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O. NILSSON

Implantation is a process whereby the blastocyst becomes embedded in the endometrium. Firstly, the blastocyst must contact the epithelium, then the trophoblast cells will start invading the endometrium. In species with delayed implantation, the blastocyst requires activation before its attachment.

Thus there are three stages involved in delayed implantation: blastocyst activation, trophoblast attachment and trophoblast invasion. The following account indicates what characterizes these three stages at a cellular and subcellular level and what suggestions structural analysis can give as to the mechanisms controlling these processes.

DELAYED IMPLANTATION

The blastocysts of some mammalian species are normally kept in a state of delay before implantation (Enders, 1963; Lanman, 1970). In some other species, for instance the mouse, a delayed implantation also can be obtained experimentally (Yoshinaga & Adams, 1966; Humphrey, 1967; Smith & Biggers, 1968; McLaren, 1971). This offers a biological

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S. BERGSTRÖM and O. NILSSON

Summary.

A gradual closure of the uterine lumen occurs during progesterone treatment of mice spayed in early pregnancy. This causes an appearance of various imprints by the endometrium on the blastocyst. Imprints bounded by a polygonal circumference are caused by the slightly protruding intercellular borders of the endometrium. Shallow imprints appearing later are produced by bulging epithelial cells. Deep, rounded imprints are caused by fungus-like protrusions of the luminal epithelium. Generally, imprints are more frequent on the blastocyst surface than on the endometrial surface, suggesting that the trophoblast cells are more malleable than uterine epithelial cells in delayed implantation. The good correlation between structures in scanning and transmission electron micrographs indicates that the preparation techniques used are satisfactory.

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S. BERGSTRÖM and O. NILSSON

Summary.

Blastocysts that have been activated for implantation by an injection of oestrogen become separated from the uterine surface by a layer of secretion. By 8 hr after the injection, the trophoblast cytoplasm contains several glycogen granules, groups of ribosomes, and mitochondria of a condensed type. These ultrastructural changes are signs of the increased metabolic activity exhibited by the trophoblast at activation. It is suggested that the uterine epithelium keeps the trophoblast inactive by delivering only a minimal nutritive medium and that the epithelium activates the trophoblast by making more nutrients, probably some carbohydrate, available as a consequence of an oestrogen-induced increase in the secretory activity.

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ANNE McLAREN and O. NILSSON

The process of implantation in the mouse is accompanied by striking changes in the ultrastructure of the uterine epithelium. During the progesteronedominated pre-attachment stage, the luminal epithelium is bordered by a fringe of regular microvilli, and a small gap separates the epithelial surface from the blastocyst or from the epithelium lining the other side of the lumen. Under the influence of oestrogen, the luminal epithelium enters on the attachment stage. The microvilli become more irregular and finally flatten out altogether, and the gap between opposing luminal surfaces, or between luminal surface and blastocyst, shrinks to 150 to 200 Å (Nilsson, 1966; Potts, 1966; Reinius, 1967). This change occurs equally in the unstimulated pseudopregnant uterus, and must therefore be considered a sensitization rather than a decidual effect (McLaren, 1969). A similar modification

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S. BERGSTRÖM and O. NILSSON

The mouse blastocyst is surrounded by the uterine secretion for about 24 hr before it implants in the uterine mucosa. The implantation seems to be initiated by oestrogen (Humphrey, 1967) and is associated with changes in the ultrastructure of the uterine epithelium (Potts & Psychoyos, 1967; Reinius, 1967). By using the technique of experimentally delayed implantation, both the blastocyst and the uterine epithelium can be kept in a pre-implantation state.

Transmission electron microscopy of rat blastocysts in pre-implantation and implantation states following the induction of delayed implantation indicates that the trophoblast surface changes from villous to smooth at implantation (Mayer, Nilsson & Reinius, 1967). This finding makes it likely that the surface properties of the trophoblast cells change when implantation is induced and that the ultrastructure of the trophoblast surface can be a useful indicator of the functional state of the tissue as a whole.

Evaluation of the appearance

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J. FRIBERG and O. NILSSON

Summary.

