Endocrine and paracrine correlates of endometrial receptivity to blastocyst implantation in the human

Indian Journal of Physiology and Pharmacology

Volumn 48, Issue 1, 2004, Pages 6-30

  Ghosh, D ^a   Sengupta, Jayasree ^a  

^a ALL INDIA INSTITUTE OF MEDICAL SCIENCES   (India)

Author keywords

Cytokines; Endocrinology; Endomterium implantation; Paracrinology; Preimplantation embryo receptivity

Indexed keywords

CELL ADHESION MOLECULE; CHORIONIC GONADOTROPIN; CYTOKINE; ESTROGEN; GLYCOPROTEIN; GROWTH FACTOR; ISOPROTEIN; LEUKEMIA INHIBITORY FACTOR; MEMBRANE PROTEIN; PROGESTERONE; RELAXIN; TRANSFORMING GROWTH FACTOR BETA;

BLASTOCYST; BLOOD VESSEL REACTIVITY; CELL DIFFERENTIATION; CORRELATION ANALYSIS; ENDOCRINE FUNCTION; ENDOMETRIUM CELL; HORMONE ACTION; HUMAN; IMPLANTATION; LUTEAL PHASE; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MOTHER; NONHUMAN; PARACRINE SIGNALING; PHYSIOLOGY; PROTEIN FUNCTION; REVIEW; TROPHOBLAST;

ANIMALS; BLASTOCYST; CELL TRANSPLANTATION; ENDOCRINE GLANDS; ENDOMETRIUM; FEMALE; HUMANS; PARACRINE COMMUNICATION;

EID: 0347990739     PISSN: 00195499     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (222)

1. Hodgen GD. Surrogate embryo transfer combined with estrogen-progesterone therapy in monkeys. J Am Med Assoc 1983; 250: 2167-2171.
2. Lutjen PJ, Trounson A, Leeton J et al. The establishment and maintenance of pregnancy using in vitro fertilization and embryo donation in a patient with primary ovarian failure. Nature 1984; 307: 174-175.
3. Navot D, Anderson TL, Droesch K et al. Hormonal manipulation of endometrial maturation. J Clin Endocrinol Metab 1986; 68: 801-807.
4. de Ziegler D, Bergeron C, Cornel C et al. Effects of luteal estradiol on the secretory transformation of human endometrium and plasma gonadotropins. J Clin Endocrinol Metab 1992; 74: 322-331.
5. Ghosh D, De P, Sengupta J. Luteal phase oestrogen is not essential for implantation and maintenance of pregnancy from surrogate embryo transfer in the rhesus monkey. Hum Reprod 1994; 9: 629-637.
6. Ghosh D, Sengupta J. Endometrial receptivity for implantation. Another relook at the issue of periimplantation oestrogen. Hum Reprod 1995; 10: 1-2.
7. Zegers-Hochschild F, Altieri E. Luteal phase estrogen is not required for establishment of pregnancy i the human. J Assist Reprod Genet 1995; 12: 224-228.
8. Simon C, Cano F, Valbuena, D et al. Clinical evidence for a detrimental effect on uterine receptivity of high serum oestradiol concentrations in high and normal responder patients. Hum Reprod 1995; 10: 2432-2437.
9. Valbuena D, Martin J, de Pablo JL et al. Increasing levels of estradiol are deleterious to embryonic implantation because they directly affect the embryo. Fertil Steril 2001; 76: 962-968.
10. Klotz DM, Hewitt SC, Ciana P et al. Requirement of estrogen receptor-alpha in insulin like growth factor-1 (IGF-1)-induced uterine responses and in vivo evidence for IGF-1/estrogen receptor cross-talk. J Biol Chem 2002; 277: 8531-8537.
11. Chen JR, Cheng JG, Shatzer T et al. Leukemia inhibitory factor can substitute for nidatory estrogen and is essential to inducing a receptive uterus for implantation but is not essential for subsequent embryogenesis. Endocrinology 2000; 141: 4365-4372.
12. Giudice LC, Dsupin BA, Jin IH et al. Differential expression of messenger ribonucleic acids encoding insulin-like growth factors and their receptors in human uterine endometrium and decidua. J Clin Endocrinol Metab 1993; 76: 1115-1122.
13. Mueller SO, Korach KS. Estrogen receptors and endcocrine diseases: lessons from estrogen receptor knockout mice. Curr Opin Pharmacol 2001; 1: 613-619.
14. Ravindranath N, Moudgal N R. Use of tamoxifen, an anti-oestrogen, in establishing a need for oestrogen in early pregnancy in the bonnet monkey (Macaca radiata). J Reprod Fertil 1987; 81: 327-336.
15. Ravindranath N, Moudgal N R. Effect of a specific estrogen antibody onpregnancy establishment in the bonnet monkey (Macaca radiata). Fertil Steril 1990; 54: 1162-1167.
16. Tseng L, Mazella J, Sun B. Modulation of aromatase activity in human endometrial stromal cells by steroids, Tamoxifen and RU486. Endocrinology, 1986; 118: 1312-1318.
17. 2 stimulates aromatase expression in endometriosis-derived stromal cells. Endocrinology 1997; 82: 600-605.
18. Edgar D H, James J B, Mills J A. Steroid secretion by human early embryos in culture. Hum. Reprod. 1993; 8: 277-278.
19. Gemzell-Danielsson K, Swahn M L, Svalander P, Bygdeman M. Early luteal phase treatment with mifepristone (RU486) for fertility regulation. Hum. Reprod. 1993; 8: 870-873.
20. Ghosh D, Sengupta J. Anti-nidatory effect of a single, post-ovulatory administration of mifepristone (RU486) in the rhesus monkey. Hum. Reprod 1993; 8: 552-558.
21. Ghosh D, Sengupta J, Hendrickx AG. Effect of a single-dose, early luteal phase administration of mifepristone (RU486) on implantation stage endometrium in the rhesus monkey. Hum Reprod. 1996; 11: 2026-2035.
