Uterine natural killer cells: A specialized differentiation regulated by ovarian hormones

Immunological Reviews

Volumn 214, Issue 1, 2006, Pages 161-185

  Anne Croy, B ^a   Van Den Heuvel, Marianne J ^b   Borzychowski, Angela M ^c   Tayade, Chandrakant ^d  

^a QUEEN S UNIVERSITY   (Canada)

^b UNIVERSITY OF WESTERN ONTARIO   (Canada)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d UNIVERSITY OF GUELPH   (Canada)

Author keywords

Angiogenesis; Endometrium; Natural killer cell; Placenta; Pregnancy; Trophoblast

Indexed keywords

HORMONE; VASOACTIVE AGENT;

ABORTION; ANGIOGENESIS; ARTERIAL BLOOD; CELL ACTIVATION; CELL DIFFERENTIATION; CELL FUNCTION; CYTOKINE PRODUCTION; CYTOLOGY; ENDOMETRIUM; FETUS WASTAGE; HUMAN; LYMPHOCYTE; LYMPHOID ORGAN; MATERNAL BLOOD; NATURAL KILLER CELL; NONHUMAN; PLACENTA DEVELOPMENT; PREGNANCY; PRESSURE MEASUREMENT; PRIORITY JOURNAL; REVIEW; RODENT; SWINE;

ANIMALS; CELL DIFFERENTIATION; FEMALE; GONADAL HORMONES; HUMANS; KILLER CELLS, NATURAL; OVARY; UTERUS;

EID: 33750695267     PISSN: 01052896     EISSN: 1600065X     Source Type: Journal    
DOI: 10.1111/j.1600-065X.2006.00447.x     Document Type: Review

References (253)

1. Austin CR, Short RV, eds. Reproduction in Mammals, 2nd edn. Cambridge: Cambridge University Press, 1984.
2. Dyce KM, Sack WO, Wensing CJG. Textbook of Veterinary Anatomy, 2nd edn. Philadelphia: W.B. Saunders Co., 1996:208.
3. Heap RB, Galil AK, Harrion FA, Jenkin G, Perry JS. Progesterone and oestrogen in pregnancy and parturition: comparative aspects and hierarchical control. Ciba Found Symp 1977;47:127-157.
4. Staples LD, Heap RB, Wooding FBP, King GJ. Migration of leukocytes into the uterus after acute removal of ovarian progesterone during early-pregnancy in the sheep. Placenta 1983;4:339-349.
5. Tanaka S, Kunath T, Hadjantonakis AK, Nagy A, Rossant J. Promotion of trophoblast stem cell proliferation by FGF4. Science 1998;282:2072-2075.
6. Spencer TE, Burghardt RC, Johnson GA, Bazer FW. Conceptus signals for establishment and maintenance of pregnancy. Anim Reprod Sci 2004;82-83:537-550.
7. Chen JR, Cheng JG, Shatzer T, Sewell L, Hernander L, Stewart CL. 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.
8. White CA, Robb L, Salamonsen LA. Uterine extracellular matrix components are altered during defective decidualization in interleukin-11 receptor alpha deficient mice. Reprod Biol Endocrinol 2004;2:76.
9. Genbacev OD, et al. Trophoblast L-selectin-mediated adhesion at the maternal-fetal interface. Science 2003;299:405-408.
10. Simister NE. Placental transport of immunoglobulin G. Vaccine 2003;21:3365-3369.
11. Butler JE, et al. Antibody repertoire development in fetal and neonatal piglets. IV. Switch recombination, primarily in fetal thymus, occurs independent of environmental antigen and is only weakly associated with repertoire diversification. J Immunol 2001;167:3239-3249.
12. Leiser R, Kaufmann P. Placental Structure - in a comparative aspect. Exp Clin Endocrinol 1994;102:122-134.
13. Loke YW, King A. Human Implantation: Cell Biology and Immunology. Cambridge: Cambridge University Press, 1995.
14. Lindheimer MD, Roberts JM, Cunningham FGE. Chesley's Hypertensive Disorders in Pregnancy, 2nd edn. Stamford: Appleton & Lange, 1999.
15. Thoresen M, Walloe L. Rapid changes in arterial blood-flow in humans measured non-invasively by an ultrasonic doppler-velocimeter. Acta Physiol Scand 1979;105:A2-A3.
16. Thaler I, Manor D, Rottem S, Timortritsch IE, Brandes JM, Itskovitz J. Hemodynamic evaluation of the female pelvic vessels using a high-frequency transvaginal image-directed doppler system. J Clin Ultrasound 1990;18:364-369.
17. Stewart IJ. Granulated metrial gland cells in 'minor' species. J Reprod Immunol 1998;40:129-146.
18. Peel S. Granulated metrial gland cells. Adv Anat Embryol Cell Biol 1989; 115:1-112.
19. Eizirik E, Murphy WJ, O'Brien SJ. Molecular dating and biogeography of the early placental mammal radiation. J Hered 2001;92:212-219.
20. Wildman DE, Chen C, Erez O, Grossman LI, Goodman M, Romero R. Evolution of the mammalian placenta revealed by phylogenetic analysis. Proc Natl Acad Sci USA 2006;103:3203-3208.
21. Vogel P. The current molecular phylogeny of eutherian mammals challenges previous interpretations of placental evolution. Placenta 2005;26:591-596.
22. Haig D. Gestational drive and the green-bearded placenta. Proc Natl Acad Sci USA 1996;93:6547-6551.
23. Koopman LA, et al. Human decidual natural killer cells are a unique NK cell subset with immunomodulatory potential. J Exp Med 2003;198:1201-1212.
24. Trundley A, Moffett A. Human uterine leukocytes and pregnancy. Tissue Antigens 2004;63:1-12.
25. Short RV. Human reproduction in an evolutionary context. Ann NY Acad Sci 1994;709:416-425.
26. Norwitz ER, Schust DJ, Fisher SJ. Mechanisms of disease - implantation and the survival of early pregnancy. N Engl J Med 2001;345:1400-1408.
27. Martin JA, Hamilton BE, Sutton PD, Ventura SJ, Menacker F, Munson ML Births: Final Data for 2003. Hyattsville: National Vital Statistics Reports, Center for Disease Control 2005; 54.
