Paracrine mediators of endometrial growth and differentiation

The Endometrium: Molecular, Cellular and Clinical Perspectives, Second Edition

Volumn , Issue , 2008, Pages 223-244

  Bigsby, Robert M ^a   Bethin, Kathleen E ^a  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 85056980219     PISSN: None     EISSN: None     Source Type: Book    
DOI: None     Document Type: Chapter

References (207)

1. Markee JE. Physiology of reproduction. Annu Rev Physiol 1951; 13: 367-96.
2. Noyes RW, Hertig AT, Rock J. Dating the endometrial biopsy. Fertil Steril 1950; 1: 3-25.
3. Carson DD, Bagchi I, Dey SK et al. Embryo implantation. Dev Biol 2000; 223: 217-37.
4. Wilcox AJ, Baird DD, Weinberg CR. Time of implantation of the conceptus and loss of pregnancy. N Engl J Med 1999; 340: 1796-9.
5. Dorfman RI. Standard methods adopted by official organizations. In: Dorfman RI, ed. Methods in Hormone Research II. New York: Academic Press, 1962: 707-29.
6. Finn CA. Oestrogen and the decidual cell reaction of implantation in mice. J Endocrinol 1965; 32: 223-9.
7. Quarmby VE, Korach KS. The influence of 17β-estradiol on patterns of cell division in the uterus. Endocrinology 1984; 114: 694-702.
8. Bigsby RM, Caperell-Grant A, Berry N, Nephew K, Lubahn D. Estrogen induces a systemic growth factor through an estrogen receptor-alpha-dependent mechanism. Biol Reprod 2004; 70: 178-83.
9. Martin L, Finn CA, Trinder G. DNA synthesis in the endometrium of progesterone-treated mice. J Endocrinol 1973; 56: 303-7.
10. Yoshinaga K. Hormonal interplay in the establishment of pregnancy. Int Rev Physiol 1977; 13: 201-23.
11. Walmer DK, Wrona MA, Hughes CL, Nelson KG. Lactoferrin expression in the mouse reproductive tract during the natural estrous cycle: correlation with circulating estradiol and progesterone. Endocrinology 1992; 131: 1458-66.
12. Finn CA, Martin L. Hormone secretion during early pregnancy in the mouse. J Endocrinol 1969; 45: 57-65.
13. Finn CA, Pope M, Milligan SR. Control of uterine stromal mitosis in relation to uterine sensitivity and decidualization in mice. J Reprod Fertil 1995; 103: 153-8.
14. Weitlauf HM. Biology of implantation. In: Knobil E, Neill JD, eds. The Physiology of Reproduction, 2nd edn New York: Raven Press, 1994: 391-440.
15. Rothchild I, Meyer RK, Spielman MA. A quantitative study of oestrogen-progesterone interaction in the formation of placentomata in the castrate rat. Am J Physiol 1940; 128: 213-24.
16. Greenwald GS. Formation of deciduomata in the lactating mouse. J Endocrinol 1958; 17: 24-8.
17. Finn CA, Martin L. Endocrine control of the timing of endometrial sensitivity to a decidual stimulus. Biol Reprod 1972; 7: 82-6.
18. Rothchild I, Meyer RK. Studies of the pretrauma factors necessary for placentoma formation in the rat. Physiol Zool 1942; 15: 216-23.
19. Paria BC, Tan J, Lubahn DB, Dey SK, Das SK. Uterine decidual response occurs in estrogen receptor-alpha-deficient mice. Endocrinology 1999; 140: 2704-10.
20. Kurita T, Kj L, Saunders PT et al. Regulation of progesterone receptors and decidualization in uterine stroma of the estrogen receptor-alpha knockout mouse. Biol Reprod 2001; 64: 272-83.
21. Curtis HS, Goulding EH, Eddy EM et al. Studies using the estrogen receptor alpha knockout uterus demonstrate that implantation but not decidualization-associated signaling is estrogen dependent. Biol Reprod 2002; 67: 1268-77.
22. Hertz R. A review of the evidence linking estrogen and cancer in animals. Pediatrics 1978; 62: 1138-42.
23. Hertz R. The estrogen problem: retrospect and prospect. In: McLachlan JA, ed. Estrogen in the Environment II. New York: Elsevier, 1985: 1-14.
24. Newbold R. Cellular and molecular effects of developmental exposure to diethylstilbestrol: implications for other environmental estrogens. Environ Health Perspect 1995; 103(Suppl 7): 83-7.
25. Cunha GR, Chung LW, Shannon JM, Reese BA. Stromal-epithelial interactions in sex differentiation. Biol Reprod 1980; 22: 19-42.
26. Cunha GR, Cooke PS, Kurita T. Role of stromal-epithelial interactions in hormonal responses. Arch Histol Cytol 2004; 67: 417-34.
27. Cunha GR, Ricke W, Thomson A et al. Hormonal, cellular, and molecular regulation of normal and neoplastic prostatic development. J Steroid Biochem Mol Biol 2004; 92: 221-36.
28. Bigsby RM, Cunha GR. Estrogen stimulation of deoxyribonucleic acid synthesis in uterine epithelial cells which lack estrogen receptors. Endocrinology 1986; 119: 390-6.
29. Bigsby RM, Aixin L, Luo K, Cunha GR. Strain differences in the ontogeny of estrogen receptors in murine uterine epithelium. Endocrinology 1990; 126: 2592-6.