22. Cameron S T, Critchley H O D, Buckely C H et al. Effect of two antiprogestins (mifepristone and onapristone) on endometrial factors of potential importance for implantation. Fertil Steril 1997; 67: 1046-1053.
23. Spencer TE, Bazer FW Biology of progesterone action during pregnancy recognition and maintenance of pregnancy. Front Biosci 2002; 7: 1879-1898.
24. Ghosh D, Kumar PGLL, Sengupta J Early luteal phase administration of mifepristone inhibits preimplantaion embryo development and viability in the rhesus monkey. Hum Reprod 1997; 12: 575-582.
25. Ghosh D, Lalitkumar PGL, Wong V et al. Preimplantation embryo morphology following early luteal phase anti-nidatory treatment with mifepristone (RU486) in the rhesus monkey. Hum Reprod 2000; 15: 180-188.
26. Edwards RG. Implantation, contraception and interception. Hum Reprod. 1994; 9: 985-989.
27. Milligan SR, Finn CA. Minimal progesterone support required for the maintenance of pregnancy in mice. Hum Reprod 1997; 12: 602-607.
28. Ghosh D, Stewart DR, Nayak NR et al. Serum concentrations of oestradiol-17β, progesterone, relaxin and chorionic gonadotrophin during blastocyst implantation in natural pregnancy cycle and in embryo transfer cycle in the rhesus monkey. Hum Reprod 1997; 12: 914-920.
29. Nayak NR, Ghosh D, Sengupta J. Effects of luteal phase administration of mifepristone (RU486) and prostaglandin analogue or inhibitor on endometrium in the rhesus monkey. Hum Reprod 1998; 13: 1047-1056.
30. Litcht P, Russu V, Wildt L. On the role of human chorionic gonadotropin (hCG) in the embryo-endometrial microenvironment: implications for differentiation and implantation. Seminars Reprod Med 2001; 19: 37-47.
31. Sunder S, Lenton EA 2000 Endocrinology of the peri-implantation period. Baillieres Best Pract Res Clin Obstet Gynaecol 2000; 14: 789-800.
32. Han SW, Lei ZM, Rao CV. Up-regulation of cyclooxygenase-2 gene expression by chorionic gonadotropin during the differentiation of human endometrial stromal cells into decidua. Endocrinology 1996; 137: 1791-1797.
33. Han SW, Lei ZM, Rao CV. Treatment of human endometrial stroma cells with chorionic gonadotropin promotes their morphological and functional differentiation into decidua. Mol Cell Endocrinol 1999; 147: 7-16.
34. Jones CJ, Fazleabas AT. Ultrastructure of epithelial plaque formation and stromal cell transformation by post-ovulatory chorionic gonadotrophin treatment in the baboon (Papio anubis). Hum Reprod 2001; 16: 2680-90.
35. Srisuparp S, Strakova Z, Fazleabas A T. The role of chorionic gonadotropin (CG) in blastocyst implantation. Arch Med Res 2001; 32: 627-634.
36. Johnson MR, Abbas AA, Allman AC J et al. The regulation of plasma relaxin levels during pregnancy. J Endocrinol 1994; 142: 261-265.
37. Rogers PAW, Murphy CR, Squires KR, MacLennan AH. Effects of relaxin on the intrauterine distribution and antimesometrial positioning and orientation of rat blastocysts before implantation. J Reprod Fertil 1983; 68: 431-435.
38. Vasilenko P, Mead JP, Weidmann JE. Uterine growth-promoting effects ofrelaxin: a morphometric and histological analysis. Biol Reprod 1986; 35: 987-995.
39. Vasilenko P, Mead JP. Growth-promoting effects of relaxin and related compositional changes in the uterus, cervix, and vagina of the rat. Endocrinology 1987; 120: 1370-1376.
40. Tseng L, Gao JG, Zhu H H et al. Effect of progestin, antiprogestin and relaxin, on the accumulation of PRL and insulin like growth factor binding protein-1 messenger ribonucleic acid in human endometrial stromal cells. Biol Reprod 1992; 47: 441-450.
41. Bryant-Greenwood GD, Rutanen E -M, Partanen S et al. Sequential appearance of relaxin, prolactin and IGF-BP1 during growth and differentiation of the human endometrium. Mol Cell Endocrinol 1993; 95: 23-29.
42. Bani Sacchi T, Bigazzi M, Bani D et al. Relaxin increased coronary flow through stimulation of nitric oxide production. Br J Pharmacol 1995; 116: 1589-1594.
43. Masini E, Bani D, Bogazzi M et al. Effect of relaxin on mast cells. In vitro and in vivo studies in rats and guinea pigs. J Clin Invest 1994; 94: 1974-1980.
44. Bani D, Bigazzi M, Masini E et al. Relaxin depresses platelet aggregation. In vitro studies on isolated human and rabbit platelets. Lab Invest 1995; 73: 709-716.
45. Bani D, Ballati L, Masini E, Bigazzi M, Bani Sacchi T. Relaxin counteracts asthma-like reaction induced by inhaled antigen in sensitized guinea pigs. Endocrinology 1997; 138: 1909-1915.
46. Unemori EN, Lewis M, Constant J et al. Relaxin induces vascular endothelial growth factor expression and angiogenesis selectively at wound sites. Wound Repair Regen 2000; 8: 361-370.
47. Johnson MR, Abdalla H, Allman ACJ et al. Relaxin in ovum donation pregnancies. Fertil Steril 1991; 56: 59-61.
48. Nikas G, Drakakis P, Loutradis D et al. Uterine pinopodes as markers of the 'nidation' window in cyclic women receiving exogenous oestradiol and progesterone. Hum Reprod 1995; 10: 1208-1213.
49. Sengupta J, Ghosh D. Blastocyst-endometrium interaction at implantation in the rhesus monkey. J Reprod Immunol 2002; 53: 227-239.