28. Medawar PB. Some immunological and endocrinological problems raised by viviparity in vertebrates. Symp Soc Exp Biol 1953;7:320-338.
29. Barker DJ. Fetal programming of coronary heart disease. Trends Endocrinol Metab 2002;13:364-368.
30. Holt RI. Fetal programming of the growth hormone-insulin-like growth factor axis. Trends Endocrinol Metab 2002;13:392-397.
31. Smith GCS, Pell JP, Walsh D. Pregnancy complications and maternal risk of ischaemic heart disease: a retrospective cohort study of 129,290 births. Lancet 2001;357:2002-2006.
32. Himmelmann A, Svensson A, Hansson L. Blood-pressure and left-ventricular mass in children with different maternal histories of hypertension - the hypertension in pregnancy offspring study. J Hypertens 1993;11:263-268.
33. Vatten LJ, Romundstad PR, Holmen TL, Hseih CC, Trichopoulos D, Stuver SO. Intrauterine exposure to preeclampsia and adolescent blood pressure, body size, and age at menarche in female offspring. Obstet Gynecol 2003;101:529-533.
34. Williams D. Pregnancy: a stress test for life. Curr Opin Obstet Gynecol 2003;15:465-471.
35. Seidman DS, Laor A, Gale R, Stevenson DK, Mashiach I, Danon YL. Pre-eclampsia and offspring's blood pressure, cognitive ability and physical development at 17-years-of-age. Br J Obstet Gynaecol 1991;98:1009-1014.
36. Allen VM, Wilson RD, Cheung A. Pregnancy outcomes after assisted reproductive technology. J Obstet Gynecol Can 2006;173:220-233.
37. Shanner L, Nisker J. Bioethics for clinicians. 26. Assisted reproductive technologies. Can Med Assoc J 2001;164:1589-1594.
38. Nyboe Andersen A, Erb K. Register data on assisted reproductive technology (ART) in Europe including a detailed description of ART in Denmark. Int J Androl 2006;29:12-16.
39. Bulmer JN, Lash GE. Human uterine natural killer cells: a reappraisal. Mol Immunol 2005;42:511-521.
40. Croy BA. Hasn't the time come to replace the term metrial gland? J Reprod Immunol 1999;42:127-129.
41. Parr EL, Young LHY, Parr MB, Young JDE. Granulated metrial gland cells of pregnant mouse uterus are natural killer-like cells that contain perforin and serine esterases. J Immunol 1990;145:2365-2372.
42. Parr EL, Parr MB, Zheng LM, Young JDE. Mouse granulated metrial gland-cells originate by local activation of uterine natural-killer lymphocytes. Biol Reprod 1991;44:834-841.
43. Gambel P, Croy BA, Moore WD, Hunziker RD, Wegmann TG, Rossant J. Characterization of immune effector cells present in early murine decidua. Cell Immunol 1985;93:303-314.
44. Croy BA, Gambel P, Rossant J, Wegmann TG. Characterization of murine decidual natural killer (NK) cells and their relevance to the success of pregnancy. Cell Immunol 1985;93:315-326.
45. Guimond MJ, Wang B, Croy BA. Engraftment of bone marrow from severe combined immunodeficient (SCID) mice reverses the reproductive deficits in natural killer cell-deficient Tg epsilon 26 mice. J Exp Med 1998;187:217-223.
46. Zheng LM, Joag SV, Parr MB, Parr EL, Young JDE. Perforin-expressing granulated metrial gland cells in murine deciduoma. J Exp Med 1991;174:1221-1226.
47. Martel D, Monier MN, Roche D, Defeo VJ, Psychoyos A. Hormonal dependence of the metrial gland - further studies on estradiol and progesterone-receptor levels in the rat. J Endocrinol 1989;120:465-472.
48. Kruse A, Martens N, Fernekorn U, Hallmann R, Butcher EC. Alterations in the expression of homing-associated molecules at the maternal/fetal interface during the course of pregnancy. Biol Reprod 2002;66:333-345.
49. Psychoyos A. La reaction deciduale est precedee de modifications precoces de la permeabilitee capillaire de l'uterus. C R Soc Biol (Paris) 1960;154:1384-1387.
50. Bany BM, Cross JC. Post-implantation mouse conceptuses produce paracrine signals that regulate the uterine endometrium undergoing decidualization. Dev Biol 2006;294:445-456.
51. Delgado SR, McBey BA, Yamashiro S, Fujita J, Kiso Y, Croy BA. Accounting for the peripartum loss of granulated metrial gland cells, a natural killer cell population, from the pregnant mouse uterus. J Leukoc Biol 1996;59:262-269.
52. Paffaro VA Jr, Bizinotto MC, Joazeiro PP, Yamada AT. Subset classification of mouse uterine natural killer cells by DBA lectin reactivity. Placenta 2003;24:479-488.
53. Mason LH, Ortaldo JR, Young HA, Kumar V, Bennett M, Anderson SK. Cloning and functional-characteristics of murine large granular lymphocyte-1 - a member of the Ly-49 gene family (Ly-49G2). J Exp Med 1995;182:293-303.
54. Stewart IJ, Webster AJ. Lectin histochemical studies of mouse granulated metrial gland cells. Histochem J 1997;29:885-892.
55. Schofield G, Kimber SJ. Leukocyte subpopulations in the uteri of leukemia inhibitory factor knockout mice during early pregnancy. Biol Reprod 2005;72:872-878.
56. Kiso Y, McBey BA, Mason L, Croy BA. Histological assessment of the mouse uterus from birth to puberty for the appearance of LGL-1+ natural killer cells. Biol Reprod 1992;47:227-232.
57. Croy BA, Kiso Y. Granulated metrial gland cells: a natural killer cell subset of the pregnant murine uterus. Microsc Res Tech 1993;25:189-200.
58. Croy BA, et al. Histological studies of gene-ablated mice support important functional roles for natural killer cells in the uterus during pregnancy. J Reprod Immunol 1997;35:111-133.
59. Parr EL, Parr MB. Localization of perforin in granulated metrial gland-cells. Am J Reprod Immunol 1987;14:9.
60. Zheng LM, et al. Immunogold labeling of perforin and serine esterases in granulated metrial gland cells. FASEB J 2006;5:79-85.
