Embryo-maternal interactions at the implantation site: A delicate equilibrium

European Journal of Obstetrics and Gynecology and Reproductive Biology

Volumn 83, Issue 1, 1999, Pages 85-100

  Duc Goiran, P ^a   Mignot, T M ^a   Bourgeois, C ^a   Ferre F ^a  

^a INSERM   (France)

Author keywords

Blastocyst; Cytokines; Endometrium; Growth factors; Implantation; Integrins; Interferons; Proteinases; Trophoblast

Indexed keywords

CHORIONIC GONADOTROPIN; COLONY STIMULATING FACTOR 1; EARLY PREGNANCY FACTOR; ENDOTHELIN 1; EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; GAMMA INTERFERON; GELATINASE; GRANULOCYTE COLONY STIMULATING FACTOR; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTEGRIN; INTERLEUKIN 1; INTERLEUKIN 6; MATRIX METALLOPROTEINASE; PLATELET DERIVED GROWTH FACTOR A; PLATELET DERIVED GROWTH FACTOR RECEPTOR; PROSTAGLANDIN E2; SOMATOMEDIN B; THROMBOCYTE ACTIVATING FACTOR; TISSUE INHIBITOR OF METALLOPROTEINASE 3; TRANSFORMING GROWTH FACTOR ALPHA; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; BLASTOCYST; EMBRYO; ENDOMETRIUM; FEMALE; GENE EXPRESSION REGULATION; HUMAN; HUMAN TISSUE; IMPLANTATION; NIDATION; PLACENTA DEVELOPMENT; PREIMPLANTATION EMBRYO; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TROPHOBLAST;

EID: 0033034933     PISSN: 03012115     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0301-2115(98)00310-8     Document Type: Article

References (109)

1. Loke YW, King A, editors. Human implantation: cell biology and immunology. Cambridge: Cambridge University Press, 1995:15-21, 33-6, 52-62, 101-20, 212-7.
2. Ezra Y., Schenker J.G. Abortion rate in assisted reproduction - true increase? Early Preg Biol Med. 1:1995;171-175.
3. Wilcox A.J., Weinberg C.R., O'Connor J.F., Baird D.D., Schlatterer J.P., Canfield R.E., Armstrong E.G., Nisula B.C. Incidence of early loss of pregnancy. New Engl J Med. 319(4):1988;189-194.
4. Larsen WJ, editor. Human embryology. New York: Churchill Livingstone, 1993:20-1.
5. Tabibzadeh S, Babaknia A. The signals and molecular pathways involved in implantation, a symbiotic interaction between blastocyst and endometrium involving adhesion and tissue invasion. Mol Human Reprod 1995;10(6):
6. Cross J.C., Werb Z., Fisher S.J. Implantation and the placenta: key pieces of the development puzzle. Science. 266:1994;1508-1518.
7. Larue L., Ohsugi M., Hirchenhain J., Kemler R. E-cadherin null mutant embryos fail to form a trophectoderm epithelium. Proc Natl Acad Sci USA. 91:1994;8263-8267.
8. Sengupta J., De P., Ghosh D. Implantation of the primate embryo. Current Science. 68(4):1995;363-373.
9. Morton H., Rolfe B., Clunie G.J.A., Anderson M.J., Morrison J. An early pregnancy factor detected in human serum by the rosette inhibition test. Lancet. 1:1977;394-397.
10. Cavanagh A.C., Morton H. The purification of early-pregnancy factor to homogeneity from human platelets and identification as chaperonin 10. Eur J Biochem. 222:1994;551-560.
11. Coulam C.B., Roussev R.G., Thomason E.J., Barnea E.R. Preimplantation factor (PIF) predicts subsequent pregnancy loss. Am J Reprod Immunol. 34:1995;88-92.