50. Nardo LG, Sabatini L, Rai R, Nardo F. 2002 Pinopode expression during human implantation. Eur J Obstet Gynecol Reprod Biol 2002; 101: 104-108.
51. Bentin-Ley U. Relevance of endometrial pinopodes for human blastocyst implantation. Hum Reprod 2000; 15: 67-73.
52. Stavreus-Evers A, Masironi B, Landgren BM et al. Immunohistochemical localization of glutaredoxin and thioredoxin in human endometrium: a possible association with pinopodes. Mol Hum Reprod 2002; 8: 546-551.
53. Ciocca DR, Oesterreich S, Chamness GC et al. Biological and clinical implications of heat shock protein 27000 (Hsp 27): a review. J Natl Cancer Inst 1993; 85: 1558-1570.
54. Arrigo A-P, Landry J. Expression and function of the low molecular weight heat shock proteins. In The Biology of Heat Shock Proteins and Molecular Chaperones, Ed Morimoto RI, Tissieres A and Georgopoulos C, Cold Spring Harbour Laboratory Press, New York, pp 335-373.
55. Ghosh D, Roy A, Sengupta J, Johannisson E. Morphological characteristics of preimplantation stage endometrium in the rhesus monkey. Hum Reprod 1993; 8: 1579-1587.
56. Enders AC, Welsh AO, Schlafke S. Implantation in the rhesus monkey: endometrial responses. Am J Anat 1985; 173: 147-169.
57. Okada Y, Asahina T, Kobayashi T et al. Studies on the mechanism of edematous changes at the endometrial stroma for implantation. Semin Thromb Hemost 2001; 27: 67-77.
58. Manners CV. Endometrial assessment in a group of infertile women stimulated cycles for IVF: immunohistochemical findings. Hum Reprod 1990; 5: 128-132.
59. Sachdeva G, Patil V, Katkam RR et al. Expression profiles of endometrial leukemia inhibitory factor, transforming growth factor beta2 (TGFbeta2), and TGFbeta2 receptor in infertile bonnet monkeys. Biol Reprod 2001; 65: 1-8.
60. Okulicz WC, Ace CI, Longcope C, Tast J. Analysis of differential gene regulation in adequate versus inadequate secretory-phase endometrial complementary deoxyribonucleic acid populations from the rhesus monkey. Endocrinology 1996; 137: 4844-4850.
61. Bell SC, Keyle JW, Waites GT. Pregnancy-associated endometrial α2-globulin, the major secretory protein of the luteal phase and first trimester pregnancy endometrium is not glycosylated prolactin but related to β-lactoglobulins. J Clin Endocrinol Metab 1987; 65: 1067-1071.
62. Dalton CF, Laird SM, Serle E et al. The measurement of CA 125 and placental protein 14 in uterine flushings in women with recurrent miscarriage: relation to endometrial morphology. Hum Reprod 1995; 10: 2680-2684.
63. Lalitkumar PG L, Sengupta J, Karande A, Ghosh D 1998 Placental protein 14 in endometrium during menstrual cycle and effect of early luteal phase mifepristone administration on its expression in implantation stage endometrium in the rhesus monkey. Hum Reprod 1998; 13: 3478-3486.
64. Wahlstrom T, Koskimies AI, Tenhunen A et al. Pregnancy proteins in endometrium after follicle aspiration for in vitro fertilization. Ann N Y Acad Sci (USA) 1985; 442: 402-407.
65. Seppala M, Koistinen R, Rutanen E -M. Uterine endocrinology and paracrinology: insulin-like growth factor binding protein-1 and placental-14 revisited. Hum Reprod 1994; 9: 917-925.
66. Sharpe-Timms KL, Zimmer RL, Trammell SE et al. Immunolocalization of progesterone-induced uterine protein-1 in human endometrium during the menstrual cycle and in the placenta throughout gestation. Am J Obstet Gynecol 1995; 173: 1569-1578.
67. Seppala M, Tiitinen A. Endometrial reponses to corpus luteum products in cycles with induced ovulation: theoretical and practical consideration. Hum Reprod 1995; 10: 67-76.
68. Sugino N, Shimamura K, Takiguchi S et al. Changes in activity of superoxide dismutase inthe human endometrium throughout the menstrual cycle and in early pregnancy. Hum Reprod 1996; 11: 1073-1678.
69. Sugino N, Shimamura K, Tamura H et al. Progesterone inhibits pseudopregnant superoxide radical production by mononuclear phagocytes in pseudopregnant rats. Endocrinology 1996; 137: 740-754.
70. Hunt JS, Chen HL, Hu X, Tabibzadeh S. Tumour necrosis factor-α messenger ribonucleic acid and protein in human endometrium. Biol Reprod 1992; 47: 141-147.
71. Laird SM, Tuckerman E, Saravelos H, Li TC. The production of tumour necrosis factor-α (TNF-α) by human endometrial cells in culture. Hum Reprod 1996; 11: 1318-1323.
72. Narimoto K, Noda Y, Shiotani M et al. Immunohistochemical assessment of superoxide dismutase expression in the human enodmetrium throughout the menstrual cycle. Acta Histochem Cytochem 1990; 24: 85-91.
73. Wuu Y-D, Pampfer S, Becquet P et al. Tumor necrosis factor α decreases the viability of mouse blastocysts in vitro and in vivo. Biol Reprod 1999; 60: 479-483.
74. Pampfer S, Vanderheyden I, Vesela J, De Hertogh R D. Neutralization of tumor necrosis factor alpha (TNF alpha) action on cell proliferation in rat blastocysts by antisense oligodeoxyribonucleotides directed against TNF alpha p60 receptor. Biol Reprod 1995; 52: 1316-1326.
75. Zhu LJ, Cullivan-Bove K, Polihronis M et al. Calcitonin is a progesterone-regulated marker that forecasts the receptive state of endometrium during implantation. Endocrinology 1998; 139: 3923-3934
76. Li Q, Wang J, Armant DR, Bagchi MK, Bagchi IC. Calcitonin down-regulates E-cadherin expression in rodent uterine epithelium during implantation. J Biol Chem 2002; 277: 46447-46455.