61. Kiso Y, Yoshizawa M, Wilson JA, McBey BA, Croy BA. Immunohistochemical analysis of beta 1-integrin receptors displayed by murine uterine natural killer cells over the course of successful pregnancy. J Reprod Immunol 1994;27:213-225.
62. Runkel F, et al. Grey, a novel mutation in the murine Lyst gene, causes the beige phenotype by skipping of exon 25. Mamm Genome 2006;17:203-210.
63. Ashkar AA, di Santo JP, Croy BA. Interferon gamma contributes to initiation of uterine vascular modification, decidual integrity, and uterine natural killer cell maturation during normal murine pregnancy. J Exp Med 2000;192:259-270.
64. Chantakru S, Kuziel WA, Maeda N, Croy BA. A study on the density and distribution of uterine natural killer cells at mid-pregnancy in mice genetically-ablated for CCR2, CCR5 and the CCR5 ligand MIP-1 alpha. J Reprod Immunol 2001;49:33-47.
65. Croy BA. Granulated metrial gland cells: hypotheses concerning possible functions during murine gestation. J Reprod Immunol 1994;27:85-94.
66. Farnsworth RL, Talamantes F. Calcyclin in the mouse decidua: expression and effects on placental lactogen secretion. Biol Reprod 1998;59:546-552.
67. Ain R, Tash JS, Soares MJ. Prolactin-like protein-A is a functional modulator of natural killer cells at the maternal-fetal interface. Mol Cell Endocrinol 2003;204:65-74.
68. Zhang JH, He H, Borzychowski AM, Takeda K, Akira S, Croy BA. Analysis of cytokine regulators inducing interferon production by mouse uterine natural killer cells. Biol Reprod 2003;69:404-411.
69. Guimond MJ, Luross, JA, Wang B, Terhost C, Croy, BA. Absence of natural killer cells during murine pregnancy is associated with reproductive compromise in TgE26 mice. Biol Reprod 1997;56:169-179.
70. Ashkar AA, et al. Assessment of requirements for IL-15 and IFN regulatory factors in uterine NK cell differentiation and function during pregnancy. J Immunol 2003;171:2937-2944.
71. Greenwood JD, Minhas K, di Santo JP, Makita M, Kiso Y, Croy BA. Ultrastructural studies of implantation sites from mice deficient in uterine natural killer cells. Placenta 2000;21:693-702.
72. Cipolla MJ, Binder ND, Osol G. Myoendometrial versus placental uterine arteries: structural, mechanical, and functional differences in late-pregnant rabbits. Am J Obstet Gynecol 1997;177:215-221.
73. Coultas L, Chawengsaksophak K, Rossant J. Endothelial cells and VEGF in vascular development. Nature 2005;438:937-945.
74. Rieben R, Seebach JD. Xenograft rejection: IgG(1), complement and NK cells team up to activate and destroy the endothelium. Trends Immunol 2005;26:2-5.
75. Costa C, Barber DF, Fodor WL. Human NK cell-mediated cytotoxicity triggered by CD86 and Gal alpha 1,3-Gal is inhibited in genetically modified porcine cells. J Immunol 2002;168:3808-3816.
76. Langer N, Beach D, Lindenbaum ES. Novel hyperactive mitogen to endothelial cells: human decidual NKG5. Am J Reprod Immunol 1999;42:263-272.
77. Hirschi KK, Rohovsky SA, D'Amore PA. PDGF, TGF-beta, and heterotypic cell-cell interactions mediate endothelial cell-induced recruitment of 10T1/2 cells and their differentiation to a smooth muscle fate. J Cell Biol 1998;141:805-814.
78. Croy BA, Ashkar AA, Minhas K, Greenwood JD. Can murine uterine natural killer cells give insights into the pathogenesis of preeclampsia? J Soc Gynecol Investig 2000;7:12-20.
79. Ashkar AA, Croy BA. Interferon-gamma contributes to the normalcy of murine pregnancy. Biol Reprod 1999;61:493-502.
80. Borzychowski AM, et al. Functional analysis of murine uterine natural killer cells genetically devoid of oestrogen receptors. Placenta 2003;24:403-411.
81. Ismail PM, Li J, Demayo FJ, O'Malley BW, Lydon JP. A novel LacZ reporter mouse reveals complex regulation of the progesterone receptor promoter during mammary gland development. Mol Endocrinol 2002;16:2475-2489.
82. Ehring GR, et al. A nongenomic mechanism for progesterone-mediated immunosuppression: inhibition of K+ channels, Ca2+ signaling, and gene expression in T lymphocytes. J Exp Med 1998;188:1593-1602.
83. Nakahira M, et al. Synergy of IL-12 and IL-18 for IFN-gamma gene expression: IL-12-induced STAT4 contributes to IFN-gamma promoter activation by up-regulating the binding activity of IL-18-induced activator protein 1. J Immunol 2002;168:1146-1153.
84. Glimcher LH, Townsend MJ, Sullivan BM, Lord GM. Recent developments in the transcriptional regulation of cytolytic effector cells. Nat Rev Immunol 2004;4:900-911.
85. Tayade C, Fang Y, Black G, Paffaro VA Jr, Croy BA. Transcription of Eomes and T-bet during differentiation and development of effector function in mouse uterine natural killer cells. J Leukoc Biol 2005;78:1347-1355.
86. Lanier LL. NK cell recognition. Annu Rev Immunol 2005;23:225-274.
87. Xie X, He H, Colonna M, Seya T, Takai T, Croy B. Pathways participating in activation of mouse uterine natural killer cells during pregnancy. Biol Reprod 2005;73:510-518.
88. Ritson A, Bulmer JN. Endometrial granulocytes in human decidua react with a naturalkiller (NK) cell marker, Nkh1. Immunology 1987;62:329-331.
89. Lang K, Drell TL, Niggernann B, Zanker KS, Entschladen F. Neurotransmitters regulate the migration and cytotoxicity in natural killer cells. Immunol Lett 2003;90:165-172.
90. van den Heuvel M, et al. A review of trafficking and activation of uterine natural killer cells. Am J Reprod Immunol 2005;54:322-331.