12. Roussev R.G., Coulam C.B., Kaider B.D., Yarkoni M., Leavis P.C., Barnea E.R. Embryonic origin of preimplantation factor (PIF): biological activity and partial characterization. Mol Human Reprod. 2:1996;883-887.
13. Chia C.M., Winston R.M., Handyside A.H. EGF, TGF-α and EGFR expression in human preimplantation embryos. Development. 121:1995;299-307.
14. Österlund C., Wramsby H., Pousette A. Temporal expression of platelet-drived growth factor (PDGF)-A and its receptor in human preimplantation embryos. Mol Hum Reprod. 2(7):1996;507-512.
15. Sharkey A. Cytokines and embryo/endometrial interactions. Reprod Med. Rev. 4:1995;87-100.
16. Kane M.T., Morgan P.M., Coonan C. Peptide growth factors and preim-plantation development. Hum Reprod Update. 3(2):1997;137-157.
17. Austgulen R., Arntzen K.J., Vatten L.J., Kahn J., Sunde A. Detection of cytokines (interleukin-1, interleukin-6, transforming growth factor-β) and soluble tumour necrosis factor receptors in embryo culture fluids during in-vitro fertilization. Hum Reprod. 10(1):1995;171-176.
18. Sheth K.V., Roca G.L., Al-Sedairy S.T., Parhar R.S., Hamilton C.J.C.M., Al-Abdul Jabbar F. Prediction of successful embryo implantation by measuring interleukin-1-alpha and immunosuppressive factors(s) in preimplantation embryo culture fluid. Fertil Steril. 55:1991;952-957.
19. Holmes P.V., Sjogren A., Hamberger L. Prostaglandin-E2 released by pre-implantation human conceptuses. J Reprod Immunol. 17:1990;79-86.
20. Collier M., O'Neill C., Ammit A.J., Saunders D.M. Biochemical and pharmacological characterization of human embryo-derived platelet activating factor. Hum Reprod. 3:1988;993-998.
21. van der Weiden R.M.F., Helmerhorst F.M., Keirse M.J.N.C. Influence of prostaglandins and platelet activating factor on implantation. Hum Reprod. 6(3):1991;436-442.
22. Roberts R.M., Cross J.C., Leaman D.W. Interferons as hormones of pregnancy. Endocrine Rev. 13:1992;432-452.
23. Aldhous P. A booster for contraceptive vaccines. Science. 266:1994;1484-1486.
24. Robertson S.A., Seamark R.F., Guilbert L.J., Wegmann T.G. The role of cytokines in gestation. Crit Rev Immunol. 14(3)(4):1994;239-292.
25. Harvey M.B., Leco K.J., Arcellana-Panlilio M.Y., Zhang X., Edwards D.R., Schultz G.A. Roles of growth factors during peri-implantation development. Mol Hum Reprod. 10(3):1995;712-718.
26. Kojima K., Kanzaki H., Iwai M., Hatayama H., Fujimoto M., Narukawa S., Higuchi T.et al. Expression of leukaemia inhibitory factor (LIF) receptor in human placenta: a possible role for LIF in the growth and differentiation of trophoblasts. Mol Hum Reprod. 10:1995;1907-1911.
27. Charnock-Jones D.S., Sharkey A.M., Fenwick P., Smith S.K. Leukaemia inhibitory factor mRNA concentration peaks in human endometrium at the time of implantation and the blastocyst contains mRNA for the receptor at this time. J Reprod Fertil. 101:1994;421-426.
28. van Eijk M.J.T., Mandelbaum J., Salat-Baroux J., Belaisch-Allart J., Plachot M., Junca A.M., Mummery C.L. Expression of leukaemia inhibitory factor receptor subunits LIFRβ and gp130 in human oocytes and preimplantation embryos. Mol Hum Reprod. 2(5):1996;355-360.
29. Das S.K., Tsukamura H., Paria B.C., Andrews G.K., Dey S.K. 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. 134:1994;971-981.