77. Benson GV, Lim H, Paria BC et al. Mechanisms of reduced fertility in Hoxa-10 mutant mice: uterine homeosis and loss of maternal Hoxa-10 expression. Development 1996; 12: 2687-2696.
78. Taylor HS, Arici A, Olive D et al. Hoxa-10 is expressed in response to sex steroids at the time of implantation. J Clin Invest 1998; 101: 1379-1384.
79. Giudice LC. Genes associated with embryonic attchement and implantation and the role of progesterone. J Reprod Med 1999; 44: 165-171.
80. Gonazalez RR, Simon C, Caballero-Campo P et al. Leptin and reproduction. Hum Reprod Update 2000; 6: 290-300.
81. Domali E, Messinis IE. Leptin in pregnancy. J Matern Fetal Neonatal Med 2003; 12: 222-230.
82. Casslen B. Inhibitors of trypsin, chymotrypsin and elastase in human uterine fluid. Acta Obstet Gynaecol Scand 1986; 65: 121-124.
83. Schatz F, Lockwood CJ. Progestin regulation of plasminogen activator inhibitor type 1 in primary cultures of endometrial stromal and decidual cells. J Clin Endocrinol Metab 1993; 77: 621-625.
84. 2-Macroglobulin production by the human endometrium. J Clin Endocrinol Metab 1995; 80: 1021-1026.
85. Marbaix E, Donnez J, Courtoy PJ, Eeckhout Y. Progesterone regulates the activity of collagenase and related gelatinases A and B in human endometrium. Proc Natl Acad Sci (USA) 1992; 89: 11789-11793.
86. Marbaix E, Kokorine I, Donnez J, Eeckhout Y, Courtoy PJ. Regulation and restricted expression of intertitial collagenase suggest a pivotal role in the initiation of menstruation. Hum Reprod 1996; 11: 134-143.
87. Berthois Y, Brux JD, Salat-Baroux J et al. A multiparametric analysis of endometrial estrogen and progesterone receptors after the post-ovulatory administration of mifepristone. Fertil Steril 1991; 55: 547-554.
88. Bischof P, Campana A. Molecular mediators of implantation. Baillieres Best Pract Res Clin Obstet Gynecol 2000; 14: 801-814.
89. Shevensky LH, Knowles BB, Damjanov I, Solter D. Monoclonal antibody to murine embryos defines a stage specific embryonic antigen on mouse embryos and human teratocarcinoma cells. Cell 1982; 30: 697-705.
90. Fenderson BA, Kojima N, Zhu Z M et al. Specific interaction between Ley and H as a possible basic for trophectoderm-endometrium recognition during implantation. Glyoconjugate J 1991; 8: 177a.
91. Ghosh D, Liu N, Zhu ZM, Sengupta J. Immunolocalization of Ley oligosccharide in endometrium during menstrual cycle and effect of early luteal phase mifepristone administration on its expression in implantation stage endometrium of the rhesus monkey. Hum Reprod 1998; 13: 1374-1379.
92. Hey NA, Graham RA, Seif MW, Aplin JD. The polymorphic epithelial mucin MUC1 in human endometrium is regulated with maximal expression in the implantation phase. J Clin Endocrinol Metab 1994; 78: 337-342.
93. Meseguer M, Aplin JD, Caballero-Campo P et al. Human endometrial mucin MUC1 is up-regulated by progesterone and down-regulated in vitro by human blastocyst. Biol Reprod 2001; 64: 590-601.
94. 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.
95. Ruoslahti E. Integrins. J Clin Invest 1991; 87: 1-5.
96. Lessey BA, Damjanovich L, Coutfaris C et al. Integrin adhesion molecules in the human endometrium. Correlation with the normal and abnormal menstrual cycle. J Clin Invest 1992; 90: 188-195.
97. Lessey BA, Castelbaum AJ, Buck CA et al. Further characterization of endometrial integrins during the menstrual cycle and in pregnancy. Fertil Steril 1994; 62: 4975-6.
98. Tabibzadeh S. Patterns of expression of integrin molecules in human endometrium throughout the menstrual cycle. Hum Reprod 1992; 7: 876-882.
99. Campbell S, Swann HR, Seif MW. Cell adhesion molecules on oocyte and preimplantation human embryo. Hum Reprod 1995; 10: 1571-1578.
100. Check JH, Bollendorf A, Askari HA. Evidence for a leukocyte adhesion factor produced by the early embryo. Am J Reprod Immunol 1995; 34: 20-25.
101. Wang J, Armant DR. Integrin-medaited adhesion an signalling during blastocyst implantation. Cells Tissue Organs 2002; 172: 190-201.
102. Bourne TH, Hagstrom HG, Granberg S et al. Ultrasound studies of vascular and morphological changes in the human uterus after a positive self-test for the urinary luteinizing hormone surge. Hum Reprod 1996; 11: 369-375.
103. Gannon BJ, Carati CJ, Verco CJ. Endometrial perfusion across the normal human menstrual cycle assessed by laser Doppler fluxmetry. Hum Reprod 1997; 12: 132-139.
104. Scholtes MCW, Wladimiroff JW, van Rijen HJM, Hop WCJ. Uterine and ovarian flow velocity waveforms in the normal menstrual cycle: a transvaginal Doppler study. Fertil Steril 1989; 52: 981-985.
105. Battaglia C, Larocca E, Lanzani A et al. Doppler ultrasound studies of the uterine arteries in spontaneous and IVF stimulated ovarian cycles. Gynecol Endocrinol 1990; 4: 245-250.
106. Steer CV, Mill C, Campbell S et al. The use of transvaginal color flow imaging after in vitro fertilization to identify optimum uterine conditions before embryo transfer. Fertil Steril 1992; 57: 372-376.