91. Zoubina EV, Smith PG. Axonal degeneration and regeneration in rat uterus during the estrous cycle. Auton Neurosci 2000;84:176-185.
92. Zoubina EV, Smith PG. Sympathetic hyper-innervation of the uterus in the estrogen receptor alpha knock-out mouse. Neuroscience 2001;103:237-244.
93. Mukouyama YS, Gerber HP, Ferrara N, Gu CH, Anderson DJ. Peripheral nerve-derived VEGF promotes arterial differentiation via neuropilin 1-mediated positive feedback. Development 2005;132:941-952.
94. Mohamed OA, Jonnaert M, Lebelle-Dumais CL, Kuroda K, Clarke HJ, Dufort D. Uterine Wnt/beta-catenin signaling is required for implantation. Proc Natl Acad Sci USA 2005;102:8579-8584.
95. Bagot CN, Kliman HJ, Taylor HS. Maternal Hoxa10 is required for pinopod formation in the development of mouse uterine receptivity to embryo implantation. Dev Dyn 2001;222:538-544.
96. Wang C, et al. Granulated metrial gland cells in the murine uterus: localization, kinetics, and the functional role in angiogenesis during pregnancy. Microsc Res Tech 2005;60:420-429.
97. Li XC-JD, et al. Angiogenic growth factor messenger ribonucleic acids in uterine natural killer cells. J Clin Endocrinol Metab 2001;86:1823-1834.
98. Leonard S, Murrant CL, van den Heuvel M, Watering R, Croy BA. Mechanisms regulating immune cell contributions to spiral artery modification-facts and hypotheses. Placenta 2006;27(Suppl.):S40-S46.
99. Mukhtar DDY, Stewart I. Migration of granulated metrial gland cells from cultured explants of mouse metrial gland tissue. Cell Tissue Res 1988;253:413-417.
100. Lindquist RL, et al. Visualizing dendritic cell networks in vivo. Nat Immunol 2004;5:1243-1250.
101. Shakhar G, et al. Stable T cell-dendritic cell interactions precede the development of both tolerance and immunity in vivo. Nat Immunol 2005;6:707-714.
102. Rzucidlo EM, Quist WC, Hamdan AD, LoGerfo FW. Interferon gamma up-regulates a novel protein in vascular smooth muscle cells. J Vasc Surg 1999;29:317-323.
103. Tenger C, Sundborger A, Jawien J, Zhou XH. IL-18 accelerates atherosclerosis accompanied by elevation of IFN-gamma and CXCL16 expression independently of T cells. Arterioscler Thromb Vasc Biol 2005;25:791-796.
104. Hunt JS, Miller L, Vassmer D, Croy BA. Expression of the inducible nitric oxide synthase gene in mouse uterine leukocytes and potential relationships with uterine function during pregnancy. Biol Reprod 1997;57:827-836.
105. Burnett TG, Hunt JS. Nitric oxide synthase-2 and expression of perforin in uterine NK cells. J Immunol 2000;164:5245-5250.
106. He H, et al. Characterization of a murine alpha 2 macroglobulin gene expressed in reproductive and cardiovascular tissue. Biol Reprod 2005;72:266-275.
107. Tayade C, Esadeg S, Fang Y, Croy BA. Functions of alpha 2 macroglobulins in pregnancy. Mol Cell Endocrinol 2005;245:60-66.
108. Chantakru S, et al. Contributions from self-renewal and trafficking to the uterine NK cell population of early pregnancy. J Immunol 2002;168:22-28.
109. Halin C, Mora JR, Sumen C, von Andrian UH. In vivo imaging of lymphocyte trafficking. Annu Rev Cell Dev Biol 2005;21:581-603.
110. Chantakru S, et al. Coordinate regulation of lymphocyte-endothelial interactions by pregnancy-associated hormones. J Immunol 2003;171:4011-4019.
111. Pendaries C, et al. The AF-1 activation-function of ER alpha may be dispensable to mediate the effect of estradiol on endothelial NO production in mice. Proc Natl Acad Sci USA 2002;99:2205-2210.
112. Shin DH, Anderson DJ. Isolation of arterial-specific genes by subtractive hybridization reveals molecular heterogeneity among arterial endothelial cells. Dev Dyn 2005;233:1589-1604.
113. Jamieson T, et al. The chemokine receptor D6 limits the inflammatory response in vivo. Nat Immunol 2005;6:403-411.
114. Hirsch E, Wang H. The molecular pathophysiology of bacterially induced preterm labor: insights from the murine model. J Soc Gynecol Investig 2005;12:145-155.
115. Clark DA, Manuel J, Lee L, Chaouat G, Gorczynski RM, Levy GA. Ecology of danger-dependent cytokine-boosted spontaneous abortion in the CBA x DBA/2 mouse model. I. Synergistic effect of LPS and (TNF-alpha+IFN-gamma) on pregnancy loss. Am J Reprod Immunol 2004;52:370-378.
116. Molina H. Complement regulation during pregnancy. Immunol Res 2005;32:187-192.
117. Baban B, Chandler P, McCool D, Marshall B, Munn DH, Mellor AL. Indoleamine 2,3-dioxygenase expression is restricted to fetal trophoblast giant cells during murine gestation and is maternal genome specific. J Reprod Immunol 2004;61:67-77.
118. Cross JC, Anson-Cartwright L, Scott IC. Transcription factors underlying the development and endocrine functions of the placenta. Recent Prog Horm Res 2002;57:221-234.
119. Erlebacher A, Zhang D, Parlow AF, Glimcher LH. Ovarian insufficiency and early pregnancy loss induced by activation of the innate immune system. J Clin Invest 2004;114:39-48.
120. Crepeau MA, Croy BA. Evidence that specific cellular immunity cannot account for death of Mus caroli embryos transferred to Mus musculus with severe combined immune deficiency disease. Transplantation 1988;45:1104-1110.
121. Mellor AL, et al. Indoleamine 2,3-dioxygenase, immunosuppression and pregnancy. J Reprod Immunol 2002;57:143-150.
122. Zenclussen, AC. CD4(+) CD25(+) T regulatory cells in murine pregnancy. J Reprod Immunol 2005;65:101-110.
123. Arck PC, et al. Stress-induced murine abortion associated with substance beta-dependent alteration in cytokines in maternal uterine decidua. Biol Reprod 1995;53:814-819.