30. Das S.K., Chakraborty I., Paria B.C., Wang X.-N., Plowman G., Dey S.K. Amphiregulin is an implantation specific and progesterone-regulated gene in the mouse uterus. Mol Endocrinol. 9(6):1995;691-705.
31. Das S.K., Wang X.-N., Paria B.C., Damm D., Abraham J.A., Klagsbrun M., Andrews G.K., Dey S.K. Heparin-binding EGF-like growth factor gene is induced in the mouse uterus temporally by the blastocyst solely at the site of its apposition: a possible ligand for interaction with blastocyst EGF-receptor in implantation. Development. 120:1994;1071-1083.
32. Horowitz G.M., Scott R.T., Drews M.R., Navot D., Hofmann G.E. Immunohistochemical localization of transforming growth factor-α in human endometrium, decidua and trophoblast. J Clin Endocrinol Metab. 76:1993;786-792.
33. Hofmann G.E., Scott R.T., Bergh P.A., Deligdisch L. Immunohistochemical localization of epidermal growth factor in human endometrium, decidua and placenta. J Clin Endocrinol Metab. 73:1991;882-887.
34. Birdsall M.A., Hopkisson J.F., Grant K.E., Barlow D.H., Mardon H.J. Expression of heparin-binding epidermal growth factor messenger RNA in the human endometrium. Mol Hum Reprod. 2(1):1996;31-34.
35. Chegini N., Rossi M.J., Masterson B.J. Platelet-derived growth factor (PDGF), epidermal growth factor (EGF), and EGF and PDGF β-receptors in human endometrial tissue: localization and in vitro action. Endocrinology. 130:1992;2373-2385.
36. Bhatt H., Brunet L.J., Stewart C.L. Uterine expression of leukemia inhibitory factor coincides with the onset of blastocyst implantation. Proc Natl Acad Sci USA. 88:1991;11408-11412.
37. Stewart C.L., Kaspar P., Brunet L.J., Bhatt H., Gadi I., Köntgenn F., Abbondanzo S.J. Blastocyst implantation depends on maternal expression of leukaemia inhibitory factor. Nature. 359:1992;76-79.
38. Chen D.-B., Hisenrath R., Yang Z.-M., Le S.-P., Kim S.-R., Chuong C.J., PoindexterIII A.N.et al. Leukaemia inhibitory factor in human endometrium during the menstrual cycle: cellular origin and action on production of glandular epithelial cell prostaglandin in vitro. Hum Reprod. 10(4):1995;911-918.
39. Klentzeris LD. The role of endometrium in implantation. Hum Reprod 1997;(12 Natl. Suppl. JBFS2) (2):170-75.
40. Starkey PM. The decidua and factors controlling placentation. In: Redman CWG, Sargent IL, Starkey PM, editors. The human placenta. Oxford: Blackwell Scientific Publications, 1993:362-413.
41. Orwig KE, Rasmussen CA, Soares MJ. Decidual signals in the establishment of pregnancy: the prolactin family. In: Foidart JM, Aplin J, Kaufmann P, Schaaps JP, editors. Trophoblast research, vol. 10, early pregnancy. New York: University of Rochester Press, 1997:329-343.
42. Nikas G., Drakakis P., Louatradis D.L., Mara-Skoufari C., Koumantakis E., Michalas S., Psychoyos A. Uterine pinopodes as markers of the "nidation window" in cycling women receiving exogenous oestradiol and progesterone. Hum Reprod. 10:1995;1208-1213.
43. Morris JE, Potter SW. An in vitro model for studying interactions between mouse trophoblast and uterine epithelial cells. A brief review of in vitro systems and observations on cell-surface changes during blastocyst attachment. In: Denker H-W, Aplin JD, editors. Trophoblast research, vol. 4, trophoblast invasion and endometrial receptivity. Novel aspects of the cell biology of embryo and implantation. New York: Plenum Medical Book Corp., 1990:51-69.