107. Wada I, Hsu CC, Williams G et al. The benefits of low dose aspirin herapy in women with impaired uterine perfusion during assisted conception. Hum Reprod 1994; 9: 1954-1957.
108. Thorp J, Waksh S, Brath P. Low-dose aspirin inhibits thromboxane, but not prostacyclin production by human placental arteries. Am J Obstet Gynaecol 1988; 159: 1381-1384.
109. 2. Hum Reprod 1997; 12: 1567-1572.
110. Sengupta J, Ghosh D. Role of progesterone on periimplantation stage endometrium-embryo interaction in the primate. Steroids 2000; 65: 753-762.
111. Cameron LT, Davenport AP, Brown MJ, Smith SK. Endothelin-1 stimulates prostaglandin release from human endometrium. Prostaglandins Leukot Essent Fatty Acids 1991; 42: 155-157.
112. 2α secretion by uterine stromal cells in vitro. Endocrinology 1993; 132: 300-308.
113. Edwards RG. Physiological and molecular aspects of human implantation. Hum Reprod 1995; 10: 1-13.
114. Bany BM, Kennedy T. Regulation by epidermal growth factor of prostaglandin production and cyclooxygenase activity in sensitized rat endometrial stromal cells in vitro. J Reprod Fertil 1995; 104: 57-62.
115. Bany BM, Kennedy T. Interleukin-1α regulates prostaglandin production and cyclooxygenase activity in sensitized rat endometrial stromal cells in vitro. Biol Reprod 1995; 53: 126-132.
116. 2α. Hum Reprod 1996; 11: 1998-2002.
117. Ghosh D, Sengupta J. Recent developments in endocrinology and paracrinology of blastocyst implantation in the primate. Hum Reprod Update 1998; 4: 153-168.
118. Nayak NR, Ghosh D, Lasley BL et al. Anti-implantation activity of luteal phase mifepristone administration is not mimicked by prostaglandin synthesis inhibitor or prostaglandin analogue in the rhesus monkey. Contraception 1997; 55: 103-114.
119. Johannisson E, Oberholzer M, Sawhn ML, Bygdeman M. Vascular changes on the human endometrium following the administration of the progesterone antagonist, RU486. Contraception 1989; 39: 103-117.
120. Lindhard A, Bentin-Ley U, Ravn V et al. Biochemical evaluation of endometrial function at the time of implantation. Fertil Steril 2002; 78: 221-233.
121. Laird SM, Tuckerman EM, Dalton CF. The production of leukemia inhibitory factor by human endometrium: presence in uterine flushings and production by cells in culture. Hum Reprod 1997; 12: 569-574.
122. Hambartsoumian E. Endometrial leukemia inhibitory factor (LIF) as a possible cause of unexplained infertility and multiple failures of implantation. Am J Reprod Immunol 1998; 39: 137-143.
123. Gemzell-Danielsson K, Swahn ML, Bygdeman M. The effect of various doses of mifepristone on endometrial leukaemia inhibitory factor expression in the midluteal phase - an immunohistochemical study. Hum Reprod 1997; 12: 1293-1297.
124. Cullinan EB, Abbondanzo SJ, Anderson PS et al. Leukemia inhibitory factor (LIF) and LIF receptor expression in human suggests a potential autocrine/paracrine function in regulating embyo implantation. Proc Natl Acad Sci (USA) 1996; 93: 3115-3120.
125. Aghajanova L, Stavreus-Evers A, Nikas Y et al. Coexpression of pinopodes and leukemia inhibitory factor, as well as its receptor, in human endometrium. Fertil Steril 2003; 79: 808-814.
126. Chen HF, Shew JY, Ho HN, Hsu WL, Yang YSY. Expression of leukemia inhibitory factor and its receptor in preimplantation embryos. Fertil Steril 1999; 72: 713-719.
127. Pepper MS, Ferrara M, Orci L, Montesano R. Leukemia inhibitory factor (LIF) inhibits angiogenesis in vito. J Cell Sci 1995; 108: 73-83.
128. Ghosh D, Kumar PGLL, Sengupta J. Effects of early luteal phase administration of mifepristone (RU486) on leukaemia inhibitory factor, transforming growth factor β and vascular endothelial growth factor in the implantation stage endometrium of the rhesus monkey. J Endocrinol 1998; 157: 115-125.
129. Ledee-Bataille N, Lapree-Delage G, Taupin JL et al. Concentration of leukemia inhibitory factor (LIF) in uterine flushing fluid is highly predictive of embryo implantation. Hum Reprod 2002; 17: 213-218.
130. 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.
131. Yue ZP, Yang ZM, Wei P et al. Leukemia inhibitory factor, leukemia inhibitory factor receptor, and glycoprotein 130 in rhesus monkey uterus during menstrual cycle and early pregnancy. Biol Reprod 2000; 63: 508-512.
132. Mitchell MH, Swanson RJ, Oehninger S. In vivo effect of leukemia inhibitory factor (LIF) and an abti-LIF polyclonal antibody on murine embryo and fetal development following exposure at the time of transcervical blastocyst transfer. Biol Reprod 2002; 67: 460-464.
133. Dunglison GF, Barlow DH, Sargent II. Leukemia inhibitory factor significantly enhances the blastocyst formation rates of human embryos cultured in serum-free medium. Hum Reprod 1996; 11: 191-196.
134. Piccini MO, Scaletti C, Vultaggio A et al. Defective production of LIF, M-CSF and Th2-type cytokines by T cells at fetomaternal interface is associated with pregnancy loss. J Reprod Immunol 2001; 52: 35-43.
135. Simon C, Frances A, Lee BY et al. Immunohistochemical localization, identification and regulation of the interleukin-1 receptor antagonist in the human endometrium. Hum Reprod 1995; 10: 2472-2477.
136. De los Santos MJ, Mercador A, Frances A et al. Role of endometrial factors in regulating secretion of components of the immunoreactive human embryonic interleukin-1 system during embryonic development. Biol Reprod 1996; 54: 563-574.
