Human chorionic gonadotropin and growth factors at the embryonic-endometrial interface control leukemia inhibitory factor (LIF) and interleukin 6 (IL-6) secretion by human endometrial epithelium
PERRIER d'HAUTERIVE, Sophie; Charlet-Renard, Jeanne de Chantal; Berndt, Sarahet al.
2004 • In Human Reproduction, 19 (11), p. 2633-2643
[en] BACKGROUND: The elucidation of the molecular mechanisms by which the embryo contributes to its implantation is an area of extensive research. The main objective of this study was to investigate the pattern of leukemia inhibitory factor (LIF) and interleukin-6 (IL-6) secretion by human endometrial epithelium, and their regulation by human chorionic gonadotropin (hCG) and other growth factors present at the embryonic-endometrial interface. METHODS: Endometrial epithelial cells (EEC) were isolated from biopsies collected at both proliferative and secretory phases of fertile women. RESULTS: HCG (1-50 IU/ml) increased LIF secretion by EEC cultures derived from follicular phase (up to 285+/-75%) or from secretory phase (up to 212+/-16%). In contrast, hCG reduced IL-6 secretion by EEC in both phases. The hCG/LH receptor gene was transcribed by EEC as evidenced by RT-PCR. Insulin-like growth factors 1 and 2 increased LIF secretion by EEC. Transforming growth factor beta1 stimulated LIF and reduced IL-6 secretion. CONCLUSIONS: Through hCG, the blastocyst may be involved in the control of its implantation (via an increase of proimplantatory LIF) and tolerance (via an inhibition of proinflammatory IL-6). Other growth factors present at the embryonic-endometrial interface are also involved in the control of LIF and IL-6 endometrial secretion.
Disciplines :
Reproductive medicine (gynecology, andrology, obstetrics)
Noël, Agnès ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie cellulaire et moléculaire appliquée à l'homme
Hazout
Foidart, Jean-Michel ; Université de Liège - ULiège > Département des sciences cliniques > Gynécologie - Obstétrique
Geenen, Vincent ; Université de Liège - ULiège > Centre d'immunologie
Language :
English
Title :
Human chorionic gonadotropin and growth factors at the embryonic-endometrial interface control leukemia inhibitory factor (LIF) and interleukin 6 (IL-6) secretion by human endometrial epithelium
Arici, A., Engin, O., Attar, E., Olive, D.L., Modulation of leukemia inhibitory factor gene expression and protein biosynthesis in human endometrium (1995) J. Clin. Endocrinol. Metab., 80, pp. 1908-1915
Bhattacharya, S., Banerjee, J., Sen, S., Manna, P.R., Human chorionic gonadotropin binding sites in the human endometrium (1993) Acta Endocrinol., 129, pp. 15-19
Bonnamy, P.J., Benhaim, A., Leymarie, P., Estrous cycle-related changes of high affinity luteinizing hormone/human chorionic gonadotropin binding sites in the rat uterus (1990) Endocrinol., 126, pp. 1264-1269
Bonnamy, P.J., Benhaim, A., Leymarie, P., Uterine luteinizing hormone/human chorionic gonadotropin-binding sites in the early pregnant rat uterus: Evidence for total occupancy in the periimplantation period (1993) Endocrinol., 132, pp. 1240-1246
Casslén, B., Sandberg, T., Gustavsson, B., Willén, R., Nilbert, M., Transforming growth factor beta1 in the human endometrium. Cyclic variation, increased expression by estradiol and progesterone, and regulation of plasminogen activators and plasminogen activator inhibitor-1 (1998) Biol. Reprod., 58, pp. 1343-1350
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 (1994) J. Reprod. Fertil., 101, pp. 421-426
Clark, D.A., Flanders, K.C., Hirte, H., Dasch, J.R., Coker, R., McAnulty, R.J., Laurent, G.J., Characterization of murine pregnancy decidua transforming growth factor beta. Transforming growth factor beta 2-like molecules of unusual molecular size released in bioactive form (1995) Biol. Reprod., 52, pp. 1380-1388