44. Lopata A. Blastocyst-endometrial interaction: an appraisal of some old and new ideas. Mol Human Reprod. 2:1996;519-525.
45. Lessey B.A., Damjanovich L., Coutifaris C., Castelbaum A., Albelda S.M., Buck C.A. Integrin adhesion molecules in the human endometrium. Correlation with the normal and abnormal menstrual cycle. J Clin Invest. 90:1992;188-195.
46. Lessey B.A., Castelbaum A.J., Buck C.A., Lei Y., Yowell C.W., Sun J. Further characterization of endometrial integrins during the menstrual cycle and in pregnancy. Fertil Steril. 62:1994;497-506.
47. Denker HW. Trophoblast-endometrial interactions at embryo implantation: a cell biological paradox. In: Denker H-W, Aplin JD, editors. Trophoblast research, vol. 4, trophoblast invasion and endometrial receptivity. Novel aspects of the cell biology of embryo implantation. New York: Plenum Medical Book Corp., 1990:3-29.
48. Bergh P.A., Navot D. The impact of embryonic development and endometrial maturity on the timing of implantation. Fertil Steril. 58(3):1992;537-542.
49. Graham C.H., Lala P.K. Mechanisms of placental invasion of the uterus and their control. Biochem Cell Biol. 70:1992;867-874.
50. Enders, AC. Implantation (embryology). In: Dulbecco R, editor. Encyclopedia of human biology vol. 4. San Diego, CA: Academic Press, 1991:423-430.
51. Kaufmann P, Burton G. Anatomy and genesis of the placenta. In: Knobil E, Neill JD, editors. The physiology of reproduction, 2nd ed. New York: Raven Press, 1994:441-484.
52. Bischof P., Haenggeli L., Campana A. Gelatinase and oncofetal fibronectin secretion is dependent on integrin expression on human cytotrophoblasts. Mol Hum Reprod. 10(3):1995;734-742.
53. Fisher S.J., Cui T., Zhang L., Hartmann L., Grahl K., Guo-Yang Z., Tarpey J., Damsky C.H. Adhesive and degradative properties of human placental cytotrophoblast cells in vitro. J Cell Biol. 109:1989;891-902.
54. Meuris S., Nagy A.M., Delogne-Desnoeck J., Jurkovic D., Jauniaux E. Temporal relationship between the human chorionic gonadotrophin peak and the establishment of intervillous blood flow in early pregnancy. Hum Reprod. 10:1995;947-950.
55. Strickland S., Richards W.G. Invasion of the trophoblasts. Cell. 71:1992;355-357.
56. Lala P.K., Hamilton G.S. Growth factors, proteases and protease inhibitors in the maternal-fetal dialogue. Placenta. 17:1996;545-555.
57. Aplin J.D. Expression of integrin α6β4 in human trophoblast and its loss from extravillous cells. Placenta. 14:1993;203-215.
58. Damsky C.H., Librach C., Lim K.H., Fitzgerald M.L., McMaster M.T., Janatpour M., Zhou Y.et al. Integrin switching regulates normal trophoblast invasion. Development. 120:1994;3657-3666.
59. Zhou Y., Damsky C.H., Chiu K., Roberts J.M., Fisher S.J. Preeclampsia is associated with abnormal expression of adhesion molecules by invasive cytotrophoblasts. J Clin Invest. 91:1993;950-960.
60. Matrisian L.M. The matrix-degrading metalloproteinases. BioEssays. 14(7):1992;455-463.
61. Puistola U., Rönnberg L., Martikainen H., Turpeenniemi-Hujanen T. The human embryo produces basement membrane collagen (type IV collagen)-degrading protease activity. Hum Reprod. 4(3):1989;309-311.
62. Librach C.L., Werb Z., Fitzgerald M.L., Chiu K., Corwin N.M., Esteves R.A., Grobelny D.et al. 92-kD type IV collagenase mediates invasion of human cytotrophoblasts. J Cell Biol. 113:1991;437-449.
