Molecular Human Reproduction, Vol. 7, No. 4, 365-371,
April 2001
© 2001 European Society of Human Reproduction and Embryology
Immunohistochemical localization of insulin-like growth factors I and II at the primary implantation site in the Rhesus monkey
1 Department of Physiology, All India Institute of Medical Sciences, New Delhi 110029, India
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There are various cellular mediators which can affect the process of blastocyst implantation by regulating the proliferation and differentiation of conceptus and maternal endometrial cells. Insulin-like growth factors I (IGF-I) and II (IGF-II) are potent mitogenic and differentiation-promoting growth factors. However, the role of IGF peptides at implantation in primate species is not well understood. The objective of the present study was to immunohistochemically localize IGF-I and IGF-II peptides in trophoblast cells and maternal endometrial cells during lacunar and villous stages of placentation in the Rhesus monkey. Female animals (n = 10) were laparotomized on estimated days 13-16 after fertilization to collect primary implantation sites which were subjected to immunohistochemical staining for IGF-I and IGF-II peptides. Cell-type specificity for IGF-I and IGF-II was evident with a very low level of IGF-I peptide immunolocalized in trophoblast cells lining lacunae, and primary and secondary villi, while moderate to high amounts of IGF-II peptide were detected in lamellar syncytiotrophoblast cells lining lacunae, early villi and cell columns, as well as in migrating trophoblast cells in the extravillous compartment and in endovascular trophoblast cells. The observed presence of IGF-II peptide in differentiated lamellar syncytiotrophoblast cells during the very early stages of implantation and placentation in the Rhesus monkey may be important in their transition to this differentiated cell population. Maternal endometrial cells showed similar distribution profiles for IGF-I and IGF-II. In conclusion, we report differential distribution of IGF-I and IGF-II peptides in trophoblast cell populations at the feto-maternal interface during lacunar and villous stages of gestation in the Rhesus monkey.
cytotrophoblast/endometrium/implantation/insulin-like growth factors/syncytiotrophoblast
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Introduction |
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The cellular events at implantation and placentation in primate species have been studied using the macaque and the baboon (Hendrickx, 1971
; Enders and Schlafke, 1986). A study of the early stages of implantation revealed that penetration of uterine epithelium by syncytial trophoblast cells occurs on day 9.5 of gestation followed by marked proliferation of cytotrophoblast cells which form the trophoblast plate (Enders et al., 1985). Endothelial basal lamina are penetrated by cytoplasmic processes arising from syncytial trophoblast cells, and at this time syncytial clefts and lacunae lined by polarized lamellar syncytiotrophblast cells also begin to develop (Enders and King, 1991). By day 12 of gestation, lacunae undergo further development and become filled with maternal blood as syncytio- and cytotrophoblast cells penetrate maternal blood vessels. The responses of maternal endometrium during trophoblast penetration is characterized by marked oedema in the upper functionalis and transformation of epithelial cells at neck of glands to form nests of plaque acini. Stromal cell decidualization along with an influx of endometrial granulated lymphocytes then begins by day 14 of gestation as plaque acini begin to degenerate (Enders et al., 1985).
The dynamic process of trophoblast invasion into maternal endometrium and vasculature is associated with extensive cell–cell and cell-matrix interactions involving various adhesion molecules and matrix metalloproteinases (Librach et al., 1991; Blankenship et al., 1993a, b; Enders and Blankenship, 1997). However, the cellular mediators which can affect the process of blastocyst implantation during the early stages of gestation remain largely unknown. Immunohistochemical analyses of receptors for oestradiol-17ß (ER) and progesterone (PR) at fetal-maternal interface in timed pre-villous and villous stages of implantation of Rhesus monkey revealed the presence of PR in syncytio- and cytotrophoblast cells, while these cells were generally ER negative. These analyses also showed that maternal endometrial cells exhibited heterogeneous staining patterns for ER and PR, and this correlated well with endometrial hyperplasia, differentiation and stromal-decidual transformation (Ghosh et al., 1999).