Cone, J.L., Brown, D.R., DeLarco, J.E., An improved method of purification of transforming growth factor, type beta from platelets (1988) Anal. Biochem., 168, pp. 71-74
Cork, B.A., Li, T.C., Warren, M.A., Laird, S.M., Interleukin-11 (IL-11) in human endometrium: Expression throughout the menstrual cycle and the effects of cytokines on endometrial IL-11 production in vitro (2001) J. Reprod. Immunol., 50, pp. 3-17
Cullinan, E.B., Abbondanzo, S.J., Anderson, P.S., Pollard, J.W., Lessey, B.A., Stewart, C.L., Leukemia inhibitory factor (LIF) and LIF receptor expression in human endometrium suggests a potential autocrine/paracrine function in regulating embryo implantation (1996) Proc. Natl. Acad. Sci. USA, 93, pp. 3115-3120
De Groote, D., Zangerle, P.F., Gevaert, Y., Direct stimulation of cytokines (IL-1 beta, TNF-alpha, IL-6, IL-2, IFN-gamma and GM-CSF) in whole blood. Comparison with isolated PBMC stimulation (1992) Cytokine, 4, pp. 239-248
Delage, G., Moreau, J.F., Taupin, J.L., In-vitro endometrial secretion of human interleukin for DA cells/leukaemia inhibitory factor by explant cultures from fertile and infertile women (1995) Hum. Reprod., 10, pp. 2483-2488
Delage, G., Moreau, J.F., Taupin, J.L., Hambartsoumian, E., Frydman, R., Tartzkovsky, B., Chaouat, G., In vitro modulation of the production of the cytokine HILDA/LIF, secreted by human endometrial explants: Preliminary results (1995) Contracept. Fertil. Sex., 23, pp. 622-625
Derecka, K., Pietila, E.M., Rajaniemi, H.J., Ziecik, A.J., Cycle dependent LH/hCG receptor gene expression in porcine nongonadal reproductive tissues (1995) J. Physiol. Pharmacol., 46, pp. 77-85
Doherty, A.S., Temeles, G.L., Schultz, R.M., Temporal pattern of IGF-I expression during mouse preimplantation embryogenesis (1994) Mol. Reprod. Dev., 37, pp. 21-26
Dokras, A., Sargent, I.L., Ross, C., Gardner, R.L., Barlow, D.H., The human blastocyst: Morphology and human chorionic gonadotrophin secretion in vitro (1991) Hum. Reprod., 6, pp. 1143-1151
Ernst, M., Jenkins, B.J., Acquiring signalling specificity from the cytokine receptor gp130 (2004) Trends Genet., 20, pp. 23-32
Fazleabas, A.T., Donnelly, K.M., Srinivasan, S., Fortman, J.D., Miller, J.B., Modulation of the baboon (Papio anubis) uterine endometrium by chorionic gonadotrophin during the period of uterine receptivity (1999) Proc. Natl. Acad. Sci. USA, 96, pp. 2543-2548
Giudice, L.C., Potential biochemical markers of uterine receptivity (1999) Hum. Reprod., 14 (SUPPL. 2), pp. 3-16
Godkin, J.D., Doré, J.J., Transforming growth factor beta and the endometrium (1998) Rev. Reprod., 3, pp. 1-6
Han, S.W., Lei, Z.M., Rao, C.V., Treatment of human endometrial stromal cells with chorionic gonadotropin promotes their morphological and functional differentiation into decidua (1999) Mol. Cell. Endocrinol., 147, pp. 7-16
Han, V.K., Carter, A.M., Spatial and temporal patterns of expression of messenger RNA for insulin-like growth factors and their binding proteins in the placenta of man and laboratory animals (2000) Placenta, 21, pp. 289-305
Irwin, J.C., Suen, L.F., Martina, N.A., Mark, S.P., Giudice, L., Role of the IGF system in trophoblast invasion and pre-eclampsia (1999) Hum. Reprod., 14 (SUPPL. 2), pp. 90-96
Jensen, J.D., Odell, W.D., Identification of LH/hCG receptors in rabbit uterus (1988) Proc. Soc. Exp. Biol. Med., 189, pp. 28-30
Jurisicova, A., Antenos, M., Kapasi, K., Meriano, J., Casper, R.F., Variability in the expression of trophectodermal markers beta-human chorionic gonadotrophin, human leukocyte antigen-G and pregnancy specific beta-1 glycoprotein by the human blastocyst (1999) Hum. Reprod., 14, pp. 1852-1858
Kauma, S., Matt, D., Strom, S., Eierman, D., Turner, T., Interleukin-1 beta, human leukocyte antigen HLA-DR alpha, and transforming growth factor-beta expression in endometrium, placenta, and placental membranes (1990) Am. J. Obstet. Gynecol., 163, pp. 1430-1437