30. Yamashita S, Newbold RR, McLachlan JA, Korach KS. The role of the estrogen receptor in uterine epithelial proliferation and cytodifferentiation in neonatal mice. Endocrinology 1990; 127: 2456-63.
31. 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: 6535-40.
32. Kurita T, Young P, Brody JR et al. Stromal progesterone receptors mediate the inhibitory effects of progesterone on estrogen- induced uterine epithelial cell deoxyribonucleic acid synthesis. Endocrinology 1998; 139: 4708-13.
33. Buchanan DL, Setiawan T, Lubahn DB et al. Tissue compartment- specific estrogen receptor-alpha participation in the mouse uterine epithelial secretory response. Endocrinology 1999; 140: 484-91.
34. Kurita T, Lee KJ, Cooke PS et al. Paracrine regulation of epithelial progesterone receptor and lactoferrin by progesterone in the mouse uterus. Biol Reprod 2000; 62: 831-8.
35. Pierro E, Minici F, Alesiani O, et al. Stromal-epithelial interactions modulate estrogen responsiveness in normal human endometrium. Biol Reprod 2001; 64: 831-8.
36. Oshita T, Nagai N, Mukai K et al. Telomerase activation in endometrial epithelial cells by paracrine effectors from stromal cells in primary cultured human endometrium. Int J Mol Med 2004; 13: 425-30.
37. Yang S, Fang Z, Gurates B et al. Stromal PRs mediate induction of 17beta-hydroxysteroid dehydrogenase type 2 expression in human endometrial epithelium: a paracrine mechanism for inactivation of E2. Mol Endocrinol 2001; 15: 2093-105.
38. Osteen KG, Rodgers WH, Gaire M et al. Stromal-epithelial interaction mediates steroidal regulation of metalloproteinase expression in human endometrium. Proc Natl Acad Sci USA 1994; 91: 10129-33.
39. Brody JR, Cunha GR. Histologic, morphometric, and immunocytochemical analysis of myometrial development in rats and mice: I. Normal development. Am J Anat 1989; 186: 1-20.
40. Cunha GR, Young P, Brody JR. Role of uterine epithelium in the development of myometrial smooth muscle cells. Biol Reprod 1989; 40: 861-71.
41. Brody JR, Cunha GR. Histologic, morphometric, and immunocytochemical analysis of myometrial development in rats and mice: II. Effects of DES on development. Am J Anat 1989; 186: 21-42.
42. Kitajewski J, Sassoon D. The emergence of molecular gynecology: homeobox and Wnt genes in the female reproductive tract. Bioessays 2000; 22: 902-10.
43. Couse JF, Korach KS. Estrogen receptor-alpha mediates the detrimental effects of neonatal diethylstilbestrol (DES) exposure in the murine reproductive tract. Toxicology 2004; 205: 55-63.
44. Lejeune B, Leroy F. Role of the uterine epithelium in inducing the decidual cell reaction. Prog Reprod Biol 1980; 7: 92-101.
45. Lejeune B, Van HJ, Leroy F. Transmitter role of the luminal uterine epithelium in the induction of decidualization in rats. J Reprod Fertil 1981; 61: 235-40.
46. Bigsby RM, Aixin L, Everett L. Stromal-epithelial interactions regulating cell proliferation in the uterus. In: Magness RR, Naftolin F, eds. Local Systems in Reproduction. New York: Raven Press, 1993: 171.
47. Ben-Shlomo I. Sharing of unrelated receptors and ligands by cognate partners: possible implications for ovarian and endometrial physiology. Reprod Biomed Online 2005; 11: 259-69.
48. Luetteke NC, Qiu TH, Fenton SE et al. Targeted inactivation of the EGF and amphiregulin genes reveals distinct roles for EGF receptor ligands in mouse mammary gland development. Development 1999; 126: 2739-50.
49. Wells A. EGF receptor. Int J Biochem Cell Biol 1999; 31: 637-43.
50. Pavelock K, Braas K, Ouafik L, Osol G, May V. Differential expression and regulation of the vascular endothelial growth factor receptors neuropilin-1 and neuropilin-2 in rat uterus. Endocrinology 2001; 142: 613-22.
51. Ghahary A, Chakrabarti S, Murphy LJ. Localization of the sites of synthesis and action of insulin-like growth factor-I in the rat uterus. Mol Endocrinol 1990; 4: 191-5.
52. Kapur S, Tamada H, Dey SK, Andrews GK. Expression of insulin-like growth factor-I (IGF-I) and its receptor in the peri-implantation mouse uterus, and cell-specific regulation of IGF-I gene expression by estradiol and progesterone. Biol Reprod 1992; 46: 208-19.
53. Sato T, Wang G, Hardy MP et al. Role of systemic and local IGF-I in the effects of estrogen on growth and epithelial proliferation of mouse uterus. Endocrinology 2002; 143: 2673-9.
54. Wang J, Niu W, Nikiforov Y et al. Targeted overexpression of IGF-I evokes distinct patterns of organ remodeling in smooth muscle cell tissue beds of transgenic mice. J Clin Invest 1997; 100: 1425-39.
55. Polakis P. Wnt signaling and cancer. Genes Dev 2000; 14: 1837-51.
56. Miller C, Pavlova A, Sassoon DA. Differential expression patterns of Wnt genes in the murine female reproductive tract during development and the estrous cycle. Mech Dev 1998; 76: 91-9.