124. Mao DL, et al. Negligible role of antibodies and C5 in pregnancy loss associated exclusively with C3-dependent mechanisms through complement alternative pathway. Immunity 2003;19:813-822.
125. Wira CR, Fahey JV, Sentman CL, Pioli PA, Shen L. Innate and adaptive immunity in female genital tract: cellular responses and interactions. Immunol Rev 2005;206:306-335.
126. Kitaya K, Yasuda J, Yagi I, Tada Y, Fushiki S, Honjo H. IL-15 expression at human endometrium and decidua. Biol Reprod 2003;63:683-687.
127. DeLoia JA, Stewart-Akers AM, Brekosky J, Kubik C. Stimulation of uterine cell cytokine production by ovarian hormones. Am J Reprod Immunol 2000;44:16-21.
128. Dunn CL, Critchley HO, Kelly RW. IL-15 regulation in human endometrial stromal cells. J Clin Endocrinol Metab 2002;87:1898-1901.
129. Chegini N, Ma C, Roberts M, Williams RS, Ripps BA. Differential expression of interleukins (IL) IL-13 and IL-15 throughout the menstrual cycle in endometrium of normal fertile women and women with recurrent spontaneous abortion. J Reprod Immunol 2002;56:93-110.
130. Kitaya K, Nakayama T, Okubo T, Kuroboshi H, Fushiki S, Honjo H. Expression of macrophage inflammatory protein-1beta in human endometrium: its role in endometrial recruitment of natural killer cells. J Clin Endocrinol Metab 2003;88:1809-1814.
131. Nakayama T, et al. Fluctuation of 6Ckine expression in human endometrium during the menstrual cycle. Fertil Steril 2003;80:1461-1465.
132. Kitaya K, Nakayama T, Daikoku N, Fushiki S, Honjo H. Spatial and temporal expression of ligands for CXCR3 and CXCR4 in human endometrium. J Clin Endocrinol Metab 2004;89:2470-2476.
133. Bulmer JN, Morrison L, Longfellow M, Ritson A, Pace D. Granulated lymphocytes in human endometrium: histochemical and immunohistochemical studies. Hum Reprod 1991;6:791-798.
134. Searle RF, Jones RK, Bulmer JN. Phenotypic analysis and proliferative responses of human endometrial granulated lymphocytes during the menstrual cycle. Biol Reprod 1999;60:871-878.
135. Frey M, et al. Differential expression and function of L-selectin on CD56bright and CD56dim natural killer cell subsets. J Immunol 1998;161:400-408.
136. King A. Uterine leukocytes and decidualization. Hum Reprod Update 2000;6:28-36.
137. Rieger L, et al. Antigen-presenting cells in human endometrium during the menstrual cycle compared to early pregnancy. J Soc Gynecol Investig 2004;11:488-493.
138. Kammerer U, Marzusch K, Krober 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.
139. King A, Jokhi PP, Burrows TD, Gardner L, Sharkey AM, Loke YW. Functions of human decidual NK cells. Am J Reprod Immunol 1996;35:258-260.
140. Ledee-Bataille N, Bonnet-Chea K, Hosny G, Dubanchet SY, 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.
141. Quenby S, Vince G, Farquharson R, Aplin J. Recurrent miscarriage: a defect in nature's quality control? Hum Reprod 2002;17:1959-1963.
142. 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.
143. Yamamoto T, Takahashi Y, Kase N, Mori H. Role of decidual natural killer (NK) cells in patients with missed abortion: differences between cases with normal and abnormal chromosome. Clin Exp Immunol 1999;116:449-452.
144. King A, Wooding P, Gardner L, Loke YW. 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 1993;8:2061-2067.
145. King A, Birkby C, Loke YW. Early human decidual cells exhibit NK activity against the K562 cell line but not against first trimester trophoblast. Cell Immunol 1989;118:337-344.
146. King A, Loke YW. Human trophoblast and JEG choriocarcinoma cells are sensitive to lysis by IL-2-stimulated decidual NK cells. Cell Immunol 1990;129:435-448.
147. Ferry BL, Starkey PM, Sargent IL, Watt GM, Jackson M, Redman CW. Cell populations in the human early pregnancy decidua: natural killer activity and response to interleukin-2 of CD56-positive large granular lymphocytes. Immunology 1990;70:446-452.
148. Ferry BL, Sargent IL, Starkey PM, Redman CW. Cytotoxic activity against trophoblast and choriocarcinoma cells of large granular lymphocytes from human early pregnancy decidua. Cell Immunol 1991;132:140-149.
149. Croy BA, Guimond MJ, Luross J, Hahnel A, Wang B, van den Heuvel M. Uterine natural killer cells do not require interleukin-2 for their differentiation or maturation. Am J Reprod Immunol 1997;37:463-470.
150. Saito S, et al. Cytokine production by CD16-CD56bright natural killer cells in the human early pregnancy decidua. Int Immunol 1993;5:559-563.
151. Jokhi PP, King A, Loke YW. Cytokine production and cytokine receptor expression by cells of the human first trimester placental-uterine interface. Cytokine 1997;9:126-137.
152. Saito S, et al. Interleukin-8 production by CD16-CD56bright natural killer cells in the human early pregnancy decidua. Biochem Biophys Res Commun 1994;200:378-383.
153. Jokhi PP, King A, Sharkey AM, Smith SK, Loke YW. Screening for cytokine messenger ribonucleic acids in purified human decidual lymphocyte populations by the reverse-transcriptase polymerase chain reaction. J Immunol 1994;153:4427-4435.
154. Sharkey AM, et al. Localization of leukemia inhibitory factor and its receptor in human placenta throughout pregnancy. Biol Reprod 1999;60:355-364.
155. Shakhar K, Ben-Elivahu S, Loewenthal R, Rosenne E, Carp H. Differences in number and activity of peripheral natural killer cells in primary versus secondary recurrent miscarriage. Fertil Steril 2003;80:368-375
156. Li XF, et al. Angiogenic growth factor messenger ribonucleic acids in uterine natural killer cells. J Clin Endocrinol Metab 2001;86:1823-1834.
