
78. Rajagopalan S., Fu J., Long E.O. Cutting edge: induction of IFNgamma production but not cytotoxicity by the killer cell Ig-like receptor KIR2DL4 (CD158d) in resting NK cells. J. Immunol. 2001, 167:1877-1881.
79. Rebmann V., Switala M., Eue I., Schwahn E., Merzenich M., Grosse-Wilde H. Rapid evaluation of soluble HLA-G levels in supernatants of in vitro fertilized embryos. Hum. Immunol. 2007, 68:251-258.
80. Robb L., Li R., Hartley L., Nandurkar H.H., Koentgen F., Begley C.G. Infertility in female mice lacking the receptor for interleukin 11 is due to a defective uterine response to implantation. Nat. Med. 1998, 4:303-308.
81. Robertson S.A., Roberts C.T., Farr K.L., Dunn A.R., Seamark R.F. Fertility impairment in granulocyte-macrophage colony-stimulating factor-deficient mice. Biol. Reprod. 1999, 60:251-261.
82. Robertson S.A., Mau V.J., Young I.G., Matthaei K.I. The effect of interleukin-6 deficiency on implantation, fetal development and parturition in mice. Proc. Aust. Soc. Reprod. Biol. 2000, 31:97.
83. Robillard P.Y., Hulsey T.C., Dekker G.A., Chaouat G. Preeclampsia and human reproduction. An essay of a long term reflection. J. Reprod. Immunol. 2003, 59:93-100.
84. Recurrent Miscarriage Immunotherapy Trialists Group Worldwide collaborative observational study and meta-analysis on allogenic leukocyte immunotherapy for recurrent spontaneous abortion. Am. J. Reprod. Immunol. 1994, 32:55-72.
85. Saito S., Nishikawa K., Morii T., Enomoto M., Narita N., Motoyoshi K., Ichijo M. Cytokine production by CD16-CD56bright natural killer cells in the human early pregnancy decidua. Int. Immunol. 1993, 5:559-563.
86. Shimada S., Kato E.H., Morikawa M., Iwabuchi K., Nishida R., Kishi R., et al. No difference in natural killer or natural killer T-cell population, but aberrant T-helper cell population in the endometrium of women with repeated miscarriage. Hum. Reprod. 2004, 19:1018-1024.
87. Stewart C.L., Kaspar P., Brunet L.J., Bhatt H., Gadi I., Kontgen F., Abbondanzo S.J. Blastocyst implantation depends on maternal expression of leukaemia inhibitory factor. Nature 1992, 359:76-79.
88. Stirrat G.M. Recurrent miscarriage. Lancet 1990, 336:673-675.
89. Tabiasco J., Perrier d'Hauterive S., Thonon F., Parinaud J., Leandri R., Foidart J.M., et al. Soluble HLA-G in IVF/ICSI embryo culture supernatants does not always predict implantation success: a multicentre study. Reprod. Biomed. Online 2009, 18:374-381.
90. Tan B.K., Vandekerckhove P., Kennedy R., Keay S.D. Investigation and current management of recurrent IVF treatment failure in the UK. BJOG 2005, 112:773-780.
91. Thomas M.L., Harger J.H., Wagener D.K., Rabin B.S., Gill T.J. HLA sharing and spontaneous abortion in humans. Am. J. Obstet. Gynecol. 1985, 151:1053-1058.
92. Thum M.Y., Abdalla H.I., Bhaskaran S., Harden E.L., Ford B., Sumar N., et al. The relationship of systemic TNFα and IFNγ with IVF treatment outcome and peripheral blood NK cells. Am. J. Reprod. Immunol. 2007, 57:210-217.
93. Toder V., Fein A., Carp H., Torchinsky A. TNFα in pregnancy loss and embryo maldevelopment: a mediator of detrimental stimuli or a protector of the fetoplacental unit?. J. Assist. Reprod. Genet. 2003, 20:73-81.
94. Tuckerman E., Laird S.M., Prakash A., Li T.C. Prognostic value of the measurement of uterine natural killer cells in the endometrium of women with recurrent miscarriage. Hum. Reprod. 2007, 22:2208-2213.
95. van der Meer A., Lukassen H.G., van Lierop M.J., Wijnands F., Mosselman S., Braat D.D., Joosten I. Membrane-bound HLA-G activates proliferation and interferon-gamma production by uterine natural killer cells. Mol. Hum. Reprod. 2004, 10:189-195.
96. Varla-Leftherioti M., Spyropoulou-Vlachou M., Niokou D., Keramitsoglou T., Darlamitsou A., Tsekoura C., et al. Natural killer (NK) cell receptors' repertoire in couples with recurrent spontaneous abortions. Am. J. Reprod. Immunol. 2003, 49:183-191.
97. Varla-Leftherioti M., Keramitsoglou T., Spyropoulou-Vlachou M., Papadimitropoulos M., Kontopoulou-Antonopoulou V., Tsekoura C., et al. 14th International HLA and Immunogenetics Workshop: report from the reproductive immunology component. Tissue Antigens 2007, 69(Suppl. 1):297-303.
98. Vercammen M.J., Verloes A., van de Velde H., Haentjens P. Accuracy of soluble human leukocyte antigen-G for predicting pregnancy among women undergoing infertility treatment: meta-analysis. Hum. Reprod. Update 2008, 14:209-218.
99. Verma S., King A., Loke Y.W. Expression of killer cell inhibitory receptors on human uterine natural killer cells. Eur. J. Immunol. 1997, 27:979-983.
100. White C.A., Johansson M., Roberts C.T., Ramsay A.J., Robertson S.A. Effect of interleukin-10 null mutation on maternal immune response and reproductive outcome in mice. Biol. Reprod. 2004, 70:123-131.
101. Wu M.Y., Chen H.F., Chen S.U., Chao K.H., Yang Y.S., Ho H.N. Increase in the production of interleukin-10 early after implantation is related to the success of pregnancy. Am. J. Reprod. Immunol. 2001, 46:386-392.
102. Yan W.-H., Lin A., Chen B.-G., Zhou M.-Y., Dai M.-Z., Chen X.-J., et al. Possible roles of KIR2DL4 expression on uNK cells in human pregnancy. Am. J. Reprod. Immunol. 2007, 57:233-242.
103. Zheng H., Fletcher D., Kozak W., Jiang M., Hofmann K.J., Conn C.A., et al. Resistance to fever induction and impaired acute-phase response in interleukin-1 beta-deficient mice. Immunity 1995, 3:9-19.
104. Zoumakis E., Margioris A.N., Stournaras C., Dermitzaki E., Angelakis E., Makrigiannakis A., et al. Corticotrophin-releasing hormone (CRH) interacts with inflammatory prostaglandins and interleukins and affects the decidualization of human endometrial stroma. Mol. Hum. Reprod. 2000, 6:344-351.