57. Hou X, Tan Y, Li M, Dey SK, Das SK. Canonical Wnt signaling is critical to estrogen-mediated uterine growth. Mol Endocrinol 2004; 18: 3035-49.
58. Das SK, Tan J, Raja S et al. Estrogen targets genes involved in protein processing, calcium homeostasis, and Wnt signaling in the mouse uterus independent of estrogen receptor-alpha and -beta. J Biol Chem 2000; 275: 28834-42.
59. Couse JF, Curtis SW, Washburn TF et al. Analysis of transcription and estrogen insensitivity in the female mouse after targeted disruption of the estrogen receptor gene. Mol Endocrinol 1995; 9: 1441-54.
60. Geum D, Sun W, Paik SK, Lee CC, Kim K. Estrogen-induced cyclin D1 and D3 gene expressions during mouse uterine cell proliferation in vivo: differential induction mechanism of cyclin D1 and D3. Mol Reprod Dev 1997; 46: 450-8.
61. 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: 21-5.
62. Huet-Hudson YM, Chakraborty C, De SK et al. Estrogen regulates the synthesis of epidermal growth factor in mouse uterine epithelial cells. Mol Endocrinol 1990; 4: 510-23.
63. Chegini N, Rossi MJ, Masterson BJ. Platelet-derived growth factor (PDGF), epidermal growth factor (EGF), and EGF and PDGF beta-receptors in human endometrial tissue: localization and in vitro action. Endocrinology 1992; 130: 2373-85.
64. Hom YK, Young P, Wiesen JF et al. Uterine and vaginal organ growth requires epidermal growth factor receptor signaling from stroma. Endocrinology 1998; 139: 913-21.
65. Lim H, Dey SK, Das SK. Differential expression of the erbB2 gene in the periimplantation mouse uterus: potential mediator of signaling by epidermal growth factor-like growth factors. Endocrinology 1997; 138: 1328-37.
66. Tzahar E, Waterman H, Chen X et al. A hierarchical network of interreceptor interactions determines signal transduction by Neu differentiation factor/neuregulin and epidermal growth factor. Mol Cell Biol 1996; 16: 5276-87.
67. Srinivasan R, Benton E, McCormick F et al. Expression of the c-erbB-3/HER-3 and c-erbB-4/HER-4 growth factor receptors and their ligands, neuregulin-1 alpha, neuregulin-1 beta, and betacellulin, in normal endometrium and endometrial cancer. Clin Cancer Res 1999; 5: 2877-83.
68. Lim H, Das SK, Dey SK. erbB genes in the mouse uterus: cellspecific signaling by epidermal growth factor (EGF) family of growth factors during implantation. Dev Biol 1998; 204: 97-110.
69. Irwin JC, Utian WH, Eckert RL. Sex steroids and growth factors differentially regulate the growth and differentiation of cultured human endometrial stromal cells. Endocrinology 1991; 129: 2385-92.
70. Chegini N, Rossi MJ, Masterson BJ. Platelet-derived growth factor (PDGF), epidermal growth factor (EGF), and EGF and PDGF ß-receptors in human endometrial tissue: localization and in vitro action. Endocrinology 1992; 130: 2373-85.
71. Das SK, Tsukamura H, Paria BC et al. Differential expression of epidermal growth factor receptor (EGF-R) gene and regulation of EGF-R bioactivity by progesterone and estrogen in the adult mouse uterus. Endocrinology 1994; 134: 971-81.
72. Chobotova K, Muchmore ME, Carver J et al. The mitogenic potential of heparin-binding epidermal growth factor in the human endometrium is mediated by the epidermal growth factor receptor and is modulated by tumor necrosis factoralpha. J Clin Endocrinol Metab 2002; 87: 5769-77.
73. Chobotova K, Karpovich N, Carver J et al. Heparin-binding epidermal growth factor and its receptors mediate decidualization and potentiate survival of human endometrial stromal cells. J Clin Endocrinol Metab 2005; 90: 913-19.
74. Lessey BA, Gui Y, Apparao KB et al. 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: 446-55.
75. Curtis SW, Washburn T, Sewall C et al. Physiological coupling of growth factor and steroid receptor signaling pathways: estrogen receptor knockout mice lack estrogen-like response to epidermal growth factor. Proc Natl Acad Sci USA 1996; 93: 12626-30.
76. Hewitt SC, Collins J, Grissom S et al. Global uterine genomics in vivo: microarray evaluation of the estrogen receptor alphagrowth factor cross-talk mechanism. Mol Endocrinol 2005; 19: 657-68.
77. Levin ER. Bidirectional signaling between the estrogen receptor and the epidermal growth factor receptor. Mol Endocrinol 2003; 17: 309-17.
78. Filardo EJ. Epidermal growth factor receptor (EGFR) transactivation by estrogen via the G-protein-coupled receptor, GPR30: a novel signaling pathway with potential significance for breast cancer. J Steroid Biochem Mol Biol 2002; 80: 231-8.
79. Vivacqua A, Bonofiglio D, Recchia AG et al. The G proteincoupled receptor GPR30 mediates the proliferative effects induced by 17beta-estradiol and hydroxytamoxifen in endometrial cancer cells. Mol Endocrinol 2006; 20: 631-46.
80. Battersby S, Critchley HO, Morgan K et al. Expression and regulation of the prokineticins (endocrine gland-derived vascular endothelial growth factor and Bv8) and their receptors in the human endometrium across the menstrual cycle. J Clin Endocrinol Metab 2004; 89: 2463-9.
