The role of growth factors and cytokines during implantation:Endocrine and paracrine interactions

Seminars in Reproductive Medicine

Volumn 27, Issue 1, 2009, Pages 62-79

  Guzeloglu Kayisli, Ozlem ^a   Kayisli, Umit Ali ^a   Taylor, Hugh S ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Blastocyst; Endometrium; Implantation; Pregnancy; Uterine biology

Indexed keywords

CHORIONIC GONADOTROPIN; CYTOKINE; EPIDERMAL GROWTH FACTOR; ESTROGEN; FOLLITROPIN; FORKHEAD TRANSCRIPTION FACTOR; GROWTH FACTOR; HEPARIN BINDING EPIDERMAL GROWTH FACTOR; INTERLEUKIN 1; INTERLEUKIN 11; INTERLEUKIN 15; INTERLEUKIN 6; JANUS KINASE; LEUKEMIA INHIBITORY FACTOR; PROGESTERONE; SOMATOMEDIN BINDING PROTEIN 1; SOMATOMEDIN C; STAT PROTEIN; THYROTROPIN; TRANSCRIPTION FACTOR; TRANSFORMING GROWTH FACTOR ALPHA; TRANSFORMING GROWTH FACTOR BETA; VASCULOTROPIN;

AUTOCRINE EFFECT; BLASTOCYST; ENDOCRINE FUNCTION; HOMEOBOX; HORMONAL REGULATION; HUMAN; MOLECULAR INTERACTION; NIDATION; NONHUMAN; PARACRINE SIGNALING; PREIMPLANTATION EMBRYO; PROTEIN FUNCTION; REPRODUCTION; REVIEW; SIGNAL TRANSDUCTION; UTERUS FUNCTION;

ANIMALS; CYTOKINES; EMBRYO IMPLANTATION; EMBRYONIC DEVELOPMENT; ENDOCRINE CELLS; FEMALE; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MODELS, BIOLOGICAL; PARACRINE COMMUNICATION; PREGNANCY; TRANSCRIPTION FACTORS;

EID: 61449260047     PISSN: 15268004     EISSN: 15264564     Source Type: Journal    
DOI: 10.1055/s-0028-1108011     Document Type: Review

References (199)

1. Tazuke SI, Giudice LC. Growth factors and cytokines in endometrium, embryonic development, and maternal:em- bryonic interactions. Semin Reprod Endocrinol 1996;14:231-245
2. Carson DD, Bagchi I, Dey SK, et al. Embryo implantation. Dev Biol 2000;223:217-237
3. Ogita H, Takai Y. Cross-talk among integrin, cadherin, and growth factor receptor:roles of nectin and nectin-like molecule. Int Rev Cytol 2008;265:1-54
4. O'Hayre M, Salanga CL, Handel TM, Allen SJ. Chemokines and cancer:migration, intracellular signalling and intercellular communication in the microenvironment. Biochem J 2008;409:635-649
5. Dey SK, Lim H, Das SK, et al. Molecular cues to implantation. Endocr Rev 2004;25:341-373
6. Makrigiannakis A, Minas V, Kalantaridou SN, Nikas G, Chrousos GP. Hormonal and cytokine regulation of early implantation. Trends Endocrinol Metab 2006;17:178- 185
7. Metcalf D. Hematopoietic cytokines. Blood 2008;111:485- 491
8. Whitman M, Melton DA. Growth factors in early embryo- genesis. Annu Rev Cell Biol 1989;5:93-117
9. Duc-Goiran P, Mignot TM, Bourgeois C, Ferre F. Embryo-maternal interactions at the implantation site:a delicate equilibrium. Eur J Obstet Gynecol Reprod Biol 1999;83:85-100
10. Makrigiannakis A, Minas V. Mechanisms of implantation. Reprod Biomed Online 2007;14:102-109
11. Red-Horse K, Zhou Y, Genbacev O, et al. Trophoblast differentiation during embryo implantation and formation of the maternal-fetal interface. J Clin Invest 2004;114:744-754
12. Wilcox AJ, Weinberg CR, O'Connor JF, et al. Incidence of early loss of pregnancy. N Engl J Med 1988;319:189-194
13. Norwitz ER, Schust DJ, Fisher SJ. Implantation and the survival of early pregnancy. N Engl J Med 2001;345:1400-1408
14. Simon C, Caballero-Campo P, Garcia-Velasco JA, Pellicer A. Potential implications of chemokines in reproductive function:an attractive idea. J Reprod Immunol 1998;38:169-193
15. Taylor E, Gomel V. The uterus and fertility. Fertil Steril 2008;89:1-16
16. Braude P, Bolton V, Moore S. Human gene expression first occurs between the four- and eight-cell stages of preim-plantation development. Nature 1988;332:459-461
17. Flach G, Johnson MH, Braude PR, Taylor RA, Bolton VN. The transition from maternal to embryonic control in the 2-cell mouse embryo. EMBO J 1982;1:681-686
18. Richter JD. Cytoplasmic polyadenylation in development and beyond. Microbiol Mol Biol Rev 1999;63:446-456
19. Yamanaka Y, Ralston A, Stephenson RO, Rossant J. Cell and molecular regulation of the mouse blastocyst. Dev Dyn 2006;235:2301-2314
20. Kodaman PH, Taylor HS. Hormonal regulation of implantation. Obstet Gynecol Clin North Am 2004;31:745-766
21. Lunghi L, Ferretti ME, Medici S, Biondi C, Vesce F. Control of human trophoblast function. Reprod Biol Endocrinol 2007;5:6
22. Johnson MH, McConnell JM. Lineage allocation and cell polarity during mouse embryogenesis. Semin Cell Dev Biol 2004;15:583-597
23. Takaoka K, Yamamoto M, Shiratori H, et al. The mouse embryo autonomously acquires anterior-posterior polarity at implantation. Dev Cell 2006;10:451-459
24. Tabin CJ. The key to left-right asymmetry. Cell 2006;127:27-32
