Embryo-maternal signalling: How the embryo starts talking to its mother to accomplish implantation

Reproductive BioMedicine Online

Volumn 6, Issue 2, 2003, Pages 244-256

  Herrler, Andreas ^a   von Rango, Ulrike ^a   Beier, Henning M ^a  

^a RWTH AACHEN UNIVERSITY   (Germany)

Author keywords

Embryo maternal signalling; Extra embryonic matrix; Maternal immunological tolerance

Indexed keywords

CHORIONIC GONADOTROPIN; COLONY STIMULATING FACTOR; HAPTOGLOBIN; INTERLEUKIN 1BETA; LEUKEMIA INHIBITORY FACTOR; MATRIX METALLOPROTEINASE; PROGESTERONE; SOMATOMEDIN; SOMATOMEDIN BINDING PROTEIN 1; SOMATOMEDIN BINDING PROTEIN 3; UTEROGLOBIN;

ARTICLE; EMBRYO; ENDOMETRIUM; ENZYME ACTIVATION; HORMONE RELEASE; HUMAN; IMMUNOLOGICAL TOLERANCE; MOLECULAR INTERACTION; NIDATION; NONHUMAN; PLACENTA; PREGNANCY; PRIMATE; PROGESTERONE RELEASE; T LYMPHOCYTE ACTIVATION; TROPHOBLAST; ZONA PELLUCIDA;

EID: 0038045153     PISSN: 14726483     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1472-6483(10)61717-8     Document Type: Article

References (86)