81. Kaser A, Winklmayr M, Lepperdinger G, Kreil G. The AVIT protein family. Secreted cysteine-rich vertebrate proteins with diverse functions. EMBO Rep 2003; 4: 469-73.
82. LeCouter J, Zlot C, Tejada M et al. Bv8 and endocrine gland-derived vascular endothelial growth factor stimulate hematopoiesis and hematopoietic cell mobilization. Proc Natl Acad Sci USA 2004; 101: 16813-18.
83. Kisliouk T, Podlovni H, Spanel-Borowski K et al. Prokineticins (endocrine gland-derived vascular endothelial growth factor and BV8) in the bovine ovary: expression and role as mitogens and survival factors for corpus luteum-derived endothelial cells. Endocrinology 2005; 146: 3950-8.
84. Tsai SJ, Wu MH, Chen HM et al. Fibroblast growth factor-9 is an endometrial stromal growth factor. Endocrinology 2002; 143: 2715-21.
85. Moller B, Rasmussen C, Lindblom B, Olovsson M. Expression of the angiogenic growth factors VEGF, FGF-2, EGF and their receptors in normal human endometrium during the menstrual cycle. Mol Hum Reprod 2001; 7: 65-72.
86. Taylor KM, Chen C, Gray CA et al. Expression of messenger ribonucleic acids for fibroblast growth factors 7 and 10, hepatocyte growth factor, and insulin-like growth factors and their receptors in the neonatal ovine uterus. Biol Reprod 2001; 64: 1236-46.
87. Chen C, Spencer TE, Bazer FW. Fibroblast growth factor-10: a stromal mediator of epithelial function in the ovine uterus. Biol Reprod 2000; 63: 959-66.
88. Koji T, Chedid M, Rubin JS et al. Progesterone-dependent expression of keratinocyte growth factor mRNA in stromal cells of the primate endometrium: keratinocyte growth factor as a progestomedin. J Cell Biol 1994; 125: 393-401.
89. Siegfried S, Pekonen F, Nyman T, Ammala M. Expression of mRNA for keratinocyte growth factor and its receptor in human endometrium. Acta Obstet Gynecol Scand 1995; 74: 410-14.
90. Hom YK, Young P, Thomson AA, Cunha GR. Keratinocyte growth factor injected into female mouse neonates stimulates uterine and vaginal epithelial growth. Endocrinology 1998; 139: 3772-9.
91. Slayden OD, Rubin JS, Lacey DL, Brenner RM. Effects of keratinocyte growth factor in the endometrium of rhesus macaques during the luteal-follicular transition. J Clin Endocrinol Metab 2000; 85: 275-85.
92. Marshburn PB, Arici AM, Casey ML. Expression of transforming growth factor-beta 1 messenger ribonucleic acid and the modulation of deoxyribonucleic acid synthesis by transforming growth factor-beta 1 in human endometrial cells. Am J Obstet Gynecol 1994; 170: 1152-8.
93. Bruner KL, Rodgers WH, Gold LI et al. Transforming growth factor beta mediates the progesterone suppression of an epithelial metalloproteinase by adjacent stroma in the human endometrium. Proc Natl Acad Sci USA 1995; 92: 7362-6.
94. Salamonsen LA, Dimitriadis E, Jones RL, Nie G. Complex regulation of decidualization: a role for cytokines and proteases - a review. Placenta 2003; 24(Suppl A): S76-85.
95. Jones RL, Salamonsen LA, Critchley HO et al. Inhibin and activin subunits are differentially expressed in endometrial cells and leukocytes during the menstrual cycle, in early pregnancy and in women using progestin-only contraception. Mol Hum Reprod 2000; 6: 1107-17.
96. Mylonas I, Jeschke U, Wiest I et al. Inhibin/activin subunits alpha, beta-A and beta-B are differentially expressed in normal human endometrium throughout the menstrual cycle. Histochem Cell Biol 2004; 122: 461-71.
97. Jones RL, Salamonsen LA, Zhao YC et al. Expression of activin receptors, follistatin and betaglycan by human endometrial stromal cells; consistent with a role for activins during decidualization. Mol Hum Reprod 2002; 8: 363-74.
98. Jones RL, Salamonsen LA, Findlay JK. Activin A promotes human endometrial stromal cell decidualization in vitro. J Clin Endocrinol Metab 2002; 87: 4001-4.
99. Tierney EP, Giudice LC. Role of activin A as a mediator of in vitro endometrial stromal cell decidualization via the cyclic adenosine monophosphate pathway. Fertil Steril 2004; 81(Suppl 1): 899-903.
100. Noda N, Minoura H, Nishiura R et al. Expression of tenascin-C in stromal cells of the murine uterus during early pregnancy: induction by interleukin-1 alpha, prostaglandin E(2), and prostaglandin F(2 alpha). Biol Reprod 2000; 63: 1713-20.
101. Singer CF, Marbaix E, Kokorine I et al. Paracrine stimulation of interstitial collagenase (MMP-1) in the human endometrium by interleukin 1alpha and its dual block by ovarian steroids. Proc Natl Acad Sci USA 1997; 94: 10341-5.
102. Singer CF, Marbaix E, Kokorine I et al. The matrix metalloproteinase-1 (MMP-1) expression in the human endometrium is inversely regulated by interleukin-1 alpha and sex steroids. Ceska Gynekol 2000; 65: 211-15.
103. Takamoto N, Zhau B, Tsai SY et al. Identification of Indian hedgehog as a progesterone-responsive gene in the murine uterus. Mol Endocrinol 2002; 16: 2338-48.
