Pleiotropy and redundancy of STAT proteins in early pregnancy

Reproduction in Domestic Animals

Volumn 42, Issue 4, 2007, Pages 343-353

  Maj, T ^a   Chelmonska Soyta, A ^a,b  

^a INSTITUTE OF IMMUNOLOGY AND EXPERIMENTAL THERAPY   (Poland)

^b WROCLAW UNIVERSITY OF ENVIRONMENTAL AND LIFE SCIENCES   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

JANUS KINASE; STAT PROTEIN;

ANIMAL; BREEDING; FEMALE; PHYSIOLOGY; PREGNANCY; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; FEMALE; JANUS KINASES; PREGNANCY; PREGNANCY, ANIMAL; SIGNAL TRANSDUCTION; STAT TRANSCRIPTION FACTORS;

EID: 34447292522     PISSN: 09366768     EISSN: 14390531     Source Type: Journal    
DOI: 10.1111/j.1439-0531.2006.00787.x     Document Type: Review

References (119)

1. Ahn HJ, Tomura M, Yu WG, Iwasaki M, Park WR, Hamaoka T, Fujiwara H, 1998 : Requirement for distinct Janus kinases and STAT proteins in T cell proliferation versus IFN-γ production following IL-12 stimulation. J Immunol 161, 5893 5900.
2. Anegon I, Cuturi MC, Godard A, Moreau M, Terqui M, Martinat-Botte F, Soulillou JP, 1994 : Presence of leukaemia inhibitory factor and interleukin 6 in porcine uterine secretions prior to conceptus attachment. Cytokine 6, 493 499.
3. Antczak M, Van Blerkom J, 1997 : Oocyte influences on early development: the regulatory proteins leptin and STAT3 are polarized in mouse and human oocytes and differentially distributed within the cells of the preimplantation stage embryo. Mol Hum Reprod 3, 1067 1086.
4. Aoki N, Matsuda T, 2000 : A cytosolic protein-tyrosine phosphatase PTP1B specifically dephosphorylates and deactivates prolactin-activated STAT5a and STAT5b. J Biol Chem 275, 39718 39726.
5. Aoki N, Matsuda T, 2002 : A nuclear protein tyrosine phosphatase TC-PTP is a potential negative regulator of the PRL-mediated signaling pathway: dephosphorylation and deactivation of signal transducer and activator of transcription 5a and 5b by TC-PTP in nucleus. Mol Endocrinol 16, 58 69.
6. Aschkenazi S, Straszewski S, Verwer KM, Foellmer H, Rutherford T, Mor G, 2002 : Differential regulation and function of the Fas/Fas ligand system in human trophoblast cells. Biol Reprod 66, 1853 1861.
7. Asselin E, Bazer FW, Fortier MA, 1997 : Recombinant ovine and bovine interferons tau regulate prostaglandin production and oxytocin response in cultured bovine endometrial cells. Biol Reprod 56, 402 408.
8. Bacon CM, Petricoin EF III., Ortaldo JR, Rees RC, Larner AC, Johnston JA, O'Shea JJ, 1995 : Interleukin 12 induces tyrosine phosphorylation and activation of STAT4 in human lymphocytes. Proc Natl Acad Sci USA 92, 7307 7311.
9. Badinga L, Guzeloglu A, Thatcher WW, 2002 : Bovine somatotropin attenuates phorbol ester-induced prostaglandin F2α production in bovine endometrial cells. J Dairy Sci 85, 537 543.
10. Barkai U, Prigent-Tessier A, Tessier C, Gibori GB, Gibori G, 2000 : Involvement of SOCS-1, the suppressor of cytokine signaling, in the prevention of prolactin-responsive gene expression in decidual cells. Mol Endocrinol 14, 554 563.
11. Basak S, Dubanchet S, Zourbas S, Chaouat G, Das C, 2002 : Expression of pro-inflammatory cytokines in mouse blastocysts during implantation: modulation by steroid hormones. Am J Reprod Immunol 47, 2 11.