1. Arici A, Engin O, Attar E, Olive DL 1995 Modulation of leukemia inhibitory factor gene expression and protein biosynthesis in human endometrium. Journal of Clinical Endocrinology and Metabolism 80, 1908-1915.
2. Baird DD, Weinberg CR, Wilcox AJ et al. 1991 Hormonal profiles of natural conception cycles ending in early, unrecognized pregnancy loss. Journal of Clinical Endocrinology and Metabolism 72, 793-800.
3. Beier HM 1966 Das Proteinmilieu im Blutserum, Uterus und in den Blastocysten des Kaninchens vor der Nidation. In: Behrmann W (ed.) Colloquium Biochemie der Morphogenese. Deutsche Forschungsgemeinschaft, Konstanz, pp. 1-10.
4. Beier HM 1968 Uteroglobin: a hormone-sensitive endometrial protein involved in blastocyst development. Biochimica et Biophysica Acta 160, 289-291.
5. Beier HM, Beier-Hellwig K 1973 Specific secretory protein of the female genital tract. Acta Endocrinologica (Kbh.) 180, 404-425.
6. Beier HM, Mootz U 1979 Significance of maternal uterine proteins in the establishment of pregnancy. In: Maternal recognition of pregnancy. Excerpta Medica/North Holland, Amsterdam-Elsevier/North-Holland, New York, Ciba Foundation Series 64, 111-140.
7. Bellone M, Iezzi G, Rovere P et al. 1997 Processing of engulfed apoptotic bodies yields T cell epitopes. Journal of Immunology 159, 5391-5399.
8. Bergeron D, Ouellette MJ, Lambert RD 1997 PGE2, but not TGFβ2, in rabbit blastocoelic fluid regulates the cytotoxic activities of NK and LAK cells. Journal of Reproductive Immunology 33, 203-219.
9. Bernardini L, Moretti-Rojas I, Brush M et al. 1995 Status of hCG/LH receptor and G proteins in human endometrium during artificial cycles of hormone replacement therapy. Journal of the Society for Gynecological Investigation 2, 630-635.
10. Bischof P 2001 Endocrine, paracrine and autocrine regulation of trophoblastic metalloproteinases. Early Pregnancy 5, 30-31.
11. Bonduelle ML, Dodd R, Liebaers I et al. 1988 Chorionic gonadotrophin-β mRNA, a trophoblast marker, is expressed in human 8-cell embryos derived from tripronucleate zygotes. Human Reproduction 3, 909-914.
12. Bottini N, Gimelfarb A, Gloria-Bottini F et al. 1999 Haptoglobin genotype and natural fertility in humans. Fertility and Sterility 72, 293-296.
13. Chao KH, Wu MY, Chen CD et al. 1999 The expression of killer cell inhibitory receptors on natural killer cells and activation status of CD4+ and CD8+ T cells in the decidua of normal and abnormal early pregnancies. Human Immunology 60, 791-797.
14. Chaouat G 2001 New insights into maternal-fetal interactions at implantation. Reproductive BioMedicine Online 2, 198-203.
15. Conover CA, Clarkson JT, Bale LK 1996 Factors regulating insulin-like growth factor binding protein-3 binding, processing, and potentiation of insulin-like growth factor action. Endocrinology 137, 2286-2292.
16. Dannhorn DR, Gierhake S, Kirchner C 1991 Uteroglobin in the developing rabbit conceptus in vivo and in vitro. Anatomy and Embryology 184, 141-152.
17. Dobryszycka W 1997 Biological functions of haptoglobin - new pieces to an old puzzle. European Journal of Clinical Chemistry and Clinical Biochemistry 35, 647-654.
18. Duncan WC 2000 The human corpus luteum: remodelling during luteolysis and maternal recognition of pregnancy. Reviews of Reproduction 5, 12-17.
19. Egawa H, Fujiwara H, Hirano T et al. 2002 Peripheral blood mononuclear cells in early pregnancy promote invasion of human choriocarcinoma cell line, Be Wo cells. Human Reproduction 17, 473-480.
20. El Ghmati SM, Van Hoeyveld EM, Van Strijp JG et al. 1996 Identification of haptoglobin as an alternative ligand for CD11b/CD18. Journal of Immunology 156, 2542-2552.
21. Ewoldsen MA, Ostlie NS, Warner CM 1987 Killing of mouse blastocyst stage embryos by cytotoxic T lymphocytes directed to major histocompatibility complex antigens. Journal of Immunology 138, 2764-2770.
22. Fazleabas AT, Kim JJ, Srinivasan S et al. 1999 Implantation in the baboon: endometrial responses. Seminars in Reproductive Endocrinology 17, 257-265.