104. Lee K, Jeong J, Kwak I et al. Indian hedgehog is a major mediator of progesterone signaling in the mouse uterus. Nat Genet 2006; 38: 1204-9.
105. Khatua A, Wang X, Ding T et al. Indian hedgehog, but not histidine decarboxylase or amphiregulin, is a progesteroneregulated uterine gene in hamsters. Endocrinology 2006; 147: 4079-92.
106. Martin L, Finn CA, Hormonal regulation of cell division in epithelial and connective tissues of the mouse uterus. J Endocrinol 1968; 41: 363-71.
107. Bigsby RM, Cunha GR. Progesterone and dexamethasone inhibition of uterine epithelial proliferation in two models of estrogen-independent growth. Am J Obstet Gynecol 1988; 158: 646-50.
108. Maslar IA, Riddick DH. Prolactin production by human endometrium during the normal menstrual cycle. Am J Obstet Gynecol 1979; 135: 751-4.
109. Croze F, Kennedy TG, Schroedter IC, Friesen HG. Expression of rat prolactin-like protein B in deciduoma of pseudopregnant rat and in decidua during early pregnancy. Endocrinology 1990; 127: 2665-72.
110. Patel OV, Yamada O, Kizaki K et al. Temporospatial expression of placental lactogen and prolactin-related protein-1 genes in the bovine placenta and uterus during pregnancy. Mol Reprod Dev 2004; 69: 146-52.
111. 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.
112. Sahgal N, Knipp GT, Liu B et al. Identification of two new nonclassical members of the rat prolactin family. J Mol Endocrinol 2000; 24: 95-108.
113. Muller H, Ishimura R, Orwig KE et al. Homologues for prolactin-like proteins A and B are present in the mouse. Biol Reprod 1998; 58: 45-51.
114. Cohick CB, Xu L, Soares MJ. Prolactin-like protein-B: heterologous expression and characterization of placental and decidual species. J Endocrinol 1997; 152: 291-302.
115. Dai G, Liu B, Szpirer C et al. Prolactin-like protein-C variant: complementary deoxyribonucleic acid, unique six exon gene structure, and trophoblast cell-specific expression. Endocrinology 1996; 137: 5009-19.
116. Jayatilak PG, Gibori G. Ontogeny of prolactin receptors in rat decidual tissue: binding by a locally produced prolactin-like hormone. J Endocrinol 1986; 110: 115-21.
117. Jabbour HN, Critchley HO. Potential roles of decidual prolactin in early pregnancy. Reproduction 2001; 121: 197-205.
118. Daly DC, Maslar IA, Rosenberg SM, Tohan N, Riddick DH. Prolactin production by luteal phase defect endometrium. Am J Obstet Gynecol 1981; 140: 587-91.
119. Jones RL, Critchley HO, Brooks J, Jabbour HN, McNeilly AS. Localization and temporal expression of prolactin receptor in human endometrium. J Clin Endocrinol Metab 1998; 83: 258-62.
120. Jabbour HN, Critchley HO, Boddy SC. 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 1998; 83: 2545-53.
121. Gu Y, Srivastava RK, Clarke DL, Linzer DI, Gibori G. The decidual prolactin receptor and its regulation by deciduaderived factors. Endocrinology 1996; 137: 4878-85.
122. Yamashita M, Matsuda M, Mori T. In situ detection of prolactin receptor mRNA and apoptotic cell death in mouse uterine tissues with adenomyosis. In Vivo 1999; 13: 57-60.
123. Reese J, Binart N, Brown N et al. Implantation and decidualization defects in prolactin receptor (PRLR)-deficient mice are mediated by ovarian but not uterine PRLR. Endocrinology 2000; 141: 1872-81.
124. Binart N, Helloco C, Ormandy CJ et al. Rescue of preimplantatory egg development and embryo implantation in prolactin receptor-deficient mice after progesterone administration. Endocrinology 2000; 141: 2691-7.
125. Deb S, Tessier C, Prigent-Tessier A et al. The expression of interleukin-6 (IL-6), IL-6 receptor, and gp130-kilodalton glycoprotein in the rat decidua and a decidual cell line: regulation by 17beta-estradiol and prolactin. Endocrinology 1999; 140: 4442-50.
126. Baran N, Kelly PA, Binart N. Characterization of a prolactinregulated gene in reproductive tissues using the prolactin receptor knockout mouse model. Biol Reprod 2002; 66: 1210-18.
127. Baran N, Kelly PA, Binart N. Decysin, a new member of the metalloproteinase family, is regulated by prolactin and steroids during mouse pregnancy. Biol Reprod 2003; 68: 1787-92.
128. Carpenter KD, Gray CA, Noel S et al. Prolactin regulation of neonatal ovine uterine gland morphogenesis. Endocrinology 2003; 144: 110-20.
129. Noel S, Herman A, Johnson GA et al. Ovine placental lactogen specifically binds to endometrial glands of the ovine uterus. Biol Reprod 2003; 68: 772-80.
130. Chilton BS, Daniel JCJ. Differences in the rabbit uterine response to progesterone as influenced by growth hormone or prolactin. J Reprod Fertil 1987; 79: 581-7.
131. Hewetson A, Chilton BS. Novel elements in the uteroglobin promoter are a functional target for prolactin signaling. Mol Cell Endocrinol 1997; 136: 1-6.