63. Bischof P., Martelli M., Campana A., Itoh Y., Ogata Y., Nagase H. Importance of matrix metalloproteinases in human trophoblast invasion. Early Preg Biol Med. 1:1995;263-269.
64. Maquoi E., Polette M., Nawrocki B., Bischof P., Noël A., Pintiaux A., Santavicca M.et al. Expression of stromelysin-3 in the human placenta and placental bed. Placenta. 18:1997;277-285.
65. Queenan J.T., Kao L.-C., Arboleda C.E., Ulloa-Aguirre A., Golos T.G., Cines D.B., Strauss J.F. Regulation of urokinase-type plasminogen activator production by cultured human cytotrophoblasts. J Biol Chem. 262:1987;10903-10906.
66. Cao J., Sato H., Takino T., Seiki M. The C-terminal region of membrane type matrix metalloproteinase is a functional transmembrane domain required for pro-gelatinase A activation. J Biol Chem. 270:1995;801-805.
67. Zini J.M., Murray S.C., Graham C.H., Lala P.K., Kariko K., Barnathan E.S., Mazar A.et al. Characterization of urokinase receptor expression by human placental trophoblasts. Blood. 79:1992;2917-2929.
68. Multhaupt H.A.B., Mazar A., Cines D.B., Warhol M.J., McCrae K.R. Expression of urokinase receptors by human trophoblast. A histochemical and ultra-structural analysis. Lab Invest. 71:1994;392-400.
69. Hofmann G.E., Glatstein I., Schatz F., Heller D., Deligdisch L. Immuno-histochemical localization of urokinase-type plasminogen activator and the plasminogen activator inhibitors 1 and 2 in early human implantation sites. Am J Obstet Gynecol. 170:1994;671-676.
70. Herz J., Clouthier D.E., Hammer R.E. LDL receptor-related protein internalizes and degrades uPA-PAI-1 complexes and is essential for embryo implantation. Cell. 71:1992;411-421.
71. Bass K.E., Morrish D., Roth I., Bhardwaj D., Taylor R., Zhou Y., Fisher S.J. Human cytotrophoblast invasion is up-regulated by epidermal growth factor: evidence that paracrine factors modify this process. Dev Biol. 164:1994;550-561.
72. Morrish D.W., Bhardwaj D., Dabbagh L.K., Marusyk H., Siy O. Epidermal growth factor induces differentiation and secretion of human chorionic gonadotropin and placental lactogen in normal human placenta. J Clin Endocrinol Metab. 65:1987;1282-1290.
73. Han V.K.M., Bassett N., Walton J., Challis J.R.G. The expression of insulin-like growth factor (IGF) and IGF-binding protein (IGFBP) genes in the human placenta and membranes: evidence for IGF-IGFBP interactions at the feto-maternal interface. J Clin Endocrinol Metab. 81:1996;2680-2693.
74. 125 I insulin-like growth factor II on trophoblast membranes of human term placenta. Biol Reprod. 58:1998;37-44.
75. Librach C.L., Feigenbaum S.L., Bass K.E., Cui T.Y., Verastas N., Sadovsky Y., Quigley J.P.et al. Interleukin-1β regulates human cytotrophoblast metallo-proteinase activity and invasion in vitro. J Biol Chem. 269:1994;17125-17131.
76. Cervar M., Kainer F., Desoye G. Endothelin-1 stimulates the invasion of first trimester trophoblast specifically via the B-type receptor, whereas its action on proliferation is mediated by both receptor subtypes. Placenta. 18:1997;A15.
77. Aplin J.D. Implantation, trophoblast differentiation and haemochorial placentation: mechanistic evidence in vivo and in vitro. J Cell Sci. 99:1991;681-692.
78. Higuchi T., Kanzaki H., Nakayama H., Fujimoto M., Hatayama H., Kojima K., Iwai M.et al. Induction of tissue inhibitor of metallo-proteinase 3 gene expression during in vitro decidualization of human endometrial stromal cells. Endocrinology. 136:1996;4973-4981.