23. Fishel SB, Edwards RG, Evans CJ 1984 Human chorionic gonadotropin secreted by preimplantation embryos cultured in vitro. Science 223, 816-818.
24. Fortin M, Ouellette MJ, Lambert RD 1997 TGF-β 2 and PGE2 in rabbit blastocoelic fluid can modulate GM-CSF production by human lymphocytes. American Journal of Reproductive Immunology 38, 129-139.
25. Gleeson LM, Chakraborty C, McKinnon T, Lala PK 2001 Insulin-like growth factor-binding protein 1 stimulates human trophoblast migration by signalling through alpha 5β1 integrin via mitogen-activated protein kinase pathway. Journal of Clinical Endocrinology and Metabolism 86, 2484-2493.
26. Guimond MJ, Wang B, Croy BA 1998 Engraftment of bone marrow from severe combined immunodeficient (SCID) mice reverses the reproductive deficits in natural killer cell-deficient tg epsilon 26 mice. Journal of Experimental Medicine 187, 217-223.
27. Gupta SK, Singh V 1988 Immunobiology of human chorionic gonadotropin. Indian Journal of Experimental Biology 26, 243-251.
28. Hahnel A, Schultz GA 1994 Insulin-like growth factor binding proteins are transcribed by preimplantation mouse embryos. Endocrinology 134, 1956-1959.
29. Han SW, Lei ZM, Rao CV 1996 Up-regulation of cyclooxygenase-2 gene expression by chorionic gonadotropin during the differentiation of human endometrial stromal cells into decidua. Endocrinology 137, 1791-1797.
30. Han SW, Lei ZM, Rao CV 1999 Treatment of human endometrial stromal cells with chorionic gonadotropin promotes their morphological and functional differentiation into decidua. Molecular and Cellular Endocrinology 147, 7-16.
31. Hearn JP 1976 Immunization against pregnancy. Proceedings of the Royal Society of London B [Biological Sciences] 195, 149-160.
32. Hearn JP 2001 Embryo implantation and embryonic stem cell development in primates. Reproduction, Fertility and Development 13, 517-522.
33. Hearn JP, Hodges JK, Gems S 1988 Early secretion of chorionic gonadotrophin by marmoset embryos in vivo and in vitro. Journal of Endocrinology 119, 249-255.
34. Hegele-Hartung C, Dreiner U, Beier HM 1991 Effect of in vitro culture on the dynamics of uteroglobin distribution in rabbit blastocysts. Anatomy and Embryology 183, 119-128.
35. Herrler A, Beier HM 2000 Early embryonic coats: morphology, function, practical applications. Cells, Tissues, Organs 166, 233-247.
36. Herrler A, Einspanier R, Beier HM 1997 Binding of IGF-I to preimplantation rabbit embryos and their coats. Theriogenology 47, 1595-1607.
37. Herrler A, Krusche CA, Beier HM 1998 Insulin and insulin-like growth factor-I promote rabbit blastocyst development and prevent apoptosis. Biology of Reproduction 59, 1302-1310.
38. Herrler A, Pell JM, Allen WR et al. 2000 Equine blastocyst secrete insulin-like growth factor-binding protein 3 (IGFBP3). Biology of Reproduction 62, 1804-1811.
39. Herrler A, Eisner S, Müller-Schöttle M, Beier HM 2001 Preimplantation maternal embryonic signalling: haptoglobin, a maternal message. Journal of Reproduction and Fertility 27, 18.
40. Herrler A, von Wolf M, Beier HM 2002 Proteins in the extraembryonic matrix of preimplantation rabbit embryos. Anatomy and Embryology http://dx.doi.org/10.1007/s00429-002-0270-9.
41. Hoffman LH, Winfrey VP, Blaeuer GL, Olson GE 1996 A haptoglobin-like glycoprotein is produced by implantation-stage rabbit endometrium. Biology of Reproduction 55, 176-184.
42. Kadyrov M, Kaufmann P, Huppertz B 2001 Expression of a cytokeratin 18 neo-epitope is a specific marker for trophoblast apoptosis in human placenta. Placenta 22, 44-48.
43. Kane MT, Morgan PM, Coonan C 1997 Peptide growth factors and preimplantation development. Human Reproduction Update 3, 137-157.
44. Lee CY, Green ML, Simmen RC, Simmen FA 1998 Proteolysis of insulin-like growth factor-binding proteins (IGFBPs) within the pig uterine lumen associated with peri-implantation conceptus development. Journal of Reproduction and Fertility 112, 369-377.