25. Tabibzadeh S, Shea W, Lessey BA, Broome J. From endometrial receptivity to infertility. Semin Reprod Endocrinol 1999;17:197-203
26. Simmons DG, Cross JC. Determinants of trophoblast lineage and cell subtype specification in the mouse placenta. Dev Biol 2005;284:12-24
27. Strowitzki T, Germeyer A, Popovici R, von Wolff M. The human endometrium as a fertility-determining factor. Hum Reprod Update 2006;12:617-630
28. Kayisli UA, Guzeloglu-Kayisli O, Arici A. Endocrine-immune interactions in human endometrium. Ann N Y Acad Sci 2004;1034:50-63
29. Aplin JD. Embryo implantation:the molecular mechanism remains elusive. Reprod Biomed Online 2006;13:833-839
30. Armant DR, Wang J, Liu Z. Intracellular signaling in the developing blastocyst as a consequence of the maternal- embryonic dialogue. Semin Reprod Med 2000;18:273-287
31. Tabibzadeh S, Babaknia A. The signals and molecular pathways involved in implantation, a symbiotic interaction between blastocyst and endometrium involving adhesion and tissue invasion. Hum Reprod 1995;10:1579-1602
32. Sharkey AM, Smith SK. The endometrium as a cause of implantation failure. Best Pract Res Clin Obstet Gynaecol 2003;17:289-307
33. Nikas G. Endometrial receptivity:changes in cell-surface morphology. Semin Reprod Med 2000;18:229-235
34. Kao LC, Tulac S, Lobo S, et al. Global gene profiling in human endometrium during the window of implantation. Endocrinology 2002;143:2119-2138
35. Sherwin JR, Sharkey AM, Cameo P, et al. Identification of novel genes regulated by chorionic gonadotropin in baboon endometrium during the window of implantation. Endocrinology 2007;148:618-626
36. Enders AC. Trophoblast-uterine interactions in the first days of implantation:models for the study of implantation events in the human. Semin Reprod Med 2000;18:255-263
37. Lessey BA, Palomino WA, Apparao KB, Young SL, Lininger RA. Estrogen receptor-alpha (ER-alpha) and defects in uterine receptivity in women. Reprod Biol Endocrinol 2006;4(suppl 1):S9
38. Achache H, Revel A. Endometrial receptivity markers, the journey to successful embryo implantation. Hum Reprod Update 2006;12:731-746
39. Huet-Hudson YM, Dey SK. Requirement for progesterone priming and its long-term effects on implantation in the mouse. Proc Soc Exp Biol Med 1990;193:259-263
40. Carpenter KD, Korach KS. Potential biological functions emerging from the different estrogen receptors. Ann N Y Acad Sci 2006;1092:361-373
41. Hewitt SC, Korach KS. Progesterone action and responses in the alpha ERKO mouse. Steroids 2000;65:551-557
42. Cooke PS, Buchanan DL, Young P, et al. Stromal estrogen receptors mediate mitogenic effects of estradiol on uterine epithelium. Proc Natl Acad Sci USA 1997;94:6535-6540
43. Curtis SW, Clark J, Myers P, Korach KS. Disruption of estrogen signaling does not prevent progesterone action in the estrogen receptor alpha knockout mouse uterus. Proc Natl Acad Sci USA 1999;96:3646-3651
44. Paria BC, Tan J, Lubahn DB, Dey SK, Das SK. Uterine decidual response occurs in estrogen receptor-alpha-deficient mice. Endocrinology 1999;140:2704-2710
45. Conneely OM, Jericevic BM. Progesterone regulation of reproductive function through functionally distinct progesterone receptor isoforms. Rev Endocr Metab Disord 2002;3:201-209
46. Nelson KG, Takahashi T, Bossert NL, Walmer DK, McLachlan JA. Epidermal growth factor replaces estrogen in the stimulation of female genital-tract growth and differentiation. Proc Natl Acad Sci USA 1991;88:21-25
47. Ignar-Trowbridge DM, Nelson KG, Bidwell MC, et al. Coupling of dual signaling pathways:epidermal growth factor action involves the estrogen receptor. Proc Natl Acad Sci USA 1992;89:4658-4662
48. Johnson DC, Chatterjee S. Epidermal growth factor (EGF) replaces estradiol for the initiation of embryo implantation in the hypophysectomized rat. Placenta 1993;14:429-438
49. Perrier d'Hauterive S, Berndt S, Tsampalas M, et al. Dialogue between blastocyst hCG and endometrial LH/hCG receptor:which role in implantation? Gynecol Obstet Invest 2007;64:156-160
50. Licht P, Russu V, Wildt L. On the role of human chorionic gonadotropin (hCG) in the embryo-endometrial micro-environment:implications for differentiation and implantation. Semin Reprod Med 2001;19:37-47
51. Zygmunt M, Hahn D, Munstedt K, Bischof P, Lang U. Invasion of cytotrophoblastic JEG-3 cells is stimulated by hCG in vitro. Placenta 1998;19:587-593
52. Milwidsky A, Finci-Yeheskel Z, Yagel S, Mayer M. Gonadotropin-mediated inhibition of proteolytic enzymes produced by human trophoblast in culture. J Clin Endocrinol Metab 1993;76:1101-1105