Insulin-like growth factor I (IGF-I) and IGF-II are potent mitogenic and differentiation-promoting growth factors (Clemens, 1991). There is robust evidence to support the importance of IGF in the regulation of fetal growth and development in mice (Baker et al., 1993; Liu et al., 1993). IGF are involved in the growth and differentiation of trophoblast cells both in vitro (Fant et al., 1986; Ritvos et al., 1988) and in vivo (Guidice et al., 1995; Coulter and Han, 1996). In a study of human placental tissue recovered between 6 and 8 weeks of gestation, IGF-II was shown to be abundantly expressed by invading cytotrophoblast cells (Han et al., 1996). IGF-II has also been shown to stimulate human trophoblast migration in vitro (Irving and Lala, 1995). However, none of these studies investigated the involvement of IGF peptides at implantation sites during early stages of implantation and placentation in a primate species. The objective of the present study was to immunohistochemically localize IGF-I and IGF-II peptides in trophoblast cells and in maternal endometrial cells during lacunar and early villous stages of placentation in the Rhesus monkey.
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Animals
Proven fertile male and female Rhesus monkeys were housed singly under semi-natural conditions in the Primate Research Facility of the All India Institute of Medical Sciences, and were fed with a regular monkey pellet diet, semi-formulated Indian bread, fresh seasonal fruits and water ad libitum. Females were allowed to cohabit with their male partners during days 8-16 of their menstrual cycles and during this time peripheral blood samples were collected once daily from female monkeys for the determination of oestradiol-17ß and progesterone in peripheral circulation by radioimmunoassays in order to detect the day of ovulation (day 0) and for the determination of chorionic gonadotrophin (mCG) levels in peripheral circulation by enzyme-linked immunosorbent assay in order to detect the day of implantation as described previously (Ghosh et al., 1996
, 1997). Vaginal smears were checked daily for the presence of spermatozoa. The experimental design of the present study was approved by the Ethics Committee on the Use of Non-Human Primates in Biomedical Research of the AIIMS.
Tissue collection, processing and analysis of implantation sites
Prediction of pregnancy was made on the basis of elevated profiles of oestradiol-17ß and progesterone and detectable mCG in peripheral circulation (Ghosh et al., 1997). On estimated days 13-16 after fertilization, animals (n = 10) were laparotomized under ketamine (12 mg/kg body weight; Parke Davis & Co., Mumbai, India) anaesthesia and after checking for the presence of functional corpus luteum, in-situ perfusion was performed using sterile phosphate-buffered saline (pH 7.4) followed by freshly prepared 4% formaldehyde in 0.1 mol/l phosphate buffer, pH 7.4. In-situ perfusion was performed for 45-60 min, and the uterus was quickly excised, placed in fresh fixative on ice and transported to the laboratory. In the laboratory, the uterus was carefully excised to expose its luminal side, the primary implant site was located and carefully excised and kept for fixation for 24 h at 4°C and then processed in a routine manner for paraffin embedding (Ghosh et al., 1999).
Based on light microscopic examination of 6 µm haematoxylin-stained paraffin wax sections of primary implantation sites, the implantation stage for each sample was classified based on earlier descriptions (Hendrickx, 1971; Enders, 1993). In the present study, lacunar (n = 4) and early villous (n = 6) stages of primary implantation sites were used. Detailed descriptions of these stages of implantation and placentation in the Rhesus monkey have been given in an earlier report (Ghosh et al., 1999).
Immunohistochemistry and analysis of immunoprecipitation
Paraffin sections (6 µm) were collected on poly-L-lysine pre-coated glass slides, and immunohistochemical localizations of IGF-I and IGF-II were performed using polyclonal antisera raised in goat against recombinant human (rh)IGF-I and rhIGF-II (R & D Systems, Minneapolis, MN, USA) using a method described earlier (Ghosh et al., 1999). To help in identifying fetal and maternal endometrial cells at the feto-maternal interface of primary implantation sites, parallel sections were used for the immunolocalization of cytokeratin and vimentin using specific monoclonal antibodies (Dako-CK MNF116 and Dako-vimentin V9, respectively) from Dako A/S (Glostrup, Denmark). All other chemicals were purchased from Sigma Chemical Company (St Louis, MO, USA). Sections were incubated with primary antibody overnight at 4°C, followed by incubation with biotinylated secondary antibody. Final visualization was achieved using the ABC peroxidase kit (Vector Laboratories, Burlingame, CA, USA) and freshly prepared 3,3'-diaminobenzidine tetrahydrochloride and hydrogen peroxide according to the protocol provided by the manufacturer. Sections were then counterstained lightly with haematoxylin.