45. Levine JS, Koh JS 1999 The role of apoptosis in autoimmunity: immunogen, antigen, and accelerant. Seminars in Nephrology 19, 34-47.
46. Licht P, Lösch A, Diettrich R, Neuwinger J 1998 Novel insights into human endometrial paracrinology and embryo-maternal communication by intrauterine microdialysis. Human Reproduction Update 4, 532-538.
47. Licht P, Russu V, Wildt L 2001 On the role of human chorionic gonadotropin (hCG) in the embryo-endometrial microenvironment: implications for differentiation and implantation. Seminars in Reproductive Medicine 19, 37-47.
48. Macklon NS, Geraedts JP, Fauser BC 2002 Conception to ongoing pregnancy: the 'black box' of early pregnancy loss. Human Reproduction Update 8 333-343.
49. Makrigiannakis A, Zoumakis E, Kalantaridou S et al. 2001 Corticotropin-releasing hormone promotes blastocyst implantation and early maternal tolerance. Nature Immunology 2, 1018-1024.
50. Mochizuki M, Maruo T, Matsuo H et al. 1998 Biology of human trophoblast. International Journal of Gynaecology and Obstetrics 60, S21-28.
51. Moffett-King A 2002 Natural killer cells and pregnancy. Nature Reviews in Immunology 2 656-663.
52. Müller-Schöttle F, Classen-Linke I, Beier-Hellwig K et al. 2000 Uteroglobin expression and release in the human endometrium. Annals of the New York Academy of Sciences 923, 332-335.
53. Müller-Schöttle F, Bogusz A, Grotzinger J et al. 2002 Full-length complementary DNA and the derived amino acid sequence of horse uteroglobin. Biology of Reproduction 66, 1723-1728.
54. Nakayama T, Fujiwara H, Maeda M et al. 2002 Human peripheral blood mononuclear cells (PBMC) in early pregnancy promote embryo invasion in vitro: HCG enhances the effects of PBMC. Human Reproduction 17, 207-212.
55. +) cells. Reproduction Abstracts Series 29, 21.
56. Ouellette MJ, Dubois CM, Bergeron D et al. 1997 TGFβ 2 in rabbit blastocoelic fluid regulates CD4 membrane expression: possible role in the success of gestation. American Journal of Reproductive Immunology 37, 125-136.
57. Ouellette MJ, St-Jacques S, Lambert RD 1999 CD8 membrane expression is down-regulated by transforming growth factor (TGF)-β 1, TGF-β2, and prostaglandin E2. American Journal of Reproductive Immunology 41, 183-191.
58. Pandian AM, Lambert RD, Roy R 1988 Immunosuppressive effects of rabbit blastocoelic fluid and embryo culture medium. Journal of Reproductive Immunology 13, 221-234.
59. Peng X, Kim JJ, Fazleabas AT 2000 Apoptosis and differentiation in baboon stromal cells: a role for chorionic gonadotropin (CG)? Biology of Reproduction 62, abstract 510.
60. Piccinni MP, Scaletti C, Mavilia C et al. 2001a Production of IL-4 and leukemia inhibitory factor by T cells of the cumulus oophorus: a favorable microenvironment for pre-implantation embryo development. European Journal of Immunology 31, 2431-2437.
61. Piccinni MP, Scaletti C, Vultaggio A et al. 2001b Defective production of LIF, M-CSF and Th2-type cytokines by T cells at fetomaternal interface is associated with pregnancy loss. Journal of Reproductive Immunology 52, 35-43.
62. Pilon AL 2000 Rational for the development of recombinant human CC10 as a therapeutic for inflammatory and fibrotic disease. Annals of the New York Academy of Sciences 923, 280-299.
63. Reshef E, Lei ZM, Rao CV et al. 1990 The presence of gonadotropin receptors in nonpregnant human uterus, human placenta, fetal membranes, and decidua. Journal of Clinical Endocrinology and Metabolism 70, 421-430.
64. Saito S, Nishikawa K, Morii T et al. 1992 Expression of activation antigens CD69, HLA-DR, interleukin-2 receptor-alpha (IL-2R alpha) and IL-2Rβ on T cells of human decidua at an early stage of pregnancy. Immunology 75, 710-712.
65. Savion S, Zeldich E, Orenstein H et al. 2002 Cytokine expression in the uterus of mice with pregnancy loss: effect of maternal immunopotentiation with GM-CSF. Reproduction 123, 399-409.