157. Eide IP, et al. Serious foetal growth restriction is associated with reduced proportions of natural killer cells in decidua basalis. Virchows Arch 2006:448:269-276.
158. Hickey M, Fraser I. Human uterine vascular structures in normal and diseased states. Microsc Res Tech 2003;60:377-389.
159. Rogers PA, Gargett CE. Endometrial angiogenesis. Angiogenesis 1998;2:287-294.
160. Kao LC, et al. Expression profiling of endometrium from women with endometriosis reveals candidate genes for disease-based implantation failure and infertility. Endocrinology 2003;144:2870-2881.
161. Hickey M, et al. Menopausal hormone therapy and irregular endometrial bleeding: a potential role for uterine natural killer cells? J Clin Endocrinol Metab 2005;90:5528-5535.
162. Rogers PA, Lederman F, Taylor N. Endometrial microvascular growth in normal and dysfunctional states. Hum Reprod Update 1998;4:503-508.
163. Fang Y. Molecular analyses of steps contributing to fetal success in pigs. MSc Thesis, University of Guelph, 2006.
164. Kukk E, et al. VEGF-C receptor binding and pattern of expression with VEGFR-3 suggests a role in lymphatic vascular development. Development 1996;122:3829-3837.
165. Williams PL, Warwick R, Dyson M, Bannister LH, eds. Gray's Anatomy, 37th edn. Edinburgh: Churchill Livingstone, 1989:856.
166. Wislocki GB, Dempsey EW. Remarks on the lymphatics of the reproductive tract of female rhesus monkey (Macaca mulatta). Anat Rec 1939;75:341-363.
167. Head JR, Seelig LL. Lymphatic vessels in the uterine endometrium of virgin rats. J Reprod Immunol 1984;6:157-166.
168. Proll J, Bensussan A, Goffin F, Foidart JM, 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.
169. von Rango U, Classen-Linke I, Kertschanska S, Kemp B, Beier HM. Effects of trophoblast invasion on the distribution of leukocytes in uterine and tubal implantation sites. Fertil Steril 2001;76:116-124.
170. Vassiliadou N, Bulmer JN. Expression of CD69 activation marker by endometrial granulated lymphocytes throughout the menstrual cycle and in early pregnancy. Immunology 1998;94:368-375.
171. Henderson TA, Saunders PT, Moffett-King A, Groome NP, Critchley HO. Steroid receptor expression in uterine natural killer cells. J Clin Endocrinol Metab 2003;88:440-449.
172. Kammerer U, et al. Unique appearance of proliferating antigen-presenting cells expressing DC-SIGN (CD209) in the decidua of early human pregnancy. Am J Pathol 2003;162:887-896.
173. Hunt JS, Petroff MG, McIntire RH, Ober C. HLA-G and immune tolerance in pregnancy. FASEB J 2005;19:681-693.
174. Redman CW, Sargent IL. Latest advances in understanding preeclampsia. Science 2005;308:1592-1594.
175. Parham P. NK cells and trophoblasts: partners in pregnancy. J Exp Med 2004;200:951-955.
176. Hiby SE, et al. Combinations of maternal KIR and fetal HLA-C genes influence the risk of preeclampsia and reproductive success. J Exp Med 2004;200:957-965.
177. Laird SM, Tuckerman EM, Cork BA, Linjawi S, Blakemore AIF, Li TC. A review of immune cells and molecules in women with recurrent miscarriage. Hum Reprod Update 2003;9:163-174.
178. Moffett A, Regan L, Braude P. Natural killer cells, miscarriage, and infertility. BMJ 2004;329:1283-1285.
179. Than GN, Bohn H, Szabo DG. Advances in Pregnancy-Related Protein Research - Functional and Clinical Applications. Boca Raton: CRC Press, 1993.
180. Borzychowski A, Croy BA, Chan WL, Redman CWG, Sargent IL. Changes in systemic type 1 and type 2 immunity in normal pregnancy and pre-eclampsia may be mediated by natural killer cells. Eur J Immunol 2005;35:3054-3063.
181. Mansour I, Reznikoff-Etievant MF, Netter A. No evidence for the expression of the progesterone receptor on peripheral blood lymphocytes during pregnancy. Hum Reprod 1994;9:1546-1549.
182. Sulke AN, Jones DB, Wood PJ. Variation in natural killer activity in peripheral blood during the menstrual cycle. BMJ (Clin Res Ed) 1985;290:884-886.
183. Sulke AN, Jones DB, Wood PJ. Hormonal modulation of human natural killer cell activity in vitro. J Reprod Immunol 1985;7:105-110.
184. Giglio T, et al. Immune cell circulating subsets are affected by gonadal function. Life Sci 1994;54:1305-1312.
185. Yovel G, Shakhar K, Ben-Eliyahu S. The effects of sex, menstrual cycle, and oral contraceptives on the number and activity of natural killer cells. Gynecol Oncol 2001;81:254-262.
186. Souza SS, et al. Influence of menstrual cycle on NK activity. J Reprod Immunol 2001;50:151-159.
187. Hanna J, et al. CXCL12 expression by invasive trophoblasts induces the specific migration of CD16- human natural killer cells. Blood 2003;102:1569-1577.
188. Red-Horse K, Drake PM, Fisher SJ. Chemokine ligand and receptor expression in the pregnant uterus: reciprocal patterns in complementary cell subsets suggest functional roles. Am J Pathol 2001;159:2199-2213.
189. van den Heuvel M, et al. Menstrual cycle hormones induce changes in functional interactions between lymphocytes and decidual vascular endothelial cells. J Clin Endocrinol Metab 2005;90:2835-2842.
190. 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.
191. bright cells are associated with fertile
192. Lin H, Mosmann TR, Guilbert L, Tuntipopipat S, Wegmann TG. Synthesis of T-helper 2-type cytokines at the maternal-fetal interface. J Immunol 1993;151:4562-4573.
193. Darmochwal-Kolarz D, Leszczynska-Gorzelak B, Rolinski J, Oleszczuk J. T helper 1-and T helper 2-type cytokine imbalance in pregnant women with pre-eclampsia. Eur J Obstet Gynecol Reprod Biol 1999;86:165-170.