79. Yagel S., Geva T.E., Solomon H., Shimonovitz S., Reich R., Finci-Yeheskel Z., Mayer M., Milwidsky A. High levels of human chorionic gonadotropin retard first trimester trophoblast invasion in vitro by decreasing urokinase plasminogen activator and collagenase activities. J Clin Endocrinol Metab. 77(6):1993;1506-1511.
80. De M., Sanford T.R., Wood G.W. Expression of interleukin 1, interleukin 6 and tumour necrosis factor α in mouse uterus during the peri-implantation period of pregnancy. J Reprod Fertil. 97:1993;83-89.
81. Simon C., Piquette G., Frances A., Polan M.L. Localization of interleukin-1 type I receptor and interleukin-1 beta in human endometrium throughout the menstrual cycle. J Clin Endocrinol Metab. 77:1993;549-555.
82. Tabibzadeh S.S., Kaffka K.L., Satyaswaroop P.G., Kilian P.L. Interleukin-1 (IL-1) regulation of human endometrial function: presence of IL-1 receptor correlates with IL-1 stimulated prostaglandin E2 production. J Clin Endocrinol Metab. 70:1990;1000-1006.
83. Tabibzadeh S.S., Sivarajah A., Carpenter D., Ohlsson-Wilhelm M., Satyaswaroop P.G. Modulation of HLA-DR expression in epithelial cells by interleukin-1 and estradiol-17β J Clin Endocrinol Metab. 71:1990;740-747.
84. Tabibzadeh S.S., Santhanam U., Sehgal P.B., May L.T. Cytokine-induced production of interferon β2/interleukin-6 by freshly explanted human endometrial stromal cells. Modulation by estradiol-17β J Immunol. 142:1989;3134-3139.
85. Rawdanowicz T.J., Hampton A.L., Nagase H., Woolley D.E., Salamonsen L.A. Matrix metalloproteinase production by cultured human endometrial stromal cells: identification of interstitial collagenase, gelatinase-A, gelatinase-B and stromelysin-1 and their differential regulation by interleukin-1α and tumor necrosis factor-α J Clin Endocrinol Metab. 79:1994;530-536.
86. Rouas-Freiss N., Marchal-Bras Gonçalvess R., Menier C., Dausset J., Carosella E.D. Direct evidence to support the role of HLA-G in protecting the fetus from maternal uterine natural killer cytolysis. Proc Natl Acad Sci USA. 94:1997;11520-11521.
87. H 2 phenomenon? Immunol Today. 14:1993;353-356.
88. Daiter E., Pampfer S., Yeung Y.G., Barad D., Stanley E.R., Pollard J.W. Expression of colony-stimulating factor-1 in the human uterus and placenta. J Clin Endocrinol Metab. 74:1992;850-858.
89. Jokhi P.P., King A., Boocock C., Loke Y.W. Secretion of colony stimulating factor-1 by human first trimester placental and decidual cell populations and the effect of this cytokine on trophoblast thymidine uptake in vitro. Hum Reprod. 10:1995;2800-2807.
90. Jokhi P.P., King A., Loke Y.W. Production of granulocyte-macrophage colony-stimulating factor by human trophoblast cells and by decidual large granular lymphocytes. Hum Reprod. 9:1994;1660-1669.
91. Lin H., Mosmann T.R., Guilbert L., Tuntipopipat S., Wegmann T.G. Synthesis of T helper 2-type cytokines at the maternal-fetal interface. J Immunol. 151:1993;4562-4573.
92. Hill J.A., Polgar K., Anderson D.J. T-helper 1-type immunity to trophoblast in women with recurrent spontaneous abortion. JAMA. 273:1995;1933-1936.