66. Seshagiri PB, Terasawa E, Hearn JP 1994 The secretion of gonadotrophin-releasing hormone by peri-implantation embryos of the rhesus monkey: comparison with the secretion of chorionic gonadotrophin. Human Reproduction 9, 1300-1307.
67. Sharkey AM, Dellow K, Blayney M et al. 1995 Stage-specific expression of cytokine and receptor messenger ribonucleic acids in human preimplantation embryos. Biology of Reproduction 53. 974-981.
68. Simón C, Mercader A. Gimeno MJ, Pellicer A 1997 The interleukin-1 system and human implantation. American Journal of Reproductive Immunology 37, 64-72.
69. Simón C, Moreno C, Remohi J, Pellicer A 1998a Molecular interactions between embryo and uterus in the adhesion phase of human implantation. Human Reproduction 13, 219-232.
70. Simón C, Valbuena D, Krussel J et al. 1998b Interleukin-1 receptor antagonist prevents embryonic implantation by a direct effect on the endometrial epithelium. Fertility and Sterility 70, 896-906.
71. Smith RM, Garside WT, Aghayan M et al. 1993 Mouse preimplantation embryos exhibit receptor-mediated binding and transcytosis of maternal insulin-like growth factor I. Biology of Reproduction 49, 1-12.
72. Spanos S, Becker DL, Winston RM, Hardy K 2000 Anti-apoptotic action of insulin-like growth factor-I during human preimplantation embryo development. Biology of Reproduction 63, 1413-1420.
73. Srisuparp S, Strakova Z, Luborsky J, Fazleabas AT 2000 Signalling pathways activated by chorionic gonadotropin (CG) in the primate endometrium. Biology Reproduction 62, abstract 33.
74. Srisuparp S, Strakova Z, Fazleabas AT 2001 The role of chorionic gonadotropin (CG) in blastocyst implantation. Archives of Medical Research 32, 627-634.
75. Steinman RM, Turley S, Mellman I, Inaba K 2000 The induction of tolerance by dendritic cells that have captured apoptotic cells. Journal of Experimental Medicine 191, 411-416.
76. Stewart EA 2001 Gonadotropins and the uterus: is there it gonad-independent pathway? Journal of the Society for Gynecological Investigation 8, 319-326.
77. Stewart EA, Sahakian M, Rhoades A et al. 1999 Messenger ribonucleic acid for the gonadal luteinizing hormone/human chorionic gonadotropin receptor is not present in human endometrium. Fertility and Sterility 71, 368-372.
78. Strakova Z, Srisuparp S, Fazleabas AT 2000 Interleukin-1β induces the expression of insulin-like growth factor binding protein-1 during decidualization in the primate. Endocrinology 141, 4664-4670.
79. Talwar GP, Singh OM, Gupta SK et al. 1997 The HSD-hCG vaccine prevents pregnancy in women: feasibility study of a reversible safe contraceptive vaccine. American Journal of Reproductive Immunology 37, 153-160.
80. Van Parijs L, Abbas AK 1998 Homeostasis and self-tolerance in the immune system: turning lymphocytes off. Science 280, 243-248.
81. Vandermolen DT, Gu Y 1996 Human endometrial expression of granulocyte colony-stimulating factor (G-CSF) and its receptor, stimulation of endometrial G-CSF production by interleukin-1β, and G-CSF inhibition of choriocarcinoma cell proliferation. American Journal of Reproductive Immunology 36, 278-284.
82. von Rango U, Classen-Linke I, Kertschanska S et al. 2001 Effects of trophoblast invasion on the distribution of leukocytes in uterine and tubal implantation sites. Fertility and Sterility 76, 116-124.
83. von Rango U, Classen-Linke I, Raven G et al. 2003 Establishment of cytokine microenvironment in human first trimester decidua is mediated by the trophoblast. Fertility and Sterility, in press.
84. Wilcox AJ, Baird DD, Weinberg CR 1999 Time of implantation of the conceptus and loss of pregnancy. New England Journal of Medicine 340, 1796-1799.
85. Woodward BJ, Lenton EA, Turner K 1993 Human chorionic gonadotrophin: embryonic secretion is a time-dependent phenomenon. Human Reproduction 8, 1463-1468.
86. Ziecik AJ, Derecka K, Gawronska B et al. 2001 Nongonadal LH/hCG receptors in pig: functional importance and parallels to human. Seminars in Reproductive Medicine 19, 19-30.