12. Bhatt H, Brunet LJ, Stewart CL, 1991 : Uterine expression of leukemia inhibitory factor coincides with the onset of blastocyst implantation. Proc Natl Acad Sci USA 88, 11408 11412.
13. Binelli M, Guzeloglu A, Badinga L, Arnold DR, Sirois J, Hansen TR, Thatcher WW, 2000 : Interferon-τ modulates phorbol ester-induced production of prostaglandin and expression of cyclooxygenase-2 and phospholipase-A2 from bovine endometrial cells. Biol Reprod 63, 417 424.
14. Binelli M, Subramaniam P, Diaz T, Johnson GA, Hansen TR, Badinga L, Thatcher WW, 2001 : Bovine interferon-τ stimulates the Janus kinase-signal transducer and activator of transcription pathway in bovine endometrial epithelial cells. Biol Reprod 64, 654 665.
15. Bjornstrom L, Kilic E, Norman M, Parker MG, Sjoberg M, 2001 : Cross-talk between Stat5b and estrogen receptor-α and -β in mammary epithelial cells. J Mol Endocrinol 27, 93 106.
16. Bonney EA, 2001 : Maternal tolerance is not critically dependent on interleukin-4. Immunology 103, 382 389.
17. Cervero A, Horcajadas JA, MartIn J, Pellicer A, Simon C, 2004 : The leptin system during human endometrial receptivity and preimplantation development. J Clin Endocrinol Metab 89, 2442 2451.
18. Cheng JG, Chen JR, Hernandez L, Alvord WG, Stewart CL, 2001 : Dual control of LIF expression and LIF receptor function regulate Stat3 activation at the onset of uterine receptivity and embryo implantation. Proc Natl Acad Sci USA 98, 8680 8685.
19. Cocchiara R, Lampiasi N, Albeggiani G, Azzolina A, Bongiovanni A, Gianaroli L, Di Blasi F, Geraci D, 1996 : A factor secreted by human embryo stimulates cytokine release by uterine mast cell. Mol Hum Reprod 2, 781 791.
20. Corvinus FM, Fitzgerald JS, Friedrich K, Markert UR, 2003 : Evidence for a correlation between trophoblast invasiveness and STAT3 activity. Am J Reprod Immunol 50, 316 321.
21. Croy BA, Ashkar AA, Foster RA, DiSanto JP, Magram J, Carson D, Gendler SJ, Grusby MJ, Wagner N, Muller W, Guimond MJ, 1997 : Histological studies of gene-ablated mice support important functional roles for natural killer cells in the uterus during pregnancy. J Reprod Immunol 35, 111 133.
22. Croy BA, Esadeg S, Chantakru S, van den Heuvel M, Paffaro VA, He H, Black GP, Ashkar AA, Kiso Y, Zhang J, 2003 : Update on pathways regulating the activation of uterine natural killer cells, their interactions with decidual spiral arteries and homing of their precursors to the uterus. J Reprod Immunol 59, 175 191.
23. Cui XS, Lee JY, Choi SH, Kwon MS, Kim T, Kim NH, 2004 : Mouse granulocyte-macrophage colony-stimulating factor enhances viability of porcine embryos in defined culture conditions. Anim Reprod Sci 84, 169 177.
24. Curlewis JD, Tam SP, Lau P, Kusters DH, Barclay JL, Anderson ST, Waters MJ, 2002 : A prostaglandin F2α analog induces suppressors of cytokine signaling-3 expression in the corpus luteum of the pregnant rat: a potential new mechanism in luteolysis. Endocrinology 143, 3984 3993.
25. Danet-Desnoyers G, Wetzels C, Thatcher WW, 1994 : Natural and recombinant bovine interferon tau regulate basal and oxytocin-induced secretion of prostaglandins F2α and E2 by epithelial cells and stromal cells in the endometrium. Reprod Fertil Dev 6, 193 202.
26. Dawn B, Xuan YT, Guo Y, Rezazadeh A, Stein AB, Hunt G, Wu WJ, Tan W, Bolli R, 2004 : IL-6 plays an obligatory role in late preconditioning via JAK-STAT signaling and upregulation of iNOS and COX-2. Cardiovasc Res 64, 61 71.