137. Arici A, Engin O, Attar E, Olive DL. Modulation of leukemia inhibitory factor gene expression and protein biosynthesis in human endometrium. J Clin Endcorinol Metab 1995; 80: 1908-1915.
138. Elias JA, Zheng T, Whiting NL, Marcovici A, Trow TK. Cytokine-cytokine synergy and protein kinase C in the regulation of lung fibroblast leukemia inhibitory factor. Am J Physiol 1994; 266L: 426-435.
139. Sawai K, Matsuzaki N, Okada T et al. Human decidual cell biosynthesis of leukemia inhibitory factor: regulation by decidual cytokines and steroid hormones. Biol Reprod 1997; 56: 1274-1280.
140. Ghosh D, Dhara S, Kumar A, Sengupta J. Immunohistochemical lozalization of receptors for progesterone and oestradiol-17β in the implantation site of the rhesus monkey. Hum Reprod 1999; 14: 505-514.
141. Sengupta J, Dhawan L, Ghosh D. Immunohistochmical localization of leukemia inhibitory factor, interlekins 1 and 6 at the primary implantation site in the rhesus monkey. Cytokines 2003 (In press).
142. 2 production by endogenous secretion of interleukin-1 in decidual cells from term fetal membrane. Adv Exp Med Biol 1997; 433: 419-422.
143. Kennard EA, Zimmerman PD, Friedman CI, Kniss DA. Interleukin-1β induces cyclooxygenase-2 in cultured human decidual cells. Am J Reprod Immunol 1995; 34: 65-71.
144. Rauk PN, Chiao JP. Interleukin-1 stimulates human uterine prostaglandin production through induction of cyclooxygenase-2 expression. Am J Reprod Immunol 2000; 43: 152-159.
145. Strakova Z, Srisuparp S, Fazleabas AT. Interleukin-1β induces the expression of insulin-like growth factor binding protein-1 during decidualization in the primate. Endocrinology 2000; 141: 4664-4670.
146. Lebovic DI, Bentzien F, Chao VA et al. Induction of an angiogenic phenotype in endometriotic stromal cell cultures by interleukin-1beta. Mol Hum Reprod 2000; 6: 269-275.
147. Jung YD, Liu W, Reinmuth N et al. Vascular endothelial growth factor is upregulated by interleukin-1 beta in human vascular smooth muscle cells via the P38 mitogen-activated protein kinase pathway. Angiogenesis 2001; 4: 155-162.
148. Coxon A, Bolon B, Estrada J et al. Inhibition of interleukin-1 but not tumor necrosis factor suppresses neovascularization in rat models of corneal angiogenesis and adjuvant arthritis. Arthritis Rheum 2002; 46: 2604-2612.
149. Salven P, HattoriK, Heissig B, Rafii S. Interleukin-1alpha promotes angiogenesis in vivo via VEGFR-2 pathway by inducing inflammatory cell VEGF synthesis and secretion. FASEB J 2002; 16: 1471-1473.
150. Simon C, Gimeno MJ, Mercader A et al. Embryonic regulation of integrins β3, α4, and α1 in human endometrial epithelial cells in vitro. J Clin Endocrinol Metab 1997; 82: 2607-2616.
151. Das C, Kumar VS, Gupta S, Kumar S. Network of cytokines, integrins and hormones in human trophoblast cell. J Reprod Immunol 2002; 53: 257-268.
152. Kataoka H, Meng JY, Itoh H et al. Localization of hepatocyte growth factor activator inhibitor type 1 in Langhans' cells of human placenta. Histochem Cell Biol 2000; 114: 469-475.
153. Simon C, Frances A, Piquette GN et al. Embryonic implantation in mice is blocked by interleukin-1 receptor antagonist. Endocrinology 1994; 134: 521-528.
154. Salamonsen LA, Dimitriadis E, Robb L. Cytokines in implantation. Seminars Rep Med 2000; 18: 299-310.
155. Laird SM, Tuckerman E, Li TC, Bolton AE. Stimulation of human endometrial epithelial cell interleukin 6 production by interleukin 1 and placental protein 14. Hum Reprod 1994; 9: 1339-1343.
156. Tabibzadeh S, Kong QF, Babaknia A, May LT. Progressive rise in the expression of interleukin-6 in human endometrium during menstrual cycle is initiated during the implantation window. Hum Reprod 1995; 10: 2793-2799.
157. Tabibzadeh SS, Santhanam U, Sehgal PB, May LT. Cytokine-induced production of IFN-β 2/IL-6 by freshly explanted human endometrial stromal cells. Modulation by estradiol-17 β. J Immunol 1989; 142: 3134-3139.
158. Girasole G, Jilka RL, Passeri G et al. 17 beta-estradiol inhibits interleukin-6 production by bone marrow-derived stromal cells and osteoblasts in vitro: a potential mechanism for the antiosteoporotic effect of estrogens. J Clin Invest 1992; 89: 883-891.
159. Ray A, Zhang DH, Siegel MD, Ray P. Regulation of interleukin-6 gene expression by steroids. Ann N Y Acad Sci 1995; 762: 79-87.
160. De M, Sanford TR, Wood GW. Expression of interleukin 1, interleukin 6 and tumour necrosis factor alpha in mouse uterus during the periimplantation period of pregnancy. J Reprod Fertil 1993; 97: 83-89.
161. Smith SK, Charnock-Jones DS, Sharkey AM. The role of leukemia inhibitory factor and interleukin-6 in human reproduction. Hum Reprod 1998; 13: 237-246.
162. Kauma SW. Cytokines in implantation. J Reprod Fertil 2000; 55: 31-42.
163. Dimitriadis E, Salamonsen LA, Robb L. Expression of interleukin-11 during the human menstrual cycle: coincidence with stromal decidualization and relationship to leukemia inhibitory factor and prolactin. Mol Hum Reprod 2000; 6: 907-913.