194. Saito S, Sakai M, Sasaki Y, Tanebe K, Tsuda H, Michimata T. Quantitative analysis of peripheral blood Th0, Th1, Th2 and the Th1:Th2 cell ratio during normal human pregnancy and preeclampsia. Clin Exp Immunol 1999;117:550-555.
195. 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.
196. de Moraes-Pinto MI, Vince GS, Flanagan BF, Hart CA, Johnson PM. Localization of IL-4 and IL-4 receptors in the human term placenta, decidua and amniochorionic membranes. Immunology 1997;90:94.
197. Trautman MS, Collmer D, Edwin SS, White W, Mitchell MD, Dudley DJ. Expression of interleukin-10 in human gestational tissues. J Soc Gynecol Investig 1997;4:253.
198. Makhseed M, Raghupathy R, Azizieh F, Al Azemi MMK, Hassan NA, Bandar A. Mitogen-induced cytokine responses of maternal peripheral blood lymphocytes indicate a differential Th-type bias in normal pregnancy and pregnancy failure. Am J Reprod Immunol 1999;42:273-281.
199. Chaouat G. Innately moving away from the Th1/Th2 paradigm in pregnancy. Clin Exp Immunol 2003;31:393-395.
200. Sacks GP, Redman CWG, Sargent IL. Monocytes are primed to produce the Th1 type cytokine IL-12 in normal human pregnancy: an intracellular flow cytometric analysis of peripheral blood mononuclear cells. Clin Exp Immunol 2003;131:490-497.
201. Noble A, Macary PA, Kemeny DM. IFN-gamma and IL-4 regulate the growth and differentiation of Cd8(+) T-cells into subpopulations with distinct cytokine profiles. J Immunol 1995;155:2928-2937.
202. Peritt D, Robertson S, Gri G, Showe L, Aste-Amezaga M, Trinchieri G. Cutting edge: differentiation of human NK cells into NK1 and NK2 subsets. J Immunol 1998;161:5821-5824.
203. Kadowaki N, et al. Distinct cytokine profiles of neonatal natural killer T cells after expansion with subsets of dendritic cells. J Exp Med 2001;193:1221-1226.
204. Chan WL, Pejnovic N, Lee CA, Al Ali NA. Human IL-18 receptor and ST2L are stable and selective markers for the respective type 1 and type 2 circulating lymphocytes. J Immunol 2001;167:1238-1244.
205. Borzychowski AM. The systemic inflammatory response in human pregnancy. PhD thesis, University of Guelph, 2005.
206. Piccinni MP, Romagnani S. Regulation of fetal allograft survival by hormone-controlled Th1- and Th2-type cytokines. Immunol Res 1996;15:141-150.
207. Lim KJH, Odukoya OA, Ajjan RA, Li TC, Weetman AP, Cooke ID. The role of T-helper cytokines in human reproduction. Fertil Steril 2000;73:136-142.
208. Roberts RM, Bazer FW. The functions of uterine secretions. J Reprod Fertil 1988;82:875-892.
209. Wooding FBP, Flint APF. Placentation. In: Lamming GE., ed. Marshall's Physiology of Reproduction, 4th edn. London: Chapman and Hall, 1994 III:233-460.
210. Dantzer V. Epitheliochorial placentation. In: Knobil E, Neil JD, eds. Encyclopedia of Reproduction. New York: Academic Press, 1999:18-28.
211. Bischof RJ, Brandon MR, Lee CS. Cellular immune responses in the pig uterus during pregnancy. J Reprod Immunol 1995;29:161-178.
212. Engelhardt H, Croy BA, King GJ. Evaluation of natural killer cell recruitment to embryonic attachment sites during early porcine pregnancy. Biol Reprod 2002;66:1185-1192.
213. Engelhardt H, Croy BA, King GJ. Conceptus influences the distribution of uterine leukocytes during early porcine pregnancy. Biol Reprod 2002;66:1875-1880.
214. Kaeoket K, Persson E, Dalin AM. Influence of pre-ovulatory insemination and early pregnancy on the infiltration by cells of the immune system in the sow endometrium. Anim Reprod Sci 2003;75:55-71.
215. Croy BA, Waterfield A, Wood W, King GJ. Normal murine and porcine embryos recruit NK cells to the uterus. Cell Immunol 1988;115:471-480.
216. Yu Z, Croy BA, Chapeau C, King GJ. Elevated endometrial natural killer cell activity during early porcine pregnancy is conceptus-mediated. J Reprod Immunol 1993;24:153-164.
217. Tayade C, Black GP, Fang Y, Croy BA. Differential gene expression in endometrium, endometrial lymphocytes, and trophoblasts during successful and abortive embryo implantation. J Immunol 2006;176:148-156.
218. Vonnahme KA, Wilson ME, Foxcroft GR, Ford SP. Impacts on conceptus survival in a commercial swine herd. J Anim Sci 2002;80:553-559.
219. Pope WF. Embryonic mortality in swine. In: Geisert RD, Zavy MT, eds. Embryonic Mortality in Domestic Species. Boca Raton: CRC Press, 1994: 53-78.
220. Bamberger AM, Schulte HM, Thuneke I, Erdmann I, Bamberger CM, Asa SL. Expression of the apoptosis-inducing Fas ligand (FasL) in human first and third trimester placenta and choriocarcinoma cells. J Clin Endocrinol Metab 1997;82:3173-3175.
221. Neale DM, Mor G. The role of Fas mediated apoptosis in preeclampsia. J Perinat Med 2005;33:471-477.
222. Zak LJ, Xu X, Hardin RT, Foxcroft GR. Impact of different patterns of feed intake during lactation in the primiparous sow on follicular development and oocyte maturation. J Reprod Fertil 1997;110:99-106.
223. Rock KL, Hearn A, Chen CJ, Shi Y. Natural endogenous adjuvants. Springer Semin Immunopathol 2005;26:231-246.
224. Gasser S, Orsulic S, Brown EJ, Raulet DH. The DNA damage pathway regulates innate immune system ligands of the NKG2D receptor. Nature 2005;436:1186-1190.