53. Yagel S, Geva TE, Solomon H, et al. High levels of human chorionic gonadotropin retard first trimester trophoblast invasion in vitro by decreasing urokinase plasminogen activator and collagenase activities. J Clin Endocrinol Metab 1993;77:1506-1511
54. Simón C, Martin JC, Pellicer A. Paracrine regulators of implantation. Baillieres Best Pract Res Clin Obstet Gynaecol 2000;14:815-826
55. Laird SM, Tuckerman EM, Li TC. Cytokine expression in the endometrium of women with implantation failure and recurrent miscarriage. Reprod Biomed Online 2006;13:
56. 13-23
57. Duval D, Reinhardt B, Kedinger C, Boeuf H. Role of suppressors of cytokine signaling (Socs) in leukemia inhibitory factor (LIF)-dependent embryonic stem cell survival. FASEB J 2000;14:1577-1584
58. Arici A, Engin O, Attar E, Olive DL. Modulation of leukemia inhibitory factor gene expression and protein biosynthesis in human endometrium. J Clin Endocrinol Metab 1995;80:1908-1915
59. Charnock-Jones DS, Sharkey AM, Fenwick P, Smith SK. Leukaemia inhibitory factor mRNA concentration peaks in human endometrium at the time of implantation and the blastocyst contains mRNA for the receptor at this time. J Reprod Fertil 1994;101:421-426
60. Aghajanova L, Stavreus-Evers A, Nikas Y, Hovatta O, Landgren BM. Coexpression of pinopodes and leukemia inhibitory factor, as well as its receptor, in human endometrium. Fertil Steril 2003;79(Suppl 1):808-814
61. Cullinan EB, Abbondanzo SJ, Anderson PS, Pollard JW, Lessey BA, Stewart CL. Leukemia inhibitory factor (LIF) and LIF receptor expression in human endometrium suggests a potential autocrine/paracrine function in regulating embryo implantation. Proc Natl Acad Sci USA 1996;93:3115-3120
62. Vogiagis D, Marsh MM, Fry RC, Salamonsen LA. Leukaemia inhibitory factor in human endometrium throughout the menstrual cycle. J Endocrinol 1996;148:95-102
63. Sharkey AM, King A, Clark DE, et al. Localization of leukemia inhibitory factor and its receptor in human placenta throughout pregnancy. Biol Reprod 1999;60:355-364
64. Lessey BA, Gui Y, Apparao KB, Young SL, Mulholland J. Regulated expression of heparin-binding EGF-like growth factor (HB-EGF) in the human endometrium:a potential paracrine role during implantation. Mol Reprod Dev 2002;62:446-455
65. Song H, Lim H, Das SK, Paria BC, Dey SK. Dysregulation of EGF family of growth factors and COX-2 in the uterus during the preattachment and attachment reactions of the blastocyst with the luminal epithelium correlates with implantation failure in LIF-deficient mice. Mol Endocrinol 2000;14:1147-1161
66. Laird SM, Tuckerman EM, Dalton CF, Dunphy BC, Li TC, Zhang X. The production of leukaemia inhibitory factor by human endometrium:presence in uterine flushings and production by cells in culture. Hum Reprod 1997;12:569-574
67. Ledee-Bataille N, Lapree-Delage G, Taupin JL, Dubanchet S, Frydman R, Chaouat G. Concentration of leukaemia inhibitory factor (LIF) in uterine flushing fluid is highly predictive of embryo implantation. Hum Reprod 2002;17:213-218
68. Giess R, Tanasescu I, Steck T, Sendtner M. Leukaemia inhibitory factor gene mutations in infertile women. Mol Hum Reprod 1999;5:581-586
69. Steck T, Giess R, Suetterlin MW, et al. Leukaemia inhibitory factor (LIF) gene mutations in women with unexplained infertility and recurrent failure of implantation after IVF and embryo transfer. Eur J Obstet Gynecol Reprod Biol 2004;112:69-73
70. Escary JL, Perreau J, Dumenil D, Ezine S, Brulet P. Leukaemia inhibitory factor is necessary for maintenance of haematopoietic stem cells and thymocyte stimulation. Nature 1993;363:361-364
71. Stewart CL, Kaspar P, Brunet LJ, et al. Blastocyst implantation depends on maternal expression of leukaemia inhibitory factor. Nature 1992;359:76-79
72. Dunglison GF, Barlow DH, Sargent IL. Leukaemia inhibitory factor significantly enhances the blastocyst formation rates of human embryos cultured in serum-free medium. Hum Reprod 1996;11:191-196
73. Nichols J, Davidson D, Taga T, Yoshida K, Chambers I, Smith A. Complementary tissue-specific expression of LIF and LIF-receptor mRNAs in early mouse embryogenesis. Mech Dev 1996;57:123-131
74. Ware CB, Horowitz MC, Renshaw BR, et al. Targeted disruption of the low-affinity leukemia inhibitory factor receptor gene causes placental, skeletal, neural and metabolic defects and results in perinatal death. Development 1995;121:1283-1299
75. Yoshida K, Taga T, Saito M, et al. Targeted disruption of gp130, a common signal transducer for the interleukin 6 family of cytokines, leads to myocardial and hematological disorders. Proc Natl Acad Sci USA 1996;93:407-411