132. Mansharamani M, Chilton BS. Prolactin augments progesterone- dependent expression of a nuclear P-type ATPase that associates with the RING domain of RUSH transcription factors in the endometrium. Ann NY Acad Sci 2000; 923: 321-4.
133. Nowak RA, Mora S, Diehl T, Rhoades AR, Stewart EA. Prolactin is an autocrine or paracrine growth factor for human myometrial and leiomyoma cells. Gynecol Obstet Invest 1999; 48: 127-32.
134. Florio P, Rossi M, Sigurdardottir M et al. Paracrine regulation of endometrial function: interaction between progesterone and corticotropin-releasing factor (CRF) and activin A. Steroids 2003; 68: 801-7.
135. Harrison GS, Wierman ME, Nett TM, Glode LM. Gonadotropin-releasing hormone and its receptor in normal and malignant cells. Endocr Relat Cancer 2004; 11: 725-48.
136. Sales KJ, Jabbour HN. Cyclooxygenase enzymes and prostaglandins in reproductive tract physiology and pathology. Prostaglandins Other Lipid Mediat 2003; 71: 97-117.
137. Jabbour HN, Sales KJ. Prostaglandin receptor signalling and function in human endometrial pathology. Trends Endocrinol Metab 2004; 15: 398-404.
138. Gross G, Imamura T, Muglia LJ. Gene knockout mice in the study of parturition. J Soc Gynecol Investig 2000; 7: 88-95.
139. Muglia LJ. Genetic analysis of fetal development and parturition control in the mouse. Pediatr Res 2000; 47: 437-43.
140. Tranguch S, Daikoku T, Guo Y, Wang H, Dey SK. Molecular complexity in establishing uterine receptivity and implantation. Cell Mol Life Sci 2005; 62: 1964-73.
141. Wang H, Dey SK. Lipid signaling in embryo implantation. Prostaglandins Other Lipid Mediat 2005; 77: 84-102.
142. Yang ZM, Das SK, Wang J et al. Potential sites of prostaglandin actions in the periimplantation mouse uterus: differential expression and regulation of prostaglandin receptor genes. Biol Reprod 1997; 56: 368-79.
143. Katsuyama M, Sugimoto Y, Morimoto K et al. Distinct cellular localization of the messenger ribonucleic acid for prostaglandin E receptor subtypes in the mouse uterus during pseudopregnancy. Endocrinology 1997; 138: 344-50.
144. Sun T, Li SJ, Diao HL et al. Cyclooxygenases and prostaglandin E synthases in the endometrium of the rhesus monkey during the menstrual cycle. Reproduction 2004; 127: 465-73.
145. Jones RL, Kelly RW, Critchley HO. Chemokine and cyclooxygenase-2 expression in human endometrium coincides with leukocyte accumulation. Hum Reprod 1997; 12: 1300-6.
146. Baird DT, Cameron ST, Critchley HO et al. Prostaglandins and menstruation. Eur J Obstet Gynecol Reprod Biol 1996; 70: 15-17.
147. Poyser NL. The control of prostaglandin production by the endometrium in relation to luteolysis and menstruation. Prostaglandins Leukot Essent Fatty Acids 1995; 53: 147-95.
148. Smith SK, Kelly RW. The release of PGF2alpha and PGE2 from separated cells of human endometrium and decidua. Prostaglandins Leukot Essent Fatty Acids 1988; 33: 91-6.
149. Marions L, Danielsson KG. Expression of cyclo-oxygenase in human endometrium during the implantation period. Mol Hum Reprod 1999; 5: 961-5.
150. Fields MJ, Shemesh M. Extragonadal luteinizing hormone receptors in the reproductive tract of domestic animals. Biol Reprod 2004; 71: 1412-18.
151. Kang J, Chapdelaine P, Parent J et al. Expression of human prostaglandin transporter in the human endometrium across the menstrual cycle. J Clin Endocrinol Metab 2005; 90: 2308-13.
152. Ross GT, Hillier SG. Luteal maturation and luteal phase defect. Clin Obstet Gynaecol 1978; 5: 391-409.
153. Balasch J, Vanrell JA. Corpus luteum insufficiency and fertility: a matter of controversy. Hum Reprod 1987; 2: 557-67.
154. Ginsburg KA. Luteal phase defect. Etiology, diagnosis, and management. Endocrinol Metab Clin North Am 1992; 21: 85-104.
155. Wuttke W, Pitzel L, Seidlova-Wuttke D, Hinney B. LH pulses and the corpus luteum: the luteal phase deficiency (LPD). Vitam Horm 2001; 63: 131-58.
156. Tavaniotou A, Albano C, Smitz J, Devroey P. Impact of ovarian stimulation on corpus luteum function and embryonic implantation. J Reprod Immunol 2002; 55: 123-30.
157. Lessey BA. Adhesion molecules and implantation. J Reprod Immunol 2002; 55: 101-12.
158. Lessey BA. Two pathways of progesterone action in the human endometrium: implications for implantation and contraception. Steroids 2003; 68: 809-15.
159. Bukulmez O, Arici A. Luteal phase defect: myth or reality. Obstet Gynecol Clin North Am 2004; 31: 727-44.
160. Bhowmick NA, Moses HL. Tumor-stroma interactions. Curr Opin Genet Dev 2005; 15: 97-101.
161. Yoshida S, Harada T, Iwabe T et al. Induction of hepatocyte growth factor in stromal cells by tumor-derived basic fibroblast growth factor enhances growth and invasion of endometrial cancer. J Clin Endocrinol Metab 2002; 87: 2376-83.