Dilutions of stock primary antibodies for incubation were pre-calibrated based on 3–5 point titration and the information provided by the manufacturer. Specificity of antibody ligand binding and visualization were assessed by: (i) omitting primary antibodies, (ii) replacing primary antibodies with unrelated immunoglobulin from the same species and other species, and (iii) omitting secondary antibodies and replacing labelled secondary antibody with unrelated labelled immunoglobulin from the same and other species. Specificities of the antibodies against IGF-I and IGF-II were further examined using immunobloting and immunoneutralization on adjacent tissue sections. For a given antibody and dilution, all sections were subjected to immunohistochemistry simultaneously. Late proliferative and mid luteal phase human endometrial tissue sections were used as positive controls.
For the assessment of immunostaining in cells of fetal and endometrial compartments, semiquantitative subjective scoring was done by all three investigators separately using a standardized 5-scale system: 0 (<5%), 1 (5–25%), 2 (26–50%), 3 (51–75%), 4 (76% and more), as described previously (Press et al., 1988; Ghosh et al., 1999). The immunostained sections which yielded coefficient of variance more than 10% in the pooled data analysis were not included. It was assumed that these measurements reflected the concentrations of the investigated proteins in fetal and maternal cells at blastocyst implantation sites.
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Figure 1A-F
shows representative lacunar and early villous stages of implantation and placentation of the Rhesus monkey. Light microscopic examination of primary implantation sites revealed the presence of lacunae lined with syncytial trophoblast cells and overlying the chorionic plate on day 13 of gestation. Between days 14 and 16 of gestation, expansion of lacunae was observed followed by the formation of primary and secondary villi along with marked expansion of the implantation area. Endometrial responses to invading trophoblast included development of subepithelial oedema and formation of epithelial plaque acini adjacent to the implanting nidus. Throughout this period, venular dilatation and penetration of the vascular compartment by cytotrophoblast cells were remarkable features at the site of implantation.
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As shown in Figures 1A-C
, all populations of trophoblast cells including migrating trophoblast cells within endometrial stroma and glands and endovascular cytotrophoblast cells within dilated blood vessels were immunopositive for cytokeratin. Endometrial glandular epithelium and plaque acinar epithelium were also cytokeratin-positive. Vimentin-positive maternal endometrial stromal cells were observed surrounding dilated blood vessels and glands at implantation sites. Extraembryonic mesenchymal cells were also vimentin positive (Figures 1D-F), and they were also occasionally stained positive for cytokeratin.
Figures 2–5 show immunolocalization of IGF-I and IGF-II in different cell types at the fetal-maternal interface and in cells of the endometrial-myometrial compartment at lacunar and early villous stages of implantation collected on days 13-16 of gestation. Table I provides the corresponding scores for immunopositive IGF-I and IGF-II peptides in cells of fetal and endometrial compartments. At the lacunar stage, immunopositive IGF-I peptide was only occasionally detected in trophoblast cells associated with lacunae and in adjoining maternal interstitium (Figure 2A; Table I), while IGF-II immunostaining was predominant in lamellar syncytiotrophoblast cells lining the syncytial cleft and lacunae (Figure 2B; Table I). Trophoblast cells within the chorionic plate exhibited a lower level of immunostaining, while cells beneath and adjacent to lacunae remained largely negative for IGF-II (Figure 2B). The villous trophoblast cells showed very low to no immunostaining for IGF-I (Table I), while discrete IGF-II peptide was seen in villous syncytiotrophoblast cells (Figure 3). Although there was only occasional staining for IGF-I and IGF-II in non-polarized trophoblast cells of the cell columns, marked immunostaining for IGF-II was observed in syncytiotrophoblasts lining the cell column, in migrating extravillous trophoblast cells (Figure 4) and in endovascular trophoblast cells (Figure 5). Figure 6 shows the absence of immunopositive staining in fetal and maternal endometrial cells in the absence of primary antibodies. In the maternal compartment, a low to moderate level of immunostaining for both IGF-I and IGF-II was seen in plaque epithelial cells, glandular epithelial cells, vascular smooth muscle cells and myometrium in lacunar and villous stages of implantation (Table I; Figure 7A-D).
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Finally, it is not possible to directly compare the relative abundance of two antigens, namely IGF-I and IGF-II, in different subsets of trophoblast cells and maternal endometrial cells at the primary implantation site based on semiquantitative immunohistochemical scoring. It is however noteworthy that the antibodies (1.0 µg/ml) used in the present study were of high sensitivity, with the detection limit being 2.5 ng/lane for IGF-I and 1.0 ng/lane for IGF-II, respectively. As shown in Figure 8
, these antibodies did not show any mutual cross-reactivity.