164. Robb L, Li R, Hartley L et al. Infertility in female mice lacking the receptor for interleukin 11 is due to defective uterine response to implantation. Nat Med 1998; 4: 303-308.
165. Ernst M, Inglese M, Waring P et al. Defective gp130-mediated signal transducer and activator of transcription (STAT) signalling results in degenerative joint disease, gastrointestinal ulceration, and failure of uterine implantation. J Exp Med 2001; 194: 189-203.
166. Das SK, Flanders KC, Andrews GK, Dey SK. Expression of transforming growth factor-β isoforms (β2 and β3) in mouse uterus: analysis of the periimplantation period and effects of ovarian steroids. Endocrinology 1992; 130: 3459-3466.
167. Arici A, MacDonald PC, Casey ML. Modulation of the levels of transforming growth factor β messenger ribonucleic acids in human stromal cells. Biol Reprod 1996; 54: 436-469.
168. Rotello RR, Lieberman RC, Purchio AF, Gerschenson LE. Coordinated regulation of apoptosis and cell prolifeartion by transforming growth factor β1 in cultured uterine epithelial cells. Proc Natl Acad Sci USA 1991; 88: 3412-3415.
169. Rotello RR, Lieberman RC, Lepoff RB, Gerschenson LE. Characterization of uterine epithelium apoptotic cell death kinetics and regulation by progesterone and RU486. Am J Pathol 1992; 140: 449-456.
170. Schultz GA, Heyner S. Growth factors in preimplantation mammalian embryos. Oxford Rev Reprod Biol 1993; 15: 43-81.
171. Liu HC, Mele Cate D, Noyes N, Rosenwaks Z. Production of insulin like growth factor binding proteins (IGFBPs) by human endometrial stromal cells is stimulated by the presence of embryos. J Assist Reprod 1995; 12: 78-87.
172. Lai YM, Wang HS, Lee CL et al. Insulin like growth factor binding proteins produced by Vero cells, human oviductal cells anf human endometrial
173. Giudice LC, Irwin JC. Roles of the insulin like growth factor family in non-pregnant human endometrium and at the decidual:trophoblast interface. Semin Reprod Endocrinol 1999; 17: 13-21.
174. Hemmings R, Langlais J, Falcone T et al. Human embryo produce transforming growth factor α activity and insulin like growth factor II. Fertil Steril 1992; 58: 101-104.
175. Bell SK, Patel SR, Jackson JA. Major secretory protein of human decidualized endometrium in pregnancy is an insulin-like growth factor binding protein. J Endocrinol 1988; 118: 317-328.
176. Irwin JC, Giudice LC. IGFBP-1 binds to the α5β1 integrin in human cytotrophoblasts and inhibits invasion into decidualized endometrium stromal cells in vitro. Growth Horm IGF Res 1998; 8: 21-23.
177. Irwin JC, Suen LF, Faessen GH et al. Insulin-like growth factor (IGF) II inhibition of endometrial stromal cell tissue inhibitor of metalloproetinase-3 and IGF-binding proetinl suggests paracrine interactions at the decidua-trophoblast interface during human implantation. J Clin Endocrinol Metab 2001; 86: 2060-2064.
178. 1 integrin via mitogen-activated protein kinase pathway. J Clin Endocrinol Metab 2001; 86: 2484-2493.
179. 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.
180. Ghosh D, Bell SC, Sengupta J. Immunohistological localization of insulin like growth factor binding protein-1 in primary implantation sites and trauma-induced decidual tissues of the rhesus monkey. Placenta 2003 (In press).
181. Dhara S, Lalitkumar PGL, Sengupta J, Ghosh D. Immunohistochemical localization of insulin like growth factors I and II at the primary implantation site in the Rhesus monkey. Mol Hum Reprod 2001; 7: 365-371.
182. Lee PD, Giudice LC, Conover CA, Powell DR. Insulin like growth factor binding protein-1: recent findings and new directions. Proc Soc Exp Biol Med 1997; 216: 319-357.
183. Fowler DJ, Nicaides KH, Miell JP et al. Insulin-like growth factor bining protein-1 (IGFBP-1): a multifunctional role in the human female reproductive tract. Hum Reprod Update 2000; 6: 495-504.
184. Giudice LC, Conover CA, Bale L et al. Identification and regulation of the IGFBP-4 protease and its physiological inhibition in the human trophoblasts and endometrial stroma: evidence fo paracrine regulation of IGF-II bioavailability in the placental bed during human implantation. J Clin Endocrinol Metab 2002; 87: 2359-2366.
185. Crossey PA, Pillai CC, Miell PP. Altered placental development and intrauterine growth restriction in IGF binding proetinl transgenic mice. J Clin Invest 2002; 110: 411-418.
186. Gratton RJ, Asano H, Han VK. The regional expression of insulin-like growth factor binding proteinl (IGFBP-1) in the placentae of women with pre-eclampsia. Placenta 2002; 23: 303-310.
187. 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: 112-118.
188. Torry DS, Holt VJ, Keenan JA et al. Vascular endothelial growth factor expression in cyclic human endometrium. Fertil Steril 1996; 66: 72-80.
189. Naresh B, Sengupta J, Bhargava V et al. Immunohistological localisation of vascular endothelial growth factor in human endometrium. Indian J Physiol Pharmacol 1999; 43: 165-70.
190. 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.
191. Greb RR, Bokowski R, Hsiu JG et al. Vacsular growth factor (VEGF) in primate endometrium. Immunohistochemical patterns during the cycle and after chronic RU486 treatment in cynomolgus monkeys. Ann NY Acad Sci (USA) 1995; 761: 376-381.
192. Hornung D, Lebovic DI, Shifren JL et al. Vectorial secretion of vascular endothelial growth factor by polarized human endometrial epithelial cells. Fertil Steril 1998; 69: 909-915.
193. Tanaka T, Kanai H, Sekiguchi K et al. Induction of VEGF gene transcription by IL-1 beta mediated through stress-actiavted MAP kinases and Spl sites in cardiac myocytes. J Mol Cell Cardiol 2000; 32: 1955-1967.