162. Fujimoto J, Hori M, Ichigo S, Tamaya T. Antiestrogenic compounds inhibit estrogen-induced expression of fibroblast growth factor family (FGF-1, 2, and 4) mRNA in well-differentiated endometrial cancer cells. Eur J Gynaecol Oncol 1997; 18: 497-501.
163. Hyder SM, Chiappetta C, Stancel GM. Triphenylethylene antiestrogens induce uterine vascular endothelial growth factor expression via their partial estrogen agonist activity. Cancer Lett 1997; 120: 165-71.
164. Sakaguchi J, Kyo S, Kanaya T et al. Aberrant expression and mutations of TGF-beta receptor type II gene in endometrial cancer. Gynecol Oncol 2005; 98: 427-33.
165. Tanaka T, Toujima S, Umesaki N. Activin A inhibits growthinhibitory signals by TGF-beta1 in differentiated human endometrial adenocarcinoma cells. Oncol Rep 2004; 11: 875-9.
166. Park DW, Ryu HS, Choi DS et al. Localization of matrix metalloproteinases on endometrial cancer cell invasion in vitro. Gynecol Oncol 2001; 82: 442-9.
167. Osteen KG, Bruner-Tran KL, Ong D, Eisenberg E. Paracrine mediators of endometrial matrix metalloproteinase expression: potential targets for progestin-based treatment of endometriosis. Ann NY Acad Sci 2002; 955: 139-46.
168. Henriet P, Cornet PB, Lemoine P et al. Circulating ovarian steroids and endometrial matrix metalloproteinases (MMPs). Ann NY Acad Sci 2002; 955: 119-38.
169. Tamura M, Sebastian S, Yang S et al. Up-regulation of cyclooxygenase-2 expression and prostaglandin synthesis in endometrial stromal cells by malignant endometrial epithelial cells. A paracrine effect mediated by prostaglandin E2 and nuclear factor-kappa B. J Biol Chem 2002; 277: 26208-16.
170. Reynolds RK, Hu C, Baker VV. Transforming growth factoralpha and insulin-like growth factor-I, but not epidermal growth factor, elicit autocrine stimulation of mitogenesis in endometrial cancer cell lines. Gynecol Oncol 1998; 70: 202-9.
171. Kleinman D, Karas M, Danilenko M et al. Stimulation of endometrial cancer cell growth by tamoxifen is associated with increased insulin-like growth factor (IGF)-I induced tyrosine phosphorylation and reduction in IGF binding proteins. Endocrinology 1996; 137: 1089-95.
172. Rutanen EM. Insulin-like growth factors in endometrial function. Gynecol Endocrinol 1998; 12: 399-406.
173. Lacey JVJ, Potischman N, Madigan MP et al. Insulin-like growth factors, insulin-like growth factor-binding proteins, and endometrial cancer in postmenopausal women: results from a U.S. case-control study. Cancer Epidemiol Biomarkers Prev 2004; 13: 607-12.
174. Augustin LS, Dal Maso L, Franceschi S et al. Association between components of the insulin-like growth factor system and endometrial cancer risk. Oncology 2004; 67: 54-9.
175. Gielen SC, Burger CW, Kuhne LC et al. Analysis of estrogen agonism and antagonism of tamoxifen, raloxifene, and ICI182780 in endometrial cancer cells: a putative role for the epidermal growth factor receptor ligand amphiregulin. J Soc Gynecol Investig 2005; 12: e55-67.
176. Berchuck A, Rodriguez G, Kinney RB et al. Overexpression of HER-2/neu in endometrial cancer is associated with advanced stage disease. Am J Obstet Gynecol 1991; 164: 15-21.
177. Bigsby RM, Li AX, Bomalaski J et al. Immunohistochemical study of HER-2/neu, epidermal growth factor receptor, and steroid receptor expression in normal and malignant endometrium. Obstet Gynecol 1992; 79: 95-100.
178. Saffari B, Jones LA, el-Naggar A et al. Amplification and overexpression of HER-2/neu (c-erbB2) in endometrial cancers: correlation with overall survival. Cancer Res 1995; 55: 5693-8.
179. Croze F, Kennedy TG, Schroedter IC et al. Expression of insulin-like growth factor-I and insulin-like growth factorbinding protein-1 in the rat uterus during decidualization. Endocrinology 1990; 127: 1995-2000.
180. Giudice LC, Mark SP, Irwin JC. Paracrine actions of insulinlike growth factors and IGF binding protein-1 in non-pregnant human endometrium and at the decidual-trophoblast interface. J Reprod Immunol 1998; 39: 133-48.
181. Tamada H, Das SK, Andrews GK, Dey SK. Cell-type-specific expression of transforming growth factor-alpha in the mouse uterus during the peri-implantation period. Biol Reprod 1991; 45: 365-72.
182. Paria BC, Das SK, Huet-Hudson YM, Dey SK. Distribution of transforming growth factor alpha precursors in the mouse uterus during the periimplantation period and after steroid hormone treatments. Biol Reprod 1994; 50: 481-91.
183. Das SK, Chakraborty I, Paria BC et al. Amphiregulin is an implantation-specific and progesterone-regulated gene in the mouse uterus. Mol Endocrinol 1995; 9: 691-705.
184. Lee DS, Yanagimoto Ueta Y, Xuan X et al. Expression patterns of the implantation-associated genes in the uterus during the estrous cycle in mice. J Reprod Dev 2005; 51: 787-98.