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Discussion |
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The observed light microscopic changes during lacuna and early villous stages of implantation and placentation at primary implantation stages in the Rhesus monkey were very similar to those reported earlier in the same species (Wislocki and Streeter, 1938
; Heuser and Streeter, 1941; Enders et al., 1985; Enders and Schlafke, 1986; Enders, 1993). All cytotrophoblast and syncytiotrophoblast cell populations were cytokeratin-positive, though no effort was made to differentiate different subsets of trophoblast cells based on their patterns of cytokeratin expression as has been reported earlier for human trophoblast cell populations (Muhlhauser et al., 1995; Vicovac and Aplin, 1996).
It is generally known that IGF-I and IGF-II are potent mitogenic and differentiation-promoting growth factors and appear to act via paracrine and autocrine as well as classical endocrine mechanisms (Rotwein, 1991). We now report for the first time that IGF-I and IGF-II peptides are localized, in a cell-type-specific manner, during the very early stages of implantation and placentation in the Rhesus monkey. A low level of IGF-I was immunolocalized in trophoblast cells lining lacunae and primary and secondary villi, while moderate to high amounts of IGF-II were detected in lamellar syncytiotrophoblast cells lining lacunae, villi and cell columns, as well as in migrating trophoblast cells in the extravillous compartment, and in endovascular trophoblast cells. Similar observations have been made in monkey placenta collected during day 65 to term (Coulter and Han, 1996) and in human placental tissue (Han et al., 1996). Maternal endometrial cells, however, showed highly comparable distribution profiles for both IGF-I and IGF-II.
The observed presence of IGF-II peptide in differentiated lamellar syncytiotrophoblast cells during the very early stages of implantation and placentation in the Rhesus monkey may be important in their transition to this differentiated cell population, since it is known that IGF-II functions as an essential survival factor during transition from the proliferating state to the differentiating state (Stewart and Rotwein, 1996). It is possible that IGF-II regulates the role of syncytiotrophoblast cells in the placental functions of nutrient and oxygen transport as well as placental hormone synthesis and secretion (Roberts and Anthony, 1994; Coulter and Han, 1996). It has also been suggested that IGF-II produced by trophoblast cells within the chorionic plate, as has been observed in the present study, may potentiate their migratory invasion (Irving and Lala, 1995) and stimulate insulin-like growth factor 1 (IGFBP-1) production by decidual cells in a paracrine manner (Irwin et al., 1993). IGFBP-1 can in turn influence integrin-mediated (Jones et al., 1993; Yelian et al., 1993) migration of cytotrophoblast cells into maternal stroma (Damsky et al., 1993; Irving and Lala, 1995; Bischof et al., 1998; Hamilton et al., 1998; Irwin and Giudice, 1998).
In the present study, very low amounts of IGF-I peptide were detected in various subsets of trophoblast cells at implantation sites. We have earlier reported that at lacunar and early villous stages of implantation and placentation, trophoblast cells of the Rhesus monkey did not express any appreciable immunostaining for the oestrogen receptor, while they were positive for the progesterone receptor (Ghosh et al., 1999). Oestrogen stimulates IGF-I gene expression and IGF-I is assumed to mediate oestrogen action in target tissues (Ghosh et al., 1991; Guidice, 1994; Murphy and Ballejo, 1994). It is likely that undetectable to low levels of ER and IGF-I in trophoblast cells in lacunar and villous stages of development in the Rhesus monkey may be functionally related to the control of trophoblast cell proliferation (Rutanen, 1998).