Kayisli, U.A., Selam, B., Guzeloglu-Kayisli, O., Demir, R., Arici, A., Human chorionic gonadotropin contributes to maternal immunotolerance and endometrial apoptosis by regulating Fas-Fas ligand system (2003) J. Immunol., 171, pp. 2305-2313
Khan, N.A., Khan, A., Savelkoul, H.F., Benner, R., Inhibition of diabetes in NOD mice by human pregnancy factor (2001) Hum. Immunol., 62, pp. 1315-1323
Kopf, M., Baumann, H., Freer, G., Freudenberg, M., Lamers, M., Kishimoto, T., Zinkernagel, R., Köhler, G., Impaired immune and acute-phase responses in interleukin-6-deficient mice (1994) Nature, 368, pp. 339-342
Laird, S.M., Li, T.C., Bolton, A.E., The production of placental protein 14 and interleukin 6 by human endometrial cells in culture (1993) Hum. Reprod., 8, pp. 793-798
Laird, S.M., Tuckerman, E., Li, T.C., Bolton, A.E., Stimulation of human endometrial epithelial cell interleukin 6 production by interleukin 1 and placental protein 14 (1994) Hum. Reprod., 9, pp. 1339-1343
Laird, S.M., Tuckerman, E.M., Dalton, C.F., Dunphy, B.C., Li, T.C., Zhang, X., The production of leukaemia-inhibitory factor by human endometrium: Presence in uterine flushings and production by cells in culture (1997) Hum. Reprod., 12, pp. 569-574
Ledee-Bataille, N., Lapree-Delage, G., Taupin, J.L., Dubanchet, S., Frydman, R., Chaouat, G., Concentration of leukaemia inhibitory factor (LIF) in uterine flushing fluid is highly predictive of embryo implantation (2002) Hum. Reprod., 17, pp. 213-218
Li, Y., Matsuzaki, N., Masuhiro, K., Kameda, T., Taniguchi, T., Saji, F., Yone, K., Tanizawa, O., Trophoblast-derived tumor necrosis factor-alpha induces release of human chorionic gonadotropin using interleukin-6 (IL-6) and IL-6-receptor-dependent system in the normal human trophoblasts (1992) J. Clin. Endocrinol. Metab., 74, pp. 184-191
Licht, P., Russu, V., Wildt, L., On the role of human chorionic gonadotropin (hCG) in the embryo-endometrial microenvironment: Implications for differentiation and implantation (2001) Semin. Reprod. Med., 19, pp. 37-47
Licht, P., von Wolff, M., Berkholz, A., Wildt, L., Evidence for cycle-dependent expression of full-length human chorionic gonadotropin/luteinizing hormone receptor mRNA in human endometrium and decidua (2003) Fertil. Steril., 79 (SUPPL. 1), pp. 718-723
Lopata, A., Oliva, K., Stanton, P.G., Robertson, D.M., Analysis of chorionic gonadotrophin secreted by cultured human blastocysts (1997) Mol. Hum. Reprod., 3, pp. 517-521
Martens, H., Malgrange, B., Robert, F., Cytokine production by human thymic epithelial cells: Control by the immune recognition of the neurohypophysial self-antigen (1996) Regul. Pept., 67, pp. 39-45
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 (1991) J. Clin. Endocrinol. Metab., 72, pp. 594-601
Merali, F.S., Arck, P.C., Beaman, K., Clark, D.A., Transforming growth factor-beta 2-related-decidual suppressor factor is not related to TJ6 protein (1996) Am. J. Reprod. Immunol., 35, pp. 342-347
Nakayama, T., Fujiwara, H., Maeda, M., Inoue, T., Yoshioka, S., Mori, T., Fujii, S., Human peripheral blood mononuclear cells (PBMC) in early pregnancy promote embryo invasion in vitro: HCG enhances the effects of PBMC (2002) Hum. Reprod., 17, pp. 207-212
Nayak, N.R., Giudice, L.C., Comparative biology of the IGF system in endometrium, decidua, and placenta, and clinical implications for foetal growth and implantation disorders (2003) Placenta, 24, pp. 281-296
Nishino, E., Matsuzaki, N., Masuhiro, K., Kameda, T., Taniguchi, T., Takagi, T., Saji, F., Tanizawa, O., Trophoblast-derived interleukin-6 (IL-6) regulates human chorionic gonadotropin release through IL-6 receptor on human trophoblasts (1990) J. Clin. Endocrinol. Metab., 71, pp. 436-441
Noyes, R.W., Hertig, A.I., Rock, I., Dating the endometrial biopsy (1950) Fertil. Steril., 1, pp. 3-25