76. Sharkey AM, Dellow K, Blayney M, Macnamee M, Charnock-Jones S, Smith SK. Stage-specific expression of cytokine and receptor messenger ribonucleic acids in human preimplantation embryos. Biol Reprod 1995;53:974-981
77. Sherwin JR, Smith SK, Wilson A, Sharkey AM. Soluble gp130 is up-regulated in the implantation window and shows altered secretion in patients with primary unexplained infertility. J Clin Endocrinol Metab 2002;87:3953-3960
78. Gearing DP, Thut CJ, VandeBos T, et al. Leukemia inhibitory factor receptor is structurally related to the IL-6 signal transducer, gp130. EMBO J 1991;10:2839-2848
79. Robertson SA, O'Connell A, Ramsey A. The effect of interleukin-6 deficiency on implantation, fetal development and parturition in mice. Proc Aust Soc Reprod Biol 2000;31:97
80. Nasu K, Matsui N, Narahara H, Tanaka Y, Miyakawa I. Effects of interferon-gamma on cytokine production by endometrial stromal cells. Hum Reprod 1998;13:2598-2601
81. Jauniaux E, Gulbis B, Schandene L, Collette J, Hustin J. Distribution of interleukin-6 in maternal and embryonic tissues during the first trimester. Mol Hum Reprod 1996;2:239-243
82. Stephanou A, Myatt L, Eis AL, Sarlis N, Jikihara H, Handwerger S. Ontogeny of the expression and regulation of interleukin-6 (IL-6) and IL-1 mRNAs by human trophoblast cells during differentiation in vitro. J Endocrinol 1995;147:487-496
83. Jasper MJ, Tremellen KP, Robertson SA. Reduced expression of IL-6 and IL-1alpha mRNAs in secretory phase endometrium of women with recurrent miscarriage. J Reprod Immunol 2007;73:74-84
84. Du XX, Williams DA. Interleukin-11:a multifunctional growth factor derived from the hematopoietic microenvironment. Blood 1994;83:2023-2030
85. Sands BE, Bank S, Sninsky CA, et al. Preliminary evaluation of safety and activity of recombinant human interleukin 11 in patients with active Crohn's disease. Gastroenterology 1999;117:58-64
86. Cork BA, Li TC, Warren MA, Laird SM. Interleukin-11 (IL-11) in human endometrium:expression throughout the menstrual cycle and the effects of cytokines on endometrial IL-11 production in vitro. J Reprod Immunol 2001;50:3-17
87. Dimitriadis E, Salamonsen LA, Robb L. Expression of interleukin-11 during the human menstrual cycle:coincidence with stromal cell decidualization and relationship to leukaemia inhibitory factor and prolactin. Mol Hum Reprod 2000;6:907-914
88. von Rango U, Alfer J, Kertschanska S, et al. Interleukin-11 expression:its significance in eutopic and ectopic human implantation. Mol Hum Reprod 2004;10:783-792
89. Chen HF, Lin CY, Chao KH, Wu MY, Yang YS, Ho HN. Defective production of interleukin-11 by decidua and chorionic villi in human anembryonic pregnancy. J Clin Endocrinol Metab 2002;87:2320-2328
90. Cork BA, Tuckerman EM, Li TC, Laird SM. Expression of interleukin (IL)-11 receptor by the human endometrium in vivo and effects of IL-11, IL-6 and LIF on the production of MMP and cytokines by human endometrial cells in vitro. Mol Hum Reprod 2002;8:841-848
91. Dimitriadis E, Robb L, Salamonsen LA. Interleukin 11 advances progesterone-induced decidualization of human endometrial stromal cells. Mol Hum Reprod 2002;8:636-643
92. Popovici RM, Kao LC, Giudice LC. Discovery of new inducible genes in in vitro decidualized human endometrial stromal cells using microarray technology. Endocrinology 2000;141:3510-3513
93. Tierney EP, Tulac S, Huang ST, Giudice LC. Activation of the protein kinase A pathway in human endometrial stromal cells reveals sequential categorical gene regulation. Physiol Genomics 2003;16:47-66
94. 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
95. Kang J, Der SD. Cytokine functions in the formative stages of a lymphocyte's life. Curr Opin Immunol 2004;16:180-190
96. Eriksson M, Meadows SK, Wira CR, Sentman CL. Unique phenotype of human uterine NK cells and their regulation by endogenous TGF-beta. J Leukoc Biol 2004;76:667-675
97. Verma S, Hiby SE, Loke YW, King A. Human decidual natural killer cells express the receptor for and respond to the cytokine interleukin 15. Biol Reprod 2000;62:959-968
98. 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
99. Ashkar AA, Black GP, Wei Q, 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
100. Dunn CL, Critchley HO, Kelly RW. IL-15 regulation in human endometrial stromal cells. J Clin Endocrinol Metab 2002;87:1898-1901
101. Bankers-Fulbright JL, Kalli KR, McKean DJ. Interleukin-1 signal transduction. Life Sci 1996;59:61-83
102. Svenson M, Hansen MB, Heegaard P, Abell K, Bendtzen K. Specific binding of interleukin 1 (IL-1) beta and IL-1 receptor antagonist (IL-1ra) to human serum. High-affinity binding of IL-1ra to soluble IL-1 receptor type I. Cytokine 1993;5:427-435