IGF-I and IGF-II peptides are abundantly present in uteri of cycling and pregnant rodents, domestic species and humans (Murphy et al., 1987; Tavakkol et al., 1988; Letcher et al., 1989; Carlsson and Billig, 1991; Guidice, 1994; Murphy and Ballejo, 1994; Gao et al., 1995). We report similar results in the Rhesus monkey during early implantation. Interestingly, endometrial plaque epithelial cells are also immunopositive for both IGF-I and IGF-II. IGF-II expression in human endometrial cells is generally high under progestin dominance (Zhou et al., 1994; Gao et al., 1995). Thus, the observed moderate level of IGF-II in maternal endometrium during early stages of placentation may arise from the high progesterone concentration in the maternal circulation at that time (Ghosh et al., 1997). However, a similar trend in the distribution of IGF-I peptide in maternal endometrium was also observed. The level of oestrogen receptor has been shown to be correlated with IGF-I production (Guidice, 1994; Murphy and Ballejo, 1994), however, the expression of oestrogen receptors occurs at a very low level in endometrial cells at the site of implantation (Salmi et al., 1996; Wang et al., 1996; Ghosh et al., 1999). On the other hand, a high level of IGF-I was observed in vascular smooth muscle and in myometrium, while these cells showed a moderate degree of IGF-II peptide. It has been observed earlier that myometrial expression of IGF-I is up-regulated by steroid hormones, while IGF-II expression appears to be constitutive in myometrial smooth muscle cells in primates (Adesanya et al., 1996). From the present results, it is likely that some other regulatory factors besides steroid hormones may be involved in the expression of IGF peptides in endometrial and myometrial cells during implantation.
In conclusion, it appears that there is differential distribution of IGF peptides in syncytiotrophoblast, cytotrophoblast and migrating trophoblast cell populations in lacunar and villous stages of gestation in the Rhesus monkey. In order to appreciate the involvement of IGF in the complex process of trophoblast invasion and decidualization in the primate uterus it appears important to examine the IGF-IGFBP-1 involvement at feto-maternal interface in the primate.
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The research study was funded from the projects supported by the Council for Scientific and Industrial Research, India, the Rockefeller Foundation and the World Health Organization. The views expressed by the authors do not necessarily reflect the views of the funding agencies.
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1 To whom correspondence should be addressed. E-mail: dghosh_57{at}hotmail.com
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Adesanya, A.O., Zhou, J. and Bondy, C.A. (1996) Sex steroid regulation of insulin like growth factor system gene expression and proliferation in primate myometrium. J. Clin. Endocrinol. Metab., 81, 1967–1974.[Abstract]
Baker, J., Liu, J.P., Robertson, E.J. and Efstratiadis, A. (1993) Role of insulin like growth factors in embryonic and post natal growth. Cell, 75, 73–82.[Web of Science][Medline]
Bischof, P., Meisser, A., Campana, A. and Tseng, L. (1998) Effects of decidua-conditioned medium and insulin like growth factor binding protein 1 on trophoblastic matrix metalloproteinases and their inhibitors. Placenta, 19, 457–464.[Web of Science][Medline]
Blankenship, T.N., Enders, A.C. and King, B.F. (1993a) Trophoblastic invasion and the development of uteroplacental arteries in the macaque: immunohistochemical localization of cytokeratins, insulin, type IV collagen, laminin and fibronectin. Cell Tissue Res., 272, 227–236.[Web of Science][Medline]
Blankenship, T.N., Enders, A.C. and King, B.F. (1993b) Trophoblastic invasion and modification of uterine veins during placental development in macaques. Cell Tissue Res., 274, 135–144.[Web of Science][Medline]
Carlsson, B. and Billig, H. (1991) Insulin like growth factor I expression during development and estrous cycle in the rat uterus. Mol. Cell. Endocrinol., 77, 175-180.[Web of Science][Medline]
Clemens, N.J. (1991) Cytokines. Bios, Oxford.
Coulter, C.L. and Han, V.K. (1996) The pattern of expression of insulin like growth factor (IGF), IGF I receptor and IGF binding protein (IGFBP) mRNAs in the Rhesus monkey placenta suggests a paracrine mode of IGF-IGFBP interaction in placental development. Placenta, 17, 451–460.[Web of Science][Medline]
Damsky, C., Sutherland, A. and Fisher, S. (1993) Extracellular matrix 5: Adhesive interactions in early mammalian embryogenesis, implantation and placentation. FASEB J., 7, 1320–1329.[Abstract]
Enders, A.C. (1993) Overview of morphology of implantation in primates. In Wolf, D.P. et al. (eds), In Vitro Fertilization and Embryo Transfer in Primates. Springer-Verlag, New York, pp. 145–157.
Enders, A.C. and Blankenship, T.N. (1997) Modification of endometrial arteries during invasion by cytotrophoblast cells in the pregnant macaque. Acta Anat., 159, 169–193.[Web of Science][Medline]
Enders, A.C. and King, B.F. (1991) Early stages of trophoblastic invasion of the maternal vascular system during implantation in the macaque and baboon. Am. J. Anat., 192, 329–346.[Web of Science][Medline]
Enders, A.C. and Schlafke, S. (1986) Implantation in non-human primates and in the human. Comp. Primate Biol., 3, 291–310.
