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  • Abstract: placenta x
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Chun-Bo Teng, Hong-Lu Diao, Hong Ma, Jing Cong, Hao Yu, Xing-Hong Ma, Li-Bin Xu and Zeng-Ming Yang

Signal transducer and activator of transcription 3 (Stat3), a member of the Stat family, is specifically activated during mouse embryo implantation. The aim of this study was to investigate the expression, activation and regulation of Stat3 in rat uterus during early pregnancy, pseudopregnancy, delayed implantation and artificial decidualization. Stat3 mRNA was highly expressed in the luminal epithelium on day 5 and in the luminal epithelium and underlying stromal cells at implantation sites on day 6 of pregnancy. There was a strong level of Stat3 protein expression and phosphorylation in the stromal cells near the lumen and in the luminal epithelium on day 5 of pregnancy, which was similar to day 5 of pseudopregnancy. In the afternoon of day 6, the strong level of Stat3 phosphorylation was detected only in the luminal epithelium. Stat3 was highly expressed and activated in the decidual cells from days 7 to 9 of pregnancy and under artificial decidualization in the present study. Our results suggest that the strong level of Stat3 activation in the luminal epithelium and underlying stromal cells during the pre-implantation period may be important for establishing uterine receptivity as in mice, and the high level of Stat3 expression and activation in decidual cells may play a role during decidualization.

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Jérôme Artus, Isabelle Hue and Hervé Acloque

In ungulates, early embryonic development differs dramatically from that of mice and humans and is characterized by an extended period of pre- and peri-implantation development in utero. After hatching from the zona pellucida, the ungulate blastocyst will stay free in the uterus for many days before implanting within the uterine wall. During this protracted peri-implantation period, an intimate dialog between the embryo and the uterus is established through a complex series of paracrine signals. The blastocyst elongates, leading to extreme growth of extra-embryonic tissues, and at the same time, the inner cell mass moves up into the trophoblast and evolves into the embryonic disc, which is directly exposed to molecules present in the uterine fluids. In the peri-implantation period, uterine glands secrete a wide range of molecules, including enzymes, growth factors, adhesion proteins, cytokines, hormones, and nutrients like amino and fatty acids, which are collectively referred to as histotroph. The identification, role, and effects of these secretions on the biology of the conceptus are still being described; however, the studies that have been conducted to date have demonstrated that histotroph is essential for embryonic development and serves a critical function during the pre- and peri implantation periods. Here, we present an overview of current knowledge on the molecular dialogue among embryonic, extraembryonic, and maternal tissues prior to implantation. Taken together, the body of work described here demonstrates the extent to which this dialog enables the coordination of the development of the conceptus with respect to the establishment of embryonic and extra-embryonic tissues as well as in preparation for implantation.

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In the guinea-pig, an ovarian or exogenous progestagen is not required for ovo-implantation, but the lack of it in females, ovariectomized 3, 4 or 5 days after mating, affects embryonic growth and development from about Day 12. Between 14 and 16 days after mating, the placenta and embryo undergo very rapid differentiation. This stage has been studied in a large series of embryos to see how they were affected by the progestagen deficiency. Growth of the embryonic swelling was slowed down but there was much variation, some embryos not getting beyond the 14-day stage and others surviving and differentiating normally up to Day 15 or 16.

The duration of embryonic viability in groups of ovariectomized mothers was tested by beginning administration of progesterone on Day 13, 14, 15 or 16. In the last group only two out of thirteen embryos survived. In the untreated series only five out of eighteen ovariectomized mothers contained live embryos on Day 16.

From the general variability and from a study of the embryos, it appeared that arrest of embryonic development and death was not caused at any precise time or stage by uterine compression but was more probably due to nutritional deficiencies associated with the absence of the ovarian progestagen.

In further experiments it was shown that pregnancy could continue after about Day 21, or even earlier, in the absence of the ovaries or of exogenous hormones. Both this and the normal differentiation of some embryos in ovariectomized mothers up to Day 16, indicate early production of sex hormones by the placenta.

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Emma S Lucas, Nigel P Dyer, Katherine Fishwick, Sascha Ott and Jan J Brosens

Endometrial stem-like cells, including mesenchymal stem cells (MSCs) and epithelial progenitor cells, are essential for cyclic regeneration of the endometrium following menstrual shedding. Emerging evidence indicates that endometrial MSCs (eMSCs) constitute a dynamic population of cells that enables the endometrium to adapt in response to a failed pregnancy. Recurrent miscarriage is associated with relative depletion of endometrial eMSCs, which not only curtails the intrinsic ability of the endometrium to adapt to reproductive failure but also compromises endometrial decidualization, an obligatory transformation process for embryo implantation. These novel findings should pave the way for more effective screening of women at risk of pregnancy failure before conception.

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Fernando Correa, Manuel L Wolfson, Paula Valchi, Julieta Aisemberg and Ana María Franchi

The endocannabinoid system (eCS), is a complex system, comprising the main endogenous ligands anandamide and 2-arachidonoyl glycerol, the cannabinoid receptors CB1 and CB2 and the biosynthetic and degrading enzymes. Cumulative evidence shows that the eCS plays an important role in reproduction, from egg fertilization to parturition. Therefore, alterations in this system, either by recreation/therapeutic use of cannabis or deregulation of the endogenous cannabinoids, might lead to adverse pregnancy outcomes, including retardation in embryo development, poor blastocyst implantation, inhibition of decidualization, miscarriage and compromised placentation. Nevertheless, the molecular mechanisms by which the eCS participates in different stages of pregnancy remain poorly understood. In this review, we will examine the evidence from animal and human studies to support the role of the eCS in implantation, early-to-late pregnancy and placentation as well as the difficulties of targeting this system for treatment of female infertility.