225. Rock KL, Shen L. Cross-presentation: underlying mechanisms and role in immune surveillance. Immunol Rev 2005;207:166-183.
226. Kammerer U, Rieger L, Kapp M, Dietl J, Ruck P. Immuncompetent cells in the endometrium of fetuses and children. Hum Reprod 2003;18:969-975.
227. Luross JA, Yamashiro S, Croy BA. A study on the relationship between parity and differentiation of granulated metrial gland cells. Placenta 1996;17:521-525.
228. Oduor-Okalo D, Katema RM, Carter AM. Placenta and fetal membranes of the four-toed elephant shrew, Petrodomus tetradactylus. Placenta 2004;25:803-809.
229. Enders, AC. Current topic: structural responses of the primate endometrium to implantation. Placenta 1991;12:309-325.
230. Martinez CM, Buendia AJ, Sanchez J, Navarro JA. Immunophenotypical characterization of lymphocyte subpopulations of the uterus of non-pregnant and pregnant goats. Anat Histol Embryol 2005;34:240-246.
231. Grunig G, Triplett L, Canady LK, Allen WR, Antczak DF. The maternal leucocyte response to the endometrial cups in horses is correlated with the developmental stages of the invasive trophoblast cells. Placenta 1995;16:539-559.
232. Allen MP, Nilsen-Hamilton M. Granzymes D, E, F, and G are regulated through pregnancy and by IL-2 and IL-15 in granulated metrial gland cells. J Immunol 1998;161:2772-2779.
233. Croy BA, Chapeau C. Evaluation of the pregnancy immunotrophism hypothesis by assessment of the reproductive performance of young adult mice of genotype scid/scid.bg/bg. J Reprod Fertil 1990;88:231-239.
234. Stewart IJ, Peel S. Granulated metrial gland cells in pregnant athymic mice. J Anat 1980;131:217 (Abstract).
235. Kokubu K, Hondo E, Namba Y, Kusakabe K, Kiso Y. Ultrastructural study of uterine natural killer cells found in pregnant, interleukin-2 receptor beta-chain overexpressed transgenic mice. J Reprod Dev 2005;51:695-698.
236. Kiso Y, Pollard JW, Croy BA. A study of granulated metrial gland cell differentiation in pregnant, macrophage-deficient, osteopetrotic (op/op) mice. Experientia 1992;48:973-975.
237. Robertson SA, Roberts CT, Farr KL, Dunn AR, Seamark RF. Fertility impairment in granulocyte-macrophage colony-stimulating factor-deficient mice. Biol Reprod 1999;60:251-261.
238. Kiso Y, McBey BA, Croy BA. Granulated metrial gland cells in the pregnant uterus of mice expressing the collagen mutation tight-skin (Tsk/+). Cell Tissue Res 1992;268:393-396.
239. Fernekorn U, Butcher EC, Behrends J, Hartz S, Kruse A. Functional involvement of P-selectin and MAdCAM-1 in the recruitment of alpha4beta7-integrin-expressing monocyte-like cells to the pregnant mouse uterus. Eur J Immunol 2004;34:3423-3433.
240. Kusakabe K, Otsuki Y, Kiso Y. Involvement of the Fas ligand and Fas system in apoptosis induction of mouse uterine natural killer cells. J Reprod Dev 2005;51:333-340.
241. Kather A, et al. Neither lymphotoxin alpha nor lymphotoxin beta receptor expression is required for biogenesis of lymphoid aggregates or differentiation of natural killer cells in the pregnant mouse uterus. Immunology 2003;108:338-345.
242. Kiso Y, Kusakabe K, Tokunaga Y, Makita M, Okada T, Sasaki F. A study of granulated metrial gland cells in the pregnant, alymphoplasia (aly/aly) mice. J Vet Med Sci 1997;59:1137-1141.
243. Miyazaki S, et al. Interleukin 2 receptor gamma chain (gamma c) knockout mice show less regularity in estrous cycle but achieve normal pregnancy without fetal compromise. Am J Reprod Immunol 2002;47:222-230.
244. Greenwood JD, Minhas K, di Santo JP, Makita M, Kiso Y, Croy BA. Ultrastructural studies of implantation sites from mice deficient in uterine natural killer cells. Placenta 2000;21:693-702.
245. Monk JM, Leonard S, McBey BA, Croy BA. Induction of murine spiral artery modification by recombinant human interferon-gamma. Placenta 2005;26:835-838.
246. Esadeg S, He H, Pijnenborg R, van Leuven F, Cross JC, Croy BA. Alpha 2 macroglobulin controls trophoblast positioning in mouse implantation sites. Placenta 2003;24:912-921.
247. Stallmach T, Ehrenstein T, Isenmann S, Muller C, Hengartner H, Kagi D. The role of perforin-expression by granular metrial gland cells in pregnancy. Eur J Immunol 1995;25:3342-3348.
248. Croy BA, Chantakru S, Narumiya S, Ichikawa A, Sugimoto Y. Prolonged gestation does not extend survival of uterine natural killer lymphocytes in mice deleted in the receptor for prostaglandin F2alpha. J Reprod Immunol 2000;46:125-129.
249. Xie X, Kang J, Anderson L, He H, Lu B, Croy B. Analysis of contributions of L-selectin and CXCR3 in mediating leukocyte homing to pregnant mouse uterus. Am J Reprod Immunol 2005;53:1-12.
250. Mulac-Jericevic B, Mullinax RA, DeMayo FJ, Lydon JP, Conneely OM. Subgroup of reproductive functions of progesterone mediated by progesterone receptor B isoform. Sicence 2000;289:1751-1754.
251. Murphy SP, Fast LD, Hanna NN, Sharma S. Uterine NK cells mediate inflammation-induced fetal demise in IL-10-null mice. J Immunol 2005;175:4084-4090.
252. Ain R, Trinh ML, Soares MJ. Interleukin-11 signaling is required for the differentiation of natural killer cells at the maternal-fetal interface. Dev Dyn 2004;231:700-708.
253. Rahman MA, Li ML, Li P, Wang HB, Dey SK, Das SK. Hoxa-10 deficiency alters region-specific gene expression and perturbs differentiation of natural killer cells during decidualization. Dev Biol 2006;290:105-117.