Human spermatozoa agglutinated head-to-head by sperm-agglutinating antibodies have been examined by means of scanning electron microscopy. Two types of union were observed, that between the anterior and middle parts of the sperm heads, and a second type where the anterior part of the head of the sperm cell attached to the postnuclear cap region of another spermatozoon. The possible significance of these findings is briefly discussed.

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K. HEDLUND and O. NILSSON

Before implantation occurs, a lumen containing secretion can be demonstrated in the uterus of the rat, mouse, hamster and guinea-pig. This luminal space disappears when implantation occurs, the apposing luminal surfaces of the mucosa coming into close contact. This phenomenon has been named the `attachment reaction' of the uterine epithelium (Nilsson, 1970).

In the rat, the preimplantation appearance of the uterine mucosa can be maintained, by giving progesterone during experimentally delayed implantation (Nilsson, 1966) or by giving progesterone to spayed rats (Ljungkvist, unpublished). Implantation and the attachment reaction do not take place until oestrogen is given (Mayer & Nilsson, 1966). In the hamster, implantation occurs without the addition of oestrogen when progesterone is given to animals ovariectomized early in pregnancy (Prasad, Orsini & Meyer, 1960; Harper, Dowd & Elliott, 1969) and in the guinea-pig, even

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SAFIA R. MUNSHI and O. NILSSON

Rabbit antiserum to ovine LH is capable of neutralizing the endogenous activity of mouse LH (Munshi & Rao, 1967). Administration to mated female mice on any one day from Days 2 to 7 after mating results in the inhibition of pregnancy. Since this inhibition can be overcome only by the continuous administration of progesterone, it has been suggested that the antiserum blocks pregnancy by inhibiting progesterone synthesis by the corpus luteum (Munshi, Purandare & Rao, 1972). These studies, however, do not indicate at what stage pregnancy is affected.

Since the various stages of pregnancy differ morphologically, microscopy has been used to examine the early stages of pregnancy in mice injected with antiserum to LH in order to find out when pregnancy is affected.

Random-bred albino mice of the NMRI strain were used. Females were placed with males overnight and examined for the presence of a vaginal plug the next morning.

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Ö. Lundkvist, I. Ljungkvist and O. Nilsson

Peanut oil injected into the uterine lumen of the rat or mouse is a well known deciduogenic stimulus (Finn & Keen, 1963; Finn & Hinchliffe, 1964, 1965). It is believed to induce a decidual reaction by a mechanism similar to that of the implanting blastocyst (Finn & Porter, 1975). This view is primarily based on the fact that the hormonal requirements for (Finn, 1965; Meyers, 1970) and the morphological changes of the stroma after (Finn & Hinchliffe, 1964, 1965) induction are similar to those for blastocyst implantation. Peanut oil has, therefore, often been used to study early decidualization (Hetherington, 1968; Miller, 1973).

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P. C. Svalander, P. Odin, B. O. Nilsson and B. Öbrink

Summary. Affinity-purified antibodies to cellCAM-105, an adhesive cell surface glycoprotein, were used in immunohistochemical investigations of rat uteri at various functional stages: (i) the oestrous, pro-oestrous, metoestrous, and dioestrous stages of the oestrous cycle, (ii) Days 1–8 of normal pregnancy, (iii) delayed implantation, (iv) 18 h after oestrogen reactivation from delay of implantation, and (v) juvenile rats, and normal ovariectomized adults, respectively, before and after experimental injection of progesterone and/or oestrogen. CellCAM-105 was present in the apical zones of the luminal and glandular epithelium cells in a stage-specific and hormone-dependent manner.

The results indicate that: (1) steroid hormones are essential for the expression of cellCAM-105 in the uterine epithelial cells; (2) progesterone induces cellCAM-105 expression in the glandular epithelium, and oestrogen induces cellCAM-105 expression in the luminal epithelium; (3) progesterone induces down-regulation of cellCAM-105 from the surface of the uterine luminal epithelium of juvenile rats; (4) cellCAM-105 is absent in the luminal epithelial cells but present in the glandular epithelial cells of the rat uterus at the time of blastocyst implantation.

Keywords: cellCAM-105; rat; uterus; oestrous cycle; implantation; progesterone; oestrogen