93. Masuhiro K., Matsuzaki N., Nishino E., Taniguchi T., Kameda T., Li Y., Saji F., Tanizawa O. Trophoblast-derived interleukin-1 (IL-1) stimulates the release of human chorionic gonadotropin by activating IL-6 and IL-6-receptor system in first trimester human trophoblasts. J Clin Endocrinol Metab. 72:1991;594-601.
94. Sawai K., Matsuzaki N., Kameda T., Hashimoto K., Okada T., Shimoya K., Nobunaga T.et al. Leukemia inhibitory factor produced at the feto-maternal interface stimulates chorionic gonadotropin production: its possible implication during pregnancy, including implantation period. J Clin Endocrinol Metab. 80(4):1995;1449-1456.
95. Iles R.K., Chard T. Enhancement of ectopic β-human chorionic gonadotrophin expression by interferon-α J Endocrinol. 123:1989;501-507.
96. Lefevre F., Martinat-Botte F., Guillomot M., Zouari K., Charley B., La Bonnardière C. Interferon-gamma gene and protein are spontaneously expressed by the trophectoderm early in gestation. Eur J Immunol. 20:1990;2485-2490.
97. Lefevre F, Boulay V, La Bonnardière C. A new type one interferon with unusual regulatory elements. J IFN Res 1991;11(Suppl. 1):Abstr. 14.
98. Zouari K, Bezard J, Reinaud P, Guillomot M, Palmer E, Martal J. Evidence for the presence of equine trophoblastic interferons during early pregnancy. J IFN Res 1991;11(Suppl. 1):Abstr. S134.
99. Lennard S.N., Stewart F., Allen W.R. Transforming growth factor beta(1) expression in the endometrium of the mare during placentation. Mol Reprod Dev. 42:1995;131-140.
100. Wooding F.B.P. Current topic: the synepitheliochorial placenta of ruminants: binucleate cell fusions and hormone production. Placenta. 13:1992;101-113.
101. Guillomot M., Michel C., Gaye P., Charlier M., Trojan J., Martal J. Cellular localization of an embryonic interferon, ovine trophoblastin and its mRNA in sheep embryos during early pregnancy. Biol Cell. 68:1990;205-211.
102. Harbison LA, Tamura K, Khan S, Christenson RK, Imakawa K. Conceptus production of immuno- and bioactive transforming growth factor β (TGFβ) during peri-implantation period. Society for the Study of Reproduction, 28th Annual Meeting, 1995:Abstr.
103. Salamonsen L.A., Nagase H., Woolley D.E. Matrix metalloproteinases and their tissue inhibitors at the ovine trophoblast-uterine interface. J Reprod Fertil. 49(Suppl.):1995;29-37.
104. Gunn L.K., Homa S.T., Searle M.J., Chard T. Lack of evidence for the production in interferon-α-like species by the cultured human pre-embryo. Hum Reprod. 9:1994;1522-1527.
105. Duc-Goiran P., Robert B., Navarro S., Civas A., Cerutti I., Rudant C., Maury M.et al. Developmental control of IFN-α expression in murine embryos. Exp Cell Res. 214:1994;570-583.
106. Duc-Goiran P., Chany C., Doly J. Unusually large interferon-α like mRNAs and high expression of interleukin-6 in human fetal annexes. J Biol Chem. 264:1989;16507-16511.
107. Charlier M., Hue D., Boisnard M., Martal J., Gaye P. Cloning and structural analysis of two distinct families of ovine interferon-α genes encoding functional class II and trophoblast (oTP) α-interferons. Mol Cell Endocrinol. 76:1991;161-171.
108. Whaley A.E., Reddy Meka C.S., Harbison L.A., Hunt J.S., Imakawa K. Identification and cellular localization of unique interferon mRNA from human placenta. J Biol Chem. 269(8):1994;10864-10868.
109. Müller U., Steinhoff U., Reis L.F.L., Hemmi S., Pavlovic J., Zinkernagel R.M., Aguet M. Functional role of type I and type II interferons in antiviral defense. Science. 264:1994;1918-1921.