Enders, A.C., Welsh, A.O. and Schlafke, S. (1985) Implantation in the Rhesus monkey: initial penetration of endometrium. Am. J. Anat., 173, 147–169.[Web of Science]
Fant, M., Munro, H. and Moses, A.C. (1986) An autocrine/paracrine role for insulin-like growth factors in the regulation of human placental growth. J. Clin. Endocrinol. Metab., 63, 499–505.
Gao, J.G., Zhu, H.H., Fan, J. et al. (1995) Progestin and antiprogestin differentially regulate the expression of insulin-like growth factors (IGF I and IGF II) messenger ribonucleic acid in human endometrial stromal cells. Biol. Reprod., 53, 355–360.[Abstract]
Ghosh, D., Danielson, K.G., Alston, J.T. and Heyner, S. (1991) Functional differentiation of mouse uterine epithelial cells grown on collagen gels or reconstituted basement membranes. In Vitro Cell. Dev. Biol., 27A, 713–718.[Web of Science]
Ghosh, D., Sengupta, J. and Hendrickx, A.G. (1996) Effect of a single-dose, early luteal phase administration of mifepristone (RU486) on implantation stage endometrium. Hum. Reprod., 11, 2026–2035.
Ghosh, D., Stewart, D., Nayak, N.R. et al. (1997) Serum concentrations of oestradiol-17ß, progesterone, relaxin and chorionic gonadotrophin during blastocyst implantation in natural pregnancy cycle and in embryo transfer cycle in the Rhesus monkey. Hum. Reprod., 12, 914–920.
Ghosh, D., Dhara, S., Kumar, A. and Sengupta, J. (1999) Immunohistochemical localization of receptors for progesterone and oestradiol-17ß in the implantation site of the Rhesus monkey. Hum. Reprod., 14, 505–514.
Guidice, L.C. (1994) Growth factors and growth modulators in human uterine endometrium: their potential relevance to reproductive medicine. Fertil. Steril, 61, 1–17.[Web of Science][Medline]
Guidice, L.C. Zegher, F., Gargosky, S.E. et al. (1995) Insulin-like growth factors and their binding protein in the term and preterm human fetus and neonate with normal and extremes of intrauterine growth. J. Clin. Endocrinol., 80, 1548–1555.
Hamilton, G.S., Lysiak, J.J., Han, V.K.M. (1998) Autocrine-paracrine regulation of human trophoblast invasiveness by IGF-II and IGFBP-1. Exp. Cell Res., 244, 147–156.[Web of Science][Medline]
Han, V.K., Bassett, N., Walton, J. and Challis, J.R.G. (1996) 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 fetomaternal interface. J. Clin. Endocrinol. Metab., 81, 2680–2693.[Abstract]
Hendrickx, A.G. (1971) Embryology of the Baboon. University of Chicago Press, London.
Heuser, C.H. and Streeter, G.L. (1941) Development of the macaque embryo. Contrib. Embryol. Carneg. Inst., 29, 15–55.
Irving, J. A. and Lala, P.K. (1995) Functional role of cell surface integrin on human trophoblast cell migration: regulation by TGF-ß, IGF II and IGFBP 1. Exp. Cell Res., 217, 419–427.[Web of Science][Medline]
Irwin, J.C. and Giudice, L.C. (1998) IGFBP 1 binds to 
5ß1 integrin in human cytotrophoblasts and inhibits their invasion into decidualized endometrial stromal cells in vitro. GH & IGF Res., 8, 21–31.
Irwin, J.C., de-las-Fuentes, L., Duspin, B.A. and Giudice, L.C. (1993) Insulin-like growth factor regulation of human endometrial stromal cell function: coordinate effects on insulin-like growth factor binding protein 1, cell proliferation and prolactin secretion. Regul. Peptides, 48, 165–177.[Web of Science][Medline]
Jones, J.I., Gockerman, A., Busby, Jr, W.H. et al. (1993) Insulin-like growth factor binding protein I stimulates cell migration and binds to the 5ß1 integrin by means of its Arg-Gly-Asp sequence. Proc. Natl. Acad. Sci. USA, 90, 10553–10557.