27. De M, Sanford TR, Wood GW, 1993 : Expression of interleukin 1, interleukin 6 and tumour necrosis factor α in mouse uterus during the peri-implantation period of pregnancy. J Reprod Fertil 97, 83 89.
28. Delassus S, Coutinho GC, Saucier C, Darche S, Kourilsky P, 1994 : Differential cytokine expression in maternal blood and placenta during murine gestation. J Immunol 152, 2411 2420.
29. Diehl S, Anguita J, Hoffmeyer A, Zapton T, Ihle JN, Fikrig E, Rincon M, 2000 : Inhibition of Th1 differentiation by IL-6 is mediated by SOCS1. Immunity 13, 805 815.
30. Ealy AD, Wagner SK, Sheils AE, Whitley NC, Kiesling DO, Johnson SE, Barbato GF, 2004 : Identification of interferon-τ isoforms expressed by the peri-implantation goat (Capra hircus) conceptus. Domest Anim Endocrinol 27, 39 49.
31. Emond V, Asselin E, Fortier MA, Murphy BD, Lambert RD, 2000 : Interferon-τ stimulates granulocyte-macrophage colony-stimulating factor gene expression in bovine lymphocytes and endometrial stromal cells. Biol Reprod 62, 1728 1737.
32. Ernst M, Inglese M, Waring P, Campbell IK, Bao S, Clay FJ, Alexander WS, Wicks IP, Tarlinton DM, Novak U, Heath JK, Dunn AR, 2001 : 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 194, 189 203.
33. Esadeg S, He H, Pijnenborg R, Van Leuven F, Croy BA, 2003 : α-2 macroglobulin controls trophoblast positioning in mouse implantation sites. Placenta 24, 912 921.
34. Feltus FA, Groner B, Melner MH, 1999 : Stat5-mediated regulation of the human type II 3beta-hydroxysteroid dehydrogenase/delta5-delta4 isomerase gene: activation by prolactin. Mol Endocrinol 13, 1084 1093.
35. Finbloom DS, Winestock KD, 1995 : IL-10 induces the tyrosine phosphorylation of Tyk2 and Jak1 and the differential assembly of STAT1 α and STAT3 complexes in human T cells and monocytes. J Immunol 155, 1079 1090.
36. Fontana V, Choren V, Vauthay L, Calvo JC, Calvo L, Cameo M, 2004 : Exogenous interferon-γ alters murine inner cell mass and trophoblast development. Effect on the expression of ErbB1, ErbB4 and heparan sulfate proteoglycan (perlecan). Reproduction 128, 717 725.
37. Frasor J, Barkai U, Zhong L, Fazleabas AT, Gibori G, 2001a : PRL-induced ERα gene expression is mediated by Janus kinase 2 (Jak2) while signal transducer and activator of transcription 5b (Stat5b) phosphorylation involves Jak2 and a second tyrosine kinase. Mol Endocrinol 15, 941 1952.
38. Frasor J, Park K, Byers M, Telleria C, Kitamura T, Yu-Lee LY, Djiane J, Park-Sarge OK, Gibori G, 2001b : Differential roles for signal transducers and activators of transcription 5a and 5b in PRL stimulation of ERα and ERβ transcription. Mol Endocrinol 15, 2172 2181.
39. Frucht DM, Aringer M, Galon J, Danning C, Brown M, Fan S, Centola M, Wu CY, Yamada N, El Gabalawy H, O'Shea JJ, 2000 : Stat4 is expressed in activated peripheral blood monocytes, dendritic cells, and macrophages at sites of Th1-mediated inflammation. J Immunol 164, 4659 4664.
40. Garzia E, Borgato S, Cozzi V, Doi P, Bulfamante G, Persani L, Cetin I, 2004 : Lack of expression of endometrial prolactin in early implantation failure: a pilot study. Hum Reprod 19, 1911 1916.
41. Gearing DP, Thut C, Vandenbos T, Gimpel SD, Delaney PB, King J, Price V, Cosman D, Beckmann MP, 1991 : Leukemia inhibitory factor receptor is structurally related to the IL-6 signal transducer, gp 130. EMBO J 10, 2839 2848.