194. Imaizumi T, Itaya H, Nasu S et al. Expression of vascular endothelial growth factor in human umbilical vein endothelial cells stimulated with interleukin 1 alpha - an autocrine regulation of angiogenesis and inflammatory reactions. Thromb Haemost 2000; 83: 949-955.
195. Levitas E, Chamoun D, Udoff LC et al. Periovulatory and interleukin-1 beta dependent up-regulation of intraovarian vascular endothelial growth factor (VEGF) in the rat: potential role for VEGF in the promotion of periovulatoy angiogenesis and vascular permeability. J Soc Gynecol Investig 2000; 7: 51-60.
196. Lebovic DI, Shifren JL, Ryan IP et al. Ovarian steroid and cytokine modulation of human endometrial angiogenesis. Hum Reprod 2000; 15: 67-77.
197. Maruyama K, Mori Y, Murasawa S et al. Interleukin-1 beta upregulates cardiac expression of vascular endothelial growth factor and its receptor KDR/flk-1 via activation of protein tyrosin kinases. J Mol Cell Cardiol 1999; 31: 607-617.
198. Wulf C, Wilson H, Dickson SE et al. Hemochorial placentation in the primate: expression of vascular endothelial growth factor, angiopoietins, and their receptors throughout pregnancy. Biol Reprod 2002; 66: 802-812.
199. Ghosh D, Sharkey AM, Charnock-Jones DS et al. Expression of vascular endothelial growth factor (VEGF) and placental growth factor (PIGF) in conceptus and endometrium in the rhesus monkey. Mol Hum Reprod 6; 935-941.
200. Ahmed A, Dunk C, Kniss D and Wilkes M. Role of VEGF receptor-1 (Flt-1) in mediating calcium dependent nitric oxide release and limiting DNA synthesis in human trophoblast cells. Lab Invest 1997; 76: 779-791.
201. Athanassiades A, Hamilton GS, Lala PK. Vascular endothelial growth factor stimulates proliferation but not migration or inavasiveness in human extravillous trophoblast. Biol Reprod 1998; 59: 643-654.
202. Hastings JM, Licence DR, Burton GJ et al. Soluble vascular endothelial growth factor receptor 1 inhibits edema and epithelial proliferation induced by 17β-estradiol in the mouse uterus. Endocrinology 2003; 144: 326-334.
203. Rowe AJ, Morris KD, Bicknell R, Fraser HM. Angiogenesis in the corpus luteum of early pregnancy in the marmoset and the effects of vascular endothelial growth factor immunoneutralization on establishment of pregnancy. Biol Reprod 2002; 67: 1180-1188.
204. Collo G, Pepper MS. Endothelial cell integrin α5β1 is modulated by cytokines and during migration in vitro. J Cell Sci 1999; 112: 569-578.
205. Gustafsson T, Anderson P, Arnqvist HJ. Different inihibitory actions of IGFBP-1, -2 and -4 on IGF-I effects in vascular smooth muscle cells. J Endocrinol 1999; 161: 245-253.
206. Dahlfors G, Arnqvist HJ. Vacsular endothelial growth factor and transforming growth factor-b1 regulate the expression of insulin like growth factor-binding protein-3, -4, and -5 in large vessel endothelial cells. Endocrinology 2000; 141: 2062-2067.
207. Jung YD, Liu W, Reinmuth N et al. Vascular growth factor is upregulated by interleukin-1 beta in human vascular smooth muscle cells via the P38 mitogen-activated protein kinase pathway. Angiogenesis 2001; 4: 155-162.
208. Pollard JW, Hunt JS, Wiktor-Jedrzejczak W, Stanley ER. A pregnancy defect in the oesteopterotic (op/op) mouse demonstrates the requirement for CSF-1 in female infertility. Dev Biol 1991; 148: 273-283.
209. Robertson SA, Roberts CT, Farr KL et al. Fertility impairment in granulocyte-macrophage colony stimulating factor deficient mice. Biol Reprod 1999; 60: 251-261.
210. 1 knock-out mice: a mutation in one cytokine gene causes a dramatic inflammatory disease. Am J Pathol 1993; 143: 3-9.
211. Shull MM, Ormsby I, Kier AB et al. Targeted disruption of the mouse transforming growth factor beta-1 gene in multifocal inflammatory disease. Nature 1992; 359: 693-699.
212. Stewart CL, Kaspar P, Brunet LJ et al. Blastocyst implantation depends on maternal expression of leukaemia inhibitory factor. Nature 1992; 359: 76-79.
213. 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.
214. Abbondanzo SJ, Cullinan FB, McIntyre K et al. Reproduction in mice lacking a functional type 1 IL-1 receptor. Endocrinology 1996; 137: 3598-3601.
215. Kopf M, Baumann H, Freer G et al. Impaired immune and acute-phase responses in interleukin-6 deficient mice. Nature 1994; 368: 339-342.
216. Robertson SA, O'Connell A, Ramsey A. The effect of interleukin 6 deiciency on implantation, fetal development and parturition in mice. Proc Aust Soc Reprod Biol 2000; 31: 97.
217. 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 aqnd haematological disorders. Proc Natl Acad Sci USA 1996; 93: 407-411.
218. 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.
219. Toder V, Fein A, Carp H, Torchinsky A. TNF-alpha in pregnancy loss and embryo maldevelopment: a mediator of detrimental stimuli or a protector of the fetoplacental unit. J Assist Reprod Gent 2003; 20: 73-81.
220. Carmeliet P, Ferreira V, Breir G et al. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 1996; 380: 435-439.
221. Fong GH, Rossant J, Gertsenstein M, Breitman ML Role of Flt-1 receptor tyrosine kinase in regulating the assembly of vesicular endothelium. Nature 1995; 376: 66-70.
222. Shalaby F, Rossant J, Yamguchi TP et al. Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature 1995; 376: 62-66.