103. Bischof P, Campana A. Molecular mediators of implantation. Baillieres Best Pract Res Clin Obstet Gynaecol 2000;14:801-814
104. Vigano P, Mangioni S, Pompei F, Chiodo I. Maternal- conceptus cross talk-a review. Placenta 2003;24(Suppl B):S56-S61
105. Hofmann GE, Scott RT Jr, Bergh PA, Deligdisch L. Immunohistochemical localization of epidermal growth factor in human endometrium, decidua, and placenta. J Clin Endocrinol Metab 1991;73:882-887
106. Bass KE, Morrish D, Roth I, et al. Human cytotrophoblast invasion is up-regulated by epidermal growth factor:evidence that paracrine factors modify this process. Dev Biol 1994;164:550-561
107. Li RH, Zhuang LZ. The effects of growth factors on human normal placental cytotrophoblast cell proliferation. Hum Reprod 1997;12:830-834
108. Kamei Y, Tsutsumi O, Kuwabara Y, Taketani Y. Intra- uterine growth retardation and fetal losses are caused by epidermal growth factor deficiency in mice. Am J Physiol 1993;264:R597-R600
109. 108.Tsutsumi O, Oka T. Epidermal growth factor deficiency during pregnancy causes abortion in mice. Am J Obstet Gynecol 1987;156:241-244
110. Johnson DC, Banerjee S, Chatterjee S. Estradiol and chlordecone (Kepone) decrease adenosine 3',5'-cyclic mono- phosphate concentrations in the ovariectomized immature rat uterus. Proc Soc Exp Biol Med 1995;210:33-38
111. Threadgill DW, Dlugosz AA, Hansen LA, et al. Targeted disruption of mouse EGF receptor:effect of genetic background on mutant phenotype. Science 1995;269:230-234
112. De La Fuente R, O'Brien MJ, Eppig JJ. Epidermal growth factor enhances preimplantation developmental competence of maturing mouse oocytes. Hum Reprod 1999;14:3060-3068
113. Goldman S, Gonen Y. Monoclonal antibodies against epidermal growth factor prevent outgrowth of mouse embryos in vitro. Hum Reprod 1998;13:2231-2233
114. Harvey MB, Leco KJ, Arcellana-Panlilio MY, Zhang X, Edwards DR, Schultz GA. Proteinase expression in early mouse embryos is regulated by leukaemia inhibitory factor and epidermal growth factor. Development 1995;121:1005-1014
115. Khamsi F, Armstrong DT, Zhang X. Expression of urokinase-type plasminogen activator in human preimplantation embryos. Mol Hum Reprod 1996;2:273-276
116. Wiley LM, Wu JX, Harari I, Adamson ED. Epidermal growth factor receptor mRNA and protein increase after the four-cell preimplantation stage in murine development. Dev Biol 1992;149:247-260
117. Lim H, Das SK, Dey SK. erbB genes in the mouse uterus:cell-specific signaling by epidermal growth factor (EGF) family of growth factors during implantation. Dev Biol 1998;204:97-110
118. Surveyor GA, Gendler SJ, Pemberton L, et al. Expression and steroid hormonal control of Muc-1 in the mouse uterus. Endocrinology 1995;136:3639-3647
119. Das SK, Chakraborty I, Paria BC, Wang XN, Plowman G, Dey SK. Amphiregulin is an implantation-specific and progesterone-regulated gene in the mouse uterus. Mol Endocrinol 1995;9:691-705
120. Das SK, Das N, Wang J, et al. Expression of betacellulin and epiregulin genes in the mouse uterus temporally by the blastocyst solely at the site of its apposition is coincident with the ''window'' of implantation. Dev Biol 1997;190:178-190
121. Leach RE, Khalifa R, Ramirez ND, et al. Multiple roles for heparin-binding epidermal growth factor-like growth factor are suggested by its cell-specific expression during the human endometrial cycle and early placentation. J Clin Endocrinol Metab 1999;84:3355-3363
122. Yoo HJ, Barlow DH, Mardon HJ. Temporal and spatial regulation of expression of heparin-binding epidermal growth factor-like growth factor in the human endometrium:a possible role in blastocyst implantation. Dev Genet 1997;21:102-108
123. Martin KL, Barlow DH, Sargent IL. Heparin-binding epidermal growth factor significantly improves human blastocyst development and hatching in serum-free medium. Hum Reprod 1998;13:1645-1652
124. Chobotova K, Spyropoulou I, Carver J, et al. Heparin- binding epidermal growth factor and its receptor ErbB4 mediate implantation of the human blastocyst. Mech Dev 2002;119:137-144
125. Tabibzadeh S, Hemmati-Brivanlou A. Lefty at the crossroads of ''stemness'' and differentiative events. Stem Cells 2006;24:1998-2006
126. Feinberg RF, Kliman HJ, Wang CL. Transforming growth factor-beta stimulates trophoblast oncofetal fibronectin synthesis in vitro:implications for trophoblast implantation in vivo. J Clin Endocrinol Metab 1994;78:1241-1248