42. Giese B, Roderburg C, Sommerauer M, Wortman SB, Metz S, Heinrich PC, Müller-Newen G, 2005 : Dimerization of the cytokine receptors gp130 and LIFR analysed in single cells. J Cell Sci 118, 5129 5140.
43. Godkin JD, Smith SE, Johnson RD, Dore JJ, 1997 : The role of trophoblast interferons in the maintenance of early pregnancy in ruminants. Am J Reprod Immunol 37, 137 143.
44. Gonzalez RR, Leary K, Petrozza JC, Leavis PC, 2003 : Leptin regulation of the interleukin-1 system in human endometrial cells. Mol Hum Reprod 9, 151 158.
45. Gonzalez RR, Rueda BR, Ramos MP, Littell RD, Glasser S, Leavis PC, 2004 : Leptin-induced increase in leukemia inhibitory factor and its receptor by human endometrium is partially mediated by interleukin 1 receptor signaling. Endocrinology 145, 3850 3857.
46. Gootwine E, 2004 : Placental hormones and fetal-placental development. Anim Reprod Sci 82-83, 551 66.
47. Guillomot M, Reinaud P, La Bonnardiere C, Charpigny G, 1998 : Characterization of conceptus-produced goat interferon tau and analysis of its temporal and cellular distribution during early pregnancy. J Reprod Fertil 112, 149 156.
48. Haddad EK, Duclos AJ, Antecka E, Lapp WS, Baines MG, 1997 : Role of interferon-γ in the priming of decidual macrophages for nitric oxide production and early pregnancy loss. Cell Immunol 181, 68 75.
49. Haimovici F, Hill JA, Anderson DJ, 1991 : The effects of soluble products of activated lymphocytes and macrophages on blastocyst implantation events in vitro. Biol Reprod 44, 69 75.
50. Hashii K, Fujiwara H, Yoshioka S, Kataoka N, Yamada S, Hirano T, Mori T, Fujii S, Maeda M, 1998 : Peripheral blood mononuclear cells stimulate progesterone production by luteal cells derived from pregnant and non-pregnant women: possible involvement of interleukin-4 and interleukin-10 in corpus luteum function and differentiation. Hum Reprod 13, 2738 2744.
51. Hubbard SR, Till JH, 2000 : Protein tyrosine kinase structure and function. Annu Rev Biochem 69, 373 398.
52. Ito S, Ansari P, Sakatsume M, Dickensheets H, Vazquez N, Donnelly RP, Larner AC, Finbloom DS, 1999 : Interleukin-10 inhibits expression of both interferon α- and interferon γ-induced genes by suppressing tyrosine phosphorylation of STAT1. Blood 93, 1456 1463.
53. Jabbour HN, Critchley HO, Boddy SC, 1998 : Expression of functional prolactin receptors in nonpregnant human endometrium: Janus kinase-2, signal transducer and activator of transcription-1 (STAT1), and STAT5 proteins are phosphorylated after stimulation with prolactin. J Clin Endocrinol Metab 83, 2545 2553.
54. Johnson PM, Arnaud P, Werner P, Galbraith RM, 1985 : Native α2-macroglobulin binds to a surface component of human placental trophoblast. Placenta 6, 323 328.
55. Jones RL, Critchley HO, Brooks J, Jabbour HN, McNeilly AS, 1998 : Localization and temporal expression of prolactin receptor in human endometrium. J Clin Endocrinol Metab 83, 258 262.
56. Kanai T, Fujii T, Kozuma S, Yamashita T, Miki A, Kikuchi A, Taketani Y, 2001a : Soluble HLA-G influences the release of cytokines from allogeneic peripheral blood mononuclear cells in culture. Mol Hum Reprod 7, 195 200.
57. Kanai T, Fujii T, Unno N, Yamashita T, Hyodo H, Miki A, Hamai Y, Kozuma S, Taketani Y, 2001b : Human leukocyte antigen-G-expressing cells differently modulate the release of cytokines from mononuclear cells present in the decidua versus peripheral blood. Am J Reprod Immunol 45, 94 99.