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B. Cook and R. H. F. Hunter

Implanatation and some related events in domestic animals

Association of the embryo with the uterine epithelium, by either superficial attachment or specific embedding in or beneath the endometrium, leads in due course to the formation of a placenta and complete dependence of the differentiating embryo upon metabolic support from the mother. The time of implantation after fertilization varies widely amongst the common domestic animals and so, therefore, do the stage and size of embryonic development at the initiation of a functional contact with the uterine tissues (Wimsatt, 1975). Delayed implantation of the blastocyst—the period of embryonic diapause found in certain species of deer, carnivore and rodents during seasonal or lactational anoestrus—has not been documented as a feature of reproduction in domestic cattle, sheep or pigs. Before considering endocrine aspects of the implantation process, it seems necessary to comment upon some of the significant stages preceding this critical phase of development. More extensive treatments of the topic can be found in the reviews of Blandau (1971), Finn (1971), McLaren (1972) and Psychoyos (1973), although rodents rather than the larger domestic species are the principal concern of such works.

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TG Burnett, JS Tash and JS Hunt

Nitric oxide (NO) has been implicated as a signalling molecule in many cellular processes. As nitric oxide synthase 2 (NOS-2) is the main isoform expressed in mouse decidua and metrial gland, mice with a targeted disruption of the gene encoding NOS-2 were used to determine the potential roles of this enzyme during pregnancy. Reproductive success and the morphology of implantation sites throughout pregnancy were compared in NOS-2 deficient (NOS-2-/-) and wild-type (WT) mice. Although there were no significant differences in the duration of gestation or birth weight, NOS-2-/- mice had significantly fewer viable embryos at mid-gestation and delivered smaller litters than did WT mice. Histological sections of uteroplacental units from WT and NOS-2-/- mice were compared to establish the mechanisms underlying the loss of fetuses. No morphological differences were observed on day 6 or day 8 of gestation, indicating that implantation and early development of implantation sites were unaffected by the absence of NOS-2. However, by mid-gestation, decidua of NOS-2-/- mice had reduced cellularity and their decidual arteries had abnormally thickened walls. These observations were quantified by morphometric measurements, which showed a significant reduction in decidual cellular area and a significant increase in the blood vessel wall:lumen ratio in NOS-2-/- mice. The increase in the thickness of the blood vessel walls was not due to abnormal cellular infiltration or to altered expression of alpha-actin in vascular smooth muscle. These results indicate that NOS-2 has a functional role in the maintenance of decidual cellular integrity and development of appropriate uterine vasculature, and may play a supportive role in promoting embryo survival.

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The role of the ovaries in the maintenance of pregnancy was studied in the ferret. Ovariectomy at the time of implantation showed that some embryos survived for 7 days after the operation but all were destroyed after 10 days, although the trophoblast continued to grow and at a much faster rate than normal. Ovariectomy performed after implantation showed that no fetal development occurred when the ovaries were removed at Day 21 post coitum, but that fetuses developed for an appreciable length of time in animals ovariectomized on Days 23 to 27 post coitum. Ovariectomy in late gestation resulted in speedy expulsion of the fetuses. An increase in the placenta:fetus ratio did not alter the response to ovariectomy in late gestation. The uteri in all ovariectomized animals showed progestational endometria when examined shortly after expulsion of the fetuses.

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J. E. Gadsby, R. B. Heap and R. D. Burton

Summary. Oestrogen synthesis by the early embryo in vitro was studied with tissue from pigs, sheep, cows, roe deer, ferrets, cats, rabbits and a plains viscacha. Definitive evidence for aromatase activity and oestrogen synthesis in preimplantation trophoblast was obtained for the pig with the formation of oestrone, oestradiol-17β and oestradiol-17α from3H-labelled androstenedione and dehydroepiandrosterone. Aromatase activity was appreciably lower in all other species studied, and labelled oestrogens were recovered only from incubations of allantochorionic tissue of roe deer, recovered shortly after implantation, and from pooled samples of early embryonic tissue of cows. High aromatase activity in preimplantation trophoblast of pigs was associated with the maternal recognition of pregnancy and the occurrence of superficial implantation in this species.

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L. K. Law, P. P. L. Tam and H. W. Yeung

Summary. α-Trichosanthin (0·3 mg/25 g) and α-momorcharin (0·2 mg/25 g) given intraperitoneally to mice on Days 4 and 6 of pregnancy led to an inhibition of implantation. In-vitro study of the effects of these proteins on developing mouse embryos showed that these proteins did not affect the transformation of morulae to blastocysts but further development was impaired: many blastocysts failed to hatch from the zona, the incidence of successful attachment to a plastic substrate decreased and the extent of trophoblastic outgrowth diminished. Inner cell mass development was less affected than was the trophoblast. The in-vivo inhibition of implantation may therefore be a consequence of the deleterious effect of these proteins on the trophoblast.