127. Tamada H, McMaster MT, Flanders KC, Andrews GK, Dey SK. Cell type-specific expression of transforming growth factor-beta 1 in the mouse uterus during the periimplantation period. Mol Endocrinol 1990;4:965-972
128. Mazella J, Tang M, Tseng L. Disparate effects of relaxin and TGFbeta1:relaxin increases, but TGFbeta1 inhibits, the relaxin receptor and the production of IGFBP-1 in human endometrial stromal/decidual cells. Hum Reprod 2004;19:1513-1518
129. Kulkarni AB, 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
130. Graham CH, Connelly I, MacDougall JR, Kerbel RS, Stetler-Stevenson WG, Lala PK. Resistance of malignant trophoblast cells to both the anti-proliferative and anti-invasive effects of transforming growth factor-beta. Exp Cell Res 1994;214:93-99
131. Caniggia I, Winter J, Lye SJ, Post M. Oxygen and placental development during the first trimester:implications for the pathophysiology of pre-eclampsia. Placenta 2000;21(supplA):S25-S30
132. Djurovic S, Schjetlein R, Wisloff F, Haugen G, Husby H, Berg K. Plasma concentrations of Lp(a) lipoprotein and TGF-beta1 are altered in preeclampsia. Clin Genet 1997;52:371-376
133. Hamilton GS, Lysiak JJ, Han VK, Lala PK. Autocrine-paracrine regulation of human trophoblast invasiveness by insulin-like growth factor (IGF)-II and IGF-binding protein (IGFBP)-1. Exp Cell Res 1998;244:147-156
134. Irving JA, Lala PK. Functional role of cell surface integrins on human trophoblast cell migration:regulation by TGF-beta, IGF-II, and IGFBP-1. Exp Cell Res 1995;217:419- 427
135. Irwin JC, de las Fuentes L, Dsupin BA, Giudice LC. Insulin-like growth factor regulation of human endometrial stromal cell function:coordinate effects on insulin-like growth factor binding protein-1, cell proliferation and prolactin secretion. Regul Pept 1993;48(1-2):165-177
136. Fowler DJ, Nicolaides KH, Miell JP. Insulin-like growth factor binding protein-1 (IGFBP-1):a multifunctional role in the human female reproductive tract. Hum Reprod Update 2000;6:495-504
137. Han VK, Bassett N, Walton J, Challis JR. The expression of insulin-like growth factor (IGF) and IGF-binding protein (IGFBP) genes in the human placenta and membranes:evidence for IGF-IGFBP interactions at the feto-maternal interface. J Clin Endocrinol Metab 1996;81(7):2680-2693
138. Makarevich AV, Markkula M. Apoptosis and cell proliferation potential of bovine embryos stimulated with insulinlike growth factor I during in vitro maturation and culture. Biol Reprod 2002;66:386-392
139. Kolle S, Stojkovic M, Boie G, Wolf E, Sinowatz F. Growth hormone-related effects on apoptosis, mitosis, and expression of connexin 43 in bovine in vitro maturation cumulusoocyte complexes. Biol Reprod 2003;68:1584-1589
140. Spanos S, Becker DL, Winston RM, Hardy K. Antiapoptotic action of insulin-like growth factor-I during human preimplantation embryo development. Biol Reprod 2000;63:1413-1420
141. Ferrara N. Vascular endothelial growth factor:basic science and clinical progress. Endocr Rev 2004;25:581-611
142. Maglione D, Guerriero V, Viglietto G, et al. Two alternative mRNAs coding for the angiogenic factor, placenta growth factor (PlGF), are transcribed from a single gene of chromosome 14. Oncogene 1993;8:925-931
143. Olofsson B, Korpelainen E, Pepper MS, et al. Vascular endothelial growth factor B (VEGF-B) binds to VEGF receptor-1 and regulates plasminogen activator activity in endothelial cells. Proc Natl Acad Sci USA 1998;95:11709-11714
144. Joukov V, Sorsa T, Kumar V, et al. Proteolytic processing regulates receptor specificity and activity of VEGF-C. EMBO J 1997;16:3898-3911
145. Achen MG, Jeltsch M, Kukk E, et al. Vascular endothelial growth factor D (VEGF-D) is a ligand for the tyrosine kinases VEGF receptor 2 (Flk1) and VEGF receptor 3 (Flt4). Proc Natl Acad Sci USA 1998;95:548-553
146. Cunningham SA, Tran TM, Arrate MP, Brock TA. Characterization of vascular endothelial cell growth factor interactions with the kinase insert domain-containing receptor tyrosine kinase. A real time kinetic study. J Biol Chem 1999;274:18421-18427
147. Park JE, Chen HH, Winer J, Houck KA, Ferrara N. Placenta growth factor. Potentiation of vascular endothelial growth factor bioactivity, in vitro and in vivo, and high affinity binding to Flt-1 but not to Flk-1/KDR. J Biol Chem 1994;269:25646-25654
148. Vuorela P, Hatva E, Lymboussaki A, et al. Expression of vascular endothelial growth factor and placenta growth factor in human placenta. Biol Reprod 1997;56:489-494
149. Rabbani ML, Rogers PA. Role of vascular endothelial growth factor in endometrial vascular events before implantation in rats. Reproduction 2001;122:85-90