58. Kaplan MH, Schindler U, Smiley ST, Grusby MJ, 1996 : Stat6 is required for mediating responses to IL-4 and for development of Th2 cells. Immunity 4, 313 319.
59. Kisseleva T, Bhattacharya S, Schroeder-Braunstein J, Schindler CW, 2002 : Signaling through the JAK/STAT pathway, recent advances and future challenges. Gene 285, 1 24.
60. Kodama H, Fukuda K, Pan J, Makino S, Baba A, Hori S, Ogawa S, 1997 : Leukemia inhibitory factor, a potent cardiac hypertrophic cytokine, activates the JAK/STAT pathway in rat cardiomyocytes. Circ Res 81, 656 663.
61. Kwak-Kim JY, Gilman-Sachs A, Kim CE, 2005 : T helper 1 and 2 immune responses in relationship to pregnancy, nonpregnancy, recurrent spontaneous abortions and infertility of repeated implantation failures. Chem Immunol Allergy 88, 64 79.
62. Lacroix MC, Guibourdenche J, Fournier T, Laurendeau I, Igout A, Goffin V, Pantel J, Tsatsaris V, Evain-Brion D, 2005 : Stimulation of human trophoblast invasion by placental growth hormone. Endocrinology 146, 2434 2444.
63. Leaman DW, Cross JC, Roberts RM, 1994 : Multiple regulatory elements are required to direct trophoblast interferon gene expression in choriocarcinoma cells and trophectoderm. Mol Endocrinol 8, 456 468.
64. Li J, Roberts RM, 1994 : Interferon-τ and interferon-α interact with the same receptors in bovine endometrium. Use of a readily iodinatable form of recombinant interferon-τ for binding studies. J Biol Chem 269, 13544 13550.
65. Lidstrom C, Matthiesen L, Berg G, Sharma S, Ernerudh J, Ekerfelt C, 2003 : Cytokine secretion patterns of NK cells and macrophages in early human pregnancy decidua and blood: implications for suppressor macrophages in decidua. Am J Reprod Immunol 50, 444 452.
66. Lim KJ, Odukoya OA, Ajjan RA, Li TC, Weetman AP, Cooke ID, 1998 : Profile of cytokine mRNA expression in peri-implantation human endometrium. Mol Hum Reprod 4, 77 81.
67. Liu T, Ogle TF, 2002 : Signal transducer and activator of transcription 3 is expressed in the decidualized mesometrium of pregnancy and associates with the progesterone receptor through protein-protein interactions. Biol Reprod 67, 114 118.
68. Martin C, Pessemesse L, De La Llosa-Hermier MP, Martal J, Djiane J, Charlier M, 2004 : Interferon-τ upregulates prolactin receptor mRNA in the ovine endometrium during the peri-implantation period. Reproduction 128, 99 105.
69. Marzusch K, Buchholz F, Ruck P, Handgretinger R, Geiselhart A, Engelmann L, Dietl J, 1997 : Interleukin-12- and interleukin-2-stimulated release of interferon-γ by uterine CD56++ large granular lymphocytes is amplified by decidual macrophages. Hum Reprod 12, 921 924.
70. Meisser A, Cameo P, Islami D, Campana A, Bischof P, 1999 : Effects of interleukin-6 (IL-6) on cytotrophoblastic cells. Mol Hum Reprod 5, 1055 1058.
71. Meyer T, Vinkemeier U, 2004 : Nucleocytoplasmic shuttling of STAT transcription factors. Eur J Biochem 271, 4606 4612.
72. Okuda A, Miyamoto Y, Skazrzynski DJ, 2002 : Regulation of endometrial prostaglandin F(2alpha) synthesis during luteolysis and early pregnancy in cattle. Domest Anim Endocrinol 23, 255 264.
73. Par G, Geli J, Kozma N, Varga P, Szekeres-Bartho J, 2003 : Progesterone regulates IL12 expression in pregnancy lymphocytes by inhibiting phospholipase A2. Am J Reprod Immunol 49, 1 5.