Letcher, R. Simmens, R.C.M., Bazer, F.W. and Simmens, F.A. (1989) Insulin-like growth factor I expression during early conceptus development in the pig. Biol. Reprod., 41, 1143–1151.[Abstract]
Librach, C.L., Werb, Z., Fitzgerald, M.L. et al. (1991) 92-kD type collagenase mediates invasion of human cytotrophoblasts. J. Cell Biol., 113, 437–449.
Liu, J.P., Baker, J., Parkins, A.S. et al. (1993) Mice carrying null mutation of the genes encoding insulin-like growth factor and type I IGF receptor. Cell, 75, 59–72.[Web of Science][Medline]
Muhlhauser, J., Crescimanno, C. and Kasper, M. et al. (1995) Differentiation of human trophoblast populations involves alterations in cytokeratin patterns. J. Histochem. Cytochem., 43, 579–589.[Abstract]
Murphy, L.J. and Ballejo, G. (1994) Growth factor and cytokine expression in the endometrium. In Findlay, J.K. (ed.), Molecular Biology of the Female Reproductive System. Academic Press, San Diego, pp. 345–377.
Murphy, L.J., Murphy, L.C. and Friesen, H.G. (1987) Estrogen induces insulin-like growth factor I expression in the rat uterus. Mol. Cell Endocrinol., 1, 445–450.
Press, M.F., Udove, J.A. and Green, G.L. (1988) Progesterone receptor distribution in human endometrium. Am. J. Pathol., 131, 121–124.
Ritvos, O., Ranta, T., Jalkanen, J. et al. (1988) Insulin like growth factor (IGF) binding protein from human decidua inhibits binding and biological action of IGF I in cultured choriocarcinoma cells. Endocrinology, 122, 2150–2157.
Roberts, R.M. and Anthony, R.V. (1994) Molecular biology of trophectoderm and placental hormones. In Findlay, J.K. (ed.), Molecular Biology of the Female Reproductive System. Academic Press, San Diego, pp., 395–437.
Rotwein, P. (1991) Structure, evolution, expression and regulation of insulin-like growth factors I and II. Growth factors, 5, 3–18.[Medline]
Rutanen, E.M. (1998) Insulin-like growth factors in endometrial function. Gynecol. Endocrinol., 12, 399–406.[Web of Science][Medline]
Salmi, A., Ammala, M. and Rutanen, E.M. (1996) Proto-oncogenes c-jun and c-fos are down regulated in human endometrium during pregnancy: relationship to oestrogen receptor status. Mol. Hum. Reprod., 2, 979–984.
Stewart, C.E.H. and Rotwein, P. (1996) Insulin-like growth factor-II is an autocrine survival factor for differentiating myoblasts. J. Biol. Chem., 271, 11330–11338.
Tavakkol, A., Simmens, F.A. and Simmens, R.C.M. (1988) Porcine insulin-like growth factor I (pIGF I): complementary deoxyribonucleic acid clonic and uterine expression of messenger ribonucleic acid encoding evolutionary conserved IGF I peptides. Mol. Reprod. Dev., 37, 1–11.
Vicovac, I. and Aplin, J.D. (1996) Epithelial-mesencymal transition during trophoblast differentiation. Acta Anat., 156, 202–216.[Web of Science][Medline]
Wang, J.D., Zhu, J.B., Fu, Y. et al. (1996) Progesterone receptor immunoreactivity at the maternofetal interface of first trimester pregnancy: a study of trophoblast populations. Hum. Reprod., 11, 413–419.
Wislocki, G.B. and Streeter, G.L. (1938) On the placentation of the macaque (Macaca mulatta) from the time of implantation until the formation of the definitive placenta. Contrib. Embryol. Carneg. Inst., 27, 1–66.
Yelian, F.D., Edgeworth, N.A., Dong, Li-Jun et al. (1993) Recombinant entactin promotes mouse primary trophoblast cell adhesion and migration through the Arg-Gly-Asp (RGD) recognition sequence. J. Cell Biol., 121, 923–929.
Zhou, J., Dsupin, B.A., Guidice, L.C. and Bondy, C.A. (1994) Insulin-like growth factor system gene expression in human endometrium during the menstrual cycle. J. Clin. Endocr. Metab., 79, 1723–1734.[Abstract]
Submitted on May 2, 2000; accepted on January 19, 2001.
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