150. Rockwell LC, Pillai S, Olson CE, Koos RD. Inhibition of vascular endothelial growth factor/vascular permeability factor action blocks estrogen-induced uterine edema and implantation in rodents. Biol Reprod 2002;67:1804-1810
151. Nayak NR, Brenner RM. Vascular proliferation and vascular endothelial growth factor expression in the rhesus macaque endometrium. J Clin Endocrinol Metab 2002;87:1845-1855
152. Shifren JL, Tseng JF, Zaloudek CJ, et al. Ovarian steroid regulation of vascular endothelial growth factor in the human endometrium:implications for angiogenesis during the menstrual cycle and in the pathogenesis of endometriosis. J Clin Endocrinol Metab 1996;81:3112-3118
153. Greb RR, Heikinheimo O, Williams RF, Hodgen GD, Goodman AL. Vascular endothelial growth factor in primate endometrium is regulated by oestrogen-receptor and progesterone-receptor ligands in vivo. Hum Reprod 1997;12:1280-1292
154. Ancelin M, Buteau-Lozano H, Meduri G, et al. A dynamic shift of VEGF isoforms with a transient and selective progesterone-induced expression of VEGF189 regulates angiogenesis and vascular permeability in human uterus. Proc Natl Acad Sci USA 2002;99:6023-6028
155. Charnock-Jones DS, Sharkey AM, Rajput-Williams J, et al. Identification and localization of alternately spliced mRNAs for vascular endothelial growth factor in human uterus and estrogen regulation in endometrial carcinoma cell lines. Biol Reprod 1993;48:1120-1128
156. Krussel JS, Casan EM, Raga F, et al. Expression of mRNA for vascular endothelial growth factor transmembraneous receptors Flt1 and KDR, and the soluble receptor sflt in cycling human endometrium. Mol Hum Reprod 1999;5:452-458
157. Hornung D, Lebovic DI, Shifren JL, Vigne JL, Taylor RN. Vectorial secretion of vascular endothelial growth factor by polarized human endometrial epithelial cells. Fertil Steril 1998;69:909-915
158. Ghosh D, Kumar PG, Sengupta J. Effect of early luteal phase administration of mifepristone (RU486) on leukaemia inhibitory factor, transforming growth factor beta and vascular endothelial growth factor in the implantation stage endometrium of the rhesus monkey. J Endocrinol 1998;157:115-125
159. Ghosh D, Sharkey AM, Charnock-Jones DS, et al. Expression of vascular endothelial growth factor (VEGF) and placental growth factor (PlGF) in conceptus and endometrium during implantation in the rhesus monkey. Mol Hum Reprod 2000;6:935-941
160. Sengupta J, Lalitkumar PG, Najwa AR, et al. Immunoneu-tralization of vascular endothelial growth factor inhibits pregnancy establishment in the rhesus monkey (Macaca mulatta). Reproduction 2007;133:1199-1211
161. Lessey BA, Castelbaum AJ. Integrins and implantation in the human. Rev Endocr Metab Disord 2002;3:107-117
162. Acosta AA, Elberger L, Borghi M, et al. Endometrial dating and determination of the window of implantation in healthy fertile women. Fertil Steril 2000;73:788-798
163. Gonzalez RR, Palomino A, Boric A, Vega M, Devoto L. A quantitative evaluation of alpha1, alpha4, alphaV and beta3 endometrial integrins of fertile and unexplained infertile women during the menstrual cycle. A flow cytometric appraisal. Hum Reprod 1999;14:2485-2492
164. Aplin JD. Adhesion molecules in implantation. Rev Reprod 1997;2:84-93
165. Somkuti SG, Yuan L, Fritz MA, Lessey BA. Epidermal growth factor and sex steroids dynamically regulate a marker of endometrial receptivity in Ishikawa cells. J Clin Endocrinol Metab 1997;82:2192-2197
166. Lessey BA. Two pathways of progesterone action in the human endometrium:implications for implantation and contraception. Steroids 2003;68:809-815
167. Curry TE Jr, Osteen KG. The matrix metalloproteinase system:changes, regulation, and impact throughout the ovarian and uterine reproductive cycle. Endocr Rev 2003;24:428-465
168. Alexander CM, Hansell EJ, Behrendtsen O, et al. Expression and function of matrix metalloproteinases and their inhibitors at the maternal-embryonic boundary during mouse embryo implantation. Development 1996;122:1723-1736
169. Rinkenberger JL, Cross JC, Werb Z. Molecular genetics of implantation in the mouse. Dev Genet 1997;21:6-20
170. Vu TH, Werb Z. Matrix metalloproteinases:effectors of development and normal physiology. Genes Dev 2000;14:2123-2133
171. Anteby EY, Greenfield C, Natanson-Yaron S, et al. Vascular endothelial growth factor, epidermal growth factor and fibroblast growth factor-4 and -10 stimulate trophoblast plasminogen activator system and metalloproteinase-9. Mol Hum Reprod 2004;10:229-235