74. Parent J, Villeneuve C, Alexenko AP, Ealy AD, Fortier MA, 2003 : Influence of different isoforms of recombinant trophoblastic interferons on prostaglandin production in cultured bovine endometrial cells. Biol Reprod 68, 1035 1043.
75. Peyman JA, 1999 : Repression of major histocompatibility complex genes by a human trophoblast ribonucleic acid. Biol Reprod 60, 23 31.
76. Peyman JA, 2001 : Mammalian expression cloning of two human trophoblast suppressors of major histocompatibility complex genes. Am J Reprod Immunol 45, 382 392.
77. Piccinni MP, Giudizi MG, Biagiotti R, Beloni L, Giannarini L, Sampognaro S, Parronchi P, Manetti R, Annunziato F, Livi C, 1995 : Progesterone favors the development of human T helper cells producing Th2-type cytokines and promotes both IL-4 production and membrane CD30 expression in established Th1 cell clones. J Immunol 155, 128 133.
78. Piekorz RP, Gingras S, Hoffmeyer A, Ihle JN, Weinstein Y, 2005 : Regulation of progesterone levels during pregnancy and parturition by signal transducer and activator of transcription 5 and 20 α-hydroxysteroid dehydrogenase. Mol Endocrinol 19, 431 440.
79. Prigent-Tessier A, Barkai U, Tessier C, Cohen H, Gibori G, 2001 : Characterization of a rat uterine cell line, U(III) cells: prolactin (PRL) expression and endogenous regulation of PRL-dependent genes; estrogen receptor beta, α2-macroglobulin, and decidual PRL involving the Jak2 and Stat5 pathway. Endocrinology 142, 1242 1250.
80. Pru JK, Rueda BR, Austin KJ, Thatcher WW, Guzeloglu A, Hansen TR, 2001 : Interferon-τ suppresses prostaglandin F2α secretion independently of the mitogen-activated protein kinase and nuclear factor kappa B pathways. Biol Reprod 64, 965 973.
81. Rawlings JS, Rosler KM, Harrison DA, 2004 : The JAK/STAT signaling pathway. J Cell Sci 117, 1281 1283.
82. Richer JK, Lange CA, Manning NG, Owen G, Powell R, Horwitz KB, 1998 : Convergence of progesterone with growth factor and cytokine signaling in breast cancer. Progesterone receptors regulate signal transducers and activators of transcription expression and activity. J Biol Chem 273, 31317 31326.
83. Robertson SA, Seamark RF, 1990 : Granulocyte-macrophage colony stimulating factor (GM-CSF) in the murine reproductive tract: stimulation by seminal factors. Reprod Fertil Dev 2, 359 368.
84. Robertson SA, Mau VJ, Tremellen KP, Seamark RF, 1996 : Role of high molecular weight seminal vesicle proteins in eliciting the uterine inflammatory response to semen in mice. J Reprod Fertil 107, 265 277.
85. Robertson SA, Roberts CT, Farr KL, Dunn AR, Seamark RF, 1999 : Fertility impairment in granulocyte-macrophage colony-stimulating factor-deficient mice. Biol Reprod 60, 251 261.
86. Robertson SA, O'Connell AC, Hudson SN, Seamark RF, 2000 : Granulocyte-macrophage colony-stimulating factor (GM-CSF) targets myeloid leukocytes in the uterus during the post-mating inflammatory response in mice. J Reprod Immunol 46, 131 154.
87. Robertson SA, Sjoblom C, Jasper MJ, Norman RJ, Seamark RF, 2001 : Granulocyte-macrophage colony-stimulating factor promotes glucose transport and blastomere viability in murine preimplantation embryos. Biol Reprod 64, 1206 1215.
88. Rosenfeld CS, Han CS, Alexenko AP, Spencer TE, Roberts RM, 2002 : Expression of interferon receptor subunits, IFNAR1 and IFNAR2, in the ovine uterus. Biol Reprod 67, 847 853.
89. Roth I, Corry DB, Locksley RM, Abrams JS, Litton MJ, Fisher SJ, 1996 : Human placental cytotrophoblasts produce the immunosuppressive cytokine interleukin 10. J Exp Med 184, 539 548.