Rao, C.V., An overview of the past, present, and future of nongonadal LH/hCG actions in reproductive biology and medicine (2001) Semin. Reprod. Med., 19, pp. 7-17
Rao, C.V., LH receptors: Follicle and endometrium (2002) J. Gynecol. Obstet. Biol. Reprod., 31, pp. 1S7-1S11
Reshef, E., Lei, Z.M., Rao, C.V., Pridham, D.D., Chegini, N., Luborsky, J.L., The presence of gonadotropin receptors in nonpregnant human uterus, human placenta, fetal membranes, and decidua (1990) J. Clin. Endocrinol. Metab., 70, pp. 421-430
Robert, F., Geenen, V., Schoenen, J., Burgeon, E., De Groote, D., Defresne, M.P., Legros, J.J., Franchimont, P., Colocalization of immunoreactive oxytocin, vasopressin and interleukin-1 in human thymic epithelial neuroendocrine cells (1991) Brain Behav. Immun., 5, pp. 102-115
Robertson, S.A., Mayrhofer, G., Seamark, R.F., Uterine epithelial cells synthesize granulocyte-macrophage colony-stimulating factor and interleukin-6 in pregnant and nonpregnant mice (1992) Biol. Reprod., 46, pp. 1069-1079
Rutanen, E.M., Insulin-like growth factors in endometrial function (1998) Gynecol. Endocrinol., 12, pp. 399-406
Salamonsen, L.A., Dimitriadis, E., Robb, L., Cytokines in implantation (2000) Semin. Reprod. Med., 18, pp. 299-310
Sawai, K., Matsuzaki, N., Kameda, T., Leukemia inhibitory factor produced at the fetomaternal interface stimulates chorionic gonadotropin production: Its possible implication during pregnancy, including implantation period (1995) J. Clin. Endocrinol. Metab., 80, pp. 1449-1456
Sharkey, A.M., Dellow, K., Blayney, M., Macnamee, M., Charnock-Jones, S., Smith, S.K., Stage-specific expression of cytokine and receptor messenger ribonucleic acids in human preimplantation embryos (1995) Biol. Reprod., 53, pp. 974-981
Stewart, C.L., Kaspar, P., Brunet, L.J., Bhatt, H., Gadi, I., Köntgen, F., Abbondanzo, S.J., Blastocyst implantation depends on maternal expression of leukaemia inhibitory factor (1992) Nature, 359, pp. 76-79. , [see comments]
Stewart, E.A., Gonadotropins and the uterus: Is there a gonad-independent pathway? (2001) J. Soc. Gynecol. Investig., 8, pp. 319-326
Stewart, E.A., Sahakian, M., Rhoades, A., Van Voorhis, B.J., Nowak, R.A., Messenger ribonucleic acid for the gonadal luteinizing hormone/human chorionic gonadotropin receptor is not present in human endometrium (1999) Fertil. Steril., 71, pp. 368-372
Tabibzadeh, S., Kong, Q.F., Babaknia, A., May, L.T., Progressive rise in the expression of interleukin-6 in human endometrium during menstrual cycle is initiated during the implantation window (1995) Hum. Reprod., 10, pp. 2793-2799
Tabibzadeh, S., Lessey, B., Satyaswaroop, P.G., Temporal and site-specific expression of transforming growth factor-beta4 in human endometrium (1998) Mol. Hum. Reprod., 4, pp. 595-602
Uzumcu, M., Coskun, S., Jaroudi, K., Hollanders, J.M., Effect of human chorionic gonadotropin on cytokine production from human endometrial cells in vitro (1998) Am. J. Reprod. Immunol., 40, pp. 83-88
Vandermolen, D.T., Gu, Y., Human endometrial interleukin-6 (IL-6): In vivo messenger ribonucleic acid expression, in vitro protein production, and stimulation thereof by IL-1 beta (1996) Fertil. Steril., 66, pp. 741-747
Zhang, M., Shi, H., Segaloff, D.L., Van Voorhis, B.J., Zheng, M., Expression and localization of luteinizing hormone receptor in the female mouse reproductive tract (2001) Biol. Reprod., 64, pp. 179-187
Zhou, X.L., Lei, Z.M., Rao, C.V., Treatment of human endometrial gland epithelial cells with chorionic gonadotropin/luteinizing hormone increases the expression of the cyclooxygenase-2 gene (1999) J. Clin. Endocrinol. Metab., 84, pp. 3364-3377
Ziecik, A.J., Stanchev, P.D., Tilton, J.E., Evidence for the presence of luteinizing hormone/human chorionic gonadotropin-binding sites in the porcine uterus (1986) Endocrinol., 119, pp. 1159-1163