172. Taylor HS, Vanden Heuvel GB, Igarashi P. A conserved Hox axis in the mouse and human female reproductive system:late establishment and persistent adult expression of the Hoxa cluster genes. Biol Reprod 1997;57:1338-1345
173. Vitiello D, Kodaman PH, Taylor HS. HOX genes in implantation. Semin Reprod Med 2007;25:431-436
174. Krumlauf R. Hox genes in vertebrate development. Cell 1994;78:191-201
175. Benson GV, Lim H, Paria BC, Satokata I, Dey SK, Maas/SN>RL. Mechanisms of reduced fertility in Hoxa-10 mutant mice:uterine homeosis and loss of maternal Hoxa- 10 expression. Development 1996;122:2687-2696
176. Taylor HS, Arici A, Olive D, Igarashi P. HOXA10 is expressed in response to sex steroids at the time of implantation in the human endometrium. J Clin Invest 1998;101:1379-1384
177. Lim H, Ma L, Ma WG, Maas RL, Dey SK. Hoxa-10 regulates uterine stromal
178. Daftary GS, Taylor HS. Molecular markers of implantation:clinical implications. Curr Opin Obstet Gynecol 2001;13:269-274
179. Accili D, Arden KC. FoxOs at the crossroads of cellular metabolism, differentiation, and transformation. Cell 2004;117:421-426
180. Christian M, Zhang X, Schneider-Merck T, et al. Cyclic AMP-induced forkhead transcription factor, FKHR, cooperates with CCAAT/enhancer-binding protein beta in differentiating human endometrial stromal cells. J Biol Chem 2002;277:20825-20832
181. Dijkers PF, Medema RH, Pals C, et al. Forkhead transcription factor FKHR-L1 modulates cytokine-depend- ent transcriptional regulation of p27(KIP1). Mol Cell Biol 2000;20:9138-9148
182. Sunters A, Fernandez de Mattos S, Stahl M, et al. FoxO3a transcriptional regulation of Bim controls apoptosis in paclitaxel-treated breast cancer cell lines. J Biol Chem 2003;278:49795-49805
183. Labied S, Kajihara T, Madureira PA, et al. Progestins regulate the expression and activity of the forkhead transcription factor FOXO1 in differentiating human endometrium. Mol Endocrinol 2006;20(1):35-44
184. Chatzaki E, Makrigiannakis A, Margioris AN, Kouimtzoglou E, Gravanis A. The Fas/FasL apoptotic pathway is involved in kappa-opioid-induced apoptosis of human endometrial stromal cells. Mol Hum Reprod 2001;7:867-874
185. Takeda K, Noguchi K, Shi W, et al. Targeted disruption of the mouse Stat3 gene leads to early embryonic lethality. Proc Natl Acad Sci USA 1997;94:3801-3804
186. Cheng JG, Chen JR, Hernandez L, Alvord WG, Stewart CL. 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 2001;98:8680-8685
187. Salamonsen LA. Crosstalk between progesterone and interleukin-11 signal transduction pathways in human endometrial stromal cells during decidualization. Reprod Fertil Dev 2003;15:73
188. Underhill-Day N, McGovern LA, Karpovich N, Mardon HJ, Barton VA, Heath JK. Functional characterization of W147A:a high-affinity interleukin-11 antagonist. Endocrinology 2003;144:3406-3414
189. Dimitriadis E, Robb L, Liu YX, et al. IL-11 and IL-11Ralpha immunolocalisation at primate implantation sites supports a role for IL-11 in placentation and fetal development. Reprod Biol Endocrinol 2003;1:34
190. Corvinus FM, Fitzgerald JS, Friedrich K, Markert UR. Evidence for a correlation between trophoblast invasiveness and STAT3 activity. Am J Reprod Immunol 2003;50:316-321
191. Kirchhof N, Carnwath JW, Lemme E, Anastassiadis K, Scholer H, Niemann H. Expression pattern of Oct-4 in preimplantation embryos of different species. Biol Reprod 2000;63(6):1698-1705
192. Avilion AA, Nicolis SK, Pevny LH, Perez L, Vivian L, Lovell-Badge R. Multipotent cell lineages in early mouse development depend on SOX2 function. Genes Dev 2003;17(1):126-140
193. Mitsui K, Tokuzawa Y, Itoh H, et al. The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 2003;113(5):631-642
194. Niwa H, Toyooka Y, Shimosato D, et al. Interaction between Oct3/4 and Cdx2 determines trophectoderm differentiation. Cell 2005;123(5):917-929
195. Hsieh-Li HM, Witte DP, Weinstein M, et al. Hoxa 11 structure, extensive antisense transcription, and function in male and female fertility. Development 1995;121(5):1373-1385
196. Harris HA. Estrogen receptor-beta:recent lessons from in vivo studies. Mol Endocrinol 2007;(1):1-13
197. Mulac-Jericevic B, Mullinax RA, DeMayo FJ, Lydon JP, Conneely OM. Subgroup of reproductive functions of progesterone mediated by progesterone receptor-B isoform. Science 2000;289(5485):1751-1754
198. Mulac-Jericevic B, Lydon JP, DeMayo FJ, Conneely OM. Defective mammary gland morphogenesis in mice lacking the progesterone receptor B isoform. Proc Natl Acad Sci USA 2003;100(17):9744-9749
199. Lydon JP, DeMayo FJ, Funk CR, et al. Mice lacking progesterone receptor exhibit pleiotropic reproductive abnormalities. Genes Dev 1995;9(18):2266-2278