90. Saijo Y, Sata F, Yamada H, Konodo T, Kato EH, Kataoka S, Shimada S, Morikawa M, Minakami H, Kishi R, 2004 : Interleukin-4 gene polymorphism is not involved in the risk of recurrent pregnancy loss. Am J Reprod Immunol 52, 143 146.
91. Schindler C, Shuai K, Prezioso VR, Darnell JE Jr., 1992 : Interferon-dependent tyrosine phosphorylation of a latent cytoplasmic transcription factor. Science 257, 809 813.
92. Sengupta J, Dhawan L, Ghosh D, 2003 : Immunohistochemical localization of leukemia inhibitory factor, interleukins 1 and 6 at the primary implantation site in the rhesus monkey. Cytokine 24, 277 285.
93. Sherwin JR, Freeman TC, Stephens RJ, Kimber S, Smith AG, Chambers I, Smith SK, Sharkey AM, 2004 : Identification of genes regulated by leukemia-inhibitory factor in the mouse uterus at the time of implantation. Mol Endocrinol 18, 2185 2195.
94. Sjoblom C, Wikland M, Robertson SA, 1999 : Granulocyte-macrophage colony-stimulating factor promotes human blastocyst development in vitro. Hum Reprod 14, 3069 3076.
95. Sjoblom C, Roberts CT, Wikland M, Robertson SA, 2005 : Granulocyte-macrophage colony-stimulating factor alleviates adverse consequences of embryo culture on fetal growth trajectory and placental morphogenesis. Endocrinology 146, 2142 2153.
96. Spencer TE, Becker WC, George P, Mirando MA, Ogle TF, Bazer FW, 1995 : Ovine interferon-τ regulates expression of endometrial receptors for estrogen and oxytocin but not progesterone. Biol Reprod 53, 732 745.
97. Spencer TE, Johnson GA, Burghardt RC, Bazer FW, 2004 : Progesterone and placental hormone actions on the uterus: insights from domestic animals. Biol Reprod 71, 2 10.
98. Starkey PM, 1991 : Expression on cells of early human pregnancy decidua, of the p75, IL-2 and p145, IL-4 receptor proteins. Immunology 73, 64 70.
99. Stewart DM, Johnson GA, Vyhlidal CA, Burghardt RC, Safe SH, Yu-Lee LY, Bazer FW, Spencer TE, 2001 : Interferon-τ activates multiple signal transducer and activator of transcription proteins and has complex effects on interferon-responsive gene transcription in ovine endometrial epithelial cells. Endocrinology 142, 98 107.
100. Stewart-Akers AM, Krasnow JS, Brekosky J, DeLoia JA, 1998 : Endometrial leukocytes are altered numerically and functionally in women with implantation defects. Am J Reprod Immunol 39, 1 11.
101. Subramaniam PS, Khan SA, Pontzer CH, Johnson HM, 1995 : Differential recognition of the type I interferon receptor by interferons tau and alpha is responsible for their disparate cytotoxicities. Proc Natl Acad Sci USA 92, 12270 12274.
102. Sugimoto N, Nakahira M, Ahn HJ, Micallef M, Hamaoka T, Kurimoto M, Fujiwara H, 2003 : Differential requirements for JAK2 and TYK2 in T cell proliferation and IFN-γ production induced by IL-12 alone or together with IL-18. Eur J Immunol 33, 243 251.
103. Sugita K, Hayakawa S, Karasaki-Suzuki M, Hagiwara H, Chishima F, Aleemuzaman S, Li JA, Nishinarita S, Yamamoto T, 2003 : Granulocyte colony stimulation factor (G-CSF) suppresses interleukin (IL)-12 and/or IL-2 induced interferon (IFN-γ) production and cytotoxicity of decidual mononuclear cells. Am J Reprod Immunol 50, 83 89.
104. Szereday L, Varga P, Szekeres-Bartho J, 1997 : Cytokine production by lymphocytes in pregnancy. Am J Reprod Immunol 38, 418 422.