185. Klonisch T, Wolf P, Hombach-Klonisch S et al. Epidermal growth factor-like ligands and erbB genes in the periimplantation rabbit uterus and blastocyst. Biol Reprod 2001; 64: 1835-44.
186. Das SK, Flanders KC, Andrews GK, Dey SK. Expression of transforming growth factor-beta isoforms (β2 and β3) in the mouse uterus analysis of the periimplantation period and effects of ovarian steroids. Endocrinology 1992; 130: 3459-66.
187. Takahashi T, Eitzman B, Bossert NL et al. Transforming growth factors β1, β2, and β3 messenger RNA and protein expression in mouse uterus and vagina during estrogeninduced growth: a comparison to other estrogen-regulated genes. Cell Growth Diff 1994; 5: 919-35.
188. Tamada H, McMaster MT, Flanders KC et al. Cell typespecific expression of transforming growth factor-beta 1 in the mouse uterus during the periimplantation period. Mol Endocrinol 1990; 4: 965-72.
189. Wada K, Nomura S, Morii E et al. Changes in levels of mRNAs of transforming growth factor (TGF)-beta1, -beta2, -beta3, TGF-beta type II receptor and sulfated glycoprotein-2 during apoptosis of mouse uterine epithelium. J Steroid Biochem Mol Biol 1996; 59: 367-75.
190. Tabibzadeh S, Lessey B, Satyaswaroop PG. Temporal and sitespecific expression of transforming growth factor-beta4 in human endometrium. Mol Hum Reprod 1998; 4: 595-602.
191. Chegini N, Zhao Y, Williams RS, Flanders KC. Human uterine tissue throughout the menstrual cycle expresses transforming growth factor-beta 1 (TGF beta 1), TGF beta 2, TGF beta 3, and TGF beta type II receptor messenger ribonucleic acid and protein and contains [125I]TGF beta 1-binding sites. Endocrinology 1994; 135: 439-49.
192. Dumont N, O’Connor-McCourt MD, Philip A. Transforming growth factor-beta receptors on human endometrial cells: identification of the type I, II, and III receptors and glycosylphosphatidylinositol anchored TGF-beta binding proteins. Mol Cell Endocrinol 1995; 111: 57-66.
193. Hyder SM, Huang JC, Nawaz Z et al. Regulation of vascular endothelial growth factor expression by estrogens and progestins. Environ Health Perspect 2000; 108(Suppl 5): 785-90.
194. Halder JB, Zhao X, Soker S et al. Differential expression of VEGF isoforms and VEGF(164)-specific receptor neuropilin-1 in the mouse uterus suggests a role for VEGF(164) in vascular permeability and angiogenesis during implantation. Genesis 2000; 26: 213-24.
195. 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: 6023-8.
196. Mulayim N, Palter SF, Kayisli UA et al. Chemokine receptor expression in human endometrium. Biol Reprod 2003; 68: 1491-5.
197. Chakraborty I, Das SK, Wang J, Dey SK. Developmental expression of the cyclo-oxygenase-1 and cyclo-oxygenase-2 genes in the peri-implantation mouse uterus and their differential regulation by the blastocyst and ovarian steroids. J Mol Endocrinol 1996; 16: 107-22.
198. Tawfik OW, Huet YM, Malathy PV et al. Release of prostaglandins and leukotrienes from the rat uterus is an early estrogenic response. Prostaglandins 1987; 34: 805-15.
199. Papay KD, Kennedy TG. Characterization of temporal and cell-specific changes in transcripts for prostaglandin E(2) receptors in pseudopregnant rat endometrium. Biol Reprod 2000; 62: 1515-25.
200. Gray K, Eitzman B, Raszmann K et al. Coordinate regulation by diethylstilbestrol of the platelet-derived growth factor-A (PDGF-A) and -B chains and the PDGF receptor alpha- and beta-subunits in the mouse uterus and vagina: potential mediators of estrogen action. Endocrinology 1995; 136: 2325-40.
201. Tulac S, Nayak NR, Kao LC et al. Identification, characterization, and regulation of the canonical Wnt signaling pathway in human endometrium. J Clin Endocrinol Metab 2003; 88: 3860-6.
202. Yoshinaga K, Hawkins RA, Stocker JF. Estrogen secretion by the rat ovary in vivo during the estrous cycle and pregnancy. Endocrinology 1969; 85: 103-12.
203. Park OK, Ramirez VD. Circulating blood progesterone is pulsatile throughout the rat oestrous cycle. Acta Endocrinol (Copenh) 1987; 116: 121-8.
204. Virgo BB, Bellward GD. Serum progesterone levels in the pregnant and postpartum laboratory mouse. Endocrinology 1974; 95: 1486-90.
205. Thorneycroft IH, Mishell DRJ, Stone SC, Kharma KM, Nakamura RM. The relation of serum 17-hydroxyprogesterone and estradiol-17-beta levels during the human menstrual cycle. Am J Obstet Gynecol 1971; 111: 947-51.
206. Ross GT, Cargille CM, Lipsett MB et al. Pituitary and gonadal hormones in women during spontaneous and induced ovulatory cycles. Recent Prog Horm Res 1970; 26: 1-62.
207. Bigsby RM, Cooke PS, Cunha GR. A simple efficient method for separating murine uterine epithelial and mesenchymal cells. Am J Physiol 1986; 251: E630-6.