105. Tabibzadeh S, Kong QF, Babaknia A, May LT, 1995 : Progressive rise in the expression of interleukin-6 in human endometrium during menstrual cycle is initiated during the implantation window. Hum Reprod 10, 2793 2799.
106. Takeda K, Tanaka T, Shi W, Matsumoto M, Minami M, Kashiwamura S, Nakanishi K, Yoshida N, Kishimoto T, Akira S, 1996 : Essential role of Stat6 in IL-4 signalling. Nature 380, 627 630.
107. Takeda K, Noguchi K, Shi W, Tanaka T, Matsumoto M, Yoshida N, Kishimoto T, Akira S, 1997 : Targeted disruption of the mouse Stat3 gene leads to early embryonic lethality. Proc Natl Acad Sci USA 94, 3801 3804.
108. Tekin S, Ealy AD, Wang SZ, Hansen PJ, 2000 : Differences in lymphocyte-regulatory activity among variants of ovine IFN-τ. J Interferon Cytokine Res 20, 1001 1005.
109. Teng CB, Diao HL, Ma H, Cong J, Yu H, Ma XH, Xu LB, Yang ZM, 2004a : Signal transducer and activator of transcription 3 (Stat3) expression and activation in rat uterus during early pregnancy. Reproduction 128, 197 205.
110. Teng CB, Diao HL, Ma XH, Xu LB, Yang ZM, 2004b : Differential expression and activation of Stat3 during mouse embryo implantation and decidualization. Mol Reprod Dev 69, 1 10.
111. von Wolff M, Thaler CJ, Strowitzki T, Broome J, Stolz W, Tabibzadeh S, 2000 : Regulated expression of cytokines in human endometrium throughout the menstrual cycle: dysregulation in habitual abortion. Mol Hum Reprod 6, 627 634.
112. Watford WT, Hissong BD, Bream JH, Kanno Y, Muul L, O'Shea JJ, 2004 : Signaling by IL-12 and IL-23 and the immunoregulatory roles of STAT4. Immunol Rev 202, 139 156.
113. Wilson R, Jenkins C, Miller H, McInnes IB, Moore J, McLean MA, Walker JJ, 2004 : Abnormal cytokine levels in non-pregnant women with a history of recurrent miscarriage. Eur J Obstet Gynecol Reprod Biol 115, 51 54.
114. Wu W, Coss D, Lorenson MY, Kuo CB, Xu X, Walker AM, 2003 : Different biological effects of unmodified prolactin and a molecular mimic of phosphorylated prolactin involve different signaling pathways. Biochemistry 42, 7561 7570.
115. Xiao CW, Liu JM, Sirois J, Goff AK, 1998 : Regulation of cyclooxygenase-2 and prostaglandin F synthase gene expression by steroid hormones and interferon-τ in bovine endometrial cells. Endocrinology 139, 2293 2299.
116. Xuan YT, Guo Y, Zhu Y, Han H, Langenbach R, Dawn B, Bolli R, 2003 : Mechanism of cyclooxygenase-2 upregulation in late preconditioning. J Mol Cell Cardiol 35, 525 537.
117. Yeaman GR, Collins JE, Currie JK, Guyre PM, Wira CR, Fanger MW, 1998 : IFN-γ is produced by polymorphonuclear neutrophils in human uterine endometrium and by cultured peripheral blood polymorphonuclear neutrophils. J Immunol 160, 5145 5153.
118. Zhong L, Parmer TG, Robertson MC, Gibori G, 1997 : Prolactin-mediated inhibition of 20 α-hydroxysteroid dehydrogenase gene expression and the tyrosine kinase system. Biochem Biophys Res Commun 235, 587 592.
119. Zoumpoulidou G, Jones MC, Fernandez de Mattos S, Francis JM, Fusi L, Lee YS, Christian M, Varshochi R, Lam EW, Brosens JJ, 2004 : Convergence of interferon-γ and progesterone signaling pathways in human endometrium: role of PIASy (protein inhibitor of activated signal transducer and activator of transcription-y). Mol Endocrinol 18, 1988 1999.